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V. Michael Holers MD

Head, Division of Rheumatology University of Colorado Denver


 

Dr. Holers is performing basic and translational research on the roles of complement receptors and membrane regulatory proteins in the immune response, with a special emphasis on B lymphocytes and autoimmune diseases. Complement is a complex system of serum proteins which, upon activation, covalently bind targets (bacteria, viruses, immune complexes) and marks them as foreign. The interaction of complement with B cell receptors also results in substantial enhancement of humoral and cellular immunity. In addition to this role, excessive activation of complement is centrally involved in autoimmunity and the tissue damage that occurs in many inflammatory diseases involving organs such as the kidney. The Holers’ laboratory has developed human and mouse models in which to study these complement related biologic processes and develop inhibitors. With regard to the natural history studies of RA, we now know that autoimmune diseases begin years before clinical signs and symptoms are apparent, when at-risk individuals manifest highly predictive autoantibodies in their serum. This observation suggests that additional therapeutic and/or prevention strategies could be considered for individuals in this at-risk but asymptomatic period. It is also relevant to determine how individuals transition from this autoantibody-positive, at-risk period to clinically active disease, and ongoing studies have been started that are related to understanding these questions.

 

 

 1993           Arrived at UCD 
 1983-1985 Research Fellowship in Rheumatology - Washington University School of Medicine
 1983-1985 Research Associate - Howard Hughes Medical Institute, St. Louis, MO
 1981-1983 Clinical Fellowship in Rheumatology- University of Colorado School of Medicine, Denver, CO
 1979-1981 Residency - Internal Medicine Barnes Hospital, St. Louis MO
 1978-1979 Internship - Internal Medicine Barnes Hospital, St. Louis MO
   

Medical School: Washington University Medical School, St. Louis, Missouri




 2000-Present Head, Division of Rheumatology - University of Colorado Denver
 1998-Present Professor of Immunology - University of Colorado Denver
 1997-Present Present Professor of Medicine - University of Colorado Denver
 1993-Present Smyth Professor of Rheumatology - University of Colorado Denver
 1994-1998 Professor of Immunology - University of Colorado Denver
 1993-1997 Associate Professor of Medicine (with tenure) - University of Colorado Denver
 1992-1993 Associate Professor of Medicine (with tenure) - Washington University School of Medicine
 1987-1993 Member - Division of Biology and Biomedical Sciences, Washington University School of Medicine
 1987-1993 Assistant Professor of Pathology - Washington University School of Medicine
 1986-1993 Assistant Investigator - Howard Hughes Medical Institute
 1986-1992 Assistant Professor of Medicine - Washington University School of Medicine
 1985-1986 Instructor in Medicine - Washington University School of Medicine








 

 

2006-Present Member, Molecular Biology Program, UCHSC
2004-Present Chair, Scientific Advisory Council, American Rheumatology Research and Education Foundation
2001 - Present Member, Structural Biology Program, UCHSC
2000-Present Member, Structural Biology Program, UCHSC
1992- Present American College of Rheumatology Abstract Selection Subcommittees
2004-2010 Member, Board of Directors American College of Rheumatology Research and Education Foundation
2004-2007 Site Director, Lupus Clinical Trials Consortium
2005-2006 Chair, Rheumatoid Arthritis Initiative Taks Force, American College of Rheumatology Research and Education Foundation
2003-2004 Chair, Task Force on Research Funding, American College of Rheumatology 2003-Present Steering Committee, NIH/NIAMS SLE Biomarkers Consortium
2002-2004 Member, Board of Directors, American College of Rheumatology 2003-2006 Program Committee Block Chair, American Immunologists
1999-2002 Member, Board of Directors, American College of Rheumatology Research and Education Foundation
1999-2002 Chair, Committee on Research, American College of Rheumatology
2000-2001 Blue Ribbon Panel on Research, National Arthritis Foundation
2000 Founding Member and Secretary, International Complement Society
2000 Pfizer Postdoctoral Fellowship Academic Advisory Board
1998-2000 International Complement Workshop Organizing Committee
1998-2000 National Arthritis Foundation Publications Committee
1996-2000 Member, Allergy and Immunology (ALY) Study Section, Center for Scientific Review, NIH
1999 Co-Chair, ACR Basic Research Conference
1997-1999 ACR National Research Conference Planning Committee, American College of Rheumatology
1998 ACR Basic Research Conference Co-Organizer
1995-1998 Member, Committee on Research, American College of Rheumatology
1997 Subcommittee Chairman, American College of Rheumatology National Meeting Abstract Selection Committee
1995, 1998 Co-Chair, Complement Symposium, AAI Meeting


 

2010 Senior Fellow of the American Asthma Foundation
2009 Freyberg Lectureship, Hospital for Special Surgery, New York, NY
2009 Christian Lectureship, Hospital for Special Surgery, New York, NY
2009 Physician Pro Tempore, Hospital for Special Surgery, New York, NY
2009 Eric Bywaters Lectureship, Hammersmith Hospital, London, UK
2009 Kroc Lectureship, University of Texas Southwestern, Dallas, TX
2009

University of Colorado Technology Transfer Lifetime Pinnacle Awardee

2008

American College of Rheumatology Distinguished Basic Investigator Award

2008 Pfizer Visiting Professor, Emory University School of Medicine
 2008

Ephraim P. and Jean S. Engleman Visiting Professor, University of California San Francisco

 2007 Ogryzlo Day Merck Frosst Canada and Schering Canada Visiting Professor, University of Toronto
 2004 Inventro of the Year, University of Colorado Denver
 2003 Pfizer Visiting Professor, Medical University of South Carolina
 2000 Member, American Association of Physicians 2002 Member, Henry Kunkel Society
 1999 Volunteer Leadership Award, National Arthritis Foundation
 1998 Harmon Foundation Research Award, Arthritis Foundation Rocky Mountain Chapter
 1997 Schwartz-Weinstein Research Award, Arthritis Foundation Rocky Mountain Chapter
 1997 Robert Wood Johnson Award, Arthritis Foundation
 1993 Member, American Society for Clinical Investigation
 1988-1991 Hulda Irene Duggan Investigator, Arthritis Foundation
 1974 Phi Beta Kappa

 

The basic and translational research focus of my laboratory is on two areas.

The first is the roles of complement receptors and membrane regulatory proteins in the immune response, with a special emphasis on B lymphocytes and autoimmune diseases.

With regard to the first area, complement is a complex system of serum proteins which, upon activation, covalently bind targets (bacteria, viruses, immune complexes, cell membranes) and marks them as foreign. These covalently attached complement fragments bind high affinity receptors on lymphocytes and FDCs. The interaction of complement with B cell receptors results in substantial enhancement of humoral immunity. In addition to this role, excessive activation of complement is centrally involved in the tissue damage that occurs in many inflammatory diseases involving organs such as the kidney. My laboratory has developed human and mouse models in which to study these complement related biologic processes.

The second is the role of autoantibodies and the evolution of autoimmunity in RA from the pre-symptomatic autoantibody-positive period through the onset of clinically active disease. 

With regard to the second area, we now know that autoimmune diseases such as RA, SLE and Type 1 Diabetes Mellitus begin years before clinical signs and symptoms are apparent. That is because these individuals manifest highly predictive autoantibodies in their serum. This observation suggests that we must extend our study of the genetic epidemiology of autoimmune diseases such as RA into this important period, and that additional therapeutic and/or prevention strategies should be considered for individuals in this at-risk but asymptomatic period. It is also relevant to determine how individuals transition from this autoantibody-positive, at-risk period to clinically active disease. My research group has established several ongoing studies in RA that are related to these questions.

 Specific areas of emphasis include:

 

  1. Roles of complement receptor type 2 (CR2, CD21) in B lymphocyte development and activation. Using both human and mouse CR2 as a model, we are analyzing the ways by which CR2 regulates B lymphocyte responses to antigens bound by complement. The specific mechanisms by which CR2 and other complement receptors act to modify B lymphocyte responses are incompletely understood, though we have shown that CR2 deficient mice have a markedly impaired humoral immune response. We are now studying the signaling responses of these receptor deficient B lymphocytes. We have also recently created human CR2 transgenic mice as a way to study structure-function relationships and the effects of over-expression of receptors on B cell development and tolerance. Finally, we are determining the three dimensional structure of the CR2 ligand binding sites for its three ligands (C3d, Epstein-Barr virus and CD23) using NMR, x-ray crystallographic and other structural techniques.
  2. Analysis of the role of complement during the development of SLE, RA and other autoimmune and inflammatory diseases. A recent interest is on the role of specific complement activation pathways (classical, alternative and lectin) in the initiation of injury. In murine studies we are using complement receptor knockouts and complement inhibitors we developed to determine how the alteration of these systems affects self tolerance and tissue injury. A major finding has been to determine that the alternative pathway and its amplification loop are absolutely essential to generate pathologic complement activation fragments in antibody-dependent and –independent disease models and to develop new generations of inhibitors to take advantage of that observation.  In patients, we have led a therapeutic trial of a complement inhibitor in patients with SLE and active glomerular disease and continue to be focused on learning how complement inhibition can positively affect patients with various human diseases.
  3. In addition to the above areas of emphasis, a study of pre-disease autoimmunity in patients at risk for the development of RA has also been initiated in collaboration with Dr. Jill Norris of the Department of Preventive Medicine and other members of the Division of Rheumatology. By using unique human populations at risk for developing RA, we are determining what RA-associated autoantibodies and other biomarkers are present that could predict the development of clinical disease. In addition, we have developed an animal model of the pathogenic role of a newly described autoantibody system directed to citrullinated antigens, commonly called anti-CCP antibodies. These studies have clearly shown that these autoantibodies are pathogenic and are opening up additional therapeutic targets and opportunities.

 

 

PATENTS (granted or in application process):

 

            “3-Dimensional Structure of Complement Receptor Type 2 and Uses Thereof”

            U.S. Patent 2004/0005538 A1, January 8, 2004

 

            “Method of Preventing Recurrent Miscarriages” U.S. Patent Application #60/470,444

 

            “Complement Receptor 2 Targeted Complement Inhibitor Fusion Proteins”

 

“Inhibition of Factor B, the Alternative Complement Pathway and Methods Related Thereto”

 

 Inhibition of Factor B and the Alternative Complement Pathway for Treatment of Traumatic Brain Injury, Spinal Cord Injury and Related Conditions”

 

Treatment of Ischemia-Reperfusion Injury with Lipid, Annexin, and Lipid-Annexin Complexes”

 

            “Targeting Complement Factor H for Treatment of Diseases”

 

“Non-invasive detection of complement-mediated inflammation using CR2-targeted nanoparticles”

 

“Ligand-specific non-antibody polypeptides that inhibit CR2 activation and methods of use thereof”

 

“Methods of modulating activity of the alternative complement pathway”

 

            “Biomarkers for the diagnosis of autoimmune disease”

 

            Complement inhibitory agents in posttraumatic and degenerative arthritis”

 

 

PEER REVIEWED PUBLICATIONS:

 

1.         Rosenberg, N. L., Lacy, J. R., Kennaugh, R. C., Holers, V. M., Neville, H. E., and Kotzin, B. L.  1985.  Treatment of refractory chronic demyelinating polyneuropathy with lymphoid irradiation.  Muscle and Nerve  8:223-232.

 

2.         Holers, V. M., and Kotzin, B. L.  1985.  Human peripheral blood monocytes display surface antigens recognized by monoclonal antinuclear antibodies.  J. Clin. Invest. 76:991-998.

 

3.         Seya, T., Holers, V. M., and Atkinson, J. P.  1985.  Purification and functional analysis of polymorphic variants of CR1.  J. Immunol. 135:2661-2667.

 

4.         Holers, V. M., Seya, T., Brown, E., O'Shea, J. J., and Atkinson, J. P.  1986.  Structural and functional studies on the human C3b/C4b receptor (CR1) purified by affinity chromatography using a monoclonal antibody.  Complement 3:63-78.

 

5.         Yu, G., Holers, V. M., Seya, T., Ballard, L., and Atkinson, J. P.  1986.  Structural and functional characterization of a C3-binding membrane protein of human platelets.  J. Clin. Invest. 78:494-501.

 

6.         Nickells, M., Seya, T., Holers, V. M., McCourt, D., Leykam, J., and Atkinson, J. P.  1986.  Analysis of C3b/C4b receptor (CR1) polymorphic variants by tryptic peptide mapping.  Mol. Immunol. 23:661-668.

 

7.         VanDyne, S., Holers, V. M., Lublin, D. M., and Atkinson, J. P.  1987.  The polymorphism of the C3b/C4b receptor in the normal population and in patients with systemic lupus erythematosus Clin. Exp. Immunol. 68:570-579.

 

8.         Holers, V. M., Chaplin, D. D., Leykam, J. F., Gruner, B. A., and Atkinson, J. P.  1987.  A human C3b/C4b receptor (CR1) poly A-mRNA polymorphism related to the CR1 allelic Mr polymorphism.  Proc. Natl. Acad. Sci. 84:2459-2463.

 

9.         Medof, M. E., Lublin, D. M., Holers, V. M., Ayers, D. J., Atkinson, J. P., Getty, R. N., Leykam, J. F., and Tykocinski, M. L.  1987.  Characterization of cDNAs coding for the complete sequence of decay accelerating factor of human complement.  Proc. Natl. Acad. Sci. 84:2007-2011.

 

10.       Lublin, D. M., Lemons, R. S., LeBeau, M. M., Holers, V. M., Tykocinski, M. L., Medof, M. E., and Atkinson, J. P.  1987.  The gene encoding Decay-Accelerating Factor (DAF) is located in the complement regulatory locus on the long arm of chromosome 1.  J. Exp. Med. 165:1731-1735.

 

11.       McNearney, T. A., Odell, C., Holers, V. M., Spear, P. G. and Atkinson, J. P.  1987.  Herpes simplex virus glycoproteins gC-1 and gC-2 bind to the third component of complement and provide protection against complement mediated neutralization of viral infectivity.  J. Exp. Med. 166:1525-1535.

 

12.       Stafford, H. A., Tykocinski, M. L., Lublin, D. M., Holers, V. M., Rose, W. F., Atkinson, J. P. and Medoff, M. E.  1987.  Normal polymorphic variations and transcription of the decay accelerating factor gene in paroxysmal nocturnal hemoglobinuria cells.  Proc. Nat'l. Acad. Sci. 85:880-884.

 

13.       Hourcade, D., Miesner, D. R., Atkinson, J. P., and Holers, V. M.  1988.  Identification of an alternative polyadenylation site in the human C3b/C4b receptor (CR1) transcriptional unit and prediction of a secreted form.  J. Exp. Med. 168:1255-1270.

 

14.       Bora, N. S., Lublin, D. M., Kumar, B. V., Hockett, R. D., Holers, V. M., and Atkinson, J. P.  1989.  Structural gene for MCP maps to within 100 kB of the 3' end of the C3b/C4b receptor (CR1) gene.  J. Exp. Med. 169:597-602.

 

15.       Fujisaku, A., Harley, J. B., Frank, M. B., Gruner, B. A., Frazier, B., and Holers, V. M.  1989.  Genomic organization and polymorphisms of the human C3d/Epstein-Barr Virus receptor (CR2).  J. Biol. Chem. 264:2118-2125.

 

16.       O'Dell, J. R., Steigerwald, J. C., Kennaugh, R. C., Hawkins, R., Holers, V. M., and Kotzin, B. L.  1989.  Lack of clinical benefit after treatment of systemic sclerosis with total lymphoidal irradiation.  J. Rheum. 16:1050-1054.

 

17.       Holers, V. M., Ruff, T. G., Parks, D. L., McDonald, J. A., Ballard, L. L., and Brown, E. J.  1989.  Molecular cloning of a murine fibronectin receptor and its expression during inflammation.  J. Exp. Med. 169:1589-1605.

 

18.       Carel, J.-C., Frazier, B., Ley, T. J., and Holers, V.M.  1989. Analysis of epitope expression and the functional repertoire of recombinant Complement Receptor 2 (CR2/CD21) in mouse and human cells.  J. Immunol. 143:923-930.

 

19.       Carel, J.-C., Myones, B. L., Frazier, B., and Holers, V. M.  1990.  Structural requirements for C3d,g/Epstein-Barr virus receptor (CR2/CD21) ligand binding, internalization and viral infection.  J. Biol. Chem. 265:12293-12299.

 

20.       Hourcade, D., Post, T. W., Holers, V. M., Lublin, D. M., and Atkinson, J. P.  1990.  Polymorphisms of the Complement activation (RCA) gene cluster.  Complement Inflammation 7:302-314.

 

21.       Molina, H., Kinoshita, T., Inoue, K., Carel, J.-C., and Holers, V.M.  1990.  A molecular and immunochemical characterization of mouse CR2: Evidence for a single gene model of mouse Complement Receptors 1 and 2.  J. Immunol. 145:2974-2983.

 

22.       Rayhel, E. J., Dehoff, M. H., and Holers, V. M.  1991.  Characterization of the human CR2 promoter reveals sequence identities with promoters for other developmentally restricted B cell proteins.  J. Immunol. 146:2021-2026.

 

23.       Ballard, L. L., Brown, E. J., and Holers, V. M.  1991.  Expression of the fibronectin receptor VLA-5 is regulated during human B cell differentiation and activation.  Clin. Exp. Immunol. 84:336-346.

 

24.       Carel, J.-C., Holers, V. M., Chick, W. L., Littman, D., and Lacy, P. E.  1991.  Expression of functional human complement receptor 2 (CR2, CD21, C3d/EBV receptor) on an insulinoma cell line induces tumor rejection but not diabetes in syngeneic rats.  Diabetes 40:809-814.

 

25.       Molina, H., Brenner, C., Jacobi, S., Gorka, J., Carel, J.-C., Kinoshita, T., and Holers, V. M.  1991.  Analysis of Epstein-Barr Virus binding sites on Complement Receptor 2 using human-mouse chimeras and peptides.  J. Biol. Chem. 266:12173-12179.

 

26.       Secrist, H., Holers, V. M., Egan, M., Nahm, M. H., Butch, A. W. and Peters, M.  1991.  Induction of IL-4 and IL-6 in vitro: variation in signalling requirements and kinetics are dependent on the anatomic source of the responding mononuclear cells.  Regional Immunol. 3:341-348.

 

27.       Molina, H., Wong, W., Kinoshita, T., Brenner, C., Foley, S., and Holers, V. M.  1992.  Distinct receptor and regulatory properties of recombinant mouse Complement Receptor 1 (CR1) and Crry, the two genetic homologs of human CR1.  J. Exp. Med. 175:121-129.

 

28.       Hourcade, D., Garcia, A. D., Post, T. W., Taillon-Miller, P., Holers, V. M., Wagner, L. M., Bora, N. S. and Atkinson, J. P.  1992.  Analysis of the Regulators of Complement Activation (RCA) gene cluster with yeast artificial chromosomes (YACs).  Genomics 12:289-300.

 

29.       Emlen, W., Holers, V. M., Arend, W. P., and Kotzin, B.  1992.  Regulation of nuclear antigen expression on the cell surface of human monocytes.  J. Immunol. 148:3042-3048.

 

30.       Levy, E., Tung, K., Ambrus, J., Kahl, L., White, G., and Holers, V. M.  1992.  Complement Receptor 2 expression on a T cell subpopulation in normals and patients with Systemic Lupus Erythematosus: Expansion in a patient with active disease.  Clin. Exp. Immunol. 90:235-244.

 

31.       Foley, S., Li, B., Dehoff, M., Molina, H., and Holers, V. M.  1993.  Mouse Crry/p65 is a regulator of the alternative pathway of complement activation.  Eur. J. Immunol. 23:1381-1384

 

32.       Li, B., Sallee, C., Dehoff, M., Foley, S., Molina, H., and Holers, V. M.  1993.  Mouse Crry/p65: Characterization of mAbs and the tissue distribution of a functional homologue of human MCP and DAF. J. Immunol. 151:4295-4305.

 

33.       Holers, V. M., Hollis, G. F., Schwartz, B. D., Evans, R. J., Strauss-Schoenberger, J., Carel, J.-C., Barney, D. L., Li, B., Stafford-Hollis, J., and Lacy, P. E.  1993.  Induction of peri-insulitis but not diabetes in islet transplants expressing a single foreign antigen: a multi-stage model of disease.  J. Immunol.  151:5041-5052.

 

34.       Aubry, J.-P., Pochon, S., Gauchat, J.-F., Holers, V. M., Graber, P., Siegfried, C., and Bonnefoy, J.-Y. 1994.  Mapping of the CD23 binding site on CD21. J. Immunol. 152:5806-5813.

 

35.       Molina, H., Kinoshita, T., Webster, C. B., and Holers, V. M. 1994. Analysis of C3b/C3d binding sites and the factor I cofactor regions within mouse complement receptors 1 and 2. J. Immunol. 153:789-795.

 

36.       Graham, I., Anderson, D. C., Holers, V. M., and Brown, E. J.  1994.  Complement receptor 3 (CR3, Mac-1, Integrin m, CD11b/CD18) is required for tyrosine phosphorylation of paxillin in adherent and non-adherent neutrophils. J. Cell Biol.  127:1139-1147.

 

37.       Kim, Y. U., Kinoshita, T., Molina, H., Hourcade, D., Seya, T., Wagner, L. M., and Holers, V. M.  1995.  Mouse complement regulatory protein Crry/p65 utilizes the specific mechanisms of both human decay-accelerating factor (DAF) and membrane cofactor protein (MCP). J. Exp. Med.  181:151-159.

 

38.       Quigg, R. J., Holers, V. M., Morgan, B. P., and Sneed, III, A. E.  1995.  Crry and CD59 regulate complement in rat glomerular epithelial cells and are inhibited by the nephritogenic antibody of passive Heymann nephritis.  J. Immunol. 154:3437-3443.

 

39.       Molina, H., Perkins, S. J., Guthridge, J., Gorka, J., Kinoshita T., and Holers, V. M.  1995.  Characterization of a complement receptor 2 (CR2, CD21) ligand binding site for C3: an initial model of ligand interaction with two linked SCR modules.  J. Immunol.  154:5426-5435.

 

40.       Kozono, Y., Duke, R. C., Schleicher, M., and Holers, V. M.  1995.  Co-ligation of mouse complement receptors 1 and 2 with sIgM rescues splenic B cells and WEHI-231 cells from anti-sIgM-induced apoptosis.  Eur. J. Immunol.  25:1013-1017.

 

41.       Quigg, R. J., Morgan, B. P., Holers, V. M., Adler, S., and Sneed, III, A. E.  1995.  Complement regulation in the rat glomerulus: Crry and CD59 regulate complement in glomerular mesangial and endothelial cells.  Kidney Intl.  48:412-421.

 

42.         Sima, M., Teitelbaum, S. L., Holers, V. M., Ruzicka, C., Osmack, P., and Ross, F. P.  1995.  Macrophage-colony-stimulating factor regulates expression of the integrins 41 and 51by murine bone marrow macrophages.  Proc. Natl. Acad. Sci. 92:5179-5183.

 

43.       Quigg, R. J., and Holers, V. M.  1995.  Characterization of rat complement receptors and regulatory proteins.  CR2 and Crry are conserved while the C3b receptor of neutrophils and platelets is distinct from CR1.  J. Immunol.  155:1481-1488.

 

44.       Bouillie, S., Barel, M., Drane, P., Cassinat, B., Balbo, M., Holers, V. M., and Frade, R. F.  1995.  Epstein-Barr virus/C3d receptor (CR2,CD21) activated by its extracellular ligands regulates pp105 phosphorylation through two distinct pathways.  Eur. J. Immunol. 25:2661-2667.

 

45.       Dunster, L. M., Schneider-Schaulies, J., Dehoff, M. H., Holers, V. M., Schwartz-Albiez, R., and ter Meulen, V.  1995.  Moesin, and not the murine functional homologue (Crry/p65) of human MCP (CD46), is involved in the entry of measles virus (strain Edmonston) into susceptible murine cell lines.  J. Gen. Virol. 76:2085-2089.

 

46.         Sawant-Mane, S., Piddlesden, S. J., Morgan, B. P., Holers, V. M., and Koski, C. L.  1996.  CD59 homologue regulates complement-dependent cytolysis of rat Schwann cells.  J. Neuroimmunol. 69:63-71.

 

47.       Molina, H., Holers, V. M., Li, B., Fang, Y.-F., Mariathasan, S., Goellner, J., Strauss-            Schoenberger, J., Karr, R. W., and Chaplin, D. D.  1996.  Markedly impaired humoral     immune response in mice deficient in complement receptors 1 and 2. Proc. Natl. Acad.     Sci. 93:3357-3361.

 

48.       Rogers, C. A., Gasque, P., Piddlesden, S.J., Okada, N., Holers, V. M., and Morgan, B. P. 1996.  Expression and function of membrane regulators of complement on rat astrocytes in culture.  Immunology 88:153-161.

 

49.       Kozono, Y., Kotzin, B. L., and Holers, V. M.  1996.  Resting B cells from NZB mice             demonstrate a defect in apoptosis induction following sIgM ligation.  J. Immunol.            156:4498-4503.

 

50.       Boackle, S. A., Holers, V. M., and Karp, D. K.  1997.  CD21 augments antigen      presentation in immune individuals.  Eur. J. Immunol. 27:122-130.

 

51.       Alexander, J. J., He, C., Adler, S., Holers, V. M., and Quigg, R. J.  1997.  Characterization of C3 receptors on cultured rat glomerular endothelial cells.  Kidney Intl. 51:1124-1132.

 

52.       Kawamoto, Y., Kojima, K., Hitsumoto, Y., Okada, H., Holers, V. M., and Miyama, A.   1997.  Studies on the serum resistance of malaria-infected erythrocytes.  Immunology 91:7-12.

 

53.       Vigneau-Hermellin, M., Vitali, L., Tardivel, I., Rabaud, M, Holers, V. M., and Carel, J.-      C.  1997.  Rejection of islets differing by a single antigen is dependent on donor MHC.        Diabetes 46:765-769.

 

54.       Quigg, R. J., Alexander, J. J., Lo, C. F., and Holers, V. M.  1997.  Characterization of C3-binding proteins on mouse neutrophils and platelets. J. Immunol. 159:2438-2444.

 

55.       Takahashi, K., Kozono, Y., Waldschmidt, T. J., Berthiaume, D., Quigg, R. J., Baron, A., and       Holers, V. M.  1997. Mouse complement receptors type 1 (CR1, CD35) and 2 (CR2, CD21):        expression on             normal B cell subpopulations and decreased levels during the development of    autoimmunity in MRL/lpr mice. J. Immunol. 159:1557-1569.

 

56.         Kearns-Jonker, M., Monell-Torrens, E., Abbasi, F., Holers, V. M., Notkins, A. L., and Sigounas, G.  1997.  EBV binds to lymphocytes of transgenic mice that express the human CR2 gene.  Virus Research 50:85-94.

 

57.       Makar, K. W., Pham, C., Dehoff, M., O'Connor, S., Jacobi, S., and Holers, V. M.  1998. An intronic silencer regulates B lymphocyte cell and stage specific expression of the human complement receptor type 2 (CR2,CD21) gene. J. Immunol. 160:1268-1278.

 

58.       Kozono, Y., Abe, R., Kozono, H., Kelly, R. G., Azuma, T. and Holers, V. M.  1998.  Crosslinking CD21/CD35 or CD19 rapidly increases both B7-1 and B7-2 expression on murine splenic B cells. J. Immunol. 160: 1565-1572.

 

59.         Quigg, R. J., Kozono, Y., Berthiaume, D., Lim, A., Salant, D. J., Weinfeld, A., Griffin, P., Kremmer, E., and Holers, V. M. 1998.  Blockade of antibody-induced glomerulonephritis with Crry-Ig, a soluble murine complement inhibitor. J. Immunol. 160:4553-4560.

 

60.       Fang, Y., Xu, C., Holers, V. M., and Molina, H.  1998.  Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a normal antigen-specific IgG response.  J. Immunol. 160:5273-5279.

 

61.       Nichols, T. C., Guthridge, J. M., Karp, D. R., Molina, H., Fletcher, D. R., and Holers, V. M.  1998.  -Glutamyl Transpeptidase, an ecto-enzyme regulator of intracellular redox potential, is a component of TM4 signal transduction complexes. Eur. J. Immunol.  28:4123-4129.

 

62.       Boackle, S. A., Morris, M. A.           , Holers, V. M., and Karp, D. R.  1998.  Complement opsonization is required for presentation of immune complexes by resting peripheral blood B cells.  J. Immunol.  161:6537-6543.

 

63.         Quigg, R. J. He, C., Lim, A. Berthiaume, D., Alexander, J. J., Kraus, D., and Holers, V. M.  1998.  Transgenic mice overexpressing the complement inhibitor Crry as a soluble protein are protected from antibody-induced glomerular injury.  J. Exp Med.  188:1321-1331.

 

64.         Nardin, A., Schlimgen, R., Holers, V. M., and Taylor, R. P., 1999.  A prototypic pathogen bound ex vivo to human erythrocyte complement receptor 1 via bispecific monoclonal antibody complexes is cleared to the liver in a mouse model. Eur. J. Immunol.  29:1581-1586.

 

65.         Alexander, J. J., Lim, A., He, C., MacDonald, R. L., Holers, V. M., and Quigg, R. J. 1999.  Renal, central nervous system and pancreatic overexpresion of recombinant soluble Crry in transgenic mice.  A novel means of protection from complement-mediated injury.  Immunopharmacology 42:245-254.

 

66.         Henson, S. E., Nichols, T. C., Holers, V. M., and Karp, D. R. 1999.  The ectoenzyme gamma glutamyl transpeptidase regulates anti-proliferative effects of S-Nitrosoglutathione on human T and B lymphocytes. J. Immunol. 163:1845-1852.

 

67.         Karp, D. K., Nichols, T. C., Oppenheimer-Marks, N., Brezinschek, R. I., and Holers, V. M.  1999.  Gamma-glutamyl transpeptidase is upregulated on memory T lymphocytes.  International Immunol.  11:1791-1800.

 

68.         Davoust, N., Nataf, S., Holers, V. M., and Barnum, S. R.  1999.  Expression of the murine complement regulatory protein Crry by glial cells and neurons.  Glia 27:162-170.

 

69.         Davoust, N., Nataf, S., Reiman, R., Holers, V. M., Campbell, I. L., and Barnum, S. R.  2000.  CNS-targeted expression of the complement inhibitor sCrry prevents experimental allergic encephalomyelitis. J. Immunol.  163:6551-6556.

 

70.         Watanabe, H., Garnier, G., Circolo, A., Wetsel, R. A., Ruiz, P., Holers, V. M., Boackle, S. A., Colten, H. R., and Gilkeson, G. S.  2000.  Modulation of renal disease and C3 consumption in MRL/lpr mice genetically deficient in factor B of the alternative complement pathway. J. Immunol.  164:786-794.

 

71.         Cunningham, P., Holers, V. M., Alexander, J. J., Guthridge, J. M., Carroll, M. C., and Quigg, R. J. 2000.  Renal complement activation occurs with endotoxin administration, but is not responsible for the resultant acute renal failure. Kidney Intl. 58:1580-1587.

 

72.         Xu, C., Mao, D., Holers, V. M., Palanca, B., Cheng, A., and Molina, H.  2000.  A critical role for the murine complement regulator Crry in fetomaternal tolerance.  Science  287:498-501.

 

73.         Marchbank, K. J., Watson, C. C., Ritsema, D. F., and Holers, V. M.  2000.  Expression of complement receptor 2 (CR2/CD21) in Cr2-/- mice restores humoral immune function. J. Immunol. 165:2354-2361.

 

74.         Makar, K. W., Uligiati, D., Hagman, J., and Holers, V. M.   2001.  A site in the complement receptor 2 (CR2/CD21) silencer is necessary for lineage specific transcriptional regulation. International Immunol. 13:657-664.

 

75.         Schiller, B., Cunningham, P., Alexander, J. J., Couser, W. G., Holers, V. M., and Quigg, R. J.  2001.  Transgenic mice over-expressing soluble complement inhibitor Crry are protected from antibody induced acute renal failure. J. Am. Soc. Nephrol.  12:71-79.

 

76.         Kaya, Z, Afanasyeva, M., Wang, Y., Dohman, K. M., Schlichting, J., Tretter, T., Fairweather, D., Holers, V. M., and Rose, N. R.  2001. Contribution of the innate immune system to autoimmune myocarditis: a role for complement.  Nature Immunol. 2:739-745.

 

77.         Szakonyi, G., Guthridge, J. M., Li, D., Young, K., Holers, V. M., and Chen, X. S. 2001. Structure of complement receptor 2 in complex with its C3d ligand.  Science 292:1725-1728.

 

78.         Springall, T., Sheerin, N. S., Abe, K., Holers, V. M., Wan, H., and Sacks, S. H.  2001  Epithelial secretion of C3 promotes colonization of the upper urinary tract by Escherichia coli. Nature Medicine 7:801-806.

 

79.         Sekine, H., Reilly, C. M., Molano, I. D., Garnier, G., Circolo, A., Ruiz, P., Holers, V. M., Boackle, S. A., and Gilkeson, G. S.  2001.  Complement component C3 is not required for full expression of immune complex glomerulonephritis in MRL/lpr mice. J. Immunol. 166:6444-6451.

 

80.         Guthridge, J. M., Rakstang, J. K., Young, K. A., Hinshelwood, J., Aslam, M., Robertson, A., Gipson, M. G., Sarrias, M. and Holers, V. M.  2001.  Structural studies in solution of the recombinant N-terminal pair of short consensus/complement repeat domains of complement receptor type 2 (CR2/CD21) and interactions with its ligand C3dg.  Biochemistry 40:5931-5941.

 

81.         Park, P., Haas, M., Cunningham, P. N., Alexander, J. J., Bao, L., Guthridge, J. M., Kraus D. M., Holers, V. M., and Quigg, R. J.  2001.  Inhibiting the complement system does not reduce injury in renal ischemia reperfusion.  J. Am. Soc. Nephrol. 12:1383-1390.

 

82.         Guthridge, J. M., Young, K., Gipson, M. G., Sarrias, M.-R., Szakonyi, G., Chen, X. S., Malaspina, A., Donoghue, E., James, J. A., Lambris, J. D., Moir, S. A., Perkins, S. J., and Holers, V. M.  2001.  Epitope mapping using the x-ray crystallographic structure of complement receptor type 2 (CR2/CD21): Identification of a highly inhibitory monoclonal antibody that directly recognizes the CR2-C3d interface.  J. Immunol. 167:5758-5766.

 

83.         Boackle, S. A., Holers, V. M., Chen, X., Szakonyi, G., Karp, D. R., Wakeland, E. K., and Morel, L.  2001.  Cr2, a candidate gene in the murine Sle1c lupus susceptibility locus, encodes a dysfunctional protein.  Immunity 15:775-785.

 

84.         Rehrig, S., Fleming, S., Anderson, J., Guthridge, J., McQueen, C., Holers, V. M., Tsokos, G. C., and Shea-Donohue, T.  2001.  Crry-Ig attenuates intestinal damage after the onset of mesenteric ischemia/reperfusion injury in mice.  J. Immunol. 167:5921-5927.

 

85.       Henson, S. E., Smith, D., Boackle, S. A., Holers, V. M., and Karp, D. R.  2001.  Generation of recombinant human C3dg tetramers for the analysis of CD21 binding and function.  J. Immunol. Meth.  258:97-109.

 

86.       Ulgiati, D., and Holers, V. M.  2001.  CR2/CD21 proximal promoter activity is critically dependent on a cell type specific repressor.  J. Immunol.  167:6912-6919.

 

87.       Bao, L., Haas, M., Boackle, S. A., Kraus, D. M., Cunningham, P. N., Park, P., Alexander, J. J., Anderson, R. K., Culhane, K., Holers, V. M., and Quigg, R. J.  2002.  Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/lpr mice J. Immunol. 168:3601-3607.

 

88.       Holers, V. M., Girardi, G., Mo, L., Guthridge, J. M., Molina, H., Pierangeli, S. S., Espinola, R., Xiaowei, L. E., Mao, D., Vialpando, C. G., and Salmon, J. E.  2002.  Complement C3 activation is required for anti-phospholipid antibody-induced fetal loss.  J. Exp. Med. 195:211-220.

 

89.       Ulgiati, D., Pham, C., and Holers, V. M.  2002.  Functional analysis of the human CR2/CD21 promoter: Characterization of basal transcriptional mechanisms.  J. Immunol. 168:6279-6285.

 

90.       Ji, H. Ohmura, K., Mahmood, U., Lee, D. M., Hofhuis, F. M., Boackle, S. A., Takahashi, K., Holers, V. M., Walport, M., Gerard, C. Ezekowitz, A., Carroll, M. C., Brenner, M., Weissleder, R., Verbeek, J. S., Duchatelle, V., Degott, C., Benoist, C., and D. Mathis.  2002.  Arthritis critically dependent upon innate immune players.  Immunity 16: 157-168.

 

91.       Fleming, S. D., Shea-Donohue, T., Guthridge, J. M., Kulik, L., Waldschmidt, T. J., Gipson, M. G., Tsokos, G. C., and Holers, V. M.  2002.  Mice deficient in complement receptors 1 and 2 lack a tissue injury-inducing subset of the natural antibody repertoire.  J. Immunol. 169:2126-2133.

 

92.       Banda, N. K., Kraus, D., Vondracek, A., Huynh, L. H., Bendele, A., Holers, V. M., and Arend, W. P.  2002.  Mechanisms of effects of complement inhibition in murine collagen-induced arthritis.  Arth. Rheum. 46:3065-3075.

 

93.         Marchbank, K. J., Kulik, L., Gipson, M. G., Morgan, B. P., and Holers, V. M.  2002.  Expression of human complement receptor type 2 (CR2/CD21) in mice during early B cell development results in a reduction in mature B cells and hypogammaglobulinemia.  J. Immunol. 169:3526-3535.

 

94.       Ji, S., Holers, V. M., Boackle, S. A., and Blatteis, C. M.  2002.  Modulation of mouse endotoxic fever by complement.  Infect. Immun.  70:2519-2525.

 

95.       Bao L., Haas, M. Kraus, D. M., Hack, B. K., Rakstang, J. K, Holers, V. M., and Quigg, R. J.  2003.  Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice.  J. Am. Soc. Nephrol.  14:670-679.

 

96.       Thurman, J. M., Ljubanovic, D., Edelstein, C. L., Gilkeson, G. S, and Holers, V. M.  2003.  Lack of a functional alternative complement pathway ameliorates ischemic renal failure in mice.  J. Immunol. 170: 1517-1523.

 

97.       Elliott, M. K., Ruiz, P., Xu, Y., Holers, V. M., and Gilkeson, G. S.  2004.  Effects of complement factor D deficiency on the development of renal disease in MRL/lpr mice.  Kidney Intl. 65:129-138.

 

98.       Alexander, J. J., Bao, L., Jacob, A., Dyanov, H. M., Rakstang, J. K., Holers, V. M., and Quigg, R. J.  2003.  Administration of the soluble complement inhibitor, Crry-Ig, reduces inflammation and aquaporin 4 expression in lupus cerebritis.  Biochim. Biophys. Acta 1639:169-176.        

 

99.         Song, H., He, C., Knaak, C., Guthridge, J. M., Holers, V. M., and Tomlinson, S.  2003.  Complement receptor 2 (CR2)-mediated targeting of complement inhibitors to sites of complement activation. J. Clin. Invest. 111:1875-1885.

 

100.      Bao, L., Zhou, J., Holers, V. M., and Quigg, R. J.  2003. Excessive matrix accumulation in the kidneys of MRL/lpr lupus mice is dependent on complement activation. J. Am. Soc. Nephrol.  14:2516-2525.

 

102.      Girardi, G., Berman, J., Redecha, P., Spruce, L., Kraus, D., Hollmann, T., Casali, P., Wetsel, R. A., Lambris, J. D., Holers, V. M., and Salmon, J. E.  2003.  Complement C5a receptors and neutrophils, but not activating Fc receptors, are critical mediators of anti-phospholipid antibody-induced fetal loss. J. Clin. Invest. 112:1644-1654.

 

103.      Aslam, M., Guthridge, J. M., Hack, B. K., Quigg, R. J., Holers, V. M., and Perkins, S. J.  2003.  The extended multidomain solution structures of the complement protein Crry and its chimaeric conjugate Crry-Ig by scattering, analytical ultracentrifugation and constrained modelling: implications for function and therapy.  J. Mol. Bio. 329:525-550.

 

104.      Banda, N.K., Kraus, D. M., Muggli, M., Bendele, A., Holers, V. M., and Arend, W. P.  2003.  Prevention of collagen-induced arthritis in mice transgenic for the complement inhibitor complement receptor 1-related gene/protein y.  J. Immunol. 171:2109-2115.

 

105.      Taube, C., Rha, Y.-H., Takeda, K., Park, J.-W., Joetham, A., Balhorn, A., Dakhama, A., Giclas, P. C., Holers, V. M., and Gelfand, E. W.  2003.  Inhibition of complement activation during airway challenge decreases airway inflammation and hyperresponsiveness.  Am. J. Resp. and Crit. Care Med. 168:1333-1341.

 

106.      Salmon, J.E., Girardi, G., and Holers, V. M.  2003.  Activation of complement mediates antiphospholipid antibody-induced pregnancy loss.  Lupus 12:535-538.

 

107.      Park, J.W., Taube, C., Joetham, A., Takeda, K., Kodama, T., Dakhama, A., McConville, G., Allen, C.B., Sfyroera, G., Schultz, L.D., Lambris, J.D., Giclas, P.C., Holers, V. M., and Gelfand, E. W.  2003.  Complement activation is critical to airway hyperresponsiveness after acute ozone exposure.  Am. J. Resp. and Crit. Care Med. 169:726-732.

 

108.      Kang, H.J., Bao, L., Xu, Y., Quigg, R.J., Giclas, P.C., and Holers, V.M.  2004. Increased serum C3 levels in Crry transgenic mice partially abrogates its complement inhibitory effects.  Clin. Exp. Immunol.  136:194-199.

 

109.      Muhlfeld, A.S., Segerer, S., Hudkins, K., Farr, A.G., Boa, L., Kraus, D., Holers, V.M., Quigg, R.J., Alpers, C.E.  2004.  Overexpression of Crry does not prevent cryoglobulin-associated membranoproliferative glomerulonephritis.  Kidney Intl.  65:1214-1223.

 

110.      Boackle, S.A., Culhane, K.K., Brown, J.M., Haas, M., Bao, L., Quigg, R.J., and Holers, V.M.  2004.  CR1/CR2 deficiency alters IgG3 autoantibody production and IgA glomerular deposition in MRL/lpr model of SLE.  Autoimmunity  37:111-123.

 

111.      Ohta, R., Kondor, N., Dohi, N., Tomlinson, S., Imai, M., Holers, V.M., Okada, N., and Okada, H.  2004.  Mouse Crry/p65 neutralized tumor vaccine induces antitumor activity in vivo.  J. Immunol.  173:205-213.

 

112.      Mikuls, T.R., O’Dell, J.R., Stoner, J.A., Parrish, L.A., Arend, W.P., Norris, J.M., and Holers, V.M.  2004.  The association of rheumatoid arthritis treatment response and disease duration with declines in serum levels of IgM rheumatoid factor and anti-CCP antibody. Arth. Rheum.  50:3776-3782.

 

113.      Fleming, S.D., Egan, R.P., Chai, C., Girardi, G., Holers, V.M., Salmon, J., Monestier, M., and Tsokos, G.C.. 2004. Antiphospholipid antibodies restore mesenteric ischemia-reperfusion-induced injury in complement receptor 2/complement receptor 1-deficient mice.  J. Immunol.  173:7055-7061.

 

114.      Thurman, J.M., Kraus, D.M., Girardi, G., Hourcade, D., Kang, H.J., Royer, P.A., Mitchell, L.M., Giclas, P.C., Salmon, J.E., Gilkeson, G.S., and Holers, V.M.  2005.  A novel inhibitor of the alternative complement pathway prevents antiphospholipid antibody-induced pregnancy loss in mice.  Mol. Immunol.  42:87-97.

 

115.      Ferucci, E.D., Majka, D.S., Parrish, L.A., Moroldo, M.B., Ryan, M., Passo, M., Thompson, S.D., Deane, K.D., Rewers, M., Arend, W.P., Glass, D.N., Norris, J.M., and Holers, V.M.  2005.  Antibodies against citrullinated peptide (CCP) are associated with HLA-DR4 in simplex and multiplex polyarticular juvenile rheumatoid arthritis.  Arth. Rheum. 52:239-246.

 

116.      Lyubchenko, T., dal Porto, J., Cambier, J.C., and Holers, V.M.  2005.  Co-ligation of the B cell receptor with complement receptor type 2 (CR2/CD21) using its natural ligand C3dg: activation without engagement of an inhibitory signaling pathway.  J. Immunol.  174:3264-3272.

 

117.      Gilbert, H.E., Eaton, J.T., Hannan, J.P., Holers, V.M., and Perkins, S.J. 2005. Solution structure of the complex between CR2 SCR 1-2 and C3d of human complement: an X-ray scattering and sedimentation modelling study.  J. Mol. Biol. 346:859-873.

 

118.      Hannan, J.P., Young, K.A., Guthridge, J.M., Asokan, R., Szakonyi, G., Chen, X.S., and Holers, V.M.  2005.  Mutational analysis of the complement receptor type 2 (CR2/CD21)–C3d interaction reveals a putative charged SCR1 binding site for C3d.  J.  Mol. Biol. 346:845-858.

 

119.      Thurman, J.M., Lucia, M.S., Ljubanovic, D., and Holers, V.M.  2005.  Acute tubular necrosis is characterized by activation of the alternative pathway of complement.  Kidney. Intl.  67:524-530.

 

120.      Li, S., Boackle, S.A., Holers, V.M., Lambris, J.D., and Blatteis, C.M.  2005.  Complement C5a is integral to the febrile response of mice to lipopolysaccharide.  Neuroimmunomodulation 12:67-80.

 

121.      Hibbert, R.G., Teriete, P., Grundy, G.J., Holers, V.M., Hannan, J.P., Sutton, B.J., Gould, H.J. and McDonnell, J.M. 2005. The structure of soluble CD23 and its interactions with IgE and CD21. J. Exp. Med 202:751-760.

 

122.      Birrell, L., Kulik, L., Morgan, B.P., Holers, V.M., and Marchbank, K.J., 2005. B cells from mice prematurely expressing human CR2/CD21 are unresponsive to T-dependent antigens. J. Immunol. 174:6974-6982.

 

123.      Atkinson, C., Song, H., Lu, B., Qiao, F., Burns, T.A., Holers, V.M., Tsokos, G.C., and Tomlinson, S.  2005. Targeted complement inhibition by C3d recognition ameliorates tissue injury without apparent increase in susceptibility to infection.  J. Clin. Invest. 115:2444-2453.

 

124.      Kuhn, K.A., Kulik, L., Tomooka, B., Braschler, K.J., Arend, W.P., Robinson, W.H., and Holers, V.M.  2006.  Antibodies to citrulline-modified proteins enhance tissue injury in inflammatory arthritis. J. Clin. Invest. 116:961-973.

 

125.      Taube, C., Thurman, J.M., Joetham, A., Takeda, K., Miyahara, N., Dakhama, A., Carroll, M.C., Giclas, P.C., Holers, V.M., and Gelfand, E.W. 2006. Factor B of the alternative pathway is critical to development of airway hyperresponsiveness. Proc. Natl. Acad. Sci. 103:8084-8089.

 

126.      Gilbert, H.E., Aslam, M., Guthridge, J.M., Holers, V.M., and Perkins, S.J.  2006.  Extended flexible linker structures in the complement chimaeric conjugate CR2-Ig by scattering, analytical ultracentrifugation and constrained modelling: Implications for function and therapy.  J.  Mol. Biol. 356:397-412.

 

127.      Thurman, J.M., Royer, P.A., Ljubanovic, D., Dursun, B., Lenderink, A.M., Edelstein, C.L., and Holers, V.M.  2006.  Treatment with an inhibitory monoclonal antibody to mouse factor B protects mice from induction of apoptosis and renal ischemia/reperfusion injury.  J. Am. Soc. Nephrol. 17:707-715..

 

128.      Kraus, D.M., Elliott, G.S., Chute, H., Horan, T., Pfenninger, K.H., Sanford, S.D., Foster, S., Scully, S., Welcher, A.A. and Holers, V.M.  2006.  Identification of a novel multiple domain complement regulatory proteins highly expressed in the central nervous system and epithelial tissues.  J. Immunol. 176:4419-4430.

 

129.      Thurman, J.M., Ljubanovic, D., Royer, P.A., Kraus, D.M., Molina, H., Barry, N.P., Proctor, G., Levi, M., and Holers, V.M.  2006.  Altered renal tubular expression of the complement inhibitor Crry permits complement activation after ischemia/reperfusion.  J. Clin. Invest. 116:357-368.

 

130.      Leinhase, I., Schmidt, O.I., Thurman, J.M., Rozanski, M., Scheffler, A., John, T., Smith, W.R., Holers, V.M., and Stahel, P.F.  2006.  Pharmacological complement inhibition at the C3 convertase level induces neuroprotective intracerebral gene expression and decreases neurological impairment after traumatic brain injury.  Exp. Neurol. 199:454-463.

 

131.      Leinhase, I., Holers, V.M., Thurman, J.M., Harhausen, D., Schmidt, O.I., Pietzcker, M., Taha, M.E., Rittirsch, D., Huber-Lang, M., Smith, W.R., Ward, P.A., and Stahel, P.F.  2006.  Reduced neuronal cell death after experimental brain injury in mice lacking a functional alternative pathway of complement activation.  BMC Neurosci. 7:55.

 

132.      Mikuls, T.R., Holers, V.M., Parrish, L.A., Alarcon, G.S., Conn, D.L., Gilkeson, G., Smith, E.A., Kamen, D.L., Jonas, B.L., Callahan, L., Howard, G., Moreland, L.W., and Bridges, Jr., S.L.  2006.  Anti-cyclic citrullinated peptide (CCP) antibody and rheumatoid factor isotypes in African Americans with early rheumatoid arthritis.  Arth. Rheum. 154:3057-3059.

 

133.      Banda, N.K., Thurman, J.M., Kraus, D.M., Wood, A., Carroll, M.C., Arend, W.P., and Holers, V.M.  2006.  Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis.  J. Immunol. 177:1904-1912.

 

134.      Schepers, A., de Vries, M.R., van Leuven, C.J., Grimbergen, J.M., Holers, V.M., Daha, M.R., van Bockel, J.H., and Quaz, P.H.A.  2006.  Inhibition of complement component C3 reduces intimal hyperplasia in apolipoprotein E3-Leiden transgenic mice.  Circulation 114:2831-2838.

 

135.      Asokan, R., Hua, J., Young, K.A., Gould, H.J., Hannan, J.P., Kraus, D.M., Szakonyi, G.,

Grundy, G.J., Chen, X.S., Crow, M.K., and Holers, V.M.  2006.  Characterization of human complement receptor type 2 (CR2/CD21) as a receptor for interferon-alpha: a potential role in systemic lupus erythematosus.  J. Immunol. 177:383-394.

 

136.      Gilbert, H.E., Asokan, R., Holers, V.M., and Perkins, S.J.  2006.  The 15 SCR flexible extracellular domains of human complement receptor type 2 can mediate multiple ligand and antigen interactions.  J. Mol. Biol. 362:1132-1147.

 

137.      Szakonyi, G., Klein, M., Hannan, J.P., Young, K.A., Ma, R., Holers, V.M., and Chen, X.  2006.  Structure of the major envelope glycoprotein gp350 of Epstein-Barr virus. Nature Struc. and Molec. Biol. 13:996-1001.

 

138.      Bhatia, S.S., Majka, D.S., Kittelson, J.M., Parrish, L.A., Ferucci, E.D., Deane, K.D., Arend, W.P., Rewers, M., Holers, V.M., and Norris, J.M.  2006.  Rheumatoid factor seropositivity is inversely associated with oral contraceptive use in women without rheumatoid arthritis.  Ann. Rheum. Dis. 66:267-269.

 

139.      Girardi, G., Yarilin, D., Thurman, J.M., Holers, V.M., and Salmon, J.E.  2006.   Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction.  J. Exp. Med. 203:2165-2175.

 

140.      Thorgersen, E.B., Ghebremariam, Y.T., Thurman, J.M., Fung, M., Nielsen, E.W., Holers, V.M., Kotwal, G.J., and Mollnes, T.E.  2007.  Candidate inhibitors of porcine complement.  Mol. Immunol. 44:1827-1834.

 

141.      Young, K.A., Parrish, L., Zerbe, G. Rewers, M., Deane, K.D., Holers, V.M., and Norris, J.M.  2007.  Perinatal and early childhood risk factors associated with rheumatoid factor positivity in a healthy pediatric population.  Ann. Rheum. Dis. 66:179-183.

 

142.      Kulik, L, Marchbank, K.J., Lyubchenko, T., Kuhn, K.K., Liubchenko, G.A., Haluszczak, C., Gibson, M.G., Boackle, S.A., and Holers, V.M.  2007.  Intrinsic B cell hypo-responsiveness results from premature expression of human CR2/CD21 during B cell development.  Eur. J. Immunol. 37:623-633.

 

143.      Ho, J., Moir, S., Kulik, L., Malaspina, A., Donoghue, E.T., Miller, N.J., Chun, T.-W., Fauci, A.S., and Holers, V.M.  2007.  Essential role for CD21 in the establishment of an extracellular HIV reservoir in lymphoid tissues. J. Immunol. 178:6968-6974.

 

144.      Looney, R.J., Diamond, B., Holers, V.M., Levesque, M., Moreland, L. Nahm, M., and St. Clair, W. 2007. Guidelines for assessing immunocompetency in clinical trials for autoimmune diseases.  Clin. Immunol. 123:235-243.

 

145.      Mihai, S., Chiriac, M.T., Takahashi, K., Thurman, J.M., Holers, V.M., Zillikens, D., Botto, M., and Sitaru, C.  2007.  The alternative pathway of complement activation is critical for blister formation in experimental epidermolysis acquisita. J. Immunol. 178:6514-6521.

 

146.      Thurman, J.M., Lenderink, A.M., Royer, P.A., Coleman, K.E., Zhou, J., Lambris, J.D., Nemenoff, R.A., Quigg, R.J., and Holers, V.M.  2007.  C3a is required for the production of CXC chemokines by tubular epithelial cells after renal ischemia/reperfusion.  J. Immunol. 178:1819-1828.

 

147.      Lyubchenko, T., Dal Porto, J., Holers, V.M., and Cambier, J.C.  2007. C3d-linked antigens break B cell anergy. J. Immunol. 179:2695-2699.

 

148.      Banda, N.K., Takahashi, K. Wood, A.K., Holers, V.M., and Arend, W.P.  2007.  Pathogenic complement activation in collagen antibody-induced arthritis in mice requires amplification by the alternative pathway. J. Immunol. 179:4101-4109.

 

149.      Twohig, J., Kulik, L., Haluszczak, C., Reuter, J., Rossbach, A., Bull, M., Holers, V.M., and Marchbank, K.J.  2007.  Defective B cell ontogeny and immune response in human complement receptor 2 (CR2, CD21) transgenic mice is partially recovered in the absence of C3. Mol. Immunol. 44:3434-3444.

 

150.      Lenderink, A.M., Ljubanovic, D., Holers, V.M., and Thurman, J.M.  2007.  The alternative pathway of complement is activated in the glomeruli and tubulointerstitium of mice with adriamycin nephropathy. Am. J. Physiol. – Renal Physiol. 293: F555-564.

 

151.      Young, K.A., Chen, X.S., Holers, V.M., and Hannan, J.P.  2007.  Isolating the Epstein-Barr virus (EBV) gp350/220 binding site on complement receptor type 2 (CR2/CD21). J. Biol. Chem. 282:36614-36625.

 

152.      Song, H., Qiao, F., Atkinson, C., Holers, V.M., and Tomlinson, S.  2007.  A complement C3 inhibitor specifically targeted to sites of complement activation effectively ameliorates collagen-induced arthritis in DBA/1J mice.  J. Immunol. 179:7860-7867.

 

153.      Leinhase, I, Rozanski, M, Harhausen, D. Thurman, J.M, Schmidt, O.I., Hossini, A.M., Taha, M.E., Rittersch, D., Ward, P.A.,  Holers, V.M., and Stahel, P.F. 2007.  Inhibition of the alternative complement activation pathway in traumatic brain injury by a monoclonal anti-factor B antibody: a randomized placebo-controlled study in mice.  J. Neuroinflamm. 4:13.

 

154.      Majka, D.S., Deane, K.D., Parrish, L.A., Lazar, A.A., Baron, A.E., Walker, C.W., Rubertone, M.V., Gilliland, W.R., Norris, J.M., and Holers, V.M.  2008.  Duration of pre-clinical rheumatoid arthritis-related autoantibody positivity increases in subjects with older age at time of disease diagnosis. Ann. Rheum. Dis. 67:801-807. PMID17974596

 

155.      Hughes, L.B., Morrison, D., Kelly, J.M., Padilla, M., Vaughn, K., Westfall, A.O., Dwividi, H., Mikuls, T.R., Holers, V.M., Parrish, L., Alarcon, G.S., Conn, D.L., Jonas, B., Callahan, L.F., Smith, E.A., Gilkeson, G., Howard, G., Moreland, L.W., Patterson, N., Reich, D., and Bridges, Jr., S.L.  2008. The HLA-DRB1 shared epitope is associated with susceptibility to rheumatoid arthritis in African-Americans through European genetic admixture. Arth. Rheum. 58:349-358. PMID18240241

 

156.      Lynch, A.M., Murphy, J., Byers, T., Gibbs, R.S., Neville, M.C., Giclas, P.C., Salmon, J.E., and Holers, V.M.  2008.  Alternative complement pathway activation fragment Bb in early pregnancy as a predictor of preeclampsia.  Am. J. Obst. And Gyn.  198:385.e1-9. PMID: 18221926

 

157.      Clark, A., Weymann, A., Hartman, E., Turmelle, Y., Carroll, M., Thurman, J., Holers, V.M., Hourcade, D.E., and Rudnick, D.A. 2008. Evidence for nontraditional activation of complement factor 3 during liver regeneration. Mol. Immunol. 45:3125-3132. PMCID2600895

 

158.      Banda, N.K., Wood, A.K., Takahashi, K., Levitt, B., Rudd, P.M., Royle, L., Abrahams, J.L., Stahl, G.L., Holers, V.M., and Arend, W.P.  2008.  Initiation of the alternative pathway of complement by immune complexes is dependent on N-glycans in IgG antibodies. Arth. Rheum. 58:3081-3089. PMCID2574875

 

159.      Zaiss, A.K., Cotter, M.J., White, L.R., Clark, S.A., Wong, N.C.W., Holers, V.M., Bartlett, J.S., and Muruve, D.A.  2008.  Complement is an essential component of the immune response to adeno-associated virus vectors. J. Virology 82:2727-2740. PMCID2259003

 

160.      Mikuls, T.R., Hughes, L.B., Westfall, A.O., Holers, V.M., Parrish, L., van der Heijde, D., van Everdingen, M., Alarcon, G.S., Conn, D.L., Jonas, B., Callahan, L.F., Smith, E.A., Gilkeson, G., Howard, G., Moreland, L.W., and Bridges, L. 2008. Cigarette smoking, disease severity and autoantibody expression in African Americans with recent-onset rheumatoid arthritis. Ann. Rheum. Dis. 67:1529-1534. PMCID2731992

 

161.      Kuhn, K.A., Cozine, C.L., Tomooka, B., Robinson, W.H., and Holers, V.M.  2008. Complement receptor CR2/CR1 deficiency protects mice from collagen-induced arthritis and associates with reduced autoantibodies to type II collagen and citrullinated antigens. Mol. Immunol. 45:2802-2819. PMID18374982

 

162.      Huang, Y., Qiao, F., Atkinson, C., Holers, V.M., and Tomlinson, S. 2008. A novel targeted inhibitor of the alternative pathway of complement and its therapeutic application in ischemia/reperfusion injury. J. Immunol. 181:8068-8076. PMCID 2782395

 

163.      Li, K. Okemefuna, A.I., Gor, J., Hannan, J.P., Asokan, R. Holers, V.M., and Perkins, S.J.  2008.  Solution structure of the complex formed between human complement C3d and full-length complement receptor type 2.  J. Mol. Biol. 384:137-150. PMID18804116

 

164.      Young, K.A., Herbert, A.P., Barlow, P.N., Holers, V.M., and Hannan, J.P.  2008.  Molecular basis for the interaction between complement receptor 2 (CR2/CD21) and Epstein-Barr virus glycoprotein gp350.  J. Virol. 82:11217-11227. PMCID2573242

 

165.      Lynch, A.M., Gibbs, R.S., Murphy, J.R., Byers, T., Neville, M.C., Giclas, P.C., Salmon, J.E., Van Hecke, T.M. and Holers, V.M.  2008.  Complement activation fragment Bb in early pregnancy and spontaneous preterm birth.  Am. J. Obst. And Gyn.  199:327-328. PMCID2586079

 

166.      Kulik, L., Fleming, S.D., Moratz, C., Reuter, J.W., Novikov, A., Chen, K., Andrews, K.A., Markaryan, A., Quigg, R.J., Silverman, G.J.,Tsokos, G.C. and Holers, V.M.  2009. Pathogenic natural antibodies recognizing annexin IV are required to develop intestinal ischemia-reperfusion injury.  J. Immunol. 182:5363-5373. PMCID2820395

 

167.      Lyubchenko, T., Nielsen, J.P., Miller, S.M., Liubchenko, G.A., and Holers, V.M.  2009. Role of initial protein phosphorylation events and localized release-activated calcium influx in B cell antigen receptor signaling.  J. Leuk. Biol. 85:298-309. PMCID2631365

 

168.      Kovacs, J.M., Hannan, J.P., Eisenmesser, E.Z., and Holers, V.M.  2009.  Mapping of the C3d ligand binding site on complement receptor 2 (CR2/CD21) using nuclear magnetic resonance and chemical shift analysis.  J. Biol. Chem. 284:9513-9520. PMCID 2666603

 

169.      Mikuls, T.R., Payne, J.B., Reinhardt, R.A, Thiele, G.M., Maziarz, E., Cannella, A.C., Holers, V.M., Kuhn, K.A., and O’Dell, J.R.  2009.  Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis.  Int. Immunopharm. 9:38-42. PMCID2748386

 

170.      Twohig, J.P., Pappworth, I.Y., Kulik, L., Bull, M., Holers, V.M., Wang, E.C.Y., and Marchbank, K.J.  2009.  Defective B cell ontogeny and immune response in mice prematurely expressing human complement receptor 2 (CR2, CD21) is similar to that seen in aging wild type mice. Mol. Immunol. 46:2002-2013. PMCID 2706330

 

171.      Feser, M., Derber, L.A., Deane, K.D., Lezotte, D.C., Weisman, M.H., Buckner, J.H., Mikuls, T., O’Dell, J.R., Gregersen, P.K., Holers, V.M., and Norris, J.M. 2009.  Plasma 25,OH vitamin D levels are not associated with rheumatoid arthritis-related autoantibodies in individuals at elevated risk for rheumatoid arthritis.  J. Rheum. 36:943-946. PMCID745328

 

172.      Pappworth, I.Y., Kulik, L., Haluszczab, C., Reuter, J.W., Holers, V.M., and Marchbank, K.J. 2009.  Increased B cell delection and significantly reducted autoantibody titre due to premature expression of human complement receptor type 2 (CR2, CD21).  Mol. Immunol.  46:1042-1049. PMCID2657831

 

173.      Xu, X., Hsu, H.-C., Chen, J., Grizzle, W.E., Chatham, W.W., Stockard, C.R., Wu, Q., Yang, P.A.,  Holers, V.M., and Mountz, J.D.  2009.  Increased expression of activation-induced cytidine deaminase is associated with anti-CCP and rheumatoid factor in rheumatoid arthritis.  Scand. J. Immunol. 70:309-316. PMID19703021

 

174.      Ricklin, D., Tzekou, A., Garcia, B.L., Hammel, M., McWhorter, W.J., Sfyroera, G., Wu, Y.Q., Holers, V.M., Herbert, A.P., Barlow, P.M., Geisbrecht, B.V. and Lambris, J.D. 2009.  A molecular insight into complement evasion by the staphylococcal complement inhibitor protein family.  J. Immunol. 183: 2565-2574. PMID19625656

 

175.      Kolfenbach, J.R., Deane, K.D., Derber, L.A., O”Donnell, C., Weisman, M.H., Buckner, J.H., Gersuk, V.H., Wei, S., Mikuls, T.R., O’Dell, J., Gregersen, P.K., Keating, R.M., Norris, J.M., and Holers, V.M.   2009.  A prospective approach to investigating the natural history of pre-clinical rheumatoid arthritis (RA) using first-degree relatives of probands with RA. Arth. Care Res. 61: 1735-1742. PMCID2795101

 

176.      Deane, K.D., Striebich, C., Goldstein, B.L., Derber, L.A., Parish, M.C., Feser, M.L., Hamburger, E.M., Brake, S., Belz, C., Goddard, J., Norris, J.M., Karlson, E.W., and Holers, V.M.  2009.  Identification of undiagnosed inflammatory arthritis in a community health fair screen.  Arth. Care Res. 61: 1642-1649. PMCID19950306

 

177.      Banda, N.K., Levitt, B., Wood, A.K., Takahashi, K., Stahl, G.L., Holers, V.M., and Arend, W.P.  2009.  Complement activation pathways in murine immune complex arthritis and in C3a and C5a generation in vitro. Clin. Exp. Immunol. 159: 100-108. PMCID2802700

 

178.      Thurman, J.M., Renner, B., Kunchithapautham, K., Ferreira, V.P., Pangburn, M.K., Ablonczy, Z., Tomlinson, S., Holers, V.M., and Rohrer, B.  2009.  Oxidative stress renders retinal pigment epithelial cells susceptible to complement-mediated injury.  J. Biol. Chem. 284:16939-16947. PMCID2719331

 

179.      Gizinski, A.M., Mascolo, M., Kervitsky, D., Meehan, R., Brown, K., Holers, V.M., and Deane, K.D.  2009.  Rheumatoid arthritis-specific autoantibodies in interstitial lung disease in the absence of articular symptoms.  Clin. Rheum. 28:611-613. PMID19252818

 

180.      Banda, N.K., Levitt, B., Glogowska, M.J., Thurman, J.M., Takahashi, K., Stahl, G.L., Tomlinson, S., Arend, W.P., and Holers, V.M.  2009.  Targeted inhibition of the complement alternative pathway with complement receptor 2 and factor H attenuates collagen antibody-induced arthritis in mice.  J. Immunol. 183:5928-5937. PMCID2828354

 

181.     Thurman, J.M., Marians, R., Emlen, W., Wood, S., Smith, C., Akana, Hl, Holers, V.M., Lesser, M., Kline, M., Hoffman, C., Christen, E., and Trachtman, H.  2009.  Alternative pathway of complement in children with diarrhea-associated hemolytic uremic syndrome.  Clin. J. Am. Soc. Nephrol. 4:1920-1924. PMCID2798880

 

182.      Serkova, N., Renner, B., Larsen, B., Stoldt, C., Hasebroock, K., Bradshaw, E.L., Holers, V.M., and Thurman, J.M. 2010.  Targeted iron oxide nanoparticles for molecular MR Imaging of renal inflammation in mice.  Radiology 255:309-310. PMCID 2858816

 

183.      Lynch, A.M, Murphy, J.R., Gibbs, R.S., Levine, R.J., Giclas, P.C., Salmon, J.E., and Holers, V.M.  2010.  Interrelationship and contribution of complement activation fragments and angiogenesis-related factors in early pregnancy to the development of preeclampsia.  Brit. J. Obstet. Gynecol. 117(4):456-62.  PMID20074261

 

184.      Briggs, F.B.S., Ramsay, P.P., Madden, E., Norris, J.M.,  Holers, V.M., Mikuls, T.R., Sokka, T., Seldin, M.F., Gregersen, P.K., Criswell, L.A., and Barcellos, L.F.  2010.  Supervised machine learning and logistic regression identifies novel epistatic risk factors with PTPN22 for rheumatoid arthritis.  Genes Immun. 11:199-208. PMID20090771

 

185.      Ercan, A., Cui, J., Chatterton, D.E.W., Deane, K.D., Hazen, M.M., Brintnell, W., O’Donnell, C., Derber, L., Weinblatt, M.E., Shadick, N.A., Bell, D.A, Cairns, E., Solomon, D.H., Holers, V.M., Rudd, P.M., and Lee, D.M.  2010.  IgG galactosylation aberrancy precedes disease onset, correlates with disease activity and is prevalent in autoantibodies in rheumatoid arthritis. Arth. Rheum. 2010 Apr 29. (Epub ahead of print) PMID20506563

 

186.      Gregersen, P.K., Amos, C.I., Lee, A.T., Lu, E., Remmers,E.F., Korman, B.D., Kastner, D.L., Seldin, M.F., Criswell, L.A., Plenge, R.M., Holers, V.M., Mikuls, T., Sokka, T., Bridges, S.L., Begovich, A., and Siminovitch, K.  2009.  REL, encoding a member of the NF-kappaB family of transcription factors, is a newly defined risk locus for rheumatoid arthritis.  Nature Genetics 41:820-823. PMCID2705058

 

187.      Briggs, F.B.S., Ramsay, P.P., Madden, E., Norris, J.M., Holers, V.M., Mikuls, T.R., Sokka, T., Seldin, M.F., Gregersen, P.K., Criswell, L.A., and Barcellos, L.F.   2010. Supervised machine learning and logistic regression identifies novel epistatic risk factors with PTPN22 for rheumatoid arthritis. Genes Immun Jan 21 (Epub ahead of print) PMID 20090771

 

188.      Kolfenbach, J.R., Deane, K.D., Derber, L.A., O’Donnell, C.I., Rosen, A., Darrah, E., Norris, J.M., and Holers, V.M.  2010 Autoimmunity to peptidyl arginine deiminase type 4 precedes clinical onset of rheumatoid arthritis. Arth. Rheum. May 23 (Epub ahead of print) PMID: 20496417

 

189.      Thurman, J.M., Renner, B., Kunchitthapauthan, K., Holers, V.M., and Rohrer, B. 2010. Aseptic injury to epithelial cells alters cell surface complement regulation in a tissue specific fashion. Adv. Exp. Med. Biol. 664:151-8. PMID20238013

 

190.      Quan, T.E., Roman, R.M., Rudenga, B.J., Holers, V.M., and Craft, J. 2010. Epstein-barr virus promotes interferon-alpha production by plasmacytoid dendritic cells. Arth. Rheum. 2010 Feb 22. (Epub ahead of print) PMID20178121

 

191.      Deane, K.D., O'Donnell, C.I., Hueber, W., Majka, D.S., Lazar, A.A., Derber, L.A., Gilliland, W.R., Edison, J.D., Norris, J.M., Robinson, W.H., and Holers, V.M.  2010. The number of elevated cytokines/chemokines in pre-clinical seropositive rheumatoid arthritis predicts time to diagnosis in an age-dependent manner. Arth. Rheum. (in press).

 

192.      Kovacs, J.M., Hannan, J.P., Eisssenmesser, E.Z., and Holers, V.M.  2010. Biophysical investigations of complement receptor 2 (CD21. CR2) ligand interactions reveal amino acid contacts unique to each receptor-ligand pair. J. Biol. Chem. (in press).

 

193.      Renner, B., Amura, C.R., Ljubanovic, D., Glogowska, M.J., Takahashi, K., Stahl, G.L., Carroll, M.C., Holers, V.M., and Thurman, J.M.  2009.  B cell subsets contribute to both renal injury and renal protection after ischemia/reperfusion.  (submitted).

 

194.      Banda, N.K., Takahashi, M., Levitt, B., Glogowska, M., Nicholas, J., Takahashi, K., Stahl, G.L., Fujita, T., Arend, W.P., and Holers, V.M.  2010. Essential role of complement MASP-1/3 in the murine collagen antibody-induced arthritis model of inflammatory arthritis. (submitted).

 

195.      Cozine, C.L., BenBarak, M., Robinson, W.H., and Holers, V.M.  2010. Anti-GITR treatment in collagen-induced arthritis results in enhanced epitope spreading to citrullinated antigens. (submitted).

 

196.      Majka, D.S., Deane, K.D., Parrish, L.A., Karlson, E.W., Ferucii, E.D., Rewers, M., Weisman, M.H., Buckner, J.H., Norris, J.M., and Holers, V.M.  2010.  Rheumatoid factor is associated with rheumatoid arthritis symptoms and mild synovitis in a cohort at risk for rheumatoid arthritis. (submitted).

 

197.      Tan, W., Wu, H., Zhao, J., Derber, L.A., Lee, D.M., Shadick, N.A., Conn, D.L, Smith, E.A., Gersub, V., Nepom, G.T., Moreland, L.W., Furst, D.E., Thompson, S.D., Jonas, B.L., Holers, V.M., Glass, D.N., Chen, P.P., Bridges, S.L, Weinblat, M.E., Paulus, H.E., and Tsao, B..P.  2010.  A functional RANKL polymorphism associated with younger age at onset of rheumatoid arthritis. (submitted).

 

198.      Willis, V.C., Gizinski, A.M., Banda, N.K., Knuckley, B., Cordova, K., Luo, Y., Causey, C.P., Levitt,B., Glogowska, M., BenBarak, M., Chandra, P., Kulik, L., Robinson, W.H., Arend, W.P., Thompson, P.R., and Holers, V.M.  2010. Cl-amidine, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis. (submitted).

 

199.      Renner, B., Ferreira, V.P., Cortes, C., Goldberg, R., Ljubanovic, D., Pangburn, M.K., Pickering, M.C., Tomlinson, S., Holers, V.M., and Thurman, J.M.  2010.  Factor H controls complement activation in the renal tubulointerstitium after ischemic injury.  (submitted).

 

200.      Lazar, A.A., Holers, V.M., Deane, K.D., Norris, J.M., and Zerbe, G.O.  2010.  Extending a Scheffe explicit solution approach to random coefficient models with censored data. (submitted).

 

 

BOOK CHAPTERS AND REVIEWS:

 

1.         Holers, V. M., Cole, J. L., Lublin, D. M., Seya, T., and Atkinson, J. P.  1985.  Human C3b- and C4b-regulatory proteins: A new multi-gene family.  Immunol. Today  6:188-192.

 

2.         Dykman, T. R., Holers, V. M., and Atkinson, J. P.  1985.  Function and structure of the C3b/C4b complement receptor, CR1 in Microbiology Loretta Leive (ed).  ASM Publ. p.19-22.

 

3.         Atkinson, J. P., Kaine, J. L., Holers, V. M., and Chan, A. C.  1986.  Complement and the Rheumatic Diseases in An Introduction to the Complement System (Ed. Ross, G.D.) Academic Press.  New York.  p.197-211.

 

4.         Holers, V. M.  1988.  Complement receptors in The Year in Immunology (Ed. Crusse, J.M., and Lewis, R.E.) S. Karger, Basel.  p.231-240.

 

5.         Hourcade, D., Holers, V. M., and Atkinson, J. P.  1989.  The regulators of complement activation (RCA) gene cluster in Adv. in Immunol. F.J. Dixon (ed)  45:381-416.

 

6.         Holers, V. M., and Brown, E. J.  1992.  Integrins in inflammation and the immune response in Scope Immunology Monograph. B. Schwartz, (ed)  p.98-110.

 

7.         Krych, M., Atkinson, J. P., and Holers, V. M.  1992.  Complement receptors in Curr. Opin. Immunol., Current Biology Ltd, London  4:8-13. 

 

8.         Holers, V. M., Kinoshita, T., and Molina, H.  1992.  Evolution of mouse and human complement C3 binding proteins: divergence of form but conservation of function.  Immunol. Today  13:231-236. 

 

9.         Moulds, J., Krych, M., Holers, V. M., Liszewski, K., and Atkinson, J.P.  1992.  Genetics of the complement system and rheumatic diseases in Rheumatic Disease Clinics of North America.  B. Dudlick, (ed)  18:893-914. 

 

10.       Holers, V. M.  1995.  Complement in Principles and Practices of Clinical Immunology. Rich, R. (ed),  Mosby, St. Louis, MO.  p.363-391.

 

11.       Holers, V. M.  1997.  Complement Receptors in Manual of Clinical Laboratory     Immunology.  (Ed. Rose, N. R., de Macario, E. C., Folds, J. D., Lane, H. C., and      Nakamura, R. M.),  ASM Press.  p.192-202.

 

12.       Holers, V. M.  1997.  Complement Deficiencies and SLE in Rheumatology, Second Edition.  (Ed. Klippel, J. H. and Dieppe, P. A.), Mosby-Wolfe, London, UK. p.8.6-8.8.

 

13.       Holers, V. M.  1997.  The Complement System in Rheumatology, Second Edition.  (Ed.             Klippel, J. H. and Dieppe, P. A.), Mosby-Wolfe, London, UK. p.4.1-4.8.

 

14.         Smyth, C.J., and Holers, V. M. 1998 (editors) Gout, Hyperuricemia and Other Crystal-Associated Arthropathies. Marcel Dekker, New York, NY.

 

15.         Holers, V. M.  1998.  Complement Receptor Type 2 (CR2/CD21) as a Central Link between Innate and Acquired Immunity. In  Clinical Immunology Newsletter 18: 7-10.

 

16.         Guthridge, J. G., and Holers, V. M. 1999. Complement Receptor Type 2 in The Complement Factsbook (Ed. Morley, B. and Walport, M. L.), Academic Press, London, UK.

 

17.         Holers, V. M.  1999.  Complement in Principles of Molecular Rheumatology (Ed. Tsokos, G.), Humana Press, Totowa, NJ. p.145-160.

 

18.         Holers, V.M.  1999.  Complement deficiency states, disease susceptibility and infection risk in Systemic Lupus Erythematosus.  Arth. Rheum.  42:2023-2025.

 

19.         Lambris, J. D., and Holers, V.M.  2000 (editors) Therapeutic Interventions in the Complement System. Humana Press, Inc., Totowa, NJ.

 

20.         Holers, V.M. 2000.  Complement as a regulatory and effector pathway in Therapeutic Interventions in the Complement System (Ed. Lambris, J. D., and Holers, V.M.).  Humana Press, Inc., Totowa, NJ. p.1-32.

 

21.         Holers, V. M.  2000.  Phenotypes of complement knockouts.  Immunopharmacology.  49:125-131.

 

22.         Holers, V. M.,  2001.  Complement in Clinical Immunology  (Ed. R. Rich), Mosby, Philadelphia, PA.  p.21.1-21.18.

 

23.         Holers, V. M.,  2001.  Complement deficiencies in Clinical Immunology  (Ed. R. Rich), Mosby, Philadelphia, PA.  p.36.1-36.10.

 

24.         Nichols, T., Karp, D. R., Holers, V. M.,  2001.  Gamma-glutamyl transpeptidase (CD224).  Prot. Rev. Web 3:7-11.

 

25.         Holers, V. M.,  2002.  Immunogenetics of rheumatic diseases in Rheumatology Secrets (Ed. S. West), Hanley and Belfus, Inc., Philadelphia, PA. p.28-38.

 

26.         Holers, V. M.,  2002.  Tolerance and autoimmunity in Rheumatology Secrets (Ed. S. West), Hanley and Belfus, Inc., Philadelphia, PA. p.38-44.

 

27.         Karp, D. R., and Holers, V. M.,  2003.  Complement in health and disease in Cecil Textbook of Medicine (Ed. L. Goldman and D. Ausiello), W. B. Saunders, Inc., Orlando, FL. p. 233-240.

 

28.         Hannan, J., Young, K., Szakonyi, G., Overduin, M. J., Perkins, S. J., and Holers, V. M.  2002.  Structure-function of complement receptor (CR) 2 and CR2-C3d complexes.  Biochem. Soc. Trans.  30:983-989.

 

29.         Perkins, S. J., Gilbert, H. E., Aslam, M., Hannan, J., Holers, V. M., and Goodship, T. H. J. 2002.  Solution structures of complement components by X-ray and neutron scattering and analytical ultracentrifugation.  Biochem. Soc. Trans.  30:996-1006.

 

30.         Boackle, S. A., and Holers, V. M.,  2002.  Role of complement in the development of autoimmunity in Current Directions in Autoimmunity (Ed., D. Nemazee and A. N. Theofilopoulos), Karger, Basel, Switzerland.  p. 154-168.

 

31.         Salmon, J. E., Girardi, G., and Holers, V. M.,  2002.  Complement activation as a mediator of antiphospholipid antibody-induced pregnancy loss and thrombosis.  Ann. Rheum. Dis. 61 (supplement II): II46-II50.

 

32.         Holers, V. M.,  2003.  Complement receptors in Biological Therapy in Rheumatology (Ed. J. S. Smolen and P. E. Lipsky), Martin Dunitz, Inc., London, UK. p.167-180.

 

33.         Holers, V. M.,  2003. Short Analytic Review: The complement system as a therapeutic target in autoimmunity.  Clin. Imm. 107:140-151.

 

34.         Majka, D. S., and Holers, V. M.  2003.  Can we accurately predict the development of rheumatoid arthritis in the preclinical phase? Arth. Rheum. 48:2701-2705.

 

35.         Boackle, S. A., and Holers, V. M.,  2004.  Complement receptor 2 and autoimmunity in Current Directions in Autoimmunity (Ed., G. Tsokos), Karger, Basel, Switzerland.  p. 33-48.

 

36.         Holers, V.M., and Thurman, J.S.  2004.  The alternative pathway of complement in disease: opportunities for therapeutic targeting.  Molec. Immunol. 41:147-152.

 

37.         Hannan, J. P., Szakonyi, G., Asokan, R., Chen, X., and Holers, V. M.  2004.  Complement receptor CR2/CD21 and CR2-C3d complexes in Structural Biology of the Complement System (Ed. J. D. Lambris), Marcell Dekker, Inc., New York, NY. p. 143-160.

 

38.         Holers, V.M. 2004. Anti-C1q autoantibodies amplify pathogenic complement activation in systemic lupus erythematosus. J. Clin. Invest. 114:616-619.

 

39.         Carroll, M.C., and Holers, V. M.,  2005.  Innate Autoimmunity in Advances in Immunology  86:137-157.

 

40.         Holers, V. M.  2005. Complement receptors and the shaping of the natural antibody repertoire.  Springer Semin. Immunopath.  26:405-423.

 

41.         Thurman, J.M., and Holers, V. M.  2006.  The central role of the alternative complement pathway in human disease.  J. Immunol. 176:1305-1310.

 

42.         Thurman, J.M., and Holers, V. M.  2006.  Complement deficient mice as model systems for kidney diseases in Complement and Kidney Disease (Ed., P. Zipfel), Birkhauer-Verlag, Basel, Switzerland.  p. 49-63.

 

43.         Holers, V. M.  2006.  Viewpoint: Are anti-cyclic citrullinated peptide antibodies pathogenic in rheumatoid arthritis?  Nature Clin. Prac. Rheum.  2:400-401.

 

44.         Majka, D.S., and Holers, V. M.  2006.  Cigarette smoking and the risk of systemic lupus erythematosus and rheumatoid arthritis.  Ann. Rheum. Dis. 65L561-563.

 

45.         Karp, D. R., and Holers, V. M.,  2007.  Complement in health and disease in Cecil Textbook of Medicine (Ed. L. Goldman and D. Ausiello), W. B. Saunders, Inc., Orlando, FL. p. 47:282-288.

 

46.         Holers, V.M., and Kulik, L.  2007.  Complement receptor 2, natural antibodies and innate immunity: inter-relationships in B cell selection and activation.  Mol. Immunol. 44:64-72.

 

47.         Holers, V. M.  2007.  Antibodies to Citrullinated Proteins: Pathogenic and Diagnostic Significance.  Curr. Rheum. Reports.  9:396-400.

 

48.         Holers, V. M.  2008.  Tolerance and autoimmunity in Rheumatology Secrets (Ed. S. West), Hanley and Belfus, Inc., Philadelphia, PA.

 

49.         Holers, V.M.  2008. Systemic lupus erythematosus: the complement system. in Rheumatology 4th Edition (Ed, M.C. Hochberg, A.J. Silman, J.S. Smolen, M.H. Weisman and M.E. Weinblatt), Mosby, Inc. St. Louis, MO.  p. 1243-1252.

 

50.         Holers, V.M., and Salmon, J.E.  2008.  Complement and pregnancy loss in Contemporary Targeted Therapies in Rheumatology (Ed, J.S. Smolen and P.E. Lipsky), Informa Healthcare, Abington, UK. 

 

51.         Holers, V. M.  2008. The spectrum of complement alternative pathway mediated diseases. Immunol. Rev. 223:300-316. PMID18613844

 

52.         Holers, V. M.  2009. Complement in Rheumatoid Arthritis. in Rheumatoid Arthritis (Ed, M.C. Hochberg, A.J. Silman, J.S. Smolen, M.H. Weisman and M.E. Weinblatt), Mosby, Inc. St. Louis, MO.

 

53.         Karp, D. R., and Holers, V. M.,  2009.  Complement in health and disease in Cecil Textbook of Medicine, W. B. Saunders, Inc., Orlando, FL. (in press).

 

54.         Deane, K.D., Norris, J.M., and Holers, V.M. 2010.  Pre-clinical rheumatoid arthritis:  identification, evaluation and future directions for investigation. Rheum. Dis. Clin. NA 13:236-241. PMCID 2879710

 

55.         Holers, V.M.  2010. Systemic lupus erythematosus: the complement system. in Rheumatology 5th Edition (Ed, M.C. Hochberg, A.J. Silman, J.S. Smolen, M.H. Weisman and M.E. Weinblatt), Mosby, Inc. St. Louis, MO.  (in press).

 

56.         Holers, V.M., Thompson, P.R., and Deane, K.D.  2010.  The central role of citrullination in rheumatoid arthritis. (submitted).

 

Rohrer, B., Long, Q., Coughlin, B., Renner, B., Huang, Y., Kunchithapautham, K., Ferreira, V., Pangburn, M., Gilkeson, G., Thurman, J., Tomlinson, S., and Holers, V.M. 2010.  A targeted inhibitor of the complement alternative pathway in models of age-related macular degeneration. in Inflammation and retinal disease: complement biology and pathology. Adv. Exp. Med. Biol. (in press).