Characterization of the renal CD4+ T-cell response in experimental autoimmune glomerulonephritis

Kidney International

Volumn 82, Issue 1, 2012, Pages 60-71

  Hopfer, Helmut ^a,b   Holzer, Julia ^b   Hünemörder, Stefanie ^b   Paust, Hans Joachim ^b   Sachs, Marlies ^b   Meyer Schwesinger, Catherine ^b   Turner, Jan Eric ^b   Panzer, Ulf ^b   Mittrücker, Hans Willi ^b  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

anti GBM disease; Goodpasture's syndrome; immunology and pathology; lymphocytes; renal injury

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G;

ALLERGIC GLOMERULONEPHRITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; BIOACCUMULATION; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE COURSE; DISEASE SEVERITY; EFFECTOR CELL; GLOMERULUS BASEMENT MEMBRANE; IMMUNOGLOBULIN DEPOSITION; IMMUNOPATHOGENESIS; KIDNEY DYSFUNCTION; KIDNEY INTERSTITIUM; KIDNEY TUBULE DAMAGE; LEUKOCYTE MIGRATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEINURIA; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL;

EID: 84862499991     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.73     Document Type: Article

References (59)

1. Hudson BG, Tryggvason K, Sundaramoorthy M et al. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med 2003; 348: 2543-2556. (Pubitemid 36706542)
2. Pusey CD. Anti-glomerular basement membrane disease. Kidney Int 2003; 64: 1535-1550. (Pubitemid 37153829)
3. Ooi JD, Holdsworth SR, Kitching AR. Advances in the pathogenesis of Goodpasture's disease: From epitopes to autoantibodies to effector T cells. J Autoimmun 2008; 31: 295-300.
4. Peto P, Salama AD. Update on antiglomerular basement membrane disease. Curr Opin Rheumatol 2011; 23: 32-37.
5. Lerner RA, Glassock RJ, Dixon FJ. The role of anti-glomerular basement membrane antibody in the pathogenesis of human glomerulonephritis. J Exp Med 1967; 126: 989-1004.
6. Pedchenko V, Bondar O, Fogo AB et al. Molecular architecture of the Goodpasture autoantigen in anti-GBM nephritis. N Engl J Med 2010; 363: 343-354.
7. Borza DB, Bondar O, Colon S et al. Goodpasture autoantibodies unmask cryptic epitopes by selectively dissociating autoantigen complexes lacking structural reinforcement: novel mechanisms for immune privilege and autoimmune pathogenesis. J Biol Chem 2005; 280: 27147-27154. (Pubitemid 41040753)
8. Vanacore RM, Ham AJ, Cartailler JP et al. A role for collagen IV cross-links in conferring immune privilege to the Goodpasture autoantigen: structural basis for the crypticity of B cell epitopes. J Biol Chem 2008; 283: 22737-22748.
9. Luo W, Wang XP, Kashtan CE et al. Alport alloantibodies but not Goodpasture autoantibodies induce murine glomerulonephritis: protection by quinary crosslinks locking cryptic alpha3(IV) collagen autoepitopes in vivo. J. Immunol 2010; 185: 3520-3528.
10. Bolton WK, Tucker FL, Sturgill BC. New avian model of experimental glomerulonephritis consistent with mediation by cellular immunity. Nonhumorally mediated glomerulonephritis in chickens. J Clin Invest 1984; 73: 1263-1276. (Pubitemid 14139520)
11. Reynolds J, Tam FW, Chandraker A et al. CD28-B7 blockade prevents the development of experimental autoimmune glomerulonephritis. J Clin Invest 2000; 105: 643-651. (Pubitemid 30146511)
12. Wu J, Hicks J, Borillo J et al. CD4+ T cells specific to a glomerular basement membrane antigen mediate glomerulonephritis. J Clin Invest 2002; 109: 517-524. (Pubitemid 34171783)
13. Cairns LS, Phelps RG, Bowie L et al. The fine specificity and cytokine profile of T-helper cells responsive to the alpha3 chain of type IV collagen in Goodpasture's disease. J Am Soc Nephrol 2003; 14: 2801-2812. (Pubitemid 37305643)
14. Zou J, Henderson L, Thomas V et al. Presentation of the Goodpasture autoantigen requires proteolytic unlocking steps that destroy prominent T cell epitopes. J Am Soc Nephrol 2007; 18: 771-779. (Pubitemid 46434494)
15. Steblay RW. Glomerulonephritis induced in sheep by injections of heterologous glomerular basement membrane and Freund's complete adjuvant. J Exp Med 1962; 116: 253-272.
16. Nishikawa K, Guo YJ, Miyasaka M et al. Antibodies to intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 prevent crescent formation in rat autoimmune glomerulonephritis. J Exp Med 1993; 177: 667-677. (Pubitemid 23104278)
17. Kalluri R, Danoff TM, Okada H et al. Susceptibility to anti-glomerular basement membrane disease and Goodpasture syndrome is linked to MHC class II genes and the emergence of T cell-mediated immunity in mice. J Clin Invest 1997; 100: 2263-2275. (Pubitemid 27500149)
18. Nakamura A, Yuasa T, Ujike A et al. Fcgamma receptor IIB-deficient mice develop Goodpasture's syndrome upon immunization with type IV collagen: a novel murine model for autoimmune glomerular basement membrane disease. J Exp Med 2000; 191: 899-906.
19. Kohda T, Okada S, Hayashi A et al. High nephritogenicity of monoclonal antibodies belonging to IgG2a and IgG2b subclasses in rat anti-GBM nephritis. Kidney Int 2004; 66: 177-186. (Pubitemid 38870093)
20. Dean EG, Wilson GR, Li M et al. Experimental autoimmune Goodpasture's disease: a pathogenetic role for both effector cells and antibody in injury. Kidney Int 2005; 67: 566-575. (Pubitemid 40139848)
21. Reynolds J, Prodromidi EI, Juggapah JK et al. Nasal administration of recombinant rat alpha3(IV)NC1 prevents the development of experimental autoimmune glomerulonephritis in the WKY rat. J Am Soc Nephrol 2005; 16: 1350-1359. (Pubitemid 41716519)
22. Robertson J, Wu J, Arends J et al. Activation of glomerular basement membrane-specific B cells in the renal draining lymph node after T cell-mediated glomerular injury. J Am Soc Nephrol 2005; 16: 3256-3263. (Pubitemid 46179331)
23. Arends J, Wu J, Borillo J et al. T cell epitope mimicry in antiglomerular basement membrane disease. J Immunol 2006; 176: 1252-1258. (Pubitemid 43099730)
24. Chen L, Hellmark T, Pedchenko V et al. A nephritogenic peptide induces intermolecular epitope spreading on collagen IV in experimental autoimmune glomerulonephritis. J Am Soc Nephrol 2006; 17: 3076-3081. (Pubitemid 44707768)
25. Hopfer H, Maron R, Butzmann U et al. The importance of cell-mediated immunity in the course and severity of autoimmune anti-glomerular basement membrane disease in mice. FASEB J 2003; 17: 860-868. (Pubitemid 36538661)
26. Striker G, Striker LJ, D'Agati VD. Goodpasture syndrome. The Renal Biopsy 1997; 8: 143-146.
27. Van Damme BJ, Fleuren GJ, Bakker WW et al. Experimental glomerulonephritis in the rat induced by antibodies directed against tubular antigens. V. Fixed glomerular antigens in the pathogenesis of heterologous immune complex glomerulonephritis. Lab Invest 1978; 38: 502-510. (Pubitemid 8338244)
28. Couser WG, Steinmuller DR, Stilmant MM et al. Experimental glomerulonephritis in the isolated perfused rat kidney. J Clin Invest 1978; 62: 1275-1287. (Pubitemid 9075757)
29. Kerjaschki D, Farquhar MG. Immunocytochemical localization of the Heymann nephritis antigen (GP330) in glomerular epithelial cells of normal Lewis rats. J Exp Med 1983; 157: 667-686. (Pubitemid 13145068)
30. Bolton WK, Chen L, Hellmark T et al. Epitope spreading and autoimmune glomerulonephritis in rats induced by a T cell epitope of Goodpasture's antigen. J Am Soc Nephrol 2005; 16: 2657-2666.
31. Walters G, Habib AM, Reynolds J et al. Glomerular T cells are of restricted clonality and express multiple CDR3 motifs across different Vbeta T-cell receptor families in experimental autoimmune glomerulonephritis. Nephron Exp Nephrol 2004; 98: e71-e81.
32. D'Agati VD, Jenette JC, Silva FG. Antiglomerular basement membrane glomerulonephritis and Goodpasture's syndrome. In: Non-neoplastic kidney disease. Fascicle 4. Atlas of nontumor pathology ARP Press: Silver Spring, Maryland, 2005, pp 361-383.
33. Teague CA, Doak PB, Simpson IJ et al. Goodpasture's syndrome: an analysis of 29 cases. Kidney Int 1978; 13: 492-504. (Pubitemid 8373075)
34. Nolasco FE, Cameron JS, Hartley B et al. Intraglomerular T cells and monocytes in nephritis: study with monoclonal antibodies. Kidney Int 1987; 31: 1160-1166. (Pubitemid 17069100)
35. Bolton WK, Innes Jr DJ, Sturgill BC et al. T-cells and macrophages in rapidly progressive glomerulonephritis: clinicopathologic correlations. Kidney Int 1987; 32: 869-876. (Pubitemid 18015518)
36. Segerer S, Schlöndorff D. Role of chemokines for the localization of leukocyte subsets in the kidney. Semin Nephrol 2007; 27: 260-274. (Pubitemid 46802915)
37. Kitching AR, Turner AL, Semple T et al. Experimental autoimmune anti-glomerular basement membrane glomerulonephritis: a protective role for IFN-gamma. J Am Soc Nephrol 2004; 15: 1764-1774. (Pubitemid 38822055)
38. Ooi JD, Phoon RKS, Holdsworth SR et al. IL-23, not IL-12, directs autoimmunity to the Goodpasture antigen. J Am Soc Nephrol 2009; 20: 980-989.
39. Paust H-J, Turner J-E, Steinmetz OM et al. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009; 20: 969-979.
40. Panzer U, Steinmetz OM, Paust H-J et al. Chemokine receptor CXCR3 mediates T cell recruitment and tissue injury in nephrotoxic nephritis in mice. J Am Soc Nephrol 2007; 18: 2071-2084. (Pubitemid 47041073)
41. Odobasic D, Gan PY, Summers SA et al. Interleukin-17A promotes early but attenuates established disease in crescentic glomerulonephritis in mice. Am J Pathol 2011; 179: 1188-1198.
42. Summers SA, Steinmetz OM, Li M et al. Th1 and Th17 cells induce proliferative glomerulonephritis. J Am Soc Nephrol 2009; 20: 2518-2524.
43. Turner J-E, Paust H-J, Steinmetz OM et al. The Th17 immune response in renal inflammation. Kidney Int 2010; 77: 1070-1075.
44. Kitching AR, Holdsworth SR. The emergence of TH17 cells as effectors of renal injury. J Am Soc Nephrol 2011; 22: 235-238.
45. Schroder K, Hertzog PJ, Ravasi T et al. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75: 163-189. (Pubitemid 38174573)
46. Korn T, Bettelli E, Oukka M et al. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
47. O'Quinn DB, Palmer MT, Lee YK et al. Emergence of the Th17 pathway and its role in host defense. Adv Immunol 2008; 99: 15-63.
48. Tipping PG, Holdsworth SR. T cells in crescentic glomerulonephritis. J Am Soc Nephrol 2006; 17: 1253-1263. (Pubitemid 43673405)
49. Darabi K, Karulin AY, Boehm BO et al. The third signal in T cell-mediated autoimmune disease? J Immunol 2004; 173: 92-99. (Pubitemid 38797330)
50. Korn T, Reddy J, Gao W et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat Med 2007; 13: 423-431. (Pubitemid 46559831)
51. Latham KA, Whittington KB, Zhou R et al. Ex vivo characterization of the autoimmune T cell response in the HLA-DR1 mouse model of collagen-induced arthritis reveals long-term activation of type II collagen-specific cells and their presence in arthritic joints. J Immunol 2005; 174: 3978-3985. (Pubitemid 40395972)
52. Díaz Gallo C, Jevnikar AM, Brennan DC et al. Autoreactive kidney-infiltrating T-cell clones in murine lupus nephritis. Kidney Int 1992; 42: 851-859.
53. Meyers CM, Tomaszewski JE, Glass JD et al. The nephritogenic T cell response in murine chronic graft-versus-host disease. J Immunol 1998; 161: 5321-5330. (Pubitemid 28519092)
54. Heymann F, Meyer-Schwesinger C, Hamilton-Williams EE et al. Kidney dendritic cell activation is required for progression of renal disease in a mouse model of glomerular injury. J Clin Invest 2009; 119: 1286-1297.
55. Hochheiser K, Engel DR, Hammerich L et al. Kidney dendritic cells become pathogenic during crescentic glomerulonephritis with proteinuria. J Am Soc Nephrol 2011; 22: 306-316.
56. Rui-Mei L, Kara AU, Sinniah R. Upregulation of major histocompatibility complex (MHC) antigen in nephritis associated with murine malaria infection. J Pathol 1998; 185: 212-218. (Pubitemid 28270936)
57. Waeckerle-Men Y, Starke A, Wahl PR et al. Limited costimulatory molecule expression on renal tubular epithelial cells impairs T cell activation. Kidney Blood Press Res 2007; 30: 421-429. (Pubitemid 350191439)
58. Ophascharoensuk V, Pippin JW, Gordon KL et al. Role of intrinsic renal cells versus infiltrating cells in glomerular crescent formation. Kidney Int 1998; 54: 416-425. (Pubitemid 28357404)
59. Mittrücker H-W, Steinhoff U, Köhler A et al. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc Natl Acad Sci USA 2007; 104: 12434-12439. (Pubitemid 47206155)