Murine membranous nephropathy: Immunization with α3(IV) collagen fragment induces subepithelial immune complexes and FcγR-independent nephrotic syndrome

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3268-3277

  Zhang, Jun Jun ^a,f   Malekpour, Mahdi ^a,g   Luo, Wentian ^a   Ge, Linna ^a   Olaru, Florina ^a   Wang, Xu Ping ^a   Bah, Maimouna ^a   Sado, Yoshikazu ^b   Heidet, Laurence ^c   Kleinau, Sandra ^d   Fogo, Agnes B ^e   Borza, Dorin Bogdan ^a,e  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b Shigei Medical Research Institute   (Japan)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d UPPSALA UNIVERSITY   (Sweden)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f ZHENGZHOU UNIVERSITY   (China)

^g TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CD16 ANTIGEN; COLLAGEN TYPE 4; COMPLEMENT COMPONENT C3; FC RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G2B ANTIBODY; UNCLASSIFIED DRUG;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CLINICAL FEATURE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CRESCENTIC GLOMERULONEPHRITIS; DISEASE SEVERITY; GLOMERULONEPHRITIS; GLOMERULUS BASEMENT MEMBRANE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNIZATION; IMMUNOPATHOGENESIS; LUNG ALVEOLITIS; MEMBRANOUS GLOMERULONEPHRITIS; MOUSE; NEPHROTIC SYNDROME; NONHUMAN; PODOCYTE; PRIORITY JOURNAL;

ALBUMINURIA; ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; BASEMENT MEMBRANE; COLLAGEN TYPE IV; COMPLEMENT C3; DISEASE MODELS, ANIMAL; GLOMERULONEPHRITIS, MEMBRANOUS; IMMUNIZATION; IMMUNOGLOBULIN G; KIDNEY; MICE; MICE, CONGENIC; MICE, INBRED DBA; NEPHROTIC SYNDROME; PULMONARY ALVEOLI; RECEPTORS, IGG; RECOMBINANT FUSION PROTEINS;

EID: 84859398103     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103368     Document Type: Article

References (68)

1. Nangaku, M., and W. G. Couser. 2005. Mechanisms of immune-deposit formation and the mediation of immune renal injury. Clin. Exp. Nephrol. 9: 183-191. (Pubitemid 41414116)
2. Glassock, R. J. 2010. The pathogenesis of idiopathic membranous nephropathy: a 50-year odyssey. Am. J. Kidney Dis. 56: 157-167.
3. Beck, L. H., Jr., R. G. Bonegio, G. Lambeau, D. M. Beck, D. W. Powell, T. D. Cummins, J. B. Klein, and D. J. Salant. 2009. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N. Engl. J. Med. 361: 11-21.
4. Debiec, H., V. Guigonis, B. Mougenot, F. Decobert, J. P. Haymann, A. Bensman, G. Deschênes, and P. M. Ronco. 2002. Antenatal membranous glomerulonephritis due to anti-neutral endopeptidase antibodies. N. Engl. J. Med. 346: 2053-2060. (Pubitemid 34680597)
5. Prunotto, M., M. L. Carnevali, G. Candiano, C. Murtas, M. Bruschi, E. Corradini, A. Trivelli, A. Magnasco, A. Petretto, L. Santucci, et al. 2010. Autoimmunity in membranous nephropathy targets aldose reductase and SOD2. J. Am. Soc. Nephrol. 21: 507-519.
6. Meyer-Schwesinger, C., S. Dehde, P. Klug, J. U. Becker, S. Mathey, K. Arefi, S. Balabanov, S. Venz, K. H. Endlich, M. Pekna, et al. 2011. Nephrotic syndrome and subepithelial deposits in a mouse model of immune-mediated anti-podocyte glomerulonephritis. J. Immunol. 187: 3218-3229.
7. Debiec, H., F. Lefeu, M. J. Kemper, P. Niaudet, G. Deschênes, G. Remuzzi, T. Ulinski, and P. Ronco. 2011. Early-childhood membranous nephropathy due to cationic bovine serum albumin. N. Engl. J. Med. 364: 2101-2110.
8. Cunningham, P. N., and R. J. Quigg. 2005. Contrasting roles of complement activation and its regulation in membranous nephropathy. J. Am. Soc. Nephrol. 16: 1214-1222. (Pubitemid 41716506)
9. Borza, D. B. 2007. Autoepitopes and alloepitopes of type IV collagen: role in the molecular pathogenesis of anti-GBM antibody glomerulonephritis. Nephron. Exp. Nephrol. 106: e37-e43.
10. Hudson, B. G., K. Tryggvason, M. Sundaramoorthy, and E. G. Neilson. 2003. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med. 348: 2543-2556. (Pubitemid 36706542)
11. Borza, D. B., K. O. Netzer, A. Leinonen, P. Todd, J. Cervera, J. Saus, and B. G. Hudson. 2000. The goodpasture autoantigen. Identification of multiple cryptic epitopes on the NC1 domain of the alpha3(IV) collagen chain. J. Biol. Chem. 275: 6030-6037. (Pubitemid 30115254)
12. Netzer, K. O., A. Leinonen, A. Boutaud, D. B. Borza, P. Todd, S. Gunwar, J. P. Langeveld, and B. G. Hudson. 1999. The Goodpasture autoantigen. Mapping the major conformational epitope(s) of alpha3(IV) collagen to residues 17-31 and 127-141 of the NC1 domain. J. Biol. Chem. 274: 11267-11274.
13. Hellmark, T., H. Burkhardt, and J. Wieslander. 1999. Goodpasture disease. Characterization of a single conformational epitope as the target of pathogenic autoantibodies. J. Biol. Chem. 274: 25862-25868.
14. Pedchenko, V., O. Bondar, A. B. Fogo, R. Vanacore, P. Voziyan, A. R. Kitching, J. Wieslander, C. Kashtan, D. B. Borza, E. G. Neilson, et al. 2010. Molecular architecture of the Goodpasture autoantigen in anti-GBM nephritis. N. Engl. J. Med. 363: 343-354.
15. Kang, J. S., C. E. Kashtan, A. N. Turner, L. Heidet, B. G. Hudson, and D. B. Borza. 2007. The alloantigenic sites of alpha3alpha4alpha5(IV) collagen: pathogenic X-linked alport alloantibodies target two accessible conformational epitopes in the alpha5NC1 domain. J. Biol. Chem. 282: 10670-10677. (Pubitemid 47093427)
16. Wang, X. P., A. B. Fogo, S. Colon, G. Giannico, S. R. Abul-Ezz, J. H. Miner, and D. B. Borza. 2005. Distinct epitopes for anti-glomerular basement membrane alport alloantibodies and goodpasture autoantibodies within the noncollagenous domain of alpha3(IV) collagen: a janus-faced antigen. J. Am. Soc. Nephrol. 16: 3563-3571. (Pubitemid 46211277)
17. Kalluri, R., A. Torre, C. F. Shield, III, E. D. Zamborsky, M. C. Werner, E. Suchin, G. Wolf, U. M. Helmchen, L. P. van den Heuvel, R. Grossman, et al. 2000. Identification of alpha3, alpha4, and alpha5 chains of type IV collagen as alloantigens for Alport posttransplant anti-glomerular basement membrane antibodies. Transplantation 69: 679-683. (Pubitemid 30129611)
18. Brainwood, D., C. Kashtan, M. C. Gubler, and A. N. Turner. 1998. Targets of alloantibodies in Alport anti-glomerular basement membrane disease after renal transplantation. Kidney Int. 53: 762-766. (Pubitemid 28124293)
19. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcgamma receptors: old friends and new family members. Immunity 24: 19-28. (Pubitemid 43077197)
20. Wakayama, H., Y. Hasegawa, T. Kawabe, T. Hara, S. Matsuo, M. Mizuno, T. Takai, H. Kikutani, and K. Shimokata. 2000. Abolition of anti-glomerular basement membrane antibody-mediated glomerulonephritis in FcRgammadeficient mice. Eur. J. Immunol. 30: 1182-1190. (Pubitemid 30216236)
21. Park, S. Y., S. Ueda, H. Ohno, Y. Hamano, M. Tanaka, T. Shiratori, T. Yamazaki, H. Arase, N. Arase, A. Karasawa, et al. 1998. Resistance of Fc receptor- deficient mice to fatal glomerulonephritis. J. Clin. Invest. 102: 1229-1238. (Pubitemid 28436283)
22. Clynes, R., C. Dumitru, and J. V. Ravetch. 1998. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 279: 1052-1054. (Pubitemid 28113310)
23. Matsumoto, K., N. Watanabe, B. Akikusa, K. Kurasawa, R. Matsumura, Y. Saito, I. Iwamoto, and T. Saito. 2003. Fc receptor-independent development of autoimmune glomerulonephritis in lupus-prone MRL/lpr mice. Arthritis Rheum. 48: 486-494. (Pubitemid 36278018)
24. Guo, S., A. S. Mühlfeld, T. A. Wietecha, C. J. Peutz-Kootstra, J. Kowalewska, K. Yi, M. Spencer, W. Pichaiwong, F. Nimmerjahn, K. L. Hudkins, and C. E. Alpers. 2009. Deletion of activating Fcgamma receptors does not confer protection in murine cryoglobulinemia-associated membranoproliferative glomerulonephritis. Am. J. Pathol. 175: 107-118.
25. Giorgini, A., H. J. Brown, H. R. Lock, F. Nimmerjahn, J. V. Ravetch, J. S. Verbeek, S. H. Sacks, and M. G. Robson. 2008. Fc gamma RIII and Fc gamma RIV are indispensable for acute glomerular inflammation induced by switch variant monoclonal antibodies. J. Immunol. 181: 8745-8752.
26. Fujii, T., Y. Hamano, S. Ueda, B. Akikusa, S. Yamasaki, M. Ogawa, H. Saisho, J. S. Verbeek, S. Taki, and T. Saito. 2003. Predominant role of FcgammaRIII in the induction of accelerated nephrotoxic glomerulonephritis. Kidney Int. 64: 1406-1416. (Pubitemid 37153807)
27. Kaneko, Y., F. Nimmerjahn, M. P. Madaio, and J. V. Ravetch. 2006. Pathology and protection in nephrotoxic nephritis is determined by selective engagement of specific Fc receptors. J. Exp. Med. 203: 789-797.
28. Tarzi, R. M., K. A. Davies, J. W. Claassens, J. S. Verbeek, M. J. Walport, and H. T. Cook. 2003. Both Fcgamma receptor I and Fcgamma receptor III mediate disease in accelerated nephrotoxic nephritis. Am. J. Pathol. 162: 1677-1683. (Pubitemid 36512851)
29. Nakamura, A., T. Yuasa, A. Ujike, M. Ono, T. Nukiwa, J. V. Ravetch, and T. Takai. 2000. 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. 191: 899-906.
30. Hopfer, H., R. Maron, U. Butzmann, U. Helmchen, H. L. Weiner, and R. Kalluri. 2003. The importance of cell-mediated immunity in the course and severity of autoimmune anti-glomerular basement membrane disease in mice. FASEB J. 17: 860-868. (Pubitemid 36538661)
31. Xie, C., R. Sharma, H. Wang, X. J. Zhou, and C. Mohan. 2004. Strain distribution pattern of susceptibility to immune-mediated nephritis. J. Immunol. 172: 5047-5055. (Pubitemid 38456432)
32. Kleinau, S., P. Martinsson, and B. Heyman. 2000. Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J. Exp. Med. 191: 1611-1616. (Pubitemid 30257357)
33. Boutaud, A., D. B. Borza, O. Bondar, S. Gunwar, K. O. Netzer, N. Singh, Y. Ninomiya, Y. Sado, M. E. Noelken, and B. G. Hudson. 2000. Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J. Biol. Chem. 275: 30716-30724.
34. Kang, J. S., X. P. Wang, J. H. Miner, R. Morello, Y. Sado, D. R. Abrahamson, and D. B. Borza. 2006. Loss of alpha3/alpha4(IV) collagen from the glomerular basement membrane induces a strain-dependent isoform switch to alpha5alpha6(IV) collagen associated with longer renal survival in Col4a3-/- Alport mice. J. Am. Soc. Nephrol. 17: 1962-1969. (Pubitemid 44036180)
35. Saus, J., J. Wieslander, J. P. Langeveld, S. Quinones, and B. G. Hudson. 1988. Identification of the Goodpasture antigen as the alpha 3(IV) chain of collagen IV. J. Biol. Chem. 263: 13374-13380.
36. Heidet, L., D. B. Borza, M. Jouin, M. Sich, M. G. Mattei, Y. Sado, B. G. Hudson, N. Hastie, C. Antignac, and M. C. Gubler. 2003. A human-mouse chimera of the alpha3alpha4alpha5(IV) collagen protomer rescues the renal phenotype in Col4a3-/- Alport mice. Am. J. Pathol. 163: 1633-1644. (Pubitemid 37175110)
37. Andrews, K. L., J. L. Mudd, C. Li, and J. H. Miner. 2002. Quantitative trait loci influence renal disease progression in a mouse model of Alport syndrome. Am. J. Pathol. 160: 721-730. (Pubitemid 34160350)
38. Tchekneva, E., M. Dikov, V. Kadkina, and D. Polosukhina. 2011. Collection station for accelerated collection of the specimens from laboratory animals. United States patent application 20110239953. 2011 Oct 6.
39. Kim, Y., R. Butkowski, B. Burke, M. M. Kleppel, J. Crosson, A. Katz, and A. F. Michael. 1991. Differential expression of basement membrane collagen in membranous nephropathy. Am. J. Pathol. 139: 1381-1388.
40. Minto, A. W., R. Kalluri, M. Togawa, E. C. Bergijk, P. D. Killen, and D. J. Salant. 1998. Augmented expression of glomerular basement membrane specific type IV collagen isoforms (alpha3-alpha5) in experimental membranous nephropathy. Proc. Assoc. Am. Physicians 110: 207-217. (Pubitemid 28235172)
41. Fervenza, F. C., S. Sethi, and U. Specks. 2008. Idiopathic membranous nephropathy: diagnosis and treatment. Clin. J. Am. Soc. Nephrol. 3: 905-919.
42. Glassock, R. J. 2004. The treatment of idiopathic membranous nephropathy: a dilemma or a conundrum? Am. J. Kidney Dis. 44: 562-566. (Pubitemid 39164634)
43. Waldman, M., and H. A. Austin, III. 2009. Controversies in the treatment of idiopathic membranous nephropathy. Nat. Rev. Nephrol. 5: 469-479.
44. Cybulsky, A. V., R. J. Quigg, and D. J. Salant. 2005. Experimental membranous nephropathy redux. Am. J. Physiol. Renal Physiol. 289: F660-F671. (Pubitemid 41324186)
45. Luo, W., X. P. Wang, C. E. Kashtan, and D. B. Borza. 2010. Alport alloantibodies but not Goodpasture autoantibodies induce murine glomerulonephritis: protection by quinary crosslinks locking cryptic a3(IV) collagen autoepitopes in vivo. J. Immunol. 185: 3520-3528.
46. Borza, D. B., O. Bondar, S. Colon, P. Todd, Y. Sado, E. G. Neilson, and B. G. Hudson. 2005. Goodpasture autoantibodies unmask cryptic epitopes by selectively dissociating autoantigen complexes lacking structural reinforcement: novel mechanisms for immune privilege and autoimmune pathogenesis. J. Biol. Chem. 280: 27147-27154. (Pubitemid 41040753)
47. Vanacore, R. M., A. J. Ham, J. P. Cartailler, M. Sundaramoorthy, P. Todd, V. Pedchenko, Y. Sado, D. B. Borza, and B. G. Hudson. 2008. 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. 283: 22737-22748.
48. Summers, S. A., O. M. Steinmetz, M. Li, J. Y. Kausman, T. Semple, K. L. Edgtton, D. B. Borza, H. Braley, S. R. Holdsworth, and A. R. Kitching. 2009. Th1 and Th17 cells induce proliferative glomerulonephritis. J. Am. Soc. Nephrol. 20: 2518-2524.
49. Nangaku, M., S. J. Shankland, and W. G. Couser. 2005. Cellular response to injury in membranous nephropathy. J. Am. Soc. Nephrol. 16: 1195-1204. (Pubitemid 41716504)
50. Nilsson, U. R., and H. J. Müller-Eberhard. 1967. Deficiency of the fifth component of complement in mice with an inherited complement defect. J. Exp. Med. 125: 1-16.
51. Oliveira, D. B. 1998. Membranous nephropathy: an IgG4-mediated disease. Lancet 351: 670-671. (Pubitemid 28098462)
52. Holdsworth, S. R., A. R. Kitching, and P. G. Tipping. 1999. Th1 and Th2 T helper cell subsets affect patterns of injury and outcomes in glomerulonephritis. Kidney Int. 55: 1198-1216. (Pubitemid 29157116)
53. Kuroki, A., M. Iyoda, T. Shibata, and T. Sugisaki. 2005. Th2 cytokines increase and stimulate B cells to produce IgG4 in idiopathic membranous nephropathy. Kidney Int. 68: 302-310. (Pubitemid 43181389)
54. Hirayama,K., I. Ebihara, S.Yamamoto,H.Kai,K.Muro,K.Yamagata,M.Kobayashi, and A. Koyama. 2002. Predominance of type-2 immune response in idiopathic membranous nephropathy. Cytoplasmic cytokine analysis. Nephron 91: 255-261. (Pubitemid 34621692)
55. Wu, C. C., J. S. Chen, S. J. Chen, S. H. Lin, A. Chen, L. C. Chang, H. K. Sytwu, and Y. F. Lin. 2007. Kinetics of adaptive immunity to cationic bovine serum albumin-induced membranous nephropathy. Kidney Int. 72: 831-840. (Pubitemid 47462076)
56. Shimizu, S., N. Sugiyama, K. Masutani, A. Sadanaga, Y. Miyazaki, Y. Inoue, M. Akahoshi, R. Katafuchi, H. Hirakata, M. Harada, et al. 2005. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J. Immunol. 175: 7185-7192. (Pubitemid 41713412)
57. Edgington, T. S., R. J. Glassock, and F. J. Dixon. 1967. Autologous immunecomplex pathogenesis of experimental allergic glomerulonephritis. Science 155: 1432-1434.
58. Barabas, A. Z., and R. Lannigan. 1981. Immune-complex nephritis in the rabbit produced by injections of rat renal tubular fraction 3 antigen. Br. J. Exp. Pathol. 62: 94-102. (Pubitemid 11095806)
59. Chen, J. S., A. Chen, L. C. Chang, W. S. Chang, H. S. Lee, S. H. Lin, and Y. F. Lin. 2004. Mouse model of membranous nephropathy induced by cationic bovine serum albumin: antigen dose-response relations and strain differences. Nephrol. Dial. Transplant. 19: 2721-2728. (Pubitemid 39480964)
60. Border, W. A., H. J. Ward, E. S. Kamil, and A. H. Cohen. 1982. Induction of membranous nephropathy in rabbits by administration of an exogenous cationic antigen. J. Clin. Invest. 69: 451-461.
61. Borza, C. M., D. B. Borza, V. Pedchenko, M. A. Saleem, P. W. Mathieson, Y. Sado, H. M. Hudson, A. Pozzi, J. Saus, D. R. Abrahamson, et al. 2008. Human podocytes adhere to the KRGDS motif of the alpha3alpha4alpha5 collagen IV network. J. Am. Soc. Nephrol. 19: 677-684.
62. Borza, C. M., A. Pozzi, D. B. Borza, V. Pedchenko, T. Hellmark, B. G. Hudson, and R. Zent. 2006. Integrin alpha3beta1, a novel receptor for alpha3(IV) noncollagenous domain and a trans-dominant Inhibitor for integrin alphavbeta3. J. Biol. Chem. 281: 20932-20939. (Pubitemid 44115434)
63. Abrahamson, D. R., B. G. Hudson, L. Stroganova, D. B. Borza, and P. L. St John. 2009. Cellular origins of type IV collagen networks in developing glomeruli. J. Am. Soc. Nephrol. 20: 1471-1479.
64. Makino, H., B. Lelongt, and Y. S. Kanwar. 1988. Nephritogenicity of proteoglycans. II. A model of immune complex nephritis. Kidney Int. 34: 195-208.
65. Icard, P., L. Pelletier, M. C. Vial, C. Mandet, R. Pasquier, A. Michel, and P. Druet. 1993. Evidence for a role of antilaminin-producing B cell clones that escape tolerance in the pathogenesis of HgCl2-induced membranous glomerulopathy. Nephrol. Dial. Transplant. 8: 122-127. (Pubitemid 23082747)
66. Basford, A. W., J. Lewis, J. P. Dwyer, and A. B. Fogo. 2011. Membranous nephropathy with crescents. J. Am. Soc. Nephrol. 22: 1804-1808.
67. Jefferson, J. A., J. W. Pippin, and S. J. Shankland. 2010. Experimental Models of Membranous Nephropathy. Drug Discov. Today Dis. Models 7: 27-33.
68. Bao, L., M. Haas, J. Pippin, Y. Wang, T. Miwa, A. Chang, A. W. Minto, M. Petkova, G. Qiao, W. C. Song, et al. 2009. Focal and segmental glomerulosclerosis induced in mice lacking decay-accelerating factor in T cells. J. Clin. Invest. 119: 1264-1274.