Table of Contents Author Guidelines Submit a Manuscript
Clinical and Developmental Immunology
Volume 2012, Article ID 579670, 8 pages
http://dx.doi.org/10.1155/2012/579670
Review Article

Mesangial Cell-Specific Antibodies Are Central to the Pathogenesis of Lupus Nephritis

1EA2216 “Immunology & Pathology” and IFR146 “ScInBios,” European University of Brittany, 29200 Brest, France
2Unit of Nephrology, Brest University Medical School Hospital, 29609 Brest, France
3Laboratory of Immunology, Brest University Medical School Hospital, BP824, 29609 Brest, France

Received 23 June 2011; Revised 31 August 2011; Accepted 4 October 2011

Academic Editor: Sara Marsal

Copyright © 2012 Guillaume Seret et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. T. Borchers, S. M. Naguwa, Y. Shoenfeld, and M. E. Gershwin, “The geoepidemiology of systemic lupus erythematosus,” Autoimmunity Reviews, vol. 9, no. 5, pp. A277–A287, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. A. Delgado-Vega, E. Sánchez, S. Löfgren, C. Castillejo-López, and M. E. Alarcón-Riquelme, “Recent findings on genetics of systemic autoimmune diseases,” Current Opinion in Immunology, vol. 22, no. 6, pp. 698–705, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. V. A. Seligman, R. F. Lum, J. L. Olson, H. Li, and L. A. Criswell, “Demographic differences in the development of lupus nephritis: a retrospective analysis,” American Journal of Medicine, vol. 112, no. 9, pp. 726–729, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. A. E. Koh, S. W. Njoroge, M. Feliu et al., “The SLAM family member CD48 protects lupus-prone mice from autoimmune nephritis,” Journal of Autoimmunity, vol. 37, no. 1, pp. 48–57, 2011. View at Publisher · View at Google Scholar · View at PubMed
  5. Z. T. Chu, N. Tsuchiya, C. Kyogoku et al., “Association of Fc-gamma receptor IIb polymorphism with susceptibility to systemic lupus erythematosus in Chinese: a common susceptibility gene in the Asian populations,” Tissue Antigens, vol. 63, no. 1, pp. 21–27, 2004. View at Publisher · View at Google Scholar
  6. Q. Z. Li, J. Zhou, R. Yang et al., “The lupus-susceptibility gene kallikrein downmodulates antibody-mediated glomerulonephritis,” Genes and Immunity, vol. 10, no. 5, pp. 503–508, 2009. View at Publisher · View at Google Scholar · View at PubMed
  7. D. Y. Chen, C. W. Hsieh, K. S. Chen, Y. M. Chen, F. J. Lin, and J. L. Lan, “Association of interleukin-18 promoter polymorphisms with WHO pathological classes and serum IL-18 levels in Chinese patients with lupus nephritis,” Lupus, vol. 18, no. 1, pp. 29–37, 2009. View at Google Scholar
  8. H. Bouali, P. Nietert, T. M. Nowling et al., “Association of the G-463A myeloperoxidase gene polymorphism with renal disease in African Americans with systemic lupus erythematosus,” Journal of Rheumatology, vol. 34, no. 10, pp. 2028–2034, 2007. View at Google Scholar
  9. P. L. De Jager, A. Richardson, T. J. Vyse, and J. D. Rioux, “Genetic variation in toll-like receptor 9 and susceptibility to systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 54, no. 4, pp. 1279–1282, 2006. View at Publisher · View at Google Scholar · View at PubMed
  10. P. Sandrin-Garcia, L. A. C. Brandão, A. V.C. Coelho et al., “Mannose binding lectin gene (MBL2) functional polymorphisms are associated with systemic lupus erythematosus in southern Brazilians,” Human Immunology, vol. 72, no. 6, pp. 516–521, 2011. View at Publisher · View at Google Scholar · View at PubMed
  11. Y. Renaudineau, B. Deocharan, S. Jousse, E. Renaudineau, C. Putterman, and P. Youinou, “Anti-alpha-actinin antibodies: a new marker of lupus nephritis,” Autoimmunity Reviews, vol. 6, no. 7, pp. 464–468, 2007. View at Publisher · View at Google Scholar · View at PubMed
  12. S. Yung, K. F. Cheung, Q. Zhang, and T. M. Chan, “Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis,” Journal of the American Society of Nephrology, vol. 21, no. 11, pp. 1912–1927, 2010. View at Publisher · View at Google Scholar · View at PubMed
  13. D. Schlöndorff and B. Banas, “The mesangial cell revisited: no cell is an island,” Journal of the American Society of Nephrology, vol. 20, no. 6, pp. 1179–1187, 2009. View at Publisher · View at Google Scholar · View at PubMed
  14. S. Akilesh, T. B. Huber, H. Wu et al., “Podocytes use FcRn to clear IgG from the glomerular basement membrane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 3, pp. 967–972, 2008. View at Publisher · View at Google Scholar · View at PubMed
  15. R. M. Tarzi, K. A. Davies, M. G. Robson et al., “Nephrotoxic nephritis is mediated by Fc-gamma receptors on circulating leukocytes and not intrinsic renal cells,” Kidney International, vol. 62, no. 6, pp. 2087–2096, 2002. View at Publisher · View at Google Scholar · View at PubMed
  16. J. Berger and N. Hinglais, “Intercapillary deposits of IgA-IgG,” Journal d'Urologie et de Nephrologie, vol. 74, no. 9, pp. 694–695, 1968. View at Google Scholar
  17. Y. Hiki, H. Iwase, M. Saitoh et al., “Reactivity of glomerular and serum IgA1 to jacalin in IgA nephropathy,” Nephron, vol. 72, no. 3, pp. 429–435, 1996. View at Google Scholar
  18. I. C. Moura, M. Arcos-Fajardo, A. Gdoura et al., “Engagement of transferrin receptor by polymeric IgA1: evidence for a positive feedback loop involving increased receptor expression and mesangial cell proliferation in IgA nephropathy,” Journal of the American Society of Nephrology, vol. 16, no. 9, pp. 2667–2676, 2005. View at Publisher · View at Google Scholar · View at PubMed
  19. I. C. Moura, M. N. Centelles, M. Arcos-Fajardo et al., “Identification of the transferrin receptor as a novel immunoglobulin IgA1 receptor and its enhanced expression on mesangial cells in IgA nephropathy,” Journal of Experimental Medicine, vol. 194, no. 4, pp. 417–425, 2001. View at Publisher · View at Google Scholar
  20. M. Endo, H. Ohi, I. Ohsawa, T. Fujita, M. Matsushita, and T. Fujita, “Glomerular deposition of mannose-binding lectin indicates a novel mechanism of complement activation in IgA nephropathy,” Nephrology Dialysis Transplantation, vol. 13, no. 8, pp. 1984–1990, 1998. View at Publisher · View at Google Scholar
  21. N. Kashihara, Y. Haruna, V. K. Kondeti, and Y. S. Kanwar, “Oxidative stress in diabetic nephropathy,” Current Medicinal Chemistry, vol. 17, no. 34, pp. 4256–4269, 2010. View at Publisher · View at Google Scholar
  22. A. Hedberg, E. S. Mortensen, and O. P. Rekvig, “Chromatin as a target antigen in human and murine lupus nephritis,” Arthritis Research and Therapy, vol. 13, article 214, 2011. View at Google Scholar
  23. M. Kalaaji, K. A. Fenton, E. S. Mortensen et al., “Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis,” Kidney International, vol. 71, no. 7, pp. 664–672, 2007. View at Publisher · View at Google Scholar · View at PubMed
  24. K. Fenton, S. Fismen, A. Hedberg et al., “Anti-dsDNA antibodies promote initiation, and acquired loss of renal dnase1 promotes progression of lupus nephritis in autoimmune (NZBxNZW)F1 mice,” PLoS One, vol. 4, no. 12, Article ID e8474, 2009. View at Publisher · View at Google Scholar · View at PubMed
  25. M. Mannik, C. E. Merrill, L. D. Stamps, and M. H. Wener, “Multiple autoantibodies form the glomerular immune deposits in patients with systemic lupus erythematosus,” Journal of Rheumatology, vol. 30, no. 7, pp. 1495–1504, 2003. View at Google Scholar
  26. G. Mostoslavsky, R. Fischel, N. Yachimovich, S. H. Sacks et al., “Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry,” European Journal of Immunology, vol. 31, no. 4, pp. 1221–1227, 2001. View at Google Scholar
  27. C. Hanrotel-Saliou, I. Segalen, Y. Le Meur, P. Youinou, and Y. Renaudineau, “Glomerular antibodies in lupus nephritis,” Clinical Reviews in Allergy and Immunology, vol. 40, pp. 151–158, 2011. View at Google Scholar
  28. J. B. Katz, W. Limpanasithikul, and B. Diamond, “Mutational analysis of an autoantibody: differential binding and pathogenicity,” Journal of Experimental Medicine, vol. 180, no. 3, pp. 925–932, 1994. View at Publisher · View at Google Scholar
  29. B. Deocharan, X. Qing, J. Lichauco, and C. Putterman, “Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA aptibodies,” Journal of Immunology, vol. 168, no. 6, pp. 3072–3078, 2002. View at Google Scholar
  30. M. C. J. van Bruggen, C. Kramers, M. N. Hylkema, R. J. T. Smeenk, and J. H. M. Berden, “Significance of anti-nuclear and anti-extracellular matrix autoantibodies for albuminuria in murine lupus nephritis; a longitudinal study on plasma and glomerular eluates in MRL/l mice,” Clinical and Experimental Immunology, vol. 105, no. 1, pp. 132–139, 1996. View at Google Scholar
  31. J. J. Weening, V. D. D'Agati, M. M. Schwartz et al., “The classification of glomerulonephritis in systemic lupus erythematosus revisited,” Journal of the American Society of Nephrology, vol. 15, no. 2, pp. 241–250, 2004. View at Publisher · View at Google Scholar
  32. S. G. Lee, Y. M. Cho, M. W. So et al., “ISN/RPS 2003 class II mesangial proliferative lupus nephritis: a comparison between cases that progressed to class III or IV and cases that did not,” Rheumatology International. In press. View at Publisher · View at Google Scholar · View at PubMed
  33. M. E. Zabaleta-Lanz, L. E. Muñoz, F. J. Tapanes et al., “Further description of early clinically silent lupus nephritis,” Lupus, vol. 15, no. 12, pp. 845–851, 2006. View at Publisher · View at Google Scholar
  34. N. A. Fathi, M. R. Hussein, H. I. Hassan, E. Mosad, H. Galal, and N. A. Afifi, “Glomerular expression and elevated serum Bcl-2 and Fas proteins in lupus nephritis: preliminary findings,” Clinical and Experimental Immunology, vol. 146, no. 2, pp. 339–343, 2006. View at Publisher · View at Google Scholar · View at PubMed
  35. S. D. Marks, S. J. Williams, K. Tullus, and N. J. Sebire, “Glomerular expression of monocyte chemoattractant protein-1 is predictive of poor renal prognosis in paediatric lupus nephritis,” Nephrology Dialysis Transplantation, vol. 23, no. 11, pp. 3521–3526, 2008. View at Publisher · View at Google Scholar · View at PubMed
  36. S. Segerer, A. Henger, H. Schmid et al., “Expression of the chemokine receptor CXCR1 in human glomerular diseases,” Kidney International, vol. 69, no. 10, pp. 1765–1773, 2006. View at Publisher · View at Google Scholar · View at PubMed
  37. L. Zheng, R. Sinniah, and S. I. Hsu, “Renal cell apoptosis and proliferation may be linked to nuclear factor-kappaB activation and expression of inducible nitric oxide synthase in patients with lupus nephritis,” Human Pathology, vol. 37, no. 6, pp. 637–647, 2006. View at Publisher · View at Google Scholar · View at PubMed
  38. A. A. Tveita, O. P. Rekvig, and S. N. Zykova, “Increased glomerular matrix metalloproteinase activity in murine lupus nephritis,” Kidney International, vol. 74, no. 9, pp. 1150–1158, 2008. View at Publisher · View at Google Scholar · View at PubMed
  39. X. Qing, J. Zavadil, M. B. Crosby et al., “Nephritogenic anti-DNA antibodies regulate gene expression in MRL/lpr mouse glomerular mesangial cells,” Arthritis and Rheumatism, vol. 54, no. 7, pp. 2198–2210, 2006. View at Publisher · View at Google Scholar · View at PubMed
  40. S. Yung, Q. Zhang, C. Z. Zhang, W. C. Kwok, L. L. Sing, and M. C. Tak, “Anti-DNA antibody induction of protein kinase C phosphorylation and fibronectin synthesis in human and murine lupus and the effect of mycophenolic acid,” Arthritis and Rheumatism, vol. 60, no. 7, pp. 2071–2082, 2009. View at Publisher · View at Google Scholar · View at PubMed
  41. M. R. Arbuckle, M. T. McClain, M. V. Rubertone et al., “Development of autoantibodies before the clinical onset of systemic lupus erythematosus,” The New England Journal of Medicine, vol. 349, no. 16, pp. 1526–1533, 2003. View at Publisher · View at Google Scholar · View at PubMed
  42. F. J. Tápanes, M. Vásquez, R. Ramírez, C. Matheus, M. A. Rodríguez, and N. Bianco, “Cluster analysis of antinuclear autoantibodies in the prognosis of SLE nephropathy: are anti-extractable nuclear antibodies protective?” Lupus, vol. 9, no. 6, pp. 437–444, 2000. View at Google Scholar
  43. T. Mehrani and M. Petri, “IgM anti-β2 glycoprotein I is protective against lupus nephritis and renal damage in systemic lupus erythematosus,” Journal of Rheumatology, vol. 38, no. 3, pp. 450–453, 2011. View at Publisher · View at Google Scholar · View at PubMed
  44. Q. Z. Li, C. Xie, T. Wu et al., “Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays,” Journal of Clinical Investigation, vol. 115, no. 12, pp. 3428–3439, 2005. View at Publisher · View at Google Scholar · View at PubMed
  45. B. Gaynor, C. Putterman, P. Valadon, L. Spatz, M. D. Scharff, and B. Diamond, “Peptide inhibition of glomerular deposition of an anti-DNA antibody,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 5, pp. 1955–1960, 1997. View at Publisher · View at Google Scholar
  46. C. Putterman and B. Diamond, “Immunization with a peptide surrogate for double-stranded DNA induces autoantibody production and renal immunoglobulin deposition,” Journal of Experimental Medicine, vol. 188, no. 1, pp. 29–38, 1998. View at Publisher · View at Google Scholar
  47. H. Amital, M. Heilweil, R. Ulmansky et al., “Treatment with a laminin-derived peptide suppresses lupus nephritis,” Journal of Immunology, vol. 175, no. 8, pp. 5516–5523, 2005. View at Google Scholar
  48. H. Du, M. Chen, Y. Zhang, M. H. Zhao, and H. Y. Wang, “Cross-reaction of anti-DNA autoantibodies with membrane proteins of human glomerular mesangial cells in sera from patients with lupus nephritis,” Clinical and Experimental Immunology, vol. 145, no. 1, pp. 21–27, 2006. View at Publisher · View at Google Scholar · View at PubMed
  49. T. M. Chan, J. K. H. Leung, S. K. N. Ho, and S. Yung, “Mesangial cell-binding anti-DNA antibodies in patients with systemic lupus erythematosus,” Journal of the American Society of Nephrology, vol. 13, no. 5, pp. 1219–1229, 2002. View at Publisher · View at Google Scholar
  50. J. M. Kaplan, S. H. Kim, K. N. North et al., “Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis,” Nature Genetics, vol. 24, no. 3, pp. 251–256, 2000. View at Publisher · View at Google Scholar · View at PubMed
  51. H. Amital, M. Heilweil-Harel, R. Ulmansky et al., “Antibodies against the VRT101 laminin epitope correlate with human SLE disease activity and can be removed by extracorporeal immunoadsorption,” Rheumatology, vol. 46, no. 9, pp. 1433–1437, 2007. View at Publisher · View at Google Scholar · View at PubMed
  52. B. Deocharan, Z. Zhou, K. Antar et al., “Alpha-actinin immunization elicits anti-chromatin autoimmunity in nonautoimmune mice,” Journal of Immunology, vol. 179, no. 2, pp. 1313–1321, 2007. View at Google Scholar
  53. S. Croquefer, Y. Renaudineau, S. Jousse et al., “The anti-alpha-actinin test completes anti-DNA determination in systemic lupus erythematosus,” Annals of the New York Academy of Sciences, vol. 1050, pp. 170–175, 2005. View at Publisher · View at Google Scholar · View at PubMed
  54. Y. Renaudineau, S. Croquefer, S. Jousse et al., “Association of alpha-actinin-binding anti-double-stranded DNA antibodies with lupus nephritis,” Arthritis and Rheumatism, vol. 54, no. 8, pp. 2523–2532, 2006. View at Publisher · View at Google Scholar · View at PubMed
  55. D. Cornec, G. E. Cornec-Le, Z. Segalen et al., “Which autoantibodies announce that lupus nephritis is on the way?” International Journal of Clinical Rheumatology, vol. 4, no. 3, pp. 287–295, 2009. View at Publisher · View at Google Scholar
  56. J. J. Manson, A. Ma, P. Rogers et al., “Relationship between anti-dsDNA, anti-nucleosome and anti-alpha-actinin antibodies and markers of renal disease in patients with lupus nephritis: a prospective longitudinal study,” Arthritis Research & Therapy, vol. 11, no. 5, p. R154, 2009. View at Google Scholar
  57. G. Guéguen, G. Dalekos, J. B. Nousbaum et al., “Double reactivity against actin and alpha-actinin defines a severe form of autoimmune hepatitis type 1,” Journal of Clinical Immunology, vol. 26, no. 6, pp. 495–505, 2006. View at Publisher · View at Google Scholar · View at PubMed
  58. G. Cesarman-Maus, N. P. Ríos-Luna, A. B. Deora et al., “Autoantibodies against the fibrinolytic receptor, annexin 2, in antiphospholipid syndrome,” Blood, vol. 107, no. 11, pp. 4375–4382, 2006. View at Publisher · View at Google Scholar · View at PubMed
  59. C. J. Kootstra, E. C. Bergijk, A. Veninga et al., “Qualitative alterations in laminin expression in experimental lupus nephritis,” American Journal of Pathology, vol. 147, no. 2, pp. 476–488, 1995. View at Google Scholar
  60. M. Reichlin, “Autoantibodies to the ribosomal P proteins in systemic lupus erythematosus,” Clinical and Experimental Medicine, vol. 6, no. 2, pp. 49–52, 2006. View at Publisher · View at Google Scholar · View at PubMed
  61. M. Mosca, D. Chimenti, F. Pratesi et al., “Prevalence and clinico-serological correlations of anti-alpha-enolase, anti-C1q, and anti-dsDNA antibodies in patients with systemic lupus erythematosus,” Journal of Rheumatology, vol. 33, no. 4, pp. 695–697, 2006. View at Google Scholar