FcγRIIB deficiency leads to autoimmunity and a defective response to apoptosis in MrL-MpJ mice

Journal of Immunology

Volumn 180, Issue 8, 2008, Pages 5670-5679

  McGaha, Tracy L ^a   Karlsson, Mikael C I ^b   Ravetch, Jeffrey V ^c  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 12; ANTINUCLEAR ANTIBODY; FC RECEPTOR; FC RECEPTOR IIB; IMMUNOGLOBULIN CLASS; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; GERMINAL CENTER; IMMUNE COMPLEX DEPOSITION; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; THYMOCYTE; ANIMAL; ANTIGEN ANTIBODY COMPLEX; B LYMPHOCYTE; C57BL MOUSE; IMMUNOLOGY; KIDNEY; KIDNEY DISEASE; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; SPLEEN;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, CD; APOPTOSIS; AUTOIMMUNITY; B-LYMPHOCYTES; DENDRITIC CELLS; GERMINAL CENTER; IMMUNOGLOBULIN ISOTYPES; INTERLEUKIN-12; KIDNEY; KIDNEY DISEASES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PLASMA CELLS; RECEPTORS, IGG; SPLEEN;

EID: 45949111444     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.8.5670     Document Type: Article

References (45)

1. Fanciulli, M., P. J. Norsworthy, E. Petretto, R. Dong, L. Harper, L. Kamesh, J. M. Heward, S. C. Gough, A. de Smith, A. I. Blakemore, et al. 2007. FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat. Genet. 39: 721-723.
2. Alarcon, G. S., G. McGwin, Jr., M. Petri, R. Ramsey-Goldman, B. J. Fessler, L. M. Vila, J. C. Edberg, J. D. Reveille, and R. P. Kimberly. 2006. Time to renal disease and end-stage renal disease in PROFILE: a multiethnic lupus cohort. PLoS Med. 3: e396.
3. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcγ receptors: old friends and new family members. Immunity 24: 19-28.
4. Siriboonrit, U., N. Tsuchiya, M. Sirikong, C. Kyogoku, S. Bejrachandra, P. Suthipinittharm, K. Luangtrakool, D. Srinak, R. Thongpradit, K. Fujiwara, et al. 2003. Association of Fcγ receptor lIb and IIIb polymorphisms with susceptibility to systemic lupus erythematosus in Thais. Tissue Antigens 61: 374-383.
5. Kono, H., C. Kyogoku, T. Suzuki, N. Tsuchiya, H. Honda, K. Yamamoto, K. Tokunaga, and Z. Honda. 2005. FcγRIIB Ile232Thr transmembrane polymorphism associated with human systemic lupus erythematosus decreases affinity to lipid rafts and attenuates inhibitory effects on B cell receptor signaling. Hum. Mol. Genet. 14: 2881-2892.
6. Kyogoku, C, H. M. Dijstelbloem, N. Tsuchiya, Y. Hatta, H. Kato, A. Yamaguchi, T. Fukazawa, M. D. Jansen, H. Hashimoto, J. G. van de Winkel, et al. 2002. Fcγ receptor gene polymorphisms in Japanese patients with systemic lupus erythematosus: contribution of FCGR2B to genetic susceptibility. Arthritis Rheum. 46: 1242-1254.
7. Chu, Z. T., N. Tsuchiya, C. Kyogoku, J. Ohashi, Y. P. Qian, S. B. Xu, C. Z. Mao, J. Y. Chu, and K. Tokunaga. 2004. Association of Fcγ receptor lIb polymorphism with susceptibility to systemic lupus erythematosus in Chinese: a common susceptibility gene in the Asian populations. Tissue Antigens 63: 21-27.
8. Su, K., J. Wu, J. C. Edberg, X. Li, P. Ferguson, G. S. Cooper, C. D. Langefeld, and R. P. Kimberly. 2004. A promoter haplotype of the immunoreceptor tyrosinebased inhibitory motif-bearing FcγRUb alters receptor expression and associates with autoimmunity: I. Regulatory FCGR2B polymorphisms and their association with systemic lupus erythematosus. J. Immunol. 172: 7186-7191.
9. Blank, M. C, R. N. Stefanescu, E. Masuda, F. Marti, P. D. King, P. B. Redecha, R. J. Wurzburger, M. G. Peterson, S. Tanaka, and L. Pricop. 2005. Decreased transcription of the human FCGR2B gene mediated by the -343 G/C promoter polymorphism and association with systemic lupus erythematosus. Hum. Genet. 117: 220-227.
10. Mackay, M., A. Stanevsky, T. Wang, C. Aranow, M. Li, S. Koenig, J. V. Ravetch, and B. Diamond. 2006. Selective dysregulation of the FcγIIB receptor on memory B cells in SLE. J. Exp. Med. 203: 2157-2164.
11. Enyedy, E. J., J. P. Mitchell, M. P. Nambiar, and G. C. Tsokos. 2001. Defective FcyRIIbl signaling contributes to enhanced calcium response in B cells from patients with systemic lupus erythematosus. Clin. Immunol. 101: 130-135.
12. Pritchard, N. R., A. J. Cutler, S. Uribe, S. J. Chadban, B. J. Morley, and K. G. Smith. 2000. Autoimmune-prone mice share a promoter haplotype associated with reduced expression and function of the Fc receptor FcγRII. Curr. Biol. 10: 227-230.
13. Jiang, Y., S. Hirose, M. Abe, R. Sanokawa-Akakura, M. Ohtsuji, X. Mi, N. Li, Y. Xiu, D. Zhang, J. Shirai, et al. 2000. Polymorphisms in IgG Fc receptor IIB regulatory regions associated with autoimmune susceptibility. Immunogenetics 51: 429-435.
14. Jiang, Y., S. Hirose, R. Sanokawa-Akakura, M. Abe, X. Mi, N. Li, Y. Miura, J. Shirai, D. Zhang, Y. Hamano, and T. Shirai. 1999. Genetically determined aberrant down-regulation of FcγRIIB1 in germinal center B cells associated with hyper-IgG and IgG autoantibodies in murine systemic lupus erythematosus. Int. Immunol. 11: 1685-1691.
15. Xiu, Y., K. Nakamura, M. Abe, N. Li, X. S. Wen, Y. Jiang, D. Zhang, H. Tsurui, S. Matsuoka, Y. Hamano, et al. 2002. Transcriptional regulation of Fcgr2b gene by polymorphic promoter region and its contribution to humoral immune responses. J. Immunol. 169: 4340-4346.
16. Yuasa, T., S. Kubo, T. Yoshino, A. Ujike, K. Matsumura, M. Ono, J. V. Ravetch, and T. Takai. 1999. Deletion of fcγ receptor IIB renders H-2 (b) mice susceptible to collagen-induced arthritis. J. Exp. Med. 189: 187-194.
17. Nakamura, A., T. Yuasa, A. Ujike, M. Ono, T. Nukiwa, J. V. Ravetch, and T. Takai. 2000. Fcγ 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.
18. Bolland, S., and J. V. Ravetch. 2000. Spontaneous autoimmune disease in FcγRIIB-deficient mice results from strain-specific epistasis. Immunity 13: 277-285.
19. ~/~ mice. J. Exp. Med. 195: 1167-1174.
20. Wakeland, E., L. Morel, K. Achey, M. Yui, and J. Longmate. 1997. Speed congenics: a classic technique in the fast lane (relatively speaking). Immunol. Today 18: 472-477.
21. McGaha, T. L., B. Sorrentino, and J. V. Ravetch. 2005. Restoration of tolerance in lupus by targeted inhibitory receptor expression. Science 307: 590-593.
22. Xie, C, Z. Liang, S. Chang, and C. Mohan. 2003. Use of a novel elution regimen reveals the dominance of polyreactive antinuclear autoantibodies in lupus kidneys. Arthritis Rheum. 48: 2343-2352.
23. McBrearty, B. A., L. D. Clark, X. M. Zhang, E. P. Blankenhorn, and E. Heber-Katz. 1998. Genetic analysis of a mammalian wound-healing trait. Proc. Natl. Acad. Sci. USA 95: 11792-11797.
24. Leferovich, J. M., K. Bedelbaeva, S. Samulewicz, X. M. Zhang, D. Zwas, E. B. Lankford, and E. Heber-Katz. 2001. Heart regeneration in adult MRL mice. Proc. Natl. Acad. Sci. USA 98: 9830-9835.
25. Heber-Katz, E., J. Leferovich, K. Bedelbaeva, D. Gourevitch, and L. Clark. 2006. Conjecture: can continuous regeneration lead to immortality? Studies in the MRL mouse. Rejuvenation Res. 9: 3-9.
26. Dhodapkar, K. M., D. Banerjee, J. Connolly, A. Kukreja, E. Matayeva, M. C. Veri, J. V. Ravetch, R. M. Steinman, and M. V. Dhodapkar. 2007. Selective blockade of the inhibitory Fcγ receptor (FcγRIIB) in human dendritic cells and monocytes induces a type I interferon response program. J. Exp. Med. 204: 1359-1369.
27. Dhodapkar, K. M., J. L. Kaufman, M. Ehlers, D. K. Banerjee, E. Bonvini, S. Koenig, R. M. Steinman, J. V. Ravetch, and M. V. Dhodapkar. 2005. Selective blockade of inhibitory Fcγ receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc. Natl. Acad. Sci. USA 102: 2910-2915.
28. Mevorach, D., J. L. Zhou, X. Song, and K. B. Elkon. 1998. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 188: 387-392.
29. Wermeling, F., Y. Chen, T. Pikkarainen, A. Scheynius, O. Winqvist, S. Izui, J. V. Ravetch, K. Tryggvason, and M. C. Karlsson. 2007. Class A scavenger receptors regulate tolerance against apoptotic cells, and autoantibodies against these receptors are predictive of systemic lupus. J. Exp. Med. 204: 2259-2265.
30. Wykes, M., A. Pombo, C. Jenkins, and G. G. MacPherson. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161: 1313-1319.
31. Dubois, B., C. Barthelemy, I. Durand, Y. J. Liu, C. Caux, and F. Briere. 1999. Toward a role of dendritic cells in the germinal center reaction: triggering of B cell proliferation and isotype switching. J. Immunol. 162: 3428-3436.
32. Johansson, B., S. Ingvarsson, P. Bjorck, and C. A. Borrebaeck. 2000. Human interdigitating dendritic cells induce isotype switching and IL-13-dependent IgM production in CD40-activated naive B cells. J. Immunol. 164: 1847-1854.
33. Santiago-Raber, M. L., C. Laporte, L. Reininger, and S. Izui. 2004. Genetic basis of murine lupus. Autoimmun. Rev. 3: 33-39.
34. + anti-DNA plasma cells. Nat. Immunol. 6: 99-106.
35. Ehlers, M., H. Fukuyama, T. L. McGaha, A. Aderem, and J. V. Ravetch. 2006. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J. Exp. Med. 203: 553-561.
36. Bharadwaj, D., C. Mold, E. Markham, and T. W. Du Clos. 2001. Serum amyloid P component binds to Fcγreceptors and opsonizes particles for phagocytosis. J. Immunol. 166: 6735-6741.
37. Bijl, M., G. Horst, J. Bijzet, H. Bootsma, P. C. Limburg, and C. G. Kallenberg. 2003. Serum amyloid P component binds to late apoptotic cells and mediates their uptake by monocyte-derived macrophages. Arthritis Rheum. 48: 248-254.
38. Bickerstaff, M. C., M. Botto, W. L. Hutchinson, J. Herbert, G. A. Tennent, A. Bybee, D. A. Mitchell, H. T. Cook, P. J. Butler, M. J. Walport, and M. B. Pepys. 1999. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 5: 694-697.
39. Bygrave, A. E., K. L. Rose, J. Cortes-Hernandez, J. Warren, R. J. Rigby, H. T. Cook, M. J. Walport, T. J. Vyse, and M. Botto. 2004. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2: E243.
40. Wandstrat, A. E., C. Nguyen, N. Limaye, A. Y. Chan, S. Subramanian, X. H. Tian, Y. S. Yim, A. Pertsemlidis, H. R. Garner, Jr., L. Morel, and E. K. Wakeland. 2004. Association of extensive polymorphisms in the SLAM /CD2 gene cluster with murine lupus. Immunity 21: 769-780.
41. Waters, S. T., M. McDuffie, H. Bagavant, U. S. Deshmukh, F. Gaskin, C. Jiang, K. S. Tung, and S. M. Fu. 2004. Breaking tolerance to double stranded DNA, nucleosome, and other nuclear antigens is not required for the pathogenesis of lupus glomerulonephritis. J. Exp. Med. 199: 255-264.
42. Takai, T., M. Ono, M. Hikida, H. Ohmori, and J. V. Ravetch. 1996. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 379: 346-349.
43. Dai, J., B. Liu, D. J. Cua, and Z. Li. 2007. Essential roles of IL-12 and dendritic cells but not IL-23 and macrophages in lupus-like diseases initiated by cell surface HSP gp96. Eur. J. Immunol. 37: 706-715.
44. Frisoni, L., L. McPhie, L. Colonna, U. Sriram, M. Monestier, S. Gallucci, and R. Caricchio. 2005. Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity? J. Immunol. 175: 2692-2701.
45. Sarmiento, L. F., L. E. Munoz, P. Chirinos, N. E. Bianco, and M. E. Zabaleta-Lanz. 2007. Opsonization by anti-dsDNA antibodies of apoptotic cells in systemic lupus erythematosus. Autoimmunity 40: 337-339.