Altered B cell homeostasis is associated with type I diabetes and carriers of the PTPN22 allelic variant

Journal of Immunology

Volumn 188, Issue 1, 2012, Pages 487-496

  Habib, Tania ^a   Funk, Andrew ^a   Rieck, Mary ^a   Brahmandam, Archana ^b   Dai, Xuezhi ^b   Panigrahi, Anil K ^c   Luning Prak, Eline T ^c   Meyer Bahlburg, Almut ^b,e   Sanda, Srinath ^a   Greenbaum, Carla ^a   Rawlings, David J ^b,d   Buckner, Jane H ^a  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD20 ANTIGEN; CD24 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; IMMUNOGLOBULIN M; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 22; PHOSPHOLIPASE C GAMMA2;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CALCIUM TRANSPORT; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; GENE REARRANGEMENT; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOSITY; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ALLELES; AUTOANTIBODIES; B-LYMPHOCYTE SUBSETS; CLONAL ANERGY; DIABETES MELLITUS, TYPE 1; FEMALE; GENOTYPE; HOMEOSTASIS; HUMANS; IMMUNE TOLERANCE; MALE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 22; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION;

EID: 84855369247     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102176     Document Type: Article

References (52)

1. Concannon, P., S. S. Rich, and G. T. Nepom. 2009. Genetics of type 1A diabetes. N. Engl. J. Med. 360: 1646-1654.
2. Gregersen, P. K., and L. M. Olsson. 2009. Recent advances in the genetics of autoimmune disease. Annu. Rev. Immunol. 27: 363-391.
3. Stanford, S. M., T. M. Mustelin, and N. Bottini. 2010. Lymphoid tyrosine phosphatase and autoimmunity: human genetics rediscovers tyrosine phosphatases. Semin. Immunopathol. 32: 127-136.
4. Vang, T., M. Congia, M. D. Macis, L. Musumeci, V. Orrú, P. Zavattari, K. Nika, L. Tautz, K. Taskén, F. Cucca, et al. 2005. Autoimmune-associated lymphoid tyrosine phosphatase is a gain-of-function variant. Nat. Genet. 37: 1317-1319. (Pubitemid 41722185)
5. Arechiga, A. F., T. Habib, Y. He, X. Zhang, Z.-Y. Zhang, A. Funk, and J. H. Buckner. 2009. Cutting edge: the PTPN22 allelic variant associated with autoimmunity impairs B cell signaling. J. Immunol. 182: 3343-3347.
6. Rieck, M., A. Arechiga, S. Onengut-Gumuscu, C. Greenbaum, P. Concannon, and J. H. Buckner. 2007. Genetic variation in PTPN22 corresponds to altered function of T and B lymphocytes. J. Immunol. 179: 4704-4710.
7. Chung, J. B., M. Silverman, and J. G. Monroe. 2003. Transitional B cells: step by step towards immune competence. Trends Immunol. 24: 343-349.
8. Nemazee, D. 2006. Receptor editing in lymphocyte development and central tolerance. Nat. Rev. Immunol. 6: 728-740. (Pubitemid 44453459)
9. Tussiwand, R., N. Bosco, R. Ceredig, and A. G. Rolink. 2009. Tolerance checkpoints in B-cell development: Johnny B good. Eur. J. Immunol. 39: 2317-2324.
10. von Boehmer, H., and F. Melchers. 2010. Checkpoints in lymphocyte development and autoimmune disease. Nat. Immunol. 11: 14-20.
11. King, L. B., and J. G. Monroe. 2000. Immunobiology of the immature B cell: plasticity in the B-cell antigen receptor-induced response fine tunes negative selection. Immunol. Rev. 176: 86-104.
12. Niiro, H., and E. A. Clark. 2002. Regulation of B-cell fate by antigen-receptor signals. Nat. Rev. Immunol. 2: 945-956. (Pubitemid 37323215)
13. Norvell, A., L. Mandik, and J. G. Monroe. 1995. Engagement of the antigen-receptor on immature murine B lymphocytes results in death by apoptosis. J. Immunol. 154: 4404-4413.
14. Su, T. T., B. Guo, B. Wei, J. Braun, and D. J. Rawlings. 2004. Signaling in transitional type 2 B cells is critical for peripheral B-cell development. Immunol. Rev. 197: 161-178. (Pubitemid 38142175)
15. Dorner, T., A.M. Jacobi, J. Lee, and P. E. Lipsky. 2011. Abnormalities of B cell subsets in patients with systemic lupus erythematosus. J. Immunol. Methods. 363: 187-197.
16. Jacobi, A. M., J. Zhang, M. Mackay, C. Aranow, and B. Diamond. 2009. Phenotypic characterization of autoreactive B cells-checkpoints of B cell tolerance in patients with systemic lupus erythematosus. PLoS ONE 4: e5776.
17. Samuels, J., Y. S. Ng, C. Coupillaud, D. Paget, and E. Meffre. 2005. Impaired early B cell tolerance in patients with rheumatoid arthritis. J. Exp. Med. 201: 1659-1667. (Pubitemid 40721009)
18. Yurasov, S., H. Wardemann, J. Hammersen, M. Tsuiji, E. Meffre, V. Pascual, and M. C. Nussenzweig. 2005. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201: 703-711. (Pubitemid 40395116)
19. Duty, J. A., P. Szodoray, N. Y. Zheng, K. A. Koelsch, Q. Zhang, M. Swiatkowski, M. Mathias, L. Garman, C. Helms, B. Nakken, et al. 2009. Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors. J. Exp. Med. 206: 139-151.
20. Yu, X., J. P. Sun, Y. He, X. Guo, S. Liu, B. Zhou, A. Hudmon, and Z. Y. Zhang. 2007. Structure, inhibitor, and regulatory mechanism of Lyp, a lymphoid-specific tyrosine phosphatase implicated in autoimmune diseases. Proc. Natl. Acad. Sci. USA 104: 19767-19772.
21. Kerns, H. M., B. Y. Ryu, B. V. Stirling, B. D. Sather, A. Astrakhan, S. Humblet-Baron, D. Liggitt, and D. J. Rawlings. 2010. B cell-specific lentiviral gene therapy leads to sustained B-cell functional recovery in a murine model of X-linked agammaglobulinemia. Blood 115: 2146-2155.
22. Dai, X., Y. Chen, L. Di, A. Podd, G. Li, K. D. Bunting, L. Hennighausen, R. Wen, and D. Wang. 2007. Stat5 is essential for early B cell development but not for B cell maturation and function. J. Immunol. 179: 1068-1079.
23. Sims, G. P., R. Ettinger, Y. Shirota, C. H. Yarboro, G. G. Illei, and P. E. Lipsky. 2005. Identification and characterization of circulating human transitional B cells. Blood 105: 4390-4398. (Pubitemid 40720786)
24. Suryani, S., D. A. Fulcher, B. Santner-Nanan, R. Nanan, M. Wong, P. J. Shaw, J. Gibson, A. Williams, and S. G. Tangye. 2010. Differential expression of CD21 identifies developmentally and functionally distinct subsets of human transitional B cells. Blood 115: 519-529.
25. Mackay, F., and P. Schneider. 2009. Cracking the BAFF code. Nat. Rev. Immunol. 9: 491-502.
26. Thien, M., T. G. Phan, S. Gardam, M. Amesbury, A. Basten, F. Mackay, and R. Brink. 2004. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20: 785-798. (Pubitemid 38757447)
27. Berard, M., P. Mondière, M. Casamayor-Pallejà, A. Hennino, C. Bella, and T. Defrance. 1999. Mitochondria connects the antigen receptor to effector caspases during B cell receptor-induced apoptosis in normal human B cells. J. Immunol. 163: 4655-4662. (Pubitemid 29501225)
28. Parry, S. L., J. Hasbold, M. Holman, and G. G. Klaus. 1994. Hypercross-linking surface IgM or IgD receptors on mature B cells induces apoptosis that is reversed by costimulation with IL-4 and anti-CD40. J. Immunol. 152: 2821-2829. (Pubitemid 24097977)
29. Panigrahi, A. K., N. G. Goodman, R. A. Eisenberg, M. R. Rickels, A. Naji, and E. T. Luning Prak. 2008. RS rearrangement frequency as a marker of receptor editing in lupus and type 1 diabetes. J. Exp. Med. 205: 2985-2994.
30. Bouaziz, J. D., K. Yanaba, G. M. Venturi, Y. Wang, R. M. Tisch, J. C. Poe, and T. F. Tedder. 2007. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc. Natl. Acad. Sci. USA 104: 20878-20883.
31. Miao, D., L. Yu, and G. S. Eisenbarth. 2007. Role of autoantibodies in type 1 diabetes. Front. Biosci. 12: 1889-1898. (Pubitemid 46846814)
32. Silveira, P. A., and S. T. Grey. 2006. B cells in the spotlight: innocent bystanders or major players in the pathogenesis of type 1 diabetes. Trends Endocrinol. Metab. 17: 128-135.
33. Skyler, J. S. 2007. Prediction and prevention of type 1 diabetes: progress, problems, and prospects. Clin. Pharmacol. Ther. 81: 768-771. (Pubitemid 46625122)
34. Xiu, Y., C. P. Wong, J. D. Bouaziz, Y. Hamaguchi, Y. Wang, S. M. Pop, R. M. Tisch, and T. F. Tedder. 2008. B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in Fc gamma R effector functions. J. Immunol. 180: 2863-2875.
35. Goodnow, C. C., R. Brink, and E. Adams. 1991. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352: 532-536. (Pubitemid 21912378)
36. Goodnow, C. C. 1996. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl. Acad. Sci. USA 93: 2264-2271. (Pubitemid 26104339)
37. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190: 75-89. (Pubitemid 29330125)
38. Meffre, E., R. Casellas, and M. C. Nussenzweig. 2000. Antibody regulation of B cell development. Nat. Immunol. 1: 379-385.
39. Poe, J. C., M. Hasegawa, and T. F. Tedder. 2001. CD19, CD21, and CD22: multifaceted response regulators of B lymphocyte signal transduction. Int. Rev. Immunol. 20: 739-762. (Pubitemid 34096204)
40. Sato, S., A. S.Miller,M. Inaoki, C. B. Bock, P. J. Jansen,M. L. Tang, and T. F. Tedder. 1996. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5: 551-562. (Pubitemid 27062065)
41. Andrews, S. F., and D. J. Rawlings. 2009. Transitional B cells exhibit a B cell receptor-specific nuclear defect in gene transcription. J. Immunol. 182: 2868-2878.
42. Chang, N. H., T. McKenzie, G. Bonventi, C. Landolt-Marticorena, P. R. Fortin, D. Gladman, M. Urowitz, and J. E. Wither. 2008. Expanded population of activated antigen-engaged cells within the naive B cell compartment of patients with systemic lupus erythematosus. J. Immunol. 180: 1276-1284.
43. Cuss, A. K., D. T. Avery, J. L. Cannons, L. J. Yu, K. E. Nichols, P. J. Shaw, and S. G. Tangye. 2006. Expansion of functionally immature transitional B cells is associated with human-immunodeficient states characterized by impaired humoral immunity. J. Immunol. 176: 1506-1516. (Pubitemid 43134294)
44. Isnardi, I., Y. S. Ng, L. Menard, G. Meyers, D. Saadoun, I. Srdanovic, J. Samuels, J. Berman, J. H. Buckner, C. Cunningham-Rundles, and E. Meffre. 2010. Complement receptor 2/CD212 human naive B cells contain mostly autoreactive unresponsive clones. Blood 115: 5026-5036.
45. Gross, A. J., J. R. Lyandres, A. K. Panigrahi, E. T. Prak, and A. L. DeFranco. 2009. Developmental acquisition of the Lyn-CD22-SHP-1 inhibitory pathway promotes B cell tolerance. J. Immunol. 182: 5382-5392.
46. Foerster, C., N. Voelxen, M. Rakhmanov, B. Keller, S. Gutenberger, S. Goldacker, J. Thiel, S. Feske, H. H. Peter, and K. Warnatz. 2010. B cell receptor-mediated calcium signaling is impaired in B lymphocytes of type Ia patients with common variable immunodeficiency. J. Immunol. 184: 7305-7313.
47. Kochi, Y., K. Myouzen, R. Yamada, A. Suzuki, T. Kurosaki, Y. Nakamura, and K. Yamamoto. 2009. FCRL3, an autoimmune susceptibility gene, has inhibitory potential on B-cell receptor-mediated signaling. J. Immunol. 183: 5502-5510.
48. Kozyrev, S. V., A. K. Abelson, J. Wojcik, A. Zaghlool, M. V. Linga Reddy, E. Sanchez, I. Gunnarsson, E. Svenungsson, G. Sturfelt, A. Jönsen, et al. 2008. Functional variants in the B-cell gene BANK1 are associated with systemic lupus erythematosus. [Published erratum appears in 2008 Nat. Genet. 40: 484.] Nat. Genet. 40: 211-216. (Pubitemid 351171404)
49. Li, X., T. S. Ptacek, E. E. Brown, and J. C. Edberg. 2009. Fcgamma receptors: structure, function and role as genetic risk factors in SLE. Genes Immun. 10: 380-389.
50. Moser, K. L., J. A. Kelly, C. J. Lessard, and J. B. Harley. 2009. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun. 10: 373-379.
51. Halverson, R., R. M. Torres, and R. Pelanda. 2004. Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat. Immunol. 5: 645-650. (Pubitemid 38811890)
52. Menard, L., D. Saadoun, I. Isnardi, Y. S. Ng, G. Meyers, C. Massad, C. Price, C. Abraham, R. Motaghedi, J. H. Buckner, et al. 2011. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J. Clin. Invest. 121: 3635-3644.