Anergic responses characterize a large fraction of human autoreactive naive B cells expressing low levels of surface IgM

Journal of Immunology

Volumn 186, Issue 8, 2011, Pages 4640-4648

  Quách, Tâm D ^a   Manjarrez Orduño, Nataly ^a   Adlowitz, Diana G ^a   Silver, Lin ^a   Yang, Hongmei ^b   Wei, Chungwen ^a   Milner, Eric C B ^a   Sanz, Iñaki ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD22 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; FAS ANTIGEN; IMMUNOGLOBULIN D ANTIBODY; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY;

ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CALCIUM TRANSPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CLONAL ANERGY; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANTIBODIES, ANTI-IDIOTYPIC; ANTIGENS, CD19; ANTIGENS, CD22; ANTIGENS, CD95; AUTOANTIGENS; B-LYMPHOCYTES; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; CLONAL ANERGY; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; ION TRANSPORT; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTORS, COMPLEMENT 3D; SELF TOLERANCE;

EID: 79955009724     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001946     Document Type: Article

References (50)

1. Goodnow, C. C., S. Adelstein, and A. Basten. 1990. The need for central and peripheral tolerance in the B cell repertoire. Science 248:1373-1379.
2. Carsetti, R., G. Köhler, and M. C. Lamers. 1995. Transitional B cells are the target of negative selection in the B cell compartment. J. Exp. Med. 181:2129-2140.
3. Hartley, S. B., J. Crosbie, R. Brink, A. B. Kantor, A. Basten, and C. C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353:765-769. (Pubitemid 21912617)
4. Roark, J. H., A. Bui, K. A. Nguyen, L. Mandik, and J. Erikson. 1997. Persistence of functionally compromised anti-double-stranded DNA B cells in the periphery of non-autoimmune mice. Int. Immunol. 9:1615-1626. (Pubitemid 27494125)
5. Liu, X., S. Shen, and T. Manser. 2009. Influence of B cell antigen receptor expression level on pathways of B cell tolerance induction. J. Immunol. 182:398-407.
6. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25:953-962. (Pubitemid 44894955)
7. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301:1374-1377. (Pubitemid 37075812)
8. Pugh-Bernard, A. E., G. J. Silverman, A. J. Cappione, M. E. Villano, D. H. Ryan, R. A. Insel, and I. Sanz. 2001. Regulation of inherently autoreactive VH4-34 B cells in the maintenance of human B cell tolerance. J. Clin. Invest. 108:1061-1070. (Pubitemid 32946080)
9. 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.
10. Abdul-Majid, K. B., and M. Abedi-Valurgerdi. 1998. T cell dependent B cell activation occurs during the induction of T cell anergy by staphylococcal enterotoxin B in mice. Immunol. Invest. 27:73-88. (Pubitemid 28193285)
11. Gett, A. V., and P. D. Hodgkin. 2000. A cellular calculus for signal integration by T cells. Nat. Immunol. 1:239-244.
12. Sanchez-Guajardo, V., J. A. M. Borghans, M. E. Marquez, S. Garcia, and A. A. Freitas. 2005. Different competitive capacities of Stat4-and Stat6-deficient CD4+ T cells during lymphophenia-driven proliferation. J. Immunol. 174:1178-1187.
13. Piriou, E., R. Kimmel, K. Chelimo, J. M. Middeldorp, P. S. Odada, R. Ploutz-Snyder, A. M. Moormann, and R. Rochford. 2009. Serological evidence for long-term Epstein-Barr virus reactivation in children living in a holoendemic malaria region of Kenya. J. Med. Virol. 81:1088-1093.
14. Tiller, T., E. Meffre, S. Yurasov, M. Tsuiji, M. C. Nussenzweig, and H. Wardemann. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329:112-124. (Pubitemid 350235462)
15. Palanichamy, A., J. Barnard, B. Zheng, T. Owen, T. Quach, C. Wei, R. J. Looney, I. Sanz, and J. H. Anolik. 2009. Novel human transitional B cell populations revealed by B cell depletion therapy. J. Immunol. 182:5982-5993.
16. Wirths, S., and A. Lanzavecchia. 2005. ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur. J. Immunol. 35:3433-3441. (Pubitemid 43025524)
17. Acevedo-Suárez, C. A., C. Hulbert, E. J. Woodward, and J. W. Thomas. 2005. Uncoupling of anergy from developmental arrest in anti-insulin B cells supports the development of autoimmune diabetes. J. Immunol. 174:827-833. (Pubitemid 40094278)
18. Healy, J. I., and C. C. Goodnow. 1998. Positive versus negative signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 16:645-670. (Pubitemid 28183380)
19. Goodnow, C. C. 1996. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl. Acad. Sci. USA 93:2264-2271. (Pubitemid 26104339)
20. Goodnow, C. C. 1997. Balancing immunity, autoimmunity, and self-tolerance. Ann. N. Y. Acad. Sci. 815:55-66. (Pubitemid 27309488)
21. Dal Porto, J. M., S. B. Gauld, K. T. Merrell, D. Mills, A. E. Pugh-Bernard, and J. Cambier. 2004. B cell antigen receptor signaling 101. Mol. Immunol. 41:599-613. (Pubitemid 38824617)
22. Gross, A. J., J. R. Lyandres, A. K. Panigrahi, E. T. L. 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.
23. Mackay, F., and J. L. Browning. 2002. BAFF: a fundamental survival factor for B cells. Nat. Rev. Immunol. 2:465-475. (Pubitemid 37328738)
24. Rui, L., C. G. Vinuesa, J. Blasioli, and C. C. Goodnow. 2003. Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 4:594-600. (Pubitemid 36701344)
25. Huggins, J., T. Pellegrin, R. E. Felgar, C. Wei, M. Brown, B. Zheng, E. C. B. Milner, S. H. Bernstein, I. Sanz, and M. S. Zand. 2007. CpG DNA activation and plasmacell differentiation of CD27-naive human B cells. Blood 109:1611-1619. (Pubitemid 46239595)
26. Capolunghi, F., S. Cascioli, E. Giorda, M. M. Rosado, A. Plebani, C. Auriti, G. Seganti, R. Zuntini, S. Ferrari, M. Cagliuso, et al. 2008. CpG drives human transitional B cells to terminal differentiation and production of natural antibodies. J. Immunol. 180:800-808.
27. Good, K. L., V. L. Bryant, and S. G. Tangye. 2006. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J. Immunol. 177:5236-5247. (Pubitemid 44527596)
28. Tangye, S. G., D. T. Avery, and P. D. Hodgkin. 2003. A division-linked mechanism for the rapid generation of Ig-secreting cells from human memory B cells. J. Immunol. 170:261-269. (Pubitemid 36026148)
29. Bachmann, M. F., U. H. Rohrer, T. M. Kündig, K. Bürki, H. Hengartner, and R. M. Zinkernagel. 1993. The influence of antigen organization on B cell responsiveness. Science 262:1448-1451. (Pubitemid 24035067)
30. Diz, R., S. K. McCray, and S. H. Clarke. 2008. B cell receptor affinity and B cell subset identity integrate to define the effectiveness, affinity threshold, and mechanism of anergy. J. Immunol. 181:3834-3840.
31. Bell, S. E., and C. C. Goodnow. 1994. A selective defect in IgM antigen receptor synthesis and transport causes loss of cell surface IgM expression on tolerant B lymphocytes. EMBO J. 13:816-826. (Pubitemid 24057512)
32. Duong, B. H., H. Tian, T. Ota, G. Completo, S. Han, J. L. Vela, M. Ota, M. Kubitz, N. Bovin, J. C. Paulson, and D. Nemazee. 2010. Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo. [Published erratum appears in 2010 J. Exp. Med. 207:445.]
33. J. Exp. Med. 207:173-187.
34. Jellusova, J., U. Wellmann, K. Amann, T. H. Winkler, and L. Nitschke. 2010. CD22 x Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J. Immunol. 184:3618-3627.
35. Nitschke, L. 2005. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr. Opin. Immunol. 17:290-297. (Pubitemid 40692664)
36. Fulcher, D. A., and A. Basten. 1994. Reduced life span of anergic self-reactive B cells in a double-transgenic model. J. Exp. Med. 179:125-134. (Pubitemid 24012977)
37. Lesley, R., Y. Xu, S. L. Kalled, D. M. Hess, S. R. Schwab, H.-B. Shu, and J. G. Cyster. 2004. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20:441-453. (Pubitemid 38482122)
38. Fields, M. L., M. H. Metzgar, B. D. Hondowicz, S.-A. Kang, S. T. Alexander, K. D. Hazard, A. C. Hsu, Y.-Z. Du, E. L. Prak, M. Monestier, and J. Erikson. 2006. Exogenous and endogenous TLR ligands activate anti-chromatin and polyreactive B cells. J. Immunol. 176:6491-6502. (Pubitemid 43787831)
39. Adams, E., A. Basten, and C. C. Goodnow. 1990. Intrinsic B-cell hyporesponsiveness accounts for self-tolerance in lysozyme/anti-lysozyme doubletransgenic mice. Proc. Natl. Acad. Sci. USA 87:5687-5691.
40. Goodnow, C. C., R. Brink, and E. Adams. 1991. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352:532-536. (Pubitemid 21912378)
41. Yokochi, T., R. D. Holly, and E. A. Clark. 1982. B lymphoblast antigen (BB-1) expressed on Epstein-Barr virus-activated B cell blasts, B lymphoblastoid cell lines, and Burkitt's lymphomas. J. Immunol. 128:823-827. (Pubitemid 12168448)
42. Lenschow, D. J., T. L. Walunas, and J. A. Bluestone. 1996. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14:233-258. (Pubitemid 26130184)
43. Evans, D. E., M. W. Munks, J. M. Purkerson, and D. C. Parker. 2000. Resting B lymphocytes as APC for naive T lymphocytes: dependence on CD40 ligand/CD40. J. Immunol. 164:688-697. (Pubitemid 30043689)
44. Serreze, D. V., S. A. Fleming, H. D. Chapman, S. D. Richard, E. H. Leiter, and R. M. Tisch. 1998. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 161:3912-3918. (Pubitemid 28468965)
45. Cambier, J. C., S. B. Gauld, K. T. Merrell, and B. J. Vilen. 2007. B-cell anergy: from transgenic models to naturally occurring anergic B cells? Nat. Rev. Immunol. 7:633-643. (Pubitemid 47123549)
46. Gauld, S. B., R. J. Benschop, K. T. Merrell, and J. C. Cambier. 2005. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 6:1160-1167. (Pubitemid 41541794)
47. Cappione, A., III, J. H. Anolik, A. Pugh-Bernard, J. Barnard, P. Dutcher, G. Silverman, and I. Sanz. 2005. Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J. Clin. Invest. 115:3205-3216. (Pubitemid 41567585)
48. Cappione, A. J., A. E. Pugh-Bernard, J. H. Anolik, and I. Sanz. 2004. Lupus IgG VH4.34 antibodies bind to a 220-kDa glycoform of CD45/B220 on the surface of human B lymphocytes. J. Immunol. 172:4298-4307. (Pubitemid 38375244)
49. 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/CD21-negative human naive B cells mostly contain autoreactive unresponsive clones. Blood 115:5026-5036.
50. Avery, D. T., E. K. Deenick, C. S. Ma, S. Suryani, N. Simpson, G. Y. Chew, T. D. Chan, U. Palendira, J. Bustamante, S. Boisson-Dupuis, et al. 2010. B cellintrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J. Exp. Med. 207:155-171.