Potentially autoreactive naturally occurring transitional T3 B lymphocytes exhibit a unique signaling profile

Journal of Autoimmunity

Volumn 38, Issue 4, 2012, Pages 293-303

  Liubchenko, Ganna A ^a   Appleberry, Holly C ^a   Holers, V Michael ^a   Banda, Nirmal K ^a   Willis, Van C ^a   Lyubchenko, Taras ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

B cells; BCR signal transduction; Ca 2+ signaling; Clonal anergy; Protein phosphorylation; Tolerance

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN COMPLEX 2 MU 1 SUBUNIT; AUTOANTIGEN; B LYMPHOCYTE RECEPTOR; CALCIUM ION; CD19 ANTIGEN; COLLAGEN TYPE 2; DOK PROTEIN; EZRIN; FOCAL ADHESION KINASE 2; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE LCK; PROTEIN KINASE SYK; PROTEIN MSK1; PROTEIN P56; PROTEIN P85; PROTEIN SHC; PROTEIN SHIP1; PROTEIN TYROSINE PHOSPHATASE SHP 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTHRITIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL TYPE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CLONAL ANERGY; CONTROLLED STUDY; FLOW CYTOMETRY; GROWTH INHIBITION; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOREACTIVITY; IMMUNOSTIMULATION; MOLECULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T3 B LYMPHOCYTE; WILD TYPE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOIMMUNITY; B-LYMPHOCYTES; CALCIUM; CLONAL ANERGY; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; PHENOTYPE; PHOSPHORYLATION; RECEPTORS, ANTIGEN, B-CELL; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 84861190584     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2011.12.005     Document Type: Article

References (43)

1. Altan-Bonnet G., Germain R.N. Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoS Biol 2005, 3:e356.
2. McKeithan T.W. Kinetic proofreading in T-cell receptor signal transduction. Proc Natl Acad Sci U S A 1995, 92:5042-5046.
3. Jankovic M., Casellas R., Yannoutsos N., Wardemann H., Nussenzweig M.C. RAGs and regulation of autoantibodies. Annu Rev Immunol 2004, 22:485-501.
4. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
5. Nemazee D., Hogquist K.A. Antigen receptor selection by editing or downregulation of V(D)J recombination. Current opinion in immunology 2003, 15:182-189.
6. Casellas R., Shih T.A., Kleinewietfeld M., Rakonjac J., Nemazee D., Rajewsky K., et al. Contribution of receptor editing to the antibody repertoire. Science 2001, 291:1541-1544.
7. Healy J.I., Goodnow C.C. Positive versus negative signaling by lymphocyte antigen receptors. Annu Rev Immunol 1998, 16:645-670.
8. Merrell K.T., Benschop R.J., Gauld S.B., Aviszus K., Decote-Ricardo D., Wysocki L.J., et al. Identification of anergic B cells within a wild-type repertoire. Immunity 2006, 25:953-962.
9. Kalled S.L. The role of BAFF in immune function and implications for autoimmunity. Immunol Rev 2005, 204:43-54.
10. Lesley R., Xu Y., Kalled S.L., Hess D.M., Schwab S.R., Shu H.B., et al. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 2004, 20:441-453.
11. Mackay F., Schneider P., Rennert P., Browning J. BAFF AND APRIL: a tutorial on B cell survival. Annu Rev Immunol 2003, 21:231-264.
12. Meffre E., Wardemann H. B-cell tolerance checkpoints in health and autoimmunity. Curr Opin Immunol 2008, 20:632-638.
13. Duty J.A., Szodoray P., Zheng N.Y., Koelsch K.A., Zhang Q., Swiatkowski M., et al. Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors. J Exp Med 2009, 206:139-151.
14. Allman D., Lindsley R.C., DeMuth W., Rudd K., Shinton S.A., Hardy R.R. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J Immunol 2001, 167:6834-6840.
15. Cooke M.P., Heath A.W., Shokat K.M., Zeng Y., Finkelman F.D., Linsley P.S., et al. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J Exp Med 1994, 179:425-438.
16. Weintraub B.C., Jun J.E., Bishop A.C., Shokat K.M., Thomas M.L., Goodnow C.C. Entry of B cell receptor into signaling domains is inhibited in tolerant B cells. J Exp Med 2000, 191:1443-1448.
17. Vilen B.J., Burke K.M., Sleater M., Cambier J.C. Transmodulation of BCR signaling by transduction-incompetent antigen receptors: implications for impaired signaling in anergic B cells. J Immunol 2002, 168:4344-4351.
18. Lyubchenko T., Dal Porto J.M., Holers V.M., Cambier J.C. Cutting edge: complement (C3d)-linked antigens break B cell anergy. J Immunol 2007, 179:2695-2699.
19. Weintraub J.P., Godfrey V., Wolthusen P.A., Cheek R.L., Eisenberg R.A., Cohen P.L. Immunological and pathological consequences of mutations in both Fas and Fas ligand. Cell Immunol 1998, 186:8-17.
20. Rathmell J.C., Fournier S., Weintraub B.C., Allison J.P., Goodnow C.C. Repression of B7.2 on self-reactive B cells is essential to prevent proliferation and allow Fas-mediated deletion by CD4(+) T cells. J Exp Med 1998, 188:651-659.
21. Feuerstein N., Chen F., Madaio M., Maldonado M., Eisenberg R.A. Induction of autoimmunity in a transgenic model of B cell receptor peripheral tolerance: changes in coreceptors and B cell receptor-induced tyrosine-phosphoproteins. J Immunol 1999, 163:5287-5297.
22. Cyster J.G., Hartley S.B., Goodnow C.C. Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 1994, 371:389-395.
23. Kilmon M.A., Rutan J.A., Clarke S.H., Vilen B.J. Low-affinity, Smith antigen-specific B cells are tolerized by dendritic cells and macrophages. J Immunol 2005, 175:37-41.
24. Gilbert M.R., Carnathan D.G., Cogswell P.C., Lin L., Baldwin A.S., Vilen B.J. Dendritic cells from lupus-prone mice are defective in repressing immunoglobulin secretion. J Immunol 2007, 178:4803-4810.
25. Acevedo-Suarez C.A., Kilkenny D.M., Reich M.B., Thomas J.W. Impaired intracellular calcium mobilization and NFATc1 availability in tolerant anti-insulin B cells. J Immunol 2006, 177:2234-2241.
26. Eris J.M., Basten A., Brink R., Doherty K., Kehry M.R., Hodgkin P.D. Anergic self-reactive B cells present self antigen and respond normally to CD40-dependent T-cell signals but are defective in antigen-receptor-mediated functions. Proc Natl Acad Sci U S A 1994, 91:4392-4396.
27. Noorchashm H., Bui A., Li H.L., Eaton A., Mandik-Nayak L., Sokol C., et al. Characterization of anergic anti-DNA B cells: B cell anergy is a T cell-independent and potentially reversible process. Int Immunol 1999, 11:765-776.
28. Vilen B.J., Famiglietti S.J., Carbone A.M., Kay B.K., Cambier J.C. B cell antigen receptor desensitization: disruption of receptor coupling to tyrosine kinase activation. J Immunol 1997, 159:231-243.
29. Gauld S.B., Benschop R.J., Merrell K.T., Cambier J.C. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat Immunol 2005, 6:1160-1167.
30. Moore A.R. Collagen-induced arthritis. Methods Mol Biol 2003, 225:175-179.
31. Reid P.A., Watts C. Constitutive endocytosis and recycling of major histocompatibility complex class II glycoproteins in human B-lymphoblastoid cells. Immunology 1992, 77:539-542.
32. Lu X., Axtell R.C., Collawn J.F., Gibson A., Justement L.B., Raman C. AP2 adaptor complex-dependent internalization of CD5: differential regulation in T and B cells. J Immunol 2002, 168:5612-5620.
33. John B., Herrin B.R., Raman C., Wang Y.N., Bobbitt K.R., Brody B.A., et al. The B cell coreceptor CD22 associates with AP50, a clathrin-coated pit adapter protein, via tyrosine-dependent interaction. J Immunol 2003, 170:3534-3543.
34. Dal Porto J.M., Burke K., Cambier J.C. Regulation of BCR signal transduction in B-1 cells requires the expression of the Src family kinase Lck. Immunity 2004, 21:443-453.
35. Frances R., Tumang J.R., Rothstein T.L. B-1 cells are deficient in Lck: defective B cell receptor signal transduction in B-1 cells occurs in the absence of elevated Lck expression. J Immunol 2005, 175:27-31.
36. Waddick K.G., Chae H.P., Tuel-Ahlgren L., Jarvis L.J., Dibirdik I., Myers D.E., et al. Engagement of the CD19 receptor on human B-lineage leukemia cells activates LCK tyrosine kinase and facilitates radiation-induced apoptosis. Radiat Res 1993, 136:313-319.
37. Jacks K.A., Koch C.A. Differential regulation of mitogen- and stress-activated protein kinase-1 and -2 (MSK1 and MSK2) by CK2 following UV radiation. J Biol Chem 2010, 285:1661-1670.
38. Darragh J., Ananieva O., Courtney A., Elcombe S., Arthur J.S. MSK1 regulates the transcription of IL-1ra in response to TLR activation in macrophages. Biochem J 2010, 425:595-602.
39. Reber L., Vermeulen L., Haegeman G., Frossard N. Ser276 phosphorylation of NF-kB p65 by MSK1 controls SCF expression in inflammation. PLoS One 2009, 4:e4393.
40. Ananieva O., Darragh J., Johansen C., Carr J.M., McIlrath J., Park J.M., et al. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat Immunol 2008, 9:1028-1036.
41. El Mchichi B., Hadji A., Vazquez A., Leca G. p38 MAPK and MSK1 mediate caspase-8 activation in manganese-induced mitochondria-dependent cell death. Cell Death Differ 2007, 14:1826-1836.
42. Cambier J.C., Gauld S.B., Merrell K.T., Vilen B.J. B-cell anergy: from transgenic models to naturally occurring anergic B cells?. Nat Rev Immunol 2007, 7:633-643.
43. Lyubchenko T., dal Porto J., Cambier J.C., Holers V.M. Coligation of the B cell receptor with complement receptor type 2 (CR2/CD21) using its natural ligand C3dg: activation without engagement of an inhibitory signaling pathway. J Immunol 2005, 174:3264-3272.