Suppression of Phosphatidylinositol 3,4,5-Trisphosphate Production Is a Key Determinant of B Cell Anergy

Immunity

Volumn 31, Issue 5, 2009, Pages 749-760

  Browne, Cecille D ^a   Del Nagro, Christopher J ^a   Cato, Matthew H ^a   Dengler, Hart S ^a   Rickert, Robert C ^a  

^a Infectious and Inflammatory Disease Center   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

AUTOANTIBODY; CD19 ANTIGEN; LIPID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BIOCHEMISTRY; CELL MATURATION; CLONAL ANERGY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE DELETION; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD19; B-LYMPHOCYTES; CLONAL ANERGY; GLYCOSYLPHOSPHATIDYLINOSITOLS; MICE; MICE, KNOCKOUT; PHOSPHATIDYLINOSITOL PHOSPHATES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 70449701417     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.08.026     Document Type: Article

References (53)

1. Aiba Y., Kameyama M., Yamazaki T., Tedder T.F., and Kurosaki T. Regulation of B cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 111 (2007) 1497-1503
2. Anzelon A.N., Wu H., and Rickert R.C. Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nat. Immunol. 4 (2003) 287-294
3. Buhl A.M., Nemazee D., Cambier J.C., Rickert R., and Hertz M. B-cell antigen receptor competence regulates B-lymphocyte selection and survival. Immunol. Rev. 176 (2000) 141-153
4. Cambier J.C., Gauld S.B., Merrell K.T., and Vilen B.J. B-cell anergy: From transgenic models to naturally occurring anergic B cells?. Nat. Rev. Immunol. 7 (2007) 633-643
5. Carter R.H., Doody G.M., Bolen J.B., and Fearon D.T. Membrane IgM-induced tyrosine phosphorylation of CD19 requires a CD19 domain that mediates association with components of the B cell antigen receptor complex. J. Immunol. 158 (1997) 3062-3069
6. Chang T.L., Capraro G., Kleinman R.E., and Abbas A.K. Anergy in immature B lymphocytes. Differential responses to receptor-mediated stimulation and T helper cells. J. Immunol. 147 (1991) 750-756
7. Cook M.C., Basten A., and Fazekas de St Groth B. Outer periarteriolar lymphoid sheath arrest and subsequent differentiation of both naive and tolerant immunoglobulin transgenic B cells is determined by B cell receptor occupancy. J. Exp. Med. 186 (1997) 631-643
8. Cooke M.P., Heath A.W., Shokat K.M., Zeng Y., Finkelman F.D., Linsley P.S., Howard M., and Goodnow C.C. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med. 179 (1994) 425-438
9. Cornall R.J., Cyster J.G., Hibbs M.L., Dunn A.R., Otipoby K.L., Clark E.A., and Goodnow C.C. Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8 (1998) 497-508
10. Cyster J.G., Hartley S.B., and Goodnow C.C. Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 371 (1994) 389-395
11. Cyster J.G., Healy J.I., Kishihara K., Mak T.W., Thomas M.L., and Goodnow C.C. Regulation of B-lymphocyte negative and positive selection by tyrosine phosphatase CD45. Nature 381 (1996) 325-328
12. Del Nagro C.J., Kolla R.V., and Rickert R.C. A critical role for complement C3d and the B cell coreceptor (CD19/CD21) complex in the initiation of inflammatory arthritis. J. Immunol. 175 (2005) 5379-5389
13. Dengler H.S., Baracho G.V., Omori S.A., Bruckner S., Arden K.C., Castrillon D.H., DePinho R.A., and Rickert R.C. Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation. Nat. Immunol. 9 (2008) 1388-1398
14. Depoil D., Fleire S., Treanor B.L., Weber M., Harwood N.E., Marchbank K.L., Tybulewicz V.L., and Batista F.D. CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat. Immunol. 9 (2008) 63-72
15. Di Cristofano A., Kotsi P., Peng Y.F., Cordon-Cardo C., Elkon K.B., and Pandolfi P.P. Impaired Fas response and autoimmunity in Pten+/- mice. Science 285 (1999) 2122-2125
16. Diamant E., Keren Z., and Melamed D. CD19 regulates positive selection and maturation in B lymphopoiesis: Lack of CD19 imposes developmental arrest of immature B cells and consequential stimulation of receptor editing. Blood 105 (2005) 3247-3254
17. Enzler T., Bonizzi G., Silverman G.J., Otero D.C., Widhopf G.F., Anzelon-Mills A., Rickert R.C., and Karin M. Alternative and classical NF-kappa B signaling retain autoreactive B cells in the splenic marginal zone and result in lupus-like disease. Immunity 25 (2006) 403-415
18. Fruman D.A., and Bismuth G. Fine tuning the immune response with PI3K. Immunol. Rev. 228 (2009) 253-272
19. Fulcher D.A., Lyons A.B., Korn S.L., Cook M.C., Koleda C., Parish C., Fazekas de St Groth B., and Basten A. The fate of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of T cell help. J. Exp. Med. 183 (1996) 2313-2328
20. Gauld S.B., Benschop R.J., Merrell K.T., and Cambier J.C. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 6 (2005) 1160-1167
21. Goodnow C.C., Brink R., and Adams E. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352 (1991) 532-536
22. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S.J., Brink R.A., Pritchard-Briscoe H., Wotherspoon J.S., Loblay R.H., Raphael K., et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334 (1988) 676-682
23. Goodnow C.C., Crosbie J., Jorgensen H., Brink R.A., and Basten A. Induction of self-tolerance in mature peripheral B lymphocytes. Nature 342 (1989) 385-391
24. Halverson R., Torres R.M., and Pelanda R. Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat. Immunol. 5 (2004) 645-650
25. Hasegawa M., Fujimoto M., Poe J.C., Steeber D.A., and Tedder T.F. CD19 can regulate B lymphocyte signal transduction independent of complement activation. J. Immunol. 167 (2001) 3190-3200
26. Healy J.I., Dolmetsch R.E., Timmerman L.A., Cyster J.G., Thomas M.L., Crabtree G.R., Lewis R.S., and Goodnow C.C. Different nuclear signals are activated by the B cell receptor during positive versus negative signaling. Immunity 6 (1997) 419-428
27. Healy J.I., and Goodnow C.C. Positive versus negative signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 16 (1998) 645-670
28. Inaoki M., Sato S., Weintraub B.C., Goodnow C.C., and Tedder T.F. CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J. Exp. Med. 186 (1997) 1923-1931
29. Jun J.E., and Goodnow C.C. Scaffolding of antigen receptors for immunogenic versus tolerogenic signaling. Nat. Immunol. 4 (2003) 1057-1064
30. Lesche R., Groszer M., Gao J., Wang Y., Messing A., Sun H., Liu X., and Wu H. Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32 (2002) 148-149
31. Lesley R., Xu Y., Kalled S.L., Hess D.M., Schwab S.R., Shu H.-B., and Cyster J.G. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20 (2004) 441-453
32. Lyubchenko T., Dal Porto J.M., Holers V.M., and Cambier J.C. Cutting edge: Complement (C3d)-linked antigens break B cell anergy. J. Immunol. 179 (2007) 2695-2699
33. Mason D.Y., Jones M., and Goodnow C.C. Development and follicular localization of tolerant B lymphocytes in lysozyme/anti-lysozyme IgM/IgD transgenic mice. Int. Immunol. 4 (1992) 163-175
34. Mecklenbrauker I., Kalled S.L., Leitges M., Mackay F., and Tarakhovsky A. Regulation of B-cell survival by BAFF-dependent PKCdelta-mediated nuclear signalling. Nature 431 (2004) 456-461
35. Mecklenbrauker I., Saijo K., Zheng N.Y., Leitges M., and Tarakhovsky A. Protein kinase Cdelta controls self-antigen-induced B-cell tolerance. Nature 416 (2002) 860-865
36. Oliver A.M., Martin F., Gartland G.L., Carter R.H., and Kearney J.F. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27 (1997) 2366-2374
37. Omori S.A., Cato M.H., Anzelon-Mills A., Puri K.D., Shapiro-Shelef M., Calame K., and Rickert R.C. Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 25 (2006) 545-557
38. Otero D.C., Anzelon A.N., and Rickert R.C. CD19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J. Immunol. 170 (2003) 73-83
39. Patke A., Mecklenbrauker I., Erdjument-Bromage H., Tempst P., and Tarakhovsky A. BAFF controls B cell metabolic fitness through a PKC{beta}- and Akt-dependent mechanism. J. Exp. Med. 203 (2006) 2551-2562
40. Phan T.G., Amesbury M., Gardam S., Crosbie J., Hasbold J., Hodgkin P.D., Basten A., and Brink R. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J. Exp. Med. 197 (2003) 845-860
41. Rickert R.C. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr. Opin. Immunol. 17 (2005) 237-243
42. Rickert R.C., Rajewsky K., and Roes J. Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 376 (1995) 352-355
43. Rickert R.C., Roes J., and Rajewsky K. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 25 (1997) 1317-1318
44. Rui L., Healy J.I., Blasioli J., and Goodnow C.C. ERK signaling is a molecular switch integrating opposing inputs from B cell receptor and T cell cytokines to control TLR4-driven plasma cell differentiation. J. Immunol. 177 (2006) 5337-5346
45. Rui L., Vinuesa C.G., Blasioli J., and Goodnow C.C. Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 4 (2003) 594-600
46. Schmidt K.N., and Cyster J.G. Follicular exclusion and rapid elimination of hen egg lysozyme autoantigen-binding B cells are dependent on competitor B cells, but not on T cells. J. Immunol. 162 (1999) 284-291
47. Suzuki A., Kaisho T., Ohishi M., Tsukio-Yamaguchi M., Tsubata T., Koni P.A., Sasaki T., Mak T.W., and Nakano T. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J. Exp. Med. 197 (2003) 657-667
48. Tamguney T., and Stokoe D. New insights into PTEN. J. Cell Sci. 120 (2007) 4071-4079
49. Thien M., Phan T.G., Gardam S., Amesbury M., Basten A., Mackay F., and Brink R. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20 (2004) 785-798
50. Verkoczy L., Duong B., Skog P., Ait-Azzouzene D., Puri K., Vela J.L., and Nemazee D. Basal B cell receptor-directed phosphatidylinositol 3-kinase signaling turns off RAGs and promotes B cell-positive selection. J. Immunol. 178 (2007) 6332-6341
51. Vilen B.J., Nakamura T., and Cambier J.C. Antigen-stimulated dissociation of BCR mIg from Ig-alpha/Ig-beta: Implications for receptor desensitization. Immunity 10 (1999) 239-248
52. Weintraub B.C., Jun J.E., Bishop A.C., Shokat K.M., Thomas M.L., and Goodnow C.C. Entry of B cell receptor into signaling domains is inhibited in tolerant B cells. J. Exp. Med. 191 (2000) 1443-1448
53. Yellen A.J., Glenn W., Sukhatme V.P., Cao X.M., and Monroe J.G. Signaling through surface IgM in tolerance-susceptible immature murine B lymphocytes. Developmentally regulated differences in transmembrane signaling in splenic B cells from adult and neonatal mice. J. Immunol. 146 (1991) 1446-1454