Fc{gamma}RIIB signals inhibit BLyS signaling and BCR-mediated BLyS receptor up-regulation

Blood

Volumn 113, Issue 7, 2009, Pages 1464-1473

  Crowley, Jenni E ^a   Stadanlick, Jason E ^a   Cambier, John C ^b   Cancro, Michael P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; BREAKPOINT CLUSTER REGION PROTEIN; FC RECEPTOR IIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL XL; PROTEIN KINASE; PROTEIN KINASE PIM 2; PROTEIN SH2; PROTEIN TYROSINE PHOSPHATASE SHP 1; UNCLASSIFIED DRUG; BCL2L1 PROTEIN, MOUSE; BCR PROTEIN, MOUSE; FC RECEPTOR; FCGR2B PROTEIN, MOUSE; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL-1,4,5-TRISPHOSPHATE 5-PHOSPHATASE; LIGAND; PHOSPHATASE; PROTEIN BCL X;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CYTOLOGY; FEMALE; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; BCL-X PROTEIN; CELL SURVIVAL; CELLS, CULTURED; FEMALE; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; LIGANDS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORIC MONOESTER HYDROLASES; PROTO-ONCOGENE PROTEINS C-BCR; RECEPTORS, IGG; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 61849128782     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-02-138651     Document Type: Article

References (60)

1. Monroe JG. B-cell positive selection and peripheral homeostasis. Immunol Rev. 2004;197:5-9.
2. Vos Q, Lees A, Wu ZQ, Snapper CM, Mond JJ. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol Rev. 2000;176:154-170.
3. Marshall LS, Aruffo A, Ledbetter JA, Noelle RJ. The molecular basis for T cell help in humoral immunity: CD40 and its ligand, gp39. J Clin Immunol. 1993;13:165-174.
4. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. 2001;19:275-290.
5. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV.A13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature. 1994;369:340.
6. Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity. 2000;13:277-285.
7. Scharenberg AM, El-Hillal O, Fruman DA, et al. Phosphatidylinositol-3,4, 5-trisphosphate (PtdIns-3,4,5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J. 1998;17:1961-1972.
8. Liu Q, Sasaki T, Kozieradzki I, et al. SHIP is a negative regulator of growth factor receptor-mediated PKB/Akt activation and myeloid cell survival. Genes Dev. 1999;13:786-791.
9. Tamir I, Stolpa JC, Helgason CD, et al. The Ras-GAP-binding protein p62dok is a mediator of inhibitory FcgammaRIIB signals in B cells. Immunity. 2000;12:347-358.
10. Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc-(gamma)RIIB. Nature. 1996;383:263-266.
11. Bolland S, Pearse RN, Kurosaki T, Ravetch JV. SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity. 1998;8:509-516.
12. D'Ambrosio D, Hippen KL, Minskoff SA, et al. Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling by Fc gamma RIIB1. Science. 1995;268:293-297.
13. D'Ambrosio D, Fong DC, Cambier JC. The SHIP phosphatase becomes associated with Fc gam-maRIIB1 and is tyrosine phosphorylated during "negative" signaling. Immunol Lett. 1996;54:77-82.
14. Wang J, Taniuchi I, Maekawa Y, Howard M, Cooper MD, Watanabe T. Expression and function of Fas antigen on activated murine B cells. Eur J Immunol. 1996;26:92-96.
15. Moore PA, Belvedere O, Orr A, et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science. 1999;285:260-263.
16. Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med. 1999;189: 1747-1756.
17. Mackay F, Browning JL. BAFF: a fundamental survival factor for B cells. Nat Rev Immunol. 2002;2:465-475.
18. Laabi Y, Gras MP, Brouet JC, Berger R, Larsen CJ, Tsapis A. The BCMA gene, preferentially expressed during B lymphoid maturation, is bidirectionally transcribed. Nucleic Acids Res. 1994;22: 1147-1154.
19. Madry C, Laabi Y, Callebaut I, et al. The characterization of murine BCMA gene defines it as a new member of the tumor necrosis factor receptor superfamily. Int Immunol. 1998;10:1693-1702.
20. Gross JA, Johnston J, Mudri S, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature. 2000;404:995-999.
21. von Bulow GU, Bram RJ. NF-AT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science. 1997;278:138-141.
22. Yan M, Marsters SA, Grewal IS, Wang H, Ashkenazi A, Dixit VM. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat Immunol. 2000;1:37-41.
23. Yan M, Brady JR, Chan B, et al. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr Biol. 2001;11:1547-1552.
24. Schiemann B, Gommerman JL, Vora K, et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science. 2001;293:2111-2114.
25. Batten M, Groom J, Cachero TG, et al. BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med. 2000;192:1453-1466.
26. Hsu BL, Harless SM, Lindsley RC, Hilbert DM, Cancro MP. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J Immunol. 2002;168:5993-5996.
27. Stohl W, Metyas S, Tan SM, et al. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum. 2003;48:3475-3486.
28. Vora KA, Wang LC, Rao SP, et al. Cutting edge: germinal centers formed in the absence of B cell-activating factor belonging to the TNF family exhibit impaired maturation and function. J Immunol. 2003;171:547-551.
29. Rahman ZS, Rao SP, Kalled SL, Manser T. Normal induction but attenuated progression of germinal center responses in BAFF and BAFF-R signaling-deficient mice. J Exp Med. 2003;198:1157-1169.
30. Treml LS, Carlesso G, Hoek KL, et al. TLR stimulation modifies BLyS receptor expression in fol-licular and marginal zone B cells. J Immunol. 2007;178:7531-7539.
31. Groom JR, Fletcher CA, Walters SN, et al. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J Exp Med. 2007;204: 1959-1971.
32. Patke A, Mecklenbrauker I, Erdjument-Bromage H, Tempst P, Tarakhovsky A. BAFF controls B cell metabolic fitness through a PKC beta- and Akt-dependent mechanism. J Exp Med. 2006;203: 2551-2562.
33. Helgason CD, Damen JE, Rosten P, et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 1998;12:1610-1620.
34. Grillot DA, Merino R, Pena JC, et al. bcl-x exhibits regulated expression during B cell development and activation and modulates lymphocyte survival in transgenic mice. J Exp Med. 1996;183: 381-391.
35. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
36. Phillips NE, Parker DC. Cross-linking of B lymphocyte Fc gamma receptors and membrane im-munoglobulin inhibits anti-immunoglobulin-induced blastogenesis. J Immunol. 1984;132:627-632.
37. Smith SH, Cancro MP. Cutting edge: B cell receptor signals regulate BLyS receptor levels in mature B cells and their immediate progenitors. J Immunol. 2003;170:5820-5823.
38. Oliver AM, Martin F, Kearney JF. IgM high CD21 high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol. 1999;162:7198-7207.
39. Li X, Martin F, Oliver AM, Kearney JF, Carter RH. Antigen receptor proximal signaling in splenic B-2 cell subsets. J Immunol. 2001;166:3122-3129.
40. Chan VW, Lowell CA, DeFranco AL. Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes. Curr Biol. 1998;8: 545-553.
41. DeFranco AL, Chan VW, Lowell CA. Positive and negative roles of the tyrosine kinase Lyn in B cell function. Semin Immunol. 1998;10:299-307.
42. Nitschke L. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr Opin Immunol. 2005;17:290-297.
43. Tedder TF, Poe JC, Haas KM. CD22: a multifunctional receptor that regulates B lymphocyte survival and signal transduction. Adv Immunol. 2005; 88:1-50.
44. Walker JA, Smith KG. CD22: an inhibitory enigma. Immunology. 2008;123:314-325.
45. Stoddart A, Ray RJ, Paige CJ. Analysis of murine CD22 during B cell development: CD22 is expressed on B cell progenitors before IgM. Int Immunol. 1997;9:1571-1579.
46. Haas KM, Sen S, Sanford IG, Miller AS, Poe JC, Tedder TF. CD22 ligand binding regulates normal and malignant B lymphocyte survival in vivo. J Immunol. 2006;177:3063-3073.
47. Kim KM, Reth M. Signaling difference between class IgM and IgD antigen receptors. Ann N Y Acad Sci. 1995;766:81-88.
48. Brink R, Goodnow CC, Crosbie J, et al. Immuno-globulin M and D antigen receptors are both capable of mediating B lymphocyte activation, deletion, or anergy after interaction with specific antigen. J Exp Med. 1992;176:991-1005.
49. Woodland RT, Fox CJ, Schmidt MR, et al. Multiple signaling pathways promote B lymphocyte stimulator dependent B-cell growth and survival. Blood. 2008;111:750-760.
50. Lesley R, Xu Y, Kalled SL, et al. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity. 2004;20:441-453.
51. Xu LG, Wu M, Hu J, Zhai Z, Shu HB. Identification of downstream genes up-regulated by the tumor necrosis factor family member TALL-1. J Leukoc Biol. 2002;72:410-416.
52. Woodland RT, Schmidt MR, Thompson CB. BLyS and B cell homeostasis. Semin Immunol. 2006; 18:318-326.
53. Kayagaki N, Yan M, Seshasayee D, et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kappaB2. Immunity. 2002;17:515-524.
54. Harless SM, Lentz VM, Sah AP, et al. Competition for BLyS-mediated signaling through Bcmd/BR3 regulates peripheral B lymphocyte numbers. Curr Biol. 2001;11:1986-1989.
55. Brauweiler AM, Cambier JC. Fc gamma RIIB activation leads to inhibition of signalling by indepen-dently ligated receptors. Biochem Soc Trans. 2003;31:281-285.
56. Brauweiler A, Tamir I, Marschner S, Helgason CD, Cambier JC. Partially distinct molecular mechanisms mediate inhibitory FcgammaRIIB signaling in resting and activated B cells. J Immunol. 2001;167:204-211.
57. Thien M, Phan TG, Gardam S, et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity. 2004;20:785-798.
58. Brauweiler A, Merrell K, Gauld SB, Cambier JC. Cutting edge: acute and chronic exposure of immature B cells to antigen leads to impaired homing and SHIP1-dependent reduction in stromal cell-derived factor-1 responsiveness. J Immunol. 2007;178:3353-3357.
59. Merrell KT, Benschop RJ, Gauld SB, et al. Identification of anergic B cells within a wild-type repertoire. Immunity. 2006;25:953-962.
60. Su K, Yang H, Li X, et al. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol. 2007;178:3272-3280.