Models of signal transduction through the B-cell antigen receptor

Immunology

Volumn 110, Issue 4, 2003, Pages 401-410

  Geisberger, Roland ^a   Crameri, Reto ^b   Achatz, Gernot ^a,c  

^a Dept of Genet and General Biology   (Austria)

^b SWISS INSTITUTE OF ALLERGY AND ASTHMA RESEARCH SIAF   (Switzerland)

^c UNIVERSITY OF SALZBURG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIBODY; B LYMPHOCYTE RECEPTOR; CD79A ANTIGEN; CD79B ANTIGEN; GLYCOPROTEIN; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN D; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN M;

ALLOSTERISM; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; GLYCOSYLATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEQUENCE ANALYSIS; SIGNAL DETECTION; SIGNAL TRANSDUCTION;

ANTIBODY FORMATION; B-LYMPHOCYTES; CELL MEMBRANE; CYTOPLASM; HUMANS; IMMUNOGLOBULIN ISOTYPES; IMMUNOGLOBULINS; MODELS, IMMUNOLOGICAL; PHOSPHORYLATION; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; TYROSINE;

EID: 0346221278     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2003.01770.x     Document Type: Review

References (94)

1. Reth M. Antigen receptors on B lymphocytes. Annu Rev Immunol 1992; 10:97.
2. Cambier JC, Pleiman CM, Clark MR. Signal transduction by the B cell antigen receptor and its coreceptors. Annu Rev Immunol 1994; 12:457.
3. Venkitaraman AR, Williams GT, Dariavach P, Neuberger MS. The B-cell antigen receptor of the five immunoglobulin classes. Nature 1991; 352:777.
4. Sanchez M, Misulovin Z, Burkhardt AL, Mahajan S, Costa T, Franke R, Bolen JB, Nussenzweig M. Signal transduction by immunoglobulin is mediated through Ig alpha and Ig beta. J Exp Med 1993; 178:1049.
5. Grupp SA, Mitchell RN, Schreiber KL, McKean DJ, Abbas AK. Molecular mechanisms that control expression of the B lymphocyte antigen receptor complex. J Exp Med 1995; 181:161.
6. Pogue SL, Goodnow CC. Ig heavy chain extracellular spacer confers unique glycosylation of the Mb-1 component of the B cell antigen receptor complex. J Immunol 1994; 152:3925.
7. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982; 157:105.
8. Zidovetzki R, Rost B, Pecht I. Role of transmembrane domains in the functions of B-and T-cell receptors. Immunol Lett 1998; 64:97.
9. Klein P, Kanehisa M, DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta 1985; 815: 468.
10. Stevens TL, Blum JH, Foy SP, Matsuuchi L, DeFranco AL. A mutation of the mu transmembrane that disrupts endoplasmic reticulum retention. Effects on association with accessory proteins and signal transduction. J Immunol 1994; 152:4397.
11. Li Q, Santini R, Rosenspire AR. Glycosylated extracellular domains of membrane immunoglobulin M contribute to its association with mb-1/B29 gene products and the B cell receptor complex. Immunol Invest 1998; 27:57.
12. Pleiman CM, Chien NC, Cambier JC. Point mutations define a mIgM transmembrane region motif that determines intersubunit signal transduction in the antigen receptor. J Immunol 1994; 152:2837.
13. Williams GT, Peaker CJ, Patel KJ, Neuberger MS. The alpha/beta sheath and its cytoplasmic tyrosines are required for signaling by the B-cell antigen receptor but not for capping or for serine/threonine-kinase recruitment. Proc Natl Acad Sci USA 1994; 91:474.
14. Mitchell RN, Barnes KA, Grupp SA, Sanchez M, Misulovin Z, Nussenzweig MC, Abbas AK. Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J Exp Med 1995; 181:1705.
15. Terashima M, Kim KM, Adachi T, Nielsen PJ, Reth M, Kohler G, Lamers MC. The IgM antigen receptor of B lymphocytes is associated with prohibitin and a prohibitin-related protein. EMBO J 1994; 13:3782.
16. Kim KM, Adachi T, Nielsen PJ, Terashima M, Lamers MC, Kohler G, Reth M. Two new proteins preferentially associated with membrane immunoglobulin D. EMBO J 1994; 13:3793.
17. Cherayil BJ, MacDonald K, Waneck GL, Pillai S. Surface transport and internalization of the membrane IgM H chain in the absence of the Mb-1 and B29 proteins. J Immunol 1993; 151:11.
18. Wu Y, Pun C, Hozumi N. Roles of calnexin and Ig-alpha beta interactions with membrane Igs in the surface expression of the B cell antigen receptor of the IgM and IgD classes. J Immunol 1997; 158:2762.
19. Foy SP, Matsuuchi L. Association of B lymphocyte antigen receptor polypeptides with multiple chaperone proteins. Immunol Lett 2001; 78:149.
20. Hendershot LM. Immunoglobulin heavy chain and binding protein complexes are dissociated in vivo by light chain addition. J Cell Biol 1990; 111:829.
21. Wienands J, Hombach J, Radbruch A, Riesterer C, Reth M. Molecular components of the B cell antigen receptor complex of class IgD differ partly from those of IgM. EMBO J 1990; 9:449.
22. Shaw AC, Mitchell RN, Weaver YK, Campos-Torres J, Abbas AK, Leder P. Mutations of immunoglobulin transmembrane and cytoplasmic domains: effects on intracellular signaling and antigen presentation. Cell 1990; 63:381.
23. Mitchell RN, Shaw AC, Weaver YK, Leder P, Abbas AK. Cytoplasmic tail deletion converts membrane immunoglobulin to a phosphatidylinositol-linked form lacking signaling and efficient antigen internalization functions. J Biol Chem 1991; 266:8856.
24. Achatz G, Nitschke L, Lamers MC. Effect of transmembrane and cytoplasmic domains of IgE on the IgE response. Science 1997; 276:409.
25. Kaisho T, Schwenk F, Rajewsky K. The roles of gamma 1 heavy chain membrane expression and cytoplasmic tail in IgG1 responses. Science 1997; 276:412.
26. Luger E, Lamers M, Achatz-Straussberger G, Geisberger R, Infuhr D, Breitenbach M, Crameri R, Achatz G. Somatic diversity of the immunoglobulin repertoire is controlled in an isotype-specific manner. Eur J Immunol 2001; 31:2319.
27. Weiser P, Riesterer C, Reth M. The internalization of the IgG2a antigen receptor does not require the association with Ig-alpha and Ig-beta but the activation of protein tyrosine kinases does. Eur J Immunol 1994; 24:665.
28. Patel KJ, Neuberger MS. Antigen presentation by the B cell antigen receptor is driven by the alpha/beta sheath and occurs independently of its cytoplasmic tyrosines. Cell 1993; 74:939.
29. Martin F, Kearney JF, Marginal-zone B cells. Nat Rev Immunol 2002; 2:323.
30. Tarlinton D. Antigen presentation by memory B cells: the sting is in the tail. Science 1997; 276:374.
31. Wienands J, Larbolette O, Reth M. Evidence for a preformed transducer complex organized by the B cell antigen receptor. Proc Natl Acad Sci USA 1996; 93:7865.
32. Kurosaki T. Genetic analysis of B cell antigen receptor signaling. Annu Rev Immunol 1999; 17:555.
33. Reth M, Wienands J. Initiation and processing of signals from the B cell antigen receptor. Annu Rev Immunol 1997; 15:453.
34. DeFranco AL. The complexity of signaling pathways activated by the BCR. Curr Opin Immunol 1997; 9:296.
35. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 2002; 3:1129.
36. Germain RN. The art of the probable: system control in the adaptive immune system. Science 2001; 293:240.
37. Schamel WW, Reth M. Monomeric and oligomeric complexes of the B cell antigen receptor. Immunity 2000; 13:5.
38. Hutchcroft JE, Harrison ML, Geahlen RL. Association of the 72-kDa protein-tyrosine kinase PTK72 with the B cell antigen receptor. J Biol Chem 1992; 267:8613.
39. Pierce SK. Lipid rafts and B-cell activation. Nat Rev Immunol 2002; 2:96.
40. Kurosaki T. Regulation of B-cell signal transduction by adaptor proteins. Nat Rev Immunol 2002; 2:354.
41. Thomas ML, Brown EJ. Positive and negative regulation of Src-family membrane kinases by CD45. Immunol Today 1999; 20:406.
42. Penninger JM, Irie-Sasaki J, Sasaki T, Oliveira-dos-Santos AJ. CD45: new jobs for an old acquaintance. Nat Immunol 2001; 2:389.
43. Yanagi S, Sugawara H, Kurosaki M, Sabe H, Yamamura H, Kurosaki T. CD45 modulates phosphorylation of both autophosphorylation and negative regulatory tyrosines of Lyn in B cells. J Biol Chem 1996; 271:30487.
44. Ogimoto M, Katagiri T, Mashima K, Hasegawa K, Mizuno K, Yakura H. Negative regulation of apoptotic death in immature B cells by CD45. Int Immunol 1994; 6:647.
45. Autero M, Saharinen J, Pessa-Morikawa T et al. Tyrosine phosphorylation of CD45 phosphotyrosine phosphatase by p50csk kinase creates a binding site for p561ck tyrosine kinase and activates the phosphatase. Mol Cell Biol 1994; 14:1308.
46. Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K, Tarakhovsky A, Okada M. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 2000; 404:999.
47. Brdicka T, Pavlistova D, Leo A et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med 2000; 191:1591.
48. Healy JI, Goodnow CC. Positive versus negative signaling by lymphocyte antigen receptors. Annu Rev Immunol 1998; 16:645.
49. Kim KM, Reth M. Function of B-cell antigen receptor of different classes. Immunol Lett 1995; 44:81.
50. Ales-Martinez JE, Warner GL, Scott DW. Immunoglobulins D and M mediate signals that are qualitatively different in B cells with an immature phenotype. Proc Natl Acad Sci USA 1988; 85:6919.
51. Carsetti R, Kohler G, Lamers MC. A role for immunoglobulin D. interference with tolerance induction. Eur J Immunol 1993; 23:168.
52. Tisch R, Roifman CM, Hozumi N. Functional differences between immunoglobulins M and D expressed on the surface of an immature B-cell line. Proc Natl Acad Sci USA 1988; 85:6914.
53. Wienands J, Reth M. Glycosyl-phosphatidylinositol linkage as a mechanism for cell-surface expression of immunoglobulin D. Nature 1992; 356:246.
54. Chaturvedi A, Siddiqui Z, Bayiroglu F, Rao KV. A GPI-linked isoform of the IgD receptor regulates resting B cell activation. Nat Immunol 2002; 3:951.
55. Peckham D, Andersen-Nissen E, Finkelman FD, Stunz LL, Ashman RF. Difference in apoptosis induction between surface IgD and IgM. Int Immunol 2001; 13:285.
56. Nitschke L, Kosco MH, Kohler G, Lamers MC. Immunoglobulin D-deficient mice can mount normal immune responses to thymus-independent and -dependent antigens. Proc Natl Acad Sci USA 1993; 90:1887.
57. Lutz C, Ledermann B, Kosco-Vilbois MH, Ochsenbein AF, Zinkernagel RM, Kohler G, Brombacher F. IgD can largely substitute for loss of IgM function in B cells. Nature 1998; 393:797.
58. Brink R, Goodnow CC, Crosbie J, Adams E, Eris J, Mason DY, Hartley SB, Basten A. Immunoglobulin 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.
59. Weiser P, Muller R, Braun U, Reth M. Endosomal targeting by the cytoplasmic tail of membrane immunoglobulin. Science 1997; 276:407.
60. Batista FD, Anand S, Presani G, Efremov DG, Burrone OR. The two membrane isoforms of human IgE assemble into functionally distinct B cell antigen receptors. J Exp Med 1996; 184:2197.
61. Geisberger R, Prlic M, Achatz-Straussberger G et al. Phage display based cloning of proteins interacting with the cytoplasmic tail of membrane immunoglobulins. Clin Dev Immunol 2003; 9:127.
62. Yellen AJ, Glenn W, Sukhatme VP, Cao XM, Monroe JG. 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 1991; 146:1446.
63. Kovesdi D, Koncz G, Ivanyi-Nagy R et al. Developmental differences in B cell receptor-induced signal transduction. Cell Signal 2002; 14:563.
64. Seyfert VL, McMahon SB, Glenn WD, Yellen AJ, Sukhatme VP, Cao XM, Monroe JG. Methylation of an immediate-early inducible gene as a mechanism for B cell tolerance induction. Science 1990; 250:797.
65. Baldwin AS Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996; 14:649.
66. Weintraub BC, Jun JE, Bishop AC, Shokat KM, Thomas ML, Goodnow CC. Entry of B cell receptor into signaling domains is inhibited in tolerant B cells. J Exp Med 2000; 191:1443.
67. Sproul TW, Malapati S, Kim J, Pierce SK. Cutting edge: B cell antigen receptor signaling occurs outside lipid rafts in immature B cells. J Immunol 2000; 165:6020.
68. Goodnow CC, Crosbie J, Jorgensen H, Brink RA, Basten A. Induction of self-tolerance in mature peripheral B lymphocytes. Nature 1989; 342:385.
69. Hartley SB, Crosbie J, Brink R, Kantor AB, Basten A, Goodnow CC. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 1991; 353:765.
70. Goodnow CC, Brink R, Adams E. Breakdown of self-tolerance in anergic B lymphocytes. Nature 1991; 352:532.
71. Cheng AM, Rowley B, Pao W, Hayday A, Bolen JB, Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 1995; 378:303.
72. Lam KP, Kuhn R, Rajewsky K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 1997; 90:1073.
73. Pracht C, Gimborn K, Reth M, Huber M. BCR mutants deficient in ligand-independent and more sensitive for ligand-dependent signaling. Eur J Immunol 2002; 32:1614.
74. Levine MH, Haberman AM, Sant'Angelo DB, Hannum LG, Cancro MP, Janeway CA Jr, Shlomchik MJ. A B-cell receptor-specific selection step governs immature to mature B cell differentiation. Proc Natl Acad Sci USA 2000; 97:2743.
75. Janeway CA Jr. How the immune system works to protect the host from infection: a personal view. Proc Natl Acad Sci USA 2001; 98:7461.
76. Maruyama M, Lam KP, Rajewsky K. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 2000; 407:636.
77. Koopman G, Keehnen RM, Lindhout E, Newman W, Shimizu Y, van Seventer GA, de Groot C, Pals ST. Adhesion through the LFA-1 (CD11a/CD18) -ICAM-1 (CD54) and the VLA-4 (CD49d) -VCAM-1 (CD106) pathways prevents apoptosis of germinal center B cells. J Immunol 1994; 152:3760.
78. Davis DM. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol 2002; 23:356.
79. Clark EA, Brugge JS. Integrins and signal transduction pathways: the road taken. Science 1995; 268:233.
80. Batista FD, Iber D, Neuberger MS. B cells acquire antigen from target cells after synapse formation. Nature 2001; 411:489.
81. Imler JL, Hoffmann JA. Toll receptors in innate immunity. Trends Cell Biol 2001; 11:304.
82. Takeda K, Akira S. Roles of Toll-like receptors in innate immune responses. Genes Cells 2001; 6:733.
83. Vinuesa CG, Goodnow CC. Immunology: DNA drives autoimmunity. Nature 2002; 416:595.
84. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002; 416:603.
85. Heyman B. Regulation of antibody responses via antibodies, complement, and Fc receptors. Annu Rev Immunol 2000; 18:709.
86. Fearon DT, Carter RH. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol 1995; 13:127.
87. Nitschke L, Carsetti R, Ocker B, Kohler G, Lamers MC. CD22 is a negative regulator of B-cell receptor signalling. Curr Biol 1997; 7:133.
88. Kelm S, Gerlach J, Brossmer R, Danzer CP, Nitschke L. The ligand-binding domain of CD22 is needed for inhibition of the B cell receptor signal, as demonstrated by a novel human CD22-specific inhibitor compound. J Exp Med 2002; 195:1207.
89. Wakabayashi C, Adachi T, Wienands J, Tsubata T. A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science 2002; 298:2392.
90. Gerber JS, Mosser DM. Stimulatory and inhibitory signals originating from the macrophage Fcgamma receptors. Microbes Infect 2001; 3:131.
91. Payet-Jamroz M, Helm SL, Wu J et al. Suppression of IgE responses in CD23-transgenic animals is due to expression of CD23 on nonlymphoid cells. J Immunol 2001; 166:4863.
92. Karagiannis SN, Warrack JK, Jennings KH, Murdock PR, Christie G, Moulder K, Sutton BJ, Gould HJ. Endocytosis and recycling of the complex between CD23 and HLA-DR in human B cells. Immunology 2001; 103:319.
93. Yu P, Kosco-Vilbois M, Richards M, Kohler G, Lamers MC. Negative feedback regulation of IgE synthesis by murine CD23. Nature 1994; 369:753.
94. Fujiwara H, Kikutani H, Suematsu S et al. The absence of IgE antibody-mediated augmentation of immune responses in CD23-deficient mice. Proc Natl Acad Sci USA 1994; 91:6835.