CD19 and CD22 regulate a B lymphocyte signal transduction pathway that contributes to autoimmunity

Keio Journal of Medicine

Volumn 49, Issue 1, 2000, Pages 1-13

  Tedder, Thomas F ^a   Sato, Shinichi ^a   Poe, Jonathan C ^a   Fujimoto, Anabu ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; B lymphocyte; CD19; CD22; Signal transduction

Indexed keywords

B LYMPHOCYTE ANTIGEN; CD19 ANTIGEN; CD22 ANTIGEN; CD22 PROTEIN, HUMAN; CD22 PROTEIN, MOUSE; CELL ADHESION MOLECULE; LECTIN; LEUKOCYTE ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE;

ANIMAL; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BIOLOGICAL MODEL; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD; ANTIGENS, CD19; ANTIGENS, CD22; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; AUTOIMMUNITY; B-LYMPHOCYTES; CELL ADHESION MOLECULES; HUMANS; LECTINS; MICE; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 0034150347     PISSN: 00229717     EISSN: None     Source Type: Journal    
DOI: 10.2302/kjm.49.1     Document Type: Review

References (100)

1. Reth M, Wienands J: Initiation and processing of signals from the B cell antigen receptor. Annu Rev Immunol 1997; 15: 453-479
2. DeFranco AL: The complexity of signaling pathways activated by the BCR. Curr Opin Immunol 1997; 9: 296-308
3. Kurosaki T: Genetic analysis of B cell antigen receptor signaling. Annu Rev Immunol 1999; 17: 555-592
4. Tamir I, Cambier JC: Antigen receptor signaling: integration of protein tyrosine kinase functions. Oncogene 1998; 17: 1353-1364
5. 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
6. Saouaf SJ, Mahajan S, Rowley RB, Kut SA, Fargnoli J, Burkhardt AL, Tsukada S, Witte ON, Bolen JB: Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc Natl Acad Sci USA 1994; 91: 9524-9528
7. Chan VW, Lowell CA, DeFranco AL: Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes. Curr Biol 1998; 8: 545-553
8. Smith KGC, Tarlinton DM, Doody GM, Hibbs ML, Fearon DT: Inhibition of the B cell by CD22: a requirement for Lyn. J Exp Med 1998; 187: 807-811
9. Cornall RJ, Cyster JG, Hibbs ML, Dunn AR, Otipoby KL, Clark EA, Goodnow CC: Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 1998; 8: 497-508
10. Nishizumi H, Horikawa K, Mlinaric-Rascan I, Yamamoto T: A double-edged kinase Lyn: a positive and negative regulator for antigen receptor-mediated signals. J Exp Med 1998; 187: 1343-1348
11. Thomas SM, Brugge JS: Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 1997; 13: 513-609
12. Sicheri F, Kuriyan J: Structures of Src-family tyrosine kinases. Curr Opin Struct Biol 1997; 7: 777-785
13. Pawson T: New impressions of Src and Hck. Nature 1997; 385: 582-585
14. Thomas ML, Brown EJ: Positive and negative regulation of Src-family membrane kinases by CD45. Immunol Today 1999; 20: 406-411
15. Tedder TF: Introduction: response-regulators of B lymphocyte signaling thresholds provide a context for antigen receptor signal transduction. Semin Immunol 1998; 10: 259-265
16. Sato S, Tuscano JM, Inaoki M, Tedder TF: CD22 negatively and positively regulates signal transduction through the B lymphocyte antigen receptor. Semin Immunol 1998; 10: 287-297
17. Fujimoto M, Poe JC, Inaoki M, Tedder TF: CD19 regulates B lymphocyte responses to transmembrane signals. Semin Immunol 1998; 10: 267-277
18. Carter RH, Doody GM, Bolen JB, Fearon DT: 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 1997; 158: 3062-3069
19. Leprince C, Draves KE, Geahlen RL, Ledbetter JA, Clark EA: CD22 associates with the human surface IgM-B cell antigen receptor complex. Proc Natl Acad Sci USA 1993; 90: 3236-3240
20. Peaker CJ, Neuberger MS: Association of CD22 with the B cell antigen receptor. Eur J Immunol 1993; 23: 1358-1363
21. Fujimoto M, Poe JC, Jansen PJ, Sato S, Tedder TF: CD19 amplifies B lymphocyte signal transduction by regulating Src-family protein tyrosine kinase activation. J Immunol 1999; 162: 7088-7094
22. Tedder TF, Inaoki M, Sato S: The CD19-CD21 complex regulates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity 1997; 6: 107-118
23. Goodnow CC: Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc Natl Acad Sci USA 1996; 93: 2264-2271
24. Sato S, Ono N, Steeber DA, Pisetsky DS, Tedder TF: CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J Immunol 1996; 157: 4371-4378
25. Inaoki M, Sato S, Weintraub BC, Goodnow CC, Tedder TF: CD19-regulated signaling thresholds control peripheral tolerance and autoantibody production in B lymphocytes. J Exp Med 1997; 186: 1923-1931
26. Prodeus AP, Goerg S, Shen LM, Pozdnyakova OO, Chu L, Alicot EM, Goodnow CC, Carroll MC: A critical role for complement in maintenance of self-tolerance. Immunity 1998; 9: 721-731
27. O'Keefe TL, Williams GT, Batista FD, Neuberger MS: Deficiency in CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J Exp Med 1999; 189: 1307-1313
28. Nishizumi H, Taniuchi I, Yamanashi Y, Kitamura D, Ilic D, Mori S, Watanabe T, Yamamoto T: Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 1995; 3: 549-560
29. Hibbs ML, Tarlinton DM, Armes J, Grail D, Hodgson G, Maglitto R, Stacker SA, Dunn AR: Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995; 83: 301-311
30. Tsui HW, Siminovitch KA, de Souza L, Tsui FW: Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat Genet 1993; 4: 124-129
31. Okano Y: Antinuclear antibody in systemic sclerosis (scleroderma). Rheum Dis Clin North Am 1996; 22: 709-735
32. Sato S, Steeber DA, Jansen PJ, Tedder TF: CD19 expression levels regulate B lymphocyte development: human CD19 restores normal function in mice lacking endogenous CD19. J Immunol 1997; 158: 4662-4669
33. Krop I, Shaffer AL, Fearon DT, Schlissel MS: The signaling activity of murine CD19 is regulated during cell development. J Immunol 1996; 157: 48-56
34. Boyd AW, Anderson KC, Freedman AS, Fisher DC, Slaughenhoupt B, Schlossman SF, Nadler LM: Studies of in vitro activation and differentiation of human B lymphocytes. I. Phenotypic and functional characterization of the B cell population responding to anti-Ig antibody. J Immunol 1985; 134: 1516-1523
35. Carroll MC: CD21/CD35 in B cell activation. Semin Immunol 1998; 10: 279-286
36. Bradbury LE, Kansas GS, Levy S, Evans RL, Tedder TF: The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J Immunol 1992; 149: 2841-2850
37. Maecker HT, Todd SC, Levy S: The tetraspanin superfamily: molecular facilitators. Faseb J 1997; 11: 428-442
38. Maecker HT, Levy S: Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med 1997; 185: 1505-1510
39. Miyazaki T, Muller U, Campbell KS: Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. Embo J 1997; 16: 4217-4225
40. Tsitsikov EN, Gutierrez-Ramos JC, Geha RS: Impaired CD19 expression and signaling enhanced antibody response to type II T independent antigen and reduction of B-1 cells in CD81-deficient mice. Proc Natl Acad Sci USA 1997; 94: 10844-10849
41. Deblandre GA, Marinx OP, Evans SS, Majjaj S, Leo O, Caput D, Huez GA, Wathelet MG: Expression cloning of an interferon-inducible 17-kDa membrane protein implicated in the control of cell growth. J Biol Chem 1995; 270: 23860-23866
42. Bradbury LE, Goldmacher VS, Tedder TF: The CD19 signal transduction complex of B lymphocytes: deletion of the CD19 cytoplasmic domain alters signal transduction but not complex formation with TAPA-1 and Leu-13. J Immunol 1993; 151: 2915-2927
43. Matsumoto AK, Martin DR, Carter RH, Klickstein LB, Ahearn JM, Fearon DT: Functional dissection of the CD21/ CD19/TAPA-1/Leu-13 complex of B lymphocytes. J Exp Med 1993; 178: 1407-1417
44. Fearon DT, Carter RH: The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol 1995; 13: 127-149
45. van Noesel CJ, Lankester AC, van Lier RA: Dual antigen recognition by B cells. Immunol Today 1993; 14: 8-11
46. Engel P, Zhou LJ, Ord DC, Sato S, Koller B, Tedder TF: Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995; 3: 39-50
47. Zhou LJ, Smith HM, Waldschmidt TJ, Schwarting R, Daley J, Tedder TF: Tissue-specific expression of the human CD19 gene in transgenic mice inhibits antigen-independent B lymphocyte development. Mol Cell Biol 1994; 14: 3884-3894
48. Rickert RC, Rajewsky K, Roes J: Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 1995; 376: 352-355
49. Sato S, Steeber DA, Tedder TF: The CD19 signal transduction molecule is a response regulator of B-lymphocyte differentiation. Proc Natl Acad Sci USA 1995; 92: 11558-11562
50. Sato S, Miller AS, Howard MC, Tedder TF: Regulation of B lymphocyte development and activation by the CD19/CD21/ CD81/Leu 13 complex requires the cytoplasmic domain of CD19. J Immunol 1997; 159: 3278-3287
51. Tedder TF, Isaacs CM: Isolation of cDNAs encoding the CD19 antigen of human and mouse B lymphocytes. A new member of the immunoglobulin superfamily. J Immunol 1989; 143: 712-717
52. van Noesel CJ, Lankester AC, van Schijndel GM, van Lier RA: The CR2/CD19 complex on human B cells contains the src-family kinase Lyn. Int Immunol 1993; 5: 699-705
53. Uckun FM, Burkhardt AL, Jarvis L, Jun X, Stealey B, Dibirdik I, Myers DE, Tuel-Ahlgren L, Bolen JB: Signal transduction through the CD19 receptor during discrete developmental stages of human B-cell ontogeny. J Biol Chem 1993; 268: 21172-21184
54. Chalupny NJ, Kanner SB, Schieven GL, Wee SF, Gilliland LK, Aruffo A, Ledbetter JA: Tyrosine phosphorylation of CD19 in pre-B and mature B cells. Embo J 1993; 12: 2691-2696
55. Bireland ML, Monroe JG: Biochemistry of antigen receptor signaling in mature and developing B lymphocytes. Crit Rev Immunol 1997; 17: 353-385
56. Fujimoto M, Fujimoto Y, Poe JC, Jansen PJ, Lowell CA, DeFranco AL, Tedder TF: CD19 is a specialized transmembrane adapter protein that amplifies Src-family protein tyrosine kinase activation. (submitted):
57. 2+ mobilization. J Exp Med 1997; 186: 1897-1910
58. Li HL, Forman MS, Kurosaki T, Pure E: Syk is required for BCR-mediated activation of p90Rsk, but not p70S6k, via a mitogen-activated protein kinase-independent pathway in B cells. J Biol Chem 1997; 272: 18200-18208
59. El-Hillal O, Kurosaki T, Yamamura H, Kinet JP, Scharenberg AM: syk kinase activation by a src kinase-initiated activation loop phosphorylation chain reaction. Proc Natl Acad Sci USA 1997; 94: 1919-1924
60. Buhl AM, Cambier JC: Phosphorylation of CD19 Y484 and Y515, and linked activaiton of phosphatidylinositol 3-kinase, are required for B cell antigen receptor-mediated activation of Bruton's tyrosine kinase. J Immunol 1999; 162: 4438-4446
61. Tuveson DA, Carter RH, Soltoff SP, Fearon DT: CD19 of B cells as a surrogate kinase insert region to bind phosphatidylinositol 3-kinase. Science 1993; 260: 986-989
62. Weng WK, Jarvis L, LeBien TW: Signaling through CD19 activates Vav/mitogen-activated protein kinase pathway and induces formation of a CD19/Vav/phosphatidylinositol 3-kinase complex in human B cell precursors. J Biol Chem 1994; 269: 32514-32521
63. Li X, Sandoval D, Freeberg L, Carter RH: Role of CD19 tyrosine 391 in synergistic activation of B lymphocytes by coligation of CD19 and membrane Ig. J Immunol 1997; 158: 5649-5657
64. O'Rourke LM, Tooze R, Turner M, Sandoval DM, Carter RH, Tybulewicz VL, Fearon DT: CD19 as a membrane-anchored adaptor protein of B lymphocytes: costimulation of lipid and protein kinases by recruitment of Vav. Immunity 1998; 8: 635-645
65. Sato S, Jansen PJ, Tedder TF: CD19 and CD22 expression reciprocally regulates tyrosine phosphorylation of Vav protein during B lymphocyte signaling. Proc Natl Acad Sci USA 1997; 94: 13158-13162
66. Zhou LJ, Ord DC, Hughes AL, Tedder TF: Structure and domain organization of the CD19 antigen of human, mouse and guinea pig B lymphocytes. Conservation of the extensive cytoplasmic domain. J Immunol 1991; 147: 1424-1432
67. Zhou S, Cantley LC: Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem Sci 1995; 20: 470-475
68. Clark MR, Johnson SA, Cambier JC: Analysis of Ig-alpha-tyrosine kinase interaction reveals two levels of binding specificity and tyrosine phosphorylated Ig-alpha stimulation of Fyn activity. Embo J 1994; 13: 1911-1919
69. Ruzzene M, Brunati AM, Donella-Deana A, Marin O, Pinna LA: Specific stimulation of c-Fgr kinase by tyrosine-phosphorylated (poly)peptides: possible implication in the sequential mode of protein phosphorylation. Eur J Biochem 1997; 245: 701-707
70. Tedder TF, Tuscano J, Sato S, Kehrl JH: CD22, a B lymphocyte-specific adhesion molecule that regulates antigen receptor signaling. Annu Rev Immunol 1997; 15: 481-504
71. Tooze RM, Doody GM, Fearon DT: Counterregulation by the coreceptors CD19 and CD22 of MAP kinase activation by membrane immunoglobulin. Immunity 1997; 7: 59-67
72. Weng WK, Shah N, O'Brien D, Van Ness B, LeBien TW: Differential induction of DNA-binding activities following CD19 cross-linking in human B lineage cells. J Immunol 1997; 159: 5502-5508
73. Li X, Carter RH: Convergence of CD19 and B cell antigen receptor signals at MEK1 in the ERK2 activation cascade. J Immunol 1998; 161: 5901-5908
74. Lankester AC, van Schijndel GM, Rood PM, Verhoeven AJ, van Lier RA: B cell antigen receptor cross-linking induced tyrosine phosphorylation and membrane translocation of a multimeric She complex that is augmented by CD19 co-ligation. Eur J Immunol 1994; 24: 2818-2825
75. Beckwith M, Jorgensen G, Longo DL: The protein product of the proto-oncogene c-cbl forms a complex with phosphatidylinositol 3-kinase p85 and CD19 in anti-IgM-stimulated human B-lymphoma cells. Blood 1996; 88: 3502-3507
76. Chalupny NJ, Aruffo A, Esselstyn JM, Chan PY, Bajorath J, Blake J, Gilliland LK, Ledbetter JA, Tepper MA: Specific binding of Fyn and phosphatidylinositol 3-kinase to the B cell surface glycoprotein CD19 through their src homology 2 domains. Eur J Immunol 1995; 25: 2978-2984
77. Marte BM, Downward J: PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem Sci 1997; 22: 355-358
78. Franke TF, Kaplan DR, Cantley LC: PI3K: downstream AKTion blocks apoptosis. Cell 1997; 88: 435-437
79. Suzuki H, Terauchi Y, Fujiwara M, Aizawa S, Yazaki Y, Kadowaki T, Koyasu S: Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science 1999; 283: 390-392
80. Fruman DA, Snapper SB, Yballe CM, Davidson L, Yu JY, Alt FW, Cantley LC: Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 1999; 283: 393-397
81. Fujimoto M, Bradney AP, Poe JC, Steeber DA, Tedder TF: Modulation of B lymphocyte antigen receptor signal transduction by a CD19/CD22 regulatory loop. Immunity 1999; 11: 191-200
82. Engel P, Nojima Y, Rothstein D, Zhou LJ, Wilson GL, Kehrl JH, Tedder TF: The same epitope on CD22 of B lymphocytes mediates the adhesion of erythrocytes, T and B lymphocytes, neutrophils and monocytes. J Immunol 1993; 150: 4719-4732
83. Kelm S, Pelz A, Schauer R, Filbin MT, Tang S, de Bellard ME, Schnaar RL, Mahoney JA, Hartnell A, Bradfield P, Crocker PR: Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily. Curr Biol 1994; 4: 965-972
84. Schulte RJ, Campbell MA, Fischer WH, Sefton BM: Tyrosine phosphorylation of CD22 during B cell activation. Science 1992; 258: 1001-1004
85. Wilson GL, Fox CH, Fauci AS, Kehrl JH: cDNA cloning of the B cell membrane protein CD22: a mediator of B-B cell interactions. J Exp Med 1991; 173: 137-146
86. Sato S, Miller AS, Inaoki M, Bock CB, Jansen PJ, Tang ML, Tedder TF: CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 1996; 5: 551-562
87. Otipoby KL, Andersson KB, Draves KE, Klaus SJ, Farr AG, Kerner JD, Perlmutter RM, Law CL, Clark EA: CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 1996; 384: 634-637
88. O'Keefe TL, Williams GT, Davies SL, Neuberger MS: Hyper-responsive B cells in CD22-deficient mice. Science 1996; 274: 798-801
89. Nitschke L, Carsetti R, Ocker B, Kohler G, Lamers MC: CD22 is a negative regulator of B-cell receptor signalling. Curr Biol 1997; 7: 133-143
90. Doody GM, Justement LB, Delibrias CC, Mathews RJ, Lin J, Thomas ML, Fearon DT: A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 1995; 269: 242-244
91. Lankester AC, van Schijndel GM, van Lier RA: Hematopoietic cell phosphatase is recruited to CD22 following B cell antigen receptor ligation. J Biol Chem 1995; 270: 20305-20308
92. Campbell MA, Klinman NR: Phosphotyrosine-dependent association between CD22 and protein tyrosine phosphatase 1C. Eur J Immunol 1995; 25: 1573-1579
93. Law CL, Sidorenko SP, Chandran KA, Zhao Z, Shen SH, Fischer EH, Clark EA: CD22 associates with protein tyrosine phosphatase 1C, Syk, and phospholipase C-γ1 upon B cell activation. J Exp Med 1996; 183: 547-560
94. Blasioli J, Paust S, Thomas ML: Definition of the sites of interaction between the protein tyrosine phosphatase SHP-1 and CD22. J Biol Chem 1999; 274: 2303-2307
95. Yohannan J, Wienands J, Coggeshall KM, Justement LB: Analysis of tyrosine phosphorylation-dependent interactions between stimulatory effector proteins and the B cell co-receptor CD22. J Biol Chem 1999; 274: 18769-18776
96. Tuscano J, Engel P, Tedder TF, Kehrl JH: Engagement of the adhesion receptor CD22 triggers a potent stimulatory signal for B cells and blocking CD22/CD22L interactions impairs T-cell proliferation. Blood 1996; 87: 4723-4730
97. Tuscano JM, Engel P, Tedder TF, Agarwal A, Kehrl JH: Involvement of p72syk kinase, p53/56lyn kinase and phosphatidyl inositol-3 kinase in signal transduction via the human B lymphocyte antigen CD22. Eur J Immunol 1996; 26: 1246-1252
98. 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: 7865-7870
99. van Oers NS, Killeen N, Weiss A: ZAP-70 is constitutively associated with tyrosine-phosphorylated TCR ζ in murine thymocytes and lymph node T cells. Immunity 1994; 1: 675-685
100. Chan VW, Meng F, Soriano P, DeFranco AL, Lowell CA: Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity 1997; 7: 69-81