SLP-76 is recruited to CD22 and dephosphorylated by SHP-1, thereby regulating B cell receptor-induced c-Jun N-terminal kinase activation

European Journal of Immunology

Volumn 35, Issue 2, 2005, Pages 644-654

  Mizuno, Kazuya ^a   Tagawa, Yuko ^a   Watanabe, Noriyuki ^a   Ogimoto, Mami ^a   Yakura, Hidetaka ^a,b  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

B cell receptor; SHP 1; Signal transduction

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD22 ANTIGEN; LAT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SH2; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEINASE; SECRETORY LEUKOCYTE PROTEINASE 76; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; ATTENUATION; B LYMPHOCYTE; CELL FRACTIONATION; CELL LINE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; DOWN REGULATION; ENZYME ACTIVATION; ENZYME SUBSTRATE; LYMPHOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SPLEEN CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD; ANTIGENS, CD22; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; B-LYMPHOCYTES; CELL ADHESION MOLECULES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LECTINS; LYMPHOCYTE ACTIVATION; MICE; ONCOGENE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE-PHOSPHATASE; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; TYROSINE;

EID: 14744284324     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425465     Document Type: Article

References (47)

1. Kelly, M. and Chan, A. C., Regulation of B cell function by linker proteins. Curr. Opin. Immunol. 2000. 12: 267-275.
2. Craxton, A., Optipoby, K. L., Jiang, A. and Clark, E. A., Signal transduction pathways that regulate the fate of B lymphocytes. Adv. Immunol. 1999. 73: 79-152.
3. Tedder, T. F., 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.
4. Fu, C., Turck, T., Kurosaki, T. and Chan, A. C., BLNK: a central linker protein in B cell activation. Immunity 1998. 9: 93-103.
5. Wienands, J., Schweikert, J., Wollscheid, B., Jumaa, H., Nielsen, P. J. and Reth, M., SLP-65: a new signaling component in B lymphocytes which requires expression of the antigen receptor for phosphorylation. J. Exp. Med. 1998. 188: 791-795.
6. Goitsuka, R., Fujimura, Y., Mamada, H., Umeda, A., Morimura, T., Uetsuka, K., Doi, K., Tsuji, S. and Kitamura, D., BASH, a novel signaling molecule preferentially expressed in B cells of the bursa of Fabricius. J. Immunol. 1998. 161: 5804-5808.
7. Ishiai, M., Kurosaki, M., Pappu, R., Okawa, K., Ronko, I., Fu, C., Shibata, M., Iwamatsu, A., Chan, A. C. and Kurosaki, T., BLNK required for coupling Syk to PLCγ2 and Rac1-JNK in B cells. Immunity 1999. 10: 117-125.
8. Pappu, R., Cheng, A. M., Li, B., Gong, Q., Chiu, C., Griffin, N., White, M., Sleckman, B. P. and Chan, A. C., Requirement for B cell linker protein (BLNK) in B cell development. Science 1999. 286: 1949-1954.
9. Jumaa, H., Wollscheid, B., Mitterer, M., Wienands, J., Reth, M. and Nielsen, P. J., Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity 1999. 11: 547-554.
10. Weber, J. R., Orstavik, S., Torgersen, K. M., Danbolt, N. C., Berg, S. F., Ryan, J. C., Tasken, K., Imboden, J. B. and Vaage, J. T., Molecular cloning of the cDNA encoding pp36, a tyrosine-phosphorylated adaptor protein selectively expressed by T cells and natural killer cells. J. Exp. Med. 1998. 187: 1157-1161.
11. Zhang, W., Sloan-Lancaster, J., Kitchen, J., Trible, R. P. and Samelson, L. E., LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998. 9: 83-92.
12. Law, C. L., Ewings, M. K., Chaudhary, P. M., Solow, S. A., Yun, T. J., Marshall, A. J., Hood, L. and Clark, E. A., GrpL, a Grb2-related adaptor protein, interacts with SLP-76 to regulate nuclear factor of activated T cell activation. J. Exp. Med. 1999. 189: 1243-1253.
13. Liu, S. K., Fang, N., Koretzky, G. A. and McGlade, C. J., The hematopoietic-specific adaptor protein Gads functions in T cell signaling via interactions with the SLP-76 and LAT adaptors. Curr. Biol. 1999. 9: 67-75.
14. Finco, T. S., Kadlecek, T., Zhang, W., Samelson, L. E. and Weiss, A., LAT is required for TCR-mediated activation of PLCγ1 and the Ras pathway. Immunity 1998. 9: 617-626.
15. Wardenburg, B. J., Pappu, R., Bu, J. Y., Mayer, B., Chernoff, J., Straus, D. and Chan, A. C., Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 1998. 9: 607-616.
16. Wunderlich, L., Farago, A., Downward, J. and Buday, L., Association of Nck with tyrosine-phosphorylated SLP-76 in activated T lymphocytes. Eur. J. Immunol. 1999. 29: 1068-1075.
17. Yablonski, D., Kuhne, M. R., Kadlecek, T. and Weiss, A., Uncoupling of nonreceptor tyrosine kinases from PLC-γ1 in an SLP-76-deficient T cell. Science 1998. 281: 413-416.
18. Cyster, J. G. and Goodnow, C. C., Tuning antigen receptor signaling by CD22: integrating cues from antigens and the microenvironment. Immunity 1997. 6: 509-517.
19. Wilson, G. L., Fox, C. H., Fauci, A. S. and Kehrl, J. H., cDNA cloning of the B cell membrane protein CD22: a mediator of B-B cell interactions. J. Exp. Med. 1991. 173: 137-146.
20. Schulte, R. J., Campbell, M. A., Fischer, W. H. and Sefton, B. M., Tyrosine phosphorylation of CD22 during B cell activation. Science 1992. 258: 1001-1004.
21. Thomas, M. L., Of ITAMs and ITIMs: turning on and off the B cell antigen receptor. J. Exp. Med. 1995. 181: 1953-1956.
22. Doody, G. M., Justement, L. B., Delibrias, C. C., Matthews, R. J., Lin, J., Thomas, M. L. and Fearon, D. T., A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 1995. 269: 242-244.
23. Lankester, A. C., van Schijndel, G. M. and van Lier, R. A., Hematopoietic cell phosphatase is recruited to CD22 following B cell antigen receptor ligation. J. Biol. Chem. 1995. 270: 20305-20308.
24. O'Keefe, T. L., Williams, G. T., Davies, S. L. and Neuberger, M. S., Hyperresponsive B cells in CD22-deficient mice. Science 1996. 274: 798-801.
25. Otipoby, K. L., Andersson, K. B., Draves, K. E., Klaus, S. J., Farr, A. G., Kerner, J. D., Perlmutter, R. M., Law, C. L. and Clark, E. A., CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 1996. 384: 634-637.
26. Cyster, J. G. and Goodnow, C. C., Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 1995. 2: 13-24.
27. Adachi, T., Flaswinkel, H., Yakura, H., Reth, M. and Tsubata, T., The B cell surface protein CD72 recruits the tyrosine phosphatase SHP-1 upon tyrosine phosphorylation. J. Immunol. 1998. 160: 4662-4665.
28. Maeda, A., Kurosaki, M., Ono, M., Takai, T. and Kurosaki, T., Requirement of SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 for paired immunoglobulin-like receptor B (PIR-B)-mediated inhibitory signal. J. Exp. Med. 1998. 187: 1355-1360.
29. Pei, D., Lorenz, U., Klingmuller, U., Neel, B. G. and Walsh, C. T., Intramolecular regulation of protein tyrosine phosphatase SH-PTP1: a new function for Src homology 2 domains. Biochemistry 1994. 33: 15483-15493.
30. 2-terminal kinase activation in B cells. J. Immunol. 2000. 165: 1344-1351.
31. 2-terminal kinase. J. Immunol. 2002. 169: 778-786.
32. Mizuno, K., Katagiri, T., Hasegawa, K., Ogimoto, M. and Yakura, H., Hematopoietic cell phosphatase, SHP-1, is constitutively associated with the SH2 domain-containing leukocyte protein, SLP-76, in B cells. J. Exp. Med. 1996. 184: 457-463.
33. Nagata, K., Nakamura, T., Kitamura, F., Kuramochi, S., Taki, S., Campbell, K. S. and Karasuyama, H., The Igα/Igβ heterodimer on μ-negative proB cells is competent for transducing signals to induce early B cell differentiation. Immunity 1997. 4: 559-570.
34. Su, Y.-W. and Jumaa, H., LAT links the pre-BCR to calcium signaling. Immunity 2003. 19: 295-305.
35. Clements, J. L., Ross-Barta, S. E., Tygrett, L. T., Waldschmidt, T. J. and Koretzky, G. A., SLP-76 expression is restricted to hemopoietic cells of monocyte, granulocyte, and T lymphocyte lineage and is regulated during T cell maturation and activation. J. Immunol. 1998. 161: 3880-3889.
36. Alizadeh, A. A., Eisen, M. B., Davis, R. E., Ma, C., Lossos, I. S., Rosenwald, A., Boldrick, J. C., Sabet, H., Tran, T., Yu, X. et al., Distinct types of diffuse large B cell lymphoma identified by gene expression profiling. Nature 2000. 403: 503-511.
37. Wong, J., Ishiai, M., Kurosaki, T. and Chan, A. C., Functional complementation of BLNK by SLP-76 and LAT linker proteins. J. Biol. Chem. 2000. 275: 33116-33122.
38. Brdickova, N., Brdicka, T., Angelisova, P., Horvath, O., Spicka, J., Hilgert, I., Paces, J., Simeoni, L., Kliche, S., Merten, C. et al., LIME: a new membrane raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J. Exp. Med. 2003. 198: 1453-1462.
39. Motto, D. G., Ross, S. E., Wu, J., Hendricks-Taylor, L. R. and Koretzky, G. A., Implication of the Grb2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J. Exp. Med. 1996. 183: 1937-1943.
40. Shultz, L. D., Schweitzer, P. A., Rajan, T. V., Yi, T., Ihle, J. N., Matthews, R. J., Thomas, M. L. and Beier, D. R., Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 1993. 73: 1445-1454.
41. Tsui, H. W., Siminovitch, K. A., de Souza, L. and Tsui, F. W., Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat. Genet. 1993. 4: 124-129.
42. Otipoby, K. L., Draves, K. E. and Clark, E. A., CD22 regulates B cell receptor-mediated signals via two domains that independently recruit Grb2 and SHP-1. J. Biol. Chem. 2001. 276: 44315-44322.
43. Tuscano, J. M., Engel, P., Tedder, T. F., Agarwal, A. and Kehrl, J. H., 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.
44. Clements, J. L., Yang, B., Ross-Barta, S. E., Eliason, S. L., Hrstka, R. F., Williamson, R. A. and Koretzky, G. A., Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science 1998. 281: 416-419.
45. Pivniouk, V., Tsitsikov, E., Swinton, P., Rathbun, G., Alt, F. W. and Geha, R. S., Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 1998. 94: 229-238.
46. Brdicka, T., Imrich, M., Angelisova, P., Brdickova, N., Horvath, O., Spicka, J., Hilgert, I., Luskova, P., Draber, P., Novak, P. et al., Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J. Exp. Med. 2002. 196: 1617-1626.
47. Janssen, E., Zhu, M., Zhang, W., Koonpaew, S. and Zhang, W., LAB: a new membrane-associated adaptor molecule in B cell activation. Nat. Immunol. 2003. 4: 117-123.