Attenuation of T cell receptor signaling by serine phosphorylation-mediated lysine 30 ubiquitination of SLP-76 protein

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34091-34100

  Wang, Xiaohong ^a   Li, Ju Pi ^b   Chiu, Li Li ^c   Lan, Joung Liang ^c,d   Chen, Der Yuan ^c,d   Boomer, Jonathan ^a   Tan, Tse Hua ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS; DOWN-REGULATION; FEEDBACK REGULATION; JNK ACTIVATION; PROTEASOMAL DEGRADATION; REGULATION MECHANISMS; T CELL RECEPTOR; T CELLS; T-CELL RECEPTORS; UBIQUITINATION; UNDERLYING MECHANISM;

AMINO ACIDS; CELL MEMBRANES; PROTEINS; SIGNALING;

PHOSPHORYLATION;

ADAPTOR PROTEIN; CD3 ANTIBODY; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; SH2 DOMAIN CONTAINING LEUKOCYTE PROTEIN 76; STRESS ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UBIQUITINATION;

14-3-3 PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JURKAT CELLS; MAP KINASE KINASE 4; MICE; MICE, MUTANT STRAINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RECEPTORS, ANTIGEN, T-CELL; SERINE; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84867241759     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.371062     Document Type: Article

References (30)

1. Koretzky, G. A., Abtahian, F., and Silverman, M. A. (2006) SLP-76 and SLP-65: complex regulation of signaling in lymphocytes and beyond. Nat. Rev. Immunol. 6, 67-78 (Pubitemid 43279754)
2. Fang, N., Motto, D. G., Ross, S. E., and Koretzky, G. A. (1996) Tyrosines 113, 128, and 145 of SLP-76 are required for optimal augmentation of NFAT promoter activity. J. Immunol. 157, 3769-3773 (Pubitemid 126449281)
3. Shui, J. W., Boomer, J. S., Han, J., Xu, J., Dement, G. A., Zhou, G., and Tan, T. H. (2007) Hematopoietic progenitor kinase 1 negatively regulates T cell receptor signaling and T cell-mediated immune responses. Nat. Immunol 8, 84-91 (Pubitemid 46242362)
4. Hu, M. C., Qiu, W. R., Wang, X., Meyer, C. F., and Tan, T. H. (1996) Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev. 10, 2251-2264 (Pubitemid 26322362)
5. Kiefer, F., Tibbles, L. A., Anafi, M., Janssen, A., Zanke, B. W., Lassam, N., Pawson, T., Woodgett, J. R., and Iscove, N. N. (1996) HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J. 15, 7013-7025 (Pubitemid 27023272)
6. Wang, W., Zhou, G., Hu, M. C., Yao, Z., and Tan, T. H. (1997) Activation of the hematopoietic progenitor kinase 1 (HPK1)-dependent, stress-activated c-Jun N-terminal kinase (JNK) pathway by transforming growth factor β (TGF-β)-activated kinase (TAK1), a kinase mediator of TGF-β signal transduction. J. Biol. Chem. 272, 22771-22775 (Pubitemid 27386096)
7. Zhou, G., Lee, S. C., Yao, Z., and Tan, T. H. (1999) Hematopoietic progenitor kinase 1 is a component of transforming growth factor β-induced c-Jun N-terminal kinase signaling cascade. J. Biol. Chem. 274, 13133-13138
8. Chen, Y. R., and Tan, T. H. (1999) Mammalian c-Jun N-terminal kinase pathway and STE-20-related kinases. Gene Ther. & Mol. Biol. 4, 83-98
9. Pombo, C. M., Kehrl, J. H., Sánchez, I., Katz, P., Avruch, J., Zon, L. I., Woodgett, J. R., Force, T., and Kyriakis, J. M. (1995) Activation of the SAPK pathway by the human STE20 homolog germinal center kinase. Nature 377, 750-754
10. Diener, K., Wang, X. S., Chen, C., Meyer, C. F., Keesler, G., Zukowski, M., Tan, T. H., and Yao, Z. (1997) Activation of the c-Jun N-terminal kinase pathway by a novel protein kinase related to human germinal center kinase. Proc. Natl. Acad. Sci. U.S.A. 94, 9687-9692 (Pubitemid 27408124)
11. Yao, Z., Zhou, G., Wang, X. S., Brown, A., Diener, K., Gan, H., and Tan, T. H. (1999) A novel human STE20-related protein kinase, HGK, that specifically activates the c-Jun N-terminal kinase signaling pathway. J. Biol. Chem. 274, 2118-2125
12. Hu, Y., Leo, C., Yu, S., Huang, B. C., Wang, H., Shen, M., Luo, Y., Daniel- Issakani, S., Payan, D. G., and Xu, X. (2004) Identification and functional characterization of a novel human misshapen/Nck-interacting kinase-related kinase, hMINKβ. J. Biol. Chem. 279, 54387-54397 (Pubitemid 40053178)
13. Shi, C. S., and Kehrl, J. H. (1997) Activation of stress-activated protein kinase/c-Jun N-terminal kinase, but not NF-κB, by the tumor necrosis factor (TNF) receptor 1 through a TNF receptor-associated factor 2- and germinal center kinase related-dependent pathway. J. Biol. Chem. 272, 32102-32107
14. Oehrl, W., Kardinal, C., Ruf, S., Adermann, K., Groffen, J., Feng, G. S., Blenis, J., Tan, T. H., and Feller, S. M. (1998) The germinal center kinase (GCK)-related protein kinases HPK1 and KHS are candidates for highly selective signal transducers of Crk family adaptor proteins. Oncogene 17, 1893-1901 (Pubitemid 28488457)
15. Ling, P., Yao, Z., Meyer, C. F., Wang, X. S., Oehrl, W., Feller, S. M., and Tan, T. H. (1999) Interaction of hematopoietic progenitor kinase 1 with adaptor proteins Crk and CrkL leads to synergistic activation of c-Jun N-terminal kinase. Mol. Cell. Biol. 19, 1359-1368 (Pubitemid 29046877)
16. Ensenat, D., Yao, Z., Wang, X. S., Kori, R., Zhou, G., Lee, S. C., and Tan, T. H. (1999) A novel Src homology 3 domain-containing adaptor protein, HIP-55, that interacts with hematopoietic progenitor kinase 1. J. Biol. Chem. 274, 33945-33950 (Pubitemid 129511722)
17. Sauer, K., Liou, J., Singh, S. B., Yablonski, D., Weiss, A., and Perlmutter, R. M. (2001) Hematopoietic progenitor kinase 1 associates physically and functionally with the adaptor proteins B cell linker protein and SLP-76 in lymphocytes. J. Biol. Chem. 276, 45207-45216
18. Boomer, J. S., and Tan, T. H. (2005) Functional interactions of HPK1 with adaptor proteins. J. Cell. Biochem. 95, 34-44 (Pubitemid 41420213)
19. Ma, W., Xia, C., Ling, P., Qiu, M., Luo, Y., Tan, T. H., and Liu, M. (2001) Leukocyte-specific adaptor protein Grap2 interacts with hematopoietic progenitor kinase 1 (HPK1) to activate JNK signaling pathway in T lymphocytes. Oncogene 20, 1703-1714 (Pubitemid 32368017)
20. Ling, P., Meyer, C. F., Redmond, L. P., Shui, J. W., Davis, B., Rich, R. R., Hu, M. C., Wange, R. L., and Tan, T. H. (2001) Involvement of hematopoietic progenitor kinase 1 in T cell receptor signaling. J. Biol. Chem. 276, 18908-18914
21. Zhou, G., Boomer, J. S., and Tan, T. H. (2004) Protein phosphatase 4 is a positive regulator of hematopoietic progenitor kinase 1. J. Biol. Chem. 279, 49551-49561 (Pubitemid 39625843)
22. Chen, Y. R., Meyer, C. F., Ahmed, B., Yao, Z., and Tan, T. H. (1999) Caspase-mediated cleavage and functional changes of hematopoietic progenitor kinase 1 (HPK1). Oncogene 18, 7370-7377 (Pubitemid 30032118)
23. Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., Michel, F., Schwartz, O., Lehmann, W. D., and Acuto, O. (2007) A novel pathway down-modulating T cell activation involves HPK1-dependent recruitment of 14-3-3 proteins on SLP-76. J. Exp. Med. 204, 681-691 (Pubitemid 46457089)
24. Newton, K., Matsumoto, M. L., Wertz, I. E., Kirkpatrick, D. S., Lill, J. R., Tan, J., Dugger, D., Gordon, N., Sidhu, S. S., Fellouse, F. A., Komuves, L., French, D. M., Ferrando, R. E., Lam, C., Compaan, D., Yu, C., Bosanac, I., Hymowitz, S. G., Kelley, R. F., and Dixit, V. M. (2008) Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678
25. LeBron, C., Chen, L., Gilkes, D. M., and Chen, J. (2006) Regulation of MDMX nuclear import and degradation by Chk2 and 14-3-3. EMBO J. 25, 1196-1206
26. Liu, Y. C., Elly, C., Yoshida, H., Bonnefoy-Berard, N., and Altman, A. (1996) Activation-modulated association of 14-3-3 proteins with Cbl in T cells. J. Biol. Chem. 271, 14591-14595 (Pubitemid 26190365)
27. Naramura, M., Kole, H. K., Hu, R. J., and Gu, H. (1998) Altered thymic positive selection and intracellular signals in Cbl-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 15547-15552 (Pubitemid 29018736)
28. Yablonski, D., Kuhne, M. R., Kadlecek, T., and Weiss, A. (1998) Uncoupling of nonreceptor tyrosine kinases from PLCγ1 in an SLP-76-deficient T cell. Science 281, 413-416
29. Chuang, H. C., Lan, J. L., Chen, D. Y., Yang, C. Y., Chen, Y. M., Li, J. P., Huang, C. Y., Liu, P. E., Wang, X., and Tan, T. H. (2011) The kinase GLK controls autoimmunity and NF-κB signaling by activating the kinase PKCθ in T cells. Nat. Immunol. 12, 1113-1118
30. Wang, X., Li, J. P., Kuo, H. K., Chiu, L. L., Dement, G. A., Lan, J. L., Chen, D. Y., Yang, C. Y., Hu, H., and Tan, T. H. (2012) Down-regulation of B cell receptor signaling by hematopoietic progenitor kinase 1 (HPK1)-mediated phosphorylation and ubiquitination of activated B cell linker protein (BLNK). J. Biol. Chem. 287, 11037-11048