HPK1 competes with ADAP for SLP-76 binding and via Rap1 negatively affects T-cell adhesion

European Journal of Immunology

Volumn 40, Issue 11, 2010, Pages 3220-3225

  Patzak, Irene M ^a,d   Königsberger, Sebastian ^a   Suzuki, Akira ^b   Mak, Tak W ^c   Kiefer, Friedemann ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF TORONTO   (Canada)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

ADAP; HPK1; LFA 1; Rap1; SLP 76

Indexed keywords

CELL ENZYME; HEMATOPOIETIC PROGENITOR KINASE 1; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PHOSPHOPROTEIN; RAP1 PROTEIN; SLP 76 PROTEIN; UNCLASSIFIED DRUG; FYB PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SERINE THREONINE KINASE; RIAM PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SKAP55 PROTEIN, MOUSE; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL POLARITY; CELL SPREADING; CONTROLLED STUDY; DEGRANULATION; ENZYME BINDING; ENZYME REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL ADHESION; CELL MEMBRANE; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; MULTIPROTEIN COMPLEXES; PHOSPHOPROTEINS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RAP1 GTP-BINDING PROTEINS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 79952108877     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040313     Document Type: Article

References (29)

1. Koretzky, G. A., Abtahian, F. and Silverman, M. A., SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond. Nat. Rev. Immunol. 2006. 6: 67-78.
2. Acuto, O., Di Bartolo, V. and Micheli, F., Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 2008. 8: 699-712.
3. Menasche, G., Kliche, S., Bezman, N. and Schraven, B., Regulation of T-cell antigen receptor-mediated inside-out signaling by cytosolic adapter proteins and Rap1 effector molecules. Immunol. Rev. 2007. 218: 82-91.
4. Wang, H. and Rudd, C. E., SKAP-55, SKAP-55-related and ADAP adaptors modulate integrin-mediated immune-cell adhesion. Trends Cell. Biol. 2008. 18: 486-493.
5. Kliche, S., Breitling, D., Togni, M., Pusch, R., Heuer, K., Wang, X., Freund, C. et al., The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol. Cell. Biol. 2006. 26: 7130-7144.
6. Menasche, G., Kliche, S., Chen, E. J., Stradal, T. E., Schraven, B. and Koretzky, G., RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation. Mol. Cell. Biol. 2007. 27: 4070-4081.
7. Raab, M., Wang, H., Lu, Y., Smith, X., Wu, Z., Strebhardt, K., Ladbury, J. E. and Rudd, C. E., T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity 2010. 32: 541-556.
8. Kinashi, T., Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 2005. 5: 546-559.
9. Medeiros, R. B., Dickey, D. M., Chung, H., Quale, A. C., Nagarajan, L. R., Billadeau, D. D. and Shimizu, Y., Protein kinase D1 and the beta 1 integrin cytoplasmic domain control beta 1 integrin function via regulation of Rap1 activation. Immunity 2005. 23: 213-226.
10. Katagiri, K., Imamura, M. and Kinashi, T., Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat. Immunol. 2006. 7: 919-928.
11. Kiefer, F., Tibbles, L. A., Anafi, M., Janssen, A., Zanke, B. W., Lassam, N., Pawson, T. et al., HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J. 1996. 15: 7013-7025.
12. Liou, J., Kiefer, F., Dang, A., Hashimoto, A., Cobb, M. H., Kurosaki, T. and Weiss, A., HPK1 is activated by lymphocyte antigen receptors and negatively regulates AP-1. Immunity 2000. 12: 399-408.
13. Hu, M. C., Qiu, W. R., Wang, X., Meyer, C. F. and Tan, T. H., Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev. 1996. 10: 2251-2264.
14. Arnold, R., Liou, J., Drexler, H. C., Weiss, A. and Kiefer, F., Caspase-mediated cleavage of hematopoietic progenitor kinase 1 (HPK1) converts an activator of NFkappaB into an inhibitor of NFkappaB. J. Biol. Chem. 2001. 276: 14675-14684.
15. Arnold, R., Patzak, I. M., Neuhaus, B., Vancauwenbergh, S., Veillette, A., Van Lint, J. and Kiefer, F., Activation of hematopoietic progenitor kinase 1 involves relocation, autophosphorylation, and transphosphorylation by protein kinase D1. Mol. Cell. Biol. 2005. 25: 2364-2383.
16. Yu, J., Riou, C., Davidson, D., Minhas, R., Robson, J. D., Julius, M., Arnold, R. et al., Synergistic regulation of immunoreceptor signaling by SLP-76-related adaptor Clnk and serine/threonine protein kinase HPK-1. Mol. Cell. Biol. 2001. 21: 6102-6112.
17. Tsuji, S., Okamoto, M., Yamada, K., Okamoto, N., Goitsuka, R., Arnold, R., Kiefer, F. and Kitamura, D., B cell adaptor containing src homology 2 domain (BASH) links B cell receptor signaling to the activation of hematopoietic progenitor kinase 1. J. Exp. Med. 2001. 194: 529-539.
18. Sauer, K., Liou, J., Singh, S. B., Yablonski, D., Weiss, A. and Perlmutter, R. M., Hematopoietic progenitor kinase 1 associates physically and functionally with the adaptor proteins B cell linker protein and SLP-76 in lymphocytes. J. Biol. Chem. 2001. 276: 45207-45216.
19. Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N. et al., A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J. Exp. Med. 2007. 204: 681-691.
20. Schulze-Luehrmann, J., Santner-Nanan, B., Jha, M. K., Schimpl, A., Avots, A. and Serfling, E., Hematopoietic progenitor kinase 1 supports apoptosis of T lymphocytes. Blood 2002. 100: 954-960.
21. Brenner, D., Golks, A., Kiefer, F., Krammer, P. H. and Arnold, R., Activation or suppression of NFkappaB by HPK1 determines sensitivity to activationinduced cell death. EMBO J. 2005. 24: 4279-4290.
22. Shui, J. W., Boomer, J. S., Han, J., Xu, J., Dement, G. A., Zhou, G. and Tan, T. H., Hematopoietic progenitor kinase 1 negatively regulates T cell receptor signaling and T cell-mediated immune responses. Nat. Immunol. 2007. 8: 84-91.
23. Sawasdikosol, S., Russo, K. M. and Burakoff, S. J., Hematopoietic progenitor kinase 1 (HPK1) negatively regulates prostaglandin E2-induced fos gene transcription. Blood 2003. 101: 3687-3689.
24. Nagata, Y., Kiefer, F., Watanabe, T. and Todokoro, K., Activation of hematopoietic progenitor kinase-1 by erythropoietin. Blood 1999. 93: 3347-3354.
25. Ensenat, D., Yao, Z., Wang, X. S., Kori, R., Zhou, G., Lee, S. C. and Tan, T. H., A novel src homology 3 domain-containing adaptor protein, HIP-55, that interacts with hematopoietic progenitor kinase 1 [published erratum appears in J Biol Chem 2000 May 5;275(18):14004]. J. Biol. Chem. 1999. 274: 33945-33950.
26. Le Bras, S., Foucault, I., Foussat, A., Brignone, C., Acuto, O. and Deckert, M., Recruitment of the actin-binding protein HIP-55 to the immunological synapse regulates T cell receptor signaling and endocytosis. J. Biol. Chem. 2004. 279: 15550-15560.
27. Mueller, K. L., Thomas, M. S., Burbach, B. J., Peterson, E. J. and Shimizu, Y., Adhesion and degranulation-promoting adapter protein (ADAP) positively regulates T cell sensitivity to antigen and T cell survival. J. Immunol. 2007. 179: 3559-3569.
28. Letschka, T., Kollmann, V., Pfeifhofer-Obermair, C., Lutz-Nicoladoni, C., Obermair, G. J., Fresser, F., Leitges, M. et al., PKC-theta selectively controls the adhesion-stimulating molecule Rap1. Blood 2008. 112: 4617-4627.
29. Alzabin, S., Pyarajan, S., Yee, H., Kiefer, F., Suzuki, A., Burakoff, S. and Sawasdikosol, S., Hematopoietic progenitor kinase 1 is a critical component of prostaglandin E2-mediated suppression of the anti-tumor immune response. Cancer Immunol. Immunother. 2010. 59: 419-429.