Sprouty-4 negatively regulates cell spreading by inhibiting the kinase activity of testicular protein kinase

Biochemical Journal

Volumn 387, Issue 3, 2005, Pages 627-637

  Tsumura, Yoshikazu ^a   Toshima, Jiro ^a   Leeksma, Onno C ^b   Ohashi, Kazumasa ^a   Mizuno, Kensaku ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Cell spreading; Cofilin; Laminin; Mitogen activated protein kinase (MAP kinase); Sprouty; Testicular protein kinase (TESK)

Indexed keywords

BACTERIA; BIOLOGICAL MEMBRANES; CELLS; FATTY ACIDS; FLUORESCENCE; LIPIDS; LIVING SYSTEMS STUDIES; MICROSCOPIC EXAMINATION; PROTEINS;

CELL SPREADING; PHOSPHORYLATES; PROTEIN KINASE; SPROUTY-4;

ENZYMES;

ALANINE; COFILIN; INTEGRIN; LAMININ; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PROTEIN SPROUTY 4; TESTICULAR PROTEIN KINASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SPREADING; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL LINE; CELL MOVEMENT; GENE EXPRESSION REGULATION; NERVE TISSUE PROTEINS; PROTEIN-SERINE-THREONINE KINASES;

EID: 18844451747     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041181     Document Type: Article

References (34)

1. Toshima, J., Ohashi, K., Okano, I., Nunoue, K., Kishioka, M., Kuma, K., Miyata, T., Hirai, M., Baba, T. and Mizuno, K. (1995) Identification and characterization of a novel protein kinase, TESK1, specifically expressed in testicular germ cells. J. Biol. Chem. 270, 31331-31337
2. Toshima, J., Koji, T. and Mizuno, K. (1998) Stage-specific expression of lestis-specific protein kinase 1 (TESK1) in rat spermatogenic cells. Biochem. Biophys. Res. Commun. 249, 107-112
3. Toshima, J., Tanaka, T. and Mizuno, K. (1999) Dual specificity protein kinase activity of testis-specific protein kinase 1 and its regulation by autophosphorylation ol serine-215 within the activation loop. J. Biol. Chem. 274, 12171-12176
4. Toshima, J., Toshima, J. Y., Suzuki, M., Noda, T. and Mizuno, K. (2001) Cell-type-specific expression of a TESK1 promoter-linked lacZ gene in transgenic mice. Biochem. Biophys. Res. Commun. 286, 566-573
5. Okano, I., Hiraoka, J., Otera, H., Nunoue, K., Ohastii, K., Iwashita, S., Hirai, M. and Mizuno, K. (1995) Identification and characterization of a novel family of serine/threonine kinases containing two N-terminal LIM motifs. J. Biol. Chem. 270, 31321-31330
6. Bamburg, J. R. (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185-230
7. Pantaloni, D., Le Clainche, C. and Carlier, M. F. (2001) Mechanism of actin-based motility. Science 292, 1502-1506
8. Yang, N., Higuchi. O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E. and Mizuno, K. (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature (London) 393, 809-812
9. Arber, S., Bardayannis, F. A., Hanser, H., Schneider, C., Stanyon, C. A., Bernard, O. and Caroni, P. (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature (London) 393, 805-809
10. Toshima, J., Toshima, J. Y., Amano, T., Yang, N., Narumiya, S. and Mizuno, K. (2001) Colilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol. Biol. Cell 12, 1131-1145
11. Amano, T., Tanabe, K., Eto, T., Narumiya, S. and Mizuno, K. (2001) LIM-kinase 2 induces formation of stress fibres, local adhesions and membrane blebs, dependent on its activation by Rho-associated kinase-catalysed phosphorylation at threonine-505. Biochem. J. 354, 149-159
12. Toshima, J. Y., Toshima, J., Watanabe, T. and Mizuno, K. (2001) Binding ol 14-3-3β regulates the kinase activity and subcellular localization of testicular protein kinase 1. J. Biol. Chem. 276, 43471-43481
13. Edwards, D. C., Sanders, L. C., Bokoch, G. M. and Gill, G. N. (1999) Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1, 253-259
14. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285, 895-898
15. Ohashi, K., Nagata, K., Maekawa, M., Ishizaki, T., Narumiya, S. and Mizuno, K. (2000) Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J. Biol. Chem. 275, 3577-3582
16. Leeksma, O. C., Van Tanja, A. E., Tsumura, Y., Toshima, J., Eldering, E., Kroes, W. G., Mellink, C., Spaargaren, M., Mizuno, K., Pannekoek, H. et al. (2002) Human sprouty 4, a new ras antagonist on 5q31, interacts with the dual specificity kinase TESK1. Eur. J. Biochem. 269, 2546-2556
17. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y and Krasnow, M. A. (1998) Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell (Cambridge, Mass.) 92, 253-263
18. Casci, T., Vinos, J. and Freeman, M. (1999) Sprouty, an intracellular inhibitor of Ras signaling. Cell (Cambridge, Mass.) 96, 655-665
19. Kramer, S., Okabe, M., Hacohen, N., Krasnow, M. A. and Hiromi, Y. (1999) Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126, 2515-2525
20. Reich, A., Sapir, A. and Shilo, B. (1999) Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126, 4139-4147
21. Minowada, G., Jarvis, L. A., Chi, C. L., Neuouser, A., Sun, X., Hacohen, N., Krasnow, M. A. and Martin, G. R. (1999) Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475
22. Guy, G. R., Wong, E. S. M., Yusoff, P., Chandramouli, S., Lo, T. L., Lim, J. and Fong, C. W. (2003) Sprouty: how does the branch manager work? J. Cell Sci. 116, 3061-3068
23. Lee, S. H., Schloss, D. J., Jarvis, L., Krasnow, M. A. and Swain, J. L. (2001) Inhibition of angiogenesis by a mouse sprouty protein. J. Biol. Chem. 276, 4128-4133
24. Impagnatiello, M. A., Weitzer, S., Cannon, G., Compagni, A., Coton, M. and Christofori, G. (2001) Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152, 1087-1098
25. Yigzaw, Y., Cartin, L., Pierre, S., Scholich, K. and Patel, T. B. (2001) The C terminus of sprouty is important for modulation of cellular migration and proliferation. J. Biol. Chem. 276, 22742-22747
26. Sasaki, A., Taketomi, T., Wakioka, T., Kato, R. and Yoshimura, A. (2001) Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor-but not epidermal growth factor-induced ERK activation. J. Biol. Chem. 276, 36804-36808
27. Gross, I., Bassit, B., Benezra, M. and Licht, J. D. (2001) Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J. Biol. Chem. 276, 46460-46468
28. Yusoff, P., Lao, D. H., Ong, S. H., Wong, E. S., Lim, J., Lo, T. L., Leong, H. F., Fong, C. W. and Guy, G. R. (2002) Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J. Biol. Chem. 277, 3195-3201
29. Hanafusa, H., Torii, S., Yasunaga, T. and Nishida, E. (2002) Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 14, 850-858
30. Sasaki, A., Taketomi, T., Kato, R., Saeki, K., Nonami, A., Sasaki, M., Kuriyama, M., Saito, N., Shibuya, M. and Yoshimura, A. (2003) Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat. Cell Biol. 5, 427-432
31. Teflt, J. D., Lee, M., Smith, S., Leinwand, M., Zhao, J., Bringas, Jr, P., Crowe, D. L. and Warburton, D. (1999) Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr. Biol. 9, 219-222
32. Yigzaw, Y., Poppleton, H. M., Sreejayan, N., Hassid, A. and Patel, T. (2003) Protein-tyrosine phosphatase-1B (PTP1B) mediates the anti-migratory actions of Sprouty. J. Biol. Chem. 278, 284-288
33. Nishita, M., Aizawa, H. and Mizuno, K. (2002) Stromal cell-derived factor 1α activates LIM kinase 1 and induces cofilin phosphorylation for T-cell chemotaxis. Mol. Cell. Biol. 22, 774-783
34. Toshima, J., Toshima, J. Y., Takeuchi, K., Mori, R. and Mizuno, K. (2001) Cofilin phosphorylation and actin reorganizalion activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells. J. Biol. Chem. 276, 31449-31458