The Fer tyrosine kinase is important for platelet-derived growth factor-BB-induced signal transducer and activator of transcription 3 (STAT3) protein phosphorylation, colony formation in soft agar, and tumor growth in vivo

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15736-15744

  Lennartsson, Johan ^a   Ma, Haisha ^a   Wardega, Piotr ^a   Pelka, Karin ^a,b   Engström, Ulla ^a   Hellberg, Carina ^a,c   Heldin, Carl Henrik ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHOSPHORYLATION; CELL TRANSFORMATION; CYTOPLASMIC TYROSINE KINASE; ENZYMATIC ACTIVITIES; LOW MOLECULAR WEIGHT; PLATELET-DERIVED GROWTH FACTORS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCERS;

ALGAE; AMINO ACIDS; CHEMICAL ACTIVATION; PHOSPHORYLATION; PLATELETS; POLYSACCHARIDES; TISSUE CULTURE; TUMORS;

ENZYMES;

JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE FER; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; STAT3 PROTEIN; STAT5 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DNA SYNTHESIS; DOWN REGULATION; ENZYME ACTIVITY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANIMAL MODELS; GROWTH FACTORS; PROTEIN-TYROSINE KINASE (TYROSINE KINASE); RECEPTOR TYROSINE KINASE; STAT3; TUMOR;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASMS; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR;

EID: 84878419114     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.476424     Document Type: Article

References (33)

1. Fredriksson, L., Li, H., and Eriksson, U. (2004) The PDGF family: four gene products form five dimeric isoforms. Cytokine Growth Factor Rev. 15, 197-204 (Pubitemid 38781045)
2. Heldin, C. H., and Westermark, B. (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316
3. Pawson, T. (1995) Protein modules and signalling networks. Nature 373, 573-580
4. Andrae, J., Gallini, R., and Betsholtz, C. (2008) Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312 (Pubitemid 351717519)
5. Greer, P. (2002) Closing in on the biological functions of Fps/Fes and Fer. Nat. Rev. Mol. Cell Biol. 3, 278-289
6. Jücker, M., McKenna, K., da Silva, A. J., Rudd, C. E., and Feldman, R. A. (1997) The Fes protein-tyrosine kinase phosphorylates a subset of macrophage proteins that are involved in cell adhesion and cell-cell signaling. J. Biol. Chem. 272, 2104-2109 (Pubitemid 27058486)
7. Allard, P., Zoubeidi, A., Nguyen, L. T., Tessier, S., Tanguay, S., Chevrette, M., Aprikian, A., and Chevalier, S. (2000) Links between Fer tyrosine kinase expression levels and prostate cell proliferation. Mol. Cell. Endocrinol. 159, 63-77 (Pubitemid 30067641)
8. Craig, A. W., and Greer, P. A. (2002) Fer kinase is required for sustained p38 kinase activation and maximal chemotaxis of activated mast cells. Mol. Cell. Biol. 22, 6363-6374
9. Voisset, E., Lopez, S., Dubreuil, P., and De Sepulveda, P. (2007) The tyrosine kinase FES is an essential effector of KITD816V proliferation signal. Blood 110, 2593-2599 (Pubitemid 47523183)
10. Zoubeidi, A., Rocha, J., Zouanat, F. Z., Hamel, L., Scarlata, E., Aprikian, A. G., and Chevalier, S. (2009) The Fer tyrosine kinase cooperates with interleukin-6 to activate signal transducer and activator of transcription 3 and promote human prostate cancer cell growth. Mol. Cancer Res. 7, 142-155
11. Itoh, T., Hasegawa, J., Tsujita, K., Kanaho, Y., and Takenawa, T. (2009) The tyrosine kinase Fer is a downstream target of the PLD-PA pathway that regulates cell migration. Sci. Signal. 2, ra52
12. Li, H., Ren, Z., Kang, X., Zhang, L., Li, X., Wang, Y., Xue, T., Shen, Y., and Liu, Y. (2009) Identification of tyrosine-phosphorylated proteins associated with metastasis and functional analysis of FER in human hepatocellular carcinoma cells. BMC Cancer 9, 366
13. Kim, L., and Wong, T. W. (1995) The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell. Biol. 15, 4553-4561
14. Iwanishi, M., Czech, M. P., and Cherniack, A. D. (2000) The protein-tyrosine kinase Fer associates with signaling complexes containing insulin receptor substrate-1 and phosphatidylinositol 3-kinase. J. Biol. Chem. 275, 38995-39000 (Pubitemid 32058911)
15. Frank, D. A. (2007) STAT3 as a central mediator of neoplastic cellular transformation. Cancer Lett. 251, 199-210
16. Kypta, R. M., Goldberg, Y., Ulug, E. T., and Courtneidge, S. A. (1990) Association between the PDGF receptor and members of the Src family of tyrosine kinases. Cell 62, 481-492
17. Craig, A. W., Zirngibl, R., Williams, K., Cole, L. A., and Greer, P. A. (2001) Mice devoid of Fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol. Cell. Biol. 21, 603-613 (Pubitemid 32037378)
18. Silva, C. M. (2004) Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis. Oncogene 23, 8017-8023
19. Rosato, R., Veltmaat, J. M., Groffen, J., and Heisterkamp, N. (1998) Involvement of the tyrosine kinase Fer in cell adhesion. Mol. Cell. Biol. 18, 5762-5770 (Pubitemid 28450527)
20. Snyder, S. P., and Theilen, G. H. (1969) Transmissible feline fibrosarcoma. Nature 221, 1074-1075
21. Mori, S., Rönnstrand, L., Yokote, K., Engström, A., Courtneidge, S. A., Claesson-Welsh, L., and Heldin, C. H. (1993) Identification of two juxtamembrane autophosphorylation sites in the PDGF β-receptor; involvement in the interaction with Src family tyrosine kinases. EMBO J. 12, 2257-2264 (Pubitemid 23194175)
22. Rönnstrand, L., Mori, S., Arridsson, A. K., Eriksson, A., Wernstedt, C., Hellman, U., Claesson-Welsh, L., and Heldin, C. H. (1992) Identification of two C-terminal autophosphorylation sites in the PDGF β-receptor: involvement in the interaction with phospholipase C-γ. EMBO J. 11, 3911-3919
23. Craig, A. W., Zirngibl, R., and Greer, P. (1999) Disruption of coiled-coil domains in Fer protein-tyrosine kinase abolishes trimerization but not kinase activation. J. Biol. Chem. 274, 19934-19942
24. Sangrar, W., Gao, Y., Zirngibl, R. A., Scott, M. L., and Greer, P. A. (2003) The fps/fes proto-oncogene regulates hematopoietic lineage output. Exp. Hematol. 31, 1259-1267 (Pubitemid 37510032)
25. Sangrar, W., Gao, Y., Bates, B., Zirngibl, R., and Greer, P. A. (2004) Activated Fps/Fes tyrosine kinase regulates erythroid differentiation and survival. Exp. Hematol. 32, 935-945 (Pubitemid 39410708)
26. Priel-Halachmi, S., Ben-Dor, I., Shpungin, S., Tennenbaum, T., Molavani, H., Bachrach, M., Salzberg, S., and Nir, U. (2000) Fer kinase activation of STAT3 is determined by the N-terminal sequence. J. Biol. Chem. 275, 28902-28910
27. Taler, M., Shpungin, S., Salem, Y., Malovani, H., Pasder, O., and Nir, U. (2003) Fer is a downstream effector of insulin and mediates the activation of signal transducer and activator of transcription 3 in myogenic cells. Mol. Endocrinol. 17, 1580-1592 (Pubitemid 36930472)
28. Salem, Y., Shpungin, S., Pasder, O., Pomp, O., Taler, M., Malovani, H., and Nir, U. (2005) Fer kinase sustains the activation level of ERK1/2 and increases the production of VEGF in hypoxic cells. Cell. Signal. 17, 341-353 (Pubitemid 39574695)
29. Putzke, A. P., Hikita, S. T., Clegg, D. O., and Rothman, J. H. (2005) Essential kinase-independent role of a Fer-like non-receptor tyrosine kinase in Caenorhabditis elegans morphogenesis. Development 132, 3185-3195 (Pubitemid 41167147)
30. Paukku, K., Valgeirsdóttir, S., Saharinen, P., Bergman, M., Heldin, C. H., and Silvennoinen, O. (2000) Platelet-derived growth factor (PDGF)-induced activation of signal transducer and activator of transcription (STAT) 5 is mediated by PDGF β-receptor and is not dependent on c-Src, Fyn, Jak1 or Jak2 kinases. Biochem. J. 345, 759-766 (Pubitemid 30099109)
31. Aggarwal, B. B., Kunnumakkara, A. B., Harikumar, K. B., Gupta, S. R., Tharakan, S. T., Koca, C., Dey, S., and Sung, B. (2009) Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann. N.Y. Acad. Sci. 1171, 59-76
32. Bowman, T., Garcia, R., Turkson, J., and Jove, R. (2000) STATs in oncogenesis. Oncogene 19, 2474-2488 (Pubitemid 30339203)
33. Bromberg, J. F., Wrzeszczynska, M. H., Devgan, G., Zhao, Y., Pestell, R. G., Albanese, C., and Darnell, J. E., Jr. (1999) Stat3 as an oncogene. Cell 98, 295-303 (Pubitemid 29380565)