Fer tyrosine kinase oligomer mediates and amplifies Src-induced tumor progression

Oncogene

Volumn 35, Issue 4, 2016, Pages 501-512

  Oneyama, C ^a   Yoshikawa, Y ^a   Ninomiya, Y ^a   Iino, T ^a   Tsukita, S ^b   Okada, M ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CSK TYROSINE-PROTEIN KINASE; CYTOSKELETON PROTEIN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; EZRIN; PROTEIN TYROSINE KINASE; PROTO-ONCOGENE PROTEIN C-FES-FPS;

ANIMAL; BAGG ALBINO MOUSE; CELL TRANSFORMATION; COLON TUMOR; DRUG SCREENING; FOCAL ADHESION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; CYTOSKELETAL PROTEINS; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, INBRED BALB C; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84955727090     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.110     Document Type: Article

References (47)

1. Jove R, Hanafusa H. Cell transformation by the viral src oncogene. Annu Rev Cell Biol 1987; 3: 31-56.
2. Brown MT, Cooper JA. Regulation, substrates and functions of src. Biochem Biophys Acta 1996; 1278: 121-149.
3. Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 1991; 351: 69-72.
4. Nada S, Yagi T, Takeda H, Tokunaga T, Nakagawa H, Ikawa Y et al. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 1993; 73: 1125-1135.
5. Okada M. Regulation of the SRC family kinases by Csk. Int J Biol Sci 2012; 8: 1385-1397.
6. Irby RB, Mao Y, Coppola D, Kang J, Loubeau JM, Trudeau W et al. Activating SRC mutation in a subset of advanced human colon cancers. Nat Genet 1999; 21: 187-190.
7. Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene 2000; 19: 5636-5642.
8. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004; 4: 470-480.
9. Hunter T, Sefton BM. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci USA 1980; 77: 1311-1315.
10. Rous P. A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J Exp Med 1911; 13: 397-411.
11. Stehelin D, Varmus HE, Bishop JM, Vogt PK. DNA related to the transforming gene (s) of avian sarcoma viruses is present in normal avian DNA. Nature 1976; 260: 170-173.
12. Takeya T, Feldman RA, Hanafusa H. DNA sequence of the viral and cellular src gene of chickens. 1. Complete nucleotide sequence of an EcoRI fragment of recovered avian sarcoma virus which codes for gp37 and pp60src. J Virol 1982; 44: 1-11.
13. Frame MC. Src in cancer: deregulation and consequences for cell behaviour. Biochem Biophys Acta 2002; 1602: 114-130.
14. Oneyama C, Hikita T, Nada S, Okada M. Functional dissection of transformation by c-Src and v-Src. Genes Cells 2008; 13: 1-12.
15. Hakak Y, Martin GS. Ubiquitin-dependent degradation of active Src. Curr Biol 1999; 9: 1039-1042.
16. Laszlo GS, Cooper JA. Restriction of Src activity by Cullin-5. Curr Biol 2009; 19: 157-162.
17. Oneyama C, Hikita T, Enya K, Dobenecker MW, Saito K, Nada S et al. The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src. Mol Cell 2008; 30: 426-436.
18. Oneyama C, Iino T, Saito K, Suzuki K, Ogawa A, Okada M. Transforming potential of Src family kinases is limited by the cholesterol-enriched membrane microdomain. Mol Cell Biol 2009; 29: 6462-6472.
19. Greer P. Closing in on the biological functions of Fps/Fes and Fer. Nat Rev Mol Cell Biol 2002; 3: 278-289.
20. Itoh T, Hasegawa J, Tsujita K, Kanaho Y, Takenawa T. The tyrosine kinase Fer is a downstream target of the PLD-PA pathway that regulates cell migration. Sci Signal 2009; 2: ra52.
21. Kogata N, Masuda M, Kamioka Y, Yamagishi A, Endo A, Okada M et al. Identification of Fer tyrosine kinase localized on microtubules as a platelet endothelial cell adhesion molecule-1 phosphorylating kinase in vascular endothelial cells. Mol Biol Cell 2003; 14: 3553-3564.
22. Lennartsson J, Ma H, Wardega P, Pelka K, Engstrom U, Hellberg C et al. 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. J Biol Chem 2013; 288: 15736-15744.
23. Allard P, Zoubeidi A, Nguyen LT, Tessier S, Tanguay S, Chevrette M et al. Links between Fer tyrosine kinase expression levels and prostate cell proliferation. Mol Cell Endocrinol 2000; 159: 63-77.
24. Kawakami M, Morita S, Sunohara M, Amano Y, Ishikawa R, Watanabe K et al. FER overexpression is associated with poor postoperative prognosis and cancer-cell survival in non-small cell lung cancer. Int J Clin Exp Pathol 2013; 6: 598-612.
25. Li H, Ren Z, Kang X, Zhang L, Li X, Wang Y et al. Identification of tyrosinephosphorylated proteins associated with metastasis and functional analysis of FER in human hepatocellular carcinoma cells. BMC Cancer 2009; 9: 366.
26. Menges CW, Chen Y, Mossman BT, Chernoff J, Yeung AT, Testa JR. A phosphotyrosine proteomic screen identifies multiple tyrosine kinase signaling pathways aberrantly activated in malignant mesothelioma. Genes Cancer 2010; 1: 493-505.
27. Miyata Y, Kanda S, Sakai H, Greer PA. Feline sarcoma-related protein expression correlates with malignant aggressiveness and poor prognosis in renal cell carcinoma. Cancer Sci 2013; 104: 681-686.
28. Anastassiadis T, Deacon SW, Devarajan K, Ma H, Peterson JR. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat Biotechnol 2011; 29: 1039-1045.
29. Heiska L, Melikova M, Zhao F, Saotome I, McClatchey AI, Carpen O. Ezrin is key regulator of Src-induced malignant phenotype in three-dimensional environment. Oncogene 2011; 30: 4953-4962.
30. Mak H, Naba A, Varma S, Schick C, Day A, SenGupta SK et al. Ezrin phosphorylation on tyrosine 477 regulates invasion and metastasis of breast cancer cells. BMC Cancer 2012; 12: 82.
31. Inoue K, Sone T, Oneyama C, Nishiumi F, Kishine H, Sasaki Y et al. A versatile nonviral vector system for tetracycline-dependent one-step conditional induction of transgene expression. Gene Ther 2009; 16: 1383-1394.
32. Craig AW, Zirngibl R, Greer P. Disruption of coiled-coil domains in Fer protein-tyrosine kinase abolishes trimerization but not kinase activation. J Biol Chem 1999; 274: 19934-19942.
33. Guo C, Stark GR. FER tyrosine kinase (FER) overexpression mediates resistance to quinacrine through EGF-dependent activation of NF-kappaB. Proc Natl Acad Sci USA 2011; 108: 7968-7973.
34. Kim L, Wong TW. The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol Cell Biol 1995; 15: 4553-4561.
35. Kim L, Wong TW. Growth factor-dependent phosphorylation of the actin-binding protein cortactin is mediated by the cytoplasmic tyrosine kinase FER. J Biol Chem 1998; 273: 23542-23548.
36. Ishizawar R, Parsons SJ. c-Src and cooperating partners in human cancer. Cancer Cell 2004; 6: 209-214.
37. Tsukita S, Oishi K, Sato N, Sagara J, Kawai A, Tsukita S. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 1994; 126: 391-401.
38. Tsukita S, Yonemura S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem 1999; 274: 34507-34510.
39. Yu Y, Khan J, Khanna C, Helman L, Meltzer PS, Merlino G. Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat Med 2004; 10: 175-181.
40. Elliott BE, Qiao H, Louvard D, Arpin M. Co-operative effect of c-Src and ezrin in deregulation of cell-cell contacts and scattering of mammary carcinoma cells. J Cell Biochem 2004; 92: 16-28.
41. Craig AW, Zirngibl R, Williams K, Cole LA, Greer PA. Mice devoid of fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol Cell Biol 2001; 21: 603-613.
42. Sangrar W, Gao Y, Scott M, Truesdell P, Greer PA. Fer-mediated cortactin phosphorylation is associated with efficient fibroblast migration and is dependent on reactive oxygen species generation during integrin-mediated cell adhesion. Mol Cell Biol 2007; 27: 6140-6152.
43. Senis YA, Sangrar W, Zirngibl RA, Craig AW, Lee DH, Greer PA. Fps/Fes and Fer non-receptor protein-tyrosine kinases regulate collagen- and ADP-induced platelet aggregation. J Thromb Haemost 2003; 1: 1062-1070.
44. Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 2000; 404: 999-1003.
45. Oneyama C, Morii E, Okuzaki D, Takahashi Y, Ikeda J, Wakabayashi N et al. MicroRNA-mediated upregulation of integrin-linked kinase promotes Src-induced tumor progression. Oncogene 2012; 31: 1623-1635.
46. Lingwood D, Simons K. Detergent resistance as a tool in membrane research. Nat Protoc 2007; 2: 2159-2165.
47. Akagi T, Sasai K, Hanafusa H. Refractory nature of normal human diploid fibroblasts with respect to oncogene-mediated transformation. Proc Natl Acad Sci USA 2003; 100: 13567-13572.