Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice

Genes and Development

Volumn 8, Issue 1, 1994, Pages 23-32

  Guy, Chantale T ^a   Muthuswamy, Senthil K ^a   Cardiff, Robert D ^b   Soriano, Philippe ^c   Muller, William J ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FRED HUTCHINSON CANCER RESEARCH CENTER   (United States)

Author keywords

c Src; mammary tumorigenesis; metastasis; PyV middle T antigen; signal transduction; transgenic mice

Indexed keywords

PROTEIN TYROSINE KINASE; VIRUS T ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HYPERPLASIA; METASTASIS; MITOGENESIS; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALIA; MAMMARY TUMOR VIRUS; MOUSE MAMMARY TUMOR VIRUS; MUS MUSCULUS; POLYOMAVIRUS; TUMOR VIRUS;

EID: 0027954475     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.8.1.23     Document Type: Article

References (45)

1. Aguzzi, A., E.F. Wagner, R.L. Williams, and S.A. Courtneidge. 1990. Sympathetic hyperplasia and neuroblastomas in transgenic mice expressing polyoma middle T antigen. New Biol. 6: 533-543.
2. Amini, S., V. DeSeau, S. Reddy, D. Shalloway, and J.B. Bolen. 1986. Regulation of pp60 c-src synthesis by inducible RNA complementary to c-src mRNA in polyomavirus-transformed rat cells. Mol. Cell. Biol. 7: 2305-2316.
3. Bautch, V.L., J. Toda, J.A. Hassell, and D. Hanahan. 1987. Endothelial cell tumors develop in transgenic mice carrying the polyomavirus middle T oncogene. Cell 51: 529.
4. Berebbi, M., P.M. Martin, Y. Berthois, A.M. Bernard, and D. Blangy. 1990. Estradiol dependence of the specific mammary tissue targeting of polyoma virus oncogenicity in nude mice. Oncogene 5: 505-509.
5. c-src is a regulatory domain and is involved in complex formation with the middle-T antigen of polyomavirus. Mol. Cell. Biol. 8: 1736-1747.
6. Chirgwin, J.M., A.E. Przybyla, R.J. MacDonald, and W.J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299.
7. Courtneidge, S.A. and A. Hebner. 1987. An 81 kDa protein complexed with middle T antigen nd pp60 c-src; A possible phosphatidylinositol kinase. Cell 50: 1031-1037.
8. Courtneidge, S.A. and A.E. Smith. 1983. Polyoma virus transforming protein associates with the product of the c-src gene. Nature 303: 435-439.
9. Courtneidge, S.A., L. Goutebroze, A. Cartwright, A. Heber, S. Scherneck, and J. Feunteun. 1991. Identification and characterization of the hamster polyomavirus middle T antigen. J. Virol. 6: 3301-3308.
10. Courtneidge, S.A., R. Dhand, D. Pilat, G.M. Twamely, M.D. Waterfield, and M. Roussel. 1993. Activation of src family kinases by colony stimulating factor-1 and their association with its receptor. EMBO J. 12: 934-950.
11. Escot, C., C. Theillet, R. Lidereau, F. Spyvatos, M.H. Champeme, J. Gest, and R. Callahan. 1986. Genetic alteration of the c-myc proto-oncogene (MYC) in human primary breast carcinomas. Proc. Natl. Acad. Sci. 83: 4834-4838.
12. Feinberg, A.P. and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6-13.
13. Grussenmeyer, T., K.Z. Scheidtmann, M.A. Hutchinson, W. Eckhart, and G. Walter. 1985. Complexes of polyoma virus medium T antigen and cellular proteins. Proc. Natl. Acad. Sci. 82: 7952-7954.
14. Guy, C.T., R.D. Cardiff, and W.J. Muller. 1992a. Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12: 954-961.
15. Guy, C.T., M.A. Webster, M. Schaller, T.J. Parson, R.D. Cardiff, and W.J. Muller. 1992b. Expression of the neu proto-oncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. 89: 10578-10582.
16. Huang, A.L., M.C. Ogtrowski, D. Berard, and G.L. Hager. 1981. Glucocorticoid regulation of Ha-MuSV p21 conferred by sequences from mouse mammary tumor virus. Cell 27: 245-255.
17. c-src protein kinase in adult and fetal human tissues. High activities in some sarcomas and mammary carcinomas. Cancer Res. 43: 1696-1702.
18. King, C.R., M.H. Kraus, and S.A. Aaronson. 1985. Amplification of a novel v-erbB-related gene in a human mammary carcinoma. Science 229: 974-976.
19. Kornbluth, S., M. Sudol, and H. Hanafusa. 1987. Association of the polyomavirus middle T antigen with c-yes protein. Nature 325:171-173.
20. Kypta, R.M., A. Hemming, and S.A. Courtneidge. 1988. Identification and characterization of p59 fyn (a src-like protein tyrosine kinase) in normal and polyoma virus transformed cells. EMBO J. 7: 3837-3844.
21. Kypta, R.M., Y. Goldberg, E.T. Ulug, and S.A. Courtneidge. 1990. Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62: 481-492.
22. Melton, D., A.P.A. Krieg, M.R. Rebagliati, T. Maniatis, K. Zinn, and M.R. Green. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12: 7035-7056.
23. Muller, W.J., E. Sinn, P.K. Pattengale, R. Wallace, and P. Leder. 1988. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54: 105-115.
24. Muthuswamy, S.K., P.M. Siegel, D.L. Dankort, M.A. Webster, and W.J. Muller. 1994. Mammary tumors expressing the neu proto-oncogene possess elevated c-src tyrosine kinase activity. Mol. Cell. Biol. 14: (in press).
25. Ottenhoff-Kalff, A.E., G. Rijksen, E.A.C.M. van Beurden, A. Hennipman, A.A. Michels, and G.E.J. Staal. 1992. Characterization of protein tyrosine kinases from human breast cancer: Involvement of the c-src oncogene product. Cancer Res. 52: 4773-4778.
26. Pallas, D.C., L.K. Shahrik, B.L. Martin, S. Jasper, T.B. Miller, D.L. Brautigan, and T.M. Roberts. 1990. Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A. Cell 60: 167-176.
27. Peles, E., S. Bacus, R. Koksi, H.S. Lu, D. Weu, S. Ogolen, R. Ben Levy and Y. Yarden. 1992. Isolation of the Neu/her 2 stimulatory ligand: A 44 kDa glycoprotein that induces differentiation of mammary tumor cells. Cell 69: 205-216.
28. c-src protein kinase activity in human tumor cell lines and tissues. J. Biol. Chem. 261: 13754-13759.
29. Seed, B. and A. Aruffo. 1987. Molecular cloning of the CD2 antigen, the T cell erythrocyte receptor, by rapidimmunoselection procedure. Proc. Natl. Acad. Sci. 84: 3365-3369.
30. Sinn, E., W.J. Muller, P. Pattengale, I. Tepler, R. Wallace, and P. Leder. 1987. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: Synergistic action of oncogenes in vivo. Cell 49: 465-475.
31. Slamon, D.J., G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire. 1987. Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235: 177-182.
32. Slamon, D.J., W. Godolphin, L.A. Jones, J.A. Holt, S.C. Wong, D.E. Keith, W.J. Levin, S.G. Stuart, J. Udore, A. Ullrich, and M.F. Press. 1989. Studies of the HER-2/neu protooncogene in human breast and ovarian cancer. Science 244: 707-712.
33. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702.
34. Southern, E.M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98: 503-517.
35. Sukegawa, J., T. Akatsuka, I. Sugawara, S. Mori, T. Yamamoto, and K. Toyoshima. 1990. Monoclonal antibodies to the amino-terminal sequence of the c-yes gene product as specific probes of its expression. Oncogene 5: 611-614.
36. c-src: A switch for binding of phosphatidylinositol 3-kinase and optimal tumorigenesis. Cell 59: 55-65.
37. Thomas, J.E, A. Aguzzi, P. Soriano, E.F. Wagner, and J. Brugge. 1993. Induction of tumor formation and cell transformation by polyoma middle T antigen in the absence of src. Oncogene 8: 2521-2526
38. Treisman, R., U. Novak, J. Favaloro, and R. Kamen. 1981. Transformation of rat cells by an altered polyoma virus genome expressing only the middle T antigen protein. Nature 292: 595-600.
39. Twamley-Stein, G.M., Pepperkok, R., Ansorge, W., and Courtneidge, S.A.E. 1993. The Src family tyrosine kinases are required for platelet-derived growth factor mediated signal transduction in NIH 3T3 cells. Proc. Natl. Acad. Sci. 90: 7696.
40. Vonderhaar, B.K. and A.E. Greco. 1979. Lobulo-alveolar development of mouse mammary glands is regulated by thyroid hormones. Endocrinology 2: 409-418.
41. Walter, G., R. Ruediger, C. Slaughter, and M. Mumby. 1990. Association of protein phosphatase 2A with polyoma virus medium tumor antigen. Proc. Natl. Acad. Sci. 87: 2521-2525.
42. Wen, D., E. Peles, R. Cupples, S.V. Suggs, S.S. Bacus, Y. Luo, G. Trail, S. Hu, S. Silbiger, R. Ben-Levy, R.A. Koski, H.S. Lu, and Y. Yarden. 1992. Neu differentiation factor: A transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69: 559-572.
43. Whitman, M., D.R. Kaplan, B. Schaffhausen, L. Cantley, and T.M. Roberts. 1985. Association of phosphatidylinositol kinase activity with polyoma middle T antigen competent for transformation. Nature 315: 239-242.
44. Williams, R.L., S.A. Courtneidge, and E.F. Wagner. 1988. Embryonic lethalities and endothelial tumors in chimeric cell mice expressing polyomavirus middle T oncogene. Cell 52: 121-131.
45. Yokota, J., T. Yamamoto, K. Toyoshima, M. Terada, T. Sugimura, H. Battifora, and M.J. Cline. 1986. Amplification of c-erbB-2 oncogene in human adenocarcinomas in vivo. Lancet I: 765-767.