Requirement for both Shc and Phosphatidylinositol 3' kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis

Molecular and Cellular Biology

Volumn 18, Issue 4, 1998, Pages 2344-2359

  Webster, Marc A ^a   Hutchinson, John N ^a   Rauh, Michael J ^a   Muthuswamy, Senthil K ^a   Anton, Martina ^a   Tortorice, Christopher G ^a   Cardiff, Robert D ^a,b   Graham, Frank L ^a   Hassell, John A ^a   Muller, William J ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; VIRUS MIDDLE T ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; BREAST EPITHELIUM; BREAST HYPERPLASIA; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VIRUS CARCINOGENESIS;

ANIMALIA; MUS MUSCULUS; POLYOMAVIRUS;

EID: 0031948388     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.4.2344     Document Type: Article

References (57)

1. Addison, C., T. Braciak, R. Ralston, W. Muller, J. Gauldie, and F. L. Graham. 1995. Intratumoral injection of an adenovirus expressing interleukin-2 induces regression and immunity in a murine breast cancer model. Proc. Natl. Acad. Sci. USA 92:8522-8526.
2. Anton, M., and F. Graham. 1995. Site-specific recombination mediated by an adenovirus vector expressing the Cre recombinase protein: a molecular switch for control of gene expression. J. Virol. 69:4600-4606.
3. Brizuela, L., E. T. Ulug, M. A. Jones, and S. A. Courtneidge. 1995. Induction of interleukin-2 transcription by the hamster polyoma virus middle T antigen: a role for Fyn in T cell signal transduction. Eur. J. Immunol. 25:385-393.
4. Bronson, R., C. Dawe, J. Carrol, and T. Benjamin. 1997. Tumor induction by a transformation-defective polyoma virus mutant blocked in signaling through Shc. Proc. Natl. Acad. Sci. USA 94:7954-7958.
5. Campbell, K. S., E. Ogris, B. Burke, W. Su, K. R. Auger, B. J. Druker, B. S. Schaffhausen, T. M. Roberts, and D. C. Pallas. 1994. Polyoma middle tumor antigen interacts with SHC protein via the NPTY (Asn-Pro-Thr-Tyr) motif in middle tumor antigen. Proc. Natl. Acad. Sci. USA 91:6344-6348.
6. Cardiff, R. D., and W. J. Muller. 1993. Transgenic mouse models of mammary tumorigenesis. Cancer Surv. 16:97-113.
7. Chang, H. W., M. Akoi, D. Fruman, K. R. Auger, A. Bellacosa, P. N. Tsi, L. W. Cantley, T. M. Roberts, and P. K. Vogt. 1997. Transformation of chicken cells by the gene encoding the catalytic subunit of PI-3-kinase. Science 276:1848-1850.
8. Cheng, S. H., R. Harvey, P. C. Espino, K. Semba, T. Yamamota, K. Toyoshima, and A. E. Smith. 1988. Peptide antibodies to the human c-fyn gene product demonstrate pp59 c-fyn is capable of complex formation with the middle-T antigen of polyomavirus. EMBO J. 7:3845-3855.
9. Cheung, A. T. W., L. J. T. Young, C. Y. Chao, P. C. Y. Chien, A. Ndoye, P. A. Barry, W. J. Muller, and R. D. Cardiff. 1997. Microcirculation and metstasis in a new mouse mammary tumor model system. Int. J. Oncol. 11:69-77.
10. Chirgwin, J. M., A. E. Przybyla, R. J. MacDonald, and W. J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources rich in ribonuclease. Biochemistry 18:5294-5299.
11. Courtneidge, S. A., and A. Hebner. 1987. An 81 kDa protein complexed with middle T antigen and pp60c-src: a possible phosphatidylinositol kinase. Cell 50:1031-1037.
12. Courtneidge, S. A., and A. E. Smith. 1983. Polyomavirus transforming protein associates with the product of the c-src cellular gene. Nature 303:435-439.
13. Dahl, J., R. Freund, J. Blenis, and T. J. Benjamin. 1996. Studies of partially transforming polyomavirus mutants establish a role for the phosphaditylinositol-3′-kinase in activation of the pp70 S6 kinase. Mol. Cell. Biol. 16: 2728-2735.
14. Dilworth, S. M., C. E. P. Brewster, M. D. Jones, L. Lanfrancone, G. Pelicci, and P. G. Pelicci. 1994. Transformation by polyomavirus middle T-antigen involves the binding and tyrosine phosphorylation of Shc. Nature 367:87-90.
15. Franke, T. F., S.-I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
16. Freund, R., C. J. Dawe, J. P. Carrol, and T. L. Benjamin. 1992. Changes m frequency, morphology and behaviour of tumors induced in mice by a Polyomavirus mutant with a specifically altered oncogene. Am. J. Pathol. 141: 1409-1425.
17. Gaviereli, Y. S., and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
18. Gotoh, N., A. Tojo, and M. Shibuya. 1996. A novel pathway from phosphorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL-3. EMBO J. 15:6197-6204.
19. Guy, C. T., R. D. Cardiff, and W. J. Muller. 1992. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12:954-961.
20. Guy, C. T., S. K. Muthuswamy, R. A. Cardiff, P. Soriano, and W. J. Muller. 1994. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes Dev. 8:23-32.
21. Guy, C. T., M. A. Webster, M. Schaller, T. J. Parsons, R. D. Cardiff, and W. J. Muller. 1992. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. USA 89:10578-10582.
22. Jelinek, M. A., and J. A. Hassell. 1992. Reversion of middle T antigen-transformed Rat-2 cells by Krev-1: implications for the role of p21 c-ras in polyomavirus-mediated transformation. Oncogene 7:1687-1698.
23. Kennedy, S. G., A. J. Wagner, S. D. Conzen, J. Jordan, A. Bellacosa, P. N. Tsichilis, and N. Hay. 1997. The PI 3′ kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701.
24. Khwaja, A., P. Rodriguez-Viciana, S. Wennstrom, P. H. Warne, and J. Downward. 1997. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:2783-2793.
25. Kiefer, F., I. Anhauser, P. Soriano, A. Aguzzi, S. A. Courtneidge, and E. F. Wagner. 1994. Endothelial cell transformation by polyomavirus middle T antigen in mice lacking Src-related kinases. Curr. Biol. 4:100-109.
26. Klippel, A., M. Kavanaugh, D. Pot, and L. T. Williams. 1997. A specific product of phosphahadityl 3′-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:338-344.
27. Kornbluth, S., M. Sudol, and H. Hanafusa. 1987. Association of the polyomavirus middle T antigen with the c-yes protein. Nature 325:171-173.
28. Kotani, K., K. Yunezawa, K. Hara, H. Ueda, Y. Kitmura, H. Sakaue, B. Calas, F. Grigorescu, M. Nishiyama, M. D. Waterfield, and M. Kasuga. 1994. Involvement of phosphoinositide 3-kinase in insulin-or IGF-1-induced membrane ruffling. EMBO J. 13:2213-2221.
29. Kulik, G., A. Klippel, and M. J. Weber. 1997. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphadityl 3-kinase, and Akt. Mol. Cell. Biol. 17:1595-1606.
30. Kypta, R. M., A. Hemming, and S. A. Courtneidge. 1988. Identification and characterization of p59 fyn (a Src like protein kinase) in normal and polyomavirus transformed cells. EMBO J. 7:3837-3844.
31. Markland, W., and A. E. Smith. 1987. Mutants of polyomavirus middle-T antigen. Biochim. Biophys. Acta 907:299-321.
32. Matsui, Y., S. Halter, J. T. Holt, B. L. Hogan, and R. J. Coffey. 1990. Development of mammary hyperplasia and neoplasia in MMTV-TGFα transgenic mice. Cell 61:1147-1155.
33. 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.
34. 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.
35. Naik, P., J. Karrin, and D. Hanahan. 1996. The rise and fall of apoptosis during multistage tumorigenesis: down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev. 10:2105-2116.
36. Pallas, D. C., H. Fu, L. C. Haehnel, W. Weller, R. J. Collier, and T. M. Roberts. 1994. Association of the polyomavirus middle tumor antigen with 14-3-3 proteins. Science 265:535-537.
37. 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.
38. Pawson, T. 1995. Protein modules and signalling networks. Nature 373:573-580.
39. Pringent, S. A., and W. J. Gullick. 1994. Identification of the c-c-erbB-3 binding sites for phosphatidylinositol 3′-kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J. 13:2831-2841.
40. Rauh, M. J., C. Tortorice, R. Daly, and W. J. Muller. 1997. Unpublished observations.
41. Rodriguez-Viciana, P., P. H. Warne, A. Khaja, B. M. Marte, D. J. Pappin, P. Das, M. Waterfield, A. Ridley, and J. Downward. 1997. Role of the phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskelton by Ras. Cell 89:457-468.
42. Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P. G. Pelicci, J. Schlessinger, and T. Pawson. 1992. Association of the Shc and Grb2/sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689-692.
43. Sinn, E., W. 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.
44. Soltoff, S., P. K. Carraway III, S. A. Pringent, W. Gullick, and L. Cantley. 1994. ErbB3 is involved in activation of phosphaditylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14:3550-3558.
45. Southern, E. M. 1975. Detection of specific sequences among different DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
46. Stokoe, D., and F. McCormick. 1997. Activation of c-Raf-1 by Ras and Src through different mechanisms: activation in vivo and in vitro. EMBO J. 16:2384-2396.
47. Su, W., W. Liu, B. S. Schaffhausen, and T. M. Roberts. 1995. Association of polyomavirus middle tumor antigen with phospholipase Gγ1. J. Biol. Chem. 270:12331-12334.
48. Surh, C. D., and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:73-77.
49. Talmage, D. A., R. Freund, D. T. Young, J., Dahl, and T. Benjamin. 1989. Phosphorylation of middle T by pp60c-src: a switch for binding of the phosphadityl inositol 3-kinase and optimal tumorigenesis. Cell 59:55-66.
50. van der Geer, P., S. Wiley, G. D. Gish, and T. Pawson. 1996. The Shc adaptor protein is highly phosphorylated at conserved twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr. Biol. 6:1435-1444.
51. Vonderhaar, B., and A. E. Greco. 1979. Lohulo-alveolar development of mouse mammary glands is regulated by thyroid hormones. Endocrinology 2:409-418.
52. 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. USA 87:2521-2525.
53. Webster, M. A., R. D. Cardiff, and W. J. Muller. 1995. Induction of mammary epithelial hyperplasias and mammary tumors in transgenic mice expressing a mammary murine tumor virus/activated c-src fusion gene. Proc. Natl. Acad. Sci. USA 92:7849-7853.
54. Webster, M. A., J. N. Hutchinson, and W. J. Muller. 1997. Unpublished observations.
55. Whitman, M., D. R. Kaplan, B. Schaffhausen, L. Cantley, and T. M. Roberts. 1985. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315:239-242.
56. Yao, R., and G. M. Cooper. 1995. Requirement for phosphaditylinositol-3 kinase in prevention of apoptosis by nerve growth factor. Science 267:2003-2006.
57. Yi, X., J. Peterson, and R. Freund. 1997. Transformation and tumorigenic properties of a mutant polyomavirus containing a middle T antigen defective in Shc binding. J. Virol. 71:6279-6286.