DNA tumor viruses and Src family tyrosine kinases, an intimate relationship

Virology

Volumn 227, Issue 2, 1997, Pages 271-280

  Messerschmitt, Anja S ^a   Dunant, Nicolas ^a   Ballmer Hofer, Kurt ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE;

CARCINOGENESIS; CONTROLLED STUDY; DNA TUMOR VIRUS; DNA VIRUS; HERPES VIRUS; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; VIRUS CELL INTERACTION;

DNA VIRUSES; HERPES; HERPESVIRIDAE; POLYOMAVIRUS; TUMOR VIRUS;

EID: 0031579241     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1996.8316     Document Type: Article

References (100)

1. Abrams, C. S., and Zhao, W. (1995). SH3 domains specifically regulate kinase activity of expressed Src family proteins. J. Biol. Chem. 270, 333-339.
2. Albrecht, J.-C., Nicholas, J., Biller, D., Cameron, K. R., Biesinger, B., Newman, C., Wittmann, S., Craxton, M. A., Coleman, H., Fleckenstein, B., and Honess, R. W. (1992). Primary structure of the Herpesvirus saimiri genome. J. Virol. 66, 5047-5058.
3. 2 signalling motif found in the cytoplasmic segments of the bovine leukaemia virus envelope protein and Epstein-Barr virus latent membrane protein 2A can elicit early and late lymphocyte activation events. EMBO J. 12, 5105-5112.
4. Biesinger, B., Müller-Fleckenstein, I., Simmer, B., Lang, G., Wittmann, S., Platzer, E., Desrosiers, R. C., and Fleckenstein, B. (1992). Stable growth transformation of human T lymphocytes by Herpesvirus saimiri. Proc. Natl. Acad. Sci. USA 89, 3116-3119.
5. lck in transformed cells. J. Biol. Chem. 270, 4729-4734.
6. Bolen, J. B., Thiele, C. J., Israel, M. A., Yonemoto, W., Lipsich, L. A., and Brugge, J. S. (1984). Enhancement of cellular src gene product associated tyrosyl kinase activity following polyoma virus infection and transformation. Cell 38, 767-777.
7. c-src interactions in polyomavirus-transformed rat cells. J. Virol. 61, 3299-3305.
8. Brizuela, L., Ulug, E. T., Jones, M. A., and Courtneidge, S. A. (1995). Induction of interleukin-2 transcription by the hamster polyomavirus middle T antigen: A role for Fyn in T cell signal transduction. Eur. J. Immunol. 25, 385-393.
9. Bröker, B. M., Tsygankov, A. Y., Muller Reckenstein, I., Guse, A. H., Chitaev, N. A., Biesinger, B., Fleckenstein, B., and Emmrich, F. (1993). Immortalization of human T cell clones by Herpesvirus saimiri. Signal transduction analysis reveals functional CD3, CD4, and IL-2 receptors. J. Immunol. 151, 1184-1192.
10. Brooks, L., Yao, Q. Y., Rickinson, A. B., and Young, P. G. (1992). Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: Coexpression of EBNA1, LMP1, and LMP2 transcripts. J. Virol. 66, 2689-2697.
11. Burkhardt, A. L., Bolen, J. B., Kieff, E., and Longnecker, R. (1992). An Epstein-Barr virus transformation-associated membrane protein interacts with src family tyrosine kinases. J. Virol. 66, 5161-5167.
12. Busson, P., McCoy, R., Sadler, R., Gilligan, K., Tursz, T., and Raab-Traub, N. (1992). Consistent transcription of the Epstein-Barr virus LMP2 gene in nasopharyngeal carcinoma. J. Virol. 66, 3257-3262.
13. Campbell, K. S., Ogris, E., Burke, B., Su, W., Auger, K. R., Druker, B. J., Schaffhausen, B. S., Roberts, T. M., and Pallas, D. C. (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.
14. Campbell, K. S., Auger, K. R., Hemmings, B. A., Roberts, T. M., and Pallas, D. C. (1995). Identification of regions in polyomavirus middle T and small t antigens important for association with protein phosphatase 2A. J. Virol. 69, 3721-3728.
15. Carlin, C. R., Tollefson, A. E., Brady, H. A., Huffman, B. L., and Wold, W. S. M. (1989). Epidermal growth factor receptor is down-regulated by a 10,400 MW protein encoded by the E3 region of adenovirus. Cell 57, 135-144.
16. c-src associated with polyomavirus middle tumor antigen. Mol. Cell. Biol. 6, 1562-1570.
17. Cayla, X., Ballmer-Hofer, K., Merlevede, W., and Goris, J. (1993). Phosphatase 2A associated with polyomavirus small-T or middle-T antigen is an okadaic acid-sensitive tyrosyl phosphatase. Eur. J. Biochem. 214, 281-286.
18. c-fyn is capable of complex formation with the middle-T antigen of polyomavirus. EMBO J. 7, 3845-3855.
19. 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.
20. c-src the middle T antigen of polyomavirus. Curr. Top. Microbiol. Immunol. 144, 109-120.
21. Cheng, S. H., Espino, P. C., Marshall, J., Harvey, R., and Smith, A. E. (1990). Stoichiometry of cellular and viral components in the polyomavirus middle-T antigen-tyrosine kinase complex. Mol. Cell. Biol. 10, 5569-5574.
22. c-src kinase by middle T antigen binding or by dephosphorylation. EMBO J. 4, 1471-1477.
23. Courtneidge, S. A., Goutebroze, L., Cartwright, A., Heber, A., Scherneck, S., and Feunteun, J. (1991). Identification and characterization of the hamster polyomavirus middle T antigen. J. Virol. 65, 3301-3308.
24. Courtneidge, S .A., Fumagalli, S., Koegl, M., Superti Furga, G., and Twamley, S. G. M. (1993). The Src family of protein tyrosine kinases: Regulation and functions. Development, 57-64.
25. Courtneidge, S. A., and Smith, A. E. (1983). Polyoma virus transforming protein associates with the product of the c-src cellular gene. Nature 303, 435-439.
26. c-src. EMBO J. 3, 585-591.
27. Cox, L. S., and Lane, D. P. (1995). Tumour suppressors, kinases and clamps: How p53 regulates the cell cycle in response to DNA damage. BioEssays 17, 501-508.
28. Dalianis, T. (1990). Studies on the polyoma virus tumor-specific transplantation antigen (TSTA). Adv. Cancer Res. 55, 57-85.
29. Delmas, V., Bastien, C., Scherneck, S., and Feunteun, J. (1985). A new member of the polyomavirus family: The hamster papovavirus complete nucleotide sequence and transformation properties. EMBO J. 4, 1279-1286.
30. Dilworth, S. M., Brewster, C. E., Jones, M. D., Lanfrancone, L., Pelicci, G., and Pelicci, P. G. (1994). Transformation by polyoma virus middle T-antigen involves the binding and tyrosine phosphorylation of Shc. Nature 367, 87-90.
31. Dilworth, S. M. (1995). Polyoma virus middle T antigen: Meddler or mimic? Trends Microbiol. 3, 31-35.
32. c-src or protein phosphatase 2A by polyomavirus middle T antigen. J. Virol. 67, 2235-2244.
33. Dunant, N. M., Senften, M., and Ballmer-Hofer, K. (1996). Polyomavirus middle-T antigen associates with the kinase domain of Src-related tyrosine kinases. J. Virol. 70, 1323-1330.
34. Eck, M. J., Atwell, S. K., Shoelson, S. E., and Harrison, S. C. (1994). Structure of the regulatory domains of the Src-family tyrosine kinase Lck. Nature 368, 764-769.
35. Eick, D., and Hermeking, H. (1994). Viruses as pacemakers in the evolution of defence mechanisms against cancer. Curr. Biol. 4, 100-109.
36. Erpel, T., and Courtneidge, S. A. (1995). Src family protein tyrosine kinases and cellular signal transduction pathways. Curr. Opin. Cell Biol. 7, 176-182.
37. Freund, R., Sotnikov, A., Bronson, R. T., and Benjamin, T. L. (1992). Polyoma virus middle T is essential for virus replication and persistence as well as for tumor induction in mice. Virology 191, 716-723.
38. Frost, J. A., Alberts, A. S., Sontag, E., Guan, K., Mumby, M. C., and Feramisco, J. R. (1994). Simian virus 40 small t antigen cooperates with mitogen-activated kinases to stimulate AP-1 activity. Mol. Cell. Biol. 14, 6244-6252.
39. Garcea, R. L., Ballmer-Hofer, K., and Benjamin, T. L. (1985). Virion assembly defect of polyomavirus hr-t mutants: Underphosphorylation of major capsid protein VP1 before viral DNA encapsidation. J. Virol. 54, 311-316.
40. Garcea, R. L., Talmage, D. A., Harmatz, A., Freund, R., and Benjamin, T. L. (1989). Separation of host range from transformation functions of the hr-t gene of polyomavirus. Virology 168, 312-319.
41. Garcea, R. L., and Benjamin, T. L. (1983). Host range transforming gene of polyoma virus plays a role in virus assembly. Proc. Natl. Acad. Sci. USA 80, 3613-3617.
42. Glenn, G. M., and Eckhart, W. (1995). Amino-terminal regions of polyomavirus middle T antigen are required for interactions with protein phosphatase 2A. J. Virol. 69, 3729-3736.
43. Goldstein, D. J., Andresson, T., Sparkowski, J. J., and Schlegel, R. (1992). The BPV-1 E5 protein, the 16 kDa membrane pore-forming protein and the PDGF receptor exist in a complex that is dependent on hydrophobic transmembrane interactions. EMBO J. 11, 4851-4859.
44. lck: Identification of novel intermolecular association. Science 252, 1523-1528.
45. Hoffman, P., Rajakumar, P., Hoffman, B., Heuertz, R., Wold, W. S. M., and Carlin, C. R. (1992). Evidence for intracellular down-regulation of the epidermal growth factor (EGF) receptor during adenovirus infection by an EGF-independent mechanism. J. Virol. 66, 197-203.
46. fyn with middle tumor antigen in murine polyomavirus-transformed rat cells. J. Virol. 63, 2343-2347.
47. Howe, L. R., and Weiss, A. (1995). Multiple kinases mediate T-cell-receptor signaling. Trends Biochem. Sci. 20, 59-64.
48. Jung, J. U., Trimble, J. J., King, N. W., Biesinger, B., Fleckenstein, B. W., and Desrosiers, R. C. (1991). Identification of transforming genes of subgroup A and C strains of Herpesvirus saimiri. Proc. Natl. Acad. Sci. USA 88, 7051-7055.
49. Jung, J. U., Lang, S. M., Friedrich, U., Jun, T., Roberts, T. M., Desrosiers, R. C., and Biesinger, B. (1995a). Identification of Lck-binding elements in tip of herpesvirus saimiri. J. Biol. Chem. 270, 20660-20667.
50. Jung, J. U., Lang, S. M., Jun, T., Roberts, T. M., Veillette, A., and Desrosiers, R. C. (1995b). Downregulation of Lck-mediated signal transduction by tip of herpesvirus saimiri. J. Virol. 69, 7814-7822.
51. Kiefer, F., Anhauser, I., Soriano, P., Aguzzi, A., Courtneidge, S. A., and Wagner, E. F. (1994a). Endothelial cell transformation by polyomavirus middle T antigen in mice lacking Src-related kinases. Curr. Biol. 4, 100-109.
52. Kiefer, F., Courtneidge, S. A., and Wagner, E. F. (1994b). Oncogenic properties of the middle T antigens of polyomaviruses. Adv. Cancer Res. 64, 125-157.
53. Kieff, E. (1996). In "Virology" (B. N. Fields, D. M. Knipe, and P. M. Howley, Eds.), 3rd ed., pp. 2343-2446.
54. Klein, G. (1994). Epstein-Barr virus strategy in normal and neoplastic B cells. Cell 77, 791-793.
55. Kornbluth, S., Sudol, M., and Hanafusa, H. (1987). Association of the polyomavirus middle-T antigen with c-yes protein. Nature 325, 171-173.
56. Kuivinen, E., Hoffman, B. L., Hoffman, P. A., and Carlin, C. R. (1993). Structurally related Class I and Class II receptor protein tyrosine kinases are down-regulated by the same E3 protein coded for by human Group C adenoviruses. J. Cell Biol. 120, 1271-1279.
57. fyn (a src-like protein tyrosine kinase) in normal and polyomavirus transformed cells. EMBO J. 7, 3837-3844.
58. 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.
59. Lane, D. P., and Benchimol, S. (1990). p53: Oncogene or anti-oncogene? Genes Dev. 4, 1-8.
60. Li, M., and Garcea, R. L. (1994). Identification of thethreonine phosphorylation sites on the polyomavirus major capsid protein VP1: Relationship to the activity of middle T antigen. J. Virol. 68, 320-327.
61. Liu, X, Brodeur, S. R., Gish, G., Zhou, S., Cantley, L. C., Laudano, A. P., and Pawson, T. (1993). Regulation of c-Src tyrosine kinase activity by the Src SH2 domain. Oncogene 8, 1119-1126.
62. Longnecker, R., Druker, B., Roberts, T. M., and Kieff, E. (1991). An Epstein-Barr virus protein associated with cell growth transformation interacts with a tyrosine kinase. J. Virol. 65, 3681-3692.
63. Longnecker, R., Miller, C. L., Miao, X. Q., Marchini, A., and Kieff, E. (1992). The only domain which distinguishes Epstein-Barr virus latent membrane protein 2A (LMP2A) from LMP2B is dispensable for lymphocyte infection and growth transformation in vitro; LMP2A is therefore nonessential. J. Virol. 66, 6461-6469.
64. Longnecker, R., Miller, C. L., Miao, X., Tomkinson, B., Kieff, E., and Miao, X. Q. (1993a). The last seven transmembrane and carboxy-terminal cytoplasmic domains of Epstein-Barr virus latent membrane protein 2 (LMP2) are dispensable for lymphocyte infection and growth transformation in vitro. J. Virol. 67, 2006-2013.
65. Longnecker, R., Miller, C. L., Tomkinson, B., Miao, X., Kieff, E., and Miao, X. Q. (1993b). Deletion of DNA encoding the first five transmembrane domains of Epstein-Barr virus latent membrane proteins 2A and 2B. J. Virol. 67, 5068-5074.
66. lck protein-tyrosine kinase is cytoskeletal and does not bind to polyomavirus middle T antigen. J. Virol. 62, 4673-4679.
67. lck. J. Virol. 70, 600-606.
68. Markland, W., and Smith, A. E. (1987). Mutants of polyomavirus middle-T antigen. Biochim. Biophys. Acta 907, 299-321.
69. Miller, C. L., Lee, J. H., Kieff, E., Burkhardt, A. L., Bolen, J. B., and Longnecker, R. (1994a). Epstein-Barr virus protein LMP2A regulat es reactivation from latency by negatively regulating tyrosine kinases involved in slg-mediated signal transduction. Infect. Agents Dis. 3, 128-136.
70. Miller, C. L., Lee, J. H., Kieff, E., and Longnecker, R. (1994b). An integral membrane protein (LMP2) blocks reactivation of Epstein-Barr virus from latency following surface immunoglobulin crosslinking. Proc. Natl. Acad. Sci. USA 91, 772-776.
71. Miller, C. L., Burkhardt, A. L., Lee, J. H., Stealey, B., Longnecker, R., Bolen, J. B., and Kieff, E. (1995). Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity 2,155-166.
72. lck. Nature 357, 161-164.
73. Mungre, S., Enderle, K., Turk, B., Porras, A., Wu, Y. Q., Mumby, M. C., and Rundell, K. (1994). Mutations which affect the inhibition of protein phosphatase 2A by simian virus 40 small-t antigen in vitro decrease viral transformation. J. Virol. 68, 1675-1681.
74. Pallas, D. C., Shahrik, L. K., Martin, B. L., Jaspers, S., Miller, T. B., Brautigan, D. L., and Roberts, T. M. (1990). Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A. Cell 60, 167-176.
75. Pallas, D. C., Fu, H., Haehnel, L. C., Weller, W., Collier, R. J., and Roberts, T. M. (1994). Association of polyomavirus middle tumor antigen with 14-3-3 proteins. Science 265, 535-537.
76. Pawson, T. (1994). SH2 and SH3 domains in signal transduction. Adv. Cancer Res. 64, 87-110.
77. Pipas, J. M. (1992). Common and unique features of T antigens encoded by the polyomavirus group. J. Virol. 66, 3979-3985.
78. Qu, L., and Rowe, D. (1992). Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J. Virol. 66, 3715-3724.
79. Reinholdsson Ljunggren, G., Ramqvist, T., Ahrlund Richter, L., and Dalianis, T. (1992). Immunization against polyoma tumors with synthetic peptides derived from the sequences of middle- and large-T antigens. Int. J. Cancer 50, 142-146.
80. Rudd, C. E., Janssen, O., Prasad, K. V., Raab, M., da Silva, A., Telfer, J. C., and Yamamoto, M. (1993). src-related protein tyrosine kinases and their surface receptors. Biochim. Biophys. Acta 1155, 239-266.
81. Ruediger, R., Roeckel, D., Fait, J., Bergqvist, A., Magnusson, G., and Walter, G. (1992). Identification of binding sites on the regulatory A subunit of protein phosphatase 2A for the catalytic C subunit and for tumor antigens of simian virus 40 and polyomavirus. Mol. Cell. Biol. 12, 4872-4882.
82. Ruediger, R., Hentz, M., Fait, J., Mumby, M., and Walter, G. (1994). Molecular model of the A subunit of protein phosphatase 2A: Interaction with other subunits and tumor antigens. J. Virol. 68, 123-129.
83. Scheidtmann, K. H., Mumby, M. C., Rundell, K., and Walter, G. (1991). Dephosphorylation of simian virus 40 large-T antigen and p53 protein by protein phosphatase 2A: Inhibition by small-t antigen. Mol. Cell. Biol. 11, 1996-2003.
84. Scherneck, S., and Feunteun, J. (1990). The hamster polyomavirus - A brief review of recent knowledge. Arch. Geshwulstforsch. 60, 271-278.
85. Seidel-Dugan, C., Meyer, B. E., Thomas, S. M., and Brugge, J. S. (1992). Effects of SH2 and SH3 deletions on the functional activities of wild-type and transforming variants of c-Src. Mol. Cell. Biol. 12, 1835-1845.
86. Songyang, Z., Sheolson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, R., Roberts, T., Ratnofsky, S., Lechleider, R. J., Neel, B. G., Birge, R. B., Fajardo, J. E., Chou, M. M., Hanafusa, H., Schaffhausen, B., and Cantley, L. C. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
87. Sontag, E., Fedorov, S., Kamibayashi, C., Robbins, D., Cobb, M., and Mumby, M. (1993). The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the map kinase pathway and induces cell proliferation. Cell 75, 887-897.
88. Srinivas, S., Schönthal, A., and Eckhart, W. (1994). Polyomavirus middle-sized tumor antigen modulates c-Jun phosphorylation and transcriptional activity. Proc. Natl. Acad. Sci. USA 91, 10064-10068.
89. Straight, S. W., Hinkle, P. M., Jewers, R. J., and McCance, D. J. (1993). The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J. Virol. 67, 4521-4532.
90. Su, W., Liu, W., Schaffhausen, B. S., and Roberts, T. M. (1995). Association of polyomavirus middle tumor antigen with phospholipase C-gamma 1. J. Biol. Chem. 270, 12331-12334.
91. Taylor, S. J., and Shalloway, D. (1996). Src and the control of cell division. BioEssays 18, 9-11.
92. Thomas, J. E., Aguzzi, A., Soriano, P., Wagner, E. R., and Brugge, J. S. (1993). Induction of tumor formation and cell transformation by polyoma middle T antigen in the absence of Src. Oncogene 8, 2521-2529.
93. Tooze, J. (1980). "DNA Tumor Viruses," 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
94. Urich, M., El Shemerly, M. Y., Besser, D., Nagamine, Y., and Ballmer-Hofer, K. (1995). Activation and nuclear translocation of mitogenactivated protein kinases by polyomavirus middle-T or serum depend on phosphatidylinositol 3-kinase. J. Biol. Chem. 270, 29286-29292.
95. van der Geer, P., and Pawson, T. (1995). The PTB domain: A new protein module implicated in signal transduction. Trends Biochem. Sci. 20, 277-280.
96. Weiss, A. (1993). T cell antigen receptor signal transduction: A tale of tails and cytoplasmic protein-tyrosine kinases. Cell 73, 209-212.
97. Whitman, M., Kaplan, D. R., Schaffhausen, B. S., Cantley, L., and Roberts, T. M. (1985). Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315, 239-242.
98. lck by Herpesvirus saimiri protein Tip. J. Biol. Chem. 271, 847-852.
99. Yang, S. I., Lickteig, R. L., Estes, R., Rundell, K., Walter, G., and Mumby, M. C. (1991). Control of protein phosphatase 2A by simian virus 40 small-t antigen. Mol. Cell. Biol. 11, 1988-1995.
100. Zullo, J, Stiles, C. D., and Garcea, R. L. (1987). Regulation of c-myc and c-fos mRNA levels by polyomavirus: Distinct roles for the capsid protein VP1 and the viral early proteins. Proc. Natl. Acad. Sci. USA 84, 1210-1214.