Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTV(D)/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis

Genes and Development

Volumn 10, Issue 15, 1996, Pages 1930-1944

  Girard, Luc ^a   Hanna, Zaher ^a,b   Beaulieu, Normand ^a   Hoemann, Caroline D ^a   Simard, Carole ^a   Kozak, Christine A ^c   Jolicoeur, Paul ^a,b,d  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

c myc; MuLV; Notch1; retrovirus; transgenic mice

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CHROMOSOME MAP; GENE EXPRESSION; GENE INSERTION; GENE MUTATION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T CELL LYMPHOMA; THYMOMA; TRANSGENIC MOUSE;

ANIMALIA; MOUSE MAMMARY TUMOR VIRUS; MUS MUSCULUS; UNIDENTIFIED RETROVIRUS;

EID: 0029808295     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.15.1930     Document Type: Article

References (69)

1. Adams, J.M., A.W. Harris, C.A. Pinkert, L.M. Corcoran, W.S. Alexander, S. Cory, R.D. Palmiter, and R.L. Brinster. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
2. Alexander, W.S., J.M. Adams, and S. Cory. 1989. Oncogene cooperation in lymphocyte transformation: Malignant conver sion of Eμ-myc transgenic pre-B cells in vitro is enhanced by v-H-ras or v-raf but not v-abl. Mol. Cell. Biol. 9: 67-73.
3. Artavanis-Tsakonas, S., K. Matsuno, and M.E. Fortini. 1995. Notch signaling. Science 268: 225-232.
4. Aster, J., W. Pear, R. Hasserjian, H. Erba, F. Davi, B. Luo, M. Scott, D. Baltimore, and J. Sklar. 1994. Functional analysis of the TAN-1 gene, a human homolog of Drosophila Notch. Cold Spring Harbor Symp. Quant. Biol. 59: 125-136.
5. Bishop, J.M. 1987. The molecular genetics of cancer. Science 235: 305-311.
6. Blackman, M., J. Kappler, and P. Marrack. 1990. The role of the T cell receptor in positive and negative selection of developing T cells. Science 248: 1335-1341.
7. Blyth, K., A. Terry, M. O'Hara, E.W. Baxter, M. Campbell, M.D. Stewart, L.A. Donehower, D.E. Onions, J.C. Neil, and E.R. Cameron. 1995. Synergy between a human c-myc transgene and p53 null genotype in murine thymic lymphomas: Contrasting effects of homozygous and heterozygous p53 loss. Oncogene 10: 1717-1723.
8. Chin, H., O.-J. Kwon, H.H. Jung, D.S. Kim, and C.A. Kozak. 1995. Genetic mapping of the mouse genes encoding the voltage-sensitive calcium channel subunits. Genomics 28: 592-595.
9. Coffman, C.R., P. Skoglund, W.A. Harris, and C.R. Kintner. 1993. Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73: 659-671.
10. Compere, S.J., P. Baldacci, A.H. Sharpe, T. Thompson, H. Land, and R. Jaenisch. 1989. The ras and myc oncogenes cooperate in tumor induction in many tissues when introduced into midgestation mouse embryos by retroviral vectors. Proc. Natl. Acad. Sci. 86: 2224-2228.
11. Corcoran, L.M., J.M. Adams, A.R. Dunn, and S. Cory. 1984. Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion. Cell 37: 113-122.
12. Del Amo, F.F., D.E. Smith, P.J. Swiatek, M. Gendron-Maguire, R.J.M. Greenspan, A.P. McMahon, and T. Gridley. 1992. Expression pattern of Match, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115: 737-744.
13. Del Amo, F.F., M. Gendron-Maguire, P.J. Swiatek, N.A. Jenkins, N.G. Copeland, and T. Gridley. 1993. Cloning, analysis, and chromosomal localization of Notch-1, a mouse homolog of Drosophila Notch. Genomics 15: 259-264.
14. Dorsky, R.I., D.H. Rapaport, and W.A. Harris. 1995. Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14: 487-496.
15. Ellisen, L.W., J. Bird, D.C. West, A.L. Soreng, T.C. Reynolds, S.D. Smith, and J. Sklar. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66: 649-661.
16. Fortini, M.E., I. Rebay, L.A. Caron, and S. Artavanis-Tsakonas. 1993. An activated notch receptor blocks cell-fate commitment in the developing drosophila eye. Nature 365: 555-557.
17. Gallahan, D. and R. Callahan. 1987. Mammary tumorigenesis in feral mice: Identification of a new int locus in mouse mammary tumor virus [Czech II]-induced mammary tumors. J. Virol. 61: 66-74.
18. Green, E.L. 1981. Breeding system. In The mouse in biomedical research (ed. H.L. Foster, J.D. Smith, and J.G. Fox), Vol. 1, pp. 91-104. Academic Press, New York, NY.
19. Harm, S.R., C.B. Thompson, and R.N. Eisenman. 1985. c-myc oncogene protein synthesis is independent of the cell cycle in human and avian cells. Nature 314: 366-369.
20. Hanna, Z., M. Jankowski, P. Tremblay, X. Jiang, A. Milatovich, U. Francke, and P. Jolicoeur. 1993. The Vin-1 gene, identified by provirus insertional mutatenesis, is the cyclin D2. Oncogene 8: 1661-1666.
21. Haupt, Y., W.S. Alexander, G. Barri, S.P. Klinken, and J.M. Adams. 1991. Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in Eμ-myc transgenic mice. Cell 65: 753-763.
22. Haupt, Y., M.L. Bath, A.W. Harris, and J.M. Adams. 1993a. bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene 8: 3161-3164.
23. Haupt, Y., A.W. Harris, and J.M. Adams. 1993b. Moloney virus induction of T-cell lymphomas in a plasmacytomagenic strain of Eμ-v-abl transgenic mice. Int. J. Cancer 55: 623-629.
24. Heikkila, R., G Schwab, E. Wickstrom, S.L. Loke, D.H. Pluznik, R. Watt, and L.M. Neckers. 1987. A c-myc antisense oligodeoxynucleotide inhibits entry into S phase but not progress from G0 to G1. Nature 328: 445-449.
25. k transcriptional repression domain by Epstein-Barr virus EBNA2. Science 268: 560-563.
26. k-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 16: 952-959.
27. Huang, M. and P. Jolicoeur. 1990. Characterization of the gag/ fusion protein encoded by the defective Duplan retrovirus inducing murine acquired immunodeficiency syndrome. J. Virol. 64: 5764-5772.
28. Jarriault, S., C. Brou, F. Logeat, E.H. Schroeter, R. Kopan, and A. Israel. 1995. Signalling downstream of activated mammalian notch. Nature 377: 355-358.
29. Jolicoeur, P., A. Laperrière, and N. Beaulieu. 1992. Efficient production of human immunodeficiency virus proteins in transgenic mice. J. Virol. 66: 3904-3908.
30. Kaczmarek, L., J.K. Hyland, R. Watt, M. Rosenberg, and R. Baserga. 1985. Microinjected c-myc as a competence factor. Science 228: 1313-1315.
31. Kopan, R. and H. Weintraub. 1993. Mouse notch: Expression in hair follicles correlates with cell fate determination. J. Cell Biol. 121: 631-641.
32. Kopan, R., J.S. Nye, and H. Weintraub. 1994. The intracellular domain of mouse Notch: A constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 120: 2385-2396.
33. Kopan, R., E.H. Schroeter, H. Weintraub, and J.S. Nye. 1996. Signal transduction by activated mNotch: Importance of proteolytic processing and its regulation by the extracellular domain. Proc. Natl. Acad. Sci. 93: 1683-1688.
34. Kung, H.J., C. Boerkoel, and T.H. Carter. 1991. Retroviral mutagenesis of cellular oncogenes: A review with insights into the mechanisms of insertional activation. Curr. Top. Microbiol. Immunol. 171: 1-25.
35. Lardelli, M. and U. Lendahl. 1993. Match A and Match B - Two mouse Notch homologues coexpressed in a wide variety of tissues. Exp. Cell Res. 204: 364-372.
36. Lardelli, M., J. Dahlstrand, and U. Lendahl. 1994. The novel notch homologue mouse notch3 lacks specific epidermal growth factor-repeats and is expressed in proliferating neuroepithelium. Mech. Dev. 46: 123-136.
37. Leder, A., P.K. Pattengale, A. Kuo, T.A. Stewart, and P. Leder. 1986. Consequences of widespread deregulation of the c-myc gene in transgenic mice: Multiple neoplasms and normal development. Cell 45: 485-495.
38. Levy, L.S. and P.A. Lobelle-Rich. 1992. Insertional mutagenesis of flvi-2 in tumors induced by infection with LC-FeLV, a myc-containing strain of feline leukemia virus. J. Virol. 66: 2885-2892.
39. Li, Y., C.A. Holland, J.W. Hartley, and N. Hopkins. 1984. Viral integration near c-myc in 10-20% of mcf 247-induced AKR lymphomas. Proc. Natl. Acad. Sci. 81: 6808-6811.
40. Lieber, T., S. Kidd, E. Alcamo, V. Corbin, and M.W. Young. 1993. Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes & Dev. 7: 1949-1965.
41. Marchuk, D., M. Drumm, A. Saulino, and F.S. Collins. 1991. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 19: 1154.
42. lo thymocytes in vivo. Science 250: 1720-1723.
43. Neil, J.C., D. Hughes, R. McFarlane, N.M. Wilkie, D.E. Onions, G. Lees, and O. Jarrett. 1984. Transduction and rearrangement of the myc gene by feline leukaemia virus in naturally occurring T-cell leukaemias. Nature 308: 814-820.
44. Nye, J.S., R. Kopan, and R. Axel. 1994. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 120: 2421-2430.
45. - T cells. Mol. Cell. Biol. 12: 3522-3530.
46. Peters, G. 1990. Oncogenes at viral integration sites. Cell Growth Differ. 1: 503-510.
47. Poirier, Y., C. Kozak, and P. Jolicoeur. 1988. Identification of a common helper provirus integration site in Abelson murine leukemia virus-induced lymphoma DNA. J. Virol. 62: 3985-3992.
48. Rabbitts, P.H., J.V. Watson, A. Lamond, A. Forster, M.A. Stinson, G. Evan, W. Fischer, E. Atherton, R. Sheppard, and T.H. Rabbitts. 1985. Metabolism of c-myc gene products: c-myc mRNA and protein expression in the cell cycle. EMBO J. 4: 2009-2015.
49. Reaume, A.G., R.A. Conlon, R. Zirngibl, T.P. Yamaguchi, and J. Rossant. 1992. Expression analysis of a Notch homologue in the mouse embryo. Dev. Biol. 154: 377-387.
50. Rebay, I., R.G. Fehon, and S. Artavanis-Tsakonas. 1993. Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74: 319-329.
51. Robbins, J., B.J. Blondel, D. Gallahan, and R. Callahan. 1992. Mouse mammary tumor gene int-3: A member of the notch gene family transforms mammary epithelial cells. J. Virol. 66: 2594-2599.
52. Rosenbaum, H., A.W. Harris, M.L. Bath, J. McNeall, E. Webb, J.M. Adams, and S. Cory. 1990. An Eμ-v-abl transgene elicits plasmacytomas in concert with an activated myc gene. EMBO J. 9: 897-905.
53. Selten, G., H.T. Cuypers, M. Zijlstra, C. Melief, and A. Berns. 1984. Involvment of c-myc in MuLV-induced T cell lymphomas in mice: Frequency and mechanisms of activation. EMBO J. 3: 3215-3222.
54. Shichiri, M., K.D. Hanson, and J.M. Sedivy. 1993. Effects of c-myc expression on proliferation, quiescence, and the G0 to G1 transition in nontransformed cells. Cell Growth Differ. 4: 93-104.
55. 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.
56. Spanopoulou, E., A. Early, J. Elliott, N. Crispe, H. Ladyman, M. Ritter, S. Watt, F. Grosveld, and D. Kioussis. 1989. Complex lymphoid and epithelial thymic tumours in Thy1-myc transgenic mice. Nature 342: 185-189.
57. Spencer, C.A. and M. Groudine. 1991. Control of c-myc regulation in normal and neoplastic cells. Adv. Cancer Res. 56: 1-48.
58. Stewart, T.A., P.K. Pattengale, and P. Leder. 1984. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38: 627-637.
59. Struhl, G., K. Fitzgerald, and I. Greenwald. 1993. Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74: 331-345.
60. Thompson, C.B., P.B. Challoner, P.E. Neiman, and M. Groudine. 1985. Levels of c-myc oncogene mRNA are invariant throughout the cell cycle. Nature 314: 363-366.
61. Tsujimoto, H., R. Fulton, K. Nishigaki, Y. Matsumoto, A. Hasegawa, A. Tsujimoto, S. Cevario, S.J. O'Brien, A. Terry, D. Onions, and J.C. Neil. 1993. A common proviral integration region, fit-1, in T-cell tumors induced by myc-containing feline leukemia viruses. Virology 196: 845-848.
62. van der Lugt, N.M.T., J. Domen, E. Verhoeven, K. Linders, H. van der Gulden, J. Allen, and A. Berns. 1995. Proviral tagging in Eμ-myc transgenic mice lacking the Pim-1 proto-oncogene leads to compensatory activation of Pim-2. EMBO J. 14: 2536-2544.
63. van Lohuizen, M., S. Verbeek, P. Krimpenfort, J. Domen, C. Saris, T. Radaszkiewicz, and A. Berns. 1989. Predisposition to lymphomagenesis in pim-1 transgenic mice: Cooperation with c-myc and N-myc in murine leukemia virus-induced tumors. Cell 56: 673-682.
64. van Lohuizen, M., S. Verbeek, B. Scheijen, E. Wientjens, H. van der Gulden, and A. Berns. 1991. Identification of cooperating oncogenes in Eμ-myc transgenic mice by provirus tagging. Cell 65: 737-752.
65. Villemur, R., Y. Monczak, E. Rassart, C. Kozak, and P. Jolicoeur. 1987. Identification of a new common provirus integration site in Gross passage A murine leukemia virus-induced mouse thymoma DNA. Mol. Cell. Biol. 7: 512-522.
66. Villeneuve, L., E. Rassart, P. Jolicoeur, M. Graham, and J.M. Adams. 1986. Proviral integration site Mis-1 in rat thymomas corresponds to the pvt-1 translocation breakpoint in murine plasmacytomas. Mol. Cell. Biol. 6: 1834-1837.
67. Weinmaster, G., V.J. Roberts, and G. Lemke. 1991. A homolog of Drosophila Notch expressed during mammalian development. Development 113: 199-205.
68. Weinmaster, G., V.J. Roberts, and G. Lemke. 1992. Notch2: A second mammalian Notch gene. Development 116: 931-941.
69. Zagouras, P., S. Stifani, C.M. Blaumueller, M.L. Carcangiu, and S. Artavanis-Tsakonas. 1995. Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc. Natl. Acad. Sci. 92: 6414-6418.