Feline leukemia virus long terminal repeat activates collagenase IV gene expression through AP-1

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 4931-4940

  Ghosh, Sajal K ^a   Faller, Douglas V ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ARTICLE; FELINE LEUKEMIA VIRUS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; VIRUS CELL INTERACTION; VIRUS GENE;

EID: 0032992985     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.4931-4940.1999     Document Type: Article

References (76)

1. Alessi, D. R., A. Cuenda, P. Cohen, D. T. Dudley, and A. R. Saltiel. 1995. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270:27489-27494.
2. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
3. Angel, P., I. Baumann, B. Stein, H. Delius, H. J. Rahmsdorf, and P. Herrlich. 1987. 12-O-Tetradecanoyl-phorbol-13-acetate induction of the human colla-genase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol. Cell. Biol. 7:2256-2266.
4. Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55:875-885.
5. Angel, P., and M. Karin. 1991. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072:129-157.
6. Berry, B. T., A. K. Ghosh, D. V. Kumar, D. A. Spodick, and P. Roy-Burman. 1988. Structure and function of endogenous feline leukemia virus long terminal repeats and adjoining regions. J. Virol. 62:3631-3641.
7. Beyaert, R., A. Cuenda, W. Vanden Berghe, S. Plaisance, J. C. Lee, G. Haegeman, P. Cohen, and W. Fiers. 1996. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 15:1914-1923.
8. Boral, A. L., S. A. Okenquist, and J. Lenz. 1989. Identification of the SL3-3 virus enhancer core as a T-lymphoma cell-specific element. J. Virol. 63:76-78.
9. Bösze, Z., H.-J. Thiesen, and P. Charnay. 1986. A transcriptional enhancer with specificity for erythroid cells is located in the long terminal repeat of the Friend murine leukemia virus. EMBO J. 5:1615-1623.
10. Boyle, W. J., T. Smeal, L. H. Defize, P. Angel, J. R. Woodgett, M. Karin, and T. Hunter. 1991. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 64:573-584.
11. Chatis, P. A., C. A. Holland, J. E. Silver, T. N. Frederickson, N. Hopkins, and J. W. Hartley. 1984. A 3′ end fragment encompassing the transcriptional enhancers of nondefective Friend virus confers erythroleukemogenicity on Moloney leukemia virus. J. Virol. 52:248-254.
12. Choi, S. Y., and D. V. Faller. 1994. The long terminal repeats of a murine retrovirus encode a trans-activator for cellular genes. J. Biol. Chem. 269: 19691-19694.
13. Choi, S.-Y., and D. V. Faller. 1995. A transcript from the long terminal repeats of a murine retrovirus associated with trans activation of cellular genes. J. Virol. 69:7054-7060.
14. Choi, S. Y., K. van de Mark, and D. V. Faller. 1997. Identification of a cis-acting element in the class I major histocompatibility complex gene promoter responsive to activation by retroviral sequences. J. Virol. 71:965-970.
15. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
16. Chumakov, I., H. Stuhlmann, K. Harbers, and R. Jaenisch. 1982. Cloning of two genetically transmitted Moloney leukemia proviral genomes: correlation between biological activity of the cloned DNA and viral genome activation in the animal. J. Virol. 42:1088-1098.
17. Cohen, P. 1997. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 7:353-361.
18. Cuenda, A., P. Cohen, V. Buee-Scherrer, and M. Goedert. 1997. Activation of stress-activated protein kinase-3 (SAPK3) by cytokines and cellular stresses is mediated via SAPKK3 (MKK6); comparison of the specificities of SAPK3 and SAPK2 (RK/p38). EMBO J 16:295-305.
19. Cuenda, A., J. Rouse, Y. N. Doza, R. Meier, P. Cohen, T. F. Gallagher, P. R. Young, and J. C. Lee. 1995. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364:229-233.
20. Dai, H. Y., G. I. Troseth, M. Gunleksrud, T. Bruland, L. A. Solberg, H. Aarset, L. I. Kristiansen, and A. Dalen. 1998. Identification of genetic determinants responsible for the rapid immunosuppressive activity and the low leukemogenic potential of a variant of Friend leukemia virus, FIS-2. J. Virol. 72:1244-1251.
21. DesGroseillers, L., and P. Jolicoeur. 1984. The tandem direct repeats within the long terminal repeat of murine leukemia viruses are the primary determinant of their leukemogenic potential. J. Virol. 52:945-952.
22. Donahue, P. R., E. A. Hoover, G. A. Beltz, N. Riedel, V. M. Hirsch, J. Overbaugh, and J. I. Mullins. 1988. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J. Virol. 62:722-731.
23. Faller, D. V. 1995. Modulation of MHC antigen expression by retroviruses, p. 150-191. In G. E. Blair, D. J. Maudsley, and C. R. Pringle (ed.), MHC antigen expression and disease. Cambridge University Press, Cambridge, England.
24. Faller, D. V., H. Weng, and S. Y. Choi. 1997. Activation of collagenase IV gene expression and enzymatic activity by the Moloney murine leukemia virus long terminal repeat. Virology 227:331-342.
25. Faller, D. V., H. Weng, D. T. Graves, and S. Y. Choi. 1997. Moloney murine leukemia virus long terminal repeat activates monocyte chemotactic protein-1 protein expression and chemotactic activity. J. Cell. Physiol. 172:240-252.
26. Faller, D. V., L. D. Wilson, and D. C. Flyer. 1988. Mechanism of induction of class I major histocompatibility antigen expression by murine leukemia virus. J. Cell. Biochem. 36:297-309.
27. Festenstein, H., and F. Garrido. 1986. MHC antigens and malignancy. Nature 322:502-503.
28. Flyer, D. C., S. J. Burakoff, and D. V. Faller. 1985. Retrovirus-induced changes in major histocompatibility complex antigen expression influence susceptibility to lysis by cytotoxic T lymphocytes. J. Immunol. 135:2287-2292.
29. Franklin, C. C., and A. S, Kraft. 1995. Constitutively active MAP kinase kinase (MEK1) stimulates SAP kinase and c-Jun transcriptional activity in U937 human leukemic cells. Oncogene 11:2365-2374.
30. Fulton, R., M. Plumb, L. Shield, and J. C. Neil. 1990. Structural diversity and nuclear protein binding sites in the long terminal repeats of feline leukemia virus. J. Virol. 64:1675-1682.
31. Ghosh, S. K., and D. V. Faller. Unpublished observation.
32. Golemis, E., Y. Li, T. N. Fredrickson, J. W. Hartley, and N. Hopkins. 1989. Distinct segments within the enhancer region collaborate to specify the type of leukemia induced by nondefective Friend and Moloney viruses. J. Virol. 63:328-337.
33. Golemis, E. A., N. A., Speck, and N. Hopkins. 1990. Alignment of U3 region sequences of mammalian type C viruses: identification of highly conserved motifs and implications for enhancer design. J. Virol. 64:534-542.
34. Goodenow, R. S., J. M. Vogel, and R. L. Linsk, 1985. Histocompatibility antigens on murine tumors. Science 230:777-783.
35. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
36. Graves, D. T., Y. L. Jiang, M. J. Williamson, and A. J. Valente. 1989. Identification of monocyte chemotactic activity produced by malignant cells. Science 245:1490-1493.
37. Hazzalin, C. A., E. Cano, A. Cuenda, M. J. Barratt, P. Cohen, and L. C. Mahadevan. 1996. p38/RK is essential for stress-induced nuclear responses: JNK/SAPKs and c-Jun/ATF-2 phosphorylation are insufficient. Curr. Biol. 6:1028-1031.
38. Hunter, T., and M. Karin. 1992. The regulation of transcription by phosphorylation. Cell 70:375-387.
39. Ishimoto, A., M. Takimoto, A. Adachi, M. Kakuyama, S. Kato, K. Kakimi, K. Fukuoka, T. Ogiu, and M. Matsuyama. 1987. Sequences responsible for erythroid and lymphoid leukemia in the long terminal repeats of Friendmink cell focus-forming and Moloney murine leukemia viruses. J. Virol. 61:1861-1866.
40. Jarrett, O., and P. H. Russell. 1978. Differential growth and transmission in cats of feline leukaemia viruses of subgroups A and B. Int. J. Cancer 21: 466-472.
41. Karin, M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270:16483-16486.
42. Koka, P., K. van de Mark, and D. V. Faller. 1991. trans-Activation of genes encoding activation-associated human T lymphocyte surface proteins by murine retroviral sequences. J. Immunol. 146:2417-2425.
43. Lenz, J., D. Celander, R. L., Crowther, R. Patarca, D. W. Perkins, and W. A. Haseltine. 1984. Determination of the leukemogenicity of a murine retrovirus by sequences within the long terminal repeat. Nature 308:467-470.
44. Levesque, K. S., L. Bonham, and L. S. Levy. 1990. ftvi-1, a common integration domain of feline leukemia virus in naturally occurring lymphomas of a particular type. J. Virol. 64:3455-3462.
45. Levy, L. S., P. A. Lobelle-Rich, and J. Overbaugh. 1993. flvi-2, a target of retroviral insertional mutagenesis in feline thymic lymphosarcomas, encodes bmi-1. Oncogene 8:1833-1838.
46. Li, Y., E. Golemis, J. W. Hartley, and N. Hopkins. 1987. Disease specificity of nondefective Friend and Moloney murine leukemia viruses is controlled by a small number of nucleotides. J. Virol. 61:693-700.
47. Liotta, L. A., K. Tryggvason, S. Garbisa, I. Hart, C. M. Foltz, and S. Shafie. 1980. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67-68.
48. Lopata, M. A., D. W. Cleveland, and B. Sollner-Webb. 1984. High level transient expression of a chloramphenicol acetyl transferase gene by DEAE-dextran mediated DNA transfection coupled with a dimethyl sulfoxide or glycerol shock treatment. Nucleic Acids Res. 12:5707-5717.
49. Matsumoto, Y., Y. Momoi, T. Watari, R. Goitsuka, H. Tsujimoto, and A. Hasegawa. 1992. Detection of enhancer repeats in the long terminal repeats of feline leukemia viruses from cats with spontaneous neoplastic and nonneoplastic diseases. Virology 189:745-749.
50. Morrison, H. L., B. Soni, and J. Lenz. 1995. Long terminal repeat enhancer core sequences in proviruses adjacent to c-myc in T-cell lymphomas induced by a murine retrovirus. J. Virol. 49:446-455.
51. Negus, R. P., G. W. Stamp, M. G. Relf, F. Burke, S. T. Malik, S. Bernasconi, P. Allavena, S. Sozzani, A. Mantovani, and F. R. Balkwill. 1995. The detection and localization of monocyte chemoattractant protein-1 (MCP-1) in human ovarian cancer. J. Clin. Investig. 95:2391-2396.
52. Nell, J. C., R. Fulton, M. Rigby, and M. Stewart 1991. Feline leukaemia virus: generation of pathogenic and oncogenic variants. Curr. Top. Microbiol. Immunol. 171:67-93.
53. O'Donnell, P. V., R. Woller, and A. Chu. 1984. Stages in development of mink cell focus-inducing (MCF) virus-accelerated leukemia in AKR mice. J. Exp. Med. 160:914-934.
54. Overbaugh, J. Personal communication.
55. Overbaugh, J., P. R. Donahue, S. L. Quackenbush, E. A. Hoover, and J. I. Mullins. 1988. Molecular cloning of a feline leukemia virus that induces fatal immunodeficiency disease in cats. Science 239:906-910.
56. Overbaugh, J., N. Riedel, E. A. Hoover, and J. I. Mullins. 1988. Transduction of endogenous envelope genes by feline leukaemia virus in vitro. Nature 332:731-734.
57. Pulverer, B. J., J. M. Kyriakis, J. Avruch, E. Nikolakaki, and J. R. Woodgett. 1991. Phosphorylation of c-jun mediated by MAP kinases. Nature 353:670-674.
58. Ray, A., S. B. Tatter, L. T. May, and P. B. Sehgal. 1988. Activation of the human "beta 2-interferon/hepatocyte-stimulating factor/interleukin 6" promoter by cytokines, viruses, and second messenger agonists. Proc. Natl. Acad. Sci. USA 85:6701-6705.
59. Riedel, N., E. A. Hoover, P. W. Gasper, M. O. Nicolson, and J. I. Mullins. 1986. Molecular analysis and pathogenesis of the feline aplastic anemia retrovirus, feline leukemia virus C-Sarma. J. Virol. 60:242-250.
60. Rohn, J. L., and J. Overbaugh. 1995. In vivo selection of long terminal repeat alterations in feline leukemia virus-induced thymic lymphomas. Virology 206:661-665.
61. Roux, P., J. M. Blanchard, A. Fernandez, N. Lamb, P. Jeanteur, and M. Piechaczyk. 1990. Nuclear localization of c-Fos, but not v-Fos proteins, is controlled by extracellular signals. Cell 63:341-351.
62. Roy-Burman, P. 1995. Endogenous env elements: partners in generation of pathogenic feline leukemia viruses. Virus Genes 11:147-161.
63. Sarma, P. S., and T. Log. 1973. Subgroup classification of feline leukemia and sarcoma viruses by viral interference and neutralization tests. Virology 54:160-169.
64. Selten, G., H. T. Cuypers, and A. Berns. 1985. Proviral activation of the putative oncogene pim-1 in MuLV-induced T cell lymphomas. EMBO J. 4:1793-1798.
65. Sheets, R. L., R. Pandey, W. C. Jen, and P. Roy-Burman. 1993. Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas. J. Virol. 67:3118-3125.
66. Sheets, R. L., R. Pandey, V. Klement, C. K. Grant, and P. Roy-Burman. 1992. Biologically selected recombinants between feline leukemia virus (FeLV) subgroup A and an endogenous FeLV element. Virology 190:849-855.
67. Short, M. K., S. A. Okenquist, and J. Lenz. 1987. Correlation of leukemogenic potential of murine retroviruses with transcriptional tissue preferences of the long terminal repeat. J. Virol. 61:1067-1072.
68. Soe, L. H., R. W. Shimlzu, J. R. Landolph, and P. Roy-Burman. 1985. Molecular analysis of several classes of endogenous feline leukemia virus elements. J. Virol. 56:701-710.
69. Speck, N. A., B. Renjifo, E. Golemix, T. Fredrickson, J. Hartley, and N. Hopkins. 1990. Mutation of the core or adjacent LVb elements of the Moloney murine leukemia virus enhancer alters disease specificity. Genes Dev. 4:233-242.
70. Starkey, C. R., P. A. Lobelle-Rich, S. Granger, B. K. Brightman, H. Fan, and L. S. Levy. 1998. Tumorigenic potential of a recombinant retrovirus containing sequences from Moloney murine leukemia virus and feline leukemia virus. J. Virol. 72:1078-1084.
71. Timmers, H. T., G. J. Pronk, J. L. Bos, and A. J. van der Eb. 1990. Analysis of the rat JE gene promoter identifies an AP-1 binding site essential for basal expression but not for TPA induction. Nucleic Acids Res. 18:23-34.
72. Tong, L., S. Pav, D. M. White, S. Rogers, K. M. Crane, C. L. Cywin. M. L. Brown, and C. A. Pargellis. 1997. A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket. Nat. Struct. Biol. 4:311-316.
73. Tsatsanis, C., R. Fulton, K. Nishigaki, H. Tsujimoto, L. Levy, A. Terry, D. Spandidos, D. Onions, and J. C. Neil. 1994. Genetic determinants of feline leukemia virus-induced lymphoid tumors: patterns of proviral insertion and gene rearrangement, J. Virol. 68:8296-8303.
74. Watanabe, H., I. Nakanishi, K. Yamashita, T. Hayakawa, and Y. Okada. 1993. Matrix metalloproteinase-9 (92 kDa gelatinase/type IV collagenase) from U937 monoblastoid cells: correlation with cellular invasion. J. Cell Sci. 104:991-999.
75. Weng, H., S. Y. Choi, and D. V. Faller. 1995. The Moloney leukemia retroviral long terminal repeat trans-activates AP-1-inducible genes and AP-1 transcription factor binding. J. Biol. Chem. 270:13637-13644.
76. Wilson, L. D., D. C. Flyer, and D. V. Faller. 1987. Murine retroviruses control class I major histocompatibility antigen gene expression via a trans effect at the transcriptional level. Mol. Cell. Biol. 7:2406-2415.