The murine gammaherpesvirus 68 v-cyclin gene is an oncogene that promotes cell cycle progression in primary lymphocytes

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 5110-5122

  Van Dyk, Linda F ^a   Hess, Jay L ^a   Katz, Jonathan D ^a   Jacoby, Meagan ^a   Speck, Samuel H ^a   Virgin IV, Herbert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL CYCLE; CONTROLLED STUDY; GENE EXPRESSION; HERPES VIRUS; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS EXPRESSION; VIRUS ONCOGENE;

EID: 0033023683     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.5110-5122.1999     Document Type: Article

References (80)

1. 1 phase in primary human T lymphocytes. J. Biol. Chem. 268:4113-4119.
2. Albrecht, J.-C., J. Nicholas, D. Biller, K. R. Cameron, B. Biesinger, C. Newman, S. Wittmann, M. A. Craxton, H. Coleman, B. Fleckenstein, and R. W. Honess. 1992. Primary structure of the herpesvirus saimiri genome. J. Virol. 66:5047-5058.
3. Arvanitakis, L., N. Yaseen, and S. Sharma. 1995. Latent membrane protein-1 induces cyclin D2 expression, pRb hyperphosphorylation, and loss of TGF-β-1-mediated growth inhibition on EBV-positive B cells. J. Immunol. 155:1047-1056.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Strahl (ed.). 1987. Current protocols in molecular biology, p. 10.2.30. John Wiley & Sons, Inc., New York, N.Y.
5. Bodrug, S. E., B. J. Warner, M. L. Bath, G. J. Lindeman, A. W. Harris, and J. M. Adams. 1994. Cyclin D1 transgene impedes lymphocyte maturation and collaborates in lymphomagenesis with the myc gene. EMBO J. 13:2124-2130.
6. Bresnahan, W. A., I. Boldogh, P. Chi, E. A. Thompson, and T. Albrecht. 1997. Inhibition of cellular Cdk2 activity blocks human cytomegalovirus replication. Virology 231:239-247.
7. 1. Virology 224:150-160.
8. Cai, W., and P. A. Schaffer. 1991. A cellular function can enhance gene expression and plating efficiency of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J. Virol. 65:4078-4090.
9. Cannell, E. J., P. J. Farrell, and A. J. Sinclair. 1996. Epstein-Barr virus exploits the normal cell pathway to regulate Rb activity during the immortalisation of primary B-cells. Oncogene 13:1413-1421.
10. 1 cell cycle arrest through induction of cyclin-dependent kinase inhibitors. EMBO J. 15:2748-2759.
11. Cesarman, E., R. G. Nador, F. Bai, R A. Bohenzky, J. J. Russo, P. S. Moore, Y. Chang, and D. M. Knowles. 1996. Kaposi's sarcoma-associated herpesvirus contains G protein-coupled receptor and cyclin D homologs which are expressed in Kaposi's sarcoma and malignant lymphoma. J. Virol. 70:8218-8223.
12. Chaffin, K. E., C. R. Beals, T. M. Wilkie, K. A. Forbush, M. I. Simon, and R. M. Perlmutter. 1990. Dissection of thymocyte signaling pathways by in vivo expression of pertussis toxin ADP-ribosyltransferase. EMBO J. 9:3821-3829.
13. Chang, Y., P. S. Moore, S. J. Talbot, C. H. Boshoff, T. Zarkowska, D. Godden-Kent, H. Paterson, R. A. Weiss, and S. Mittnacht. 1996. Cyclin encoded by KS herpesvirus. Nature 382:410.
14. Cohn, S. M., and M. W. Lieberman. 1984. The use of antibodies to 5-bromo-2′-deoxyuridine for the isolation of DNA sequences containing excision-repair sites. J. Biol. Chem. 259:12456-12462.
15. Cosgrove, D., D. Gray, A. Dierich, J. Kaufman, M. Lemeur, C. Benoist, and D. Mathis. 1991. Mice lacking MHC class II molecules. Cell 66:1051-1066.
16. Danielson, P. E., S. Forss-Petter, M. A. Brow, L. Calavetta, J. Douglass, R. J. Milner, and J. G. Sutcliffe. 1988. p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7:261-267.
17. Davis, M. A., M. A. Sturzl, C. Blasig, A. Schreier, H. G. Guo, M. Reitz, S. R. Opalenik, and P. J. Browning. 1997. Expression of human herpesvirus 8-encoded cyclin D in Kaposi's sarcoma spindle cells. J. Natl. Cancer Inst. 89:1868-1874.
18. Dighe, A. S., D. Campbell, C.-S. Hsieh, S. Clarke, D. R. Greaves, S. Gordon, K. M. Murphy, and R. D. Schreiber. 1995. Tissue specific targeting of cytokine unresponsiveness in transgenic mice. Immunity 3:657-666.
19. Dittmer, D., M. Lagunoff, R. Renne, K. Staskus, A. Haase, and D. Ganem. 1998. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J. Virol. 72:8309-8315.
20. 1/S transition. J. Virol. 71:1629-1634.
21. Dowdy, S. F., P. W. Hinds, K. Louie, S. I. Reed, A. Arnold, and R. A. Weinberg. 1993. Physical interaction of the retinoblastoma protein with human D cyclins. Cell 73:499-511.
22. Ewen, M. E., H. K. Sluss, C. J. Sherr, H. Matsushime, J.-Y. Kato, and D. M. Livingston. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73:487-497.
23. Fehling, H. J., and H. von Boehmer. 1997. Early αβ T cell development in the thymus of normal and genetically altered mice. Curr. Opin. Immunol. 9:263-275.
24. Flore, O., and S. J. Gao, 1997. Effect of DNA synthesis inhibitors on Kaposi's sarcoma-associated herpesvirus cyclin and major capsid protein gene expression. AIDS Res. Hum. Retroviruses 13:1229-1233.
25. Godden-Kent, D., S. J. Talbot, C. Boshoff, Y. Chang, P. Moore, R. A. Weiss, and S. Mittnacht. 1997. The cyclin encoded by Kaposi's sarcoma-associated herpesvirus stimulates cdk6 to phosphorylate the retinoblastoma protein and histone H1. J. Virol. 71:4193-4198.
26. Hardwick, J. M. 1997. Virus-induced apoptosis. Adv. Pharmacol. 41:295-336.
27. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948-962.
28. Hogan, B., F. Costatini, and E. Lacy. 1998. Manipulating the mouse embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
29. Hollyoake, M., A. Stuhler, P. Farrell, J. Gordon, and A. Sinclair. 1995. The normal cell cycle activation program is exploited during the infection of quiescent B lymphocytes by Epstein-Barr virus. Cancer Res. 55:4784-4787.
30. Jault, F. M., J.-M. Jault, F. Ruchti, E. A. Fortunato, C. Clark, J. Corbeil, D. D. Richman, and D. H. Spector. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
31. Jung, J. U., M. Stäger, and R. C. Desrosiers. 1994. Virus-encoded cyclin. Mol. Cell. Biol. 14:7235-7244.
32. Katz, J. D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell 74:1089-1100.
33. Kawaguchi, Y., C. Van Sant, and B. Roizman. 1997. Herpes simplex virus 1 a regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3. J. Virol. 71:7328-7336.
34. Kedes, D. H., M. Lagunoff, R. Renne, and D. Ganem. 1997. Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi's sarcoma-associated herpesvirus. J. Clin. Invest. 100:2606-2610.
35. Kulwichit, W., R. H. Edwards, E. M. Davenport, J. F. Baskar, V. Godfrey, and N. Raab-Traub. 1998. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc. Natl. Acad. Sci. USA 95:11963-11968.
36. LaPierre, L. A., J. W. Casey, and D. L. Holzschu. 1998. Walleye retroviruses associated with skin tumors and hyperplasias encode cyclin D homologs. J. Virol. 72:8765-8771.
37. Li, M., H. Lee, D.-W. Yoon, J.-C. Albrecht, B. Fleckenstein, F. Neipel, and J. U. Jung. 1997. Kaposi's sarcoma-associated herpesvirus encodes a functional cyclin. J. Virol. 71:1984-1991.
38. 1 phase cell cycle check point. Immunity 8:57-65.
39. Lovec, H., A. Grzeschiczek, M. B. Kowalski, and T. Moroy. 1994. Cyclin D1/bcl-1 cooperates with myc genes in the generation of B-cell lymphoma in transgenic mice. EMBO J. 13:3487-3495.
40. 1 to S. J. Virol. 70:8850-8857.
41. Marrack, P., and J. Kappler. 1997. Positive selection of thymocytes bearing αβ T cell receptors. Curr. Opin. Immunol. 9:250-255.
42. 1 cyclins. Cell 71:323-334.
43. 1 phase of the cell cycle. Cell 65:701-713.
44. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14:2077-2086.
45. Mittrucker, H. W., K. Pfeffer, R Schmits, and T. W. Mak. 1995. T-lymphocyte development and function in gene-targeted mutant mice. Immunol. Rev. 148:115-150.
46. Mueller, A., R. Odze, T. D. Jenkins, A. Shahsesfaei, H. Nakagawa, T. Inomoto, and A. K. Rustgi. 1997. A transgenic mouse model with cyclin D1 overexpression results in cell cycle, epidermal growth factor receptor, and p53 abnormalities. Cancer Res. 57:5542-5549.
47. Murphy, C., C. Kretschmer, B. Biesinger, J. Beckers, J. U. Jung, R. C. Desrosiers, H. K. Muller-Hermelink, B. W. Fleckenstein, and U. Ruther. 1994. Epithelial tumors induced by a herpesvirus oncogene in transgenic mice. Oncogene 9:221-226.
48. Nakagawa, H., T. C. Wang, L. Zukerberg, R. Odze, K. Togawa, G. H. May, J. Wilson, and A. K. Rustgi. 1997. The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach. Oncogene 14:1185-1190.
49. Nicholas, J., K. R. Cameron, and R. W. Honess. 1992. Herpesvirus saimiri encodes homologs of G protein-coupled receptors and cyclins. Nature 355: 362-365.
50. +) thymocytes in normal and genetically modified mice. J. Immunol. 154:5103-5113.
51. Puglielli, M. T., M. Woisetschlaeger, and S. H. Speck. 1996. oriP is essential for EBNA gene promoter activity in Epstein-Barr virus-immortalized lymphoblastoid cell lines. J. Virol. 70:5758-5768.
52. Rainbow, L., G. M. Platt, G. R. Simpson, R. Sarid, S.-J. Gao, H. Stoiber, C. S. Herrington, P. S. Moore, and T. F. Schulz. 1997. The 222-to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J. Virol. 71:5915-5921.
53. Robles, A. I., F. Larcher, R. B. Whalin, R. Murillas, E. Richie, I. B. Gimenez-Conti, J. L. Jorcano, and C. J. Conti. 1996. Expression of cyclin D1 in epithelial tissues of transgenic mice results in epidermal hyperproliferation and severe thymic hyperplasia. Proc. Natl. Acad. Sci. USA 93:7634-7638.
54. Rogers, H. W., M. P. Callery, B. Deck, and E. R. Unanue. 1996. Listeria monocytogenes induces apoptosis of infected hepatocytes. J. Immunol. 156: 679-684.
55. Russo, J. J., R. A. Bohenzky, M.-C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14867.
56. Salvant, B. S., E. A. Fortunato, and D. H. Spector. 1998. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J. Virol. 72:3729-3741.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Sarid, R., O. Flore, R. A. Bohenzky, Y. Chang, and P. S. Moore. 1998. Transcription mapping of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome in a body cavity-based lymphoma cell line (BC-1). J. Virol. 72:1005-1012.
59. Schang, L. M., A. Hossain, and C. Jones. 1996. The latency-related gene of bovine herpesvirus 1 encodes a product which inhibits cell cycle progression. J. Virol. 70:3807-3814.
60. Schang, L. M., J. Phillips, and P. A. Schaffer. 1998. Requirement for cellular cyclin-dependent kinases in herpes simplex virus replication and transcription. J. Virol. 72:5626-5637.
61. Shan, B., and W.-H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:8166-8173.
62. Shindler, K. S., and K. A. Roth. 1996. Double immunofluorescent staining using two unconjugated primary antisera raised in the same species. J. Histochem. Cytochem. 44:1331-1335.
63. Sinclair, A. J., I. Palmero, A. Holder, G. Peters, and P. J. Farrell. 1995. Expression of cyclin D2 in Epstein-Barr virus-positive Burkitt's lymphoma cell lines is related to methylation status of the gene. J. Virol. 69:1292-1295.
64. Sofer-Levi, Y., and D. Resnitzky. 1996. Apoptosis induced by ectopic expression of cyclin D1 but not cyclin E. Oncogene 13:2431-2437.
65. Soonpaa, M. H., G. Y. Koh, L. Pajak, S. Jing, H. Wang, M. T. Franklin, K. K. Kim, and L. J. Field. 1997. Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. J. Clin. Investig. 99:2644-2654.
66. Surh, C. D., and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100-103.
67. Swanton, C., D. J. Mann, B. Fleckenstein, F. Neipel, G. Peters, and N. Jones. 1997. Herpes viral cyclin/Cdk6 complexes evade inhibition by CDK inhibitor proteins. Nature 390:184-187.
68. Tommasino, M., and L. Crawford. 1995. Human papillomavirus E6 and E7: proteins which deregulate the cell cycle. Bioessays 17:509-518.
69. Tornell, J., S. Farzad, A. Espander-Jansson, G. Matejka, O. Isaksson, and L. Rymo. 1996. Expression of Epstein-Barr nuclear antigen 2 in kidney tubule cells induce tumors in transgenic mice. Oncogene 12:1521-1528.
70. Virgin, H. W., IV, P. Latreille, P. Wamsley, K. Hallsworth, K. E. Weck, A. J. Dal Canto, and S. H. Speck. 1997. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J. Virol. 71:5894-5904.
71. Virgin, H. W., IV, R. M. Presti, X.-Y. Li, C. Liu, and S. H. Speck. 1999. Three distinct regions of the murine gammaherpesvirus 68 genome are transcriptionally active in latently infected mice. J. Virol. 73:2321-2332.
72. Wang, T. C., R. D. Cardiff, L. Zukerberg, E. Lees, A. Arnold, and E. V. Schmidt 1994. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature 369:669-671.
73. Weck, K. E., M. L. Barkon, L. L Yoo, S. H. Speck, and H. W. Virgin IV. 1996. Mature B cells are required for acute splenic infection, but not for establishment of latency, by murine gammaherpesvirus 68. J. Virol. 70:6775-6780.
74. Weck, K. E., A. J. Dal Canto, J. D. Gould, A. K. O'Guin, K. A. Roth, J. E. Saffitz, S. H. Speck, and H. W. Virgin IV. 1997. Murine gammaherpesvirus causes large vessel arterilis in mice lacking interferon-gamma responsiveness: a new model for virus induced vascular disease. Nat. Med. 3:1346-1353.
75. White, E. 1995. Regulation of p53-dependent apoptosis by E1A and E1B. Curr. Top. Microbiol. Immunol. 199:34-58.
76. Wildin, R. S., A. M. Garvin, S. Pawar, D. B. Lewis, K. M. Abraham, K. A. Forbush, S. F. Ziegler, J. M. Allen, and R. M. Perlmutter. 1991. Develop-mental regulation of lck gene expression in T lymphocytes. J. Exp. Med. 173:383-393.
77. Wilson, J. B., J. L. Bell, and A. J. Levine. 1996. Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice. EMBO J. 15:3117-3126.
78. Wilson, J. B., W. Weinberg, R. Johnson, S. Yuspa, and A. J. Levine. 1990. Expression of the BNLF-1 oncogene of Epstein-Barr virus in the skin of transgenic mice induces hyperplasia and aberrant expression of keratin 6. Cell 61:1315-1327.
79. Wu, X., and A. J. Levine. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602-3606.
80. Zuniga-Pflucktr, J. C., and M. J. Lenardo. 1996. Regulation of thymocyte development from immature progenitors. Curr. Opin. Immunol. 8:215-224.