Identification of domains within the human cytomegalovirus major immediate-early 86-kilodalton protein and the retinoblastoma protein required for physical and functional interaction with each other

Journal of Virology

Volumn 71, Issue 11, 1997, Pages 8176-8185

  Fortunato, Elizabeth A ^a   Sommer, Marvin H ^a,b   Yoder, Kristine ^a   Spector, Deborah H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN; RETINOBLASTOMA PROTEIN;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; VIRUS DNA CELL DNA INTERACTION; VIRUS EXPRESSION;

EID: 0030863391     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.11.8176-8185.1997     Document Type: Article

References (70)

1. Albrecht, T., I. Boldogh, M. Fons, C. H. Lee, S. AbuBakar, J. M. Russell, and W. W. Au. 1989. Cell-activation responses to cytomegalovirus infection: relationship to the phasing of CMV replication and to the induction of cellular damage. Subcell. Biochem. 15:157-202.
2. Albrecht, T., M. P. Fons, C. Z. Deng, and I. Boldogh. 1997. Increased frequency of specific locus mutation following human cytomegalovirus infection. Virology 230:48-61.
3. Arlt, H., D. Lang, S. Gebert, and T. Stamminger. 1994. Identification of binding sites for the 86-kilodalton IE2 protein of human cytomegalovirus within an IE2-responsive viral early promoter. J. Virol. 68:4117-4125.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1989. Current protocols in molecular biology. John Wiley & Sons, New York, N.Y.
5. Bresnahan, W. A., I. Boldogh, E. A. Thompson, and T. Albrecht. 1996. Human cytomegalovirus inhibits cellular DNA synthesis and arrests productively infected cells in late G1 Virology 224:150-160.
6. Britt, W., and C. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields et al. (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
7. Caswell, R., L. Bryant, and J. Sinclair. 1996. Human cytomegalovirus immediate-early 2 (IE2) protein can transactivate the human hsp70 promoter by alleviation of Dr1-mediated repression. Virology 70:4028-4037.
8. Caswell, R., C. Hagemeier, C.-J. Chiou, G. Hayward, T. Kouzarides, and J. Sinclair. 1993. The human cytomegalovirus 86K immediate early (IE) 2 protein requires the basic region of the TATA-box binding protein (TBP) for binding, and interacts with TBP and transcription factor TFIIB via regions of IE2 required for transcriptional regulation. J. Gen. Virol. 74:2691-2698.
9. Chen, P.-L., D. J. Riley, S. Chen-Kiang, and W.-H. Lee. 1996. Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc. Natl. Acad. Sci. USA 93:465-169.
10. Cherrington, J. M., E. L. Khoury, and E. S. Mocarski. 1991. Human cytomegalovirus IE2 negatively regulates α gene expression via a short target sequence near the transcription start site. J. Virol. 65:887-896.
11. Choi, K. S., S.-J. Kim, and S. Kim. 1995. The retinoblastoma gene product negatively regulates transcriptional activation mediated by the human cytomegalovirus IE2 protein. Virology 208:450-456.
12. Cress, W. D., and J. R. Nevins. 1996. Use of the E2F transcription factor by DNA tumor virus regulatory proteins. Curr. Top. Microbiol. Immunol. 208: 63-78.
13. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
14. 1/S transition. J. Virol. 71:1629-1634.
15. Dunaief, J. L., B. E. Strober, S. Guha, P. A. Khavari, K. Alin, J. Luban, M. Begemann, G. R. Crabtree, and S. P. Goff. 1994. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79:119-130.
16. Furnari, B. A., E. Poma, T. F. Kowalik, S.-M. Huong, and E.-S. Huang. 1993. Human cytomegalovirus immediate-early gene 2 protein interacts with itself and with several novel cellular proteins. J. Virol. 67:4981-4991.
17. Gu, W., J. W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal-Ginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
18. Hagemeier, C., A. J. Bannister, A. Cook, and T. Kouzarides. 1993. The activation domain of transcription factor PU.1 binds the retinoblastoma (RB) protein and the transcription factor TFIID in vitro: RB shows sequence similarity to TFIID and TFIIB. Proc. Natl. Acad. Sci. USA 90:1580-1584.
19. Hagemeier, C., R. Caswell, G. Hayhurst, J. Sinclair, and T. Kouzarides. 1994. Functional interaction between the HCMV IE2 transactivator and the retinoblastoma protein. EMBO J. 13:2897-2903.
20. Hagemeier, C., S. Walker, R. Caswell, T. Kouzarides, and J. Sinclair. 1992. The human cytomegalovirus 80-kilodalton but not the 72-kilodalton immediate-early protein transactivates heterologous promoters in a TATA box-dependent mechanism and interacts directly with TFIID. J. Virol. 66:4452-4456.
21. Hateboer, G., H. T. M. Timmers, A. K. Rustgi, M. Billaud, L. J. Van 'T Veer, and R. Bernards. 1993. TATA-binding protein and the retinoblastoma gene product bind to overlapping epitopes on c-Myc and adenovirus E1A protein. Proc. Natl. Acad. Sci. USA 90:8489-8493.
22. Hayhurst, G. P., L. A. Bryant, R. C. Caswell, S. M. Walker, and J. H. Sinclair. 1995. CCAAT box-dependent activation of the TATA-less human DNA polymerase a promoter by the human cytomegalovirus 72-kilodalton major immediate-early protein. J. Virol. 69:182-188.
23. Hermiston, T. W., C. L. Malone, and M. F. Stinski. 1990. Human cytomegalovirus immediate-early two-protein region involved in negative regulation of the major immediate-early promoter. J. Virol. 64:3532-3536.
24. Hiebert, S. W. 1993. Regions of the retinoblastoma gene product required for its interaction with the E2F transcription factor are necessary for E2 promoter repression and pRb-mediated growth suppression. Mol. Cell. Biol. 13:3384-3391.
25. Hinds, P. W., S. Mittnacht, V. Dulic, A. Arnold, S. I. Reed, and R. A. Weinberg. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70:993-1006.
26. Huang, H., J. Yee, J. Shew, P. Chen, R. Bookstein, T. Friedmann, E. Lee, and W. Lee. 1988. Suppression of the neoplastic phenotype by replacement of the RB gene in human cancer cells. Science 242:1563-1566.
27. 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.
28. Jenkins, D. E., C. L. Martens, and E. S. Mocarski. 1994. Human cytomegalovirus late protein encoded by ie2: a transactivator as well as a repressor of gene expression. J. Gen. Virol. 75:2337-2348.
29. Jupp, R., S. Hoffmann, R. M. Stenberg, J. A. Nelson, and P. Ghazal. 1993. Human cytomegalovirus IE86 protein interacts with promoter-bound TATA-binding protein via a specific region distinct from the autorepression domain. J. Virol. 67:7539-7546.
30. Kaye, F. J., R. A. Kratzke, J. L. Gerster, and J. M. Horowitz. 1990. A single amino acid substitution results in a retinoblastoma protein defective in phosphorylation and oncoprotein binding. Proc. Natl. Acad. Sci. USA 87: 6922-6926.
31. Klucher, K. M., M. Sommer, J. T. Kadonaga, and D. H. Spector. 1993. In vivo and in vitro analysis of transcriptional activation mediated by the human cytomegalovirus major immediate-early proteins. Mol. Cell. Biol. 13:1238-1250.
32. Kwon, H., A. N. Imbalzano, P. A. Khavari, R. E. Kingston, and M. R. Green. 1994. Nucleosome disruption and enhancement of activator binding by a human SWI/SNF complex. Nature (London) 370:477-481.
33. Lang, D., S. Gebert, H. Arlt, and T. Stamminger. 1995. Functional interaction between the human cytomegalovirus 86-kilodalton IE2 protein and the cellular transcription factor CREB. J. Virol. 69:6030-6037.
34. Lang, D., and T. Stamminger. 1993. The 86-kilodalton IE-2 protein of human cytomegalovirus is a sequence-specific DNA-binding protein that interacts directly with the negative autoregulatory response element located near the cap site of the IE-1/2 enhancer-promoter. J. Virol. 67:323-331.
35. Liu, B., T. W. Hermiston, and M. F. Stinski. 1991. A cis-acting element in the major immediate-early (IE) promoter of human cytomegalovirus is required for negative regulation by IE2. J. Virol. 65:897-903.
36. 1 to S. J. Virol. 70:8850-8857.
37. Lukac, D. M., J. R. Manuppello, and J. C. Alwine. 1994. Transcriptional activation by the human cytomegalovirus immediate-early proteins: requirements for simple promoter structures and interactions with multiple components of the transcription complex. J. Virol. 68:5184-5193.
38. Macias, M. P., and M. F. Stinski. 1993. An in vitro system for human cytomegalovirus immediate early 2 protein (IE-2)-mediated site-dependent repression of transcription and direct binding of IE2 to the major immediateearly promoter. Proc. Natl. Acad. Sci. USA 90:707-711.
39. Margolis, M. J., S. Panjovic, E. L. Wong, M. Wade, R. Jupp, J. A. Nelson, and J. C. Azizkhan. 1995. Interaction of the 72-kilodalton human cytomegalovirus IE1 gene product with E2F1 coincides with E2F-dependent activation of dihydrofolate reductase transcription. J. Virol. 69:7759-7767.
40. Mocarski, E. S. 1996. Cytomegaloviruses and their replication, p. 2447-2492. In B. N. Fields et al. (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
41. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titer retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
42. Pizzorno, M. C., and G. S. Hayward. 1990. The IE2 gene products of human cytomegalovirus specifically down-regulate expression from the major immediate-early promoter through a target sequence located near the cap site J. Virol. 64:6154-6165.
43. Pizzorno, M. C., M.-A. Mullen, Y.-N. Chang, and G. S. Hayward. 1991. The functionally active IE2 immediate-early regulatory protein of human cytomegalovirus is an 80-kilodalton polypeptide that contains two distinct activator domains and a duplicated nuclear localization signal. J. Virol 65:3839-3852.
44. Poma, E. E., T. F. Kowalik, L. Zhu, J. H. Sinclair, and E.-S. Huang. 1996. The human cytomegalovirus IE1-72 protein interacts with the cellular p107 protein and relieves p107-mediated transcriptional repression of an E2F-responsive promoter. J. Virol. 70:7867-7877.
45. Qian, Y., C. Luckey, L. Horton, M. Esser, and D. J. Templeton. 1992. Biological function of the retinoblastoma protein requires distinct domains for hyperphosphorylation and transcription factor binding. Mol. Cell. Biol. 12:5363-5372.
46. Qin, X.-Q., T. Chittenden, D. M. Livingston, and W. G. Kaelin, Jr. 1992. Identification of the growth suppressor domain within the retinoblastoma gene product. Genes Dev. 6:953-964.
47. Qin, X.-Q., D. M. Livingston, M. Ewen, W. R. Sellers, Z. Arany, and W. G. Kaelin, Jr. 1995. The transcription factor E2F-1 is a downstream target of RB action. Mol. Cell. Biol. 15:742-755.
48. Samaniego, L. A., M. J. Tevethia, and D. J. Spector. 1994. The human cytomegalovirus 86-kilodalton immediate-early 2 protein: synthesis as a precursor polypeptide and interaction with a 75-kilodalton protein of probably viral origin. J. Virol. 68:720-729.
49. Schwartz, R., B. Helmich, and D. H. Spector. 1996. CREB and CREB-binding proteins play an important role in the IE2 86-mediated transactivation of the human cytomegalovirus 2.2-kb RNA promoter. J. Virol. 70:6955-6966.
50. Schwartz, R., M. H. Sommer, A. Scully, and D. H. Spector. 1994. Site-specific binding of the human cytomegalovirus IE2 86-kilodalton protein to an early gene promoter. J. Virol. 68:5613-5622.
51. Scatty, A. L., M. H. Sommer, R. Schwartz, and D. H. Spector. 1995. The human cytomegalovirus IE2 86-kilodalton protein interacts with an early gene promoter via site-specific DNA binding and protein-protein associations. J. Virol. 69:6533-6540.
52. Sellers, W. R., J. W. Rodgers, and W. G. Kaelin, Jr. 1995. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. USA 92:11544-11548.
53. Shen, Y., H. Zhu, and T. Shenk. 1997. Human cytomegalovirus IE1 and IE2 proteins are mutagenic and mediate "hit-and-run" oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc. Natl. Acad. Sci. USA 94:3341-3345.
54. Shew, J., B. Lin, P. Chen, B. Tseng, T. Yang-Feng, and W. H. Lee. 1990. C-terminal truncation of the retinoblastoma gene product leads to functional inactivation. Proc. Natl. Acad. Sci. USA 87:6-10.
55. Sommer, M. H., A. L. Scully, and D. H. Spector. 1994. Transactivation by the human cytomegalovirus IE2 86-kilodalton protein requires a domain that binds to both the TATA box-binding protein and the retinoblastoma protein. J. Virol. 68:6223-6231.
56. Spector, D. J., and M. J. Tevethia. 1994. Protein-protein interactions between human cytomegalovirus IE2-580aa and pUL84 in lytically infected cells. J. Virol. 68:7549-7553.
57. Speir, E., R. Modali, E.-S. Huang, M. B. Leon, F. Sahwl, T. Finkel, and S. E. Epstein. 1994. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265:391-394.
58. Strober, B. E., J. L. Dunaief, S. Guha, and S. P. Goff. 1996. Functional interactions between the hBRM/hBRG1 transcriptional activators and the pRB family of proteins. Mol. Cell. Biol. 16:1576-1583.
59. Taya, Y. 1997. RB kinases and RB-binding proteins: new points of view. Trends Biochem. Sci. 22:14-17.
60. Templeton, D. J., S. H. Park, L. Lanier, and R. A. Weinberg. 1991. Non-functional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, viral oncoprotein association and nuclear tethering. Proc. Natl. Acad. Sci. USA 88:3033-3039.
61. Tsai, H.-L., G.-H. Kou, S.-C. Chen, C.-W. Wu, and Y.-S. Lin. 1996. Human cytomegalovirus immediate-early protein IE2 tethers a transcriptional repression domain to p53. J. Biol. Chem. 271:3534-3540.
62. Wang, J. Y. 1997. Retinoblastoma protein in growth suppression and death protection. Curr. Opin. Genet. Dev. 7:39-45.
63. Wang, J. Y. J., E. S. Knudsen, and P. J. Welch. 1994. The retinoblastoma tumor suppressor protein. Adv. Cancer Res. 64:25-85.
64. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
65. Welch, P. J., and J. Y. J. Wang. 1993. A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell 75:779-790.
66. Welch, P. J., and J. Y. J. Wang. 1995. Disruption of retinoblastoma protein function by coexpression with its C pocket fragment. Genes Dev. 9:31-46.
67. Welch, P. J., and J. Y. J. Wang. 1995. Abrogation of retinoblastoma protein function by c-Abl through tyrosine kinase-dependent and -independent mechanisms. Mol. Cell. Biol. 15:5542-5551.
68. Yoo, Y. D., C.-J. Chiou, K. S. Choi, Y. Yi, S. Michelson, S. Kim, G. S. Hayward, and S.-J. Kim. 1996. The IE2 regulatory protein of human cytomegalovirus induces expression of the human transforming growth factor β1 gene through an Egr-1 binding site. J. Virol. 70:7062-7070.
69. Zhou, Y. F., M. B. Leon, M. A. Waclawiw, J. J. Popma, Z. X. Yu, T. Finkel, and S. E. Epstein. 1996. Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N. Engl. J. Med. 335:624-630.
70. Zhu, H., Y. Shen, and T. Shenk. 1995. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69:7960-7970.