Two distinct upstream regulatory domains containing multicopy cellular transcription factor binding sites provide basal repression and inducible enhancer characteristics to the immediate-early IES (US3) promoter from human cytomegalovirus

Journal of Virology

Volumn 70, Issue 8, 1996, Pages 5312-5328

  Chan, Yu Jiun ^a   Tseng, Wen Ping ^a   Hayward, Gary S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DOWN REGULATION; ENHANCER REGION; GENE REPRESSION; HELA CELL; HUMAN CYTOMEGALOVIRUS; IMMEDIATE EARLY GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; RNA SPLICING; VERO CELL; VIRUS LATENCY; VIRUS TRANSCRIPTION;

EID: 0029897324     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.8.5312-5328.1996     Document Type: Article

References (68)

1. Biegalke, B. J. 1995. Regulation of human cytomegalovirus US3 gene transcription by a cis-repressive sequence. J. Virol. 69:5362-5367.
2. Boshart, M., F. Weber, G. Jahn, K. Dorsch-Hasler, B. Fleckenstein, and W. Schaffner. 1985. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41:521-530.
3. Chan, Y.-J. 1996. A model for CMV latency and reactivation: role of cellular factors and signal transduction in transcriptional regulation of the CMV immediate-early gene promoter/enhancer regions. Ph.D. thesis. Johns Hopkins University, Baltimore, Md.
4. Chan, Y.-J., C. J. Chiou, and G. S. Hayward. Synergistic interactions between overlapping binding sites for the serum response factor (SRF) and ELK-1 proteins mediate both basal enhancement and phorbol ester responsiveness of primate cytomegalovirus major immediate-early promoters in monocyte and T-lymphocyte cell types. Submitted for publication.
5. Chan, Y.-J., I. Waheed, and G. S. Hayward. Unpublished data.
6. Chang, Y. N., S. Crawford, J. Stall, D. R. Rawlins, K.-T. Jeang, and G. S. Hayward. 1990. The palindromic series I repeats in the simian cytomegalovirus major immediate-early promoter behave as both strong basai enhancers and cyclic AMP response elements. J. Virol. 64:264-277.
7. Chang, Y. N., K.-T. Jeang, C. J. Chiou, Y. J. Chan, M. Pizzorno, and G. S. Hayward. 1993, Identification of a large bent DNA domain and binding sites for serum response factor adjacent to the NFI repeat cluster and enhancer region in the major IE94 promoter from simian cytomegalovirus. J. Virol. 67:516-529.
8. Cherrington, J. M., E. L. Khoury, and E. S. Mocarski. 1991. Human cytomegalovirus ie2 negatively regulates a gene expression via a short target sequence near the transcription start site. J. Virol. 65:887-896.
9. Chiou, C. J., Y.-J. Chan, and G. S. Hayward. Phorbol ester stimulation induces expression from multiple response elements in the major immediate-early enhancer regions of human and simian cytomegalovirus in monocyte and lymphocyte cell types and can lead to activation of the full lytic cycle in non-permissive U-937 cells. Submitted for publication.
10. Cohen, P., S. Klumpp, and D. L. Schelling. 1989. An improved procedure for identifying and quantitating protein phosphatases in mammalian tissues. FEBS Lett. 250:596-600.
11. Colberg-Poley, A. M., L. D. Santomenna, P. P. Harlow, P. A. Benfield, and D. J. Tenney. 1992. Human cytomegalovirus US3 and UL36-38 immediate-early proteins regulate gene expression. J. Virol. 66:95-105.
12. Cowell, I. G. 1994. Repression versus activation in the control of gene transcription. Trends Biochem. Sci. 19:38-42.
13. de Wet, J. R., K. V. Wood, M. DeLuca, D. R. Helinski, and S. Subramani. 1987. Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell Biol. 7:725-737.
14. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
15. Geelen, J. L., R. Boom, G. P. Klaver, R. P. Minnaar, M. C. Feltkamp, F. J. van Milligen, C. J. Sol, and J. van der Noordaa. 1987. Transcriptional activation of the major immediate early transcription unit of human cytomegalovirus by heat-shock, arsenite and protein synthesis inhibitors. J. Gen. Virol. 68:2925-2931.
16. Gonczol, E., P. W. Andrews, and S. A. Plotkin. 1984. Cytomegalovirus replicates in differentiated but not in undifferentiated human embryonal carcinoma cells. Science 224:159-161.
17. Hsieh, J. J., and S. D. Hayward. 1995. Masking of the CBF1/RBPJ kappa transcriptional repression domain by Epstein-Barr virus EBNA2. Science 268:560-563.
18. Hunninghake, G. W., M. M. Monick, B. Liu, and M. F. Stinski. 1989. The promoter-regulatory region of the major immediate-early gene of human cytomegalovirus responds to T-lymphocyte stimulation and contains functional cyclic AMP-response elements. J. Virol. 63:3026-3033.
19. Jeang, K.-T., M. S. Cho, and G. S. Hayward. 1984. Abundant constitutive expression of the immediate-early 94K protein from cytomegalovirus (Colburn) in a DNA-transfected mouse cell line. Mol. Cell. Biol. 4:2214-2223.
20. Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:4830-4841.
21. Jones, T. R., and V. P. Muzithras. 1992. A cluster of dispensable genes within the human cytomegalovirus genome short component: IRS1, US1 through US5, and the US6 family. J. Virol. 66:2541-2546.
22. Keleher, C. A., C. Goutte, and A. D. Johnson. 1988. The yeast cell-type-specific repressor alpha 2 acts cooperatively with a non-cell-type-specific protein. Cell 53:927-936.
23. Kollert-Jons, A., E. Bogner, and K. Radsak. 1991. A 15-kilobase-pair region of the human cytomegalovirus genome which includes US1 through US13 is dispensable for growth in cell culture. J. Virol. 65:5184-5189.
24. Kondo, K., H. Kaneshima, and E. S. Mocarski. 1994. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA 91:11879-11883.
25. Kothari, S., J. Baillie, J. G. Sissons, and J. H. Sinclair. 1991. The 21bp repeat element of the human cytomegalovirus major immediate early enhancer is a negative regulator of gene expression in undifferentiated cells. Nucleic Acids Res. 19:1767-1771.
26. Kouzarides, T., A. T. Bankier, S. C. Satchwell, E. Preddy, and B. G. Barrell. 1988. An immediate early gene of human cytomegalovirus encodes a potential membrane glycoprotein. Virology 165:151-164.
27. LaFemina, R., and G. S. Hayward. 1986. Constitutive and retinoic acid-inducible expression of cytomegalovirus immediate-early genes in human teratocarcinoma cells. J. Virol. 58:434-440.
28. LaFemina, R. L., and G. S. Hayward. 1988. Differences in cell-type-specific blocks to immediate early gene expression and DNA replication of human, simian and murine cytomegalovirus. J. Gen. Virol. 69:355-374.
29. LaFemina, R. L., and G. S. Hayward. 1983. Replicative forms of human cytomegalovirus DNA with joined termini are found in permissively infected human cells but not in non-permissive Balb/c-3T3 mouse cells. J. Gen. Virol. 64:373-389.
30. LaFemina, R. L., M. C. Pizzorno, J. D. Mosca, and G. S. Hayward. 1989. Expression of the acidic nuclear immediate-early protein (IE1) of human cytomegalovirus in stable cell lines and its preferential association with metaphase chromosomes. Virology 172:584-600.
31. Lathey, J. L., and S. A. Spector. 1991. Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. J. Virol. 65:6371-6375.
32. Lehming, N., D. Thanos, J. M. Brickman, J. Ma, T. Maniatis, and M. Ptashne. 1994. An HMG-like protein that can switch a transcriptional activator to a repressor. Nature (London) 371:175-179.
33. Licht, J. D., M. J. Grossel, J. Figge, and U. M. Hansen. 1990. Drosophila Kruppel protein is a transcriptional repressor. Nature (London) 346:76-79.
34. Lieberman, P. M., J. M. Hardwick, J. Sample, G. S. Hayward, and S. D. Hayward. 1990. The Zta transactivator involved in induction of lytic cycle gene expression in Epstein-Barr virus-infected lymphocytes binds to both AP-1 and ZRE sites in target promoter and enhancer regions. J. Virol. 64:1143-1155.
35. Ling, P. D., D. R. Rawlins, and S. D. Hayward. 1993. The Epstein-Barr virus immortalizing protein EBNA-2 is targeted to DNA by a cellular enhancer-binding protein. Proc. Natl. Acad. Sci. USA 90:9237-9241.
36. 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.
37. Liu, R., J. Baillie, J. G. Sissons, and J. H. Sinclair. 1994. The transcription factor YY1 binds to negative regulatory elements in the human cytomegalovirus major immediate early enhancer/promoter and mediates repression in non-permissive cells. Nucleic Acids Res. 22:2453-2459.
38. Nabel, G., and D. Baltimore. 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature (London) 326:711-713.
39. Nelson, J. A., C. Reynolds-Kohler, and B. A. Smith. 1987. Negative and positive regulation by a short segment in the 5′-flanking region of the human cytomegalovirus major immediate-early gene. Mol. Cell. Biol. 7:4125-4129.
40. O'Hare, P., and G. S. Hayward. 1984. Expression of recombinant genes containing herpes simplex virus delayed-early and immediate-early regulatory regions and trans activation by herpesvirus infection. J. Virol. 52:522-531.
41. 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.
42. Pizzorno, M. C., P. O'Hare, L. Sha, R. L. LaFemina, and G. S. Hayward. 1988. trans-activation and autoregulation of gene expression by the immediate-early region 2 gene products of human cytomegalovirus. J. Virol. 62: 1167-1179.
43. Renkawitz, R. 1990. Transcriptional repression in eukaryotes. Trends Genet. 6:192-197.
44. Rice, G. P., R. D. Schrier, and M. B. A. Oldstone. 1984. Cytomegalovirus infects human lymphocytes and monocytes: virus expression is restricted to immediate-early gene products. Proc. Natl. Acad. Sci. USA 81:6134-6138.
45. Roberts, M. S., A. Boundy, P. O'Hare, M. C. Pizzorno, D. M. Ciufo, and G. S. Hayward. 1988. Direct correlation between a negative autoregulatory response element at the cap site of the herpes simplex virus type 1 IE175 (α4) promoter and a specific binding site for the IE175 (ICP4) protein. J. Virol. 62:4307-4320.
46. Sambucetti, L. C., J. M. Cherrington, G. W. Wilkinson, and E. S. Mocarski. 1989. NF-kappa B activation of the cytomegalovirus enhancer is mediated by a viral transactivator and by T cell stimulation. EMBO J. 8:4251-4258.
47. Smith, M. R., and W. C. Greene. 1989. The same 50-kDa cellular protein binds to the negative regulatory elements of the interleukin 2 receptor alpha-chain gene and the human immunodeficiency virus type 1 long terminal repeat. Proc. Natl. Acad. Sci. USA 86:8526-8530.
48. Stamminger, T., H. Fickenscher, and B. Fleckenstein. 1990. Cell type-specific induction of the major immediate early enhancer of human cytomegalovirus by cyclic AMP. J. Gen. Virol. 71:105-113.
49. Stasiak, P. C., and E. S. Mocarski. 1992. Transactivation of the cytomegalovirus ICP36 gene promoter requires the α gene product TRS1 in addition to IE1 and IE2. J. Virol. 66:1050-1058.
50. Stinski, M. F., and T. J. Roehr. 1985. Activation of the major immediate-early gene of human cytomegalovirus by cis-acting elements in the promoterregulatory sequence and by virus-specific trans-acting components. J. Virol. 55:431-441.
51. Sun, S. C., S. B. Maggirwar, and E. Harhaj. 1995. Activation of NF-kappa B by phosphatase inhibitors involves the phosphorylation of I kappa B alpha at phosphatase 2A-sensitive sites. J. Biol. Chem. 270:18347-18351.
52. Taylor-Wiedeman, J., J. G. Sissons, L. K. Borysiewicz, and J. H. Sinclair. 1991. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J. Gen. Virol. 72:2059-2064.
53. Taylor-Wiedeman, J., P. Sissons, and J. Sinclair. 1994. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68:1597-1604.
54. Tenney, D. J., L. D. Santomenna, K. B. Goudie, and A. M. Colberg-Poley. 1993. The human cytomegalovirus US3 immediate-early protein lacking the putative transmembrane domain regulates gene expression. Nucleic Acids Res. 21:2931-2937.
55. Thevenin, C., S. J. Kim, and J. H. Kehrl. 1991. Inhibition of protein phosphatases by okadaic acid induces API in human T cells. J. Biol. Chem. 266:9363-9366.
56. Thomsen, D. R., R. M. Stenberg, W. F. Goins, and M. F. Stinski. 1984. Promoter-regulatory region of the major immediate early gene of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 81:659-663.
57. Toorkey, C. B., and D. R. Carrigan. 1989. Immunohistochemical detection of an immediate early antigen of human cytomegalovirus in normal tissues. J. Infect. Dis. 160:741-751.
58. Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 14:2876-2883.
59. Vazquez, J., G. Farkas, M. Gaszner, A. Udvardy, M. Muller, K. Hagstrom, H. Gyurkovics, L. Sipos, J. Gauzi, M. Galloni, et al. 1993. Genetic and molecular analysis of chromatin domains. Cold Spring Harbor Symp, Quant. Biol. 58:45-54.
60. Waheed, I., Y.-J. Chan, and G. S. Hayward. Unpublished data.
61. Weinshenker, B. G., S. Wilton, and G. P. Rice. 1988. Phorbol ester-induced differentiation permits productive human cytomegalovirus infection in a monocytic cell line. J. Immunol. 140:1625-1631.
62. Weston, K. 1988. An enhancer element in the short unique region of human cytomegalovirus regulates the production of a group of abundant immediate early transcripts. Virology 162:406-416.
63. Weston, K., and B. G. Barrell. 1986. Sequence of the short unique region, short repeats, and part of the long repeats of human cytomegalovirus. J. Mol. Biol. 192:177-208.
64. Wu, T. C., W. A. Lee, M. C. Pizzorno, W. C. Au, V. J. Chan, R. H. Hruban, G. M. Hutchins, and G. S. Hayward. 1992. Localization of the human cytomegalovirus 2.7-kb major early beta-gene transcripts by RNA in situ hybridization in permissive and nonpermissive infections. Am. J. Pathol. 141:1247-1254.
65. Wu, T. C., M. C. Pizzorno, G. S. Hayward, S. Willoughby, D. A. Neumann, N. R. Rose, A. A. Ansari, W. E. Beschorner, K. L. Baughman, and A. Herskowitz. 1992. In situ detection of human cytomegalovirus immediate-early gene transcripts within cardiac myocytes of patients with HIV-associated cardiomyopathy. AIDS 6:777-785.
66. Yamanishi, K., and F. Rapp. 1979. Induction of host DNA synthesis and DNA polymerase by DNA-negative temperature-sensitive mutants of human cytomegalovirus. Virology 94:237-241.
67. Zerbini, M., M. Musiani, and M. La Placa. 1985. Effect of heat shock on Epstein-Barr virus and cytomegalovirus expression. J. Gen. Virol. 66:633-636.
68. Zhao, K., C. M. Hart, and U. K. Laemmli. 1995. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81: 879-889.