Two Sp1/Sp3 binding sites in the major immediate-early proximal enhancer of human cytomegalovirus have a significant role in viral replication

Journal of Virology

Volumn 79, Issue 15, 2005, Pages 9597-9607

  Isomura, Hiroki ^a   Stinski, Mark F ^b   Kudoh, Ayumi ^a   Daikoku, Tohru ^a   Shirata, Noriko ^a   Tsurumi, Tatsuya ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL ACETYLTRANSFERASE; KANAMYCIN; RESTRICTION ENDONUCLEASE; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; VIRUS DNA;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA REPLICATION; DNA SEQUENCE; ENHANCER REGION; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMEDIATE EARLY GENE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TATA BOX; TRANSCRIPTION INITIATION SITE; VIRUS RECOMBINANT; VIRUS REPLICATION; WESTERN BLOTTING;

BINDING SITES; CYTOMEGALOVIRUS; FIBROBLASTS; GENE EXPRESSION REGULATION, VIRAL; GENES, IMMEDIATE-EARLY; HUMANS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; TRANSCRIPTION FACTORS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5;

EID: 22544446190     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.15.9597-9607.2005     Document Type: Article

References (74)

1. Aoyama, T., T. Okamoto, S. Nagayama, K. Nishijo, T. Ishibe, K. Yasura, T. Nakayama, T. Nakamura, and J. Toguchida. 2004. Methylation in the core-promoter region of the chondromodulin-I gene determines the cell-specific expression by regulating the binding of transcriptional activator Sp3. J. Biol. Chem. 279:28789-28797.
2. Apt, D., R. M. Watts, G. Suske, and H. U. Bernard. 1996. High Sp1/Sp3 ratios in epithelial cells during epithelial differentiation and cellular transformation correlate with the activation of the HPV-16 promoter. Virology 224:281-291.
3. Baldick, C. J., A. Marchini, C. E. Patterson, and T. Shenk. 1997. Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J. Virol. 71:4400-4408.
4. Benedict, C. A., A. Angulo, G. Patterson, S. Ha, H. Huang, M. Messerle, C. F. Ware, and P. Ghazal. 2004. Neutrality of the canonical NF-κB-dependent pathway for human and murine cytomegalovirus transcription and replication in vitro. J. Virol. 78:741-750.
5. Boekhoudt, G. H., Z. Guo, G. W. Beresford, and J. M. Boss. 2003. Communication between NF-κB and Sp1 controls histone acetylation within the proximal promoter of the monocyte chemoattractant protein 1 gene. J. Immunol. 170:4139-4147.
6. Bresnahan, W. A., and T. E. Shenk. 2000. UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells. Proc. Natl. Acad. Sci. USA 97:14506-14511.
7. Britt, W. J., and C. A. Alford. 1996. Cytomegaloviruses, p. 2493-2523. In D. M. Knipe, B. Roizman, P. M. Howley, T. P. Monath, S. E. Straus, R. M. Chanock, J. L. Melnick, and B. N. Fields (ed.), Fields virology, 3rd ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
8. Butz, K., and F. Hoppe-Seyler. 1993. Transcriptional control of human papillomavirus (HPV) oncogene expression: composition of the HPV type 18 upstream regulatory region. J. Virol. 67:6476-6486.
9. Chang, C.-P., C. L. Malone, and M. F. Stinski. 1989. A human cytomegalovirus early gene has three inducible promoters that are regulated differentially at various times after infection. J. Virol. 63:281-290.
10. 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 basal enhancers and cyclic-AMP response elements. J. Virol. 64:264-277.
11. Chen, J. L., L. D. Attardi, C. P. Verrijzer, K. Yokomori, and R. Tjian. 1994. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell 79:93-105.
12. 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.
13. Dorsch-Hasler, K., G. M. Keil, F. Weber, J. M. Schaffner, and U. H. Koszinowski. 1985. A long and complex enhancer activates transcription of the gene coding for the highly abundant immediate early mRNA in murine cytomegalovirus. Proc. Natl. Acad. Sci. USA 82:8325-8329.
14. Dunn, W., C. Chou, H. Li, R. Hai, D. Patterson, V. Stolc, H. Zhu, and F. Liu. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 100:14223-14228.
15. Ellis, H. M., D. Yu, T. DiTizio, and D. L. Court. 2001. High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc. Natl. Acad. Sci. USA 98:6742-6746.
16. Emami, K. H., W. W. Navarre, and S. T. Smale. 1995. Core promoter specificities of the Sp1 and VP16 transcriptional activation domains. Mol. Cell. Biol. 15:5906-5916.
17. Fish, K. N., W. Britt, and J. A. Nelson. 1996. A novel mechanism for persistence of human cytomegalovirus in macrophages. J. Virol. 70:1855-1862.
18. Fish, K. N., A. S. Depto, A. V. Moses, W. Britt, and J. A. Nelson. 1995. Growth kinetics of human cytomegalovirus are altered in monocyte-derived macrophages. J. Virol. 69:3737-3743.
19. Gawn, J. M., and R. F. Greaves. 2002. Absence of IE1 p72 protein function during low-multiplicity infection by human cytomegalovirus results in a broad block to viral delayed-early gene expression. J. Virol. 76:4441-4455.
20. Graham, F. L., and A. J. van der Eb. 1973. A new technique for the assay of infectivity of adenovirus 5 DNA. Virology 52:456-467.
21. Greaves, R. F., and E. S. Mocarski. 1998. Defective growth correlates with reduced accumulation of viral DNA replication protein after low-multiplicity infection by a human cytomegalovirus ie1 mutant. J. Virol. 72:366-379.
22. Hahn, G., R. Jores, and E. S. Mocarski. 1998. Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc. Natl. Acad. Sci. USA 95:3937-3942.
23. Hahn, G., D. Rose, M. Wagner, S. Rhiel, and M. A. McVoy. 2003. Cloning of the genomes of human cytomegalovirus strains Toledo, TownevarRIT3, and Towne long as BACs and site-directed mutagenesis using a PCR-based technique. Virology 307:164-177.
24. Hermiston, T. W., C. L. Malone, P. R. Witte, and M. F. Stinski. 1987. Identification and characterization of the human cytomegalovirus immediate-early region 2 gene that stimulates gene expression from an inducible promoter. J. Virol. 61:3214-3221.
25. Ho, M. 1991. Cytomegalovirus: biology and infection. Plenum Publishing Corp., New York, N.Y.
26. Huang, L., and M. F. Stinski. 1995. Binding of cellular repressor protein or the IE2 protein to a cis-acting negative regulatory element upstream of a human cytomegalovirus early promoter. J. Virol. 69:7612-7621.
27. Ibanez, C. E., R. Schrier, P. Ghazal, C. Wiley, and J. A. Nelson. 1991. Human cytomegalovirus productively infects primary differentiated macrophages. J. Virol. 65:6581-6588.
28. Ihn, H., and M. Trojanowska. 1997. Sp3 is a transcriptional activator of the human alpha2(I) collagen gene. Nucleic Acids Res. 25:3712-3717.
29. Isomura, H., and M. F. Stinski. 2003. The human cytomegalovirus major immediate-early enhancer determines the efficiency of immediate-early gene transcription and viral replication in permissive cells at low multiplicity of infection. J. Virol. 77:3602-3614.
30. Isomura, H., T. Tsurumi, and M. F. Stinski. 2004. Role of the proximal enhancer of the major immediate-early promoter in human cytomegalovirus replication. J. Virol. 78:12788-12799.
31. Jeang, K. F., D. R. Rawlins, P. J. Rosenfeld, J. H. Shero, T. J. Kelly, and G. S. Hayward. 1987. Multiple tandemly repeated binding sites for cellular nuclear factor 1 that surround the major immediate-early promoters of simian and human cytomegalovirus. J. Virol. 61:1559-1570.
32. Keller, M. J., D. G. Wheeler, E. Cooper, and J. L. Meier. 2003. Role of the human cytomegalovirus major immediate-early promoter's 19-base-pair-repeat cyclic AMP-response element in acutely infected cells. J. Virol. 77:6666-6675.
33. Kingsley, C., and A. Winoto. 1992. Cloning of GT box-binding proteins: a novel Sp1 multigene family regulating T-cell receptor gene expression. Mol. Cell. Biol. 12:4251-4261.
34. Kitazawa, S., R. Kitazawa, and S. Maeda. 1999. Transcriptional regulation of rat cyclin D1 gene by CpG methylation status in promoter region. J. Biol. Chem. 274:28787-28793.
35. Kobayashi, M., and K. Kawakami. 1997. Synergism of the ATF/CRE site and GC box in the housekeeping Na,K-ATPase alpha 1 subunit gene is essential for constitutive expression. Biochem. Biophys. Res. Commun. 241:169-174.
36. 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.
37. Kondo, K., J. Xu, and E. S. Mocarski. 1996. Human cytomegalovirus latent gene expression in granulocyte-macrophage progenitors in culture and in seropositive individuals. Proc. Natl. Acad. Sci. USA 93:11137-11142.
38. Lackner, D. F., and N. Muzyczka. 2002. Studies of the mechanism of transactivation of the adeno-associated virus p19 promoter by Rep protein. J. Virol. 76:8225-8235.
39. Lashmit, P. E., J. L. Meier, and M. F. Stinski. 2002. Mutation of a consensus Fox (HNF-3) protein binding site upstream of the human cytomegalovirus UL127 promoter results in a loss of repression of gene expression. J. Virol. 78:5113-5123.
40. Lashmit, P. E., M. F. Stinski, E. A. Murphy, and G. C. Bullock. 1998. A cis repression sequence adjacent to the transcription start site of the human cytomegalovirus US3 gene is required to down regulate gene expression at early and late times after infection. J. Virol. 72:9575-9584.
41. Lathey, J. L., and S. A. Spector. 1991. Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. J. Virol. 65:6371-6375.
42. Liang, Y., D. F. Robinson, J. Dennig, G. Suske, and W. E. Fahl. 1996. Transcriptional regulation of the SIS/PDGF-B gene in human osteosarcoma cells by the Sp family of transcription factors. J. Biol. Chem. 271:11792-11797.
43. 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.
44. Liu, B., and M. F. Stinski. 1992. Human cytomegalovirus contains a tegument protein that enhances transcription from promoters with upstream ATF and AP-1 cis-acting elements. J. Virol. 66:4434-4444.
45. Lundquist, C. A., J. L. Meier, and M. F. Stinski. 1999. A strong negative transcriptional regulatory region between the human cytomegalovirus UL127 gene and the major immediate-early enhancer. J. Virol. 73:9039-9052.
46. Macias, M. P., L. Huang, P. E. Lashmit, and M. F. Stinski. 1996. Cellular and viral protein binding to a cytomegalovirus promoter transcription initiation site: effects on transcription. J. Virol. 70:3628-3635.
47. Marchini, A., H. Liu, and H. Zhu. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J. Virol. 75:1870-1878.
48. Meier, J. L. 2001. Reactivation of the human cytomegalovirus major immediate-early regulatory region and viral replication in embryonal NTera2 cells: role of trichostatin A, retinoic acid, and deletion of the 21-base-pair repeats and modulator. J. Virol. 75:1581-1593.
49. Meier, J. L., M. J. Keller, and J. J. McCoy. 2002. Requirement of multiple cis-acting elements in the human cytomegalovirus major immediate-early distal enhancer for viral gene expression and replication. J. Virol. 76:313-326.
50. Meier, J. L., and J. A. Pruessner. 2000. The human cytomegalovirus major immediate-early distal enhancer region is required for efficient viral replication and immediate-early gene expression. J. Virol. 74:1602-1613.
51. Meier, J. L., and M. F. Stinski. 1997. Effect of a modulator deletion on transcription of the human cytomegalovirus major immediate-early genes in infected undifferentiated and differentiated cells. J. Virol. 71:1246-1255.
52. Meier, J. L., and M. F. Stinski. 1996. Regulation of human cytomegalovirus immediate-early gene expression. Intervirology 39:331-342.
53. Murphy, J. C., W. Fischle, E. Verdin, and J. H. Sinclair. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21:1112-1120.
54. Owen, G. I., J. K. Richer, L. Tung, G. Takimoto, and K. B. Horwitz. 1998. Progesterone regulates transcription of the p21(WAF1) cyclin-dependent kinase inhibitor gene through Sp1 and CBP/p300. J. Biol. Chem. 273:10696-10701.
55. Pereira, D. J., and N. Muzyczka. 1997. The cellular transcription factor SP1 and an unknown cellular protein are required to mediate Rep protein activation of the adeno-associated virus p19 promoter. J. Virol. 71:1747-1756.
56. 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 located near the cap site. J. Virol. 64:6154-6165.
57. Saluja, D., M. F. Vassallo, and N. Tanese. 1998. Distinct subdomains of human TAFII130 are required for interactions with glutamine-rich transcriptional activators. Mol. Cell. Biol. 18:5734-5743.
58. Sapetschnig, A., F. Koch, G. Rischitor, T. Mennenga, and G. Suske. 2004. Complexity of translationally controlled transcription factor Sp3 isoform expression. J. Biol. Chem. 279:42095-42105.
59. Sinzger, C., A. Grefte, B. Plachter, A. S. H. Gouw, T. Hauw The, and G. Jahn. 1995. Fibroblasts, epithelial cells, endothelial cells, and smooth muscle cells are the major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J. Gen. Virol. 76:741-750.
60. Sinzger, C., B. Plachter, A. Grefte, A. S. H. Gouw, T. H. The, and G. Jahn. 1996. Tissue macrophages are infected by human cytomegalovirus. J. Infect. Dis. 173:240-245.
61. Stinski, M. F. 1999. Cytomegalovirus promoter for expression in mammalian cells, p. 211-233. In J. M. Ferandez and J. P. Hoeffler (ed.), Gene expression systems: using nature for the art of expression. Academic Press, San Diego, Calif.
62. Stinski, M. F. 1978. Sequence of protein synthesis in cells infected by human cytomegalovirus: early and late virus-induced polypeptides. J. Virol. 26:686-701.
63. Supp, D. M., D. P. Witte, W. W. Branford, E. P. Smith, and S. S. Potter. 1996. Sp4, a member of the Sp1-family of zinc finger transcription factors, is required for normal murine growth, viability, and male fertility. Dev. Biol. 176:284-299.
64. Suske, G. 1999. The Sp-family of transcription factors. Gene 238:291-300.
65. 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.
66. Tsai, E. Y., J. V. Falvo, A. V. Tsytsykova, A. K. Barczak, A. M. Reimold, L. H. Glimcher, M. J. Fenton, D. C. Gordon, I. F. Dunn, and A. E. Goldfeld. 2000. A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor alpha promoter in vivo. Mol. Cell. Biol. 20:6084-6094.
67. Verrijzer, C. P., J. L. Chen, K. Yokomori, and R. Tjian. 1995. Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II. Cell 81:1115-1125.
68. Verrijzer, C. P., K. Yokomori, J. L. Chen, and R. Tjian. 1994. Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science 264:933-941.
69. Wathen, M. W., and M. F. Stinski. 1982. Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. J. Virol. 41:462-477.
70. Yurochko, A. D., E.-S. Hwang, L. Rasmussen, S. Keay, L. Pereira, and E.-S. Huang. 1997. The human cytomegalovirus UL55 (gB) and UL75 (gH) glycoprotein ligands initiate the rapid activation of Sp1 and NF-κB during infection. J. Virol. 71:5051-5059.
71. Yurochko, A. D., T. F. Kowalik, S. M. Huong, and E. S. Huang. 1995. Human cytomegalovirus upregulates NF-kappa B activity by transactivating the NF-kappa B p105/p50 and p65 promoters. J. Virol. 69:5391-5400.
72. Yurochko, A. D., M. W. Mayo, E. E. Poma, A. S. Baldwin, Jr., and E. S. Huang. 1997. Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-kappaB promoters. J. Virol. 71:4638-4648.
73. Zhao, L., and L. S. Chang. 1997. The human POLD1 gene. Identification of an upstream activator sequence, activation by Sp1 and Sp3, and cell cycle regulation. J. Biol. Chem. 272:4869-4882.
74. Zhu, W. G., K. Srinivasan, Z. Dai, W. Duan, L. J. Druhan, H. Ding, L. Yee, M. A. Villalona-Calero, C. Plass, and G. A. Otterson. 2003. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol. Cell. Biol. 23:4056-4065.