The differentiation-specific factor CDP/Cut represses transcription and replication of human papillomaviruses through a conserved silencing element

Journal of Virology

Volumn 74, Issue 1, 2000, Pages 401-410

  O'Connor, Mark J ^a,b   Stünkel, Walter ^a   Koh, Choon Heng ^a   Zimmermann, Holger ^a   Bernard, Hans Ulrich ^a  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b KuDOS Pharmaceutical Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; REPRESSOR PROTEIN;

ARTICLE; EPISOME; EPITHELIUM; GENE OVEREXPRESSION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; REGULATOR GENE; SILENCER GENE; TISSUE DIFFERENTIATION; TRANSCRIPTION REGULATION; VIRUS INHIBITION;

EID: 0343750713     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.1.401-410.2000     Document Type: Article

References (69)

1. Ai, W., E. Toussaint, and A. Roman. 1999. CCAAT displacement protein binds to and negatively regulates human papillomavirus type 6 E6, E7, and E1 promoters. J. Virol. 73:4220-4229.
2. Anderson, B., A. Hariri, M. R. Pittelkow, and M. G. Rosenfeld. 1997. Characterization of Skin-1a/i POU domain factors and linkage to papillomavirus gene expression. J. Biol. Chem. 272:15905-15913.
3. Andres, V., M. D. Chiara, and V. Mahdavi. 1994. A new bipartite DNA-binding domain: cooperative interaction between the cut repeat and homeo domain of the cut homeo proteins. Genes Dev. 8:245-257.
4. Apt, D., V. Liu, and H. U. Bernard. 1994. Cloning and functional analysis of spliced isoforms of human nuclear factor I-X: interference with transcriptional activation by NFI/CTF in a cell type specific manner. Nucleic Acids Res. 22:3825-3833.
5. Apt, D., R. M. Watts, G. Suske, and H. U. Bernard. 1996. High Sp1/Sp3 rations in epithelial cells during epithelial differentiation and cellular transformation correlate with the activation of the HPV-16 promoter. Virology 224:281-291.
6. Aufiero, B., E. J. Neufeld, and S. H. Orkin. 1994. Sequence-specific DNA binding of individual cut repeat of the human CCAAT displacement/cut homeodomain protein. Proc. Natl. Acad. Sci. USA 91:7757-7761.
7. Banan, M., I. C. Rojas, W. H. Lee, H. L. King, J. V. Harriss, R. Kobayashi, C. F. Webb, and P. D. Gottlieb. 1197. Interaction of the nuclear matrix associated region (MAR)-binding proteins, SATB1 and CDP/Cux, with a MAR element (L2a) in an upstream regulatory region of the mouse CD8a gene. J. Biol. Chem. 272:18440-18452.
8. Barberis, A., G. Superti-Furga, and M. Busslinger. 1987. Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell 50:347-359.
9. Bauknecht, T., P. Angel, H. D. Royer, and H. zur Hausen. 1992. Identification of a negative regulatory domain in the human papillomavirus type 18 promoter: interaction with the transcriptional repressor YY1. EMBO J. 11: 4607-4617.
10. Bedell, M. A., J. B. Hudson, T. R. Golub, M. E. Turyk, M. Hosken, G. D. Wilbanks, and L. A. Laimins. 1991. Amplification of human papillomavirus genomes in vitro is dependent on epithelial differentiation. J. Virol. 65: 2254-2260.
11. Chan, W. K., G. Klock, and H. U. Bernard. 1989. Progesterone and glucocorticoid response elements occur in the long control regions of several human papillomaviruses involved in anogenital neoplasia. J. Virol. 63:3261-3269.
12. Chiang, C. M., M. Ustav, A. Stenlund, T. F. Ho, T. R. Broker, and L. Chow. 1992. Viral E1 and E2 proteins support replication of homologous and heterologous papillomaviral origins. Proc. Natl. Acad. Sci. USA 89:5799-5803.
13. Chong, T., D. Apt, B. Gloss, M. Isa, and H. U. Bernard. 1991 The enhancer of human papillomavirus-16: Binding sites for the ubiquitous transcription factors oct-1, NFA, TEF-2, NFI, and API participate in the epithelial specific transcription. J. Virol. 65:5933-5943.
14. Cripe, T. P., T. H. Haugen, J. P. Turk, F. Tabatabai, P. G. Schmid, M. Dürst, L. Gissmann, A. Roman, and L. P. Turek. 1987. Transcriptional regulation of the human papillomavirus-16 E6-E7 promoter by a keratinocyte-dependent enhancer, and by viral E2 trans-activator and repressor gene products: implications for cervical carcinogenesis. EMBO J. 6:3745-3753.
15. Del Vecchio, A. M., H. Romanczuk, P. M. Howley, and C. C. Baker. 1992. Transient replication of human papillomavirus DNAs. J. Virol. 66:5949-5948.
16. Demeret, C., C. Desaintes, M. Yaniv, and F. Thierry. 1997. Different mechanisms contribute to the E2-mediated transcriptional repression of human papillomavirus type 18 viral oncogenes. J. Virol. 71:9343-9349.
17. Dignam, J. D., R. M. Lebowitz, 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.
18. Dollard, S. C., T. R. Broker, and L. T. Chow. 1993. Regulation of the human papillomavirus type 11 E6 promoter by viral and host transcription factors in primary human keratinocytes. J. Virol. 67:1721-1726.
19. Dong, G., T. R. Broker, and L. T. Chow. 1994. Human papillomavirus type 11 E2 proteins repress the homologous E6 promoter by interfering with the binding of host transcription factors to adjacent elements. J. Virol. 68: 1115-1127.
20. Flores, E. R., and P. F. Lambert. 1997. Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J. Virol. 71:7167-7179.
21. Frattini, M. G., and L. A. Laimins. 1994. Binding of the human papillomavirus E1 origin-recognition protein is regulated through complex formation with the E2 enhancer-binding protein. Proc. Natl. Acad. Sci. USA 91:12398-12402.
22. Frattini, M. G., H. B. Lim, and L. A. Laimins. 1996. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiation-dependent late expression. Proc. Natl. Acad. Sci. USA 93:3062-3067.
23. Gloss, B., H. U. Bernard, K. Seedorf, and G. Klock. 1987. The upstream regulatory region of the human papillomavirus-16 contains and E2 protein independent enhancer which is specific for cervical carcinoma cells and regulated by glucocorticoid hormones. EMBO J. 6:3735-3743.
24. Gloss, B., T. Chong, and H. U. Bernard. 1989. Numerous nuclear proteins bind the long control region of human papillomavirus type 16: a subset of 6 of 23 DNase I-protected segments coincides with the location of the cell-type-specific enhancer. J. Virol. 63:1142-1152.
25. Harada, R., G. Beruhe, O. J. Tamplin, C. Denis-Larose, and A. Nepveu. 1995. DNA-binding specificity of the cut repeats from the human cut-like protein. Mol. Cell. Biol. 15:129-140.
26. Holt, S. E., and V. G. Wilson. 1995. Mutational analysis of the 18-base-pair inverted repeat element at the bovine papillomavirus origin of replication: identification of critical sequences for E1 binding and in vivo replication. J. Virol. 69:6525-6532.
27. Hubert, W. G., T. Kanaya, and L. A. Laimins. 1999. DNA replication of human papillomavirus type 31 is modulated by elements of the upstream regulatory region that lie 5′ of the minimal origin. J. Virol. 73:1835-1845.
28. Iftner, T., M. Oft, S. Bohm, S. P. Wilczynski, and H. Pfister. 1992. Transcription of the E6 and E7 genes of human papillomavirus type 6 in anogenital condylomata is restricted to undifferentiated cell layers of the epithelium. J. Virol. 66:4639-4646.
29. International Agency for Research on Cancer. 1995. Human papillomaviruses. IARC Monogr. Eval. Carcinog. Risks Hum. 84:35-86.
30. Kopan, R., and E. Fuchs. 1989. A new look into an old problem: keratins as tools to investigate determination, morphogenesis, and differentiation in skin. Genes Dev. 3:1-15.
31. Kuo, S. R., J. S. Liu, T. R. Broker, and L. T. Chow. 1994. Cell-free replication of the human papillomavirus DNA with homologous viral E1 and E2 proteins and human cell extracts. J. Biol. Chem. 269:24058-24065.
32. Kyo, S., A. Tam, and L. A. Laimins. 1995. Transcriptional activity of human papillomavirus type 31b enhancer is regulated through synergistic interaction of AP-1 with two novel cellular factors. Virology 211:184-197.
33. Law, M. F., D. R. Lowy, I. Dvoretzky, and P. M. Howley. 1981. Mouse cells transformed by bovine papillomavirus contain only extrachromosomal viral DNA sequences. Proc. Natl. Acad. Sci. USA 78:2727-2731.
34. Lee, D., H. Sohn, G. V. Kalpana, and J. Choe. 1999. Interaction of E1 and hSNF5 proteins stimulates replication of human papillomavirus DNA. Nature 399:487-491.
35. Li, S., L. Moy, N. Pittman, G. Shue, B. Aufiero, E. J. Neufeld, N. S. LeLeiko, and M. J. Walsh. 1999. Transcriptional repression of the cystic fibrosis transmembrane conductance regulator gene, mediated by CCAAT displacement protein/cut homolog, is associated with histone deacetylation. J. Biol. Chem. 274:7803-7815.
36. Lievens, P. M., J. J. Donady, C. Tufarelli, and E. J. Neufeld. 1995. Repressor activity of CCAAT displacement protein in HL-60 myeloid leukemia cells. J. Biol. Chem. 270:12745-12750.
37. Lu, J. Z., Y. N. Sun, R. C. Rose, W. Bonnez, and D. J. McCance. 1993. Two E2 binding sites (E2BS) alone or one E2BS plus an A/T-rich region are minimal requirements for the replication of the human papillomavirus type 11 origin. J. Virol. 67:7131-7139.
38. Mailly, F., G. Berube, R. Harada, P. L. Mao, S. Phillips, and A. Nepveu. 1996. The human cut homeodomain protein can repress gene expression by two distinct mechanisms: active repression and competition for binding site occupancy. Mol. Cell. Biol. 16:5346-5357.
39. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual, p. 90. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
40. May, M., X. P. Dong, E. Beyer-Finkler, F. Stubenrauch, P. G. Fuchs, and H. Pfister. 1994. The E6/E7 promoter of extrachromosomal HPV16 DNA in cervical cancers escapes from cellular repression by mutation of target sequences for YY1. EMBO J. 13:1460-1466.
41. Mendoza, R., L. Gandhi, and M. R. Botchan. 1995. E1 recognition sequences in the bovine papillomavirus type 1 origin of DNA replication: interaction between half sites of the inverted repeats. J. Virol. 69:3789-3798.
42. Mohr, I. J., R. Clark, S. Sun, E. J. Androphy, P. MacPherson, and M. R. Botchan. 1990. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science 250:1694-1699.
43. Myers, G., H. U. Bernard, H. Dellus, M. Favre, J. Icenogle, M. van Ranst, and C. Wheeler. 1994. Human papillomaviruses. A compilation and analysis of nucleic acid and amino acid sequences, sect. II-LCR, p. 14-16. Los Alamos National Laboratory, Los Alamos, N.M.
44. Neufeld, E. J., D. G. Skalnick, P. M. J. Lievens, and S. H. Orkin. 1992. Human CCAAT displacement protein is homologous to the Drosophila homeoprotein, cut. Nat. Genet. 1:50-55.
45. Nuovo, G. J., P. MacConnell, A. Forde, and P. Delvenne. 1991. Detection of human papillomavirus DNA in formalin-fixed tissues by in situ hybridization after amplification by polymerase chain reaction. Am. J. Pathol. 139:847-854.
46. O'Connor, M., S. Y. Chan, and H. U. Bernard. 1995. Transcription factor binding sites in the long control regions of genital HPVs, part III-A, p. 21-40. In G. Myers, H. U. Bernard, H. Delius, C. Baker, J. Icenogle, A. Halpern, and C. Wheeler (ed.), Human papillomaviruses 1995 compendium. Los Alamos National Laboratory, Los Alamos, N.M. USA.
47. O'Connor, M. J., W. Stünkel, H. Zimmermann, C. H. Koh, and H. U. Bernard. 1998. A novel YY1-independent silencer represses the activity of the human papillomavirus type 16 enhancer. J. Virol. 72:10083-10092.
48. O'Connor, M. J., S. H. Tan, C. H. Tan, and H. U. Bernard. 1996. YY1 represses human papillomavirus type 16 transcription by quenching AP-1 activity. J. Virol. 70:6529-6539.
49. Pattison, S., D. G. Skalnik, and A. Roman. 1997. CCAAT displacement protein, a regulator of differentiation-specific gene expression, binds a negative regulatory element within the 5′ end of the human papillomavirus type 6 long control region. J. Virol. 71:2013-2022.
50. Piirsoo, M., E. Ustav, T. Mandel, A. Stenlund, and M. Ustav. 1996. Cis and trans requirements for stable episomal maintenance of the BPV-1 replicator. EMBO J. 15:1-11.
51. Russell, J., and M. R. Botchan. 1995. cis-acting components of human papillomavirus (HPV) DNA replication: linker substitution analysis of the HPV type 11 origin. J. Virol. 69:651-660.
52. Sallaja, G., R. M. Watts, and H. U. Bernard. 1999. Many different papillomaviruses have low transcriptional activity in spite of strong epithelial specific enhancers. J. Gen. Virol. 80:1715-1724.
53. Schule, R., M. Muller, H. Otsuka-Murakami, and R. Renkawitz. 1988. Cooperativity of the glucocorticoid receptor and the CACCC-box binding factor. Nature 332:87-90.
54. Sedman, J., and A. Stenlund. 1996. The initiator protein E1 binds to the bovine papillomavirus origin of replication as a trimeric ring-like structure. EMBO J. 15:5085-5092.
55. Skalnik, D. G., E. C. Strauss, and S. H. Orkin. 1991. CCAAT displacement protein as a repressor of the myelomonocytic-specific gp91-phox gene promoter. J. Biol. Chem. 266:16736-16744.
56. Spalholz, B. A., A. A. McBride, T. Sarafi, and J. Quintero. 1993. Binding of bovine papillomavirus E1 to the origin is not sufficient for DNA replication. Virology 193:201-212.
57. Stoler, M. H., S. M. Wolinsky, A. Whitbeck, T. R. Broker, and L. T. Chow. 1989. Differentiation-linked human papillomavirus types 6 and 11 transcription in genital condylomata revealed by in situ hybridization with message-specific RNA probes. Virology 172:331-340.
58. Stünkel, W., and H. U. Bernard. 1999. The chromatin structure of the long control region of human papillomavirus type 16 represses viral oncoprotein expression. J. Virol. 73:1918-1930.
59. Sverdrup, F., and S. A. Khan. 1995. Two E2 binding sites alone are sufficient to function as the minimal origin of replication of human papillomavirus type 18 DNA. J. Virol. 69:1319-1323.
60. Tan, S. H., D. Bartsch, E. Schwarz, and H. U. Bernard. 1998. Nuclear matrix attachment regions of human papillomavirus type 16 point toward conservation of these genomic elements in all genital papillomaviruses. J. Virol. 72: 3610-3622.
61. Tan, S. H., L. E. C. Leong, P. Walker, and H. U. Bernard. 1994. The human papillomavirus type 16 E2 transcription factor binds with low cooperativity to two flanking sites and represses the E6 promoter through displacement of SpI and TFIID. J. Virol. 68:6411-6420.
62. Thierry, F., G. Spyrou, M. Yaniv, and P. M. Howley. 1992. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J. Virol. 66:3740-3748.
63. Ustav, E., M. Ustav, P. Szymanski, and A. Stenlund. 1993. The bovine papillomavirus origin of replication requires a binding site for the E2 transcriptional activator. Proc. Natl. Acad. Sci. USA 90:898-902.
64. Ustav, M., E. Ustav, P. Szymanski, and A. Stenlund. 1991. Identification of the origin of replication of bovine papillomavirus and characterization of the viral origin recognition factor E1. EMBO J. 10:4321-4329.
65. Wang, Z., A. Goldstein, R. T. Zong, D. Lin, E. J. Neufeld, R. H. Scheuermann, and P. W. Tucker. 1999. Cux/CDP homeoprotein is a component of NF-mNR and represses the immunoglobulin heavy chain intronic enhancer by antagonizing the bright transcription enhancer. Mol. Cell. Biol. 19:284-298.
66. Westin, G., T. Gerster, M. M. Muller, G. Schaffner, and W. Schaffner. 1987. OVEC, a versatile system to study transcription in mammalian cells and cell-free extracts. Nucleic Acids Res. 15:6787-6798.
67. Yang, W. M., C. Inouye, Y. Zeng, D. Bearss, and E. Seto. 1996. Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc. Natl. Acad. Sci. USA 93: 12845-12850.
68. Yukawa, K., K. Butz, T. Yasui, H. Kikutani, and F. Hoppe-Seyler. 1996. Regulation of human papillomavirus transcription by the differentiation-dependent epithelial factor Epoc-1/skn-1a. J. Virol. 70:10-16.
69. zur Hausen, H. 1996. Papillomavirus infections - a major cause of human cancers. Biochim. Biophys. Acta 1288:F55-F78.