Interaction of papillomavirus E2 protein with the Brm chromatin remodeling complex leads to enhanced transcriptional activation

Journal of Virology

Volumn 81, Issue 5, 2007, Pages 2213-2220

  Kumar, R Ajay ^a   Naidu, Samisubbu R ^a   Wang, Xiaoyu ^a   Imbalzano, Anthony N ^a   Androphy, Elliot J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DNA BINDING PROTEIN; GLYCOPROTEIN E2; PROTEIN BRAHMA; PROTEIN SWI; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPISOME; EPSTEIN BARR VIRUS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; BINDING SITES; BOVINE PAPILLOMAVIRUS 1; CATTLE; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; HELA CELLS; HUMAN PAPILLOMAVIRUS 16; HUMANS; MICE; NIH 3T3 CELLS; ONCOGENE PROTEINS, VIRAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; VIRAL PROTEINS;

HUMAN HERPESVIRUS 4; PAPILLOMAVIRIDAE;

EID: 33847191723     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01746-06     Document Type: Article

References (90)

1. Androphy, E. J., D. R. Lowy, and J. T. Schiller. 1987. Bovine papillomavirus E2 trans-activating gene product binds to specific sites in papillomavirus DNA. Nature 325:70-73.
2. Bechtold, V., P. Beard, and K. Raj. 2003. Human papillomavirus type 16 E2 protein has no effect on transcription from episomal viral DNA. J. Virol. 77:2021-2028.
3. Benson, J. D., R. Lawande, and P. M. Howley. 1997. Conserved interaction of the papillomavirus E2 transcriptional activator proteins with human and yeast TFIIB proteins, J. Virol. 71:8041-8047.
4. Boner, W., E. R. Taylor, E. Tsirimonaki, K. Yamane, M. S. Campo, and I. M. Morgan. 2002. A functional interaction between the human papillomavirus 16 transcription/replication factor E2 and the DNA damage response protein TopBP1. J. Biol. Chem. 277:22297-22303.
5. Breeden, L., and K. Nasmyth. 1987. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48:389-397.
6. Breiding, D. E., M. J. Grossel, and E. J. Androphy. 1996. Genetic analysis of the bovine papillomavirus E2 transcriptional activation domain. Virology 221:34-43.
7. Breiding, D. E., F. Sverdrup, M. J. Grossel, N. Moscufo, W. Boonchai, and E. J. Androphy. 1997. Functional interaction of a novel cellular protein with the papillomavirus E2 transactivation domain. Mol. Cell. Biol. 17:7208-7219.
8. Brown, R. C., S. Pattison, J. van Ree, E. Coghill, A. Perkins, S. M. Jane, and J. M. Cunningham. 2002. Distinct domains of erythroid Krüppel-like factor modulate chromatin remodeling and transactivation at the endogenous β-globin gene promoter. Mol. Cell. Biol. 22:161-170.
9. Chiba, H., M. Muramatsu, A. Nomoto, and H. Kato. 1994. Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. Nucleic Acids Res. 22:1815-1820.
10. Cote, J., J. Quinn, J. L. Workman, and C. L. Peterson. 1994. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265:53-60.
11. de la Serna, I. L., Y. Ohkawa, and A. N. Imbalzano. 2006. Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat. Rev. Genet. 7:461-473.
12. del Mar Pena, L. M., and L. A. Laimins. 2001. Differentiation- dependent chromatin rearrangement coincides with activation of human papillomavirus type 31 late gene expression, J. Virol. 75:10005-10013.
13. 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.
14. 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.
15. Dostatni, N., P. F. Lambert, R. Sousa, J. Ham, P. M. Howley, and M. Yaniv. 1991. The functional BPV-1 E2 trans-activating protein can act as a repressor by preventing formation of the initiation complex. Genes Dev. 5:1657-1671.
16. Dostatni, N., F. Thierry, and M. Yaniv. 1988. A dimer of BPV-1 E2 containing a protease resistant core interacts with its DNA target. EMBO J. 7:3807-3816.
17. Duan, H., C. A. Heckman, and L. M. Boxer. 2005. Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas. Mol. Cell. Biol. 25:1608-1619.
18. Fan, H. Y., K. W. Trotter, T. K. Archer, and R. E. Kingston. 2005. Swapping function of two chromatin remodeling complexes. Mol. Cell 17:805-815.
19. Favre, M., F. Breitburd, O. Croissant, and G. Orth. 1977. Chromatin-like structures obtained after alkaline disruption of bovine and human papillomaviruses. J. Virol. 21:1205-1209.
20. Fehrmann, F., and L. A. Laimins. 2003. Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation. Oncogene 22:5201-5207.
21. Fry, C. J., and C. L. Peterson. 2001. Chromatin remodeling enzymes: who's on first? Curr. Biol. 11:R185-R197.
22. Gallimore, P. H., and A. S. Turnell. 2001. Adenovirus E1A: remodelling the host cell, a life or death experience. Oncogene 20:7824-7835.
23. 0 cells. Mol. Cell 12:255-260.
24. Gloss, B., M. Kalantari, and H. U. Bernard. 2005. Analysis of the regulation of viral transcription. Methods Mol. Med. 119:261-278.
25. Goodwin, E. C., and D. DiMaio. 2000. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. USA 97:12513-12518.
26. Goodwin, E. C., L. K. Naeger, D. E. Breiding, E. J. Androphy, and D. DiMaio. 1998. Transactivation-competent bovine papillomavirus E2 protein is specifically required for efficient repression of human papillomavirus oncogene expression and for acute growth inhibition of cervical carcinoma cell lines. J. Virol. 72:3925-3934.
27. Hawley-Nelson, P., E. J. Androphy, D. R. Lowy, and J. T. Schiller. 1988. The specific DNA recognition sequence of the bovine papillomavirus E2 protein is an E2-dependent enhancer. EMBO J. 7:525-531.
28. Hou, S. Y., S. Y. Wu, T. Zhou, M. C. Thomas, and C. M. Chiang. 2000. Alleviation of human papillomavirus E2-mediated transcriptional repression via formation of a TATA binding protein (or TFIID)-TFIIB-RNA polymerase II-TFIIF preinitiation complex. Mol. Cell. Biol. 20:113-125.
29. Huang, M., F. Qian, Y. Hu, C. Ang, Z. Li, and Z. Wen. 2002. Chromatin-remodelling factor BRG1 selectively activates a subset of interferon-alpha-inducible genes. Nat. Cell Biol. 4:774-781.
30. Ilves, I., S. Kivi, and M. Ustav. 1999. Long-term episomal maintenance of bovine papillomavirus type 1 plasmids is determined by attachment to host chromosomes, which is mediated by the viral E2 protein and its binding sites. J. Virol. 73:4404-4412.
31. Ilves, I., K. Maemets, T. Silla, K. Janikson, and M. Ustav. 2006. Brd4 is involved in multiple processes of the bovine papillomavirus type 1 life cycle. J. Virol. 80:3660-3665.
32. Imbalzano, A. N., H. Kwon, M. R. Green, and R. E. Kingston. 1994. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370:481-485.
33. Jaskelioff, M., I. M. Gavin, C. L. Peterson, and C. Logie. 2000. SWI-SNF-mediated nucleosome remodeling: role of histone octamer mobility in the persistence of the remodeled state. Mol. Cell. Biol. 20:3058-3068.
34. Kadam, S., and B. M. Emerson. 2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11:377-389.
35. Khavari, P. A., C. L. Peterson, J. W. Tamkun, D. B. Mendel, and G. R. Crabtree. 1993. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:170-174.
36. Kovelman, R., G. K. Bilter, E. Glezer, A. Y. Tsou, and M. S. Barbosa. 1996. Enhanced transcriptional activation by E2 proteins from the oncogenic human papillomaviruses. J. Virol. 70:7549-7560.
37. Kuzmichev, A., Y. Zhang, H. Erdjument-Bromage, P. Tempst, and D. Reinberg. 2002. Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Mol. Cell. Biol. 22:835-848.
38. 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 SW1/SNF complex. Nature 370:477-481.
39. Lambert, P. F., N. Dostatni, A. A. McBride, M. Yaniv, P. M. Howley, and B. Arcangioli. 1989. Functional analysis of the papilloma virus E2 trans-activator in Saccharomyces cerevisiae. Genes Dev. 3:38-48.
40. Lee, D., C. Lim, T. Seo, H. Kwon, H. Min, and J. Choe. 2002. The viral oncogene human papillomavirus E7 deregulates transcriptional silencing by Brm-related gene 1 via molecular interactions. J. Biol. Chem. 277:48842-48848.
41. 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.
42. Li, R., and M. R. Botchan. 1994. Acidic transcription factors alleviate nucleosome-mediated repression of DNA replication of bovine papillomavirus type 1. Proc. Natl. Acad. Sci. USA 91:7051-7055.
43. Li, R., and M. R. Botchan. 1993. The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell 73:1207-1221.
44. Li, R., J. Knight, G. Bream, A. Stenlund, and M. Botchan. 1989. Specific recognition nucleotides and their DNA context determine the affinity of E2 protein for 17 binding sites in the BPV-1 genome. Genes Dev. 3:510-526.
45. Lieberman, P. M. 2006. Chromatin regulation of virus infection. Trends Microbiol. 14:132-140.
46. Liu, H., H. Kang, R. Liu, X. Chen, and K. Zhao. 2002. Maximal induction of a subset of interferon target genes requires the chromatin-remodeling activity of the BAF complex. Mol. Cell. Biol. 22:6471-6479.
47. Liu, K., Y. Luo, F. T. Lin, and W. C. Lin. 2004. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev. 18:673-686.
48. Liu, R., H. Liu, X. Chen, M. Kirby, P. O. Brown, and K. Zhao. 2001. Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell 106:309-318.
49. Logie, C., and C. L. Peterson. 1997. Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J. 16:6772-6782.
50. Marzio, G., M. Tyagi, M. I. Gutierrez, and M. Giacca. 1998. HIV-1 tat transactivator recruits p300 and CREB-binding protein histone acetyltransferases to the viral promoter. Proc. Natl. Acad. Sci. USA 95:13519-13524.
51. McBride, A. A., J. B. Bolen, and P. M. Howley. 1989. Phosphorylation sites of the E2 transcriptional regulatory proteins of bovine papillomavirus type 1. J. Virol. 63:5076-5085.
52. McBride, A. A., J. C. Byrne, and P. M. Howley. 1989. E2 polypeptides encoded by bovine papillomavirus type 1 form dimers through the common carboxyl-terminal domain: transactivation is mediated by the conserved amino-terminal domain. Proc. Natl. Acad. Sci. USA 86:510-514.
53. Morrissey, L. C., J. Barsoum, and E. J. Androphy. 1989. Trans-activation by the bovine papillomavirus E2 protein in Saccharomyces cerevisiae. J. Virol. 63:4422-4425.
54. Muchardt, C., and M. Yaniv. 1993. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J. 12:4279-4290.
55. Neely, K. E., A. H. Hassan, C. E. Brown, L. Howe, and J. L. Workman. 2002. Transcription activator interactions with multiple SWI/SNF subunits. Mol. Cell. Biol. 22:1615-1625.
56. Neigeborn, L., and M. Carlson. 1987. Mutations causing constitutive invertase synthesis in yeast: genetic interactions with snf mutations. Genetics 115:247-253.
57. Pal, S., R. Yun, A. Datta, L. Lacomis, H. Erdjument-Bromage, J. Kumar, P. Tempst, and S. Sif. 2003. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23:7475-7487.
58. Peng, Y. C., D. E. Breiding, F. Sverdrup, J. Richard, and E. J. Androphy. 2000. AMF-1/Gps2 binds p300 and enhances its interaction with papillomavirus E2 proteins. J. Virol. 74:5872-5879.
59. Peterson, C. L. 2002. Chromatin remodeling: nucleosomes bulging at the seams. Curr. Biol. 12:R245-R247.
60. Peterson, C. L., and J. W. Tamkun. 1995. The SWI-SNF complex: a chromatin remodeling machine? Trends Biochem. Sci. 20:143-146.
61. Peterson, C. L., and J. L. Workman. 2000. Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr. Opin. Genet. Dev. 10:187-192.
62. Phelan, M. L., S. Sif, G. J. Narlikar, and R. E. Kingston. 1999. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol. Cell 3:247-253.
63. Prakash, S. S., S. R. Grossman, R. B. Pepinsky, L. A. Laimins, and E. J. Androphy. 1992. Amino acids necessary for DNA contact and dimerization imply novel motifs in the papillomavirus E2 trans-activator. Genes Dev. 6:105-116.
64. Rank, N. M., and P. F. Lambert. 1995. Bovine papillomavirus type 1 E2 transcriptional regulators directly bind two cellular transcription factors, TFIID and TFIIB. J. Virol. 69:6323-6334.
65. Rehtanz, M., H. M. Schmidt, U. Warthorst, and G. Steger. 2004. Direct interaction between nucleosome assembly protein 1 and the papillomavirus E2 proteins involved in activation of transcription. Mol. Cell. Biol. 24:2153-2168.
66. Roberts, C. W., and S. H. Orkin. 2004. The SWI/SNF complex-chromatin and cancer. Nat. Rev. Cancer 4:133-142.
67. Saha, A., J. Wittmeyer, and B. R. Cairns. 2006. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell. Biol. 7:437-447.
68. Salma, N., H. Xiao, E. Mueller, and A. N. Imbalzano. 2004. Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor γ nuclear hormone receptor. Mol. Cell. Biol. 24:4651-4663.
69. Schweiger, M. R., J. You, and P. M. Howley. 2006. Bromodomain protein 4 mediates the papillomavirus E2 transcriptional activation function. J. Virol. 80:4276-4285.
70. Sif, S., A. J. Saurin, A. N. Imbalzano, and R. E. Kingston. 2001. Purification and characterization of mSin3A-containing Brgl and hBrm chromatin remodeling complexes. Genes Dev. 15:603-618.
71. Sif, S., P. T. Stukenberg, M. W. Kirschner, and R. E. Kingston. 1998. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12:2842-2851.
72. Smith, C. L., R. Horowitz-Scherer, J. F. Flanagan, C. L. Woodcock, and C. L. Peterson. 2003. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat. Struct. Biol. 10:141-145.
73. Spalholz, B. A., Y. C. Yang, and P. M. Howley. 1985. Transactivation of a bovine papilloma virus transcriptional regulatory element by the E2 gene product. Cell 42:183-191.
74. Steger, G., J. Ham, O. Lefebvre, and M. Yaniv. 1995. The bovine papillomavirus 1 E2 protein contains two activation domains: one that interacts with TBP and another that functions after TBP binding. EMBO J. 14:329-340.
75. Stern, M., R. Jensen, and I. Herskowitz. 1984. Five SWI genes are required for expression of the HO gene in yeast. J. Mol. Biol. 178:853-868.
76. Swindle, C. S., and J. A. Engler. 1998. Association of the human papillomavirus type 11 E1 protein with histone H1. J. Virol. 72:1994-2001.
77. Tamkun, J. W., R. Deuring, M. P. Scott, M. Kissinger, A. M. Pattatucci, T. C. Kaufman, and J. A. Kennison. 1992. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68:561-572.
78. Tan, S. H., L. C. Leong, P. A. 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 Sp1 and TFIID. J. Virol. 68:6411-6420.
79. Thierry, F., and M. Yaniv. 1987. The BPV-1 trans-acting protein can be either an activator or a repressor of the HPV 18 regulatory region. EMBO J. 6:3391-3397.
80. Ushikai, M., M. J. Lace, Y. Yamakawa, M. Kono, J. Anson, T. Ishiji, S. Parkkinen, N. Wicker, M. E. Valentine, I. Davidson, L. P. Turek, and T. H. Haugen. 1994. trans activation by the full-length E2 proteins of human papillomavirus type 16 and bovine papillomavirus type 1 in vitro and in vivo: cooperation with activation domains of cellular transcription factors. J. Virol. 68:6655-6666.
81. Utley, R. T., J. Cote, T. Owen-Hughes, and J. L. Workman. 1997. SWI/SNF stimulates the formation of disparate activator-nucleosome complexes but is partially redundant with cooperative binding. J. Biol. Chem. 272:12642-12649.
82. Vignali, M., A. H. Hassan, K. E. Neely, and J. L. Workman. 2000. ATP-dependent chromatin-remodeling complexes. Mol. Cell. Biol. 20:1899-1910.
83. Wang, W., J. Cote, Y. Xue, S. Zhou, P. A. Khavari, S. R. Biggar, C. Muchardt, G. V. Kalpana, S. P. Goff, M. Yaniv, J. L. Workman, and G. R. Crabtree. 1996. Purification and biochemical heterogeneity of the mammalian SWI-SNF com-plex. EMBO J. 15:5370-5382.
84. Wen, J., S. Huang, H. Rogers, L. A. Dickinson, T. Kohwi-Shigematsu, and C. T. Noguchi. 2005. SATB1 family protein expressed during early erythroid differentiation modifies globin gene expression. Blood 105:3330-3339.
85. Whitehouse, I., A. Flaus, B. R. Cairns, M. F. White, J. L. Workman, and T. Owen-Hughes. 1999. Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400:784-787.
86. Wu, D. Y., G. V. Kalpana, S. P. Goff, and W. H. Schubach. 1996. Epstein-Barr virus nuclear protein 2 (EBNA2) binds to a component of the human SNF-SWI complex, hSNF5/Ini1. J. Virol. 70:6020-6028.
87. Wu, Z., H. P. Kim, H. H. Xue, H. Liu, K. Zhao, and W. J. Leonard. 2005. Interleukin-21 receptor gene induction in human T cells is mediated by T-cell receptor-induced Sp1 activity. Mol. Cell. Biol. 25:9741-9752.
88. Yang, L., R. Li, I. J. Mohr, R. Clark, and M. R. Botchan. 1991. Activation of BPV-1 replication in vitro by the transcription factor E2. Nature 353:628-632.
89. Yao, J. M., D. E. Breiding, and E. J. Androphy. 1998. Functional interaction of the bovine papillomavirus E2 transactivation domain with TFIIB. J. Virol. 72:1013-1019.
90. Yung, E., M. Sorin, A. Pal, E. Craig, A. Morozov, O. Delattre, J. Kappes, D. Ott, and G. V. Kalpana. 2001. Inhibition of HIV-1 virion production by a transdominant mutant of integrase interactor 1. Nat. Med. 7:920-926.