Transcription factor YY1 interacts with retroviral integrases and facilitates integration of moloney murine leukemia virus cDNA into the host chromosomes

Journal of Virology

Volumn 84, Issue 16, 2010, Pages 8250-8261

  Inayoshi, Yujin ^a   Okino, Yuuki ^a   Miyake, Katsuhide ^a   Mizutani, Akifumi ^a   Yamamoto Kishikawa, Junko ^a   Kinoshita, Yuya ^a   Morimoto, Yusuke ^a   Imamura, Kazuhito ^a   Morshed, Mahboob ^a   Kono, Ken ^a   Itoh, Toshinari ^a   Nishijima, Ken Ichi ^a   Iijima, Shinji ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INTEGRASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR YY1;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; DNA SYNTHESIS; ENHANCER REGION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; MOLONEY LEUKEMIA ONCOVIRUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SOUTHERN BLOTTING; VIRUS TYPING;

AVIAN SARCOMA VIRUSES; CELL FRACTIONATION; DNA, COMPLEMENTARY; DNA, VIRAL; GENE KNOCKDOWN TECHNIQUES; HIV-1; HUMANS; IMMUNOPRECIPITATION; INTEGRASES; MOLONEY MURINE LEUKEMIA VIRUS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; VIRAL PROTEINS; VIRUS INTEGRATION; YY1 TRANSCRIPTION FACTOR;

AVIAN SARCOMA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 77954982680     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02681-09     Document Type: Article

References (70)

1. Austen, M., B. Lüscher, and J. M. Lüscher-Firzlaff. 1997. Characterization of the transcriptional regulator YY1. J. Biol. Chem. 272:1709-1717.
2. Belak, Z. R., and N. Ovsenek. 2007. Assembly of the Yin Yang 1 transcription factor into messenger ribonucleoprotein particles requires direct RNA binding activity. J. Biol. Chem. 282:37913-37920.
3. Busschots, K., A. Voet, M. De Maeyer, J.-C. Rain, S. Emiliani, R. Benarous, L. Desender, Z. Debyser, and F. Christ. 2007. Identification of the LEDGF/p75 binding site in HIV-1 integrase. J. Mol. Biol. 365:1480-1492.
4. Caretti, G., M. Di Padova, B. Micales, G. E. Lyons, and V. Sartorelli. 2004. The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev. 18:2627-2638.
5. Cherepanov, P., G. Maertens, P. Proost, B. Devreese, J. Van Beeumen, Y. Engelborghs, E. De Clercq, and Z. Debyser. 2003. HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 278:372-381.
6. Ciuffi, A., M. Llano, E. Poeschla, C. Hoffmann, J. Leipzig, P. Shinn, J. R. Ecker, and F. Bushman. 2005. A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 11:1287-1289.
7. Coull, J. J., F. Romerio, J.-M. Sun, J. L. Volker, K. M. Galvin, J. R. Davie, Y. Shi, U. Hansen, and D. M. Margolis. 2000. The human factors YY1 and LSF repress the human immunodeficiency virus type 1 long terminal repeat via recruitment of histone deacetylase 1. J. Virol. 74:6790-6799.
8. Dar, M. J., B. Monel, L. Krishnan, M.-C. Shun, F. Di Nunzio, D. E. Helland, and A. Engelman. 2009. Biochemical and virological analysis of the 18-residue C-terminal tail of HIV-1 integrase. Retrovirology 6:94.
9. DeLorbe, W. J., P. A. Luciw, H. M. Goodman, H. E. Varmus, and J. M. Bishop. 1980. Molecular cloning and characterization of avian sarcoma virus circular DNA molecules. J. Virol. 36:50-61.
10. Derse, D., B. Crise, Y. Li, G. Princler, N. Lum, C. Stewart, C. F. McGrath, S. H. Hughes, D. J. Munroe, and X. Wu. 2007. Human T-cell leukemia virus type 1 integration target sites in the human genome: comparison with those of other retroviruses. J. Virol. 81:6731-6741.
11. Drelich, M., R. Wilhelm, and J. Mous. 1992. Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. Virology 188:459-468.
12. Engelman, A., and R. Craigie. 1992. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 66:6361-6369.
13. Engelman, A., A. B. Hickman, and R. Craigie. 1994. The core and carboxylterminal domains of the integrase protein of human immunodeficiency virus type 1 each contribute to nonspecific DNA binding. J. Virol. 68:5911-5917.
14. Engelman, A., I. Oztop, N. Vandegraaff, and N. K. Raghavendra. 2009. Quantitative analysis of HIV-1 preintegration complexes. Methods 47:283-290.
15. Flanagan, J. R., K. G. Becker, D. L. Ennist, S. L. Gleason, P. H. Driggers, B.-Z. Levi, E. Appella, and K. Ozato. 1992. Cloning of a negative transcription factor that binds to the upstream conserved region of Moloney murine leukemia virus. Mol. Cell. Biol. 12:38-44.
16. García, E., C. Marcos-Gutiérrez, M. del Mar Lorente, J. C. Moreno, and M. Vidal. 1999. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1. EMBO J. 18:3404-3418.
17. Gordon, S., G. Akopyan, H. Garban, and B. Bonavida. 2006. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25:1125-1142.
18. Greger, J. G., R. A. Katz, A. M. Ishov, G. G. Maul, and A. M. Skalka. 2005. The cellular protein Daxx interacts with avian sarcoma virus integrase and viral DNA to repress viral transcription. J. Virol. 79:4610-4618.
19. He, G., and D. M. Margolis. 2002. Counterregulation of chromatin deacetylation and histone deacetylase occupancy at the integrated promoter of human immunodeficiency virus type 1 (HIV-1) by the HIV-1 repressor YY1 and HIV-1 activator Tat. Mol. Cell. Biol. 22:2965-2973.
20. Holman, A. G., and J. M. Coffin. 2005. Symmetrical base preferences surrounding HIV-1, avian sarcoma/leukosis virus, and murine leukemia virus integration sites. Proc. Natl. Acad. Sci. U. S. A. 102:6103-6107.
21. Hotta, A., Y. Saito, K. Kyogoku, Y. Kawabe, K. Nishijima, M. Kamihira, and S. Iijima. 2006. Characterization of transient expression system for retroviral vector production. J. Biosci. Bioeng. 101:361-368.
22. Iba, H., T. Mizutani, and T. Ito. 2003. SWI/SNF chromatin remodelling complex and retroviral gene silencing. Rev. Med. Virol. 13:99-110.
23. Johnson, M. S., M. A. McClure, D.-F. Feng, J. Gray, and R. F. Doolittle. 1986. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc. Natl. Acad. Sci. U. S. A. 83:7648-7652.
24. Kalpana, G. V., S. Marmon, W. Wang, G. R. Crabtree, and S. P. Goff. 1994. Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266:2002-2006.
25. Kamihira, M., K. Ono, K. Esaka, K. Nishijima, R. Kigaku, H. Komatsu, T. Yamashita, K. Kyogoku, and S. Iijima. 2005. High-level expression of single-chain Fv-Fc fusion protein in serum and egg white of genetically manipulated chickens by using a retroviral vector. J. Virol. 79:10864-10874.
26. Kulkosky, J., K. S. Jones, R. A. Katz, J. P. G. Mack, and A. M. Skalka. 1992. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol. 12:2331-2338.
27. Lai, L., H. Liu, X. Wu, and J. C. Kappes. 2001. Moloney murine leukemia virus integrase protein augments viral DNA synthesis in infected cells. J. Virol. 75:11365-11372.
28. Lee, J.-S., K. M. Galvin, R. H. See, R. Eckner, D. Livingston, E. Moran, and Y. Shi. 1995. Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes Dev. 9:1188-1198.
29. Lee, J.-S., K. M. Galvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. U. S. A. 90:6145-6149.
30. Lewinski, M. K., M. Yamashita, M. Emerman, A. Ciuffi, H. Marshall, G. Crawford, F. Collins, P. Shinn, J. Leipzig, S. Hannenhalli, C. C. Berry, J. R. Ecker, and F. D. Bushman. 2006. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog. 2:611-622.
31. Lewis, P. F., and M. Emerman. 1994. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J. Virol. 68:510-516.
32. Li, L., J. M. Olvera, K. E. Yoder, R. S. Mitchell, S. L. Butler, M. Lieber, S. L. Martin, and F. D. Bushman. 2001. Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J. 20:3272-3281.
33. Li, M., and R. Craigie. 2005. Processing of viral DNA ends channels the HIV-1 integration reaction to concerted integration. J. Biol. Chem. 280: 29334-29339.
34. Maertens, G., P. Cherepanov, W. Pluymers, K. Busschots, E. De Clercq, Z. Debyser, and Y. Engelborghs. 2003. LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 278:33528-33539.
35. Mansharamani, M., D. R. M. Graham, D. Monie, K. K. Lee, J. E. K. Hildreth, R. F. Siliciano, and K. L. Wilson. 2003. Barrier-to-autointegration factor BAF binds p55 Gag and matrix and is a host component of human immunodeficiency virus type 1 virions. J. Virol. 77:13084-13092.
36. Marshall, H. M., K. Ronen, C. Berry, M. Llano, H. Sutherland, D. Saenz, W. Bickmore, E. Poeschla, and F. D. Bushman. 2007. Role of PSIP1/LEDGF/p75 in lentiviral infectivity and integration targeting. PLoS One 2:e1340.
37. Mitchell, R. S., B. F. Beitzel, A. R. W. Schroder, P. Shinn, H. Chen, C. C. Berry, J. R. Ecker, and F. D. Bushman. 2004. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2:e234.
38. Ono, K., M. Kamihira, Y. Kuga, H. Matsumoto, A. Hotta, T. Itoh, K. Nishijima, N. Nakamura, H. Matsuda, and S. Iijima. 2003. Production of anti-prion scFv-Fc fusion proteins by recombinant animal cells. J. Biosci. Bioeng. 95:231-238.
39. Palko, L., H. W. Bass, M. J. Beyrouthy, and M. M. Hurt. 2004. The Yin Yang-1 (YY1) protein undergoes a DNA-replication-associated switch in localization from the cytoplasm to the nucleus at the onset of S phase. J. Cell Sci. 117:465-476.
40. Petkova, V., M. J. Romanowski, I. Sulijoadikusumo, D. Rohne, P. Kang, T. Shenk, and A. Usheva. 2001. Interaction between YY1 and the retinoblastoma protein. J. Biol. Chem. 276:7932-7936.
41. Puglia, J., T. Wang, C. Smith-Snyder, M. Cote, M. Scher, J. N. Pelletier, S. John, C. B. Jonsson, and M. J. Roth. 2006. Revealing domain structure through linker-scanning analysis of the murine leukemia virus (MuLV) RNase H and MuLV and human immunodeficiency virus type 1 integrase proteins. J. Virol. 80:9497-9510.
42. Roe, T., T. C. Reynolds, G. Yu, and P. O. Brown. 1993. Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 12:2099-2108.
43. Satijn, D. P. E., K. M. Hamer, J. den Blaauwen, and A. P. Otte. 2001. The Polycomb group protein EED interacts with YY1, and both proteins induce neural tissue in Xenopus embryos. Mol. Cell. Biol. 21:1360-1369.
44. Segura-Totten, M., and K. L. Wilson. 2004. BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol. 14:261-266.
45. Serhan, F., M. Penaud, C. Petit, T. Leste-Lasserre, S. Trajcevski, D. Klatzmann, G. Duisit, P. Sonigo, and P. Moullier. 2004. Early detection of a two-long-terminal-repeat junction molecule in the cytoplasm of recombinant murine leukemia virus-infected cells. J. Virol. 78:6190-6199.
46. Shi, Y., J.-S. Lee, and K. M. Galvin. 1997. Everything you have ever wanted to know about Yin Yang 1. . . . Biochim. Biophys. Acta 1332:F49-F66.
47. Shields, A., O. N. Witte, E. Rothenberg, and D. Baltimore. 1978. High frequency of aberrant expression of Moloney murine leukemia virus in clonal infections. Cell 14:601-609.
48. Shun, M.-C., N. K. Raghavendra, N. Vandergraaff, J. E. Daigle, S. Hughes, P. Kellam, P. Cherepanov, and A. Engelman. 2007. LEDGF/p75 functions downstream from preintegration complex formation to effect gene-specific HIV-1 integration. Genes Dev. 21:1767-1778.
49. Simon, J. A., and R. E. Kingston. 2009. Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10:697-708.
50. Studamire, B., and S. P. Goff. 2008. Host proteins interacting with the Moloney murine leukemia virus integrase: multiple transcriptional regulators and chromatin binding factors. Retrovirology 5:48.
51. Suzuki, Y., and R. Craigie. 2007. The road to chromatin-nuclear entry of retroviruses. Nat. Rev. Microbiol. 5:187-196.
52. Suzuki, Y., H. Yang, and R. Craigie. 2004. LAP2α and BAF collaborate to organize the Moloney murine leukemia virus preintegration complex. EMBO J. 23:4670-4678.
53. Thomas, M. J., and E. Seto. 1999. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236:197-208.
54. Tsukahara, T., H. Agawa, S. Matsumoto, M. Matsuda, S. Ueno, Y. Yamashita, K. Yamada, N. Tanaka, K. Kojima, and T. Takeshita. 2006. Murine leukemia virus vector integration favors promoter regions and regional hot spots in a human T-cell line. Biochem. Biophys. Res. Commun. 345:1099-1107.
55. Villanueva, R. A., C. B. Jonsson, J. Jones, M. M. Georgiadis, and M. J. Roth. 2003. Differential multimerization of Moloney murine leukemia virus integrase purified under nondenaturing conditions. Virology 316: 146-160.
56. Violot, S., S. S. Hong, D. Rakotobe, C. Petit, B. Gay, K. Moreau, G. Billaud, S. Priet, J. Sire, O. Schwartz, J.-F. Mouscadet, and P. Boulanger. 2003. The human Polycomb group EED protein interacts with the integrase of human immunodeficiency virus type 1. J. Virol. 77:12507-12522.
57. Wang, C.-Y., Y.-J. Liang, Y.-S. Lin, H.-M. Shih, Y.-S. Jou, and W. C. Y. Yu. 2004. YY1AP, a novel co-activator of YY1. J. Biol. Chem. 279:17750-17755.
58. Wilkinson, T. A., K. Januszyk, M. L. Phillips, S. S. Tekeste, M. Zhang, J. T. Miller, S. F. J. Le Grice, R. T. Clubb, and S. A. Chow. 2009. Identifying and characterizing a functional HIV-1 reverse transcriptase-binding site on integrase. J. Biol. Chem. 284:7931-7939.
59. Woerner, A. M., and C. J. Marcus-Sekura. 1993. Characterization of a DNA binding domain in the C-terminus of HIV-1 integrase by deletion mutagenesis. Nucleic Acids Res. 21:3507-3511.
60. Wu, S., Y. Shi, P. Mulligan, F. Gay, J. Landry, H. Liu, J. Lu, H. H. Qi, W. Wang, J. A. Nickoloff, C. Wu, and Y. Shi. 2007. A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Mol. Biol. 14:1165-1172.
61. Wu, X., Y. Li, B. Crise, and S. M. Burgess. 2003. Transcription start regions in the human genome are favored targets for MLV integration. Science 300:1749-1751.
62. Wu, X., H. Liu, H. Xiao, J. A. Conway, E. Hehl, G. V. Kalpana, V. Prasad, and J. C. Kappes. 1999. Human immunodeficiency virus type 1 integrase protein promotes reverse transcription through specific interactions with the nucleoprotein reverse transcription complex. J. Virol. 73:2126-2135.
63. Xi, H., Y. Yu, Y. Fu, J. Foley, A. Halees, and Z. Weng. 2007. Analysis of overrepresented motifs in human core promoters reveals dual regulatory roles of YY1. Genome Res. 17:798-806.
64. Yan, N., P. Cherepanov, J. E. Daigle, A. Engelman, and J. Lieberman. 2009. The SET complex acts as a barrier to autointegration of HIV-1. PLoS Pathog. 5:e1000327.
65. Yang, F., O. Leon, N. J. Greenfield, and M. J. Roth. 1999. Functional interactions of the HHCC domain of Moloney murine leukemia virus integrase revealed by nonoverlapping complementation and zinc-dependent dimerization. J. Virol. 73:1809-1817.
66. 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. U. S. A. 93:12845-12850.
67. Yang, W.-M., Y.-L. Yao, J.-M. Sun, J. R. Davie, and E. Seto. 1997. Isolation and characterization of cDNAs corresponding to an additional member of the human histone deacetylase gene family. J. Biol. Chem. 272:28001-28007.
68. Yao, Y-L., W.-M. Yang, and E. Seto. 2001. Regulation of transcription factor YY1 by acetylation and deacetylation. Mol. Cell. Biol. 21:5979-5991.
69. Yung, E., M. Sorin, E.-J. Wang, S. Perumal, D. Ott, and G. V. Kalpana. 2004. Specificity of interaction of INI1/hSNF5 with retroviral integrases and its functional significance. J. Virol. 78:2222-2231.
70. Zheng, R., T. M. Jenkins, and R. Craigie. 1996. Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity. Proc. Natl. Acad. Sci. U. S. A. 93:13659-13664.