1887

Abstract

Integrase interactor 1 (Ini1/hSNF5/BAF47/SMARCB1), the core subunit of the ATP-dependent chromatin-remodelling complex SWI/SNF, is a cellular interaction partner of the human immunodeficiency virus type 1 (HIV-1) integrase. Ini1/hSNF5 is recruited to HIV-1 pre-integration complexes before nuclear migration, suggesting a function in the integration process itself or a contribution to the preferential selection of transcriptionally active genes as integration sites of HIV-1. More recent evidence indicates, however, that, whilst Ini1/hSNF5 is dispensable for HIV-1 transduction per se, it may have an inhibitory effect on the early steps of HIV-1 replication but facilitates proviral transcription by enhancing Tat function. These partially contradictory observations prompted an investigation of the immediate and long-term effects of Ini1/hSNF5 depletion on the basal transcriptional potential of the virus promoter. Using small interfering RNAs, it was shown that Ini1/hSNF5-containing SWI/SNF complexes mediate transcriptional repression of the basal activity of the integrated HIV-1 long terminal repeat. Transient depletion of Ini1/hSNF5 during integration was accompanied by an early boost of HIV-1 replication. After the reappearance of Ini1/hSNF5, expression levels decreased and this was associated with increased levels of histone methylation at the virus promoter in the long term, indicative of epigenetic gene silencing. These results demonstrate the opposing effects of Ini1/hSNF5-containing SWI/SNF complexes on basal and Tat-dependent transcriptional activity of the HIV-1 promoter. It is proposed that Ini1/hSNF5 may be recruited to the HIV-1 pre-integration complex to initiate, immediately after integration, one of two mutually exclusive transcription programmes, namely post-integration latency or high-level, Tat-dependent gene expression.

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2009-10-01
2019-11-18
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References

  1. Adler, H. T., Chinery, R., Wu, D. Y., Kussick, S. J., Payne, J. M., Fornace, A. J., Jr & Tkachuk, D. C. ( 1999; ). Leukemic HRX fusion proteins inhibit GADD34-induced apoptosis and associate with the GADD34 and hSNF5/INI1 proteins. Mol Cell Biol 19, 7050–7060.
    [Google Scholar]
  2. Agbottah, E., Deng, L., Dannenberg, L. O., Pumfery, A. & Kashanchi, F. ( 2006; ). Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology 3, 48 [CrossRef]
    [Google Scholar]
  3. Angelov, D., Charra, M., Seve, M., Cote, J., Khochbin, S. & Dimitrov, S. ( 2000; ). Differential remodeling of the HIV-1 nucleosome upon transcription activators and SWI/SNF complex binding. J Mol Biol 302, 315–326.[CrossRef]
    [Google Scholar]
  4. Ariumi, Y., Serhan, F., Turelli, P., Telenti, A. & Trono, D. ( 2006; ). The integrase interactor 1 (INI1) proteins facilitate Tat-mediated human immunodeficiency virus type 1 transcription. Retrovirology 3, 47 [CrossRef]
    [Google Scholar]
  5. Boese, A., Sommer, P., Gaussin, A., Reimann, A. & Nehrbass, U. ( 2004; ). Ini1/hSNF5 is dispensable for retrovirus-induced cytoplasmic accumulation of PML and does not interfere with integration. FEBS Lett 578, 291–296.[CrossRef]
    [Google Scholar]
  6. Brigati, C., Giacca, M., Noonan, D. M. & Albini, A. ( 2003; ). HIV Tat, its TARgets and the control of viral gene expression. FEMS Microbiol Lett 220, 57–65.[CrossRef]
    [Google Scholar]
  7. Bukrinsky, M. ( 2006; ). SNFing HIV transcription. Retrovirology 3, 49 [CrossRef]
    [Google Scholar]
  8. Bushman, F. D. ( 2003; ). Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115, 135–138.[CrossRef]
    [Google Scholar]
  9. Bushman, F., Lewinski, M., Ciuffi, A., Barr, S., Leipzig, J., Hannenhalli, S. & Hoffmann, C. ( 2005; ). Genome-wide analysis of retroviral DNA integration. Nat Rev Microbiol 3, 848–858.[CrossRef]
    [Google Scholar]
  10. Cheng, S. W., Davies, K. P., Yung, E., Beltran, R. J., Yu, J. & Kalpana, G. V. ( 1999; ). c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function. Nat Genet 22, 102–105.[CrossRef]
    [Google Scholar]
  11. Ciuffi, A., Llano, M., Poeschla, E., Hoffmann, C., Leipzig, J., Shinn, P., Ecker, J. R. & Bushman, F. ( 2005; ). A role for LEDGF/p75 in targeting HIV DNA integration. Nat Med 11, 1287–1289.[CrossRef]
    [Google Scholar]
  12. Ciuffi, A., Diamond, T. L., Hwang, Y., Marshall, H. M. & Bushman, F. D. ( 2006; ). Modulating target site selection during human immunodeficiency virus DNA integration in vitro with an engineered tethering factor. Hum Gene Ther 17, 960–967.[CrossRef]
    [Google Scholar]
  13. Felsenfeld, G. & Groudine, M. ( 2003; ). Controlling the double helix. Nature 421, 448–453.[CrossRef]
    [Google Scholar]
  14. Greger, J. G., Katz, R. A., Ishov, A. M., Maul, G. G. & Skalka, A. M. ( 2005; ). The cellular protein Daxx interacts with avian sarcoma virus integrase and viral DNA to repress viral transcription. J Virol 79, 4610–4618.[CrossRef]
    [Google Scholar]
  15. Han, Y., Lassen, K., Monie, D., Sedaghat, A. R., Shimoji, S., Liu, X., Pierson, T. C., Margolick, J. B., Siliciano, R. F. & Siliciano, J. D. ( 2004; ). Resting CD4+ T cells from human immunodeficiency virus type 1 (HIV-1)-infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J Virol 78, 6122–6133.[CrossRef]
    [Google Scholar]
  16. He, G., Ylisastigui, L. & Margolis, D. M. ( 2002; ). The regulation of HIV-1 gene expression: the emerging role of chromatin. DNA Cell Biol 21, 697–705.[CrossRef]
    [Google Scholar]
  17. Henderson, A., Holloway, A., Reeves, R. & Tremethick, D. J. ( 2004; ). Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol Cell Biol 24, 389–397.[CrossRef]
    [Google Scholar]
  18. Hwang, S., Lee, D., Gwack, Y., Min, H. & Choe, J. ( 2003; ). Kaposi's sarcoma-associated herpesvirus K8 protein interacts with hSNF5. J Gen Virol 84, 665–676.[CrossRef]
    [Google Scholar]
  19. Iba, H., Mizutani, T. & Ito, T. ( 2003; ). SWI/SNF chromatin remodelling complex and retroviral gene silencing. Rev Med Virol 13, 99–110.[CrossRef]
    [Google Scholar]
  20. Imbalzano, A. N. & Jones, S. N. ( 2005; ). Snf5 tumor suppressor couples chromatin remodeling, checkpoint control, and chromosomal stability. Cancer Cell 7, 294–295.[CrossRef]
    [Google Scholar]
  21. Jordan, A., Defechereux, P. & Verdin, E. ( 2001; ). The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J 20, 1726–1738.[CrossRef]
    [Google Scholar]
  22. Kalpana, G. V., Marmon, S., Wang, W., Crabtree, G. R. & Goff, S. P. ( 1994; ). Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266, 2002–2006.[CrossRef]
    [Google Scholar]
  23. Katsani, K. R., Mahmoudi, T. & Verrijzer, C. P. ( 2003; ). Selective gene regulation by SWI/SNF-related chromatin remodeling factors. Curr Top Microbiol Immunol 274, 113–141.
    [Google Scholar]
  24. Khorasanizadeh, S. ( 2004; ). The nucleosome: from genomic organization to genomic regulation. Cell 116, 259–272.[CrossRef]
    [Google Scholar]
  25. Kingston, R. E. & Narlikar, G. J. ( 1999; ). ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13, 2339–2352.[CrossRef]
    [Google Scholar]
  26. Kingston, R. E., Bunker, C. A. & Imbalzano, A. N. ( 1996; ). Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev 10, 905–920.[CrossRef]
    [Google Scholar]
  27. Kwiatkowski, B., Chen, S. Y. & Schubach, W. H. ( 2004; ). CKII site in Epstein–Barr virus nuclear protein 2 controls binding to hSNF5/Ini1 and is important for growth transformation. J Virol 78, 6067–6072.[CrossRef]
    [Google Scholar]
  28. Lassen, K., Han, Y., Zhou, Y., Siliciano, J. & Siliciano, R. F. ( 2004; ). The multifactorial nature of HIV-1 latency. Trends Mol Med 10, 525–531.[CrossRef]
    [Google Scholar]
  29. Lee, D., Sohn, H., Kalpana, G. V. & Choe, J. ( 1999; ). Interaction of E1 and hSNF5 proteins stimulates replication of human papillomavirus DNA. Nature 399, 487–491.[CrossRef]
    [Google Scholar]
  30. Lee, D., Kim, J. W., Seo, T., Hwang, S. G., Choi, E. J. & Choe, J. ( 2002; ). SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J Biol Chem 277, 22330–22337.[CrossRef]
    [Google Scholar]
  31. Lusic, M., Marcello, A., Cereseto, A. & Giacca, M. ( 2003; ). Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J 22, 6550–6561.[CrossRef]
    [Google Scholar]
  32. Mahmoudi, T., Parra, M., Vries, R. G., Kauder, S. E., Verrijzer, C. P., Ott, M. & Verdin, E. ( 2006; ). The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. J Biol Chem 281, 19960–19968.[CrossRef]
    [Google Scholar]
  33. Maison, C. & Almouzni, G. ( 2004; ). HP1 and the dynamics of heterochromatin maintenance. Nat Rev Mol Cell Biol 5, 296–304.[CrossRef]
    [Google Scholar]
  34. Marcello, A., Lusic, M., Pegoraro, G., Pellegrini, V., Beltram, F. & Giacca, M. ( 2004; ). Nuclear organization and the control of HIV-1 transcription. Gene 326, 1–11.[CrossRef]
    [Google Scholar]
  35. Maroun, M., Delelis, O., Coadou, G., Bader, T., Segeral, E., Mbemba, G., Petit, C., Sonigo, P., Rain, J. C. & other authors ( 2006; ). Inhibition of early steps of HIV-1 replication by SNF5/Ini1. J Biol Chem 281, 22736–22743.[CrossRef]
    [Google Scholar]
  36. Martens, J. A. & Winston, F. ( 2003; ). Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13, 136–142.[CrossRef]
    [Google Scholar]
  37. Pal, S., Yun, R., Datta, A., Lacomis, L., Erdjument-Bromage, H., Kumar, J., Tempst, P. & Sif, S. ( 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.[CrossRef]
    [Google Scholar]
  38. Peterson, C. L. & Laniel, M. A. ( 2004; ). Histones and histone modifications. Curr Biol 14, R546–R551.[CrossRef]
    [Google Scholar]
  39. Pumfery, A., Deng, L., Maddukuri, A., de la Fuente, C., Li, H., Wade, J. D., Lambert, P., Kumar, A. & Kashanchi, F. ( 2003; ). Chromatin remodeling and modification during HIV-1 Tat-activated transcription. Curr HIV Res 1, 343–362.[CrossRef]
    [Google Scholar]
  40. Rozenblatt-Rosen, O., Rozovskaia, T., Burakov, D., Sedkov, Y., Tillib, S., Blechman, J., Nakamura, T., Croce, C. M., Mazo, A. & Canaani, E. ( 1998; ). The C-terminal SET domains of ALL-1 and TRITHORAX interact with the INI1 and SNR1 proteins, components of the SWI/SNF complex. Proc Natl Acad Sci U S A 95, 4152–4157.[CrossRef]
    [Google Scholar]
  41. Schroder, A. R., Shinn, P., Chen, H., Berry, C., Ecker, J. R. & Bushman, F. ( 2002; ). HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521–529.[CrossRef]
    [Google Scholar]
  42. Sif, S., Saurin, A. J., Imbalzano, A. N. & Kingston, R. E. ( 2001; ). Purification and characterization of mSin3A-containing Brg1 and hBrm chromatin remodeling complexes. Genes Dev 15, 603–618.[CrossRef]
    [Google Scholar]
  43. Sirven, A., Ravet, E., Charneau, P., Zennou, V., Coulombel, L., Guetard, D., Pflumio, F. & Dubart-Kupperschmitt, A. ( 2001; ). Enhanced transgene expression in cord blood CD34+-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol Ther 3, 438–448.[CrossRef]
    [Google Scholar]
  44. Sommer, P., Vartanian, J. P., Wachsmuth, M., Henry, M., Guetard, D. & Wain-Hobson, S. ( 2004; ). Anti-termination by SIV Tat requires flexibility of the nascent TAR structure. J Mol Biol 344, 11–28.[CrossRef]
    [Google Scholar]
  45. Studamire, B. & Goff, S. P. ( 2008; ). Host proteins interacting with the Moloney murine leukemia virus integrase: multiple transcriptional regulators and chromatin binding factors. Retrovirology 5, 48 [CrossRef]
    [Google Scholar]
  46. Treand, C., du Chene, I., Bres, V., Kiernan, R., Benarous, R., Benkirane, M. & Emiliani, S. ( 2006; ). Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter. EMBO J 25, 1690–1699.[CrossRef]
    [Google Scholar]
  47. Turelli, P., Doucas, V., Craig, E., Mangeat, B., Klages, N., Evans, R., Kalpana, G. & Trono, D. ( 2001; ). Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol Cell 7, 1245–1254.[CrossRef]
    [Google Scholar]
  48. Van Lint, C., Emiliani, S., Ott, M. & Verdin, E. ( 1996; ). Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J 15, 1112–1120.
    [Google Scholar]
  49. Van Maele, B., Busschots, K., Vandekerckhove, L., Christ, F. & Debyser, Z. ( 2006; ). Cellular co-factors of HIV-1 integration. Trends Biochem Sci 31, 98–105.[CrossRef]
    [Google Scholar]
  50. Verdin, E., Paras, P., Jr & Van Lint, C. ( 1993; ). Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J 12, 3249–3259.
    [Google Scholar]
  51. Versteege, I., Sevenet, N., Lange, J., Rousseau-Merck, M. F., Ambros, P., Handgretinger, R., Aurias, A. & Delattre, O. ( 1998; ). Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394, 203–206.[CrossRef]
    [Google Scholar]
  52. Wang, W., Cote, J., Xue, Y., Zhou, S., Khavari, P. A., Biggar, S. R., Muchardt, C., Kalpana, G. V., Goff, S. P. & other authors ( 1996; ). Purification and biochemical heterogeneity of the mammalian SWI–SNF complex. EMBO J 15, 5370–5382.
    [Google Scholar]
  53. Wu, D. Y., Kalpana, G. V., Goff, S. P. & Schubach, W. H. ( 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.
    [Google Scholar]
  54. Wu, D. Y., Krumm, A. & Schubach, W. H. ( 2000; ). Promoter-specific targeting of human SWI–SNF complex by Epstein–Barr virus nuclear protein 2. J Virol 74, 8893–8903.[CrossRef]
    [Google Scholar]
  55. Zennou, V., Petit, C., Guetard, D., Nehrbass, U., Montagnier, L. & Charneau, P. ( 2000; ). HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101, 173–185.[CrossRef]
    [Google Scholar]
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