Human immunodeficiency virus integration efficiency and site selection in quiescent CD4+ T cells

Journal of Virology

Volumn 83, Issue 12, 2009, Pages 6222-6233

  Vatakis, Dimitrios N ^a   Kim, Sanggu ^a   Kim, Namshin ^a,c   Chow, Samson A ^a   Zack, Jerome A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Mailcode 736322 ^*  (United States)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL STIMULATION; CHROMOSOME MAP; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INVERSE POLYMERASE CHAIN REACTION; LONG TERMINAL REPEAT; LYMPHOCYTE ACTIVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS DNA CELL DNA INTERACTION; CELL LINE; COMPARATIVE STUDY; CYTOLOGY; DNA SEQUENCE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CHROMOSOME MAPPING; DNA, VIRAL; HIV; HIV INFECTIONS; HIV LONG TERMINAL REPEAT; HUMANS; LYMPHOCYTE ACTIVATION; SEQUENCE ANALYSIS, DNA; VIRUS INTEGRATION;

EID: 66149094202     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00356-09     Document Type: Article

References (84)

1. Adams, M., L. Sharmeen, J. Kimpton, J. Romeo, J. Garcia, B. Peterlin, M. Groudine, and M. Emerman. 1994. Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc. Natl. Acad. Sci. USA 91:3862-3866.
2. + T cells even at low inoculums as demonstrated with an improved assay for HIV-1 integration. Virology 368:60-72.
3. Al-Mawsawi, L. Q., F. Christ, R. Dayam, Z. Debyser, and N. Neamati. 2008. Inhibitory profile of a LEDGF/p75 peptide against HIV-1 integrase: insight into integrase-DNA complex formation and catalysis. FEBS Lett. 582:1425-1430.
4. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837. (Pubitemid 46802390)
5. Baxter, J., S. Sauer, A. Peters, R. John, R. Williams, M. L. Caparros, K. Arney, A. Otte, T. Jenuwein, M. Merkenschlager, and A. G. Fisher. 2004. Histone hypomethylation is an indicator of epigenetic plasticity in quiescent lymphocytes. EMBO J. 23:4462-4472. (Pubitemid 39601971)
6. Beissbarth, T., and T. P. Speed. 2004. GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 20:1464-1465.
7. Böhnlein, E., J. W. Lowenthal, M. Siekevitz, D. W. Ballard, B. R. Franza, and W. C. Greene. 1988. The same inducible nuclear proteins regulates mitogen activation of both the interleukin-2 receptor-alpha gene and type 1 HIV. Cell 53:827-836.
8. Bor, Y. C., M. D. Miller, F. D. Bushman, and L. E. Orgel. 1996. Targetsequence preferences of HIV-1 integration complexes in vitro. Virology 222:283-288. (Pubitemid 26281383)
9. Boyle, A. P., S. Davis, H. P. Shulha, P. Meltzer, E. H. Margulies, Z. Weng, T. S. Furey, and G. E. Crawford. 2008. High-resolution mapping and characterization of open chromatin across the genome. Cell 132:311-322. (Pubitemid 351172431)
10. Bukrinsky, M. I., T. L. Stanwick, M. P. Dempsey, and M. Stevenson. 1991. Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 254:423-427. (Pubitemid 21917358)
11. Bushman, F., M. Lewinski, A. Ciuffi, S. Barr, J. Leipzig, S. Hannenhalli, and C. Hoffmann. 2005. Genome-wide analysis of retroviral DNA integration. Nat. Rev. Microbiol. 3:848-858.
12. Bushman, F. D. 2003. Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115:135-138. (Pubitemid 37329577)
13. Bushman, F. D. 1994. Tethering human immunodeficiency virus 1 integrase to a DNA site directs integration to nearby sequences. Proc. Natl. Acad. Sci. USA 91:9233-9237.
14. Bushman, F. D., and R. Craigie. 1990. Sequence requirements for integration of Moloney murine leukemia virus DNA in vitro. J. Virol. 64:5645-5648. (Pubitemid 20364562)
15. Bushman, F. D., T. Fujiwara, and R. Craigie. 1990. Retroviral DNA integration directed by HIV integration protein in vitro. Science 249:1555-1558. (Pubitemid 20341932)
16. Carteau, S., C. Hoffmann, and F. Bushman. 1998. Chromosome structure and human immunodeficiency virus type 1 cDNA integration: centromeric alphoid repeats are a disfavored target. J. Virol. 72:4005-4014. (Pubitemid 28188704)
17. Cherepanov, P., Z. Y. Sun, S. Rahman, G. Maertens, G. Wagner, and A. Engelman. 2005. Solution structure of the HIV-1 integrase-binding domain in LEDGF/p75. Nat. Struct. Mol. Biol. 12:526-532.
18. + T cells. Nature 435:108-114.
19. Chun, T. W., L. Carruth, D. Finzi, X. Shen, J. A. DiGiuseppe, H. Taylor, M. Hermankova, K. Chadwick, J. Margolick, T. C. Quinn, Y. H. Kuo, R. Brookmeyer, M. A. Zeiger, P. Barditch-Crovo, and R. F. Siliciano. 1997. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387:183-188. (Pubitemid 27209433)
20. Chun, T. W., L. Stuyver, S. B. Mizell, L. A. Ehler, J. A. Mican, M. Baseler, A. L. Lloyd, M. A. Nowak, and A. S. Fauci. 1997. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 94:13193-13197.
21. Ciuffi, A., and F. D. Bushman. 2006. Retroviral DNA integration: HIV and the role of LEDGF/p75. Trends Genet. 22:388-395. (Pubitemid 44015973)
22. 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.
23. Coffin, J. M. 1992. Retroviral DNA integration. Dev. Biol. Stand. 76:141-151.
24. Di Santo, J. P. 2001. Lung Krupple-like factor: a quintessential player in T cell quiescence. Nat. Immunol. 2:667-668.
25. Dolan, J., A. Chen, I. T. Weber, R. W. Harrison, and J. Leis. 2009. Defining the DNA substrate binding sites on HIV-1 integrase. J. Mol. Biol. 385:568-579.
26. Embretson, J., M. Zupancic, J. L. Ribas, A. Burke, P. Racz, K. Tenner-Racz, and A. T. Haase. 1993. Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362:359-362. (Pubitemid 23101311)
27. Engelman, A., and P. Cherepanov. 2008. The lentiviral integrase binding protein LEDGF/p75 and HIV-1 replication. PLoS Pathog. 4:e1000046. (Pubitemid 351631084)
28. Festenstein, R., S. N. Pagakis, K. Hiragami, D. Lyon, A. Verreault, B. Sekkali, and D. Kioussis. 2003. Modulation of heterochromatin protein 1 dynamics in primary mammalian cells. Science 299:719-721. (Pubitemid 36159489)
29. + lymphocytes. Nature 426:853-857.
30. + T lymphocytes. Mol. Immunol. 42:627-641.
31. Han, Y., K. Lassen, D. Monie, A. R. Sedaghat, S. Shimoji, X. Liu, T. C. Pierson, J. B. Margolick, R. F. Siliciano, and J. D. Siliciano. 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. (Pubitemid 38715910)
32. Han, Y., Y. B. Lin, W. An, J. Xu, H. C. Yang, K. O'Connell, D. Dordai, J. D. Boeke, J. D. Siliciano, and R. F. Siliciano. 2008. Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell Host Microbe 4:134-146.
33. Herrmann, C. H., and A. P. Rice. 1995. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl-terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J. Virol. 69:1612-1620.
34. Hosack, D. A., G. Dennis, Jr., B. T. Sherman, H. C. Lane, and R. A. Lempicki. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol. 4:R70.
35. + T cell populations during effective highly active antiretroviral therapy. J. Infect. Dis. 195:716-725.
36. Jones, K. A., and B. M. Peterlin. 1994. Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem. 63:717-743.
37. Jordan, A., D. Bisgrove, and E. Verdin. 2003. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J. 22:1868-1877. (Pubitemid 36460143)
38. Jordan, A., P. Defechereux, and E. Verdin. 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. (Pubitemid 32299409)
39. Julias, J. G., M. J. McWilliams, S. G. Sarafianos, E. Arnold, and S. H. Hughes. 2002. Mutations in the RNase H domain of HIV-1 reverse transcriptase affect the initiation of DNA synthesis and the specificity of RNase H cleavage in vivo. Proc. Natl. Acad. Sci. USA 99:9515-9520.
40. Kim, S., N. Kim, B. Dong, D. Boren, S. A. Lee, J. Das Gupta, C. Gaughan, E. A. Klein, C. Lee, R. H. Silverman, and S. A. Chow. 2008. Integration site preference of xenotropic murine leukemia virus-related virus, a new human retrovirus associated with prostate cancer. J. Virol. 82:9964-9977.
41. Kim, S., Y. Kim, T. Liang, J. S. Sinsheimer, and S. A. Chow. 2006. A high-throughput method for cloning and sequencing human immunodeficiency virus type 1 integration sites. J. Virol. 80:11313-11321. (Pubitemid 44706571)
42. Korin, Y. D., and J. A. Zack. 1999. Nonproductive human immunodeficiency virus type 1 infection in nucleoside-treated G0 lymphocytes. J. Virol. 73:6526-6532. (Pubitemid 29327833)
43. Korin, Y. D., and J. A. Zack. 1998. Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J. Virol. 72:3161-3168. (Pubitemid 28175559)
44. + T cells in vivo. J. Virol. 78:9105-9114.
45. + T cells. PLoS Pathog. 2:e68.
46. Lewinski, M. K., D. Bisgrove, P. Shinn, H. Chen, C. Hoffmann, S. Hannenhalli, E. Verdin, C. C. Berry, J. R. Ecker, and F. D. Bushman. 2005. Genomewide analysis of chromosomal features repressing human immunodeficiency virus transcription. J. Virol. 79:6610-6619. (Pubitemid 40677292)
47. 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:e60.
48. Llano, M., S. Delgado, M. Vanegas, and E. M. Poeschla. 2004. Lens epithelium-derived growth factor/p75 prevents proteasomal degradation of HIV-1 integrase. J. Biol. Chem. 279:55570-55577.
49. Llano, M., D. T. Saenz, A. Meehan, P. Wongthida, M. Peretz, W. H. Walker, W. Teo, and E. M. Poeschla. 2006. An essential role for LEDGF/p75 in HIV integration. Science 314:461-464. (Pubitemid 44628966)
50. 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.
51. Maxfield, L. F., C. D. Fraize, and J. M. Coffin. 2005. Relationship between retroviral DNA-integration-site selection and host cell transcription. Proc. Natl. Acad. Sci. USA 102:1436-1441.
52. McWilliams, M. J., J. G. Julias, and S. H. Hughes. 2008. Mutations in the human immunodeficiency virus type 1 polypurine tract (PPT) reduce the rate of PPT cleavage and plus-strand DNA synthesis. J. Virol. 82:5104-5108. (Pubitemid 351657072)
53. Mitchell, R., C. Y. Chiang, C. Berry, and F. Bushman. 2003. Global analysis of cellular transcription following infection with an HIV-based vector. Mol. Ther. 8:674-687.
54. Mitchell, R. S., B. F. Beitzel, A. R. 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.
55. Nabel, G., and D. Baltimore. 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326: 711-713. (Pubitemid 17059793)
56. O'Brien, W. A., A. Namazi, H. Kalhor, S. H. Mao, J. A. Zack, and I. S. Chen. 1994. Kinetics of human immunodeficiency virus type 1 reverse transcription in blood mononuclear phagocytes are slowed by limitations of nucleotide precursors. J. Virol. 68:1258-1263. (Pubitemid 24022239)
57. O'Doherty, U., W. J. Swiggard, D. Jeyakumar, D. McGain, and M. H. Malim. 2002. A sensitive, quantitative assay for human immunodeficiency virus type 1 integration. J. Virol. 76:10942-10950. (Pubitemid 35176211)
58. O'Doherty, U., W. J. Swiggard, and M. H. Malim. 2000. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74:10074-10080.
59. Oh, J., M. J. McWilliams, J. G. Julias, and S. H. Hughes. 2008. Mutations in the U5 region adjacent to the primer binding site affect tRNA cleavage by human immunodeficiency virus type 1 reverse transcriptase in vivo. J. Virol. 82:719-727.
60. Pierson, T. C., Y. Zhou, T. L. Kieffer, C. T. Ruff, C. Buck, and R. F. Siliciano. 2002. Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76:8518-8531. (Pubitemid 34864046)
61. + T cells. J. Virol. 81:13938-13942.
62. Poeschla, E. M. 2008. Integrase, LEDGF/p75 and HIV replication. Cell Mol. Life Sci. 65:1403-1424.
63. Pruss, D., F. D. Bushman, and A. P. Wolffe. 1994. Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc. Natl. Acad. Sci. USA 91:5913-5917.
64. Pruss, D., R. Reeves, F. D. Bushman, and A. P. Wolffe. 1994. The influence of DNA and nucleosome structure on integration events directed by HIV integrase. J. Biol. Chem. 269:25031-25041.
65. Rich, E. A., I. S. Chen, J. A. Zack, M. L. Leonard, and W. A. O'Brien. 1992. Increased susceptibility of differentiated mononuclear phagocytes to productive infection with human immunodeficiency virus-1 (HIV-1). J. Clin. Investig. 89:176-183.
66. Schröder, A. R., P. Shinn, H. Chen, C. Berry, J. R. Ecker, and F. Bushman. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110:521-529. (Pubitemid 35232295)
67. Schuitemaker, H., N. A. Kootstra, R. A. Fouchier, B. Hooibrink, and F. Miedema. 1994. Productive HIV-1 infection of macrophages restricted to the cell fraction with proliferative capacity. EMBO J. 13:5929-5936.
68. Shun, M. C., N. K. Raghavendra, N. Vandegraaff, 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. (Pubitemid 47076476)
69. Spina, C. A., J. C. Guatelli, and D. D. Richman. 1995. Establishment of a stable, inducible form of human immunodeficiency virus type 1 DNA in quiescent CD4 lymphocytes in vitro. J. Virol. 69:2977-2988.
70. Stevenson, M., B. Brichacek, N. Heinzinger, S. Swindells, S. Pirruccello, E. Janoff, and M. Emerman. 1995. Molecular basis of cell cycle dependent HIV-1 replication. Implications for control of virus burden. Adv. Exp. Med. Biol. 374:33-45.
71. Stevenson, M., T. L. Stanwick, M. P. Dempsey, and C. A. Lamonica. 1990. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 9:1551-1560. (Pubitemid 20137012)
72. Svarovskaia, E. S., R. Barr, X. Zhang, G. C. Pais, C. Marchand, Y. Pommier, T. R. Burke, Jr., and V. K. Pathak. 2004. Azido-containing diketo acid derivatives inhibit human immunodeficiency virus type 1 integrase in vivo and influence the frequency of deletions at two-long-terminal-repeat-circle junctions. J. Virol. 78:3210-3222. (Pubitemid 38568261)
73. + T cells in the absence of activating stimuli. J. Virol. 79:14179-14188.
74. + T cells while short ones are degraded. AIDS Res. Hum. Retrovir. 20:285-295.
75. Swingler, S., B. Brichacek, J. M. Jacque, C. Ulich, J. Zhou, and M. Stevenson. 2003. HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424:213-219. (Pubitemid 36858691)
76. Tong-Starksen, S. E., P. A. Luciw, and B. M. Peterlin. 1987. Human immunodeficiency virus long terminal repeat responds to T-cell activation signals. Proc. Natl. Acad. Sci. USA 84:6845-6849.
77. Vandekerckhove, L., F. Christ, B. Van Maele, J. De Rijck, R. Gijsbers, C. Van den Haute, M. Witvrouw, and Z. Debyser. 2006. Transient and stable knockdown of the integrase cofactor LEDGF/p75 reveals its role in the replication cycle of human immunodeficiency virus. J. Virol. 80:1886-1896. (Pubitemid 43228728)
78. + T cells. J. Virol. 81:3574-3582.
79. Wang, G. P., A. Ciuffi, J. Leipzig, C. C. Berry, and F. D. Bushman. 2007. HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res. 17:1186-1194. (Pubitemid 47204862)
80. Weidhaas, J. B., E. L. Angelichio, S. Fenner, and J. M. Coffin. 2000. Relationship between retroviral DNA integration and gene expression. J. Virol. 74:8382-8389. (Pubitemid 30666689)
81. Yu, J. J., T. L. Wu, M. K. Liszewski, J. Dai, W. J. Swiggard, C. Baytop, I. Frank, B. L. Levine, W. Yang, T. Theodosopoulos, and U. O'Doherty. 2008. A more precise HIV integration assay designed to detect small differences finds lower levels of integrated DNA in HAART treated patients. Virology 379:78-86.
82. Zack, J. A., S. J. Arrigo, S. R. Weitsman, A. S. Go, A. Haislip, and I. S. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61:213-222. (Pubitemid 20149353)
83. Zack, J. A., A. M. Haislip, P. Krogstad, and I. S. Chen. 1992. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J. Virol. 66:1717-1725.
84. + T cells. J. Virol. 79:2199-2210.