Characterization of the behavior of functional viral genomes during the early steps of human immunodeficiency virus type 1 infection

Journal of Virology

Volumn 83, Issue 15, 2009, Pages 7524-7535

  Arfi, Vanessa ^a,b,c   Lienard, Julia ^a,b,c   Nguyen, Xuan Nhi ^a,b,c   Berger, Gregory ^a,b,c   Rigal, Dominique ^d   Darlix, Jean Luc ^a,b,c   Cimarelli, Andrea ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c UNIVERSITÉ LYON 1   (France)

^d ETABLISSEMENT FRANÇAIS DU SANG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CYCLOPHILIN A; CYCLOSPORIN; VIRUS DNA; VIRUS NUCLEOPROTEIN;

ARTICLE; CELL TYPE; CONTROLLED STUDY; DNA SYNTHESIS; DNA TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; REVERSE TRANSCRIPTION; TARGET CELL; VIRUS CAPSID; VIRUS DNA CELL DNA INTERACTION; VIRUS ENTRY; VIRUS GENOME;

CAPSID PROTEINS; CELL LINE; DNA, VIRAL; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; KINETICS; REVERSE TRANSCRIPTION; VIRUS ASSEMBLY; VIRUS INTEGRATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 67650860274     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00429-09     Document Type: Article

References (61)

1. Aiken, C. 1997. Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J. Virol. 71:5871-5877.
2. Andreadis, S., T. Lavery, H. E. Davis, J. M. Le Doux, M. L. Yarmush, and J. R. Morgan. 2000. Toward a more accurate quantitation of the activity of recombinant retroviruses: alternatives to titer and multiplicity of infection. J. Virol. 74:3431-3439.
3. Arfi, V., L. Riviere, L. Jarrosson-Wuilleme, C. Goujon, D. Rigal, J. L. Darlix, and A. Cimarelli. 2008. Characterization of the early steps of infection of primary blood monocytes by human immunodeficiency virus type 1. J. Virol. 82:6557-6565.
4. Arhel, N., A. Genovesio, K. A. Kim, S. Miko, E. Perret, J. C. Olivo-Marin, S. Shorte, and P. Charneau. 2006. Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat. Methods 3:817-824.
5. Arhel, N. J., S. Souquere-Besse, S. Munier, P. Souque, S. Guadagnini, S. Rutherford, M. C. Prevost, T. D. Allen, and P. Charneau. 2007. HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J. 26:3025-3037.
6. Auewarakul, P., P. Wacharapornin, S. Srichatrapimuk, S. Chutipongtanate, and P. Puthavathana. 2005. Uncoating of HIV-1 requires cellular activation. Virology 337:93-101.
7. Barbosa, P., P. Charneau, N. Dumey, and F. Clavel. 1994. Kinetic analysis of HIV-1 early replicative steps in a coculture system. AIDS Res. Hum. Retrovir. 10:53-59.
8. Berger, G., C. Goujon, J. L. Darlix, and A. Cimarelli. 2009. SIV(MAC) Vpx improves the transduction of dendritic cells with nonintegrative HIV-1-derived vectors. Gene Ther. 16:159-163.
9. Braaten, D., E. K. Franke, and J. Luban. 1996. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J. Virol. 70:3551-3560.
10. Brass, A. L., D. M. Dykxhoorn, Y. Benita, N. Yan, A. Engelman, R. J. Xavier, J. Lieberman, and S. J. Elledge. 2008. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319:921-926.
11. Bukrinskaya, A., B. Brichacek, A. Mann, and M. Stevenson. 1998. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188:2113-2125.
12. Bukrinsky, M. 2004. A hard way to the nucleus. Mol. Med. 10:1-5.
13. Bukrinsky, M. I., N. Sharova, M. P. Dempsey, T. L. Stanwick, A. G. Bukrinskaya, S. Haggerty, and M. Stevenson. 1992. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc. Natl. Acad. Sci. USA 89:6580-6584.
14. Chabes, A., and B. Stillman. 2007. Constitutively high dNTP concentration inhibits cell cycle progression and the DNA damage checkpoint in yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104:1183-1188.
15. Collin, M., and S. Gordon. 1994. The kinetics of human immunodeficiency virus reverse transcription are slower in primary human macrophages than in a lymphoid cell line. Virology 200:114-120.
16. Darlix, J. L., J. L. Garrido, N. Morellet, Y. Mely, and H. de Rocquigny. 2007. Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv. Pharmacol. 55:299-346.
17. Gao, W. Y., A. Cara, R. C. Gallo, and F. Lori. 1993. Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit human immunodeficiency virus type 1 replication. Proc. Natl. Acad. Sci. USA 90:8925-8928.
18. Groschel, B., and F. Bushman. 2005. Cell cycle arrest in G2/M promotes early steps of infection by human immunodeficiency virus. J. Virol. 79:5695-5704.
19. Harris, D., N. Kaushik, P. K. Pandey, P. N. Yadav, and V. N. Pandey. 1998. Functional analysis of amino acid residues constituting the dNTP binding pocket of HIV-1 reverse transcriptase. J. Biol. Chem. 273:33624-33634.
20. Hatziioannou, T., D. Perez-Caballero, S. Cowan, and P. D. Bieniasz. 2005. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79: 176-183.
21. Iordanskiy, S., R. Berro, M. Altieri, F. Kashanchi, and M. Bukrinsky. 2006. Intracytoplasmic maturation of the human immunodeficiency virus type 1 reverse transcription complexes determines their capacity to integrate into chromatin. Retrovirology. 3:4.
22. Jarrosson-Wuilleme, L., C. Goujon, J. Bernaud, D. Rigal, J. L. Darlix, and A. Cimarelli. 2006. Transduction of nondividing human macrophages with gammaretrovirus-derived vectors. J. Virol. 80:1152-1159.
23. Kimpton, J., and M. Emerman. 1992. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene. J. Virol. 66:2232-2239.
24. Koning, R., Y. Zhou, D. Elleder, T. L. Diamond, M. C. Bonamy, J. T. Irelan, C. Chiang, B. P. Tu, P. D. De Jesus, C. E. Lilley, S. Seidel, A. M. Opaluch, J. S. Caldwelll, M. D. Weitzman, K. L. Kuhen, S. Bandyopadhyay, T. Ideker, A. P. Orth, L. J. Miraglia, F. D. Bushman, J. A. Young, and S. K. Chanda. 2008. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135:49-60.
25. 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.
26. 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.
27. Lin, Z. P., M. F. Belcourt, R. Carbone, J. S. Eaton, P. G. Penketh, G. S. Shadel, J. G. Cory, and A. C. Sartorelli. 2007. Excess ribonucleotide reductase R2 subunits coordinate the S phase checkpoint to facilitate DNA damage repair and recovery from replication stress. Biochem. Pharmacol. 73:760-772.
28. Luban, J., K. L. Bossolt, E. K. Franke, G. V. Kalpana, and S. P. Goff. 1993. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73:1067-1078.
29. Managlia, E. Z., A. Landay, and L. Al-Harthi. 2006. Interleukin-7 induces HIV replication in primary naive T cells through a nuclear factor of activated T-cell (NFAT)-dependent pathway. Virology 350:443-452.
30. McDonald, D., M. A. Vodicka, G. Lucero, T. M. Svitkina, G. G. Borisy, M. Emerman, and T. J. Hope. 2002. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159:441-452.
31. Miller, M. D., C. M. Farnet, and F. D. Bushman. 1997. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71:5382-5390.
32. Nakajima, N., R. Lu, and A. Engelman. 2001. Human immunodeficiency virus type 1 replication in the absence of integrase-mediated dna recombination: definition of permissive and nonpermissive T-cell lines. J. Virol. 75:7944-7955.
33. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
34. Nash, K. L., and A. M. Lever. 2004. Green fluorescent protein: green cells do not always indicate gene expression. Gene Ther. 11:882-883.
35. Neil, S., F. Martin, Y. Ikeda, and M. Collins. 2001. Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J. Virol. 75:5448-5456.
36. Nermut, M. V., and A. Fassati. 2003. Structural analyses of purified human immunodeficiency virus type 1 intracellular reverse transcription complexes. J. Virol. 77:8196-8206.
37. Nisole, S., and A. Saib. 2004. Early steps of retrovirus replicative cycle. Retrovirology 1:9.
38. O'Brien, W. A. 1994. HIV-1 entry and reverse transcription in macrophages. J. Leukoc. Biol. 56:273-277.
39. 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.
40. Piatak, M., Jr., M. S. Saag, L. C. Yang, S. J. Clark, J. C. Kappes, K. C. Luk, B. H. Hahn, G. M. Shaw, and J. D. Lifson. 1993. High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 259:1749-1754.
41. Pierson, T. C., T. L. Kieffer, C. T. Ruff, C. Buck, S. J. Gange, and R. F. Siliciano. 2002. Intrinsic stability of episomal circles formed during human immunodeficiency virus type 1 replication. J. Virol. 76:4138-4144.
42. Ravot, E., G. Comolli, F. Lori, and J. Lisziewicz. 2002. High efficiency lentiviral gene delivery in non-dividing cells by deoxynucleoside treatment. J. Gene Med. 4:161-169.
43. Schwartz, O., V. Marechal, B. Friguet, F. Arenzana-Seisdedos, and J. M. Heard. 1998. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J. Virol. 72:3845-3850.
44. Sokolskaja, E., D. M. Sayah, and J. Luban. 2004. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J. Virol. 78:12800-12808.
45. Stremlau, M., M. Perron, M. Lee, Y. Li, B. Song, H. Javanbakht, F. Diaz-Griffero, D. J. Anderson, W. I. Sundquist, and J. Sodroski. 2006. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. USA 103:5514-5519.
46. Thomas, J. A., D. E. Ott, and R. J. Gorelick. 2007. Efficiency of human immunodeficiency virus type 1 postentry infection processes: evidence against disproportionate numbers of defective virions. J. Virol. 81:4367-4370.
47. Towers, G. J., T. Hatziioannou, S. Cowan, S. P. Goff, J. Luban, and P. D. Bieniasz. 2003. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9:1138-1143.
48. Triques, K., and M. Stevenson. 2004. Characterization of restrictions to human immunodeficiency virus type 1 infection of monocytes. J. Virol. 78:5523-5527.
49. Vandegraaff, N., R. Kumar, C. J. Burrell, and P. Li. 2001. Kinetics of human immunodeficiency virus type 1 (HIV) DNA integration in acutely infected cells as determined using a novel assay for detection of integrated HIV DNA. J. Virol. 75:11253-11260.
50. Van Maele, B., J. De Rijck, E. De Clercq, and Z. Debyser. 2003. Impact of the central polypurine tract on the kinetics of human immunodeficiency virus type 1 vector transduction. J. Virol. 77:4685-4694.
51. Vatakis, D. N., G. Bristol, T. A. Wilkinson, S. A. Chow, and J. A. Zack. 2007. Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4+ T cells. J. Virol. 81:3574-3582.
52. + T cells display altered HIV infection kinetics: implications for efficacy of antiviral agents. J. Virol. 83:3374-3378.
53. Yap, M. W., M. P. Dodding, and J. P. Stoye. 2006. Trim-cyclophilin A fusion proteins can restrict human immunodeficiency virus type 1 infection at two distinct phases in the viral life cycle. J. Virol. 80:4061-4067.
54. Yin, L., D. Braaten, and J. Luban. 1998. Human immunodeficiency virus type 1 replication is modulated by host cyclophilin A expression levels. J. Virol. 72:6430-6436.
55. Ylinen, L. M., T. Schaller, A. Price, A. J. Fletcher, M. Noursadeghi, L. C. James, and G. J. Towers. 2009. Cyclophilin A levels dictate infection effi-ciency of human immunodeficiency virus type 1 capsid escape mutants A92E and G94D. J. Virol. 83:2044-2047.
56. 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.
57. 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.
58. Zamborlini, A., J. Lehmann-Che, E. Clave, M. L. Giron, J. Tobaly-Tapiero, P. Roingeard, S. Emiliani, A. Toubert, H. de The, and A. Saib. 2007. Centrosomal pre-integration latency of HIV-1 in quiescent cells. Retrovirology 4:63.
59. Zhang, H., G. Dornadula, J. Orenstein, and R. J. Pomerantz. 2000. Morphologic changes in human immunodeficiency virus type 1 virions secondary to intravirion reverse transcription: evidence indicating that reverse transcription may not take place within the intact viral core. J. Hum. Virol. 3:165-172.
60. Zhang, H., G. Dornadula, and R. J. Pomerantz. 1996. Endogenous reverse transcription of human immunodeficiency virus type 1 in physiological microenviroments: an important stage for viral infection of nondividing cells. J. Virol. 70:2809-2824.
61. + T cells. J. Virol. 79:2199-2210.