Reverse transcription complex: The key player of the early phase of HIV replication

Future Virology

Volumn 2, Issue 1, 2007, Pages 49-64

  Iordanskiy, Sergey N ^a,b   Bukrinsky, Michael I ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b D I IVANOVSKY INSTITUTE OF VIROLOGY   (Russian Federation)

Author keywords

HIV 1; Nuclear transport; Preintegration complex; Retrovirus; Reverse transcription; Uncoating

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; ADENOSINE TRIPHOSPHATE DERIVATIVE; COMPLEMENTARY DNA; CORE PROTEIN; CYCLOPHILIN A; CYTOSKELETON PROTEIN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; INTEGRASE; LYSOSOME ENZYME; MATRIX PROTEIN; NEF PROTEIN; P21 ACTIVATED KINASE; POLYPROTEIN; RNA DIRECTED DNA POLYMERASE; TRIPARTITE MOTIF PROTEIN 5; VAV PROTEIN; VIRUS FUSION PROTEIN; VIRUS PROTEIN;

CELL MEMBRANE TRANSPORT; DNA SYNTHESIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION; REVIEW; RNA METABOLISM; RNA STRUCTURE; RNA SYNTHESIS; SIMIAN IMMUNODEFICIENCY VIRUS; UBIQUITINATION; VIRION; VIRUS CELL TRANSFORMATION; VIRUS CORE; VIRUS DNA CELL DNA INTERACTION; VIRUS REPLICATION; VIRUS VIRULENCE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34249295243     PISSN: 17460794     EISSN: None     Source Type: Journal    
DOI: 10.2217/17460794.2.1.49     Document Type: Review

References (105)

1. Bukrinsky MI, Sharova N, McDonald TL, Pushkarskaya T, Tarpley WG, Stevenson M: Association of integrase, matrix, and reverse transcriptase antigens of human immunodeficiency virus type 1 with viral nucleic acids following acute infection. Proc. Natl Acad. Sci. USA 90, 6125-6129 (1993).
2. Miller MD, Farnet CM, Bushman FD: Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71, 5382-5390 (1997).
3. Lin CW, Engelman A: The barrier-to-autointegration factor is a component of functional human immunodeficiency virus type 1 preintegration complexes. J. Virol. 77, 5030-5036 (2003).
4. Llano M, Vanegas M, Fregoso O et al.: LEDGF/p75 determines cellular trafficking of diverse lentiviral but not murine oncoretroviral integrase proteins and is a component of functional lentiviral preintegration complexes. J. Virol. 78, 9524-9537 (2004).
5. Weinberg JB, Matthews TJ, Cullen BR, Malim MH: Productive human immunodeficiency virus type 1 (HIV-1) infection of nonproliferating human monocytes. J. Exp. Med. 174, 1477-1482 (1991).
6. Bukrinsky MI, Sharova N, Dempsey MP et al.: Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc. Natl Acad. Sci. USA 89, 6580-6584 (1992).
7. Lehmann-Che J, Giron ML, Delelis O et al.: Protease-dependent uncoating of a complex retrovirus. J. Virol. 79, 9244-9253 (2005).
8. Lewis P, Hensel M, Emerman M: Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO J. 11, 3053-3058 (1992).
9. Roe T, Reynolds TC, Yu G, Brown PO: Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 12, 2099-2108 (1993).
10. Nisole S, Saib A: Early steps of retrovirus replicative cycle. Retro Virology 1, 9 (2004).
11. Pornillos O, Garrus JE, Sundquist WI: Mechanisms of enveloped RNA virus budding. Trends Cell Biol. 12, 569-579 (2002).
12. Haffar O, Bukrinsky M: Nuclear translocation as a novel target for anti-HIV drugs. Expert Rev. Anti Infect. Ther. 3, 41-50 (2005).
13. Goff SP: Retrovirus restriction factors. Mol, Cell 16, 849-859 (2004).
14. Romano G: Current development of lentiviral-mediated gene transfer. Drug News Perspect. 18, 128-134 (2005).
15. Farnet CM, Haseltine WA: Integration of human immunodeficiency virus type 1 DNA in vitro. Proc. Natl. Acad.Sci. USA 87, 4164-4168 (1990).
16. Dvorin JD, Malim MH: Intracellular trafficking of HIV-1 cores: journey to the center of the cell. Curr. Top. Microbiol. Immunol. 281, 179-208 (2003).
17. Khan M, Garcia-Barrio M, Powell MD: Treatment of human immunodeficiency virus type 1 virions depleted of cyclophilin a by natural endogenous reverse transcription restores infectivity. J. Virol. 77, 4431-4434 (2003).
18. Trono, D: Partial reverse transcripts in virions from human immunodeficiency and murine leukemia viruses. J. Virol. 66, 4893-4900 (1992).
19. Zhang H, Dornadula. G, Orenstein J, Pomerantz RJ: 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 (2000).
20. Campbell EM, Nunez R, Hope TJ: Disruption of the actin cytoskeleton can complement the ability of Nef to enhance human immunodeficiency virus type 1 infectivity. J. Virol. 78, 5745-5755 (2004).
21. Bukrinskaya A. Brichacek B, Mann A, Stevenson M: Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188, 2113-2125 (1998).
22. Hottiger M, Gramatikoff K, Georgiev O, Chaponnier C, Schaffner W, Hubscher U: The large subunit of HIV-1 reverse transcriptase interacts with β-actin. Nucleic Acids Res. 23, 736-741 (1995).
23. Pal R, Reitz MS Jr, Tschachler E, Gallo RC, Samgadharan MG, Veronese FD: Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res. Hum. Retroviruses 6, 721-730 (1990).
24. Bukrinskaya AG, Ghorpade A, Heinzinger NK, Smithgall TE, Lewis RE, Stevenson M: Phosphorylation-dependent human immunodeficiency virus type 1 infection and nuclear targeting of viral DNA. Proc. Natl Acad Sci. USA 93, 367-371 (1996).
25. Jacque JM, Mann A, Enslen H et al.: Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 17, 2607-2618 (1998).
26. Kaushik R, Ratner L: Role of human immunodeficiency virus type 1 matrix phosphorylation in an early postentry step of virus replication. J. Virol. 78, 2319-2326 (2004).
27. Konvalinka J, Heuser AM, Hruskova-Heidingsfeldova O et al.; Proteolytic processing of particle-associated retroviral polyproteins by homologous and heterologous viral proteinases. Eur. J. Biochem. 228, 191-198 (1995).
28. Krausslich HG, Facke M, Heuser AM, Konvalinka J, Zentgraf H: The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J. Virol. 69, 3407-3419 (1995).
29. Kotov A, Zhou J, Flicker P, Aiken C: Association of nef with the human immunodeficiency virus type 1 core. J. Virol. 73, 8824-8830 (1999).
30. Kaplan AH, Swanstrom R: Human immunodeficiency virus type 1 Gag proteins are processed in two cellular compartments. Proc. Natl. Acad. Sci. USA 88, 4528-4532 (1991).
31. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI: Assembly and analysis of conical models for the HIV-1 core. Science 283, 80-83 (1999).
32. Iordanskiy S, Berro, R, Altieri M, Kashanchi F, Bukrinsky M: Intracytoplasmic maturation of the human immunodeficiency virus type 1 reverse transcription complexes determines their capacity to integrate into chromatin. Retro Virology 3, 4 (2006).
33. Dismuke DJ, Aiken C: Evidence for a functional link between uncoating of the human immunodeficiency virus type 1 core and nuclear import of the viral preintegration complex. J. Virol. 80, 3712-3720 (2006).
34. McDonald D, Vodicka MA, Lucero G et al.: Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159, 441-452 (2002).
35. Grewe C, Beck A, Gelderblom HR: HIV: early virus-cell interactions. J. Acquir. Immune Defic. Syndr. 3, 965-974 (1990).
36. Bowerman B, Brown PO, Bishop JM, Varmus HE: A nucleoprotein complex mediates the integration of retroviral DNA. Genes Dev. 3, 469-478 (1989).
37. Li S, Hill CP, Sundquist WI, Finch JT: Image reconstructions of helical assemblies of the HIV-1 CA protein Nature 407, 409-413 (2000).
38. Stremlau M, Perron M, Lee M et al.: Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor. Proc. Natl Acad. Sci. USA 103, 5514-5519 (2006).
39. Forshey BM, von Schwedler U, Sundquist WI, Aiken C: Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76, 5667-5677 (2002).
40. Lanman J, Lam TT, Emmett MR, Marshall AG, Sakalian M, Prevelige PE Jr: Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11, 676-677 (2004).
41. Briggs JA, Simon MN, Gross I et al.: The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11, 672-675 (2004).
42. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS: HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61, 213-222 (1990).
43. Bukrinsky MI, Stanwick TL, Dempsey MP, Stevenson M: Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 254, 423-427 (1991).
44. + T cells are infectible by human immunodeficiency virus but do not release virus after activation. J. Virol. 69, 5659-5665 (1995).
45. Pierson TC, Zhou Y, Kieffer TI, Ruff CT, Buck C, Siliciano RF: Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76, 8518-8531 (2002).
46. Korin YD, Zack JA: 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 (1998).
47. Groschel B, Bushman F: Cell cycle arrest in G2/M promotes early steps of infection by human immunodeficiency virus. J. Virol. 79, 5695-5704 (2005).
48. Auewarakul P, Wacharapornin P, Srichatrapimuk S, Chutipongtanate S, Puthavathana P: Uncoating of HIV-1 requires cellular activation. Virology 337, 93-101 (2005).
49. Narayan S, Young JA: Reconstitution of retroviral fusion and uncoating in a cell-free system. Proc. Natl. Acad. Sci. USA 101, 7721-7726 (2004).
50. Gurer C, Cimarelli A, Luban J: Specific incorporation of heat shock protein 70 family members into primate lentiviral virions. J. Virol. 76, 4666-4670 (2002).
51. Gurer C, Hoglund A, Hoglund S, Luban J: ATPγS disrupts human immunodeficiency virus type 1 virion core integrity. J. Virol. 79, 5557-5567 (2005).
52. DesGroseillers L, Jolicoeur P: Physical mapping of the Fv-1 tropism host range determinant of BALB/c murine leukemia viruses. J. Virol. 48, 685-696 (1983).
53. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J: The cytoplasmic body component TRIM5α. restricts HIV-1 infection in Old World monkeys. Nature 427, 848-853 (2004).
54. Hatziioannou T, Martin-Serrano J, Zang T, Bieniasz PD: Matrix-induced inhibition of membrane binding contributes to human immunodeficiency virus type 1 particle assembly defects in murine cells. J. Virol. 79, 15586-15589 (2005).
55. Wu X, Anderson JL, Campbell EM, Joseph AM, Hope TJ: Proteasome inhibitors uncouple rhesus TRIM5α restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. USA 103, 7465-7470 (2006).
56. Braaten D, Franke EK, Luban J: 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 (1996).
57. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP: Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73, 1067-1078 (1993).
58. Towers GJ, Hatziioannou T, Cowan S, Goff SP, Luban J, Bieniasz PD: Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9, 1138-1143 (2003).
59. Sokolskaja E, Sayah DM, Luban J: Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J. Virol. 78, 12800-12808 (2004).
60. Keckesova Z, Ylinen LM, Towers GJ: Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5α antiviral activity. J. Virol. 80, 4683-4690 (2006).
61. Jonckheere H, Anne J, De Clercq E.: The HIV-1 reverse transcription (RT) process as target for RT inhibitors. Med. Res. Rev. 20, 129-154 (2000).
62. Forshey BM, Aiken C: Disassembly of human immunodeficiency virus type 1 cores in vitro reveals association of Nef with the subviral ribonucleoprotein complex. J. Virol. 77, 4409-4414 (2003).
63. Fournier C, Cortay JC, Carbonnelle C, Ehresmann C, Marquet R, Boulanger P: The HIV-1 Nef protein enhances the affinity of reverse transcriptase for RNA in vitro. Virus Genes 25, 255-269 (2002).
64. Mansky LM, Temin HM: Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol.69, 5087-5094 (1995).
65. Chen R, Le Rouzic E, Kearney JA, Mansky LM, Benichou S: Vpr-mediated incorporation of UNG2 into HIV-1 particles is required to modulate the virus mutation rate and for replication in macrophages. J. Biol. Chem. 279, 28419-28425 (2004).
66. Le Rouzic E, Benichou S: The Vpr protein from HIV-1, distinct roles along the viral life cycle. Retro Virology2, 11 (2005).
67. Kaiser SM, Emerman M: Uracil DNA glycosylase is dispensable for human immunodeficiency virus type 1 replication and does not contribute to the antiviral effects of the cytidine deaminase Apobec3G. J. Virol. 80, 875-882 (2006).
68. Schrofelbauer B, Yu Q, Zeitlin SG, Landau NR: Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases. J. Virol. 79, 10978-10987 (2005).
69. Zhu K, Dobard C, Chow SA: Requirement for integrase during reverse transcription of human immunodeficiency virus type 1 and the effect of cysteine mutations of integrase on its interactions with reverse transcriptase. J. Virol. 78, 5045-5055 (2004).
70. Sheehy Am, Gaddis NC, Choi JD, Malim MH: Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646-650 (2002).
71. Bishop KN, Holmes RK, Sheehy AM, Malim MH: APOBEC-mediated editing of viral RNA. Science 305, 645 (2004).
72. Guo F, Cen S, Niu M, Saadatmand J, Kleiman L: The inhibition of tRNALys3-primed reverse transcription by human APOBEC3G during HIV-1 replication. J. Virol. DOI: 10.1128/JVI.01038.06 (2006) (Epub ahead of print).
73. + T cells. Nature 435, 108-114 (2005).
74. Bishop KN, Holmes RK, Malim MH: Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J. Virol. 80, 8450-8458 (2006).
75. Zheng YH, Peterlin BM: Intracellular immunity to HIV-1, newly defined retroviral battles inside infected cells. Retro Virology 2, 25 (2005).
76. Mansky LM, Preveral S, Selig L, Benarous R, Benichou S: The interaction of vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type I in vivo mutation rate. J. Virol. 74, 7039-7047 (2000).
77. Fassati A, Goff SP: Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J. Virol. 75, 3626-3635 (2001).
78. Li L, Olvera JM, Yoder KE et al.: Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J. 20, 3272-3281 (2001).
79. Cherepanov P, Maertens G, Proost P et al.: HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 278, 372-381 (2003).
80. Farnet CM, Bushman FD: HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell 88, 483-492 (1997).
81. Turelli P, Doucas V, Craig E et al: Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol. Cell 7, 1245-1254 (2001).
82. Chen H, Engelman A: The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc. Natl Acad. Sci. USA 95, 15270-15274 (1998).
83. Nermut MV, Fassad A: Structural analyses of purified human immunodeficiency virus type 1 intracellular reverse transcription complexes. J. Virol. 77, 8196-8206 (2003).
84. Khiytani DK, Dimmock NJ: Characterization of a human immunodeficiency virus type 1 pre-integration complex in which the majority of the cDNA is resistant to DNase I digestion. J. Gen. Virol. 83, 2523-2532 (2002).
85. Feldherr CM, Akin D: Variations in signal-mediated nuclear transport during the cell cycle in BALB/c 3T3 ca. Exp. Cell Res. 215, 206-210 (1994).
86. Mattaj IW, Englmeier L: Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67, 265-306 (1998).
87. Lee GE, Murray JW, Wolkoff AW, Wilson DW: Reconstitution of herpes simplex virus microtubule-dependent trafficking in vitro. J. Virol. 80, 4264-4275 (2006).
88. Trotman LC, Mosberger N, Fornerod M, Stidwill RP, Greber UF: Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3, 1092-1100 (2001).
89. Wisnivesky JP, Leopold PL, Crystal RG: Specific binding of the adenovinis capsid to the nuclear envelope. Hum. Gene Ther. 10, 2187-2195 (1999).
90. Sodeik B: Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8, 465-472 (2000).
91. Taunton J: Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr. Opin. Cell Biol. 13, 85-91 (2001).
92. Sodeik B: Unchain my heart, baby let me go - the entry and intracellular transport of HIV. J. Cell Biol. 159, 393-395 (2002).
93. Tang Y, Winkler U, Freed EO et al.: Cellular motor protein KIF-4 associates with retroviral Gag. J. Virol. 73, 10508-10513 (1999).
94. Petit C, Giron ML, Tobaly-Tapiero J et al.: Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116, 3433-3442 (2003).
95. Garcia-Mata R, Gao YS, Sztul E: Hassles with taking out the garbage: aggravating aggresomes. Traffic 3, 388-396 (2002).
96. Wei BL, Denton PW, O'Neill E, Luo T, Foster JL, Garcia JV: Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 9, 5705-5712 (2005).
97. Schwartz O, Marechal V, Friguet B, Arenzana-Seisdedos F, Heard JM: Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J. Virol. 72, 3845-3850 (1998).
98. Campbell EM, Hope TJ: Gene therapy progress and prospects: viral trafficking during infection. Gene Ther. 12, 1353-1359 (2005).
99. Bukrinsky M: A hard way to the nucleus. Mol. Med. 10, 1-5 (2004).
100. Yamashita M, Emerman M: The cell cycle independence of HIV infections is not determined by known karyophilic viral elements.PLoS Pathog. 1, E18 (2006).
101. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, Charneau P: HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101, 173-185 (2000).
102. Dvorin JD, Bell P, Maul GG, Yamashita M, Emerman M, Malim MH: Reassessment of the roles of integrase and the central DNA flap in human immunodeficiency virus type 1 nuclear import. J. Virol. 76, 12087-12096 (2002).
103. Arhel NJ, Souquere-Besse S, Charneau P: Wild-type and central DNA flap defective HIV-1 lentiviral vector genomes: intracallular visualization at ultrastructural resolution levels. Retro Virology 3, 38 (2006).
104. Jacque JM, Stevenson M: The inner-nuclear-envelope protein emerin regulates HIV-1 infectivity. Nature 441, 641-645 (2006).
105. Beitzel B, Bushman F: Construction and analysis of cells lacking the HMGA gene family. Nucleic Acids Res. 31, 5025-5032 (2003).