Intracellular trafficking of retroviral genomes during the early phase of infection: Viral exploitation of cellular pathways

Journal of Gene Medicine

Volumn 3, Issue 6, 2001, Pages 517-528

  Goff, Stephen P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Nuclear entry; Reverse transcription; Virus entry

Indexed keywords

CIRCULAR DNA; VIRUS DNA; VIRUS RNA;

ANIMAL; CELL CYCLE; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; RETROVIRUS; RETROVIRUS INFECTION; REVIEW; TIME; TRANSPORT AT THE CELLULAR LEVEL; VIRION; VIROLOGY; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME;

ANIMALS; BIOLOGICAL TRANSPORT; CELL CYCLE; DNA, CIRCULAR; DNA, VIRAL; GENOME, VIRAL; HUMANS; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; RNA, VIRAL; TIME FACTORS; TRANSCRIPTION, GENETIC; VIRION; VIRUS INTEGRATION;

EID: 0035524975     PISSN: 1099498X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-2254(200111)3:6<517::AID-JGM234>3.0.CO;2-E     Document Type: Review

References (138)

1. Chicurel M. Virology. Probing HIV's elusive activities within the host cell. Science 2000; 290: 1876-1879.
2. Sodeik B. Mechanisms of viral transport in the cytoplasm. Trends Microbiol 2000; 8: 465-172.
3. Whittaker GR, Kann M, Helenius A. Viral entry into the nucleus. Annu Rev Cell Dev Biol 2000; 16: 627-651.
4. Cullen BR. Journey to the center of the cell. Cell 2001; 105: 697-700.
5. Ploubidou A, Way M. Viral transport and the cytoskeleton. Curr Opin Cell Biol. 2001; 13: 97-105.
6. Goff SP. Retroviridae: the retroviruses and their replication. In Fields Virology, Knipe DM, Howley PM, eds. Lippincott, Williams & Wilkins: Philadelphia, PA, 2001; 1871-1939.
7. Kizhatil K, Albritton LM. Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. J Virol 1997; 71: 7145-7156.
8. Lavillette D, Boson B, Russell SJ, et al. Activation of membrane fusion by murine leukemia viruses is controlled in cis or in trans by interactions between the receptor-binding domain and a conserved disulfide loop of the carboxy terminus of the surface glycoprotein. J Virol 2001; 75: 3685-3695.
9. Katen LJ, Januszeski MM, Anderson WF, et al. Infectious entry by amphotropic as well as ecotropic murine leukemia viruses occurs through an endocytic pathway. J Virol 2001; 75: 5018-5026.
10. Fassati A, Goff SP. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J Virol 1999; 73: 8919-8925.
11. Fassati A, Goff SP. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J Virol 2001; 75: 3626-3635.
12. Karageorgos L, Li P, Burrell C. Characterization of HIV replication complexes early after cell-to-cell infection. AIDS Res Hum Retroviruses 1993; 9: 817-823.
13. Miller MD, Farnet CM, Bushman FD. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J Virol 1997; 71: 5382-5390.
14. Bukrinskaya A, Brichacek B, Mann A, et al. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J Exp Med 1998; 188: 2113-2125.
15. Rothenberg E, Baltimore D. Synthesis of long, representative DNA copies of the murine RNA tumor virus genome. J Virol 1975; 17: 168-174.
16. Rothenberg E, Baltimore D. Increased length of DNA made by virions of murine leukemia virus at limiting magnesium ion concentration. J Virol 1977; 21: 168-178.
17. Rothenberg E, Smotkin D, Baltimore D, et al. In vitro synthesis of infectious DNA of murine leukaemia virus. Nature 1977; 269: 122-126.
18. Zhang H, Dornadula G, Pomerantz RJ. Endogenous reverse transcription of human immunodeficiency virus type 1 in physiological microenviroments: an important stage for viral infection of nondividing cells. J Virol 1996; 70: 2809-2824.
19. Zhang H, Dornadula G, Pomerantz RJ. Natural endogenous reverse transcription of HIV-1. J Reprod Immunol 1998; 41: 255-260.
20. Zhang H, Dornadula G, Orenstein J, et al. 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 2000; 3: 165-172.
21. Zack JA, Arrigo SJ, Weitsman SR, et al. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990; 61: 213-222.
22. Zack JA, Haislip AM, Krogstad P, et al. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J Virol 1992; 66: 1717-1725.
23. O'Brien WA, Namazi A, Kalhor H, et al. Kinetics of human immunodeficiency virus type 1 reverse transcription in blood mononuclear phagocytes are slowed by limitations of nucleotide precursors. J Virol 1994; 68: 1258-1263.
24. Kootstra NA, Zwart BM, Schuitemaker H. Diminished human immunodeficiency virus type 1 reverse transcription and nuclear transport in primary macrophages arrested in early G(1) phase of the cell cycle. J Virol 2000; 74: 1712-1717.
25. Reicin AS, Paik S, Berkowitz RD, et al. Linker insertion mutations in the human immunodeficiency virus type 1 gag gene: effects on virion particle assembly, release, and infectivity. J Virol 1995; 69: 642-650.
26. Cairns TM, Craven RC. Viral DNA synthesis defects in assembly-competent rous sarcoma virus CA mutants. J Virol 2001; 75: 242-250.
27. 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 1996; 70: 3551-3560.
28. Franke EK, Yuan HE, Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 1994; 372: 359-362.
29. Gao G, Goff SP. Somatic cell mutants resistant to retrovirus replication: intracellular blocks during the early stages of infection. Mol Biol Cell 1999; 10: 1705-1717.
30. Telesnitsky A, Goff SP. Reverse transcriptase and the generation of retroviral DNA. In Retroviruses, Coffin JM, Hughes SH, Varmus HE, eds. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1997; 121-160.
31. Wei SQ, Mizuuchi K, Craigie R. Footprints on the viral DNA ends in Moloney murine leukemia virus preintegration complexes reflect a specific association with integrase. Proc Natl Acad Sci U S A 1998; 95: 10535-10540.
32. Chen H, Wei SQ, Engelman A. Multiple integrase functions are required to form the native structure of the human immunodeficiency virus type I intasome. J Biol Chem 1999; 274: 17358-17364.
33. Risco C, Menendez-Arias L, Copeland TD, et al. Intracellular transport of the murine leukemia virus during acute infection of NIH 3T3 cells: nuclear import of nucleocapsid protein and integrase. J Cell Sci 1995; 108: 3039-3050.
34. Liu B, Dai R, Tian CJ, et al. Interaction of the human immunodeficiency virus type 1 nucleocapsid with actin. J Virol 1999; 73: 2901-2908.
35. Wilk T, Gowen B, Fuller SD. Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein. J Virol 1999; 73: 1931-1940.
36. Rey O, Canon J, Krogstad P. HIV-1 Gag protein associates with F-actin present in microfilaments. Virology 1996; 220: 530-534.
37. Perrin-Tricaud C, Davoust J, Jones IM. Tagging the human immunodeficiency virus gag protein with green fluorescent protein. Minimal evidence for colocalisation with actin. Virology 1999; 255: 20-25.
38. Kim W, Tang Y, Okada Y, et al. Binding of murine leukemia virus Gag polyproteins to KIF4, a microtubule-based motor protein. J Virol 1998; 72: 6898-6901.
39. Tang Y, Winkler U, Freed EO, et al. Cellular motor protein KIF-4 associates with retroviral Gag. J Virol 1999; 73: 10508-10513.
40. Heine UI, Demsey AE, Tucker RW, et al. Intracellular type A retrovirus movement associated with an intact microtubule system. J Gen Virol 1985; 66: 275-282.
41. Saib A, Puvion-Dutilleul F, Schmid M, et al. Nuclear targeting of incoming human foamy virus Gag proteins involves a centriolar step. J Virol 1997; 71: 1155-1161.
42. Pincus T, Rowe WP, Lilly F. A major genetic locus affecting resistance to infection with murine leukemia viruses. II. Apparent identity to a major locus described for resistance to friend murine leukemia virus. J Exp Med 1971; 133: 1234-1241.
43. Rowe WP, Humphrey JB, Lilly F. A major genetic locus affecting resistance to infection with murine leukemia viruses. 3. Assignment of the Fv-1 locus to linkage group 8 of the mouse. J Exp Med 1973; 137: 850-853.
44. Jolicoeur P. The Fv-1 gene of the mouse and its control of murine leukemia virus replication. Curr Top Microbiol Immunol 1979; 86: 67-122.
45. Hopkins N, Schindler J, Hynes R. Six NB-tropic murine leukemia viruses derived from a B-tropic virus of BALB/c have altered p30. J Virol 1977; 21: 309-318.
46. DesGroseillers L, Jolicoeur P. Physical mapping of the Fv-1 tropism host range determinant of BALB/c murine leukemia viruses. J Virol 1983; 48: 685-696.
47. Ou C-Y, Boone LR, Koh CK, et al. Nucleotide sequences of gag-pol regions that determine the Fv-1 host range property of BALB/c N-tropic and B-tropic murine leukemia viruses. J Virol 1983; 48: 779-784.
48. Bishop KN, Bock M, Towers G, et al. Identification of the regions of Fv1 necessary for murine leukemia virus restriction. J Virol 2001; 75: 5182-5188.
49. Best S, Le Tissier P, Towers G, et al. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 1996; 382: 826-829.
50. Pryciak PM, Varmus HE. Fv-1 restriction and its effects on murine leukemia virus integration in vivo and in vitro. J Virol 1992; 66: 5959-5966.
51. Towers G, Bock M, Martin S, et al. A conserved mechanism of retrovirus restriction in mammals. Proc Natl Acad Sci U S A 2000; 97: 12295-12299.
52. Varmus HE, Padgett T, Heasley S, et al. Cellular functions are required for the synthesis and integration of avian sarcoma virus-specific DNA. Cell 1977; 11: 307-319.
53. Miller DG, Adam MA, Miller AD. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol Cell Biol 1990; 10: 4239-4242.
54. Lewis P, Hensel M, Emerman M. Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO J 1992; 11: 3053-3058.
55. Roe T, Reynolds TC, Yu G, et al. Integration of murine leukemia virus DNA depends on mitosis. EMBO J 1993; 12: 2099-2108.
56. Lewis PF, Emerman M. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J Virol 1994; 68: 510-516.
57. Fouchier RA, Malim MH. Nuclear import of human immunodeficiency virus type-1 preintegration complexes. Adv Virus Res 1999; 52: 275-299.
58. Weinberg JB, Matthews TJ, Cullen BR, et al. Productive human immunodeficiency virus type 1 (HIV-1) infection of non-proliferating human monocytes. J Exp Med 1991; 174: 1477-1482.
59. Bukrinsky MI, Sharova N, Dempsey MP, et al. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc Natl Acad Sci U S A 1992; 89: 6580-6584.
60. Hatziioannou T, Goff SP. Infection of nondividing cells by Rous sarcoma virus. J Virol 2001; 75: 9526-9531.
61. Bieniasz PD, Weiss RA, McClure MO. Cell cycle dependence of foamy retrovirus infection. J Virol 1995; 69: 7295-7299.
62. Linial ML. Foamy viruses are unconventional retroviruses. J Virol 1999; 73: 1747-1755.
63. Naldini L, Blomer U, Gage FH, et al. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 1996; 93: 11382-11388.
64. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-267.
65. Blomer U, Naldini L, Kafri T, et al. Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J Virol 1997; 71: 6641-6649.
66. Neil S, Martin F, Ikeda Y, et al. Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol 2001; 75: 5448-5456.
67. Deminie CA, Emerman M. Functional exchange of an oncoretrovirus and a lentivirus matrix protein. J Virol 1994; 68: 4442-4449.
68. Parveen Z, Krupetsky A, Engelstadter M, et al. Spleen necrosis virus-derived C-type retroviral vectors for gene transfer to quiescent cells. Nature Biotechnol 2000; 18: 623-629.
69. Gallay P, Stitt V, Mundy C, et al. Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import. J Virol 1996; 70: 1027-1032.
70. Gulizia J, Dempsey MP, Sharova N, et al. Reduced nuclear import of human immunodeficiency virus type 1 preintegration complexes in the presence of a prototypic nuclear targeting signal. J Virol 1994; 68: 2021-2025.
71. Farnet CM, Haseltine WA. Determination of viral proteins present in the human immunodeficiency virus type 1 pre-integration complex. J Virol 1991; 65: 1910-1915.
72. Bukrinsky MI, Sharova N, McDonald TL, et al. 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 U S A 1993; 90: 6125-6129.
73. Depienne C, Roques P, Creminon C, et al. Cellular distribution and karyophilic properties of matrix, integrase, and vpr proteins from the human and simian immunodeficiency viruses. Exp Cell Res 2000; 260: 387-395.
74. Sharova N, Bukrinskaya A. p17 and p17-containing gag precursors of input human immunodeficiency virus are transported into the nuclei of infected cells. AIDS Res Hum Retroviruses 1991; 7: 303-306.
75. Bukrinsky MI, Haggerty S, Dempsey MP, et al. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 1993; 365: 666-669.
76. Haffar OK, Popov S, Dubrovsky L, et al. Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. J Mol Biol 2000; 299: 359-368.
77. von Schwedler U, Kornbluth RS, Trono D. The nuclear localization signal of the matrix protein of human immunodeficiency virus type 1 allows the establishment of infection in macrophages and quiescent T lymphocytes. Proc Natl Acad Sci U S A 1994; 91: 6992-6996.
78. Gallay P, Swingler S, Aiken C, et al. HIV-1 infection of nondividing cells: C-terminal tyrosine phosphorylation of the viral matrix protein is a key regulator. Cell 1995; 80: 379-388.
79. Gallay P, Swingler S, Song J, et al. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell 1995; 83: 569-576.
80. Bukrinskaya AG, Ghorpade A, Heinzinger NK, et al. Phosphorylation-dependent human immunodeficiency virus type 1 infection and nuclear targeting of viral DNA. Proc Natl Acad Sci U S A 1996; 93: 367-371.
81. Camaur D, Gallay P, Swingler S, et al. Human immunodeficiency virus matrix tyrosine phosphorylation: characterization of the kinase and its substrate requirements. J Virol 1997; 71: 6834-6841.
82. Freed EO, Englund G, Martin MA. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J Virol 1995; 69: 3949-3954.
83. Fouchier RA, Meyer BE, Simon JH, et al. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J 1997; 16: 4531-4539.
84. Kootstra NA, Schuitemaker H. Phenotype of HIV-1 lacking a functional nuclear localization signal in matrix protein of gag and Vpr is comparable to wild-type HIV-1 in primary macrophages. Virology 1999; 253: 170-180.
85. Freed EO, Englund G, Maldarelli F, et al. Phosphorylation of residue 131 of HIV-1 matrix is not required for macrophage infection. Cell 1997; 88: 171-173; discussion 173-174.
86. Reil H, Bukovsky AA, Gelderblom HR, et al. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J 1998; 17: 2699-2708.
87. Heinzinger NK, Bukinsky MI, Haggerty SA, et al. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc Natl Acad Sci U S A 1994; 91: 7311-7315.
88. Fouchier RA, Meyer BE, Simon JH, et al. Interaction of the human immunodeficiency virus type 1 Vpr protein with the nuclear pore complex. J Virol 1998; 72: 6004-6013.
89. Popov S, Rexach M, Ratner L, et al. Viral protein R regulates docking of the HIV-1 preintegration complex to the nuclear pore complex. J Biol Chem 1998; 273: 13347-13352.
90. Popov S, Rexach M, Zybarth G, et al. Viral protein R regulates nuclear import of the HIV-1 pre-integration complex. EMBO J 1998; 17: 909-917.
91. Vodicka MA, Koepp DM, Silver PA, et al. HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev 1998; 12: 175-185.
92. Kamata M, Aida Y. Two putative alpha-helical domains of human immunodeficiency virus type 1 Vpr mediate nuclear localization by at least two mechanisms. J Virol 2000; 74: 7179-7186.
93. Jenkins Y, McEntee M, Weis K, et al. Characterization of HIV-1 vpr nuclear import: analysis of signals and pathways. J Cell Biol 1998; 143: 875-885.
94. Karni O, Friedler A, Zakai N, et al. A peptide derived from the N-terminal region of HIV-1 Vpr promotes nuclear import in permeabilized cells: elucidation of the NLS region of the Vpr. FEBS Lett 1998; 429: 421-425.
95. Zhou Y, Lu Y, Ratner L. Arginine residues in the C-terminus of HIV-1 Vpr are important for nuclear localization and cell cycle arrest. Virology 1998; 242: 414-424.
96. Nie Z, Bergeron D, Subbramanian RA, et al. The putative alpha helix 2 of human immunodeficiency virus type 1 Vpr contains a determinant which is responsible for the nuclear translocation of proviral DNA in growth-arrested cells. J Virol 1998; 72: 4104-4115.
97. Bukrinsky MI, Haffar OK. HIV-1 nuclear import: matrix protein is back on center stage, this time together with Vpr. Mol Med 1998; 4: 138-143.
98. Sato A, Yoshimoto J, Isaka Y, et al. Evidence for direct association of Vpr and matrix protein p17 within the HIV-1 virion. Virology 1996; 220: 208-212.
99. Agostini I, Popov S, Li J, et al. Heat-shock protein 70 can replace viral protein R of HIV-1 during nuclear import of the viral preintegration complex. Exp Cell Res 2000; 259: 398-403.
100. Fletcher TM, Brichacek B, Sharova N, et al. Nuclear import and cell cycle arrest functions of the HIV-1 Vpr protein are encoded by two separate genes in HIV-2/SIV(SM). EMBO J 1996; 15: 6155-6165.
101. Pancio HA, Vander Heyden N, Ratner L. The C-terminal proline-rich tail of human immunodeficiency virus type 2 Vpx is necessary for nuclear localization of the viral preintegration complex in nondividing cells. J Virol 2000; 74: 6162-6167.
102. Mahalingam S, Van Tine B, Santiago ML, et al. Functional analysis of the simian immunodeficiency virus vpx protein: identification of packaging determinants and a novel nuclear targeting domain. J Virol 2001; 75: 362-374.
103. Gallay P, Hope T, Chin D, et al. HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proc Natl Acad Sci U S A 1997; 94: 9825-9830.
104. Moore SP, Rinckel LA, Garfinkel DJ. A Ty1 integrase nuclear localization signal required for retrotransposition. Mol Cell Biol 1998; 18: 1105-1114.
105. Pluymers W, Cherepanov P, Schols D, et al. Nuclear localization of human immunodeficiency virus type 1 integrase expressed as a fusion protein with green fluorescent protein. Virology 1999; 258: 327-332.
106. Petit C, Schwartz O, Mammano F. The karyophilic properties of human immunodeficiency virus type 1 integrase are not required for nuclear import of proviral DNA. J Virol 2000; 74: 7119-7126.
107. Tsurutani N, Kubo M, Maeda Y, et al. Identification of critical amino acid residues in human immunodeficiency virus type 1 IN required for efficient proviral DNA formation at steps prior to integration in dividing and nondividing cells. J Virol 2000; 74: 4795-4806.
108. Bouyac-Bertoia M, Dvorin JD, Fouchier RA, et al. Hiv-1 infection requires a functional integrase nls. Mol Cell 2001; 7: 1025-1035.
109. Kukolj G, Jones KS, Skalka AM. Subcellular localization of avian sarcoma virus and human immunodeficiency virus type 1 integrases. J Virol 1997; 71: 843-847.
110. Kukolj G, Katz RA, Skalka AM. Characterization of the nuclear localization signal in the avian sarcoma virus integrase. Gene 1998; 223: 157-163.
111. Chameau P, Alizon M, Clavel F. A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J Virol 1992; 66: 2814-2820.
112. Chameau P, Mirambeau G, Roux P, et al. HIV-1 reverse transcription. A termination step at the center of the genome. J Mol Biol 1994; 241: 651-662.
113. Sirven A, Pflumio F, Zennou V, et al. The human immunodeficiency virus type-1 central DNA flap is a crucial determinant for lentiviral vector nuclear import and gene transduction of human hematopoietic stem cells. Blood 2000; 96: 4103-4110.
114. Stevenson M. HIV nuclear import: What's the flap? Nature Med 2000; 6: 626-628.
115. Zennou V, Petit C, Guetard D, et al. HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 2000; 101: 173-185.
116. 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 2001; 20: 3272-3281.
117. Roth DB, Wilson JH. Relative rates of homologous and nonhomologous recombination in transfected DNA. Proc Natl Acad Sci U S A 1985; 82: 3355-3359.
118. Bukrinsky M, Sharova N, Stevenson M. Human immunodeficiency virus type 1 2-LTR circles reside in a nucleoprotein complex which is different from the preintegration complex. J Virol 1993; 67: 6863-6865.
119. Yuan B, Li X, Goff SP. Mutations altering the Moloney murine leukemia virus p12 Gag protein affect virion production and early events of the virus life cycle. EMBO J 1999; 18: 4700-4710.
120. Brown PO. Integration. In Retroviruses, Coffin JM, Hughes SH, Varmus HE, eds. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1997; 161-203.
121. Bushman FD. Host proteins in retroviral cDNA integration. Adv Virus Res 1999; 52: 301-317.
122. Lee MS, Craigie R. A previously unidentified host protein protects retroviral DNA from autointegration. Proc Natl Acad Sci U S A 1998; 95: 1528-1533.
123. Cai M, Huang Y, Zheng R, et al. Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration. Nat Struct Biol 1998; 5: 903-909.
124. Umland TC, Wei SQ, Craigie R, et al. Structural basis of DNA bridging by barrier-to-autointegration factor. Biochemistry 2000; 39: 9130-9138.
125. Zheng R, Ghirlando R, Lee MS, et al. Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleo-protein complex. Proc Natl Acad Sci U S A 2000; 97: 8997-9002.
126. Chen H, Engelman A. The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc Natl Acad Sci U S A 1998; 95: 15270-15274.
127. Farnet CM, Bushman FD. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell 1997; 88: 483-492.
128. Li L, Yoder K, Hansen MS, et al. Retroviral cDNA integration: stimulation by HMG I family proteins. J Virol 2000; 74: 10965-10974.
129. Kalpana GV, Marmon S, Wang W, et al. Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 1994; 266: 2002-2006.
130. Carteau S, Gorelick RJ, Bushman FD. Coupled integration of human immunodeficiency virus type 1 cDNA ends by purified integrase in vitro: stimulation by the viral nucleocapsid protein. J Virol 1999; 73: 6670-6679.
131. Scherdin U, Rhodes K, Breindl M. Transcriptionally active genome regions are preferred targets for retrovirus integration. J Virol 1990; 64: 907-912.
132. Vijaya S, Steffen DL, Robinson HL. Acceptor sites for retroviral integrations map near DNase I-hypersensitive sites in chromatin. J Virol 1986; 60: 683-692.
133. Weidhaas JB, Angelichio EL, Fenner S, et al. Relationship between retroviral DNA integration and gene expression. J Virol 2000; 74: 8382-8389.
134. Brin E, Yi J, Skalka AM, et al. Modeling the late steps in HIV-1 retroviral integrase-catalyzed DNA integration. J Biol Chem 2000; 275: 39287-39295.
135. Yoder KE, Bushman FD. Repair of gaps in retroviral DNA integration intermediates. J Virol 2000; 74: 11191-11200.
136. Daniel R, Katz RA, Skalka AM. A role for DNA-PK in retroviral DNA integration. Science 1999; 284: 644-647.
137. Kotecki M, Reddy PS, Cochran BH. Isolation and characterization of a near-haploid human cell line. Exp Cell Res 1999; 252: 273-280.
138. Elbashir SM, Harborth J, Lendeckel W, et al. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001; 411: 494-498.