Role of phosphorylation in the nuclear biology of HIV-1

Current Medicinal Chemistry

Volumn 18, Issue 19, 2011, Pages 2904-2912

  Francis, A C ^a   Di Primio, C ^b   Allouch, A ^b   Cereseto, A ^a  

^a UNIVERSITY OF TRENTO   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

Author keywords

Capsid; HIV 1; Integrase; Kinases; Matrix; Nucleus; Phosphorylation; Rev; Tat; Vpr

Indexed keywords

CD4 ANTIGEN; COMPLEMENTARY DNA; DNA; INTEGRASE; PROTEIN SERINE THREONINE KINASE; VIRUS PROTEIN;

ARTICLE; CATALYSIS; DNA REPAIR; GENOME; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LIFE CYCLE; NONHUMAN; NUCLEAR MEDICINE; PHOSPHORYLATION; RNA REPLICATION; VIRUS REPLICATION;

ANTI-HIV AGENTS; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; VIRUS INTEGRATION; VIRUS REPLICATION;

EID: 79960018683     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986711796150478     Document Type: Article

References (157)

1. Frankel, A. D.; Young, J. A. HIV-1: fifteen proteins and an RNA. Annu Rev Biochem, 1998, 67, 1-25. (Pubitemid 28411121)
2. Freed, E. O. HIV-1 replication. Somat Cell Mol Genet, 2001, 26(1-6), 13-33. (Pubitemid 35332977)
3. Arhel, N. Revisiting HIV-1 uncoating. Retrovirology, 2010, 7, 96.
4. Coffin, J. M.; Hughes, S. H.; Varmus, H. E., Retroviruses. 1997.
5. Suzuki, Y.; Craigie, R. The road to chromatin - nuclear entry of retroviruses. Nat Rev Microbiol, 2007, 5(3), 187-196. (Pubitemid 46291278)
6. Yamashita, M.; Emerman, M. Retroviral infection of non-dividing cells: old and new perspectives. Virology, 2006, 344(1), 88-93. (Pubitemid 41814454)
7. Fassati, A. HIV infection of non-dividing cells: a divisive problem. Retrovirology, 2006, 3, 74.
8. Christ, F.; Thys, W.; De Rijck, J.; Gijsbers, R.; Albanese, A.; Arosio, D.; Emiliani, S.; Rain, J.-C.; Benarous, R.; Cereseto, A.; Debyser, Z. Transportin-SR2 Imports HIV into the Nucleus. Current Biology, 2008, 18(16), 1192-1202.
9. Konig, R.; Zhou, Y.; Elleder, D.; Diamond, T. L.; Bonamy, G. M.; Irelan, J. T.; Chiang, C. Y.; Tu, B. P.; De Jesus, P. D.; Lilley, C. E.; Seidel, S.; Opaluch, A. M.; Caldwell, J. S.; Weitzman, M. D.; Kuhen, K. L.; Bandyopadhyay, S.; Ideker, T.; Orth, A. P.; Miraglia, L. J.; Bushman, F. D.; Young, J. A.; Chanda, S. K. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell, 2008, 135(1), 49-60.
10. Vandegraaff, N.; Engelman, A. Molecular mechanisms of HIV integration and therapeutic intervention. Expert Rev Mol Med, 2007, 9(6), 1-19. (Pubitemid 46358400)
11. Daniel, R.; Katz, R. A.; Merkel, G.; Hittle, J. C.; Yen, T. J.; Skalka, A. M. Wortmannin potentiates integrase-mediated killing of lymphocytes and reduces the efficiency of stable transduction by retroviruses. Mol Cell Biol, 2001, 21(4), 1164-1172. (Pubitemid 32114965)
12. Daniel, R.; Kao, G.; Taganov, K.; Greger, J. G.; Favorova, O.; Merkel, G.; Yen, T. J.; Katz, R. A.; Skalka, A. M. Evidence that the retroviral DNA integration process triggers an ATR-dependent DNA damage response. Proc Natl Acad Sci U S A, 2003, 100(8), 4778-4783. (Pubitemid 36457805)
13. Daniel, R.; Marusich, E.; Argyris, E.; Zhao, R. Y.; Skalka, A. M.; Pomerantz, R. J. Caffeine inhibits human immunodeficiency virus type 1 transduction of nondividing cells. J Virol, 2005, 79(4), 2058-2065. (Pubitemid 40204563)
14. Lau, A.; Swinbank, K. M.; Ahmed, P. S.; Taylor, D. L.; Jackson, S. P.; Smith, G. C.; O'Connor, M. J. Suppression of HIV-1 infection by a small molecule inhibitor of the ATM kinase. Nat Cell Biol, 2005, 7(5), 493-500. (Pubitemid 40637409)
15. Butler, S. L.; Hansen, M. S.; Bushman, F. D. A quantitative assay for HIV DNA integration in vivo. Nat Med, 2001, 7(5), 631-634. (Pubitemid 32448333)
16. Li, L.; Olvera, J. M.; Yoder, K. E.; Mitchell, R. S.; Butler, S. L.; Lieber, M.; Martin, S. L.; Bushman, F. D. Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J, 2001, 20(12), 3272-3281. (Pubitemid 32612014)
17. Kilzer, J. M.; Stracker, T.; Beitzel, B.; Meek, K.; Weitzman, M.; Bushman, F. D. Roles of host cell factors in circularization of retroviral dna. Virology, 2003, 314(1), 460-467. (Pubitemid 37153330)
18. Peterlin, B. M.; Trono, D. Hide, shield and strike back: how HIV-infected cells avoid immune eradication. Nat Rev Immunol, 2003, 3(2), 97-107. (Pubitemid 37328688)
19. Pollard, V. W.; Malim, M. H. The HIV-1 Rev protein. Annu Rev Microbiol, 1998, 52, 491-532. (Pubitemid 28481200)
20. Adamson, C. S.; Freed, E. O. Human immunodeficiency virus type 1 assembly, release, and maturation. Adv Pharmacol, 2007, 55, 347-387.
21. Goff, S. P. Host factors exploited by retroviruses. Nat Rev Microbiol, 2007, 5(4), 253-263. (Pubitemid 46443602)
22. Van Maele, B.; Busschots, K.; Vandekerckhove, L.; Christ, F.; Debyser, Z. Cellular co-factors of HIV-1 integration. Trends Biochem Sci, 2006, 31(2), 98-105. (Pubitemid 43221842)
23. Bryant, M.; Ratner, L. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proceedings of the National Academy of Sciences of the United States of America, 1990, 87(2), 523-527.
24. Ono, A.; Freed, E. O. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. Journal of virology, 1999, 73(5), 4136.
25. Spearman, P.; Horton, R.; Ratner, L.; Kuli-Zade, I. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism. Journal of virology, 1997, 71(9), 6582.
26. Ono, A.; Ablan, S. D.; Lockett, S. J.; Nagashima, K.; Freed, E. O. Phosphatidylinositol (4, 5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(41), 14889-14894. (Pubitemid 39410770)
27. Ono, A.; Waheed, A. A.; Freed, E. O. Depletion of cellular cholesterol inhibits membrane binding and higher-order multimerization of human immunodeficiency virus type 1 Gag. Virology, 2007, 360(1), 27-35.
28. Bhattacharya, J.; Repik, A.; Clapham, P. R. Gag Regulates Association of Human Immunodeficiency Virus Type 1 Envelope with Detergent-Resistant Membranes. J. Virol., 2006, 80(11), 5292-5300.
29. Bukrinsky, M. I.; Haggerty, S.; Dempsey, M. P.; Sharova, N.; Adzhubel, A.; Spitz, L.; Lewis, P.; Goldfarb, D.; Emerman, M.; Stevenson, M. A nuclear localization signal within HIV-1 matrix protein that governs infection of nondividing cells. Nature, 1993, 365(6447), 666-669. (Pubitemid 23350541)
30. Von Schwedler, U.; Kornbluth, R. S.; 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(15), 6992-6996. (Pubitemid 24226788)
31. Gallay, P.; Swingler, S.; Aiken, C.; Trono, D. HIV-1 infection of nondividing cells: C-terminal tyrosine phosphorylation of the viral matrix protein is a key regulator. Cell, 1995, 80(3), 379-388.
32. Bukrinskaya, A. G.; Ghorpade, A.; Heinzinger, N. K.; Smithgall, T. E.; Lewis, R. E.; Stevenson, M. Phosphorylation-dependent human immunodeficiency virus type 1 infection and nuclear targeting of viral DNA. Proceedings of the National Academy of Sciences of the United States of America, 1996, 93(1), 367-371. (Pubitemid 26038160)
33. Kaushik, R.; Ratner, L. Role of human immunodeficiency virus type 1 matrix phosphorylation in an early postentry step of virus replication. Journal of virology, 2004, 78(5), 2319.
34. Haffar, O. K.; Popov, S.; Dubrovsky, L.; Agostini, I.; Tang, H.; Pushkarsky, T.; Nadler, S. G.; Bukrinsky, M. Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. Journal of Molecular Biology, 2000, 299(2), 359-368.
35. Gallay, P.; Stitt, V.; Mundy, C.; Oettinger, M.; Trono, D. Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import. Journal of virology, 1996, 70(2), 1027.
36. Freed, E. O.; Orenstein, J. M.; Buckler-White, A. J.; Martin, M. A. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol., 1994, 68(8), 5311-5320. (Pubitemid 24226606)
37. Fouchier, R. A.; Meyer, B. E.; Simon, J. H.; Fischer, U.; Malim, M. H. 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. The EMBO journal, 1997, 16(15), 4531-4539. (Pubitemid 27326590)
38. Mannioui, A.; Nelson, E.; Schiffer, C.; Felix, N.; Le Rouzic, E.; Benichou, S.; Gluckman, J. C.; Canque, B. Human immunodeficiency virus type 1 KK26-27 matrix mutants display impaired infectivity, circularization and integration but not nuclear import. Virology, 2005, 339(1), 21-30. (Pubitemid 41096062)
39. Reil, H.; Bukovsky, A. A.; Gelderblom, H. R.; Gottlinger, H. G. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J, 1998, 17(9), 2699-2708. (Pubitemid 28221204)
40. Freed, E. O.; Englund, G.; Martin, M. A. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J. Virol., 1995, 69(6), 3949-3954.
41. Burnette, B.; Yu, G.; Felsted, R. L. Phosphorylation of HIV-1 gag proteins by protein kinase C. The Journal of biological chemistry, 1993, 268(12), 8698-8703. (Pubitemid 23118656)
42. Cartier, C.; Deckert, M.; Grangeasse, C.; Trauger, R.; Jensen, F.; Bernard, A.; Cozzone, A.; Desgranges, C.; Boyer, V. Association of ERK2 mitogenactivated protein kinase with human immunodeficiency virus particles. Journal of virology, 1997, 71(6), 4832-4837. (Pubitemid 27204180)
43. Jacque, J. M.; Mann, A.; Enslen, H.; Sharova, N.; Brichacek, B.; Davis, R. J.; Stevenson, M. Modulation of HIV-1 infectivity by MAPK, a virionassociated kinase. EMBO J, 1998, 17(9), 2607-2618. (Pubitemid 28221196)
44. Cartier, C.; Deckert, M.; Grangeasse, C.; Trauger, R.; Jensen, F.; Bernard, A.; Cozzone, A.; Desgranges, C.; Boyer, V. Association of ERK2 mitogenactivated protein kinase with human immunodeficiency virus particles. J. Virol., 1997, 71(6), 4832-4837. (Pubitemid 27204180)
45. Gallay, P.; Swingler, S.; Song, J.; Bushman, F.; Trono, D. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell, 1995, 83(4), 569-576.
46. Cohen, E. A.; Terwilliger, E. F.; Jalinoos, Y.; Proulx, J.; Sodroski, J. G.; Haseltine, W. A. Identification of HIV-1 vpr Product and Function. JAIDS Journal of Acquired Immune Deficiency Syndromes, 1990, 3(1), 11-18. (Pubitemid 20062850)
47. Yuan, X. I. N.; Matsuda, Z.; Matsuda, M.; Essex, M. A. X.; Lee, T.-H. Human Immunodeficiency Virus vpr Gene Encodes a Virion-Associated Protein. AIDS research and human retroviruses, 1990, 6(11), 1265-1271.
48. Tristem, M.; Marshall, C.; Karpas, A.; Hill, F. Evolution of the primate lentiviruses: evidence from vpx and vpr. The EMBO journal, 1992, 11(9), 3405-3412.
49. Paxton, W.; Connor, R. I.; Landau, N. R. Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis. Journal of virology, 1993, 67(12), 7229-7237. (Pubitemid 23343849)
50. Bachand, F.; Yao, X. J.; Hrimech, M.; Rougeau, N.; Cohen, E. A. Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 gag precursor. The Journal of biological chemistry, 1999, 274(13), 9083-9091. (Pubitemid 29164715)
51. Andersen, J. L.; Le Rouzic, E.; Planelles, V. HIV-1 Vpr: Mechanisms of G2 arrest and apoptosis. Experimental and Molecular Pathology, 2008, 85(1), 2-10.
52. Yao, X. J.; Mouland, A. J.; Subbramanian, R. A.; Forget, J.; Rougeau, N.; Bergeron, D.; Cohen, E. A. Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. Journal of virology, 1998, 72(6), 4686-4693. (Pubitemid 28215643)
53. Goh, W. C.; Rogel, M. E.; Kinsey, C. M.; Michael, S. F.; Fultz, P. N.; Nowak, M. A.; Hahn, B. H.; Emerman, M. HIV-1 Vpr increases viral expression by manipulation of the cell cycle: A mechanism for selection of Vpr in vivo. Nat Med, 1998, 4(1), 65-71. (Pubitemid 28133081)
54. He, J.; Choe, S.; Walker, R.; Di Marzio, P.; Morgan, D. O.; Landau, N. R. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol., 1995, 69(11), 6705-6711.
55. Planelles, V.; Bachelerie, F.; Jowett, J. B.; Haislip, A.; Xie, Y.; Banooni, P.; Masuda, T.; Chen, I. S. Fate of the human immunodeficiency virus type 1 provirus in infected cells: a role for vpr. J. Virol., 1995, 69(9), 5883-5889.
56. Heinzinger, N. K.; Bukinsky, M. I.; Haggerty, S. A.; Ragland, A. M.; Kewalramani, V.; Lee, M. A.; Gendelman, H. E.; Ratner, L.; Stevenson, M.; Emerman, M. 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(15), 7311-7315. (Pubitemid 24226853)
57. Connor, R. I.; Chen, B. K.; Choe, S.; Landau, N. R. Vpr Is Required for Efficient Replication of Human Immunodeficiency Virus Type-1 in Mononuclear Phagocytes. Virology, 1995, 206(2), 935-944.
58. Rey, F.; Bouhamdan, M.; Navarro, J. M.; Agostini, I.; Willetts, K.; Bouyac, M.; Tamalet, C.; Spire, B.; Vigne, R.; Sire, J. A role for human immunodeficiency virus type 1 Vpr during infection of peripheral blood mononuclear cells. J Gen Virol, 1998, 79(Pt 5), 1083-1087. (Pubitemid 28203848)
59. Le Rouzic, E.; Benichou, S. The Vpr protein from HIV-1: distinct roles along the viral life cycle. Retrovirology, 2005, 2, 11.
60. Kootstra, N. A.; 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(2), 170-180. (Pubitemid 29393303)
61. Yamashita, M.; Emerman, M. The cell cycle independence of HIV infections is not determined by known karyophilic viral elements. PLoS Pathog, 2005, 1(3), e18.
62. Zufferey, R.; Nagy, D.; Mandel, R. J.; Naldini, L.; Trono, D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol, 1997, 15(9), 871-875.
63. Neil, S.; Martin, F.; Ikeda, Y.; Collins, M. Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol, 2001, 75(12), 5448-5456. (Pubitemid 32488137)
64. Fouchier, R. A. M.; Meyer, B. E.; Simon, J. H. M.; Fischer, U.; Albright, A. V.; Gonzalez-Scarano, F.; Malim, M. H. Interaction of the Human Immunodeficiency Virus Type 1 Vpr Protein with the Nuclear Pore Complex. J. Virol., 1998, 72(7), 6004-6013. (Pubitemid 28283389)
65. Jenkins, Y.; McEntee, M.; Weis, K.; Greene, W. C. Characterization of HIV-1 vpr nuclear import: analysis of signals and pathways. The Journal of cell biology, 1998, 143(4), 875-885. (Pubitemid 28547389)
66. Vodicka, M. A.; Koepp, D. M.; Silver, P. A.; Emerman, M. HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes & Development, 1998, 12(2), 175-185. (Pubitemid 28060448)
67. Le Rouzic, E.; Mousnier, A. E.; Rustum, C.; Stutz, F. C.; Hallberg, E.; Dargemont, C.; Benichou, S. Docking of HIV-1 Vpr to the nuclear envelope is mediated by the interaction with the nucleoporin hCG1. The Journal of biological chemistry, 2002, 277(47), 45091-45098. (Pubitemid 36159110)
68. Fouchier, R. A.; Meyer, B. E.; Simon, J. H.; Fischer, U.; Albright, A. V.; Gonz'Alez-Scarano, F.; Malim, M. H. Interaction of the human immunodeficiency virus type 1 Vpr protein with the nuclear pore complex. Journal of virology, 1998, 72(7), 6004-6013. (Pubitemid 28283389)
69. Nitahara-Kasahara, Y.; Kamata, M.; Yamamoto, T.; Zhang, X.; Miyamoto, Y.; Muneta, K.; Iijima, S.; Yoneda, Y.; Tsunetsugu-Yokota, Y.; Aida, Y. Novel Nuclear Import of Vpr Promoted by Importin {alpha} Is Crucial for Human Immunodeficiency Virus Type 1 Replication in Macrophages. J. Virol., 2007, 81(10), 5284-5293. (Pubitemid 46744437)
70. Lu, Y. L.; Spearman, P.; Ratner, L. Human immunodeficiency virus type 1 viral protein R localization in infected cells and virions. J. Virol., 1993, 67(11), 6542-6550. (Pubitemid 23309120)
71. Zhou, Y.; Ratner, L. Phosphorylation of human immunodeficiency virus type 1 Vpr regulates cell cycle arrest. Journal of virology, 2000, 74(14), 6520-6527. (Pubitemid 30429820)
72. Agostini, I.; Popov, S.; Hao, T.; Li, J. H.; Dubrovsky, L.; Chaika, O.; Chaika, N.; Lewis, R.; Bukrinsky, M. Phosphorylation of Vpr regulates HIV type 1 nuclear import and macrophage infection. AIDS research and human retroviruses, 2002, 18(4), 283-288. (Pubitemid 34253146)
73. Muller, B.; Tessmer, U.; Schubert, U.; Krausslich, H.-G. Human Immunodeficiency Virus Type 1 Vpr Protein Is Incorporated into the Virion in Significantly Smaller Amounts than Gag and Is Phosphorylated in Infected Cells. J. Virol., 2000, 74(20), 9727-9731.
74. Barnitz, R. A.; Wan, F.; Tripuraneni, V.; Bolton, D. L.; Lenardo, M. J. Protein kinase A phosphorylation activates Vpr-induced cell cycle arrest during human immunodeficiency virus type 1 infection. Journal of virology, 2010, 84(13), 6410-6424.
75. Bukovsky, A.; Gottlinger, H. Lack of integrase can markedly affect human immunodeficiency virus type 1 particle production in the presence of an active viral protease. J. Virol., 1996, 70(10), 6820-6825. (Pubitemid 26307392)
76. Quillent, C.; Borman, A. M.; Paulous, S.; Dauguet, C.; Clavel, F. Extensive Regions ofpolAre Required for Efficient Human Immunodeficiency Virus Polyprotein Processing and Particle Maturation. Virology, 1996, 219(1), 29-36. (Pubitemid 26182906)
77. Wu, X.; Liu, H.; Xiao, H.; Conway, J. A.; Hehl, E.; Kalpana, G. V.; Prasad, V.; Kappes, J. C. Human Immunodeficiency Virus Type 1 Integrase Protein Promotes Reverse Transcription through Specific Interactions with the Nucleoprotein Reverse Transcription Complex. J. Virol., 1999, 73(3), 2126-2135. (Pubitemid 29098117)
78. Zhu, K.; Dobard, C. Requirement for integrase during reverse transcription of human immunodeficiency virus type 1 and the effect of cysteine mutations of integrase on its interactions with. Journal of virology, 2004.
79. Briones, M. S.; Dobard, C. W.; Chow, S. A. Role of Human Immunodeficiency Virus Type 1 Integrase in Uncoating of the Viral Core. J. Virol., 2010, 84(10), 5181-5190.
80. Hearps, A. HIV-1 integrase is capable of targeting DNA to the nucleus via an Importin $\alpha$/$\beta$-dependent mechanism. Biochemical Journal, 2006.
81. Gallay, P.; Hope, T.; Chin, D.; Trono, D. 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(18), 9825-9830. (Pubitemid 27408149)
82. Bouyac-Bertoia, M.; Dvorin, J. D.; Fouchier, R. A. M.; Jenkins, Y.; Meyer, B. E.; Wu, L. I.; Emerman, M.; Malim, M. H. HIV-1 Infection Requires a Functional Integrase NLS. Molecular Cell, 2001, 7(5), 1025-1035. (Pubitemid 32525749)
83. Pluymers, W.; Cherepanov, P.; Schols, D.; Clercq, E. D. Nuclear localization of human immunodeficiency virus type 1 integrase expressed as a fusion protein with green fluorescent protein. Virology, 1999.
84. Gallay, P.; Hope, T.; Chin, D.; Trono, D. HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proceedings of the National Academy of Sciences of the United States of America, 1997, 94(18), 9825-9830. (Pubitemid 27408149)
85. Armon-Omer, A.; Graessmann, A.; Loyter, A. A Synthetic Peptide Bearing the HIV-1 Integrase 161-173 Amino Acid Residues Mediates Active Nuclear Import and Binding to Importin [alpha]: Characterization of a Functional Nuclear Localization Signal. Journal of Molecular Biology, 2004, 336(5), 1117-1128. (Pubitemid 38229701)
86. Petit, C.; Schwartz, O. The karyophilic properties of human immunodeficiency virus type 1 integrase are not required for nuclear import of proviral DNA. Journal of Virology, 2000.
87. Depienne, C.; Mousnier, A.; Leh, H.; Le Rouzic, E.; Dormont, D.; Benichou, S.; Dargemont, C. Characterization of the nuclear import pathway for HIV-1 integrase. Journal of Biological Chemistry, 2001, 276(21), 18102.
88. Fassati, A.; G'Orlich, D.; Harrison, I.; Zaytseva, L.; Mingot, J. E.-M. Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7. The EMBO journal, 2003, 22(14), 3675-3685. (Pubitemid 36898344)
89. Zaitseva, L.; Cherepanov, P.; Leyens, L.; Wilson, S. J.; Rasaiyaah, J.; Fassati, A. HIV-1 exploits importin 7 to maximize nuclear import of its DNA genome. Retrovirology, 2009, 6(11), 1-18.
90. Zielske, S. P.; Stevenson, M. Importin 7 may be dispensable for human immunodeficiency virus type 1 and simian immunodeficiency virus infection of primary macrophages. Journal of virology, 2005, 79(17), 11541.
91. Brass, A. L.; Dykxhoorn, D. M.; Benita, Y.; Yan, N.; Engelman, A.; Xavier, R. J.; Lieberman, J.; Elledge, S. J. Identification of Host Proteins Required for HIV Infection Through a Functional Genomic Screen. Science, 2008, 319(5865), 921-926. (Pubitemid 351263756)
92. Maertens, G.; Cherepanov, P.; Pluymers, W.; Busschots, K.; De Clercq, E.; Debyser, Z.; Engelborghs, Y. LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. Journal of Biological Chemistry, 2003, 278(35), 33528.
93. Llano, M.; Saenz, D. T.; Meehan, A.; Wongthida, P.; Peretz, M.; Walker, W. H.; Teo, W.; Poeschla, E. M. An Essential Role for LEDGF/p75 in HIV Integration. Science, 2006, 314(5798), 461-464. (Pubitemid 44628966)
94. Vandekerckhove, L.; Christ, F.; Van Maele, B.; De Rijck, J.; Gijsbers, R.; Van Den Haute, C.; Witvrouw, M.; Debyser, Z. Transient and stable knockdown of the integrase cofactor LEDGF/p75 reveals its role in the replication cycle of human immunodeficiency virus. J Virol, 2006, 80(4), 1886-1896. (Pubitemid 43228728)
95. Zielske, S. P.; Stevenson, M. Modest but reproducible inhibition of human immunodeficiency virus type 1 infection in macrophages following LEDGFp75 silencing. J Virol, 2006, 80(14), 7275-7280. (Pubitemid 44025225)
96. Cereseto, A.; Manganaro, L.; Gutierrez, M. I.; Terreni, M.; Fittipaldi, A.; Lusic, M.; Marcello, A.; Giacca, M. Acetylation of HIV-1 integrase by p300 regulates viral integration. EMBO J, 2005, 24(17), 3070-3081. (Pubitemid 41486343)
97. Topper, M.; Luo, Y.; Zhadina, M.; Mohammed, K.; Smith, L.; Muesing, M. A. Posttranslational acetylation of the human immunodeficiency virus type 1 integrase carboxyl-terminal domain is dispensable for viral replication. J Virol, 2007, 81(6), 3012-3017. (Pubitemid 46447066)
98. Terreni, M.; Valentini, P.; Liverani, V.; Gutierrez, M. I.; Di Primio, C.; Di Fenza, A.; Tozzini, V.; Allouch, A.; Albanese, A.; Giacca, M.; Cereseto, A. GCN5-dependent acetylation of HIV-1 integrase enhances viral integration. Retrovirology, 2010, 7, 18.
99. Manganaro, L.; Lusic, M.; Gutierrez, M. I.; Cereseto, A.; Del Sal, G.; Giacca, M. Concerted action of cellular JNK and Pin1 restricts HIV-1 genome integration to activated CD4+ T lymphocytes. Nat Med, 2010, 16(3), 329-333.
100. Yamashita, M.; Emerman, M. Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol, 2004, 78(11), 5670-5678. (Pubitemid 38661654)
101. Dismuke, D. J.; 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, 2006, 80(8), 3712-3720.
102. Yamashita, M.; Perez, O.; Hope, T. J.; Emerman, M. Evidence for direct involvement of the capsid protein in HIV infection of nondividing cells. PLoS Pathog, 2007, 3(10), 1502-1510. (Pubitemid 350085614)
103. Qi, M.; Yang, R.; Aiken, C. Cyclophilin A-dependent restriction of human immunodeficiency virus type 1 capsid mutants for infection of nondividing cells. J Virol, 2008, 82(24), 12001-12008.
104. Cartier, C.; Hemonnot, B. E. E.; Gay, B.; Bardy, M.; Sanchiz, C. E.; Devaux, C.; Briant, L. Active cAMP-dependent protein kinase incorporated within highly purified HIV-1 particles is required for viral infectivity and interacts with viral capsid protein. The Journal of biological chemistry, 2003, 278(37), 35211-35219. (Pubitemid 37102287)
105. Cartier, C.; Sivard, P.; Tranchat, C.; Decimo, D.; Desgranges, C.; Boyer, V. Identification of three major phosphorylation sites within HIV-1 capsid. Role of phosphorylation during the early steps of infection. The Journal of biological chemistry, 1999, 274(27), 19434-19440.
106. Wacharapornin, P.; Lauhakirti, D.; Auewarakul, P. The effect of capsid mutations on HIV-1 uncoating. Vi rology, 2007, 358(1), 48-54. (Pubitemid 46048879)
107. Brun, S.; Solignat, M.; Gay, B.; Bernard, E.; Chaloin, L.; Fenard, D.; Devaux, C.; Chazal, N.; Briant, L. VSV-G pseudotyping rescues HIV-1 CA mutations that impair core assembly or stability. Retrovirology, 2008, 15, 1-15.
108. Vink, C; Groenink, M.; Elgersma, Y.; Fouchier, R. A.; Tersmette, M.; Plasterk, R. H. Analysis of the junctions between human immunodeficiency virus type 1 proviral DNA and human DNA. J Virol, 1990, 64(11), 5626-5627. (Pubitemid 20364558)
109. Daniel, R.; Katz, R. A.; Skalka, A. M. A role for DNA-PK in retroviral DNA integration. Science, 1999, 284(5414), 644-647. (Pubitemid 29289589)
110. Daniel, R; Greger, J. G.; Katz, R. A.; Taganov, K. D.; Wu, X.; Kappes, J. C; Skalka, A. M. Evidence that stable retroviral transduction and cell survival following DNA integration depend on components of the nonhomologous end joining repair pathway. J Virol, 2004, 78(16), 8573-8581. (Pubitemid 39025123)
111. Baekelandt, V.; Claeys, A.; Cherepanov, P.; De Clercq, E.; De Strooper, B.; Nuttin, B.; Debyser, Z. DNA-Dependent protein kinase is not required for efficient lentivirus integration. J Virol, 2000, 74(23), 11278-11285. (Pubitemid 32223997)
112. Dehart, J. L.; Andersen, J. L.; Zimmerman, E. S.; Ardon, O.; An, D. S.; Blackett, J.; Kim, B.; Planelles, V. The ataxia telangiectasia-mutated and Rad3-related protein is dispensable for retroviral integration. J Virol, 2005, 79(3), 1389-1396. (Pubitemid 40459086)
113. Ariumi, Y.; Turelli, P.; Masutani, M.; Trono, D. DNA damage sensors ATM, ATR, DNA-PKcs, and PARP-1 are dispensable for human immunodeficiency virus type 1 integration. J Virol, 2005, 79(5), 2973-2978. (Pubitemid 40270576)
114. Jeanson, L.; Subra, F.; Vaganay, S.; Hervy, M.; Marangoni, E.; Bourhis, J.; Mouscadet, J. F. Effect of Ku80 depletion on the preintegrative steps of HIV-1 replication in human cells. Virology, 2002, 300(1), 100-108.
115. Pagans, S.; Pedal, A.; North, B. J.; Kaehlcke, K.; Marshall, B. L.; Dorr, A.; Hetzer-Egger, C; Henklein, P.; Frye, R; McBurney, M. W.; Hruby, H.; Jung, M.; Verdin, E.; Ott, M. SIRT1 regulates HIV transcription via Tat deacetylation. PLoS biology, 2005, 3(2), e41.
116. Muesing, M. A.; Smith, D. H.; Capon, D. J. Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell, 1987, 48(4), 691-701. (Pubitemid 18096946)
117. Wei, P.; Garber, M. E.; Fang, S. M.; Fischer, W. H.; Jones, K. A. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell, 1998, 92(4), 451-462. (Pubitemid 28101109)
118. ™Ery, T.; Peng, J.; Ramanathan, Y; Marshall, N.; Marshall, T.; Amendt, B.; Mathews, M. B.; Price, D. H. Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes & Development, 1997, 11(20), 2622-2632. (Pubitemid 27452386)
119. Kim, Y. K.; Bourgeois, C. F.; Isel, C; Churcher, M. J.; Karn, J. Phosphorylation of the RNA Polymerase II Carboxyl-Terminal Domain by CDK9 Is Directly Responsible for Human Immunodeficiency Virus Type 1 Tat-Activated Transcriptional Elongation. Mol. Cell. Biol, 2002, 22(13), 4622-4637. (Pubitemid 34620399)
120. Zhou, M.; Deng, L.; Kashanchi, F.; Brady, J. N.; Shatkin, A. J.; Kumar, A. The Tat/TAR-dependent phosphorylation of RNA polymerase II C-terminal domain stimulates cotranscriptional capping of HIV-1 mRNA. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(22), 12666-12671. (Pubitemid 37339956)
121. Herrmann, C. H.; Rice, A. P. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxylterminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J. Virol, 1995, 69(3), 1612-1620.
122. Yang, X.; Gold, M. O.; Tang, D. N.; Lewis, D. E.; Aguilar-Cordova, E.; Rice, A. P.; Herrmann, C. H. TAK, an HIV Tat-associated kinase, is a member of the cyclin-dependent family of protein kinases and is induced by activation of peripheral blood lymphocytes and differentiation of promonocytic cell lines. Proceedings of the National Academy of Sciences of the United States of America, 1997, 94(23), 12331-12336.
123. Nekhai, S.; Shukla, R. R; Fernandez, A.; Kumar, A.; Lamb, N. J. Cell cycledependent stimulation of the HIV-1 promoter by Tat-associated CAK activator. Virology, 2000, 266(2), 246-256. (Pubitemid 30070629)
124. Nekhai, S.; Zhou, M.; Fernandez, A.; Lane, W. S.; Lamb, N. J. C; Brady, J.; Kumar, A. HIV-1 Tat-associated RNA polymerase C-terminal domain kinase, CDK2, phosphorylates CDK7 and stimulates Tat-mediated transcription. Biochem. J, 2002, 364(3), 649-657. (Pubitemid 34680840)
125. Romani, B.; Engelbrecht, S.; Glashoff, R. H. Functions of Tat: the versatile protein of human immunodeficiency virus type 1. The Journal of general virology, 2010, 91(Pt 1), 1-12.
126. Ammosova, T.; Berro, R; Jerebtsova, M.; Jackson, A.; Charles, S.; Klase, Z.; Southerland, W.; Gordeuk, V; Kashanchi, F.; Nekhai, S. Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription. Retrovirology, 2006, 3(1), 78.
127. Holmes, A. M. In vitro phosphorylation of human immunodeficiency virus type 1 Tat protein by protein kinase C: evidence for the phosphorylation of amino acid residue serine-46. Archives of biochemistry and biophysics, 1996, 335(1), 8-12. (Pubitemid 26382674)
128. Brand, S. R.; Kobayashi, R; Mathews, M. B. The Tat Protein of Human Immunodeficiency Virus Type 1 Is a Substrate and Inhibitor of the Interferon-induced, Virally Activated Protein Kinase, PKR. Journal of Biological Chemistry, 1997, 272(13), 8388-8395. (Pubitemid 27147798)
129. Endo-Munoz, L.; Warby, T.; Harrich, D.; McMillan, N. A. J. Phosphorylation of HIV Tat by PKR increases interaction with TAR RNA and enhances transcription. Virology journal, 2005, 2, 17.
130. Kiernan, R. E.; Vanhulle, C; Schiltz, L.; Adam, E.; Xiao, H.; Maudoux, F.; Calomme, C; Burny, A.; Nakatani, Y; Jeang, K.-T.; Benkirane, M.; Van Lint, C. HIV-1 Tat transcriptional activity is regulated by acetylation. EMBO J, 1999, 18(21), 6106-6118. (Pubitemid 29515686)
131. Ott, M.; Schnölzer, M.; Garnica, J.; Fischle, W.; Emiliani, S.; Rackwitz, H.-R.; Verdin, E. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Current Biology, 1999, 9(24), 1489-1493.
132. Deng, L.; Ammosova, T.; Pumfery, A.; Kashanchi, F.; Nekhai, S. HIV-1 Tat interaction with RNA polymerase II C-terminal domain (CTD) and a dynamic association with CDK2 induce CTD phosphorylation and transcription from HIV-1 promoter. The Journal of biological chemistry, 2002, 277(37), 33922-33929.
133. Cochrane, A. W.; Golub, E.; Volsky, D.; Ruben, S.; Rosen, C. A. Functional significance of phosphorylation to the human immunodeficiency virus Rev protein. J. Virol., 1989, 63(10), 4438-4440. (Pubitemid 19229446)
134. Malim, M. H.; B'Ohnlein, S.; Hauber, J.; Cullen, B. R. Functional dissection of the HIV-1 Rev trans-activator-derivation of a trans-dominant repressor of Rev function. Cell, 1989, 58(1), 205-214. (Pubitemid 19180092)
135. Thomas, S. L.; Oft, M.; Jaksche, H.; Casari, G.; Heger, P.; Dobrovnik, M.; Bevec, D.; Hauber, J. Functional analysis of the human immunodeficiency virus type 1 Rev protein oligomerization interface. Journal of virology, 1998, 72(4), 2935-2944. (Pubitemid 28175531)
136. Hope, T. J. The Ins and Outs of HIV Rev. Archives of biochemistry and biophysics, 1999, 365(2), 186-191. (Pubitemid 29391625)
137. Groom, H. C. T.; Anderson, E. C.; Lever, A. M. L. Rev: beyond nuclear export. The Journal of general virology, 2009, 90(Pt 6), 1303-1318.
138. Hauber, J.; Bouvier, M.; Malim, M. H.; Cullen, B. R. Phosphorylation of the rev gene product of human immunodeficiency virus type 1. Journal of virology, 1988, 62(12), 4801-4804. (Pubitemid 19006151)
139. Meggio, F.; Marin, O.; Boschetti, M.; Sarno, S.; Pinna, L. A. HIV-1 Rev transactivator: a beta-subunit directed substrate and effector of protein kinase CK2. Molecular and cellular biochemistry, 2001, 227(1-2), 145-151. (Pubitemid 34048379)
140. Marin, O.; Sarno, S.; Boschetti, M.; Pagano, M. A.; Meggio, F.; Ciminale, V.; D'Agostino, D. M.; Pinna, L. A. Unique features of HIV-1 Rev protein phosphorylation by protein kinase CK2 ('casein kinase-2'). FEBS letters, 2000, 481(1), 63-67. (Pubitemid 30662378)
141. Meggio, F.; D'Agostino, D. M.; Ciminale, V.; Chieco-Bianchi, L.; Pinna, L. A. Phosphorylation of HIV-1 Rev Protein: Implication of Protein Kinase CK2 and Pro-Directed Kinases. Biochemical and Biophysical Research Communications, 1996, 226(2), 547-554. (Pubitemid 26331938)
142. McCune, J. M. Viral latency in HIV disease. Cell, 1995, 82(2), 183-188.
143. Zack, J. A.; Arrigo, S. J.; Weitsman, S. R.; Go, A. S.; Haislip, A.; Chen, I. S. Y. HIV-1 entry into quiescent primary lymphocytes: Molecular analysis reveals a labile, latent viral structure. Cell, 1990, 61(2), 213-222.
144. Brass, A. L.; Dykxhoorn, D. M.; Benita, Y.; Yan, N.; Engelman, A.; Xavier, R. J.; Lieberman, J.; Elledge, S. J. Identification of host proteins required for HIV infection through a functional genomic screen. Science, 2008, 319(5865), 921.
145. Freed, E. O.; Martin, M. A. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol., 1996, 70(1), 341-351. (Pubitemid 126508804)
146. Camaur, D.; Gallay, P.; Swingler, S.; Trono, D. Human immunodeficiency virus matrix tyrosine phosphorylation: characterization of the kinase and its substrate requirements. Journal of virology, 1997, 71(9), 6834-6841. (Pubitemid 27355344)
147. Swingler, S.; Gallay, P.; Camaur, D.; Song, J.; Abo, A.; Trono, D. The Nef protein of human immunodeficiency virus type 1 enhances serine phosphorylation of the viral matrix. Journal of virology, 1997, 71(6), 4372-4377. (Pubitemid 27204125)
148. Ammosova, T.; Berro, R.; Jerebtsova, M.; Jackson, A.; Charles, S.; Klase, Z.; Southerland, W.; Gordeuk, V. R.; Kashanchi, F.; Nekhai, S. Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription. Retrovirology, 2006, 21, 1-21.
149. McMillan, N. A. J.; Chun, R. F.; Siderovski, D. P.; Galabru, J.; Toone, W. M.; Samuel, C. E.; Mak, T. W.; Hovanessian, A. G.; Jeang, K.-T.; Williams, B. R. G. HIV-1 Tat Directly Interacts with the Interferon-Induced, Double-Stranded RNA-Dependent Kinase, PKR. Virology, 1995, 213(2), 413-424.
150. Cochrane, A.; Kramer, R.; Ruben, S.; Levine, J.; Rosen, C. A. The human immunodeficiency virus rev protein is a nuclear phosphoprotein. Virology, 1989, 171(1), 264-266. (Pubitemid 19180796)
151. Schang, L. M. Cyclin-dependent kinases as cellular targets for antiviral drugs. Journal of Antimicrobial Chemotherapy, 2002, 50(6), 779-792. (Pubitemid 36032796)
152. Schang, L. M. Effects of pharmacological cyclin-dependent kinase inhibitors on viral transcription and replication. Biochimica et biophysica acta, 2004, 1697(1-2), 197-209. (Pubitemid 38326772)
153. Schubert, U.; Strebel, K. Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments. Journal of virology, 1994, 68(4), 2260-2271.
154. Vincent, M. J.; Jabbar, M. A. The Human Immunodeficiency Virus Type 1 Vpu Protein: A Potential Regulator of Proteolysis and Protein Transport in the Mammalian Secretory Pathway. Virology, 1995, 213(2), 639-649.
155. Manganaro, L.; Lusic, M.; Gutierrez, M. I.; Cereseto, A.; Del Sal, G.; Giacca, M. Concerted action of cellular JNK and Pin1 restricts HIV-1 genome integration to activated CD4+ T lymphocytes. Nature medicine, 2010, 16(3), 329-333.
156. Muthumani, K.; Wadsworth, S. A.; Dayes, N. S.; Hwang, D. S.; Choo, A. Y.; Abeysinghe, H. R.; Siekierka, J. J.; Weiner, D. B. Suppression of HIV-1 viral replication and cellular pathogenesis by a novel p38/JNK kinase inhibitor. AIDS, 2004, 18(5), 739-748. (Pubitemid 38535001)
157. Qatsha, K. A.; Rudolph, C.; Marme, D.; Schachtele, C.; May, W. S. Go 6976, a selective inhibitor of protein kinase C, is a potent antagonist of human immunodeficiency virus 1 induction from latent/low-level-producing reservoir cells in vitro. Proc Natl Acad Sci U S A, 1993, 90(10), 4674-4678. (Pubitemid 23148968)