Cyclophilin A promotes HIV-1 reverse transcription but its effect on transduction correlates best with its effect on nuclear entry of viral cDNA

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  De Iaco, Alberto ^a   Luban, Jeremy ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Capsid; Cyclophilin A; Cyclosporine A; HIV 1; Nuclear transport; Virion uncoating

Indexed keywords

CYCLOPHILIN A; DNA, COMPLEMENTARY; HELA CELLS; HIV CORE PROTEIN P24; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; REVERSE TRANSCRIPTION; TRANSDUCTION, GENETIC; VIRUS INTEGRATION;

EID: 84893204722     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-11     Document Type: Article

References (51)

1. Franke EK, Yuan HE, Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 1994, 372:359-362. 10.1038/372359a0, 7969494.
2. Thali M, Bukovsky A, Kondo E, Rosenwirth B, Walsh CT, Sodroski J, Gottlinger HG. Functional association of cyclophilin A with HIV-1 virions. Nature 1994, 372:363-365. 10.1038/372363a0, 7969495.
3. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 1993, 73:1067-1078. 10.1016/0092-8674(93)90637-6, 8513493.
4. Braaten D, Ansari H, Luban J. The hydrophobic pocket of cyclophilin is the binding site for the human immunodeficiency virus type 1 Gag polyprotein. J Virol 1997, 71:2107-2113. 191305, 9032343.
5. Dorfman T, Weimann A, Borsetti A, Walsh CT, Gottlinger HG. Active-site residues of cyclophilin A are crucial for its incorporation into human immunodeficiency virus type 1 virions. J Virol 1997, 71:7110-7113. 192007, 9261445.
6. Colgan J, Yuan HE, Franke EK, Luban J. Binding of the human immunodeficiency virus type 1 Gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires Gag dimerization. J Virol 1996, 70:4299-4310. 190362, 8676452.
7. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, Hill CP. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 1996, 87:1285-1294. 10.1016/S0092-8674(00)81823-1, 8980234.
8. Sokolskaja E, Berthoux L, Luban J. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J Virol 2006, 80:2855-2862. 10.1128/JVI.80.6.2855-2862.2006, 1395419, 16501094.
9. Bosco DA, Eisenmesser EZ, Pochapsky S, Sundquist WI, Kern D. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc Natl Acad Sci USA 2002, 99:5247-5252. 10.1073/pnas.082100499, 122755, 11929983.
10. Luban J. Cyclophilin A, TRIM5, and resistance to human immunodeficiency virus type 1 infection. J Virol 2007, 81:1054-1061. 10.1128/JVI.01519-06, 1797489, 16956947.
11. 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. 190230, 8648689.
12. Sokolskaja E, Sayah DM, Luban J. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J Virol 2004, 78:12800-12808. 10.1128/JVI.78.23.12800-12808.2004, 524981, 15542632.
13. Braaten D, Luban J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J 2001, 20:1300-1309. 10.1093/emboj/20.6.1300, 145517, 11250896.
14. Wainberg MA, Dascal A, Blain N, Fitz-Gibbon L, Boulerice F, Numazaki K, Tremblay M. The effect of cyclosporine A on infection of susceptible cells by human immunodeficiency virus type 1. Blood 1988, 72:1904-1910.
15. Yin L, Braaten D, Luban J. Human immunodeficiency virus type 1 replication is modulated by host cyclophilin A expression levels. J Virol 1998, 72:6430-6436. 109799, 9658084.
16. Song C, Aiken C. Analysis of human cell heterokaryons demonstrates that target cell restriction of cyclosporine-resistant human immunodeficiency virus type 1 mutants is genetically dominant. J Virol 2007, 81:11946-11956. 10.1128/JVI.00620-07, 2168785, 17715216.
17. Ylinen LM, Schaller T, Price A, Fletcher AJ, Noursadeghi M, James LC, Towers GJ. Cyclophilin A levels dictate infection efficiency of human immunodeficiency virus type 1 capsid escape mutants A92E and G94D. J Virol 2009, 83:2044-2047. 10.1128/JVI.01876-08, 2643744, 19073742.
18. Matsuoka S, Dam E, Lecossier D, Clavel F, Hance AJ. Modulation of HIV-1 infectivity and cyclophilin A-dependence by Gag sequence and target cell type. Retrovirology 2009, 6:21. 10.1186/1742-4690-6-21, 2653016, 19254360.
19. Hatziioannou T, Perez-Caballero D, Cowan S, Bieniasz PD. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J Virol 2005, 79:176-183. 10.1128/JVI.79.1.176-183.2005, 538701, 15596813.
20. Braaten D, Franke EK, Luban J. Cyclophilin A is required for the replication of group M human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus SIV(CPZ)GAB but not group O HIV-1 or other primate immunodeficiency viruses. J Virol 1996, 70:4220-4227. 190352, 8676442.
21. Aberham C, Weber S, Phares W. Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J Virol 1996, 70:3536-3544. 190228, 8648687.
22. 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, 82:12001-12008. 10.1128/JVI.01518-08, 2593355, 18829762.
23. De Iaco A, Luban J. Inhibition of HIV-1 infection by TNPO3 depletion is determined by capsid and detectable after viral cDNA enters the nucleus. Retrovirology 2011, 8:98. 10.1186/1742-4690-8-98, 3267670, 22145813.
24. Ambrose Z, Lee K, Ndjomou J, Xu H, Oztop I, Matous J, Takemura T, Unutmaz D, Engelman A, Hughes SH, KewalRamani VN. Human immunodeficiency virus type 1 capsid mutation N74D alters cyclophilin A dependence and impairs macrophage infection. J Virol 2012, 86:4708-4714. 10.1128/JVI.05887-11, 3318671, 22301145.
25. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG, Vandegraaff N, Baumann JG, Wang R, Yuen W, et al. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 2010, 7:221-233. 10.1016/j.chom.2010.02.007, 2841689, 20227665.
26. De Iaco A, Santoni F, Vannier A, Guipponi M, Antonarakis S, Luban J. TNPO3 protects HIV-1 replication from CPSF6-mediated capsid stabilization in the host cell cytoplasm. Retrovirology 2013, 10:20. 10.1186/1742-4690-10-20, 3599327, 23414560.
27. Yang R, Aiken C. A mutation in alpha helix 3 of CA renders human immunodeficiency virus type 1 cyclosporin A resistant and dependent: rescue by a second-site substitution in a distal region of CA. J Virol 2007, 81:3749-3756. 10.1128/JVI.02634-06, 1866112, 17267487.
28. Braaten D, Aberham C, Franke EK, Yin L, Phares W, Luban J. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J Virol 1996, 70:5170-5176. 190472, 8764025.
29. Li Y, Kar AK, Sodroski J. Target cell type-dependent modulation of human immunodeficiency virus type 1 capsid disassembly by cyclophilin A. J Virol 2009, 83:10951-10962. 10.1128/JVI.00682-09, 2772774, 19656870.
30. Yamashita M, Emerman M. Cellular restriction targeting viral capsids perturbs human immunodeficiency virus type 1 infection of nondividing cells. J Virol 2009, 83:9835-9843. 10.1128/JVI.01084-09, 2748051, 19625401.
31. Shah VB, Shi J, Hout DR, Oztop I, Krishnan L, Ahn J, Shotwell MS, Engelman A, Aiken C. The host proteins transportin SR2/TNPO3 and cyclophilin A exert opposing effects on HIV-1 uncoating. J Virol 2013, 87:422-432. 10.1128/JVI.07177-11, 3536424, 23097435.
32. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, KewalRamani VN, et al. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog 2011, 7:e1002439. 10.1371/journal.ppat.1002439, 3234246, 22174692.
33. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365. 10.1038/nature09976, 3081621, 21512573.
34. Cimarelli A, Sandin S, Hoglund S, Luban J. Rescue of multiple viral functions by a second-site suppressor of a human immunodeficiency virus type 1 nucleocapsid mutation. J Virol 2000, 74:4273-4283. 10.1128/JVI.74.9.4273-4283.2000, 111944, 10756042.
35. Butler SL, Hansen MS, Bushman FD. A quantitative assay for HIV DNA integration in vivo. Nat Med 2001, 7:631-634. 10.1038/87979, 11329067.
36. Takada K, Horinouchi K, Ono Y, Aya T, Osato T, Takahashi M, Hayasaka S. An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 1991, 5:147-156. 10.1007/BF00571929, 1647567.
37. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H, Parks WP. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 1973, 51:1417-1423.
38. Smith SD, Shatsky M, Cohen PS, Warnke R, Link MP, Glader BE. Monoclonal antibody and enzymatic profiles of human malignant T-lymphoid cells and derived cell lines. Cancer Res 1984, 44:5657-5660.
39. Sayah DM, Luban J. Selection for loss of Ref1 activity in human cells releases human immunodeficiency virus type 1 from cyclophilin A dependence during infection. J Virol 2004, 78:12066-12070. 10.1128/JVI.78.21.12066-12070.2004, 523284, 15479848.
40. 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 2002, 418:646-650. 10.1038/nature00939, 12167863.
41. Neagu MR, Ziegler P, Pertel T, Strambio-De-Castillia C, Grutter C, Martinetti G, Mazzucchelli L, Grutter M, Manz MG, Luban J. Potent inhibition of HIV-1 by TRIM5-cyclophilin fusion proteins engineered from human components. J Clin Invest 2009, 119:3035-3047. 10.1172/JCI39354, 2752079, 19741300.
42. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006, 103:5514-5519. 10.1073/pnas.0509996103, 1459386, 16540544.
43. Hulme AE, Perez O, Hope TJ. Complementary assays reveal a relationship between HIV-1 uncoating and reverse transcription. Proc Natl Acad Sci USA 2011, 108:9975-9980. 10.1073/pnas.1014522108, 3116424, 21628558.
44. Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, Hue S, Barclay WS, Schulz R, Malim MH. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502:559-562. 10.1038/nature12542, 24048477.
45. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, Schoggins JW, Rice CM, Yamashita M, Hatziioannou T, Bieniasz PD. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 2013, 502:563-566. 10.1038/nature12653, 24121441.
46. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, Cen S, Guo F, Liang C. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 2013, 14:398-410. 10.1016/j.chom.2013.08.015, 24055605.
47. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998, 72:9873-9880. 110499, 9811723.
48. Berthoux L, Towers GJ, Gurer C, Salomoni P, Pandolfi PP, Luban J. As(2)O(3) enhances retroviral reverse transcription and counteracts Ref1 antiviral activity. J Virol 2003, 77:3167-3180. 10.1128/JVI.77.5.3167-3180.2003, 149754, 12584341.
49. Kaul A, Stauffer S, Berger C, Pertel T, Schmitt J, Kallis S, Zayas M, Lohmann V, Luban J, Bartenschlager R. Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics. PLoS Pathog 2009, 5:e1000546. 10.1371/journal.ppat.1000546, 2718831, 19680534.
50. Pizzato M, Erlwein O, Bonsall D, Kaye S, Muir D, McClure MO. A one-step SYBR Green I-based product-enhanced reverse transcriptase assay for the quantitation of retroviruses in cell culture supernatants. J Virol Methods 2009, 156:1-7. 10.1016/j.jviromet.2008.10.012, 19022294.
51. Maudru T, Peden KW. Adaptation of the fluorogenic 5′-nuclease chemistry to a PCR-based reverse transcriptase assay. Biotechniques 1998, 25:972-975.