HIV-1 uncoating is facilitated by dynein and kinesin 1

Journal of Virology

Volumn 88, Issue 23, 2014, Pages 13613-13625

  Lukic, Zana ^a   Dharan, Adarsh ^a   Fricke, Thomas ^b   Diaz Griffero, Felipe ^b   Campbell, Edward M ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; CYCLOSPORIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN 1; NOCODAZOLE; SMALL INTERFERING RNA; KIF5B PROTEIN, HUMAN; KINESIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL MIGRATION; DEPOLYMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LIFE CYCLE; MICROBIAL POPULATION DYNAMICS; MICROTUBULE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION; VIRION; VIRUS GENOME; VIRUS PARTICLE; VIRUS UNCOATING; ANIMAL; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANIMALS; CELL LINE; DYNEINS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; KINESIN; VIRUS UNCOATING;

EID: 84908676379     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02219-14     Document Type: Article

References (38)

1. Coffin JM, Hughes SH, Varmus HE. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Butler SL, Hansen MS, Bushman FD. 2001. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 7:631-634. http://dx.doi.org/10.1038 /87979.
3. Fassati A, Goff SP. 2001. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J. Virol. 75:3626-3635. http://dx.doi.org/10.1128/JVI.75.8.3626-3635.2001.
4. Fassati A, Goff SP. 1999. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J. Virol. 73:8919-8925.
5. Miller MD, Farnet CM, Bushman FD. 1997. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71:5382-5390.
6. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG, Emerman M, Hope TJ. 2002. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159:441-452. http://dx.doi.org/10.1083/jcb.200203150.
7. Hulme AE, Perez O, Hope TJ. 2011. Complementary assays reveal a relationship between HIV-1 uncoating and reverse transcription. Proc. Natl. Acad. Sci. U. S. A. 108:9975-9980. http://dx.doi.org/10.1073/pnas.1014522108.
8. Perez-Caballero D, Hatziioannou T, Zhang F, Cowan S, Bieniasz PD. 2005. Restriction of human immunodeficiency virus type 1 by TRIMCypA occurs with rapid kinetics and independently of cytoplasmic bodies, ubiquitin, and proteasome activity. J. Virol. 79:15567-15572. http://dx.doi.org/10.1128/JVI.79.24.15567-15572.2005.
9. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG, Vandegraaff N, Baumann JG, Wang R, Yuen W, Takemura T, Shelton K, Taniuchi I, Li Y, Sodroski J, Littman DR, Coffin JM, Hughes SH, Unutmaz D, Engelman A, KewalRamani VN. 2010. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7:221-233. http: //dx.doi.org/10.1016/j.chom.2010.02.007.
10. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, KewalRamani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers GJ. 2011. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 7:e1002439. http://dx.doi.org/10.1371/journal.ppat.1002439.
11. Yamashita M, Emerman M. 2004. Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J. Virol. 78:5670-5678. http: //dx.doi.org/10.1128/JVI.78.11.5670-5678.2004.
12. Zhou L, Sokolskaja E, Jolly C, James W, Cowley SA, Fassati A. 2011. Transportin 3 promotes a nuclear maturation step required for efficient HIV-1 integration. PLoS Pathog. 7:e1002194. http://dx.doi.org/10.1371 /journal.ppat.1002194.
13. Sabo Y, Walsh D, Barry DS, Tinaztepe S, de Los Santos K, Goff SP, Gundersen GG, Naghavi MH. 2013. HIV-1 induces the formation of stable microtubules to enhance early infection. Cell Host Microbe 14:535- 546. http://dx.doi.org/10.1016/j.chom.2013.10.012.
14. Campbell EM, Perez O, Anderson JL, Hope TJ. 2008. Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5. J. Cell Biol. 180:549-561. http://dx.doi.org/10.1083/jcb.200706154.
15. Lehmann M, Milev MP, Abrahamyan L, Yao XJ, Pante N, Mouland AJ. 2009. Intracellular transport of human immunodeficiency virus type 1 genomic RNA and viral production are dependent on dynein motor function and late endosome positioning. J. Biol. Chem. 284:14572-14585. http://dx.doi.org/10.1074/jbc.M808531200.
16. Pawlica P, Le Sage V, Poccardi N, Tremblay MJ, Mouland AJ, Berthoux L. 2014. Functional evidence for the involvement of microtubules and dynein motor complexes in TRIM5-mediated restriction of retroviruses. J. Virol. 88:5661-5676. http://dx.doi.org/10.1128/JVI.03717-13.
17. Gupta V, Palmer KJ, Spence P, Hudson A, Stephens DJ. 2008. Kinesin-1 (uKHC/KIF5B) is required for bidirectional motility of ER exit sites and efficient ER-to-Golgi transport. Traffic 9:1850-1866. http://dx.doi.org/10.1111/j.1600-0854.2008.00811.x.
18. Firestone AJ, Weinger JS, Maldonado M, Barlan K, Langston LD, O'Donnell M, Gelfand VI, Kapoor TM, Chen JK. 2012. Small-molecule inhibitors of the AAA_ ATPase motor cytoplasmic dynein. Nature 484: 125-129. http://dx.doi.org/10.1038/nature10936.
19. Gaudin R, de Alencar BC, Arhel N, Benaroch P. 2013. HIV trafficking in host cells: motors wanted! Trends Cell Biol. 23:652-662. http://dx.doi.org /10.1016/j.tcb.2013.09.004.
20. Simm M, Shahabuddin M, Chao W, Allan JS, Volsky DJ. 1995. Aberrant Gag protein composition of a human immunodeficiency virus type 1 vif mutant produced in primary lymphocytes. J. Virol. 69:4582-4586.
21. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. 2006. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5 restriction factor. Proc. Natl. Acad. Sci. U. S. A. 103:5514-5519. http://dx.doi.org/10.1073/pnas.0509996103.
22. Yang Y, Luban J, Diaz-Griffero F. 2014. The fate of HIV-1 capsid: a biochemical assay for HIV-1 uncoating. Methods Mol. Biol. 1087:29-36. http://dx.doi.org/10.1007/978-1-62703-670-2_3.
23. Wu X, Anderson JL, Campbell EM, Joseph AM, Hope TJ. 2006. Proteasome inhibitors uncouple rhesus TRIM5 restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U. S. A. 103:7465-7470. http://dx.doi.org/10.1073/pnas.0510483103.
24. Hulme AE, Hope TJ. 2014. The cyclosporin A washout assay to detect HIV-1 uncoating in infected cells. Methods Mol. Biol. 1087:37-46. http: //dx.doi.org/10.1007/978-1-62703-670-2_4.
25. Sayah DM, Sokolskaja E, Berthoux L, Luban J. 2004. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430:569-573. http://dx.doi.org/10.1038/nature02777.
26. Yoder A, Guo J, Yu D, Cui Z, Zhang XE,WuY. 2011. Effects of microtubule modulators on HIV-1 infection of transformed and resting CD4 T cells. J. Virol. 85:3020-3024. http://dx.doi.org/10.1128/JVI.02462-10.
27. Cavrois M, De Noronha C, Greene WC. 2002. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat. Biotechnol. 20:1151-1154. http://dx.doi.org/10.1038/nbt745.
28. Campbell EM, Perez O, Melar M, Hope TJ. 2007. Labeling HIV-1 virions with two fluorescent proteins allows identification of virions that have productively entered the target cell. Virology 360:286-293. http://dx.doi.org/10.1016/j.virol.2006.10.025.
29. Murray JM, Appleton PL, Swedlow JR, Waters JC. 2007. Evaluating performance in three-dimensional fluorescence microscopy. J. Microsc. 228:390-405. http://dx.doi.org/10.1111/j.1365-2818.2007.01861.x.
30. Yuste R (ed). 2011. Imaging: a laboratory manual, 1st ed, vol 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Briggs JA, Simon MN, Gross I, Krausslich HG, Fuller SD, Vogt VM, Johnson MC. 2004. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11:672-675. http://dx.doi.org/10.1038/nsmb785.
32. Li S, Hill CP, Sundquist WI, Finch JT. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407:409-413. http: //dx.doi.org/10.1038/35030177.
33. Yang Y, Fricke T, Diaz-Griffero F. 2013. Inhibition of reverse transcriptase activity increases stability of the HIV-1 core. J. Virol. 87:683-687. http://dx.doi.org/10.1128/JVI.01228-12.
34. Strunze S, Engelke MF, Wang IH, Puntener D, Boucke K, Schleich S, Way M, Schoenenberger P, Burckhardt CJ, Greber UF. 2011. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10:210-223. http://dx.doi.org/10.1016/j.chom.2011.08.010.
35. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5 restricts HIV-1 infection in Old World monkeys. Nature 427:848-853. http://dx.doi.org/10.1038/nature02343.
36. Jolly AL, Gelfand VI. 2011. Bidirectional intracellular transport: utility and mechanism. Biochem. Soc. Trans. 39:1126-1130. http://dx.doi.org /10.1042/BST0391126.
37. Welte MA. 2010. Bidirectional transport: matchmaking for motors. Curr. Biol. 20:R410-R413. http://dx.doi.org/10.1016/j.cub.2010.03.018.
38. Radtke K, Kieneke D, Wolfstein A, Michael K, Steffen W, Scholz T, Karger A, Sodeik B. 2010. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog. 6:e1000991. http://dx.doi.org/10.1371/journal.ppat.1000991.