KIF5B and Nup358 Cooperatively Mediate the Nuclear Import of HIV-1 during Infection

PLoS Pathogens

Volumn 12, Issue 6, 2016, Pages

  Dharan, Adarsh ^a   Talley, Sarah ^a   Tripathi, Abhishek ^a   Mamede, João I ^b   Majetschak, Matthias ^a   Hope, Thomas J ^b   Campbell, Edward M ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CYCLOPHILIN A; KINESIN 1; NUCLEOPORIN; POLYCLONAL ANTIBODY; CHAPERONE; KIF5B PROTEIN, HUMAN; KINESIN; RAN-BINDING PROTEIN 2;

ARTICLE; CELL NUCLEUS MEMBRANE; FLOW CYTOMETRY; GENE SEQUENCE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMAGE ANALYSIS; NONHUMAN; NUCLEAR IMPORT; PROTEIN DEPLETION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING; CELL NUCLEUS; FLUORESCENCE MICROSCOPY; GENE SILENCING; HEK293 CELL LINE; HELA CELL LINE; HUMAN; IMAGE PROCESSING; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PATHOGENICITY; PHYSIOLOGY; VIROLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; BLOTTING, WESTERN; CELL NUCLEUS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; KINESIN; MICROSCOPY, FLUORESCENCE; MOLECULAR CHAPERONES; NUCLEAR PORE COMPLEX PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84978870712     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005700     Document Type: Article

References (52)

1. Yamashita M, Emerman M, (2004) Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol78: 5670–5678. 15140964
2. Yamashita M, Perez O, Hope TJ, Emerman M, (2007) Evidence for direct involvement of the capsid protein in HIV infection of nondividing cells. PLoS Pathog3: 1502–1510. 17967060
3. Campbell EM, Hope TJ, (2015) HIV-1 capsid: the multifaceted key player in HIV-1 infection. Nat Rev Microbiol13: 471–483. doi: 10.1038/nrmicro350326179359
4. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J, (2010) The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol11: 1005–1013. doi: 10.1038/ni.194120871604
5. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, et al. (2013) HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature503: 402–405. doi: 10.1038/nature1276924196705
6. Gao D, Wu J, Wu YT, Du F, Aroh C, et al. (2013) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science341: 903–906. doi: 10.1126/science.124093323929945
7. Lahaye X, Satoh T, Gentili M, Cerboni S, Conrad C, et al. (2013) The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity39: 1132–1142. doi: 10.1016/j.immuni.2013.11.00224269171
8. Briggs JA, Simon MN, Gross I, Krausslich HG, Fuller SD, et al. (2004) The stoichiometry of Gag protein in HIV-1. Nat Struct Mol Biol11: 672–675. 15208690
9. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI, (1999) Assembly and analysis of conical models for the HIV-1 core. Science283: 80–83. 9872746
10. Lowe AR, Siegel JJ, Kalab P, Siu M, Weis K, et al. (2010) Selectivity mechanism of the nuclear pore complex characterized by single cargo tracking. Nature467: 600–603. doi: 10.1038/nature0928520811366
11. Pante N, Kann M, (2002) Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell13: 425–434. 11854401
12. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, et al. (2008) Identification of host proteins required for HIV infection through a functional genomic screen. Science319: 921–926. doi: 10.1126/science.115272518187620
13. Konig R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, et al. (2010) Human host factors required for influenza virus replication. Nature463: 813–817. doi: 10.1038/nature0869920027183
14. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, et al. (2008) Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe4: 495–504. doi: 10.1016/j.chom.2008.10.00418976975
15. Strambio-De-Castillia C, Niepel M, Rout MP, (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol11: 490–501. doi: 10.1038/nrm292820571586
16. Di Nunzio F, Danckaert A, Fricke T, Perez P, Fernandez J, et al. (2012) Human nucleoporins promote HIV-1 docking at the nuclear pore, nuclear import and integration. PLoS One7: e46037. doi: 10.1371/journal.pone.004603723049930
17. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, et al. (2008) Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell135: 49–60. doi: 10.1016/j.cell.2008.07.03218854154
18. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, et al. (2011) HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog7: e1002439. doi: 10.1371/journal.ppat.100243922174692
19. Zhang R, Mehla R, Chauhan A, (2010) Perturbation of host nuclear membrane component RanBP2 impairs the nuclear import of human immunodeficiency virus -1 preintegration complex (DNA). PLoS One5: e15620. doi: 10.1371/journal.pone.001562021179483
20. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, et al. (2010) Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe7: 221–233. doi: 10.1016/j.chom.2010.02.00720227665
21. Matreyek KA, Engelman A, (2011) The requirement for nucleoporin NUP153 during human immunodeficiency virus type 1 infection is determined by the viral capsid. J Virol85: 7818–7827. doi: 10.1128/JVI.00325-1121593146
22. Matreyek KA, Yucel SS, Li X, Engelman A, (2013) Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog9: e1003693. doi: 10.1371/journal.ppat.100369324130490
23. Bhattacharya A, Alam SL, Fricke T, Zadrozny K, Sedzicki J, et al. (2014) Structural basis of HIV-1 capsid recognition by PF74 and CPSF6. Proc Natl Acad Sci U S A111: 18625–18630. doi: 10.1073/pnas.141994511225518861
24. Price AJ, Fletcher AJ, Schaller T, Elliott T, Lee K, et al. (2012) CPSF6 defines a conserved capsid interface that modulates HIV-1 replication. PLoS Pathog8: e1002896. doi: 10.1371/journal.ppat.100289622956906
25. Price AJ, Jacques DA, McEwan WA, Fletcher AJ, Essig S, et al. (2014) Host cofactors and pharmacologic ligands share an essential interface in HIV-1 capsid that is lost upon disassembly. PLoS Pathog10: e1004459. doi: 10.1371/journal.ppat.100445925356722
26. Bichel K, Price AJ, Schaller T, Towers GJ, Freund SM, et al. (2013) HIV-1 capsid undergoes coupled binding and isomerization by the nuclear pore protein NUP358. Retrovirology10.
27. Meehan AM, Saenz DT, Guevera R, Morrison JH, Peretz M, et al. (2014) A cyclophilin homology domain-independent role for Nup358 in HIV-1 infection. PLoS Pathog10: e1003969. doi: 10.1371/journal.ppat.100396924586169
28. Lukic Z, Dharan A, Fricke T, Diaz-Griffero F, Campbell EM, (2014) HIV-1 Uncoating is Facilitated by Dynein and Kinesin-1. J Virol88: 13613–13625. doi: 10.1128/JVI.02219-1425231297
29. Malikov V, da Silva ES, Jovasevic V, Bennett G, de Souza Aranha Vieira DA, et al. (2015) HIV-1 capsids bind and exploit the kinesin-1 adaptor FEZ1 for inward movement to the nucleus. Nat Commun6: 6660. doi: 10.1038/ncomms766025818806
30. Pawlica P, Berthoux L, (2014) Cytoplasmic Dynein Promotes HIV-1 Uncoating. Viruses6: 4195–4211. doi: 10.3390/v611419525375884
31. Berthoux L, Sebastian S, Sokolskaja E, Luban J, (2004) Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J Virol78: 11739–11750. 15479815
32. De Iaco A, Luban J, (2011) Inhibition of HIV-1 infection by TNPO3 depletion is determined by capsid and detectable after viral cDNA enters the nucleus. Retrovirology8: 98. doi: 10.1186/1742-4690-8-9822145813
33. Sastri J, O'Connor C, Danielson CM, McRaven M, Perez P, et al. (2010) Identification of residues within the L2 region of rhesus TRIM5alpha that are required for retroviral restriction and cytoplasmic body localization. Virology405: 259–266. doi: 10.1016/j.virol.2010.06.01520633914
34. Campbell EM, Perez O, Anderson JL, Hope TJ, (2008) Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5alpha. J Cell Biol180: 549–561. doi: 10.1083/jcb.20070615418250195
35. 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. Traffic9: 1850–1866. doi: 10.1111/j.1600-0854.2008.00811.x18817524
36. Hutten S, Walde S, Spillner C, Hauber J, Kehlenbach RH, (2009) The nuclear pore component Nup358 promotes transportin-dependent nuclear import. J Cell Sci122: 1100–1110. doi: 10.1242/jcs.04015419299463
37. Lukic Z, Dharan A, Fricke T, Diaz-Griffero F, Campbell EM, (2014) HIV-1 uncoating is facilitated by dynein and kinesin 1. J Virol88: 13613–13625. doi: 10.1128/JVI.02219-1425231297
38. Butler SL, Hansen MS, Bushman FD, (2001) A quantitative assay for HIV DNA integration in vivo. Nat Med7: 631–634. 11329067
39. Hirokawa N, Noda Y, Tanaka Y, Niwa S, (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol10: 682–696. doi: 10.1038/nrm277419773780
40. Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, et al. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol20: 473–477. 11981560
41. Ke R, Nong RY, Fredriksson S, Landegren U, Nilsson M, (2013) Improving precision of proximity ligation assay by amplified single molecule detection. PLoS One8: e69813. doi: 10.1371/journal.pone.006981323874999
42. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, et al. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods3: 995–1000. 17072308
43. Trifilieff P, Rives ML, Urizar E, Piskorowski RA, Vishwasrao HD, et al. (2011) Detection of antigen interactions ex vivo by proximity ligation assay: endogenous dopamine D2-adenosine A2A receptor complexes in the striatum. Biotechniques51: 111–118. doi: 10.2144/00011371921806555
44. Zatloukal B, Kufferath I, Thueringer A, Landegren U, Zatloukal K, et al. (2014) Sensitivity and specificity of in situ proximity ligation for protein interaction analysis in a model of steatohepatitis with Mallory-Denk bodies. PLoS One9: e96690. doi: 10.1371/journal.pone.009669024798445
45. Hulme AE, Kelley Z, Foley D, Hope TJ, (2015) Complementary assays reveal a low level of CA associated with nuclear HIV-1 viral complexes. J Virol.
46. Joseph J, Dasso M, (2008) The nucleoporin Nup358 associates with and regulates interphase microtubules. FEBS Lett582: 190–196. 18070602
47. Arhel N, Genovesio A, Kim KA, Miko S, Perret E, et al. (2006) Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat Methods3: 817–824. 16990814
48. Chin CR, Perreira JM, Savidis G, Portmann JM, Aker AM, et al. (2015) Direct Visualization of HIV-1 Replication Intermediates Shows that Capsid and CPSF6 Modulate HIV-1 Intra-nuclear Invasion and Integration. Cell Rep13: 1717–1731. doi: 10.1016/j.celrep.2015.10.03626586435
49. Peng K, Muranyi W, Glass B, Laketa V, Yant SR, et al. (2014) Quantitative microscopy of functional HIV post-entry complexes reveals association of replication with the viral capsid. Elife3: e04114. doi: 10.7554/eLife.0411425517934
50. Lee K, Mulky A, Yuen W, Martin TD, Meyerson NR, et al. (2012) HIV-1 capsid-targeting domain of cleavage and polyadenylation specificity factor 6. J Virol86: 3851–3860. doi: 10.1128/JVI.06607-1122301135
51. Sowd GA, Serrao E, Wang H, Wang W, Fadel HJ, et al. (2016) A critical role for alternative polyadenylation factor CPSF6 in targeting HIV-1 integration to transcriptionally active chromatin. Proc Natl Acad Sci U S A113: E1054–1063. doi: 10.1073/pnas.152421311326858452
52. Strunze S, Engelke MF, Wang IH, Puntener D, Boucke K, et al. (2011) Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe10: 210–223. doi: 10.1016/j.chom.2011.08.01021925109