CPSF6 Defines a Conserved Capsid Interface that Modulates HIV-1 Replication

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Price, Amanda J ^a   Fletcher, Adam J ^b   Schaller, Torsten ^b,d   Elliott, Tom ^a   Lee, KyeongEun ^c   KewalRamani, Vineet N ^c   Chin, Jason W ^a   Towers, Greg J ^b   James, Leo C ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NATIONAL CANCER INSTITUTE   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR 6; CYCLOPHILIN A; KARYOPHERIN; NUCLEOPORIN; PROTEIN RANBP 2; PROTEIN TNPO 3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRINAE; MUTATION; NONHUMAN; PROTEIN BINDING; RNA PROCESSING; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; BETA KARYOPHERINS; CAPSID PROTEINS; CELL LINE, TUMOR; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HIV INFECTIONS; HIV-1; HUMANS; INDOLES; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTATION; NUCLEAR PORE COMPLEX PROTEINS; PHENYLALANINE; PROTEIN BINDING; SEQUENCE ALIGNMENT; VIRUS INTERNALIZATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 84866162552     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002896     Document Type: Article

References (43)

1. Fassati A, Goff SP, (2001) Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J Virol 75: 3626-3635.
2. Miller MD, Farnet CM, Bushman FD, (1997) Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J Virol 71: 5382-5390.
3. 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: 9975-80.
4. Arhel NJ, Souquere-Besse S, Munier S, Souque P, Guadagnini S, et al. (2007) HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J 26: 3025-3037.
5. Arhel N, (2010) Revisiting HIV-1 uncoating. Retrovirology 7: 96.
6. 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 Pathog 7: e1002439.
7. Arfi V, Lienard J, Nguyen XN, Berger G, Rigal D, et al. (2009) Characterization of the behavior of functional viral genomes during the early steps of human immunodeficiency virus type 1 infection. J Virol 83: 7524-7535.
8. Charneau P, Mirambeau G, Roux P, Paulous S, Buc H, et al. (1994) HIV-1 reverse transcription. A termination step at the center of the genome. J Mol Biol 241: 651-662.
9. Bukrinsky MI, Sharova N, Dempsey MP, Stanwick TL, Bukrinskaya AG, et al. (1992) Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc Natl Acad Sci U S A 89: 6580-6584.
10. Qi M, Yang R, Aiken C, (2008) Cyclophilin A-dependent restriction of human immunodeficiency virus type 1 capsid mutants for infection of nondividing cells. J Virol 82: 12001-12008.
11. Yamashita M, Perez O, Hope TJ, Emerman M, (2007) Evidence for direct involvement of the capsid protein in HIV infection of nondividing cells. PLoS Pathog 3: 1502-1510.
12. Ylinen LM, Schaller T, Price A, Fletcher AJ, Noursadeghi M, et al. (2009) Cyclophilin A levels dictate infection efficiency of human immunodeficiency virus type 1 capsid escape mutants A92E and G94D. J Virol 83: 2044-2047.
13. Dismuke DJ, Aiken C, (2006) 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 80: 3712-3720.
14. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI, (2003) Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 77: 5439-5450.
15. Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, et al. (2009) X-ray structures of the hexameric building block of the HIV capsid. Cell 137: 1282-1292.
16. 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. Science 319: 921-926.
17. Christ F, Thys W, De Rijck J, Gijsbers R, Albanese A, et al. (2008) Transportin-SR2 imports HIV into the nucleus. Curr Biol 18: 1192-1202.
18. 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. Cell 135: 49-60.
19. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, et al. (2010) Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7: 221-233.
20. Ocwieja KE, Brady TL, Ronen K, Huegel A, Roth SL, et al. (2011) HIV Integration Targeting: A Pathway Involving Transportin-3 and the Nuclear Pore Protein RanBP2. PLoS Pathog 7: e1001313.
21. Cribier A, Segeral E, Delelis O, Parissi V, Simon A, et al. (2011) Mutations affecting interaction of integrase with TNPO3 do not prevent HIV-1 cDNA nuclear import. Retrovirology 8: 104.
22. 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. Retrovirology 8: 98.
23. Krishnan L, Matreyek KA, Oztop I, Lee K, Tipper CH, et al. (2010) The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase. J Virol 84: 397-406.
24. Logue EC, Taylor KT, Goff PH, Landau NR, (2011) The cargo-binding domain of transportin 3 is required for lentivirus nuclear import. J Virol 85: 12950-12961.
25. Zhou L, Sokolskaja E, Jolly C, James W, Cowley SA, et al. (2011) Transportin 3 Promotes a Nuclear Maturation Step Required for Efficient HIV-1 Integration. PLoS Pathog 7: e1002194.
26. Ruepp MD, Aringhieri C, Vivarelli S, Cardinale S, Paro S, et al. (2009) Mammalian pre-mRNA 3′ end processing factor CF I m 68 functions in mRNA export. Mol Biol Cell 20: 5211-5223.
27. Ruegsegger U, Blank D, Keller W, (1998) Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. Mol Cell 1: 243-253.
28. Dettwiler S, Aringhieri C, Cardinale S, Keller W, Barabino SM, (2004) Distinct sequence motifs within the 68-kDa subunit of cleavage factor Im mediate RNA binding, protein-protein interactions, and subcellular localization. J Biol Chem 279: 35788-35797.
29. Kataoka N, Bachorik JL, Dreyfuss G, (1999) Transportin-SR, a nuclear import receptor for SR proteins. J Cell Biol 145: 1145-1152.
30. Lai MC, Lin RI, Huang SY, Tsai CW, Tarn WY, (2000) A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J Biol Chem 275: 7950-7957.
31. 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 Virol 86: 3851-60.
32. Hatziioannou T, Cowan S, Von Schwedler UK, Sundquist WI, Bieniasz PD, (2004) Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J Virol 78: 6005-6012.
33. Shi J, Aiken C, (2006) Saturation of TRIM5 alpha-mediated restriction of HIV-1 infection depends on the stability of the incoming viral capsid. Virology 350: 493-500.
34. Yang R, Shi J, Byeon IJ, Ahn J, Sheehan JH, et al. (2012) Second-site suppressors of HIV-1 capsid mutations: restoration of intracellular activities without correction of intrinsic capsid stability defects. Retrovirology 9: 30.
35. Bogan AA, Thorn KS, (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280: 1-9.
36. Ternois F, Sticht J, Duquerroy S, Krausslich HG, Rey FA, (2005) The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat Struct Mol Biol 12: 678-682.
37. Kelly BN, Kyere S, Kinde I, Tang C, Howard BR, et al. (2007) Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J Mol Biol 373: 355-366.
38. Blair WS, Pickford C, Irving SL, Brown DG, Anderson M, et al. (2010) HIV capsid is a tractable target for small molecule therapeutic intervention. PLoS Pathog 6: e1001220.
39. Yang Q, Coseno M, Gilmartin GM, Doublie S, (2011) Crystal structure of a human cleavage factor CFI(m)25/CFI(m)68/RNA complex provides an insight into poly(A) site recognition and RNA looping. Structure 19: 368-377.
40. Collaborative Computational Project N (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
41. Besnier C, Takeuchi Y, Towers G, (2002) Restriction of lentivirus in monkeys. Proc Natl Acad Sci U S A 99: 11920-11925.
42. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-533.
43. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33: W299-302.