Structural and Functional Role of INI1 and LEDGF in the HIV-1 Preintegration Complex

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Maillot, Benoit ^a,f   Lévy, Nicolas ^a   Eiler, Sylvia ^a   Crucifix, Corinne ^a   Granger, Florence ^a   Richert, Ludovic ^b   Didier, Pascal ^b   Godet, Julien ^b   Pradeau Aubreton, Karine ^a   Emiliani, Stéphane ^c   Nazabal, Alexis ^d   Lesbats, Paul ^e,g   Parissi, Vincent ^e   Mely, Yves ^b   Moras, Dino ^a   Schultz, Patrick ^a   Ruff, Marc ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b Faculté de Pharmacie   (France)

^c INSTITUT COCHIN   (France)

^d Medical   (Switzerland)

^e University Victor Segalen   (France)

^f EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^g IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL DNA; INTEGRASE; INTEGRASE INTERACTOR PROTEIN 1; LENS EPITHELIUM DERIVED GROWTH FACTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANISOTROPY; ARTICLE; BINDING AFFINITY; BINDING SITE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DISSOCIATION CONSTANT; DNA BINDING; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STABILITY; FLUORESCENCE CORRELATION SPECTROSCOPY; FUNCTIONAL PROTEOMICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; INTEGRASE 1 BINDING DOMAIN; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PREINTEGRATION COMPLEX; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN PURIFICATION; STOICHIOMETRY; STRUCTURAL PROTEOMICS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; VIRUS DNA CELL DNA INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CHROMOSOMAL PROTEINS, NON-HISTONE; CRYOELECTRON MICROSCOPY; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HIV INTEGRASE; HIV-1; HUMANS; MASS SPECTROMETRY; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; TRANSCRIPTION FACTORS; VIRUS INTEGRATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876146955     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060734     Document Type: Article

References (74)

1. Briones MS, Dobard CW, Chow SA, (2010) Role of human immunodeficiency virus type 1 integrase in uncoating of the viral core. JVirol 84: 5181-5190.
2. Wu X, Liu H, Xiao H, Conway JA, Hehl E, et al. (1999) Human immunodeficiency virus type 1 integrase protein promotes reverse transcription through specific interactions with the nucleoprotein reverse transcription complex. JVirol 73: 2126-2135.
3. Ao Z, Danappa JK, Wang B, Zheng Y, Kung S, et al. (2010) Importin alpha3 interacts with HIV-1 integrase and contributes to HIV-1 nuclear import and replication. J Virol 84: 8650-8663.
4. Hendrix J, Gijsbers R, De RJ, Voet A, Hotta JI, et al. (2011) The transcriptional co-activator LEDGF/p75 displays a dynamic scan-and-lock mechanism for chromatin tethering. Nucleic Acids Res 39: 1310-1325.
5. Chiu TK, Davies DR, (2004) Structure and function of HIV-1 integrase. CurrTopMedChem 4: 965-977.
6. Jenkins TM, Hickman AB, Dyda F, Ghirlando R, Davies DR, et al. (1995) Catalytic domain of human immunodeficiency virus type 1 integrase: identification of a soluble mutant by systematic replacement of hydrophobic residues. ProcNatlAcadSciUSA 92: 6057-6061.
7. Dyda F, Hickman AB, Jenkins TM, Engelman A, Craigie R, et al. (1994) Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266: 1981-1986.
8. Goldgur Y, Dyda F, Hickman AB, Jenkins TM, Craigie R, et al. (1998) Three new structures of the core domain of HIV-1 integrase: an active site that binds magnesium. ProcNatlAcadSciUSA 95: 9150-9154.
9. Greenwald J, Le V, Butler SL, Bushman FD, Choe S, (1999) The mobility of an HIV-1 integrase active site loop is correlated with catalytic activity. Biochemistry 38: 8892-8898.
10. Maignan S, Guilloteau JP, Zhou-Liu Q, Clement-Mella C, Mikol V, (1998) Crystal structures of the catalytic domain of HIV-1 integrase free and complexed with its metal cofactor: high level of similarity of the active site with other viral integrases. JMolBiol 282: 359-368.
11. Chen JC, Krucinski J, Miercke LJ, Finer-Moore JS, Tang AH, et al. (2000) Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding. ProcNatlAcadSciUSA 97: 8233-8238.
12. Wang JY, Ling H, Yang W, Craigie R, (2001) Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J 20: 7333-7343.
13. Cherepanov P, Ambrosio AL, Rahman S, Ellenberger T, Engelman A, (2005) Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75. ProcNatlAcadSciUSA 102: 17308-17313.
14. Li X, Krishnan L, Cherepanov P, Engelman A, (2011) Structural biology of retroviral DNA integration. Virology 411: 194-205.
15. Ballandras A, Moreau K, Robert X, Confort MP, Merceron R, et al. (2011) A crystal structure of the catalytic core domain of an avian sarcoma and leukemia virus integrase suggests an alternate dimeric assembly. PLoS One 6: e23032.
16. Maertens GN, Hare S, Cherepanov P, (2010) The mechanism of retroviral integration from X-ray structures of its key intermediates. Nature 468: 326-329.
17. Michel F, Crucifix C, Granger F, Eiler S, Mouscadet JF, et al. (2009) Structural basis for HIV-1 DNA integration in the human genome, role of the LEDGF/P75 cofactor. EMBO J 28: 980-991.
18. Krishnan L, Li X, Naraharisetty HL, Hare S, Cherepanov P, et al. (2010) Structure-based modeling of the functional HIV-1 intasome and its inhibition. ProcNatlAcadSciUSA 107: 15910-15915.
19. Fitzkee NC, Masse JE, Shen Y, Davies DR, Bax A, (2010) Solution conformation and dynamics of the HIV-1 integrase core domain. JBiolChem 285: 18072-18084.
20. Kessl JJ, Li M, Ignatov M, Shkriabai N, Eidahl JO, et al. (2011) FRET analysis reveals distinct conformations of IN tetramers in the presence of viral DNA or LEDGF/p75. Nucleic Acids Res.
21. Mouscadet JF, Delelis O, Marcelin AG, Tchertanov L, (2010) Resistance to HIV-1 integrase inhibitors: A structural perspective. Drug ResistUpdat 13: 139-150.
22. 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.
23. 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.
24. Rain JC, Cribier A, Gerard A, Emiliani S, Benarous R, (2009) Yeast two-hybrid detection of integrase-host factor interactions. Methods 47: 291-297.
25. 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 HostMicrobe 4: 495-504.
26. Jager S, Cimermancic P, Gulbahce N, Johnson JR, McGovern KE, et al. (2011) Global landscape of HIV-human protein complexes. Nature 481: 365-370.
27. Kalpana GV, Marmon S, Wang W, Crabtree GR, Goff SP, (1994) Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266: 2002-2006.
28. Cherepanov P, Maertens G, Proost P, Devreese B, Van BJ, et al. (2003) HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. JBiolChem 278: 372-381.
29. Maertens G, Cherepanov P, Pluymers W, Busschots K, De CE, et al. (2003) LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. JBiolChem 278: 33528-33539.
30. Emiliani S, Mousnier A, Busschots K, Maroun M, Van MB, et al. (2005) Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. JBiolChem 280: 25517-25523.
31. Morozov A, Yung E, Kalpana GV, (1998) Structure-function analysis of integrase interactor 1/hSNF5L1 reveals differential properties of two repeat motifs present in the highly conserved region. ProcNatlAcadSciUSA 95: 1120-1125.
32. Agbottah E, Deng L, Dannenberg LO, Pumfery A, Kashanchi F, (2006) Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology 3: 48.
33. Ariumi Y, Serhan F, Turelli P, Telenti A, Trono D, (2006) The integrase interactor 1 (INI1) proteins facilitate Tat-mediated human immunodeficiency virus type 1 transcription. Retrovirology 3: 47.
34. Bukrinsky M, (2006) SNFing HIV transcription. Retrovirology 3: 49.
35. Mahmoudi T, Parra M, Vries RG, Kauder SE, Verrijzer CP, et al. (2006) The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. JBiolChem 281: 19960-19968.
36. Treand C, du CI, Bres V, Kiernan R, Benarous R, et al. (2006) Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter. EMBO J 25: 1690-1699.
37. Boese A, Sommer P, Holzer D, Maier R, Nehrbass U, (2009) Integrase interactor 1 (Ini1/hSNF5) is a repressor of basal human immunodeficiency virus type 1 promoter activity. JGenVirol 90: 2503-2512.
38. Yung E, Sorin M, Pal A, Craig E, Morozov A, et al. (2001) Inhibition of HIV-1 virion production by a transdominant mutant of integrase interactor 1. NatMed 7: 920-926.
39. Yung E, Sorin M, Wang EJ, Perumal S, Ott D, et al. (2004) Specificity of interaction of INI1/hSNF5 with retroviral integrases and its functional significance. JVirol 78: 2222-2231.
40. Sorin M, Cano J, Das S, Mathew S, Wu X, et al. (2009) Recruitment of a SAP18-HDAC1 complex into HIV-1 virions and its requirement for viral replication. PLoSPathog 5: e1000463.
41. Lesbats P, Botbol Y, Chevereau G, Vaillant C, Calmels C, et al. (2011) Functional coupling between HIV-1 integrase and the SWI/SNF chromatin remodeling complex for efficient in vitro integration into stable nucleosomes. PLoSPathog 7: e1001280.
42. Sorin M, Yung E, Wu X, Kalpana GV, (2006) HIV-1 replication in cell lines harboring INI1/hSNF5 mutations. Retrovirology 3: 56.
43. Maroun M, Delelis O, Coadou G, Bader T, Segeral E, et al. (2006) Inhibition of early steps of HIV-1 replication by SNF5/Ini1. JBiolChem 281: 22736-22743.
44. Plewniak F, Bianchetti L, Brelivet Y, Carles A, Chalmel F, et al. (2003) PipeAlign: A new toolkit for protein family analysis. Nucleic Acids Res 31: 3829-3832.
45. The_UniProt_Consortium (2010) The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 38: D142-D148.
46. Yanes O, Nazabal A, Wenzel R, Zenobi R, Aviles FX, (2006) Detection of noncovalent complexes in biological samples by intensity fading and high-mass detection MALDI-TOF mass spectrometry. JProteomeRes 5: 2711-2719.
47. Fernandes MX, Ortega A, Lopez Martinez MC, Garcia T, (2002) Calculation of hydrodynamic properties of small nucleic acids from their atomic structure. Nucleic Acids Res 30: 1782-1788.
48. Egele C, Piemont E, Didier P, Ficheux D, Roques B, et al. (2007) The single-finger nucleocapsid protein of moloney murine leukemia virus binds and destabilizes the TAR sequences of HIV-1 but does not promote efficiently their annealing. Biochemistry 46: 14650-14662.
49. Busschots K, Vercammen J, Emiliani S, Benarous R, Engelborghs Y, et al. (2005) The interaction of LEDGF/p75 with integrase is lentivirus-specific and promotes DNA binding. JBiolChem 280: 17841-17847.
50. Guiot E, Carayon K, Delelis O, Simon F, Tauc P, et al. (2006) Relationship between the oligomeric status of HIV-1 integrase on DNA and enzymatic activity. JBiolChem 281: 22707-22719.
51. Van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M, (1996) A new generation of the IMAGIC image processing system. JStructBiol 116: 17-24.
52. Rosenthal PB, Henderson R, (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. JMolBiol 333: 721-745.
53. Desfarges S, Salin B, Calmels C, Andreola ML, Parissi V, et al. (2009) HIV-1 integrase trafficking in S. cerevisiae: a useful model to dissect the microtubule network involvement of viral protein nuclear import. Yeast 26: 39-54.
54. Jayappa KD, Ao Z, Yao X, (2012) The HIV-1 passage from cytoplasm to nucleus: the process involving a complex exchange between the components of HIV-1 and cellular machinery to access nucleus and successful integration. Int J Biochem Mol Biol 3: 70-85.
55. Ao Z, Jayappa KD, Wang B, Zheng Y, Wang X, et al. (2012) Contribution of host nucleoporin 62 in HIV-1 integrase chromatin association and viral DNA integration. J Biol Chem 287: 10544-10555.
56. Turelli P, Doucas V, Craig E, Mangeat B, Klages N, et al. (2001) Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. MolCell 7: 1245-1254.
57. Iordanskiy S, Berro R, Altieri M, Kashanchi F, Bukrinsky M, (2006) Intracytoplasmic maturation of the human immunodeficiency virus type 1 reverse transcription complexes determines their capacity to integrate into chromatin. Retrovirology 3: 4.
58. Azoulay J, Clamme JP, Darlix JL, Roques BP, Mely Y, (2003) Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. JMolBiol 326: 691-700.
59. Clamme JP, Azoulay J, Mely Y, (2003) Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. BiophysJ 84: 1960-1968.
60. Rios CD, Jordan BA, Gomes I, Devi LA, (2001) G-protein-coupled receptor dimerization: modulation of receptor function. PharmacolTher 92: 71-87.
61. Kim SA, Heinze KG, Schwille P, (2007) Fluorescence correlation spectroscopy in living cells. NatMethods 4: 963-973.
62. Lesbats P, Metifiot M, Calmels C, Baranova S, Nevinsky G, et al. (2008) In vitro initial attachment of HIV-1 integrase to viral ends: control of the DNA specific interaction by the oligomerization state. Nucleic Acids Res 36: 7043-7058.
63. Suhre K, Navaza J, Sanejouand YH, (2006) NORMA: a tool for flexible fitting of high-resolution protein structures into low-resolution electron-microscopy-derived density maps. Acta CrystallogrDBiolCrystallogr 62: 1098-1100.
64. Tama F, Miyashita O, Brooks CL III, (2004) Flexible multi-scale fitting of atomic structures into low-resolution electron density maps with elastic network normal mode analysis. JMolBiol 337: 985-999.
65. Navaza J, Lepault J, Rey FA, varez-Rua C, Borge J, (2002) On the fitting of model electron densities into EM reconstructions: a reciprocal-space formulation. Acta CrystallogrDBiolCrystallogr 58: 1820-1825.
66. Winn MD, Isupov MN, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta CrystallogrDBiolCrystallogr 57: 122-133.
67. The_CCP4_suite (1994) Programs for protein crystallography. Acta CrystallogrDBiolCrystallogr 50: 760-763.
68. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta CrystallogrDBiolCrystallogr 60: 2126-2132.
69. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. JComputChem 25: 1605-1612.
70. DeLano WL (2002) The PyMOL Molecular Graphics System (Delano Scientific, Paolo Alto, CA).
71. Hare S, Di NF, Labeja A, Wang J, Engelman A, et al. (2009) Structural basis for functional tetramerization of lentiviral integrase. PLoSPathog 5: e1000515.
72. Hare S, Gupta SS, Valkov E, Engelman A, Cherepanov P, (2010) Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464: 232-236.
73. Hare S, Shun MC, Gupta SS, Valkov E, Engelman A, et al. (2009) A novel co-crystal structure affords the design of gain-of-function lentiviral integrase mutants in the presence of modified PSIP1/LEDGF/p75. PLoSPathog 5: e1000259.
74. Yang ZN, Mueser TC, Bushman FD, Hyde CC, (2000) Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase. JMolBiol 296: 535-548.