A homology model of HIV-1 integrase and analysis of mutations designed to test the model

Journal of Molecular Biology

Volumn 425, Issue 12, 2013, Pages 2133-2146

  Johnson, Barry C ^a   Métifiot, Mathieu ^b   Ferris, Andrea ^a   Pommier, Yves ^b   Hughes, Stephen H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

dimerization; HIV; infectivity; integration; modeling

Indexed keywords

CYSTEINE; HELIX LOOP HELIX PROTEIN; INTEGRASE; VIRUS ENZYME;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DELETION MUTANT; DIMERIZATION; DNA BINDING; DNA CROSS LINKING; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; REVERSE TRANSCRIPTION; SEQUENCE ALIGNMENT; SIMIAN IMMUNODEFICIENCY VIRUS; SPUMA VIRUS; VIRION; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS MUTANT; VIRUS REPLICATION; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN SPUMARETROVIRUS;

EID: 84878252974     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.03.027     Document Type: Article

References (51)

1. H. Chen, and A. Engelman Asymmetric processing of human immunodeficiency virus type 1 cDNA in vivo: implications for functional end coupling during the chemical steps of DNA transposition Mol. Cell. Biol. 21 2001 6758 6767
2. S.Q. Wei, K. Mizuuchi, and R. Craigie A large nucleoprotein assembly at the ends of the viral DNA mediates retroviral DNA integration EMBO J. 16 1997 7511 7520
3. C. Vink, E. Yeheskiely, G.A. van der Marel, J.H. van Boom, and R.H. Plasterk Site-specific hydrolysis and alcoholysis of human immunodeficiency virus DNA termini mediated by the viral integrase protein Nucleic Acids Res. 19 1991 6691 6698
4. P.A. Sherman, and J.A. Fyfe Human immunodeficiency virus integration protein expressed in Escherichia coli possesses selective DNA cleaving activity Proc. Natl Acad. Sci. USA 87 1990 5119 5123
5. E. Guiot, K. Carayon, O. Delelis, F. Simon, P. Tauc, and E. Zubin Relationship between the oligomeric status of HIV-1 integrase on DNA and enzymatic activity J. Biol. Chem. 281 2006 22707 22719
6. F.D. Bushman, T. Fujiwara, and R. Craigie Retroviral DNA integration directed by HIV integration protein in vitro Science 249 1990 1555 1558
7. F.D. Bushman, and R. Craigie Activities of human immunodeficiency virus (HIV) integration protein in vitro: specific cleavage and integration of HIV DNA Proc. Natl. Acad. Sci. USA 88 1991 1339 1343
8. H.P. Muller, and H.E. Varmus DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes EMBO J. 13 1994 4704 4714
9. D. Pruss, R. Reeves, F.D. Bushman, and A.P. Wolffe The influence of DNA and nucleosome structure on integration events directed by HIV integrase J. Biol. Chem. 269 1994 25031 25041
10. M.A. Muesing, D.H. Smith, C.D. Cabradilla, C.V. Benton, L.A. Lasky, and D.J. Capon Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus Nature 313 1985 450 458
11. E. Brin, J. Yi, A.M. Skalka, and J. Leis Modeling the late steps in HIV-1 retroviral integrase-catalyzed DNA integration J. Biol. Chem. 275 2000 39287 39295
12. R. Zheng, T.M. Jenkins, and R. Craigie Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity Proc. Natl Acad. Sci. USA 93 1996 13659 13664
13. Y. Goldgur, F. Dyda, A.B. Hickman, T.M. Jenkins, R. Craigie, and D.R. Davies Three new structures of the core domain of HIV-1 integrase: an active site that binds magnesium Proc. Natl Acad. Sci. USA 95 1998 9150 9154
14. S. Maignan, J.P. Guilloteau, Q. Zhou-Liu, C. Clement-Mella, and V. Mikol 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 J. Mol. Biol. 282 1998 359 368
15. A.M. Woerner, M. Klutch, J.G. Levin, and C.J. Marcus-Sekura Localization of DNA binding activity of HIV-1 integrase to the C-terminal half of the protein AIDS Res. Hum. Retroviruses 8 1992 297 304
16. M. Cai, R. Zheng, M. Caffrey, R. Craigie, G.M. Clore, and A.M. Gronenborn Solution structure of the N-terminal zinc binding domain of HIV-1 integrase Nat. Struct. Biol. 4 1997 567 577
17. J.C. Chen, J. Krucinski, L.J. Miercke, J.S. Finer-Moore, A.H. Tang, A.D. Leavitt, and R.M. Stroud Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding Proc. Natl Acad. Sci. USA 97 2000 8233 8238
18. P.J. Lodi, J.A. Ernst, J. Kuszewski, A.B. Hickman, A. Engelman, and R. Craigie Solution structure of the DNA binding domain of HIV-1 integrase Biochemistry 34 1995 9826 9833
19. J.Y. Wang, H. Ling, W. Yang, and R. Craigie Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein EMBO J. 20 2001 7333 7343
20. A.P. Eijkelenboom, R. Sprangers, K. Hard, R.A. Puras Lutzke, R.H. Plasterk, R. Boelens, and R. Kaptein Refined solution structure of the C-terminal DNA-binding domain of human immunovirus-1 integrase Proteins 36 1999 556 564
21. S. Hare, S.S. Gupta, E. Valkov, A. Engelman, and P. Cherepanov Retroviral intasome assembly and inhibition of DNA strand transfer Nature 464 2010 232 236
22. S. Hare, S.J. Smith, M. Metifiot, A. Jaxa-Chamiec, Y. Pommier, S.H. Hughes, and P. Cherepanov Structural and functional analyses of the second-generation integrase strand transfer inhibitor dolutegravir (S/GSK1349572) Mol. Pharmacol. 80 2011 565 572
23. S. Hare, A.M. Vos, R.F. Clayton, J.W. Thuring, M.D. Cummings, and P. Cherepanov Molecular mechanisms of retroviral integrase inhibition and the evolution of viral resistance Proc. Natl Acad. Sci. USA 107 2010 20057 20062
24. G.N. Maertens, S. Hare, and P. Cherepanov The mechanism of retroviral integration from X-ray structures of its key intermediates Nature 468 2010 326 329
25. A. Faure, C. Calmels, C. Desjobert, M. Castroviejo, A. Caumont-Sarcos, and L. Tarrago-Litvak HIV-1 integrase crosslinked oligomers are active in vitro Nucleic Acids Res. 33 2005 977 986
26. B.C. Johnson, M. Metifiot, Y. Pommier, and S.H. Hughes Molecular dynamics approaches estimate the binding energy of HIV-1 integrase inhibitors and correlate with in vitro activity Antimicrob. Agents Chemother. 56 2012 411 419
27. L. Krishnan, X. Li, H.L. Naraharisetty, S. Hare, P. Cherepanov, and A. Engelman Structure-based modeling of the functional HIV-1 intasome and its inhibition Proc. Natl Acad. Sci. USA 107 2010 15910 15915
28. O. Goethals, M. Van Ginderen, A. Vos, M.D. Cummings, K. Van Der Borght, and L. Van Wesenbeeck Resistance to raltegravir highlights integrase mutations at codon 148 in conferring cross-resistance to a second-generation HIV-1 integrase inhibitor Antiviral Res. 91 2011 167 176
29. Z. Chen, Y. Yan, S. Munshi, Y. Li, J. Zugay-Murphy, and B. Xu X-ray structure of simian immunodeficiency virus integrase containing the core and C-terminal domain (residues 50-293) - an initial glance of the viral DNA binding platform J. Mol. Biol. 296 2000 521 533
30. Z.N. Yang, T.C. Mueser, F.D. Bushman, and C.C. Hyde Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase J. Mol. Biol. 296 2000 535 548
31. K.V. Kishan, and V. Agrawal SH3-like fold proteins are structurally conserved and functionally divergent Curr. Protein Pept. Sci. 6 2005 143 150
32. R.A. Lutzke, C. Vink, and R.H. Plasterk Characterization of the minimal DNA-binding domain of the HIV integrase protein Nucleic Acids Res. 22 1994 4125 4131
33. Y. Kim, J. Sidney, C. Pinilla, A. Sette, and B. Peters Derivation of an amino acid similarity matrix for peptide: MHC binding and its application as a Bayesian prior BMC Bioinformatics 10 2009 394
34. E. Serrao, W. Thys, J. Demeulemeester, L.Q. Al-Mawsawi, F. Christ, Z. Debyser, and N. Neamati A symmetric region of the HIV-1 integrase dimerization interface is essential for viral replication PLoS One 7 2012 e45177
35. P. Cherepanov, A.L. Ambrosio, S. Rahman, T. Ellenberger, and A. Engelman Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75 Proc. Natl Acad. Sci. USA 102 2005 17308 17313
36. M.J. Dar, B. Monel, L. Krishnan, M.C. Shun, F. Di Nunzio, D.E. Helland, and A. Engelman Biochemical and virological analysis of the 18-residue C-terminal tail of HIV-1 integrase Retrovirology 6 2009 94
37. T.S. Heuer, and P.O. Brown Mapping features of HIV-1 integrase near selected sites on viral and target DNA molecules in an active enzyme-DNA complex by photo-cross-linking Biochemistry 36 1997 10655 10665
38. D. Esposito, and R. Craigie Sequence specificity of viral end DNA binding by HIV-1 integrase reveals critical regions for protein-DNA interaction EMBO J. 17 1998 5832 5843
39. A. Chen, I.T. Weber, R.W. Harrison, and J. Leis Identification of amino acids in HIV-1 and avian sarcoma virus integrase subsites required for specific recognition of the long terminal repeat ends J. Biol. Chem. 281 2006 4173 4182
40. Z. Zhao, C.J. McKee, J.J. Kessl, W.L. Santos, J.E. Daigle, and A. Engelman Subunit-specific protein footprinting reveals significant structural rearrangements and a role for N-terminal Lys-14 of HIV-1 integrase during viral DNA binding J. Biol. Chem. 283 2008 5632 5641
41. Z. Hobaika, L. Zargarian, Y. Boulard, R.G. Maroun, O. Mauffret, and S. Fermandjian Specificity of LTR DNA recognition by a peptide mimicking the HIV-1 integrase {alpha}4 helix Nucleic Acids Res. 37 2009 7691 7700
42. F. Michel, C. Crucifix, F. Granger, S. Eiler, J.F. Mouscadet, and S. Korolev Structural basis for HIV-1 DNA integration in the human genome, role of the LEDGF/P75 cofactor EMBO J. 28 2009 980 991
43. A.A. Johnson, W. Santos, G.C. Pais, C. Marchand, R. Amin, and T.R. Burke Jr. Integration requires a specific interaction of the donor DNA terminal 5′-cytosine with glutamine 148 of the HIV-1 integrase flexible loop J. Biol. Chem. 281 2006 461 467
44. R. Lu, H.Z. Ghory, and A. Engelman Genetic analyses of conserved residues in the carboxyl-terminal domain of human immunodeficiency virus type 1 integrase J. Virol. 79 2005 10356 10368
45. C.W. Dobard, M.S. Briones, and S.A. Chow Molecular mechanisms by which human immunodeficiency virus type 1 integrase stimulates the early steps of reverse transcription J. Virol. 81 2007 10037 10046
46. K.D. Mohammed, M.B. Topper, and M.A. Muesing Sequential deletion of the integrase (Gag-Pol) carboxyl terminus reveals distinct phenotypic classes of defective HIV-1 J. Virol. 85 2011 4654 4666
47. A. Engelman, G. Englund, J.M. Orenstein, M.A. Martin, and R. Craigie Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication J. Virol. 69 1995 2729 2736
48. M. Metifiot, K. Maddali, A. Naumova, X. Zhang, C. Marchand, and Y. Pommier Biochemical and pharmacological analyses of HIV-1 integrase flexible loop mutants resistant to raltegravir Biochemistry 49 2010 3715 3722
49. A. Engelman In vivo analysis of retroviral integrase structure and function Adv. Virus Res. 52 1999 411 426
50. J.G. Julias, A.L. Ferris, P.L. Boyer, and S.H. Hughes Replication of phenotypically mixed human immunodeficiency virus type 1 virions containing catalytically active and catalytically inactive reverse transcriptase J. Virol. 75 2001 6537 6546
51. X.Z. Zhao, E.A. Semenova, B.C. Vu, K. Maddali, C. Marchand, and S.H. Hughes 2,3-Dihydro-6,7-dihydroxy-1H-isoindol-1-one-based HIV-1 integrase inhibitors J. Med. Chem. 51 2008 251 259