Structural biology of retroviral DNA integration

Virology

Volumn 411, Issue 2, 2011, Pages 194-205

  Li, Xiang ^a   Krishnan, Lavanya ^a   Cherepanov, Peter ^b   Engelman, Alan ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

AIDS; HIV 1; Integrase; Integrase strand transfer inhibitor; Integration; Prototype foamy virus; Raltegravir; Structural biology; X ray crystallography

Indexed keywords

INTEGRASE;

AMINO ACID SEQUENCE; AVIAN SARCOMA VIRUS; BOVINE IMMUNODEFICIENCY LIKE VIRUS; CRYSTAL STRUCTURE; CRYSTALLIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; RETROVIRUS; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS DNA CELL DNA INTERACTION; VIRUS MORPHOLOGY; VIRUS MUTATION; VISNA VIRUS; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DNA, VIRAL; HIV-1; HUMANS; INTEGRASES; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINATION, GENETIC; SPUMAVIRUS; VIRUS INTEGRATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN SPUMARETROVIRUS;

EID: 79952070221     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.12.008     Document Type: Review

References (142)

1. Alexander F., Leis J., Soltis D.A., Crowl R.M., Danho W., Poonian M.S., Pan Y.C., Skalka A.M. Proteolytic processing of avian sarcoma and leukosis viruses pol-endo recombinant proteins reveals another pol gene domain. J. Virol. 1987, 61:534-542.
2. Alian A., Griner S.L., Chiang V., Tsiang M., Jones G., Birkus G., Geleziunas R., Leavitt A.D., Stroud R.M. Catalytically-active complex of HIV-1 integrase with a viral DNA substrate binds anti-integrase drugs. Proc. Natl Acad. Sci. USA 2009, 106:8192-8197.
3. Bao K.K., Wang H., Miller J.K., Erie D.A., Skalka A.M., Wong I. Functional oligomeric state of avian sarcoma virus integrase. J. Biol. Chem. 2003, 278:1323-1327.
4. Baumann H., Knapp S., Lundbäck T., Ladenstein R., Härd T. Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus. Nat. Struct. Biol. 1994, 1:808-819.
5. Baus J., Liu L., Heggestad A.D., Sanz S., Fletcher B.S. Hyperactive transposase mutants of the Sleeping Beauty transposon. Mol. Ther. 2005, 12:1148-1156.
6. Bera S., Pandey K.K., Vora A.C., Grandgenett D.P. Molecular interactions between HIV-1 integrase and the two viral DNA ends within the synaptic complex that mediates concerted integration. J. Mol. Biol. 2009, 389:183-198.
7. Berthoux L., Sebastian S., Muesing M.A., Luban J. The role of lysine 186 in HIV-1 integrase multimerization. Virology 2007, 364:227-236.
8. Bujacz G., Jaskolski M., Alexandratos J., Wlodawer A., Merkel G., Katz R.A., Skalka A.M. High-resolution structure of the catalytic domain of avian sarcoma virus integrase. J. Mol. Biol. 1995, 253:333-346.
9. Bujacz G., Alexandratos J., Qing Z.L., Clement-Mella C., Wlodawer A. The catalytic domain of human immunodeficiency virus integrase: ordered active site in the F185H mutant. FEBS Lett. 1996, 398:175-178.
10. Bujacz G., Jaskólski M., Alexandratos J., Wlodawer A., Merkel G., Katz R.A., Skalka A.M. The catalytic domain of avian sarcoma virus integrase: conformation of the active-site residues in the presence of divalent cations. Structure 1996, 4:89-96.
11. Bujacz G., Alexandratos J., Wlodawer A., Merkel G., Andrake M., Katz R.A., Skalka A.M. Binding of different divalent cations to the active site of avian sarcoma virus integrase and their effects on enzymatic activity. J. Biol. Chem. 1997, 272:18161-18168.
12. Burke C.J., Sanyal G., Bruner M.W., Ryan J.A., LaFemina R.L., Robbins H.L., Zeft A.S., Middaugh C.R., Cordingley M.G. Structural implications of spectroscopic characterization of a putative zinc finger peptide from HIV-1 integrase. J. Biol. Chem. 1992, 267:9639-9644.
13. Bushman F.D., Craigie R. Activities of human immunodeficiency virus (HIV) integration protein in vitro: specific cleavage and integration of HIV DNA. Proc. Natl Acad. Sci. USA 1991, 88:1339-1343.
14. Bushman F.D., Fujiwara T., Craigie R. Retroviral DNA integration directed by HIV integration protein in vitro. Science 1990, 249:1555-1558.
15. Bushman F.D., Engelman A., Palmer I., Wingfield P., Craigie R. Domains of the integrase protein of human immunodeficiency virus type 1 responsible for polynucleotidyl transfer and zinc binding. Proc. Natl Acad. Sci. USA 1993, 90:3428-3432.
16. Busschots K., Vercammen J., Emiliani S., Benarous R., Engelborghs Y., Christ F., Debyser Z. The interaction of LEDGF/p75 with integrase is lentivirus-specific and promotes DNA binding. J. Biol. Chem. 2005, 280:17841-17847.
17. Cai M., Zheng R., Caffrey M., Craigie R., Clore G.M., Gronenborn A.M. Solution structure of the N-terminal zinc binding domain of HIV-1 integrase. Nat. Struct. Biol. 1997, 4:567-577.
18. Cai M., Huang Y., Caffrey M., Zheng R., Craigie R., Clore G.M., Gronenborn A.M. Solution structure of the His12 --> Cys mutant of the N-terminal zinc binding domain of HIV-1 integrase complexed to cadmium. Protein Sci. 1998, 7:2669-2674.
19. Carteau S., Hoffmann C., Bushman F. Chromosome structure and human immunodeficiency virus type 1 cDNA integration: centromeric alphoid repeats are a disfavored target. J. Virol. 1998, 72:4005-4014.
20. Carteau S., Gorelick R.J., Bushman F.D. Coupled integration of human immunodeficiency virus type 1 cDNA ends by purified integrase in vitro: stimulation by the viral nucleocapsid protein. J. Virol. 1999, 73:6670-6679.
21. Chaconas G. Studies on a "jumping gene machine": higher-order nucleoprotein complexes in Mu DNA transposition. Biochem. Cell Biol. 1999, 77:487-491.
22. Chen H., Wei S.-Q., Engelman A. Multiple integrase functions are required to form the native structure of the human immunodeficiency virus type I intasome. J. Biol. Chem. 1999, 274:17358-17364.
23. Chen J.C., Krucinski J., Miercke L.J.W., Finer-Moore J.S., Tang A.H., Leavitt A.D., Stroud R.M. Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding. Proc. Natl Acad. Sci. USA 2000, 97:8233-8238.
24. Chen Z., Yan Y., Munshi S., Li Y., Zugay-Murphy J., Xu B., Witmer M., Felock P., Wolfe A., Sardana V. 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. 2000, 296:521-533.
25. Chen A., Weber I.T., Harrison R.W., Leis J. 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. 2006, 281:4173-4182.
26. Chen X., Tsiang M., Yu F., Hung M., Jones G.S., Zeynalzadegan A., Qi X., Jin H., Kim C.U., Swaminathan S., Chen J.M. Modeling, analysis, and validation of a novel HIV integrase structure provide insights into the binding modes of potent integrase inhibitors. J. Mol. Biol. 2008, 380:504-519.
27. Cherepanov P., Maertens G., Proost P., Devreese B., Van Beeumen J., Engelborghs Y., De Clercq E., Debyser Z. HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 2003, 278:372-381.
28. Cherepanov P., Devroe E., Silver P.A., Engelman A. Identification of an evolutionarily-conserved domain in LEDGF/p75 that binds HIV-1 integrase. J. Biol. Chem. 2004, 279:48883-48892.
29. Cherepanov P., Ambrosio A.L., Rahman S., Ellenberger T., Engelman A. Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75. Proc. Natl Acad. Sci. USA 2005, 102:17308-17313.
30. Cherepanov P., Sun Z.-Y.J., Rahman S., Maertens G., Wagner G., Engelman A. Solution structure of the HIV-1 integrase-binding domain in LEDGF/p75. Nat. Struct. Mol. Biol. 2005, 12:526-532.
31. Chiu T.K., Davies D.R. Structure and function of HIV-1 integrase. Curr. Top. Med. Chem. 2004, 4:965-977.
32. Chow S.A., Vincent K.A., Ellison V., Brown P.O. Reversal of integration and DNA splicing mediated by integrase of human immunodeficiency virus. Science 1992, 255:723-726.
33. Christ F., Voet A., Marchand A., Nicolet S., Desimmie B.A., Marchand D., Bardiot D., Van der Veken N.J., Van Remoortel B., Strelkov S.V., De Maeyer M., Chaltin P., Debyser Z. Rational design of small-molecule inhibitors of the LEDGF/p75-integrase interaction and HIV replication. Nat. Chem. Biol. 2010, 6:442-448.
34. Cooper D.A., Steigbigel R.T., Gatell J.M., Rockstroh J.K., Katlama C., Yeni P., Lazzarin A., Clotet B., Kumar P.N., Eron J.E., Schechter M., Markowitz M., Loutfy M.R., Lennox J.L., Zhao J., Chen J., Ryan D.M., Rhodes R.R., Killar J.A., Gilde L.R., Strohmaier K.M., Meibohm A.R., Miller M.D., Hazuda D.J., Nessly M.L., DiNubile M.J., Isaacs R.D., Teppler H., Nguyen B.-Y., the BENCHMRK Study Teams Subgroup and resistance analyses of raltegravir for resistant HIV-1 infection. N. Engl. J. Med. 2008, 359:355-365.
35. Craigie R., Fujiwara T., Bushman F. The IN protein of Moloney murine leukemia virus processes the viral DNA ends and accomplishes their integration in vitro. Cell 1990, 62:829-837.
36. Dar M.J., Monel B., Krishnan L., Shun M.C., Di Nunzio F., Helland D.E., Engelman A. Biochemical and virological analysis of the 18-residue C-terminal tail of HIV-1 integrase. Retrovirology 2009, 6:94.
37. Davies D.R., Goryshin I.Y., Reznikoff W.S., Rayment I. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 2000, 289:77-85.
38. Delelis O., Carayon K., Guiot E., Leh H., Tauc P., Brochon J.C., Mouscadet J.F., Deprez E. Insight into the integrase-DNA recognition mechanism. A specific DNA-binding mode revealed by an enzymatically labeled integrase. J. Biol. Chem. 2008, 283:27838-27849.
39. Delelis O., Malet I., Na L., Tchertanov L., Calvez V., Marcelin A.-G., Subra F., Deprez E., Mouscadet J.-F. The G140S mutation in HIV integrases from raltegravir-resistant patients rescues catalytic defect due to the resistance Q148H mutation. Nucleic Acids Res. 2009, 37:1193-1201.
40. Dicker I.B., Samanta H.K., Li Z., Hong Y., Tian Y., Banville J., Remillard R.R., Walker M.A., Langley D.R., Krystal M. Changes to the HIV long terminal repeat and to HIV integrase differentially impact HIV integrase assembly, activity, and the binding of strand transfer inhibitors. J. Biol. Chem. 2007, 282:31186-31196.
41. Drelich M., Wilhelm R., Mous J. Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. Virology 1992, 188:459-468.
42. Dyda F., Hickman A.B., Jenkins T.M., Engelman A., Craigie R., Davies D.R. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 1994, 266:1981-1986.
43. Eijkelenboom A.P., Puras Lutzke R.A., Boelens R., Plasterk R.H., Kaptein R., Hård K. The DNA-binding domain of HIV-1 integrase has an SH3-like fold. Nat. Struct. Biol. 1995, 2:807-810.
44. Eijkelenboom A.P., van den Ent F.M., Vos A., Doreleijers J.F., Hard K., Tullius T.D., Plasterk R.H., Kaptein R., Boelens R. The solution structure of the amino-terminal HHCC domain of HIV-2 integrase: a three-helix bundle stabilized by zinc. Curr. Biol. 1997, 7:739-746.
45. Eijkelenboom A.P., Sprangers R., Hård K., Puras Lutzke R.A., Plasterk R.H., Boelens R., Kaptein R. Refined solution structure of the C-terminal DNA-binding domain of human immunovirus-1 integrase. Proteins 1999, 36:556-564.
46. Eijkelenboom A.P., van den Ent F.M., Wechselberger R., Plasterk R.H., Kaptein R., Boelens R. Refined solution structure of the dimeric N-terminal HHCC domain of HIV-2 integrase. J. Biomol. NMR 2000, 18:119-128.
47. Ellison V., Gerton J., Vincent K.A., Brown P.O. An essential interaction between distinct domains of HIV-1 integrase mediates assembly of the active multimer. J. Biol. Chem. 1995, 270:3320-3326.
48. Engelman A. Reverse transcription and integration. Retroviruses: Molecular Biology, Genomics and Pathogenesis 2010, 129-159. Caister Academic Press, Norfolk, UK. R. Kurth, N. Bannert (Eds.).
49. Engelman A., Cherepanov P. The lentiviral integrase binding protein LEDGF/p75 and HIV-1 replication. PLoS Pathog. 2008, 4:e1000046.
50. Engelman A., Craigie R. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 1992, 66:6361-6369.
51. Engelman A., Bushman F.D., Craigie R. Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J. 1993, 12:3269-3275.
52. Engelman A., Hickman A.B., Craigie R. The core and carboxyl-terminal domains of the integrase protein of human immunodeficiency virus type 1 each contribute to nonspecific DNA binding. J. Virol. 1994, 68:5911-5917.
53. Engelman A., Liu Y., Chen H., Farzan M., Dyda F. Structure-based mutagenesis of the catalytic domain of human immunodeficiency virus type 1 integrase. J. Virol. 1997, 71:3507-3514.
54. Espeseth A.S., Felock P., Wolfe A., Witmer M., Grobler J., Anthony N., Egbertson M., Melamed J.Y., Young S., Hamill T., Cole J.L., Hazuda D.J. HIV-1 integrase inhibitors that compete with the target DNA substrate define a unique strand transfer conformation for integrase. Proc. Natl Acad. Sci. USA 2000, 97:11244-11249.
55. Faure A., Calmels C., Desjobert C., Castroviejo M., Caumont-Sarcos A., Tarrago-Litvak L., Litvak S., Parissi V. HIV-1 integrase crosslinked oligomers are active in vitro. Nucleic Acids Res. 2005, 33:977-986.
56. Gao K., Butler S.L., Bushman F. Human immunodeficiency virus type 1 integrase: arrangement of protein domains in active cDNA complexes. EMBO J. 2001, 20:3565-3576.
57. Goldgur Y., Dyda F., Hickman A.B., Jenkins T.M., Craigie R., Davies D.R. Three new structures of the core domain of HIV-1 integrase: an active site that binds magnesium. Proc. Natl Acad. Sci. USA 1998, 95:9150-9154.
58. Goldgur Y., Craigie R., Cohen G.H., Fujiwara T., Yoshinaga T., Fujishita T., Sugimoto H., Endo T., Murai H., Davies D.R. Structure of the HIV-1 integrase catalytic domain complexed with an inhibitor: a platform for antiviral drug design. Proc. Natl Acad. Sci. USA 1999, 96:13040-13043.
59. Goodarzi G., Im G.J., Brackmann K., Grandgenett D. Concerted integration of retrovirus-like DNA by human immunodeficiency virus type 1 integrase. J. Virol. 1995, 69:6090-6097.
60. Greenwald J., Le V., Butler S.L., Bushman F.D., Choe S. The mobility of an HIV-1 integrase active site loop is correlated with catalytic activity. Biochemistry 1999, 38:8892-8898.
61. Grobler J.A., Stillmock K., Hu B., Witmer M., Felock P., Espeseth A.S., Wolfe A., Egbertson M., Bourgeois M., Melamed J., Wai J.S., Young S., Vacca J., Hazuda D.J. Diketo acid inhibitor mechanism and HIV-1 integrase: implications for metal binding in the active site of phosphotransferase enzymes. Proc. Natl Acad. Sci. USA 2002, 99:6661-6666.
62. Gupta K., Diamond T., Hwang Y., Bushman F., Van Duyne G.D. Structural properties of HIV integrase. Lens epithelium-derived growth factor oligomers. J. Biol. Chem. 2010, 285:20303-20315.
63. Hare S., Di Nunzio F., Labeja A., Wang J., Engelman A., Cherepanov P. Structural basis for functional tetramerization of lentiviral integrase. PLoS Pathog. 2009, 5:e1000515.
64. Hare S., Shun M.C., Gupta S.S., Valkov E., Engelman A., Cherepanov P. A novel co-crystal structure affords the design of gain-of-function lentiviral integrase mutants in the presence of modified PSIP1/LEDGF/p75. PLoS Pathog. 2009, 5:e1000259.
65. Hare S., Gupta S.S., Valkov E., Engelman A., Cherepanov P. Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 2010, 464:232-236.
66. Hare S., Vos A.M., Clayton R.F., Thuring J.W., Cummings M.D., Cherepanov P. Molecular mechanisms of retroviral integrase inhibition and the evolution of viral resistance. Proc. Natl Acad. Sci. USA 2010, 107:20057-20062.
67. Harper A.L., Skinner L.M., Sudol M., Katzman M. Use of patient-derived human immunodeficiency virus type 1 integrases to identify a protein residue that affects target site selection. J. Virol. 2001, 75:7756-7762.
68. Hickman A.B., Palmer I., Engelman A., Craigie R., Wingfield P. Biophysical and enzymatic properties of the catalytic domain of HIV-1 integrase. J. Biol. Chem. 1994, 269:29279-29287.
69. Hindmarsh P., Ridky T., Reeves R., Andrake M., Skalka A.M., Leis J. HMG protein family members stimulate human immunodeficiency virus type 1 and avian sarcoma virus concerted DNA integration in vitro. J. Virol. 1999, 73:2994-3003.
70. Holman A.G., Coffin J.M. Symmetrical base preferences surrounding HIV-1, avian sarcoma/leukosis virus, and murine leukemia virus integration sites. Proc. Natl Acad. Sci. USA 2005, 102:6103-6107.
71. Jacobo-Molina A., Ding J., Nanni R.G., Clark A.D., Lu X., Tantillo C., Williams R.L., Kamer G., Ferris A.L., Clark P. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc. Natl Acad. Sci. USA 1993, 90:6320-6324.
72. Jaskolski M., Alexandratos J.N., Bujacz G., Wlodawer A. Piecing together the structure of retroviral integrase, an important target in AIDS therapy. FEBS J. 2009, 276:2926-2946.
73. Jenkins T.M., Hickman A.B., Dyda F., Ghirlando R., Davies D.R., Craigie R. Catalytic domain of human immunodeficiency virus type 1 integrase: identification of a soluble mutant by systematic replacement of hydrophobic residues. Proc. Natl Acad. Sci. USA 1995, 92:6057-6061.
74. Jenkins T.M., Engelman A., Ghirlando R., Craigie R. A soluble active mutant of HIV-1 integrase: involvement of both the core and the C-terminal domains in multimerization. J. Biol. Chem. 1996, 271:7712-7718.
75. Johnson M.S., McClure M.A., Feng D.F., Gray J., Doolittle R.F. Computer analysis of retroviral pol genes: Assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc. Natl Acad. Sci. USA 1986, 83:7648-7652.
76. Jonsson C., Donzella G., Gaucan E., Smith C., Roth M. Functional domains of Moloney murine leukemia virus integrase defined by mutation and complementation analysis. J. Virol. 1996, 70:4585-4597.
77. Kaneko T., Li L., Li S.S. The SH3 domain - a family of versatile peptide- and protein-recognition module. Front. Biosci. 2008, 13:4938-4952.
78. Katz R.A., Merkel G., Kulkosky J., Leis J., Skalka A.M. The avian retroviral IN protein is both necessary and sufficient for integrative recombination in vitro. Cell 1990, 63:87-95.
79. Katz R.A., Gravuer K., Skalka A.M. A preferred target DNA structure for retroviral integrase in vitro. J. Biol. Chem. 1998, 273:24190-24195.
80. Katzman M., Katz R.A., Skalka A.M., Leis J. The avian retroviral integration protein cleaves the terminal sequences of linear viral DNA at the in vivo sites of integration. J. Virol. 1989, 63:5319-5327.
81. Kohlstaedt L.A., Wang J., Friedman J.M., Rice P.A., Steitz T.A. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 1992, 256:1783-1790.
82. Kotova S., Li M., Dimitriadis E.K., Craigie R. Nucleoprotein intermediates in HIV-1 DNA integration visualized by atomic force microscopy. J. Mol. Biol. 2010, 399:491-500.
83. Krishnan L., Li X., Naraharisetty H.L., Hare S., Cherepanov P., Engelman A. Structure-based modeling of the functional HIV-1 intasome and its inhibition. Proc. Natl Acad. Sci. USA 2010, 107:15010-15915.
84. Kuduvalli P.N., Rao J.E., Craig N.L. Target DNA structure plays a critical role in Tn7 transposition. EMBO J. 2001, 20:924-932.
85. Kulkosky J., Jones K.S., Katz R.A., Mack J.P., Skalka A.M. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol. 1992, 12:2331-2338.
86. Kulkosky J., Katz R.A., Merkel G., Skalka A.M. Activities and substrate specificity of the evolutionarily conserved central domain of retroviral integrase. Virology 1995, 206:448-456.
87. Langley D.R., Samanta H.K., Lin Z., Walker M.A., Krystal M.R., Dicker I.B. The terminal (catalytic) adenosine of the HIV LTR controls the kinetics of binding and dissociation of HIV integrase strand transfer inhibitors. Biochemistry 2008, 47:13481-13488.
88. Leavitt A.D., Shiue L., Varmus H.E. Site-directed mutagenesis of HIV-1 integrase demonstrates differential effects on integrase functions in vitro. J. Biol. Chem. 1993, 268:2113-2119.
89. Lee S.P., Han M.K. Zinc stimulates Mg2+-dependent 3'-processing activity of human immunodeficiency virus type 1 integrase in vitro. Biochemistry 1996, 35:3837-3844.
90. Lee S.P., Xiao J., Knutson J.R., Lewis M.S., Han M.K. Zn2+ promotes the self-association of human immunodeficiency virus type-1 integrase in vitro. Biochemistry 1997, 36:173-180.
91. Li M., Craigie R. Processing of viral DNA ends channels the HIV-1 integration reaction to concerted integration. J. Biol. Chem. 2005, 280:29334-29339.
92. Li M., Mizuuchi M., Burke T.R., Craigie R. Retroviral DNA integration: reaction pathway and critical intermediates. EMBO J. 2006, 25:1295-1304.
93. Lodi P.J., Ernst J.A., Kuszewski J., Hickman A.B., Engelman A., Craigie R., Clore G.M., Gronenborn A.M. Solution structure of the DNA binding domain of HIV-1 integrase. Biochemistry 1995, 34:9826-9833.
94. Lubkowski J., Yang F., Alexandratos J., Merkel G., Katz R.A., Gravuer K., Skalka A.M., Wlodawer A. Structural basis for inactivating mutations and pH-dependent activity of avian sarcoma virus integrase. J. Biol. Chem. 1998, 273:32685-32689.
95. Lubkowski J., Yang F., Alexandratos J., Wlodawer A., Zhao H., Burke T.R., Neamati N., Pommier Y., Merkel G., Skalka A.M. Structure of the catalytic domain of avian sarcoma virus integrase with a bound HIV-1 integrase-targeted inhibitor. Proc. Natl Acad. Sci. USA 1998, 95:4831-4836.
96. Lubkowski J., Dauter Z., Yang F., Alexandratos J., Merkel G., Skalka A.M., Wlodawer A. Atomic resolution structures of the core domain of avian sarcoma virus integrase and its D64N mutant. Biochemistry 1999, 38:13512-13522.
97. Maertens G., Cherepanov P., Pluymers W., Busschots K., De Clercq E., Debyser Z., Engelborghs Y. LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 2003, 278:33528-33539.
98. Maertens G.N., Hare S., Cherepanov P. The mechanism of retroviral integration through X-ray structures of its key intermediates. Nature 2010, 468:326-329.
99. Maignan S., Guilloteau J.P., Zhou-Liu Q., Clement-Mella C., Mikol V. 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. 1998, 282:359-368.
100. McColl D.J., Chen X. Strand transfer inhibitors of HIV-1 integrase: bringing IN a new era of antiretroviral therapy. Antiviral Res. 2010, 85:101-118.
101. McKee C.J., Kessl J.J., Shkriabai N., Dar M.J., Engelman A., Kvaratskhelia M. Dynamic modulation of HIV-1 integrase structure and function by cellular lens epithelium-derived growth factor (LEDGF) protein. J. Biol. Chem. 2008, 283:31802-31812.
102. Metifiot M., Marchand C., Maddali K., Pommier Y. Resistance to integrase inhibitors. Viruses 2010, 2:1347-1366.
103. Michel F., Crucifix C., Granger F., Eiler S., Mouscadet J.F., Korolev S., Agapkina J., Ziganshin R., Gottikh M., Nazabal A., Emiliani S., Benarous R., Moras D., Schultz P., Ruff M. Structural basis for HIV-1 DNA integration in the human genome, role of the LEDGF/P75 cofactor. EMBO J. 2009, 28:980-991.
104. Molteni V., Greenwald J., Rhodes D., Hwang Y., Kwiatkowski W., Bushman F.D., Siegel J.S., Choe S. Identification of a small-molecule binding site at the dimer interface of the HIV integrase catalytic domain. Acta Crystallogr. D Biol. Crystallogr. 2001, 57(Pt 4):536-544.
105. Nowak M.G., Sudol M., Lee N.E., Konsavage W.M., Katzman M. Identifying amino acid residues that contribute to the cellular-DNA binding site on retroviral integrase. Virology 2009, 389:141-148.
106. Nowotny M. Retroviral integrase superfamily: the structural perspective. EMBO Rep. 2009, 10:144-151.
107. Nowotny M., Gaidamakov S.A., Crouch R.J., Yang W. Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 2005, 121:1005-1016.
108. Pahl A., Flügel R.M. Endonucleolytic cleavages and DNA-joining activities of the integration protein of human foamy virus. J. Virol. 1993, 67:5426-5434.
109. Pahl A., Flügel R.M. Characterization of the human spuma retrovirus integrase by site-directed mutagenesis, by complementation analysis, and by swapping the zinc finger domain of HIV-1. J. Biol. Chem. 1995, 270:2957-2966.
110. Pandey K.K., Bera S., Zahm J., Vora A., Stillmock K., Hazuda D., Grandgenett D.P. Inhibition of human immunodeficiency virus type 1 concerted integration by strand transfer inhibitors which recognize a transient structural intermediate. J. Virol. 2007, 81:12189-12199.
111. Poeschla E.M. Integrase, LEDGF/p75 and HIV replication. Cell. Mol. Life Sci. 2008, 65:1403-1424.
112. Pruss D., Bushman F., Wolffe A. Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc. Natl Acad. Sci. USA 1994, 91:5913-5917.
113. Pryciak P.M., Varmus H.E. Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection. Cell 1992, 69:769-780.
114. Réty S., Reaeábková L., Dubanchet B., Silhán J., Legrand P., Lewit-Bentley A. Structural studies of the catalytic core of the primate foamy virus (PFV-1) integrase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2010, 66:881-886.
115. Sherman P.A., Fyfe J.A. Human immunodeficiency virus integration protein expressed in Escherichia coli possesses selective DNA cleaving activity. Proc. Natl Acad. Sci. USA 1990, 87:5119-5123.
116. Sinha S., Grandgenett D.P. Recombinant human immunodeficiency virus type 1 integrase exhibits a capacity for full-site integration in vitro that is comparable to that of purified preintegration complexes from virus-infected cells. J. Virol. 2005, 79:8208-8216.
117. Sinha S., Pursley M.H., Grandgenett D.P. Efficient concerted integration by recombinant human immunodeficiency virus type 1 integrase without cellular or viral cofactors. J. Virol. 2002, 76:3105-3113.
118. Steitz T.A., Steitz J.A. A general two-metal-ion mechanism for catalytic RNA. Proc. Natl Acad. Sci. USA 1993, 90:6498-6502.
119. Stevens S.W., Griffith J.D. Sequence analysis of the human DNA flanking sites of human immunodeficiency virus type 1 integration. J. Virol. 1996, 70:6459-6462.
120. Summa V., Petrocchi A., Bonelli F., Crescenzi B., Donghi M., Ferrara M., Fiore F., Gardelli C., Gonzalez Paz O., Hazuda D.J., Jones P., Kinzel O., Laufer R., Monteagudo E., Muraglia E., Nizi E., Orvieto F., Pace P., Pescatore G., Scarpelli R., Stillmock K., Witmer M.V., Rowley M. Discovery of raltegravir, a potent, selective orally bioavailable HIV-integrase inhibitor for the treatment of HIV-AIDS infection. J. Med. Chem. 2008, 51:5843-5855.
121. Swanstrom R., Wills J.W. Synthesis, assembly, and processing of viral proteins. Retroviruses 1997, 263-334. Cold Spring Harbor Laboratory Press, Plainview, New York. J.M. Coffin, S.H. Hughes, H.E. Varmus (Eds.).
122. Tang J., Maddali K., Pommier Y., Sham Y.Y., Wang Z. Scaffold rearrangement of dihydroxypyrimidine inhibitors of HIV integrase: docking model revisited. Bioorg. Med. Chem. Lett. 2010, 20:3275-3279.
123. Trobridge G.D., Miller D.G., Jacobs M.A., Allen J.M., Kiem H.-P., Kaul R., Russell D.W. Foamy virus vector integration sites in normal human cells. Proc. Natl Acad. Sci. USA 2006, 103:1498-1503.
124. Turlure F., Devroe E., Silver P.A., Engelman A. Human cell proteins and human immunodeficiency virus DNA integration. Front. Biosci. 2004, 9:3187-3208.
125. Valkov E., Gupta S.S., Hare S., Helander A., Roversi P., McClure M., Cherepanov P. Functional and structural characterization of the integrase from the prototype foamy virus. Nucleic Acids Res. 2009, 37:243-255.
126. van Gent D.C., Groeneger A.A., Plasterk R.H. Mutational analysis of the integrase protein of human immunodeficiency virus type 2. Proc. Natl Acad. Sci. USA 1992, 89:9598-9602.
127. van Gent D.C., Vink C., Groeneger A.A., Plasterk R.H. Complementation between HIV integrase proteins mutated in different domains. EMBO J. 1993, 12:3261-3267.
128. Van Maele B., Busschots K., Vandekerckhove L., Christ F., Debyser Z. Cellular co-factors of HIV-1 integration. Trends Biochem. Sci. 2006, 31:98-105.
129. Vanegas M., Llano M., Delgado S., Thompson D., Peretz M., Poeschla E. Identification of the LEDGF/p75 HIV-1 integrase-interaction domain and NLS reveals NLS-independent chromatin tethering. J. Cell Sci. 2005, 118:1733-1743.
130. Vink C., Oude Groeneger A.M., Plasterk R.H. Identification of the catalytic and DNA-binding region of the human immunodeficiency virus type I integrase protein. Nucleic Acids Res. 1993, 21:1419-1425.
131. Wang J.-Y., Ling H., Yang W., Craigie R. Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J. 2001, 20:7333-7343.
132. Wei S.-Q., Mizuuchi K., Craigie R. A large nucleoprotein assembly at the ends of the viral DNA mediates retroviral DNA integration. EMBO J. 1997, 16:7511-7520.
133. Wielens J., Headey S.J., Jeevarajah D., Rhodes D.I., Deadman J., Chalmers D.K., Scanlon M.J., Parker M.W. Crystal structure of the HIV-1 integrase core domain in complex with sucrose reveals details of an allosteric inhibitory binding site. FEBS Lett. 2010, 584:1455-1462.
134. Woerner A.M., Marcus-Sekura C.J. Characterization of a DNA binding domain in the C-terminus of HIV-1 integrase by deletion mutagenesis. Nucleic Acids Res. 1993, 21:3507-3511.
135. Woerner A.M., Klutch M., Levin J.G., Marcus-Sekura C.J. Localization of DNA binding activity of HIV-1 integrase to the C-terminal half of the protein. AIDS Res. Hum. Retroviruses 1992, 8:297-304.
136. Wu X., Li Y., Crise B., Burgess S.M., Munroe D.J. Weak palindromic consensus sequences are a common feature found at the integration target sites of many retroviruses. J. Virol. 2005, 79:5211-5214.
137. Yanagihara K., Mizuuchi K. Mismatch-targeted transposition of Mu: a new strategy to map genetic polymorphism. Proc. Natl Acad. Sci. USA 2002, 99:11317-11321.
138. Yang F., Roth M.J. Assembly and catalysis of concerted two-end integration events by Moloney murine leukemia virus integrase. J. Virol. 2001, 75:9561-9670.
139. Yang Z.-N., Mueser T.C., Bushman F.D., Hyde C.C. Crystal structure of an active two-domain derivative of rous sarcoma virus integrase. J. Mol. Biol. 2000, 296:535-548.
140. Yao X., Fang S., Qiao W., Geng Y., Shen Y. Crystal structures of catalytic core domain of BIV integrase: implications for the interaction between integrase and target DNA. Protein Cell 2010, 1:363-370.
141. Zhao Z., McKee C.J., Kessl J.J., Santos W.L., Daigle J.E., Engelman A., Verdine G., Kvaratskhelia M. 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. 2008, 283:5632-5641.
142. Zheng R., Jenkins T.M., Craigie R. Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity. Proc. Natl Acad. Sci. USA 1996, 93:13659-13664.