Contribution of the C-terminal region within the catalytic core domain of HIV-1 integrase to yeast lethality, chromatin binding and viral replication

Retrovirology

Volumn 5, Issue , 2008, Pages

  Xu, Zaikun ^a   Zheng, Yingfeng ^a   Ao, Zhujun ^a   Clement, Martin ^b   Mouland, Andrew J ^c   Kalpana, Ganjam V ^d   Belhumeur, Pierre ^b   Cohen, Éric A ^b,e   Yao, XiaoJian ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; INTEGRASE; DNA BINDING PROTEIN; NONHISTONE PROTEIN; P31 INTEGRASE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PSIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMARCB1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CELL LINE; CHROMATIN; CONTROLLED STUDY; CULTURE MEDIUM; FUNGAL STRAIN; FUNGUS GROWTH; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MAMMAL CELL; MOLECULAR MECHANICS; MUTAGENESIS; NONHUMAN; PHENOTYPE; PLASMID; PROTEIN DOMAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; VIRUS MUTANT; VIRUS REPLICATION; YEAST; AMINO ACID SUBSTITUTION; ANIMAL; CERCOPITHECUS; ENZYME ACTIVE SITE; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MISSENSE MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; SACCHAROMYCES CEREVISIAE; VESICULAR STOMATITIS VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ANIMALS; CATALYTIC DOMAIN; CELL LINE; CERCOPITHECUS AETHIOPS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; GENETIC COMPLEMENTATION TEST; HIV INTEGRASE; HIV-1; HUMANS; MICROBIAL VIABILITY; MUTAGENESIS; MUTATION, MISSENSE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; VIRUS REPLICATION;

EID: 58149529842     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-5-102     Document Type: Article

References (53)

1. Bukrinsky MI Stanwick TL Dempsey MP Stevenson M: Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 1991, 254:423-427. 10.1126/science.1925601 1925601
2. Petitjean G Al Tabaa Y Tuaillon E Mettling C Baillat V Reynes J Segondy M Vendrell JP: Unintegrated HIV-1 provides an inducible and functional reservoir in untreated and highly active antiretroviral therapy-treated patients. Retrovirology 2007, 4:60. 2048509 17727722 10.1186/ 1742-4690-4-60
3. 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. 10.1016/j.tibs.2005.12.002 16403635
4. 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. 10.1074/jbc.M209278200 12407101
5. Ciuffi A Llano M Poeschla E Hoffmann C Leipzig J Shinn P Ecker JR Bushman F: A role for LEDGF/p75 in targeting HIV DNA integration. Nat Med 2005, 11:1287-1289. 10.1038/nm1329 16311605
6. Llano M Saenz DT Meehan A Wongthida P Peretz M Walker WH Teo W Poeschla EM: An essential role for LEDGF/p75 in HIV integration. Science 2006, 314:461-464. 10.1126/science.1132319 16959972
7. 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. 10.1074/jbc.M303594200 12796494
8. Cherepanov P Ambrosio AL 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. 1297672 16260736 10.1073/pnas.0506924102
9. Cherepanov P Sun ZY 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. 10.1038/nsmb937 15895093
10. Busschots K Voet A De Maeyer M Rain JC Emiliani S Benarous R Desender L Debyser Z Christ F: Identification of the LEDGF/p75 binding site in HIV-1 integrase. J Mol Biol 2007, 365:1480-1492. 10.1016/ j.jmb.2006.10.094 17137594
11. Llano M S D Vanegas M Poeschla EM: LEDGF/p75 prevents proteasomal degradation of HIV-1 integrase. J Biol Chem 2004, 279:33430-33436. 10.1074/jbc.M404633200 15173169
12. Shun MC Raghavendra NK Vandegraaff N Daigle JE Hughes S Kellam P Cherepanov P Engelman A: LEDGF/p75 functions downstream from preintegration complex formation to effect gene-specific HIV-1 integration. Genes Dev 2007, 21:1767-1778. 1920171 17639082 10.1101/ gad.1565107
13. Kalpana GV Marmon S Wang W Crabtree GR Goff SP: Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 1994, 266:2002-2006. 10.1126/science.7801128 7801128
14. Wang W Côté J Xue Y Zhou S Khavari PA Biggar SR Muchardt C Kalpana GV Goff SP Yaniv M Workman JL Crabtree GR: Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. Embo J 1996, 15:5370-5382. 452280 8895581
15. Sorin M Yung E Wu X Kalpana GV: HIV-1 replication in cell lines harboring INI1/hSNF5 mutations. Retrovirology 2006, 3:56. 1592304 16945155 10.1186/1742-4690-3-56
16. Yung E Sorin M Wang EJ Perumal S Ott D Kalpana GV: Specificity of interaction of INI1/hSNF5 with retroviral integrases and its functional significance. J Virol 2004, 78:2222-2231. 369229 14963118 10.1128/ JVI.78.5.2222-2231.2004
17. Ariumi Y Serhan F Turelli P Telenti A Trono D: The integrase interactor 1 (INI1) proteins facilitate Tat-mediated human immunodeficiency virus type 1 transcription. Retrovirology 2006, 3:47. 1557532 16889668 10.1186/ 1742-4690-3-47
18. Wu X Liu H Xiao H Conway JA Hehl E Kalpana GV Prasad V Kappes JC: Human immunodeficiency virus type 1 integrase protein promotes reverse transcription through specific interactions with the nucleoprotein reverse transcription complex. J Virol 1999, 73:2126-2135. 104457 9971795
19. Ao Z Fowke KR Cohen EA Yao X: Contribution of the C-terminal tri-lysine regions of human immunodeficiency virus type 1 integrase for efficient reverse transcription and viral DNA nuclear import. Retrovirology 2005, 2:62. 1277849 16232319 10.1186/1742-4690-2-62
20. Bukovsky A Gottlinger H: Lack of integrase can markedly affect human immunodeficiency virus type 1 particle production in the presence of an active viral protease. J Virol 1996, 70:6820-6825. 190728 8794322
21. Engelman A Englund G Orenstein JM Martin MA Craigie R: Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J Virol 1995, 69:2729-2736. 188965 7535863
22. Gallay P Hope T Chin D Trono D: HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proc Natl Acad Sci USA 1997, 94(9825):9830-23276. 9275210 10.1073/pnas.94.18.9825
23. Ikeda T Nishitsuji H Zhou X Nara N Ohashi T Kannagi M Masuda T: Evaluation of the functional involvement of human immunodeficiency virus type 1 integrase in nuclear import of viral cDNA during acute infection. J Virol 2004, 78:11563-11573. 523288 15479797 10.1128/ JVI.78.21.11563-11573.2004
24. Nakamura T Masuda T Goto T Sano K Nakai M Harada S: Lack of infectivity of HIV-1 integrase zinc finger-like domain mutant with morphologically normal maturation. Biochem Biophys Res Commun 1997, 239:715-722. 10.1006/ bbrc.1997.7541 9367835
25. Engelman A Cherepanov P: The lentiviral integrase binding protein LEDGF/ p75 and HIV-1 replication. PLoS Pathog 2008, 4:e1000046. 2275779 18369482 10.1371/journal.ppat.1000046
26. Caumont AB Jamieson GA Pichuantes S Nguyen AT Litvak S Dupont C: Expression of functional HIV-1 integrase in the yeast Saccharomyces cerevisiae leads to the emergence of a lethal phenotype: Potential use for inhibitor screening. Curr Genet 1996, 29:503-510. 10.1007/BF02426953 8662188
27. Parissi V Caumont AB de Soultrait VR Calmels C Pichuantes S Litvak S Dupont CH: Selection of amino acid substitutions restoring activity of HIV-1 integrase mutated in its catalytic site using the yeast Saccharomyces cerevisiae. J Mol Biol 2000, 295:755-765. 10.1006/ jmbi.1999.3416 10656788
28. Parissi V Caumont A de Soultrait VR Desjobert C Calmels C Fournier M Gourgue G Bonneu M Tarrago-Litvak L Litvak S: The lethal phenotype observed after HIV-1 integrase expression in yeast cells is related to DNA repair and recombination events. Gene 2003, 322:157-168. 10.1016/ j.gene.2003.08.020 14644507
29. Parissi V Caumont A Richard de Soultrait V Dupont CH Pichuantes S Litvak S: Inactivation of the SNF5 transcription factor gene abolishes the lethal phenotype induced by the expression of HIV-1 integrase in yeast. Gene 2000, 247:129-136. 10.1016/S0378-1119(00)00108-6 10773452
30. Calmels C de Soultrait VR Caumont A Desjobert C Faure A Fournier M Tarrago-Litvak L Parissi V: Biochemical and random mutagenesis analysis of the region carrying the catalytic E152 amino acid of HIV-1 integrase. Nucleic Acids Res 2004, 32:1527-1538. 390286 14999095 10.1093/nar/gkh298
31. Cannon PM Wilson W Byles E Kingsman SM Kingsman AJ: Human immunodeficiency virus type 1 integrase: Effect on viral replication of mutations at highly conserved residues. J Virol 1994, 68:4768-4775. 236416 8035478
32. Limon A Devroe E Lu R Ghory HZ Silver PA Engelman A: Nuclear localization of human immunodeficiency virus type 1 preintegration complexes (PICs): V165A and R166A are pleiotropic integrase mutants primarily defective for integration, not PIC nuclear import. J Virol 2002, 76:10598-10607. 136649 12368302 10.1128/JVI.76.21.10598-10607.2002
33. Lu R Limon A Devroe E Silver PA Cherepanov P Engelman A: Class II integrase mutants with changes in putative nuclear localization signals are primarily blocked at a postnuclear entry step of human immunodeficiency virus type 1 replication. J Virol 2004, 78:12735-12746. 525011 15542626 10.1128/JVI.78.23.12735-12746.2004
34. Wiskerchen M Muesing MA: Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J Virol 1995, 69:376-386. 188585 7983732
35. Berthoux L Sebastian S Muesing MA Luban J: The role of lysine 186 in HIV-1 integrase multimerization. Virology 2007, 364:227-236. 2149894 17397894 10.1016/j.virol.2007.02.029
36. Desfarges S San Filippo J Fournier M Calmels C Caumont-Sarcos A Litvak S Sung P Parissi V: Chromosomal integration of LTR-flanked DNA in yeast expressing HIV-1 integrase: Down regulation by RAD51. Nucleic Acids Res 2006, 34:6215-6224. 1693895 17090598 10.1093/nar/gkl843
37. Liang C Stillman B: Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev 1997, 11(3375):3386-316796. 9407030 10.1101/gad.11.24.3375
38. Feller A Ramos F Pierard A Dubois E: In Saccharomyces cerevisae, feedback inhibition of homocitrate synthase isoenzymes by lysine modulates the activation of LYS gene expression by Lys14p. Eur J Biochem 1999, 261:163-170. 10.1046/j.1432-1327.1999.00262.x 10103047
39. Llano M Vanegas M Hutchins N Thompson D Delgado S Poeschla EM: Identification and characterization of the chromatin-binding domains of the HIV-1 integrase interactor LEDGF/p75. J Mol Biol 2006, 360:760-773. 10.1016/j.jmb.2006.04.073 16793062
40. Davis LI Blobel G: Identification and characterization of a nuclear pore complex protein. Cell 1986, 45:699-709. 10.1016/0092-8674(86)90784-1 3518946
41. Emiliani S Mousnier A Busschots K Maroun M van Maele B Tempé D Vandekerckhove L Moisant F Ben-Slama L Witvrouw M Christ F Rain JC Dargemont C Debyser Z Benarous R: Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J Biol Chem 2005, 280:25517-25523. 10.1074/ jbc.M501378200 15855167
42. Ao Z Huang G Yao H Xu Z Labine M Cochrane AW Yao X: Interaction of human immunodeficiency virus type 1 integrase with cellular nuclear import receptor importin 7 and its impact on viral replication. J Biol Chem 2007, 282:13456-13467. 10.1074/jbc.M610546200 17360709
43. Fletcher TM 3rd Soares MA McPhearson S Hui H Wiskerchen M Muesing MA Shaw GM Leavitt AD Boeke JD Hahn BH: Complementation of integrase function in HIV-1 virions. Embo J 1997, 16:5123-5138. 1170146 9305653 10.1093/emboj/16.16.5123
44. Wu X Liu H Xiao H Conway JA Hunter E Kappes JC: Functional RT and IN incorporated into HIV-1 particles independently of the Gag/Pol precursor protein. Embo J 1997, 16:5113-5122. 1170145 9305652 10.1093/emboj/ 16.16.5113
45. Dyda F Hickman AB Jenkins TM Engelman A Craigie R Davies DR: Crystal structure of the catalytic domain of HIV-1 integrase: Similarity to other polynucleotidyl transferase. Science 1994, 266:1981-1986. 10.1126/ science.7801124 7801124
46. McKee CJ Kessl JJ Shkriabai N Dar MJ Engelman A Kvaratskhelia M: Dynamic modulation of HIV-1 integrase structure and function by cellular LEDGF protein. J Biol Chem 2008, 283(46):31802-31812. 10.1074/jbc.M805843200 18801737
47. Parissi V Calmels C De Soultrait VR Caumont A Fournier M Chaignepain S Litvak S: Functional interactions of human immunodeficiency virus type 1 integrase with human and yeast HSP60. J Virol 2001, 75:11344-11353. 114720 11689615 10.1128/JVI.75.23.11344-11353.2001
48. Yao XJ Lemay J Rougeau N Clément M Kurtz S Belhumeur P Cohen E: Genetic Selection of peptide inhibitors of human immunodeficiency virus type 1 (HIV-1) Vpr. J Biol Chem 2002, 277:48816-48826. 10.1074/ jbc.M207982200 12379652
49. Yao XJ Subbramanian RA Rougeau N Boisvert F Bergeron D Cohen EA: Mutagenic analysis of human immunodeficiency virus type 1 Vpr: Role of a predicted N-terminal alpha-helical structure in Vpr nuclear localization and virion incorporation. J Virol 1995, 69:7032-7044. 189623 7474123
50. Ao Z Yao X Cohen EA: Assessment of the role of the central DNA flap in human immunodeficiency virus type 1 replication by using a single-cycle replication system. J Virol 2004, 78:3170-3177. 353776 14990738 10.1128/ JVI.78.6.3170-3177.2004
51. Vandegraaff N Devroe E Turlure F Silver PA Engelman A: Biochemical and genetic analyses of integrase-interacting proteins lens epithelium-derived growth factor (LEDGF)/p75 and hepatoma-derived growth factor related protein 2 (HRP2) in preintegration complex function and HIV-1 replication. Virology 2006, 346:415-426. 10.1016/ j.virol.2005.11.022 16337983
52. Yao XJ Mouland AJ Subbramanian RA Forget J Rougeau N Bergeron D Cohen EA: Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. J Virol 1998, 72:4686-4693. 109992 9573232
53. Yao XJ Kobinger G Dandache S Rougeau N Cohen E: HIV-1 Vpr-chloramphenicol acetyltransferase fusion proteins: Sequence requirement for virion incorporation and analysis of antiviral effect. Gene Ther 1999, 6:1590-1599. 10.1038/sj.gt.3300988 10490769