Changes in the accessibility of the HIV-1 Integrase C-terminus in the presence of cellular proteins

Retrovirology

Volumn 7, Issue , 2010, Pages

  Benkhelifa Ziyyat, Sofia ^a,b   Bucher, Stéphanie ^a   Zanta Boussif, Maria Antonietta ^a   Pasquet, Julie ^a   Danos, Olivier ^a,c  

^a GÉNÉTHON   (France)

^b UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; INTEGRASE; LENS EPITHELIUM DERIVED GROWTH FACTOR; MATRIX PROTEIN; PROTEIN P75; REAGENT; STREPTAVIDIN; BIOTIN; P31 INTEGRASE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PSIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PROTEIN DEPLETION; PROTEIN INTERACTION; REVERSE TRANSCRIPTION; VIRION; VIRUS ENTRY; VIRUS INFECTION; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; METABOLISM; METHODOLOGY; PHYSIOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; STAINING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BIOTIN; CELL LINE; HIV INTEGRASE; HIV-1; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; STAINING AND LABELING; TRANSCRIPTION FACTORS;

EID: 77950538860     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-7-27     Document Type: Article

References (46)

1. Delelis O, Carayon K, Saib A, Deprez E, Mouscadet JF. Integrase and integration: biochemical activities of HIV-1 integrase. Retrovirology 2008, 5:114. 10.1186/1742-4690-5-114, 2615046, 19091057.
2. Turlure F, Devroe E, Silver PA, Engelman A. Human cell proteins and human immunodeficiency virus DNA integration. Front Biosci 2004, 9:3187-3208. 10.2741/1472, 15353349.
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. Llano M, Delgado S, Vanegas M, Poeschla EM. Lens Epithelium-derived Growth Factor/p75 Prevents Proteasomal Degradation of HIV-1 Integrase. J Biol Chem 2004, 279:55570-55577. 10.1074/jbc.M408508200, 15475359.
5. Mulder LCF, Muesing MA. Degradation of HIV-1 Integrase by the N-end Rule Pathway. J Biol Chem 2000, 275:29749-29753. 10.1074/jbc.M004670200, 10893419.
6. Lin CW, Engelman A. The barrier-to-autointegration factor is a component of functional human immunodeficiency virus type 1 preintegration complexes. J Virol 2003, 77:5030-5036. 10.1128/JVI.77.8.5030-5036.2003, 152146, 12663813.
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, 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.
9. 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.
10. Emiliani S, Mousnier A, Busschots K, Maroun M, Van Maele B, Tempe 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.
11. 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.
12. Cherepanov P, Ambrosio ALB, Rahman S, Ellenberger T, Engelman A. Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75. PNAS 2005, 102:17308-17313. 10.1073/pnas.0506924102, 1297672, 16260736.
13. 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. 10.1038/nm1329, 16311605.
14. Poeschla EM. Integrase, LEDGF/p75 and HIV replication. Cell Mol Life Sci 2008, 65:1403-1424. 10.1007/s00018-008-7540-5, 18264802.
15. Belshan M, Schweitzer CJ, Donnellan MR, Lu R, Engelman A. In vivo biotinylation and capture of HIV-1 matrix and integrase proteins. J Virol Methods 2009, 159:178-184. 10.1016/j.jviromet.2009.03.017, 19490971.
16. de Boer E, Rodriguez P, Bonte E, Krijgsveld J, Katsantoni E, Heck A, Grosveld F, Strouboulis J. Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. PNAS 2003, 100:7480-7485. 10.1073/pnas.1332608100, 164612, 12802011.
17. Brussel A, Sonigo P. Analysis of early human immunodeficiency virus type 1 DNA synthesis by use of a new sensitive assay for quantifying integrated provirus. J Virol 2003, 77:10119-10124. 10.1128/JVI.77.18.10119-10124.2003, 224570, 12941923.
18. Llano M, Vanegas M, Fregoso O, Saenz D, Chung S, Peretz M, Poeschla EM. LEDGF/p75 Determines Cellular Trafficking of Diverse Lentiviral but Not Murine Oncoretroviral Integrase Proteins and Is a Component of Functional Lentiviral Preintegration Complexes. J Virol 2004, 78:9524-9537. 10.1128/JVI.78.17.9524-9537.2004, 506940, 15308744.
19. Rahman S, Lu R, Vandegraaff N, Cherepanov P, Engelman A. Structure-based mutagenesis of the integrase-LEDGF/p75 interface uncouples a strict correlation between in vitro protein binding and HIV-1 fitness. Virology 2007, 357:79-90. 10.1016/j.virol.2006.08.011, 16959283.
20. 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.
21. Daugaard M, Kirkegaard-Sorensen T, Ostenfeld MS, Aaboe M, Hoyer-Hansen M, Orntoft TF, Rohde M, Jaattela M. Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res 2007, 67:2559-2567. 10.1158/0008-5472.CAN-06-4121, 17363574.
22. Vandekerckhove L, Christ F, Van Maele B, De Rijck J, Gijsbers R, Haute C, Witvrouw M, Debyser Z. Transient and stable knockdown of the integrase cofactor LEDGF/p75 reveals its role in the replication cycle of human immunodeficiency virus. J Virol 2006, 80:1886-1896. 10.1128/JVI.80.4.1886-1896.2006, 1367129, 16439544.
23. Arhel N, Genovesio A, Kim KA, Miko S, Perret E, Olivo-Marin JC, Shorte S, Charneau P. Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat Methods 2006, 3:817-824. 10.1038/nmeth928, 16990814.
24. Petit C, Schwartz O, Mammano F. Oligomerization within Virions and Subcellular Localization of Human Immunodeficiency Virus Type 1 Integrase. J Virol 1999, 73:5079-5088. 112553, 10233971.
25. Topper M, Luo Y, Zhadina M, Mohammed K, Smith L, Muesing MA. Posttranslational Acetylation of the Human Immunodeficiency Virus Type 1 Integrase Carboxyl-Terminal Domain Is Dispensable for Viral Replication. J Virol 2007, 81:3012-3017. 10.1128/JVI.02257-06, 1865993, 17182677.
26. Cereseto A, Manganaro L, Gutierrez MI, Terreni M, Fittipaldi A, Lusic M, Marcello A, Giacca M. Acetylation of HIV-1 integrase by p300 regulates viral integration. Embo J 2005, 24:3070-3081. 10.1038/sj.emboj.7600770, 1201351, 16096645.
27. Engelman A, Cherepanov P. The lentiviral integrase binding protein LEDGF/p75 and HIV-1 replication. PLoS Pathog 2008, 4:e1000046. 10.1371/journal.ppat.1000046, 2275779, 18369482.
28. Jaskolski M, Alexandratos JN, Bujacz G, Wlodawer A. Piecing together the structure of retroviral integrase, an important target in AIDS therapy. Febs J 2009, 276:2926-2946. 10.1111/j.1742-4658.2009.07009.x, 19490099.
29. Asante-Appiah E, Seeholzer SH, Skalka AM. Structural determinants of metal-induced conformational changes in HIV-1 integrase. J Biol Chem 1998, 273:35078-35087. 10.1074/jbc.273.52.35078, 9857042.
30. Asante-Appiah E, Skalka AM. A metal-induced conformational change and activation of HIV-1 integrase. J Biol Chem 1997, 272:16196-16205. 10.1074/jbc.272.26.16196, 9195919.
31. Michel F, Crucifix C, Granger F, Eiler S, Mouscadet JF, 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. 10.1038/emboj.2009.41, 2670869, 19229293.
32. Zhao Z, McKee CJ, Kessl JJ, Santos WL, Daigle JE, 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. 10.1074/jbc.M705241200, 2806305, 18093980.
33. 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. 10.1093/nar/gki241, 549407, 15718297.
34. McKee CJ, Kessl JJ, Shkriabai N, Dar MJ, 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. 10.1074/jbc.M805843200, 2581560, 18801737.
35. Jenkins TM, Engelman A, Ghirlando R, Craigie R. A soluble active mutant of HIV-1 integrase: involvement of both the core and carboxyl-terminal domains in multimerization. J Biol Chem 1996, 271:7712-7718. 10.1074/jbc.271.13.7712, 8631811.
36. 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.
37. Hamamoto S, Nishitsuji H, Amagasa T, Kannagi M, Masuda T. Identification of a novel human immunodeficiency virus type 1 integrase interactor, Gemin2, that facilitates efficient viral cDNA synthesis in vivo. J Virol 2006, 80:5670-5677. 10.1128/JVI.02471-05, 1472599, 16731905.
38. Luo K, Wang T, Liu B, Tian C, Xiao Z, Kappes J, Yu XF. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 2007, 81:7238-7248. 10.1128/JVI.02584-06, 1933265, 17428847.
39. Violot S, Hong SS, Rakotobe D, Petit C, Gay B, Moreau K, Billaud G, Priet S, Sire J, Schwartz O, Mouscadet JF, Boulanger P. The Human Polycomb Group EED Protein Interacts with the Integrase of Human Immunodeficiency Virus Type 1. J Virol 2003, 77:12507-12522. 10.1128/JVI.77.23.12507-12522.2003, 262565, 14610174.
40. Hehl EA, Joshi P, Kalpana GV, Prasad VR. Interaction between human immunodeficiency virus type 1 reverse transcriptase and integrase proteins. J Virol 2004, 78:5056-5067. 10.1128/JVI.78.10.5056-5067.2004, 400328, 15113887.
41. Wilkinson TA, Januszyk K, Phillips ML, Tekeste SS, Zhang M, Miller JT, Le Grice SF, Clubb RT, Chow SA. Identifying and characterizing a functional HIV-1 reverse transcriptase-binding site on integrase. J Biol Chem 2009, 284:7931-7939. 10.1074/jbc.M806241200, 2658086, 19150986.
42. Zhu K, Dobard C, Chow SA. Requirement for Integrase during Reverse Transcription of Human Immunodeficiency Virus Type 1 and the Effect of Cysteine Mutations of Integrase on Its Interactions with Reverse Transcriptase. J Virol 2004, 78:5045-5055. 10.1128/JVI.78.10.5045-5055.2004, 400327, 15113886.
43. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998, 72:8463-8471. 110254, 9765382.
44. Olivier A, Jeanson-Leh L, Bouma G, Compagno D, Blondeau J, Seye K, Charrier S, Burns S, Thrasher AJ, Danos O, Vainchenker W, Galy. A partial down-regulation of WASP is sufficient to inhibit podosome formation in dendritic cells. Mol Ther 2006, 13:729-737. 10.1016/j.ymthe.2005.11.003, 16360341.
45. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997, 15:871-875. 10.1038/nbt0997-871, 9306402.
46. Delenda C, Gaillard C. Real-time quantitative PCR for the design of lentiviral vector analytical assays. Gene Ther 2005, 12(Suppl 1):S36-50. 10.1038/sj.gt.3302614, 16231054.