Peptides derived from HIV-1 integrase that bind rev stimulate viral genome integration

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Levin, Aviad ^a   Hayouka, Zvi ^a   Helfer, Markus ^b   Brack Werner, Ruth ^b   Friedler, Assaf ^a   Loyter, Abraham ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GAG PROTEIN; INTEGRASE; PROTEIN INR 1; PROTEIN INR 2; REV PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; P31 INTEGRASE PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PEPTIDE;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME REGULATION; GENE LIBRARY; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS REPLICATION; BINDING SITE; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

BINDING SITES; CELLS, CULTURED; DNA, VIRAL; GENOME, VIRAL; HELA CELLS; HIV INTEGRASE; HIV-1; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROTEIN CONFORMATION; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS INTEGRATION;

EID: 58349109557     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004155     Document Type: Article

References (64)

1. Bukrinsky MI, Sharova N, McDonald TL, Pushkarskaya T, Tarpley WG, et al. (1993) Association of integrase, matrix, and reverse transcriptase antigens of human immunodeficiency virus type 1 with viral nucleic acids following acute infection. Proc Natl Acad Sci U S A 90: 6125-6129.
2. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, et al. (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101: 173-185.
3. Depienne C, Roques P, Creminon C, Fritsch L, Casseron R, et al. (2000) Cellular distribution and karyophilic properties of matrix, integrase, and Vpr proteins from the human and simian immunodeficiency viruses. Exp Cell Res 260: 387-395.
4. Farnet CM, Haseltine WA (1991) Determination of viral proteins present in the human immunodeficiency virus type 1 preintegration complex. J Virol 65: 1910-1915.
5. Haffar OK, Popov S, Dubrovsky L, Agostini I, Tang H, et al. (2000) Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. J Mol Biol 299: 359-368.
6. Jenkins Y, McEntee M, Weis K, Greene WC (1998) Characterization of HIV-1 vpr nuclear import: analysis of signals and pathways. J Cell Biol 143: 875-885.
7. Miller MD, Farnet CM, Bushman FD (1997) Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J Virol 71: 5382-5390.
8. Sherman MP, Greene WC (2002) Slipping through the door: HIV entry into the nucleus. Microbes Infect 4: 67-73.
9. Engelman A, Mizuuchi K, Craigie R (1991) HIV-1 DNA integration: mechanism of viral DNA cleavage and DNA strand transfer. Cell 67: 1211-1221.
10. 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. J Biol Chem 281: 22707-22719.
11. Chen A, Weber IT, Harrison RW, Leis J (2006) 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: 4173-4182.
12. Heuer TS, Brown PO (1998) Photo-cross-linking studies suggest a model for the architecture of an active human immunodeficiency virus type 1 integrase-DNA complex. Biochemistry 37: 6667-6678.
13. Van Maele B, Busschots K, Vandekerckhove L, Christ F, Debyser Z (2006) Cellular co-factors of HIV-1 integration. Trends Biochem Sci 31: 98-105.
14. Emiliani S, Mousnier A, Busschots K, Maroun M, Van Maele B, et al. (2005) Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J Biol Chem 280: 25517-25523.
15. Maertens G, Cherepanov P, Pluymers W, Busschots K, De Clercq E, et al. (2003) LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J Biol Chem 278: 33528-33539.
16. Butler SL, Hansen MS, Bushman FD (2001) A quantitative assay for HIV DNA integration in vivo. Nat Med 7: 631-634.
17. Gelderblom HC, Vatakis DN, Burke SA, Lawrie SD, Bristol GC, et al. (2008) Viral complementation allows HIV-1 replication without integration. Retrovirology 5: 60.
18. Odawara T, Oshima M, Doi K, Iwamoto A, Yoshikura H (1998) Threshold number of provirus copies required per cell for efficient virus production and interference in moloney murine leukemia virus-infected NIH 3T3 cells. J Virol 72: 5414-5424.
19. Afanasieva TA, Pekarik V, Grazia D'Angelo M, Klein MA, Voigtlander T, et al. (2001) Insertional mutagenesis of preneoplastic astrocytes by Moloney murine leukemia virus. J Neurovirol 7: 169-181.
20. Tsuruo T, Baluda MA (1977) Integration of proviral DNA in chicken cells infected with Schmidt-Ruppin Rous sarcoma virus is not enhanced by DNA repair. J Virol 23: 533-542.
21. Tai CK, Kasahara N (2008) Replication-competent retrovirus vectors for cancer gene therapy. Front Biosci 13: 3083-3095.
22. Rosenbluh J, Hayouka Z, Loya S, Levin A, Armon-Omer A, et al. (2007) Interaction between HIV-1 Rev and integrase proteins: a basis for the development of anti-HIV peptides. J Biol Chem 282: 15743-15753.
23. Freed EO, Martin MA (2001) HIVs and their replication. In: Howley PM, ed. Fields Virology. Philadelphia: Lippincott Williams and Wilkins. pp 1971-2041.
24. Pollard VW, Malim MH (1998) The HIV-1 Rev protein. Annu Rev Microbiol 52: 491-532.
25. Wolff H, Hadian K, Ziegler M, Weierich C, Kramer-Hammerle S, et al. (2006) Analysis of the influence of subcellular localization of the HIV Rev protein on Rev-dependent gene expression by multi-fluorescence live-cell imaging. Exp Cell Res 312: 443-456.
26. Freed EO (2001) HIV-1 replication. Somat Cell Mol Genet 26: 13-33.
27. Wolff B, Cohen G, Hauber J, Meshcheryakova D, Rabeck C (1995) Nucleocytoplasmic transport of the Rev protein of human immunodeficiency virus type 1 is dependent on the activation domain of the protein. Exp Cell Res 217: 31-41.
28. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, et al. (1997) Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387: 183-188.
29. Wu Y (2008) The second chance story of HIV-1 DNA: Unintegrated? Not a problem! Retrovirology 5: 61.
30. Kelly J, Beddall MH, Yu D, Iyer SR, Marsh JW, et al. (2008) Human macrophages support persistent transcription from unintegrated HIV-1 DNA. Virology 372: 300-312.
31. Wu Y, Marsh JW (2003) Early transcription from nonintegrated DNA in human immunodeficiency virus infection. J Virol 77: 10376-10382.
32. Wu Y (2004) HIV-1 gene expression: lessons from provirus and non-integrated DNA. Retrovirology 1: 13.
33. Watts NR, Misra M, Wingfield PT, Stahl SJ, Cheng N, et al. (1998) Three-dimensional structure of HIV-1 Rev protein filaments. J Struct Biol 121: 41-52.
34. Fineberg K, Fineberg T, Graessmann A, Luedtke NW, Tor Y, et al. (2003) Inhibition of nuclear import mediated by the Rev-arginine rich motif by RNA molecules. Biochemistry 42: 2625-2633.
35. 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. Proc Natl Acad Sci U S A 97: 8233-8238.
36. Hayouka Z, Rosenbluh J, Levin A, Loya S, Lebendiker M, et al. (2007) Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc Natl Acad Sci U S A 104: 8316-8321.
37. Armon-Omer A, Levin A, Hayouka Z, Butz K, Hoppe-Seyler F, et al. (2008) Correlation between shiftide activity and HIV-1 integrase inhibition by a peptide selected from a combinatorial library. J Mol Biol 376: 971-982.
38. Hariton-Gazal E, Rosenbluh J, Zakai N, Fridkin G, Brack-Werner R, et al. (2005) Functional analysis of backbone cyclic peptides bearing the arm domain of the HIV-1 Rev protein: characterization of the karyophilic properties and inhibition of Rev-induced gene expression. Biochemistry 44: 11555-11566.
39. Kramer-Hammerle S, Ceccherini-Silberstein F, Bickel C, Wolff H, Vincendeau M, et al. (2005) Identification of a novel Rev-interacting cellular protein. BMC Cell Biol 6: 20.
40. Baba M, Pauwels R, Balzarini J, Arnout J, Desmyter J, et al. (1988) Mechanism of inhibitory effect of dextran sulfate and heparin on replication of human immunodeficiency virus in vitro. Proc Natl Acad Sci U S A 85: 6132-6136.
41. Mitsuya H, Looney DJ, Kuno S, Ueno R, Wong-Staal F, et al. (1988) Dextran sulfate suppression of viruses in the HIV family: inhibition of virion binding to CD4+ cells. Science 240: 646-649.
42. Nakashima H, Yoshida O, Baba M, De Clercq E, Yamamoto N (1989) Anti-HIV activity of dextran sulphate as determined under different experimental conditions. Antiviral Res 11: 233-246.
43. Rigourd M, Lanchy JM, Le Grice SF, Ehresmann B, Ehresmann C, et al. (2000) Inhibition of the initiation of HIV-1 reverse transcription by 3′-azido-3′-deoxythymidine. Comparison with elongation. J Biol Chem 275: 26944-26951.
44. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, et al. (2004) Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: E234.
45. Paul TA, Quackenbush SL, Sutton C, Casey RN, Bowser PR, et al. (2006) Identification and characterization of an exogenous retrovirus from atlantic salmon swim bladder sarcomas. J Virol 80: 2941-2948.
46. Coffin JM, Hugbes SH, Varmus HE (1997) Historical introduction to the general properties of retroviruses. Retroviruses: Cold spring harbor laboratory press. pp 1-25.
47. Jenkins TM, Engelman A, Ghirlando R, Craigie R (1996) A soluble active mutant of HIV-1 integrase: involvement of both the core and carboxyl-terminal domains in multimerization. J Biol Chem 271: 7712-7718.
48. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, et al. (2000) Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74: 8358-8367.
49. Kimpton J, Emerman M (1992) Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J Virol 66: 2232-2239.
50. Hayouka Z, Rosenbluh J, Levin A, Loya S, Lebendiker M, et al. (2007) Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc Natl Acad Sci U S A 104: 8316-8321.
51. Kohler F, Cardon G, Pohlman M, Gill R, Schider O (1989) Enhancement of transformation rates in higher plants by low-does irradiation: are DNA repair systems involved in incorporation of exogenous DNA into the plant genome? Plant Mol Biol 12: 189-199.
52. Cullen BR (1987) Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol 152: 684-704.
53. Ratner L, Haseltine W, Patarca R, Livak KJ, Starcich B, et al. (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313: 277-284.
54. Gummuluru S, Kinsey CM, Emerman M (2000) An in vitro rapid-turnover assay for human immunodeficiency virus type 1 replication selects for cell-to-cell spread of virus. J Virol 74: 10882-10891.
55. Rosenbluh J, Kapelnikov A, Shalev DE, Rusnati M, Bugatti A, et al. (2006) Positively charged peptides can interact with each other, as revealed by solid phase binding assays. Anal Biochem 352: 157-168.
56. Melchior F, Paschal B, Evans J, Gerace L (1993) Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J Cell Biol 123: 1649-1659.
57. Craigie R, Mizuuchi K, Bushman FD, Engelman A (1991) A rapid in vitro assay for HIV DNA integration. Nucleic Acids Res 19: 2729-2734.
58. Hwang Y, Rhodes D, Bushman F (2000) Rapid microtiter assays for poxvirus topoisomerase, mammalian type IB topoisomerase and HIV-1 integrase: application to inhibitor isolation. Nucleic Acids Res 28: 4884-4892.
59. Pannecouque C, Pluymers W, Van Maele B, Tetz V, Cherepanov P, et al. (2002) New class of HIV integrase inhibitors that block viral replication in cell culture. Curr Biol 12: 1169-1177.
60. Yamamoto N, Tanaka C, Wu Y, Chang MO, Inagaki Y, et al. (2006) Analysis of human immunodeficiency virus type 1 integration by using a specific, sensitive and quantitative assay based on real-time polymerase chain reaction. Virus Genes 32: 105-113.
61. Field FJ, Born E, Murthy S, Mathur SN (2002) Polyunsaturated fatty acids decrease the expression of sterol regulatory element-binding protein-1 in CaCo-2 cells: effect on fatty acid synthesis and triacylglycerol transport. Biochem J 368: 855-864.
62. Chesebro B, Buller R, Portis J, Wehrly K (1990) Failure of human immunodeficiency virus entry and infection in CD4-positive human brain and skin cells. J Virol 64: 215-221.
63. Brack-Werner R, Kleinschmidt A, Ludvigsen A, Mellert W, Neumann M, et al. (1992) Infection of human brain cells by HIV-1: restricted virus production in chronically infected human glial cell lines. Aids 6: 273-285.
64. Li CK (1985) ELISA-based determination of immunological binding constants. Mol Immunol 22: 321-327.