Potent inhibition of HIV-1 replication by backbone cyclic peptides bearing the Rev arginine rich motif

Journal of Biomedical Science

Volumn 14, Issue 5, 2007, Pages 565-584

  Chaloin, Laurent ^a   Smagulova, Fatima ^a   Hariton Gazal, Elana ^b   Briant, Laurence ^a   Loyter, Abraham ^b   Devaux, Christian ^a  

^a University of Montpellier I and II   (France)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Antiviral peptides; Arginine rich motif; Backbone cyclic peptide; HIV; Rev

Indexed keywords

CYCLOPEPTIDE; CYSTEINE; GP160ENV PROTEIN; MESSENGER RNA; OLIGONUCLEOTIDE; PR55GAG PROTEIN; PROTEIN; PROTEIN PRECURSOR; REV PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

ANALYTIC METHOD; ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN SITU HYBRIDIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MOTIF; T LYMPHOCYTE; VIRUS INHIBITION; VIRUS REPLICATION;

AMINO ACID MOTIFS; ANTI-HIV AGENTS; ARGININE; GENE PRODUCTS, REV; HELA CELLS; HIV ENVELOPE PROTEIN GP160; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; MODELS, MOLECULAR; PEPTIDES, CYCLIC; PROTEIN PRECURSORS; RNA, VIRAL; T-LYMPHOCYTES; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34548672161     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1007/s11373-007-9180-4     Document Type: Article

References (55)

1. Frankel A.D., Young J.A. (1998) HIV-1: fifteen proteins and an RNA, Annu. Rev. Biochem. 67: 1-25
2. Gait M.J., Karn J. (1993) RNA recognition by the human immunodeficiency virus Tat and Rev proteins, Trends Biochem. Sci. 18: 255-259
3. Emerman M., Malim M.H. (1998) HIV-1 regulatory/accessory genes: keys to unraveling viral and host cell biology, Science 280: 1880-1884
4. Yedavalli V.S., Neuveut C., Chi Y.H., Kleiman L., Jeang K.T. (2004) Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function, Cell 119: 381-392
5. Dayton A.I. (2004) Within you, without you: HIV-1 Rev and RNA export, Retrovirology 1: 35
6. Fang J., Kubota S., Yang B., Zhou N., Zhang H., Godbout R., Pomerantz R.J. (2004) A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev, Virology 330: 471-480
7. Sanchez-Velar N., Udofia E.B., Yu Z., Zapp M.L. (2004) hRIP, a cellular cofactor for Rev function, promotes release of HIV RNAs from the perinuclear region, Genes Dev. 18: 23-34
8. Zolotukhin A.S., Felber B.K. (1999) Nucleoporins nup98 and nup214 participate in nuclear export of human immunodeficiency virus type 1 Rev, J. Virol. 73: 120-127
9. Kjems J., Askjaer P. (2000) Rev protein and its cellular partners, Adv. Pharmacol. 48: 251-298
10. Kjems J., Brown M., Chang D.D., Sharp P.A. (1991) Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element, Proc. Natl. Acad. Sci. USA 88: 683-687
11. Cochrane A. (2004) Controlling HIV-1 Rev function, Curr. Drug Targets Immune Endocr. Metabol. Disord. 4: 287-295
12. Cochrane A.W., Perkins A., Rosen C.A. (1990) Identification of sequences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function, J. Virol. 64: 881-885
13. Sandri-Goldin R.M. (2004) Viral regulation of mRNA export, J. Virol. 78: 4389-4396
14. Cullen B.R., Malim M.H. (1991) The HIV-1 Rev protein: prototype of a novel class of eukaryotic post-transcriptional regulators, Trends Biochem. Sci. 16: 346-350
15. Cmarko D., Boe S.O., Scassellati C., Szilvay A.M., Davanger S., Fu X.D., Haukenes G., Kalland K.H., Fakan S. (2002) Rev inhibition strongly affects intracellular distribution of human immunodeficiency virus type 1 RNAs, J. Virol. 76: 10473-10484
16. Puglisi J.D., Chen L., Blanchard S., Frankel A.D. (1995) Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA complex, Science 270: 1200-1203
17. Battiste J.L., Mao H., Rao N.S., Tan R., Muhandiram D.R., Kay L.E., Frankel A.D., Williamson J.R. (1996) Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex, Science 273: 1547-1551
18. Ye X., Gorin A., Ellington A.D., Patel D.J. (1996) Deep penetration of an alpha-helix into a widened RNA major groove in the HIV-1 rev peptide-RNA aptamer complex, Nat. Struct. Biol. 3: 1026-1033
19. Gosser Y., Hermann T., Majumdar A., Hu W., Frederick R., Jiang F., Xu W., Patel D.J. (2001) Peptide-triggered conformational switch in HIV-1 RRE RNA complexes, Nat. Struct. Biol. 8: 146-150
20. Weiss M.A., Narayana N. (1998) RNA recognition by arginine-rich peptide motifs, Biopolymers 48: 167-180
21. Gilon C., Halle D., Chorev M., Selinger Z., Byk G. (1991) Backbone cyclization: a new method for conferring conformational constraint on peptides, Biopolymers 31: 745-750
22. Bitan G., Zeltser I., Byk G., Halle D., Mashriki Y., Gluhov E.V., Sukhotinsky I., Hanani M., Selinger Z., Gilon C. (1996) Backbone cyclization of the C-terminal part of substance P. Part 1: the important role of the sulphur in position 11, J. Pept. Sci. 2: 261-269
23. Byk G., Halle D., Zeltser I., Bitan G., Selinger Z., Gilon C. (1996) Synthesis and biological activity of NK-1 selective, N-backbone cyclic analogs of the C-terminal hexapeptide of substance P, J. Med. Chem. 39: 3174-3178
24. Friedler A., Friedler D., Luedtke N.W., Tor Y., Loyter A., Gilon C. (2000) Development of a functional backbone cyclic mimetic of the HIV-1 Tat arginine-rich motif, J. Biol. Chem. 275: 23783-23789
25. Hariton-Gazal E., Rosenbluh J., Zakai N., Fridkin G., Brack-Werner R., Wolff H., Devaux C., Gilon C., Loyter A. (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
26. Mossmann T.R. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays, J. Immunol. Methods 65: 55-63
27. Falb E., Yechezkel T., Salitra Y., Gilon C. (1999) In situ generation of Fmoc-amino acid chlorides using bis-(trichloromethyl) carbonate and its utilization for difficult couplings in solid-phase peptide synthesis, J. Pept. Res. 53: 507-517
28. Friedler A., Zakai N., Karni O., Broder Y.C., Baraz L., Kotler M., Loyter A., Gilon C. (1998) Backbone cyclic peptide, which mimics the nuclear localization signal of human immunodeficiency virus type 1 matrix protein, inhibits nuclear import and virus production in nondividing cells, Biochemistry 37: 5616-5622
29. Barre-Sinoussi F., Chermann J.C., Rey F., Nugeyre M.T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vezinet-Brun F., Rouzioux C., Rozenbaum W., Montagnier L. (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS), Science 220: 868-871
30. 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
31. Mochizuki N., Otsuka N., Matsuo K., Shiino T., Kojima A., Kurata T., Sakai K., Yamamoto N., Isomura S., Dhole T.N., Takebe Y., Matsuda M., Tatsumi M. (1999) An infectious DNA clone of HIV type 1 subtype C, AIDS Res. Hum. Retroviruses 15: 1321-1324
32. Vendeville A., Rayne F., Bonhoure A., Bettache N., Montcourrier P., Beaumelle B. (2004) HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses, Mol. Biol. Cell 15: 2347-2360
33. Jacques P.S., Wohrl B.M., Ottmann M., Darlix J.L., Le Grice S.F. (1994) Mutating the "primer grip" of p66 HIV-1 reverse transcriptase implicates tryptophan-229 in template-primer utilization, J. Biol. Chem. 269: 26472-26478
34. Restle T., Muller B., Goody R.S. (1990) Dimerization of human immunodeficiency virus type 1 reverse transcriptase. A target for chemotherapeutic intervention, J. Biol. Chem. 265: 8986-8988
35. Briant L., Robert-Hebmann V., Acquaviva C., Pelchen-Matthews A., Marsh M., Devaux C. (1998) The protein tyrosine kinase p56lck is required for triggering NF-kappaB activation upon interaction of human immunodeficiency virus type 1 envelope glycoprotein gp120 with cell surface CD4, J. Virol. 72: 6207-6214
36. Chartrand P., Bertrand E., Singer R.H., Long R.M. (2000) Sensitive and high-resolution detection of RNA in situ, Methods Enzymol. 318: 493-506
37. Smagulova F., Maurel S., Morichaud Z., Devaux C., Mougel M., Houzet L. (2005) The highly structured encapsidation signal of MuLV RNA is involved in the nuclear export of its unspliced RNA, J. Mol. Biol. 354: 1118-1128
38. Cregut D., Liautard J.P., Chiche L. (1994) Homology modelling of annexin I: implicit solvation improves side-chain prediction and combination of evaluation criteria allows recognition of different types of conformational error, Protein Eng. 7: 1333-1344
39. Luthy R., Bowie J.U., Eisenberg D. (1992) Assessment of protein models with three-dimensional profiles, Nature 356: 83-85
40. Li Z., Scheraga H.A. (1987) Monte Carlo-minimization approach to the multiple-minima problem in protein folding, Proc. Natl. Acad. Sci. USA 84: 6611-6615
41. Wallace A.C., Laskowski R.A., Thornton J.M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions, Protein Eng. 8: 127-134
42. Fineberg K., Fineberg T., Graessmann A., Luedtke N.W., Tor Y., Lixin R., Jans D.A., Loyter A. (2003) Inhibition of nuclear import mediated by the Rev-arginine rich motif by RNA molecules, Biochemistry 42: 2625-2633
43. Truant R., Cullen B.R. (1999) The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals, Mol. Cell Biol. 19: 1210-1217
44. Rey F., Barre-Sinoussi F., Schmidtmayerova H., Chermann J.C. (1987) Detection and titration of neutralizing antibodies to HIV using an inhibition of the cytopathic effect of the virus on MT4 cells, J. Virol. Methods 16: 239-249
45. Bar S., Alizon M. (2004) Role of the ectodomain of the gp41 transmembrane envelope protein of human immunodeficiency virus type 1 in late steps of the membrane fusion process, J. Virol. 78: 811-820
46. Murriel C.L., Dowdy S.F. (2006) Influence of protein transduction domains on intracellular delivery of macromolecules, Expert Opin. Drug Deliv. 3: 739-746
47. van Vlerken L.E., Vyas T.K. and Amiji M.M., Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery. Pharm Res. DOI: 10.1007/s11095-007-9284-6, 2007
48. Pollard V.W., Malim M.H. (1998) The HIV-1 Rev protein, Annu. Rev. Microbiol. 52: 491-532
49. Friedler A., Luedtke N.W., Friedler D., Loyter A., Tor Y. and Gilon C., In: Fields G.B., Tam J.P. and Barany G. (Ed), Backbone cyclic proteinomimetics derived from the arginine-rich domain of HIV-1 Tat and Rev proteins: one sequence, two conformations, two biological functions, Peptides for the new millenium, proceedings of the 16th American peptide symposium, Minneapolis, 1999, 28-29, 1999
50. Tan R., Frankel A.D. (1995) Structural variety of arginine-rich RNA-binding peptides, Proc. Natl. Acad. Sci. USA 92: 5282-5286
51. Furnes C., Arnesen T., Askjaer P., Kjems J., Szilvay A.M. (2005) HIV-1 Rev oligomerization is not obligatory in the presence of an extra basic domain, Retrovirology 2: 39
52. Patel D.J. (1999) Adaptive recognition in RNA complexes with peptides and protein modules, Curr. Opin. Struct. Biol. 9: 74-87
53. Williamson J.R. (2000) Induced fit in RNA-protein recognition, Nat. Struct. Biol. 7: 834-837
54. Harada K., Martin S.S., Frankel A.D. (1996) Selection of RNA-binding peptides in vivo, Nature 380: 175-179
55. Harada K., Martin S.S., Tan R., Frankel A.D. (1997) Molding a peptide into an RNA site by in vivo peptide evolution, Proc. Natl. Acad. Sci. USA 94: 11887-11892