Single-nucleotide changes in the HIV rev-response element mediate resistance to compounds that inhibit rev function

Journal of Virology

Volumn 85, Issue 8, 2011, Pages 3940-3949

  Shuck Lee, Deidra ^c   Chang, Hua ^d   Sloan, Emily A ^a   Hammarskjold, Marie Louise ^a   Rekosh, David ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d Shanghai CDC ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 5 ETHYL 4,6 DIMETHYLTHIENO[2,3 B]PYRIDINE 2 CARBOXAMIDE; 4 AMINO 6 METHOXY 2 (TRIFLUOROMETHYL) 3 QUINOLINECARBONITRILE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; REV PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ARTICLE; BASE PAIRING; BINDING SITE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; POINT MUTATION; PRIORITY JOURNAL; REV RESPONSE ELEMENT; VIROGENESIS; VIRUS MUTATION; VIRUS REPLICATION; VIRUS STRAIN;

ANTI-HIV AGENTS; DRUG RESISTANCE, VIRAL; GENES, ENV; HIV; NUCLEIC ACID CONFORMATION; POINT MUTATION; RNA, VIRAL; SELECTION, GENETIC; VIRUS REPLICATION;

EID: 79952836893     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02683-10     Document Type: Article

References (54)

1. Askjaer, P., T. H. Jensen, J. Nilsson, L. Englmeier, and J. Kjems. 1998. The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J. Biol. Chem. 273:33414-33422.
2. Bartel, D. P., M. L. Zapp, M. R. Green, and J. W. Szostak. 1991. HIV-1 Rev regulation involves recognition of non-Watson-Crick base pairs in viral RNA. Cell 67:529-536.
3. Battiste, J. L., et al. 1996. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science 273:1547-1551. (Pubitemid 26301665)
4. Battiste, J. L., R. Tan, A. D. Frankel, and J. R. Williamson. 1994. Binding of an HIV Rev peptide to Rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry 33:2741-2747.
5. Chin, D. J. 1992. Inhibition of human immunodeficiency virus type 1 Rev-Rev-response element complex formation by complementary oligonucleotides. J. Virol. 66:600-607.
6. Cochrane, A. 2009. How does the journey affect the message(RNA)? RNA Biol. 6:169-170.
7. Cochrane, A. W., C. H. Chen, and C. A. Rosen. 1990. Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the env mRNA. Proc. Natl. Acad. Sci. U. S. A. 87:1198-1202.
8. Cochrane, A. W., M. T. McNally, and A. J. Mouland. 2006. The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 3:18.
9. Cook, K. S., et al. 1991. Characterization of HIV-1 REV protein: binding stoichiometry and minimal RNA substrate. Nucleic Acids Res. 19:1577-1583. (Pubitemid 21913254)
10. Daefler, S., M. E. Klotman, and S. F. Wong. 1990. Trans-activating rev protein of the human immunodeficiency virus 1 interacts directly and specifically with its target RNA. Proc. Natl. Acad. Sci. U. S. A. 87:4571-4575.
11. Daly, T. J., K. S. Cook, G. S. Gray, T. E. Maione, and J. R. Rusche. 1989. Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 342:816-819.
12. Daly, T. J., et al. 1993. Pertubation of the carboxy terminus of HIV-1 Rev affects multimerization on the Rev responsive element. Biochemistry 32: 8945-8954. (Pubitemid 23268820)
13. Daugherty, M. D., I. D'Orso, and A. D. Frankel. 2008. A solution to limited genomic capacity: using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA. Mol. Cell 31:824-834.
14. Daugherty, M. D., B. Liu, and A. D. Frankel. 2010. Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat. Struct. Mol. Biol. 17:1337-1342.
15. Dayton, A. I., J. G. Sodroski, C. A. Rosen, W. C. Goh, and W. A. Haseltine. 1986. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell 44:941-947.
16. Dayton, E. T., et al. 1992. Extensive sequence-specific information throughout the CAR/RRE, the target sequence of the human immunodeficiency virus type 1 Rev protein. J. Virol. 66:1139-1151.
17. Dayton, E. T., D. M. Powell, and A. I. Dayton. 1989. Functional analysis of CAR, the target sequence for the Rev protein of HIV-1. Science 246:1625-1629.
18. Dillon, P. J., P. Nelbock, A. Perkins, and C. A. Rosen. 1990. Function of the human immunodeficiency virus types 1 and 2 Rev proteins is dependent on their ability to interact with a structured region present in env gene mRNA. J. Virol. 64:4428-4437.
19. Feinberg, M. B., D. Baltimore, and A. D. Frankel. 1991. The role of Tat in the human immunodeficiency virus life cycle indicates a primary effect on transcriptional elongation. Proc. Natl. Acad. Sci. U. S. A. 88:4045-4049.
20. Feinberg, M. B., R. F. Jarrett, A. Aldovini, R. C. Gallo, and F. Wong-Staal. 1986. HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell 46:807-817. (Pubitemid 16027929)
21. Felber, B. K., M. Hadzopoulou-Cladaras, C. Cladaras, T. Copeland, and G. N. Pavlakis. 1989. Rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl. Acad. Sci. U. S. A. 86:1496-1499.
22. Fenster, S. D., R. W. Wagner, B. C. Froehler, and D. J. Chin. 1994. Inhibition of human immunodeficiency virus type-1 env expression by C-5 propyne oligonucleotides specific for Rev-response element stem-loop V. Biochemistry 33:8391-8398.
23. Groom, H. C., E. C. Anderson, J. A. Dangerfield, and A. M. Lever. 2009. Rev. regulates translation of human immunodeficiency virus type 1 RNAs. J. Gen. Virol. 90:1141-1147.
24. Groom, H. C., E. C. Anderson, and A. M. Lever. 2009. Rev: beyond nuclear export. J. Gen. Virol. 90:1303-1318.
25. Guzik, B. W., et al. 2001. NXT1 (p15) is a crucial cellular cofactor in TAP-dependent export of intron-containing RNA in mammalian cells. Mol. Cell. Biol. 21:2545-2554.
26. Hadzopoulou-Cladaras, M., et al. 1989. The rev (trs/art) protein of human immunodeficiency virus type 1 affects viral mRNA and protein expression via a cis-acting sequence in the env region. J. Virol. 63:1265-1274. (Pubitemid 19061368)
27. Hamm, T. E., D. Rekosh, and M. L. Hammarskjöld. 1999. Selection and characterization of human immunodeficiency virus type 1 mutants that are resistant to inhibition by the transdominant negative RevM10 protein. J. Virol. 73:5741-5747.
28. Hammarskjöld, M.-L., et al. 1989. Regulation of human immunodeficiency virus env expression by the rev gene product. J. Virol. 63:1959-1966. (Pubitemid 19107791)
29. Hammarskjöld, M. L. 1997. Regulation of retroviral RNA export. Semin. Cell Dev. Biol. 8:83-90.
30. Heaphy, S., et al. 1990. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 60:685-693.
31. Holland, S. M., N. Ahmad, R. K. Maitra, P. Wingfield, and S. Venkatesan. 1990. Human immunodeficiency virus Rev protein recognizes a target sequence in Rev-responsive element RNA within the context of RNA secondary structure. J. Virol. 64:5966-5975.
32. Huang, X. J., et al. 1991. Minimal Rev-response element for type 1 human immunodeficiency virus. J. Virol. 65:2131-2134.
33. Iwai, S., C. Pritchard, D. A. Mann, J. Karn, and M. J. Gait. 1992. Recognition of the high affinity binding site in Rev-response element RNA by the human immunodeficiency virus type-1 Rev protein. Nucleic Acids Res. 20: 6465-6472.
34. Jain, C., and J. G. Belasco. 2001. Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants. Mol. Cell 7:603-614.
35. Jin, L., B. W. Guzik, Y. C. Bor, D. Rekosh, and M. L. Hammarskjöld. 2003. Tap and NXT promote translation of unspliced mRNA. Genes Dev. 17: 3075-3086.
36. Kjems, J., A. D. Frankel, and P. A. Sharp. 1991. Specific regulation of mRNA splicing in vitro by a peptide from HIV-1 Rev. Cell 67:169-178.
37. Kuiken, C., et al. (ed.). 2010. HIV sequence compendium 2010. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, NM.
38. Legiewicz, M., et al. 2008. Resistance to RevM10 inhibition reflects a conformational switch in the HIV-1 Rev response element. Proc. Natl. Acad. Sci. U. S. A. 105:14365-14370.
39. Malim, M. H., and B. R. Cullen. 1991. HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 65:241-248.
40. Malim, M. H., J. Hauber, S. V. Le, J. V. Maizel, and B. R. Cullen. 1989. The HIV-1 Rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338:254-257.
41. Malim, M. H., et al. 1990. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 60:675-683.
42. Olsen, H. S., A. W. Cochrane, P. J. Dillon, C. M. Nalin, and C. A. Rosen. 1990. Interaction of the human immunodeficiency virus type 1 Rev protein with a structured region in env mRNA is dependent on multimer formation mediated through a basic stretch of amino acids. Genes Dev. 4:1357-1364.
43. Olsen, H. S., P. Nelbock, A. W. Cochrane, and C. A. Rosen. 1990. Secondary structure is the major determinant for interaction of HIV rev protein with RNA. Science 247:845-848.
44. Pollard, V. W., and M. H. Malim. 1998. The HIV-1 Rev protein. Annu. Rev. Microbiol. 52:491-532.
45. Rosen, C. A., E. Terwilliger, A. Dayton, J. G. Sodroski, and W. A. Haseltine. 1988. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc. Natl. Acad. Sci. U. S. A. 85:2071-2075.
46. Shuck-Lee, D., et al. 2008. Heterocyclic compounds that inhibit Rev-RRE function and human immunodeficiency virus type 1 replication. Antimicrob. Agents Chemother. 52:3169-3179.
47. Symensma, T. L., L. Giver, M. Zapp, G. B. Takle, and A. D. Ellington. 1996. RNA aptamers selected to bind human immunodeficiency virus type 1 Rev in vitro are Rev responsive in vivo. J. Virol. 70:179-187.
48. Tan, R., L. Chen, J. A. Buettner, D. Hudson, and A. D. Frankel. 1993. RNA recognition by an isolated alpha helix. Cell 73:1031-1040.
49. Tan, R., and A. D. Frankel. 1994. Costabilization of peptide and RNA structure in an HIV Rev peptide-RRE complex. Biochemistry 33:14579-14585.
50. Tiley, L. S., M. H. Malim, H. K. Tewary, P. G. Stockley, and B. R. Cullen. 1992. Identification of a high-affinity RNA-binding site for the human immunodeficiency virus type 1 Rev protein. Proc. Natl. Acad. Sci. U. S. A. 89:758-762. (Erratum, 89:1997.)
51. Wehrly, K., and B. Chesebro. 1997. p24 antigen capture assay for quantification of human immunodeficiency virus using readily available inexpensive reagents. Methods 12:288-293. (Pubitemid 27371252)
52. Wu, Y., M. H. Beddall, and J. W. Marsh. 2007. Rev-dependent indicator T cell line. Curr. HIV Res. 5:394-402.
53. Zapp, M. L., and M. R. Green. 1989. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 342:714-716.
54. Zapp, M. L., T. J. Hope, T. G. Parslow, and M. R. Green. 1991. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: a dual function for an arginine-rich binding motif. Proc. Natl. Acad. Sci. U. S. A. 88:7734-7748.