Protein structure and oligomerization are important for the formation of export-competent HIV-1 Rev-RRE complexes

Protein Science

Volumn 17, Issue 3, 2008, Pages 420-430

  Edgcomb, Stephen P ^a   Aschrafi, Angelique ^a   Kompfner, Elizabeth ^a   Williamson, James R ^a   Gerace, Larry ^a   Hennig, Mirko ^a,b,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

HIV 1; Nuclear export; Rev; RRE; Viral latency

Indexed keywords

MESSENGER RNA; OLIGOMER; REV PROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CIRCULAR DICHROISM; CORRELATION ANALYSIS; DNA RESPONSIVE ELEMENT; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHILICITY; HYDROPHOBICITY; NONHUMAN; NUCLEAR EXPORT SIGNAL; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REV RESPONSE ELEMENT; RNA BINDING; RNA TRANSLATION; RNA TRANSPORT; VIRUS LATENCY;

AMINO ACID SEQUENCE; BINDING SITES; GENES, REPORTER; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA TRANSPORT; RNA, MESSENGER; RNA, VIRAL; SEQUENCE ALIGNMENT; VARIATION (GENETICS);

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 39549100997     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073246608     Document Type: Article

References (55)

1. Andersen, N.H., Liu, Z., and Prickett, K.S. 1996. Efforts toward deriving the CD spectrum of a 3(10) helix in aqueous medium. FEBS Lett. 399: 47-52.
2. Andrade, M.A., Chacon, P., Merelo, J.J., and Moran, F. 1993. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6: 383-390.
3. Auer, M., Gremlich, H.U., Seifert, J.M., Daly, T.J., Parslow, T.G., Casari, G., and Gstach, H. 1994. Helix-loop-helix motif in HIV-1 Rev. Biochemistry 33: 2988-2996.
4. Aukrust, I., Evensen, L., Hollas, H., Berven, F., Atkinson, R.A., Trave, G., Flatmark, T., and Vedeler, A. 2006. Engineering, biophysical characterisation and binding properties of a soluble mutant form of annexin A2 domain IV that adopts a partially folded conformation. J. Mol. Biol. 363: 469-481.
5. Bevec, D., Jaksche, H., Oft, M., Wohl, T., Himmelspach, M., Pacher, A., Schebesta, M., Koettnitz, K., Dobrovnik, M., Csonga, R., et al. 1996. Inhibition of HIV-1 replication in lymphocytes by mutants of the Rev cofactor eIF-5A. Science 271: 1858-1860.
6. Blanco, F.J., Hess, S., Pannell, L.K., Rizzo, N.W., and Tycko, R. 2001. Solid-state NMR data support a helix-loop-helix structural model for the N-terminal half of HIV-1 Rev in fibrillar form. J. Mol. Biol. 313: 845-859.
7. Bobbitt, K.R., Addo, M.M., Altfeld, M., Filzen, T., Onafuwa, A.A., Walker, B.D., and Collins, K.L. 2003. Rev activity determines sensitivity of HIV-1-infected primary T cells to CTL killing. Immunity 18: 289-299.
8. Bogerd, H. and Greene, W.C. 1993. Dominant negative mutants of human T-cell leukemia virus type I Rex and human immunodeficiency virus type 1 Rev fail to multimerize in vivo. J. Virol. 67: 2496-2502.
9. Bohnlein, E., Berger, J., and Hauber, J. 1991. Functional mapping of the human immunodeficiency virus type 1 Rev RNA binding domain: New insights into the domain structure of Rev and Rex. J. Virol. 65: 7051-7055.
10. Brice, P.C., Kelley, A.C., and Butler, P.J. 1999. Sensitive in vitro analysis of HIV-1 Rev multimerization. Nucleic Acids Res. 27: 2080-2085.
11. Churchill, M.J., Chiavaroli, L., Wesselingh, S.L., and Gorry, P.R. 2007. Persistence of attenuated HIV-1 rev alleles in an epidemiologically linked cohort of long-term survivors infected with nef-deleted virus. Retrovirology 4: 43. doi: 10.1186/1742-4690-4-43.
12. Cole, J.L., Gehman, J.D., Shafer, J.A., and Kuo, L.C. 1993. Solution oligomerization of the rev protein of HIV-1: Implications for function. Biochemistry 32: 11769-11775.
13. Daly, T.J., Rusche, J.R., Maione, T.E., and Frankel, A.D. 1990. Circular dichroism studies of the HIV-1 Rev protein and its specific RNA binding site. Biochemistry 29: 9791-9795.
14. de Oliveira, T., Salemi, M., Gordon, M., Vandamme, A.M., van Rensburg, E.J., Engelbrecht, S., Coovadia, H.M., and Cassol, S. 2004. Mapping sites of positive selection and amino acid diversification in the HIV genome: An alternative approach to vaccine design? Genetics 167: 1047-1058.
15. Fang, J., Acheampong, E., Dave, R., Wang, F., Mukhtar, M., and Pomerantz, R.J. 2005. The RNA helicase DDX1 is involved in restricted HIV-1 Rev function in human astrocytes. Virology 336: 299-307.
16. Greenfield, N.J. 1996. Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal. Biochem. 235: 1-10.
17. Hammerschmid, M., Palmeri, D., Ruhl, M., Jaksche, H., Weichselbraun, I., Bohnlein, E., Malim, M.H., and Hauber, J. 1994. Scanning mutagenesis of the arginine-rich region of the human immunodeficiency virus type 1 Rev trans activator. J. Virol. 68: 7329-7335.
18. Havlin, R.H., Blanco, F.J., and Tycko, R. 2007. Constraints on protein structure in HIV-1 Rev and Rev-RNA supramolecular assemblies from two-dimensional solid state nuclear magnetic resonance. Biochemistry 46: 3586-3593.
19. Hope, T.J. 1999. The ins and outs of HIV Rev. Arch. Biochem. Biophys. 365: 186-191.
20. Hope, T.J., McDonald, D., Huang, X.J., Low, J., and Parslow, T.G. 1990. Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: Essential residues near the amino terminus. J. Virol. 64: 5360-5366.
21. Hope, T.J., Bond, B.L., McDonald, D., Klein, N.P., and Parslow, T.G. 1991. Effector domains of human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type I Rex are functionally interchangeable and share an essential peptide motif. J. Virol. 65: 6001-6007.
22. Hua, J., Caffrey, J.J., and Cullen, B.R. 1996. Functional consequences of natural sequence variation in the activation domain of HIV-1 Rev. Virology 222: 423-429.
23. Iversen, A.K., Shpaer, E.G., Rodrigo, A.G., Hirsch, M.S., Walker, B.D., Sheppard, H.W., Merigan, T.C., and Mullins, J.I. 1995. Persistence of attenuated rev genes in a human immunodeficiency virus type 1-infected asymptomatic individual. J. Virol. 69: 5743-5753.
24. Jain, C. and Belasco, J.G. 1996. A structural model for the HIV-1 Rev-RRE complex deduced from altered-specificity Rev variants isolated by a rapid genetic strategy. Cell 87: 115-125.
25. Jain, C. and Belasco, J.G. 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.
26. Madore, S.J., Tiley, L.S., Malim, M.H., and Cullen, B.R. 1994. Sequence requirements for Rev multimerization in vivo. Virology 202: 186-194.
27. Malim, M.H. and Cullen, B.R. 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.
28. Malim, M.H., Bohnlein, S., Hauber, J., and Cullen, B.R. 1989a. Functional dissection of the HIV-1 Rev trans-activator - derivation of a trans-dominant repressor of Rev function. Cell 58: 205-214.
29. Malim, M.H., Hauber, J., Le, S.Y., Maizel, J.V., and Cullen, B.R. 1989b. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338: 254-257.
30. Mann, D.A., Mikaélian, I., Zemmel, R.W., Green, S.M., Lowe, A.D., Kimura, T., Singh, M., Butler, P.J., Gait, M.J., and Karn, J. 1994. A molecular rheostat. Co-operative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression. J. Mol. Biol. 241: 193-207.
31. Mirny, L.A. and Shakhnovich, E.I. 1999. Universally conserved positions in protein folds: Reading evolutionary signals about stability, folding kinetics and function. J. Mol. Biol. 291: 177-196.
32. Novitsky, V., Smith, U.R., Gilbert, P., McLane, M.F., Chigwedere, P., Williamson, C., Ndung'u, T., Klein, I., Chang, S.Y., Peter, T., et al. 2002. Human immunodeficiency virus type 1 subtype C molecular phylogeny: Consensus sequence for an AIDS vaccine design? J. Virol. 76: 5435-5451.
33. Oelrichs, R., Tsykin, A., Rhodes, D., Solomon, A., Ellett, A., McPhee, D., and Deacon, N. 1998. Genomic sequence of HIV type 1 from four members of the Sydney Blood Bank Cohort of long-term nonprogressors. AIDS Res. Hum. Retroviruses 14: 811-814.
34. Papathanasopoulos, M.A., Patience, T., Meyers, T.M., McCutchan, F.E., and Morris, L. 2003. Full-length genome characterization of HIV type 1 subtype C isolates from two slow-progressing perinatally infected siblings in South Africa. AIDS Res. Hum. Retroviruses 19: 1033-1037.
35. Paulucci, A.A., Hicks, L., Machado, A., Miranda, M.T., Kay, C.M., and Farah, C.S. 2002. Specific sequences determine the stability and cooperativity of folding of the C-terminal half of tropomyosin. J. Biol. Chem. 277: 39574-39584.
36. Pollard, V.W. and Malim, M.H. 1998. The HIV-1 Rev protein. Annu. Rev. Microbiol. 52: 491-532.
37. Pomerantz, R.J., Trono, D., Feinberg, M.B., and Baltimore, D. 1990. Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: A molecular model for latency. Cell 61: 1271-1276.
38. Reddy, T.R., Xu, W., Mau, J.K., Goodwin, C.D., Suhasini, M., Tang, H., Frimpong, K., Rose, D.W., and Wong-Staal, F. 1999. Inhibition of HIV replication by dominant negative mutants of Sam68, a functional homolog of HIV-1 Rev. Nat. Med. 5: 635-642.
39. Ruhl, M., Himmelspach, M., Bahr, G.M., Hammerschmid, F., Jaksche, H., Wolff, B., Aschauer, H., Farrington, G.K., Probst, H., Bevec, D., et al. 1993. Eukaryotic initiation factor 5A is a cellular target of the human immunodeficiency virus type 1 Rev activation domain mediating trans-activation. J. Cell Biol. 123: 1309-1320.
40. Sanchez-Velar, N., Udofia, E.B., Yu, Z., and 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.
41. Soros, V. and Cochrane, A. 2001. Alterations in HIV-1 Rev transport in response to cell stress. Virology 280: 199-210.
42. Szebeni, A., Mehrotra, B., Baumann, A., Adam, S.A., Wingfield, P.T., and Olson, M.O. 1997. Nucleolar protein B23 stimulates nuclear import of the HIV-1 Rev protein and NLS-conjugated albumin. Biochemistry 36: 3941-3949.
43. Szilvay, A.M., Brokstad, K.A., Boe, S.O., Haukenes, G., and Kalland, K.H. 1997. Oligomerization of HIV-1 Rev mutants in the cytoplasm and during nuclear import. Virology 235: 73-81.
44. Tan, R. and Frankel, A.D. 1994. Costabilization of peptide and RNA structure in an HIV Rev peptide-RRE complex. Biochemistry 33: 14579-14585.
45. Tan, R., Chen, L., Buettner, J.A., Hudson, D., and Frankel, A.D. 1993. RNA recognition by an isolated α helix. Cell 73: 1031-1040.
46. Thomas, S.L., Hauber, J., and Casari, G. 1997. Probing the structure of the HIV-1 Rev trans-activator protein by functional analysis. Protein Eng. 10: 103-107.
47. Thomas, S.L., Oft, M., Jaksche, H., Casari, G., Heger, P., Dobrovnik, M., Bevec, D., and Hauber, J. 1998. Functional analysis of the human immunodeficiency virus type 1 Rev protein oligomerization interface. J. Virol. 72: 2935-2944.
48. Trikha, R. and Brighty, D.W. 2005. Phenotypic analysis of human immunodeficiency virus type 1 Rev trimerization-interface mutants in human cells. J. Gen. Virol. 86: 1509-1513.
49. Valdar, W.S. 2002. Scoring residue conservation. Proteins 48: 227-241.
50. Vaz, D.C., Rodrigues, J.R., Sebald, W., Dobson, C.M., and Brito, R.M. 2006. Enthalpic and entropic contributions mediate the role of disulfide bonds on the conformational stability of interleukin-4. Protein Sci. 15: 33-44.
51. Whitmore, L. and Wallace, B.A. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32: W668-W673. doi: 10.1093/nar/gkh371.
52. Wingfield, P.T., Stahl, S.J., Payton, M.A., Venkatesan, S., Misra, M., and Steven, A.C. 1991. HIV-1 Rev expressed in recombinant Escherichia coli: Purification, polymerization, and conformational properties. Biochemistry 30: 7527-7534.
53. Wodrich, H., Schambach, A., and Krausslich, H.G. 2000. Multiple copies of the Mason-Pfizer monkey virus constitutive RNA transport element lead to enhanced HIV-1 Gag expression in a context-dependent manner. Nucleic Acids Res. 28: 901-910.
54. Yedavalli, V.S., Neuveut, C., Chi, Y.H., Kleiman, L., and Jeang, K.T. 2004. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119: 381-392.
55. Zhai, X., Srivastava, A., Drummond, D.C., Daleke, D., and Lentz, B.R. 2002. Phosphatidylserine binding alters the conformation and specifically enhances the cofactor activity of bovine factor Va. Biochemistry 41: 5675-5684.