A long-awaited structure is rev-ealed

Viruses

Volumn 3, Issue 5, 2011, Pages 484-492

  Hammarskjold, Marie Louise ^a   Rekosh, David ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Hiv 1; Nuclear cytoplasmic export; Protein structure; Rev; Rna export; Rna protein binding; Rre; X ray crystallography

Indexed keywords

MESSENGER RNA; REV PROTEIN;

ARTICLE; COMPLEX FORMATION; DNA RESPONSIVE ELEMENT; HUMAN IMMUNODEFICIENCY VIRUS; HYDROPHOBICITY; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA BINDING; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

DIMERIZATION; HIV INFECTIONS; HIV-1; HUMANS; PROTEIN BINDING; RESPONSE ELEMENTS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA, VIRAL;

EID: 79957861435     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v3050484     Document Type: Article

References (61)

1. Daugherty, M.D.; D'Orso, I.; Frankel, A.D. A solution to limited genomic capacity: Using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA. Mol. Cell 2008, 31, 824-834.
2. Daugherty, M.D.; Booth, D.S.; Jayaraman, B.; Cheng, Y.; Frankel, A.D. HIV Rev response element (RRE) directs assembly of the Rev homooligomer into discrete asymmetric complexes. Proc. Nat. Acad. Sci. U. S. A. 2010, 107, 12481-12486.
3. Daugherty, M.D.; Liu, B.; Frankel, A.D. Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat. Struct. Mol. Biol. 2010, 17, 1337-1342.
4. DiMattia, M.A.; Watts, N.R.; Stahl, S.J.; Rader, C.; Wingfield, P.T.; Stuart, D.I.; Steven, A.C.; Grimes, J.M. Implications of the HIV-1 Rev dimer structure at 3.2 a resolution for multimeric binding to the Rev response element. Proc. Nat. Acad. Sci. U. S. A. 2010, 107, 5810-5814.
5. Feinberg, M.B.; Jarrett, R.F.; Aldovini, A.; Gallo, R.C.; Wong-Staal, F. HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell 1986, 46, 807-817.
6. Sodroski, J.; Goh, W.C.; Rosen, C.; Dayton, A.; Terwilliger, E.; Haseltine, W. A second post-transcriptional trans-activator gene required for HTLV-III replication. Nature 1986, 321, 412-417.
7. Pollard, V.W.; Malim, M.H. The HIV-1 Rev protein. Annu. Rev. Microbiol. 1998, 52, 491-532.
8. Daly, T.J.; Cook, K.S.; Gray, G.S.; Maione, T.E.; Rusche, J.R. Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 1989, 342, 816-819.
9. Zapp, M.L.; Green, M.R. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 1989, 342, 714-716.
10. Cochrane, A.W.; Chen, C.H.; Rosen, C.A. Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the Env mRNA. Proc. Nat. Acad. Sci. U. S. A. 1990, 87, 1198-1202.
11. Daefler, S.; Klotman, M.E.; Wong, S.F. Trans-activating Rev protein of the human immunodeficiency virus 1 interacts directly and specifically with its target RNA. Proc. Nat. Acad. Sci. U. S. A. 1990, 87, 4571-4575.
12. Heaphy, S.; Dingwall, C.; Ernberg, I.; Gait, M.J.; Green, S.M.; Karn, J.; Lowe, A.D.; Singh, M.; Skinner, M.A. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 1990, 60, 685-693.
13. Holland, S.M.; Ahmad, N.; Maitra, R.K.; Wingfield, P.; Venkatesan, S. Human immunodeficiency virus Rev protein recognizes a target sequence in Rev-responsive element RNA within the context of RNA secondary structure. J. Virol. 1990, 64, 5966-5975.
14. Malim, M.H.; Tiley, L.S.; McCarn, D.F.; Rusche, J.R.; Hauber, J.; Cullen, B.R. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 1990, 60, 675-683.
15. Rosen, C.A.; Terwilliger, E.; Dayton, A.; Sodroski, J.G.; Haseltine, W.A. Intragenic cis-acting Art gene-responsive sequences of the human immunodeficiency virus. Proc. Nat. Acad. Sci. U. S. A. 1988, 85, 2071-2075.
16. Hadzopoulou-Cladaras, M.; Felber, B.K.; Cladaras, C.; Athanassopoulos, A.; Tse, A.; Pavlakis, G.N. 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. 1989, 63, 1265-1274.
17. Hammarskjöld, M.-L.; Heimer, J.; Hammarskjöld, B.; Sangwan, I.; Albert, L.; Rekosh, D. Regulation of human immunodeficiency virus env expression by the Rev gene product. J. Virol. 1989, 63, 1959-1966.
18. Malim, M.H.; Hauber, J.; Le, S.V.; Maizel, J.V.; Cullen, B.R. The HIV-1 Rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989, 338, 254-257.
19. Felber, B.K.; Hadzopoulou-Cladaras, M.; Cladaras, C.; Copeland, T.; Pavlakis, G.N. Rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Nat. Acad. Sci. U. S. A. 1989, 86, 1496-1499.
20. Legrain, P.; Seraphin, B.; Rosbash, M. Early commitment of yeast pre-mRNA to the spliceosome pathway. Mol. Cell. Biol. 1988, 8, 3755-3760.
21. Chang, D.D.; Sharp, P.A. Regulation by HIV Rev depends upon recognition of splice sites. Cell 1989, 59, 789-795.
22. Hope, T.J.; Bond, B.L.; McDonald, D.; Klein, N.P.; Parslow, T.G. 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. 1991, 65, 6001-6007.
23. Fischer, U.; Huber, J.; Boelens, W.C.; Mattaj, I.W.; Luhrmann, R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 1995, 82, 475-483.
24. Wen, W.; Meinkoth, J.L.; Tsien, R.Y.; Taylor, S.S. Identification of a signal for rapid export of proteins from the nucleus. Cell 1995, 82, 463-473.
25. Meyer, B.E.; Malim, M.H. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 1994, 8424, 1538-1547.
26. Fornerod, M.; Ohno, M.; Yoshida, M.; Mattaj, I.W. Crm1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90, 1051-1060.
27. Neville, M.; Stutz, F.; Lee, L.; Davis, L.I.; Rosbash, M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 1997, 7, 767-775.
28. Ossareh-Nazari, B.; Bachelerie, F.; Dargemont, C. Evidence for a role of Crm1 in signal-mediated nuclear protein export. Science 1997, 278, 141-144.
29. Fukuda, M.; Asano, S.; Nakamura, T.; Adachi, M.; Yoshida, M.; Yanagida, M.; Nishida, E. Crm1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 1997, 390, 308-311.
30. M.-L. Regulation of retroviral rna export. Semin. Cell Dev. Biol. 1997, 8, 83-90.
31. Purcell, D.F.; Martin, M.A. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 1993, 67, 6365-6378.
32. Li, Y.; Bor, Y.C.; Misawa, Y.; Xue, Y.; Rekosh, D.; Hammarskjold, M.L. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 2006, 443, 234-237.
33. J.J.U., S.; Abraham, B.; Clatterbuck, S.; Beemon, K. L. Tap and Dbp5, but not Gag, are involved in DR-mediated nuclear export of unspliced rous sarcoma virus RNA. Virology 2007, 363, 376-386.
34. Bray, M.; Prasad, S.; Dubay, J.W.; Hunter, E.; Jeang, K.T.; Rekosh, D.; Hammarskjold, M.L. A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent. Proc. Nat. Acad. Sci. U. S. A. 1994, 91, 1256-1260.
35. Ernst, R.; Bray, M.; Rekosh, D.; Hammarskjöld, M.-L. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol. Cell. Biol. 1997, 17, 135-144.
36. Hidaka, M.; Inoue, J.; Yoshida, M.; Seiki, M. Post-transcriptional regulator (Rex) of HTLV-1 initiates expression of viral structural proteins but suppresses expression of regulatory proteins. EMBO J. 1988, 7, 519-523.
37. Seiki, M.; Inoue, J.; Hidaka, M.; Yoshida, M. Two cis-acting elements responsible for posttranscriptional trans-regulation of gene expression of human T-cell leukemia virus type 1. Proc. Nat. Acad. Sci. U. S. A. 1988, 85, 7124-7128.
38. Mertz, J.A.; Simper, M.S.; Lozano, M.M.; Payne, S.M.; Dudley, J.P. Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J. Virol. 2005, 79, 14737-14747.
39. Martarano, L.; Stephens, R.; Rice, N.; Derse, D. Equine infectious anemia virus trans-regulatory protein Rev controls viral mRNA stability, accumulation, and alternative splicing. J. Virol. 1994, 68, 3102-3111.
40. Fridell, R.A.; Partin, K.M.; Carpenter, S.; Cullen, B.R. Identification of the activation domain of equine infectious anemia virus Rev. J. Virol. 1993, 67, 7317-7323.
41. Caporale, M.; Arnaud, F.; Mura, M.; Golder, M.; Murgia, C.; Palmarini, M. The signal peptide of a simple retrovirus envelope functions as a posttranscriptional regulator of viral gene expression. J. Virol. 2009, 83, 4591-4604.
42. Hofacre, A.; Nitta, T.; Fan, H. Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of Gag protein. J. Virol. 2009, 83, 12483-12498.
43. Nitta, T.; Hofacre, A.; Hull, S.; Fan, H. Identification and mutational analysis of a Rej response element in Jaagsiekte sheep retrovirus RNA. J. Virol. 2009, 83, 12499-12511.
44. Bodem, J.; Schied, T.; Gabriel, R.; Rammling, M.; Rethwilm, A. Foamy virus nuclear RNA export is distinct from that of other retroviruses. J. Virol. 2011, 85, 2333-2341.
45. Cook, K.S.; Fisk, G.J.; Hauber, J.; Usman, N.; Daly, T.J.; Rusche, J.R. Characterization of HIV-1 Rev protein: Binding stoichiometry and minimal RNA substrate. Nucleic Acids Res. 1991, 19, 1577-1583.
46. Kjems, J.; Brown, M.; Chang, D.D.; Sharp, P.A. Structural analysis of the interaction between the human immunodeficiency virus rev protein and the Rev response element. Proc. Nat. Acad. Sci. U. S. A. 1991, 88, 683-687.
47. Madore, S.J.; Tiley, L.S.; Malim, M.H.; Cullen, B.R. Sequence requirements for Rev multimerization in vivo. Virology 1994, 202, 186-194.
48. Zapp, M.L.; Hope, T.J.; Parslow, T.G.; Green, M.R. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: A dual function for an arginine-rich binding motif. Proc. Nat. Acad. Sci. U. S. A. 1991, 88, 7734-7748.
49. Olsen, H.S.; Cochrane, A.W.; Dillon, P.J.; Nalin, C.M.; Rosen, C.A. 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. 1990, 4, 1357-1364.
50. Pond, S.J.; Ridgeway, W.K.; Robertson, R.; Wang, J.; Millar, D.P. HIV-1 Rev protein assembles on viral RNA one molecule at a time. Proc. Nat. Acad. Sci. U. S. A. 2009, 106, 1404-1408.
51. Charpentier, B.; Stutz, F.; Rosbash, M. A dynamic in vivo view of the HIV-1 Rev-RRE interaction. J. Mol. Biol. 1997, 266, 950-962.
52. Bartel, D.P.; Zapp, M.L.; Green, M.R.; Szostak, J.W. HIV-1 Rev regulation involves recognition of non-watson-crick base pairs in viral RNA. Cell 1991, 67, 529-536.
53. Battiste, J.L.; Tan, R.; Frankel, A.D.; Williamson, J.R. Binding of an HIV Rev peptide to Rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry 1994, 33, 2741-2747.
54. Battiste, J.L.; Mao, H.; Rao, N.S.; Tan, R.; Muhandiram, D.R.; Kay, L.E.; Frankel, A.D.; Williamson, J.R. Alpha helix-RNA major groove recognition in an HIV-1 Rev peptide-RRE RNA complex. Science 1996, 273, 1547-1551.
55. Tan, R.; Frankel, A.D. Costabilization of peptide and RNA structure in an HIV Rev peptide-RRE complex. Biochemistry 1994, 33, 14579-14585.
56. Cole, J.L.; Gehman, J.D.; Shafer, J.A.; Kuo, L.C. Solution oligomerization of the Rev protein of HIV-1. Biochemistry 1993, 32, 11769-11775.
57. Wingfield, P.T.; Stahl, S.J.; Payton, M.A.; Venkatesan, S.; Misra, M.; Steven, A.C. HIV-1 Rev expressed in recombinant escherichia coli: Purification, polymerization, and conformational properties. Biochemistry 1991, 30, 7527-7534.
58. Heaphy, S.; Finch, J.T.; Gait, M.J.; Karn, J.; Singh, M. Human immunodeficiency virus type 1 regulator of virion expression, Rev, forms nucleoprotein filaments after binding to a purine-rich "bubble" located within the Rev-responsive region of viral mRNAs. Proc. Nat. Acad. Sci. U. S. A. 1991, 88, 7366-7370.
59. Jain, C.; Belasco, J.G. A structural model for the HIV-1 Rev-RRE complex deduced from altered-specificity Rev variants isolated by a rapid genetic strategy. Cell 1996, 87, 115-125.
60. Jain, C.; Belasco, J.G. Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants. Mol. Cell 2001, 7, 603-614.
61. Zhou, P.; Wagner, G. Overcoming the solubility limit with solubility enhancement tags: Successful applications in biomolecular nmr studies. J. Biomol. NMR 2009, 46, 23-31.