A dynamic in vivo view of the HIV-I Rev-RRE interaction

Journal of Molecular Biology

Volumn 266, Issue 5, 1997, Pages 950-962

  Charpentier, Bruno ^a   Stutz, Françoise ^a   Rosbash, Michael ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

HIV 1; In vivo probing; Oligomerization; Rev; RRE

Indexed keywords

REV PROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA BINDING; STRUCTURAL GENE; VIRUS TYPING;

EID: 0031567148     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0858     Document Type: Article

References (61)

1. Bartel, D. P., Zapp, M. L., Green, M. R. & Szostak, J. W. (1991). HIV-1 rev regulation involves recognition of non-Watson-Crick base pairs in viral RNA. Cell, 67, 529-536.
2. Battiste, J. L., Tan, R., Frankel, A. D. & Williamson, J. R. (1994). Binding of an HIV rev peptide to rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry, 33, 2741-2747.
3. Battiste, J. L., Mao, H., Rao, N. S., Tan, R., Muhandiram, D. R., Kay, L. E., Frankel, A. D. & Williamson, J. R. (1996). α Helix-RNA major groove recognition in an HIV-1 Rev peptide-RRE RNA complex. Science, 273, 1547-1551.
4. Berger, J., Aepinus, C., Dobrovnik, M., Fleckenstein, B., Hauber, J. & Bohnlein, E. (1991). Mutational analysis of functional domains in the HIV-1 rev transregulatory protein. Virology, 183, 630-635.
5. Brighty, D. W. & Rosenberg, M. (1994). A cis-acting repressive sequence that overlaps the Rev-responsive element of human immunodeficiency virus type 1 regulates nuclear retention of env mRNAs independently of known splice signals. Proc. Natl Acad. Sci. USA, 91, 8314-8318.
6. Charpentier, B. & Rosbash, M. (1996). Intramolecular structure in yeast introns aids the early steps of in vitro spliceosome assembly. RNA, 2, 509-522.
7. Cochrane, A. W., Chen, C.-H. & Rosen, C. A. (1990). Specific interaction of the human immunodeficiency virus rev protein with a structured region in the env mRNA. Proc. Natl Acad. Sci. USA, 87, 1198-1202.
8. Cullen, B. R. (1992). Mechanism of action of regulatory proteins encoded by complex retroviruses. Microbiol. Rev. 56, 375-394.
9. D'Alesio, J. M. (1982). Gel Electrophoresis of Nucleic Acids: A Practical Approach (Rickwood, D. & Hames, B. D., eds), IRL Press, Washington DC.
10. Daly, T. J., Cook, K. S., Gray, G. S., Maione, T. E. & Rusche, J. R. (1989). Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature, 342, 816-819.
11. Daly, T. J., Doten, R. C., Rusche, J. R. & Auer, M. (1995). The amino-terminal domain of HIV-1 rev is required for discrimination of the RRE from non-specific RNA. J. Mol. Biol. 253, 243-258.
12. Dayton, E. T., Powell, D. M. & Dayton, A. I. (1989). Functional analysis of CAR, the target sequence for the rev protein. Science, 246, 1625-1629.
13. Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J.-P. & Ehresmann, B. (1987). Probing the structure of RNAs in solution. Nucl. Acids Res. 15, 9109-9128.
14. Emerman, M., Vazeux, R. & Peden, K. (1989). The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell, 57, 1155-1165.
15. Fischer, U., Meyer, S., Teufel, M., Heckel, C., Luhrmann, R. & Rautmann, G. (1994). Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J. 13, 4105-4112.
16. Fridell, R. A., Bogerd, H. P. & Cullen, B. R. (1996). Nuclear export of late HIV-1 mRNAs occurs via a cellular protein export pathway. Proc. Natl Acad. Sci. USA, 93, 4421-4424.
17. Gait, M. J. & Karn, J. (1993). RNA recognition by the human immunodeficiency virus tat and rev proteins. Trends Biol. Sci. 18, 255-259.
18. Hadzopoulo-Cladaras, M., Felber, B. K., Cladaras, C., Athanassopoulos, A., Tse, A. & Pavlakis, G. N. (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.
19. Hammarskjöld, M.-L., Heimer, J., Hammarskjold, B., Sangwan, I., Albert, L. & Rekosh, D. (1989). Regulation of human immunodeficiency virus env gene expression by the rev gene product. J. Virol. 63, 1959-1966.
20. Harris, K. A. J., Crothers, D. M. & Ullu, E. (1995). In vivo structural analysis of spliced leader RNAs in Trypanosoma brucei and Leptomonas collosoma: a flexible structure that is independent of cap4 methylations. RNA, 1, 351-362.
21. Heaphy, S., Dingwall, C., Ernberg, I., Gait, M. J., Green, S. M., Karn, J., Lowe, A. D., Singh, M. & Skinner, M. A. (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.
22. Heaphy, S., Finch, J. T., Gait, M. J., Karn, J. & Singh, M. (1991). 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. Natl Acad. Sci. USA, 88, 7366-7370.
23. Holland, S. M., Chavez, M., Gerstberger, S. & Venkatesan, S. (1992). A specific sequence with a bulged guanosine residue(s) in a stem-bulge-stem structure of Rev-responsive element RNA is required for trans activation by human immunodeficiency virus type 1 Rev. J. Virol. 66, 3699-3706.
24. Hope, T. J., Bond, B. C., McDonald, D., Klein, N. P. & Parslow, T. G. (1991). Effector domains of human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type 1 Rex are functionally interchangeable and share an essential peptide motif. J. Virol. 65, 6001-6007.
25. Huang, X., Hope, T. J., Bond, B. L., McDonald, D., Grahl, K. & Parslow, T. G. (1991). Minimal Rev-response element for type 1 human immunodeficiency virus. J. Virol. 65(4), 2131-2134.
26. Inoue, T. & Cech, T. R. (1985). Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc. Natl Acad. Sci. USA, 82, 648-652.
27. Ito, H., Fukuda, Y., Murata, K. & Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
28. Iwai, S., Pritchard, C., Mann, D. A., Karn, J. & Gait, M. J. (1992). Recognition of the high affinity binding site in rev-response element RNA by the human immunodeficiency virus type-1 ev protein. Nucl. Acids Res. 20, 6465-6472.
29. Jain, C. & 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, 1-20.
30. Kalland, K.-H., Szilvay, A. M., Brokstad, K. A., Saetrevik, W. & Haukenes, G. (1994). The human immunodeficiency virus type 1 Rev protein shuttles between the cytoplasm and nuclear compartments. Mol. Cell. Biol. 14, 7436-7444.
31. 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.
32. Kjems, J., Calnan, B. J., Frankel, A. D. & Sharp, P. A. (1992). Specific binding of a basic peptide from HIV-1 Rev. EMBO J, 11(3), 1119-1129.
33. Leclerc, F., Cedergren, R. & Ellington, A. D. (1994). A three-dimensional model of the rev-binding element of HIV-1 derived from analyses of aptamers. Struct. Biol. 1, 293-300.
34. Legrain, P. & Rosbash, M. (1989). Some cis-and transacting mutants for splicing target pre-mRNA to the cytoplasm. Cell, 57, 573-583.
35. Madore, S. J., Tiley, L. S., Malim, M. H. & Cullen, B. R. (1994). Sequence requirements for Rev multimerization in vivo. Virology, 202, 186-194.
36. Maldarelli, F., Martin, M. A. & Strebel, K. (1991). Identification of posttranscriptionally active inhibitory sequences in human immunodeficiency virus type 1 RNA: novel level of gene regulation. J. Virol. 65, 5732-5743.
37. Malim, M. H. & 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.
38. Malim, M. H., Böhnlein, S., Hauber, J. & 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.
39. Malim, M. H., Hauber, J., Le, S.-Y., Maizel, J. V. & 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.
40. Malim, M. H., Tiley, L. S., McCarn, D. F., Rusche, J. R., Hauber, J. & Cullen, B. R. (1990). HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell, 60, 675-683.
41. Malim, M. H., McCarn, D. F., Tiley, L. S. & Cullen, B. R. (1991). Mutational definition of the human immunodeficiency virus type I Rev activation domain. J. Virol. 65, 4248-4254.
42. Mann, D. A., Mikaelian, I., Zemmel, R. W., Green, S. M., Lowe, A. D., Kimura, T., Singh, M., Butler, P. J. G., Gait, M. J. & Karn, J. (1994). 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.
43. Mermer, B., Felber, B. K., Campbell, M. & Pavlakis, G. N. (1990). Identification of trans-dominant HIV-1 rev protein mutants by direct transfer of bacterially produced proteins into human cells. Nucl. Acids Res. 18, 2037-2044.
44. Meyer, B. E. & Malim, M. H. (1994). The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 8, 1538-1547.
45. Peterson, R. D., Bartel, D. P., Szostak, J. W., Horvath, S. J. & Feigon, J. (1994). H NMR studies of the high-affinity rev binding site of the rev responsive element of HIV-1 mRNA: base pairing in the core binding element. Biochemistry, 33, 5357-5366.
46. Pikielny, C. W. & Rosbash, M. (1985). mRNA splicing efficiency in yeast and the contribution of nonconserved sequences. Cell, 41, 119-126.
47. Rosen, C. A., Terwilliger, E., Dayton, A., Sodroski, J. G. & Haseltine, W. (1988). Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc. Natl Acad. Sci. USA, 85, 2071-2075.
48. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). In Molecular Cloning: A Laboratory Manual 2nd edit., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Séraphin, B. & Rosbash, M. (1991). The yeast branch-point sequence is not required for the formation of a stable U1 snRNP-pre-mRNA complex and is recognized in the absence of U2 snRNA. EMBO J. 10, 1209-1216.
50. Stutz, F. & Rosbash, M. (1994). A functional interaction between Rev and yeast pre-mRNA is related to splicing complex formation. EMBO J. 13, 4096-4104.
51. Stutz, F., Neville, M. & Rosbash, M. (1995). Identification of a novel nuclear pore-associated protein as a functional target of the HIV-1 Rev protein in yeast. Cell, 82, 495-506.
52. Tan, R., Chen, L., Buettner, J. A., Hudson, D. & Frankel, A. D. (1993). RNA recognition by an isolated alpha-helix. Cell, 7, 1031-1040.
53. Tiley, L. S., Malim, M. H., Tewary, H. K., Stockley, P. G. & Cullen, B. R. (1992). Identification of a high-affinity RNA-binding site for the human immunodeficiency virus type 1 Rev protein. Proc. Natl Acad. Sci. USA, 89, 758-762.
54. Wen, W., Meinkoth, J. L., Tsien, R. Y. & Taylor, S. S. (1995). Identification of a signal for rapid export of proteins from the nucleus. Cell, 82, 463-473.
55. Werstuck, G., Zapp, M. L. & Green, M. R. (1996). A non-canonical base pair within the human immunodeficiency virus rev-responsive element is involved in both rev and small molecule recognition. Curr. Biol. 3, 129-137.
56. 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.
57. Zapp, M. L. & Green, M. R. (1989). Sequence-specific RNA binding by the HIV-1 Rev protein. Nature, 342, 714-716.
58. Zapp, M. L., Hope, T. J., Parslow, T. G. & Green, M. R. (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. USA, 88, 7734-7738.
59. Zapp, M. L., Stern, S. & Green, M. R. (1993). Small molecules that selectively block RNA binding of HIV-1 rev protein inhibit rev function and viral production. Cell 74, 969-976.
60. Zaug, A. J. & Cech, T. R. (1995). Analysis of the structure of Tetrahymena nuclear RNAs in vivo: telomerase RNA, the self-splicing rRNA intron, and U2 snRNA. RNA, 1, 363-374.
61. Zemmel, R. W., Kelley, A. C., Karn, J. & Butler, P. J. G. (1996). Flexible regions of RNA structure facilitate co-operative Rev assembly on the Rev-response element. J. Mol. Biol. 258, 763-777.