The HIV-1 Rev response element: An RNA scaffold that directs the cooperative assembly of a homo-oligomeric ribonucleoprotein complex

RNA Biology

Volumn 9, Issue 1, 2012, Pages 6-11

  Fernandes, Jason D ^a,b   Jayaraman, Bhargavi ^a   Frankel, Alan D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Assembly; Export; HIV; Oligomer; Rev; RNA; RRE; Scaffold; Virus

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; OLIGOMER; REV PROTEIN; RIBONUCLEOPROTEIN; VIRUS RNA;

ARTICLE; CELL NUCLEUS; CONSENSUS SEQUENCE; CYTOPLASM; GENETIC CONSERVATION; GENOME ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; LIFE CYCLE; NONHUMAN; NUCLEIC ACID STRUCTURE; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; REV RESPONSIVE ELEMENT; RNA STRUCTURE; SEQUENCE ALIGNMENT; VIRION; VIRUS GENOME; VIRUS ISOLATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84856804646     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.9.1.18178     Document Type: Article

References (52)

1. Kjems J, Brown M, Chang DD, Sharp PA. Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element. Proc Natl Acad Sci USA 1991; 88:683-7; PMID:1992459; http://dx.doi.org/10.1073/ pnas.88.3.683
2. Sodroski J, Goh WC, Rosen C, Dayton A, Terwilliger E, Haseltine W. A second post-transcriptional transactivator gene required for HTLV-III replication. Nature 1986; 321:412-7; PMID:3012355; http://dx. doi.org/10.1038/321412a0
3. Rosen CA, Terwilliger E, Dayton A, Sodroski JG, Haseltine WA. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc Natl Acad Sci USA 1988; 85:2071-5; PMID:2832844; http://dx.doi.org/10.1073/ pnas.85.7.2071
4. Hadzopoulou-Cladaras M, Felber BK, Cladaras C, Athanassopoulos A, Tse A, Pavlakis GN. 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; 63:1265-74; PMID:2783738
5. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989; 338:254-7; PMID:2784194; http://dx.doi.org/10.1038/338254a0
6. Emerman M, Vazeux R, Peden K. The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell 1989; 57: 1155-65; PMID:2736624; http://dx.doi.org/10.1016/ 0092-8674(89)90053-6
7. Chang DD, Sharp PA. Regulation by HIV Rev depends upon recognition of splice sites. Cell 1989; 59:789-95; PMID:2686839; http://dx.doi.org/10. 1016/0092-8674(89)90602-8
8. Hammarskjöld ML, Heimer J, Hammarskjold B, Sangwan I, Albert L, Rekosh D. Regulation of human immunodeficiency virus env expression by the rev gene product. J Virol 1989; 63:1959-66; PMID:2704072
9. Mann DA, Mikaelian I, Zemmel RW, Green SM, Lowe AD, Kimura T, et al. A molecular rheostat. Cooperative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression. J Mol Biol 1994; 241:193- 207; PMID:8057359; http://dx.doi.org/10.1006/jmbi. 1994.1488
10. Dayton ET, Powell DM, Dayton AI. Functional analysis of CAR, the target sequence for the Rev protein of HIV-1. Science 1989; 246:1625-9; PMID: 2688093; http://dx.doi.org/10.1126/science.2688093
11. Charpentier B, Stutz F, Rosbash M. A dynamic in vivo view of the HIV-I Rev-RRE interaction. J Mol Biol 1997; 266:950-62; PMID:9086273; http://dx.doi.org/ 10.1006/jmbi.1996.0858
12. Zapp ML, Green MR. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 1989; 342: 714-6; PMID:2556643; http://dx.doi.org/10.1038/ 342714a0
13. Daly TJ, Cook KS, Gray GS, Maione TE, Rusche JR. Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 1989; 342: 816-9; PMID:2481237; http://dx.doi.org/10.1038/ 342816a0
14. Olsen HS, Nelbock P, Cochrane AW, Rosen CA. Secondary structure is the major determinant for interaction of HIV rev protein with RNA. Science 1990; 247:845-8; PMID:2406903; http://dx.doi.org/ 10.1126/science.2406903
15. Cochrane AW, Chen CH, Rosen CA. Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the env mRNA. Proc Natl Acad Sci USA 1990; 87:1198-202; PMID: 2405396; http://dx.doi.org/10. 1073/pnas.87.3.1198
16. Heaphy S, Dingwall C, Ernberg I, Gait MJ, Green SM, Karn J, et al. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 1990; 60:685-93; PMID:1689218; http://dx.doi.org/10. 1016/0092-8674(90)90671-Z
17. Malim MH, Cullen BR. HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 1991; 65:241-8; PMID:2015625; http:// dx.doi.org/10.1016/0092- 8674(91)90158-U
18. Cook KS, Fisk GJ, Hauber J, Usman N, Daly TJ, Rusche JR. Characterization of HIV-1 REV protein: binding stoichiometry and minimal RNA substrate. Nucleic Acids Res 1991; 19:1577-83; PMID:2027765; http://dx.doi.org/10.1093/nar/19.7. 1577
19. Hope TJ, McDonald D, Huang XJ, Low J, Parslow TG. Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: essential residues near the amino terminus. J Virol 1990; 64:5360-6; PMID:2120472
20. Malim MH, Tiley LS, McCarn DF, Rusche JR, Hauber J, Cullen BR. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 1990; 60:675-83; PMID:2406030; http://dx.doi.org/10. 1016/0092-8674(90)90670-A
21. Huang XJ, Hope TJ, Bond BL, McDonald D, Grahl K, Parslow TG. Minimal Rev-response element for type 1 human immunodeficiency virus. J Virol 1991; 65:2131-4; PMID:2002556
22. Heaphy S, Finch JT, Gait MJ, 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 Natl Acad Sci USA 1991; 88:7366-70; PMID:1871141; http://dx.doi.org/10.1073/pnas.88.16.7366
23. Kjems J, Calnan BJ, Frankel AD, Sharp PA. Specific binding of a basic peptide from HIV-1 Rev. EMBO J 1992; 11:1119-29; PMID:1547776
24. Tan R, Chen L, Buettner JA, Hudson D, Frankel AD. RNA recognition by an isolated alpha helix. Cell 1993; 73:1031-40; PMID:7684657; http://dx.doi.org/10. 1016/0092-8674(93)90280-4
25. Battiste JL, Mao H, Rao NS, Tan R, Muhandiram DR, Kay LE, et al. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science 1996; 273:1547-51; PMID:8703216; http:// dx.doi.org/10.1126/science.273. 5281.1547
26. Daugherty MD, D'Orso I, Frankel AD. A solution to limited genomic capacity: using adaptable binding surfaces to assemble the functional HIV Rev oligomer on RNA. Mol Cell 2008; 31:824-34; PMID:18922466; http://dx.doi.org/10. 1016/j.molcel.2008.07.016
27. Jain C, Belasco JG. 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; 7:603-14; PMID:11463385; http://dx. doi.org/10.1016/ S1097-2765(01)00207-6
28. Edgcomb SP, Aschrafi A, Kompfner E, Williamson JR, Gerace L, Hennig M. Protein structure and oligomerization are important for the formation of exportcompetent HIV-1 Rev-RRE complexes. Protein Sci 2008; 17:420-30; PMID:18218716; http://dx.doi.org/ 10.1110/ps.073246608
29. Daugherty MD, Liu B, Frankel AD. Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat Struct Mol Biol 2010; 17:1337-42; PMID:20953181; http://dx.doi.org/10.1038/nsmb.1902
30. DiMattia MA, Watts NR, Stahl SJ, Rader C, Wingfield PT, Stuart DI, et al. Implications of the HIV-1 Rev dimer structure at 3.2 A resolution for multimeric binding to the Rev response element. Proc Natl Acad Sci USA 2010; 107:5810-4; PMID:20231488; http:// dx.doi.org/10.1073/pnas.0914946107
31. Daugherty MD, Booth DS, Jayaraman B, Cheng Y, Frankel AD. HIV Rev response element (RRE) directs assembly of the Rev homooligomer into discrete asymmetric complexes. Proc Natl Acad Sci USA 2010; 107:12481-6; PMID:20616058; http://dx.doi. org/10.1073/pnas.1007022107
32. Pond SJ, Ridgeway WK, Robertson R, Wang J, Millar DP. HIV-1 Rev protein assembles on viral RNA one molecule at a time. Proc Natl Acad Sci USA 2009; 106:1404-8; PMID:19164515; http://dx.doi.org/10. 1073/pnas.0807388106
33. McDonald D, Hope TJ, Parslow TG. Posttranscriptional regulation by the human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type I Rex proteins through a heterologous RNA binding site. J Virol 1992; 66:7232-8; PMID:1433516
34. Venkatesan S, Gerstberger SM, Park H, Holland SM, Nam Y. Human immunodeficiency virus type 1 Rev activation can be achieved without Rev-responsive element RNA if Rev is directed to the target as a Rev/MS2 fusion protein which tethers the MS2 operator RNA. J Virol 1992; 66:7469-80; PMID: 1433526
35. Nam YS, Petrovic A, Jeong KS, Venkatesan S. Exchange of the basic domain of human immunodeficiency virus type 1 Rev for a polyarginine stretch expands the RNA binding specificity, and a minimal arginine cluster is required for optimal RRE RNA binding affinity, nuclear accumulation, and trans-activation. J Virol 2001; 75: 2957-71; PMID:11222721; http://dx.doi.org/10.1128/ JVI.75.6.2957-2971.2001
36. Kjems J, Sharp PA. The basic domain of Rev from human immunodeficiency virus type 1 specifically blocks the entry of U4/U6.U5 small nuclear ribonucleoprotein in spliceosome assembly. J Virol 1993; 67:4769-76; PMID:8331728
37. Symensma TL, Baskerville S, Yan A, Ellington AD. Polyvalent Rev decoys act as artificial Rev-responsive elements. J Virol 1999; 73:4341-9; PMID:10196332
38. Good MC, Zalatan JG, Lim WA. Scaffold proteins: hubs for controlling the flow of cellular information. Science 2011; 332:680-6; PMID:21551057; http://dx. doi.org/10.1126/science.1198701
39. Noller HF. RNA structure: reading the ribosome. Science 2005; 309:1508-14; PMID:16141058; http:// dx.doi.org/10.1126/science.1111771
40. Wahl MC, Will CL, Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18; PMID:19239890; http://dx.doi. org/10.1016/j.cell.2009.02.009
41. Zappulla DC, Cech TR. Yeast telomerase RNA: a flexible scaffold for protein subunits. Proc Natl Acad Sci USA 2004; 101:10024-9; PMID:15226497; http:// dx.doi.org/10.1073/pnas.0403641101
42. Ataide SF, Schmitz N, Shen K, Ke A, Shan SO, Doudna JA, et al. The crystal structure of the signal recognition particle in complex with its receptor. Science 2011; 331:881-6; PMID:21330537; http:// dx.doi.org/10.1126/ science.1196473
43. Malim MH, Bohnlein S, Hauber J, Cullen BR. Functional dissection of the HIV-1 Rev trans-activator-derivation of a trans-dominant repressor of Rev function. Cell 1989; 58:205-14; PMID:2752419; http://dx.doi.org/10.1016/0092- 8674(89)90416-9
44. Legiewicz M, Badorrek CS, Turner KB, Fabris D, Hamm TE, Rekosh D, et al. Resistance to RevM10 inhibition reflects a conformational switch in the HIV-1 Rev response element. Proc Natl Acad Sci USA 2008; 105:14365-70; PMID:18776047; http:// dx.doi.org/10.1073/pnas.0804461105
45. Lesnik EA, Sampath R, Ecker DJ. Rev response elements (RRE) in lentiviruses: an RNAMotif algorithm-based strategy for RRE prediction. Med Res Rev 2002; 22:617- 36; PMID:12369091; http://dx.doi.org/10.1002/med. 10027
46. 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; 85:2333-41; PMID: 21159877; http://dx.doi.org/10.1128/JVI.01518-10
47. Ahmed YF, Hanly SM, Malim MH, Cullen BR, Greene WC. Structure-function analyses of the HTLV-I Rex and HIV-1 Rev RNA response elements: insights into the mechanism of Rex and Rev action. Genes Dev 1990; 4:1014-22; PMID:2116986; http://dx.doi.org/10.1101/ gad.4.6.1014
48. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, Rekosh D, et al. A small element from the Mason- Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Revindependent. Proc Natl Acad Sci USA 1994; 91:1256- 60; PMID:8108397; http://dx.doi.org/10.1073/pnas. 91.4.1256
49. Braun IC, Rohrbach E, Schmitt C, Izaurralde E. TAP binds to the constitutive transport element (CTE) through a novel RNA-binding motif that is sufficient to promote CTE-dependent RNA export from the nucleus. EMBO J 1999; 18:1953-65; PMID:10202158; http://dx.doi.org/10.1093/emboj/18.7.1953
50. Tabernero C, Zolotukhin AS, Valentin A, Pavlakis GN, Felber BK. The posttranscriptional control element of the simian retrovirus type 1 forms an extensive RNA secondary structure necessary for its function. J Virol 1996; 70:5998-6011; PMID:8709222
51. Wodrich H, Schambach A, Krausslich HG. 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 2000; 28:901-10; PMID:10648781; http:// dx.doi.org/10.1093/nar/28.4.901
52. Pollard VW, Malim MH. The HIV-1 Rev protein. Annu Rev Microbiol 1998; 52:491-532; PMID: 9891806; http://dx.doi.org/10.1146/annurev.micro. 52.1.491