In vivo SELEX of single-stranded domains in the HIV-1 leader RNA

Journal of Virology

Volumn 88, Issue 4, 2014, Pages 1870-1880

  van Bel, Nikki ^a   Das, Atze T ^a   Berkhout, Ben ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGIONS; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE LIBRARY; HIV-1; INVERTED REPEAT SEQUENCES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; REGULATORY SEQUENCES, NUCLEIC ACID; SELEX APTAMER TECHNIQUE;

EID: 84893456497     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02942-13     Document Type: Article

References (79)

1. Lu K, Heng X, Summers MF. 2011. Structural determinants and mechanism of HIV-1 genome packaging. J. Mol. Biol. 410:609-633. http://dx.doi.org/10.1016/j.jmb.2011.04.029.
2. Abbink TE, Berkhout B. 2003. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J. Biol. Chem. 278:11601-11611. http://dx.doi.org/10.1074/jbc.M210291200.
3. Feinberg MB, Baltimore D, Frankel AD. 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. http://dx.doi.org/10.1073/pnas.88.9.4045.
4. Laspia MF, Rice AP, Mathews MB. 1989. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59:283-292. http://dx.doi.org/10.1016/0092-8674(89)90290-0.
5. Richter S, Ping YH, Rana TM. 2002. TAR RNA loop: a scaffold for the assembly of a regulatory switch in HIV replication. Proc. Natl. Acad. Sci. U.S.A. 99:7928-7933. http://dx.doi.org/10.1073/pnas.122119999.
6. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA. 1998. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92:451-462. http://dx.doi.org/10.1016/S0092-8674(00)80939-3.
7. Jalalirad M, Saadatmand J, Laughrea M. 2012. Dominant role of the 5' TAR bulge in dimerization of HIV-1 genomic RNA, but no evidence of TAR-TAR kissing during in vivo virus assembly. Biochemistry 51:3744-3758. http://dx.doi.org/10.1021/bi300111p.
8. Helga-Maria C, Hammarskjold ML, Rekosh D. 1999. An intact TAR element and cytoplasmic localization are necessary for efficient packaging of human immunodeficiency virus type 1 genomic RNA. J. Virol. 73:4127-4135.
9. McBride MS, Schwartz MD, Panganiban AT. 1997. Efficient encapsidation ofhumanimmunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J. Virol. 71:4544-4554.
10. Vrolijk MM, Ooms M, Harwig A, Das AT, Berkhout B. 2008. Destabilization of the TAR hairpin affects the structure and function of the HIV-1 leader RNA. Nucleic Acids Res. 36:4352-4363. http://dx.doi.org/10.1093/nar/gkn364.
11. Das AT, Vrolijk MM, Harwig A, Berkhout B. 2012. Opening of the TAR hairpin in the HIV-1 genome causes aberrantRNAdimerization and packaging. Retrovirology 9:59. http://dx.doi.org/10.1186/1742-4690-9-59.
12. Brown PH, Tiley LS, Cullen BR. 1991. Efficient polyadenylation within the human immunodeficiency virus type 1 long terminal repeat requires flanking U3-specific sequences. J. Virol. 65:3340-3343.
13. DeZazzo JD, Kilpatrick JE, Imperiale MJ. 1991. Involvement of long terminal repeat U3 sequences overlapping the transcription control region in human immunodeficiency virus type 1 mRNA 3' end formation. Mol. Cell. Biol. 11:1624-1630.
14. Valsamakis A, Zeichner S, Carswell S, Alwine JC. 1991. The human immunodeficiency virus type 1 polyadenylylation signal: a 3' long terminal repeat element upstream of the AAUAAA necessary for efficient polyadenylylation. Proc. Natl. Acad. Sci. U.S.A. 88:2108-2112. http://dx.doi.org/10.1073/pnas.88.6.2108.
15. Valsamakis A, Schek N, Alwine JC. 1992. Elements upstream of the AAUAAA within the human immunodeficiency virus polyadenylation signal are required for efficient polyadenylation in vitro. Mol. Cell. Biol. 12:3699-3705.
16. Marquet R, Isel C, Ehresmann C, Ehresmann B. 1995. tRNAs as primer of reverse transcriptases. Biochimie 77:113-124. http://dx.doi.org/10.1016/0300-9084(96)88114-4.
17. Telesnitsky A, Goff SP. 1997. Reverse transcriptase and the generation of retroviral DNA. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
18. Beerens N, Groot F, Berkhout B. 2001. Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J. Biol. Chem. 276:31247-31256. http://dx.doi.org/10.1074/jbc.M102441200.
19. Beerens N, Berkhout B. 2002. The tRNA primer activation signal in the human immunodeficiency virus type 1 genome is important for initiation and processive elongation of reverse transcription. J. Virol. 76:2329-2339. http://dx.doi.org/10.1128/jvi.76.5.2329-2339.2002.
20. Berkhout B, Vastenhouw NL, Klasens BI, Huthoff H. 2001. Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription. RNA 7:1097-1114. http://dx.doi.org/10.1017/S1355838201002035.
21. Chen J, Nikolaitchik O, Singh J, Wright A, Bencsics CE, Coffin JM, Ni N, Lockett S, Pathak VK, Hu WS. 2009. High efficiency of HIV-1 genomic RNA packaging and heterozygote formation revealed by single virion analysis. Proc. Natl. Acad. Sci. U.S.A. 106:13535-13540. http://dx.doi.org/10.1073/pnas.0906822106.
22. Moore MD, Fu W, Nikolaitchik O, Chen J, Ptak RG, Hu WS. 2007. Dimer initiation signal of human immunodeficiency virus type 1: its role in partner selection during RNA copackaging and its effects on recombination. J. Virol. 81:4002-4011. http://dx.doi.org/10.1128/JVI.02589-06.
23. Haddrick M, Lear AL, Cann AJ, Heaphy S. 1996. Evidence that a kissing loop structure facilitates genomic RNA dimerisation in HIV-1. J. Mol. Biol. 259:58-68. http://dx.doi.org/10.1006/jmbi.1996.0301.
24. Laughrea M, Jette L. 1996. Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNAs can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimer formation. Biochemistry 35:1589-1598. http://dx.doi.org/10.1021/bi951838f.
25. Skripkin E, Paillart JC, Marquet R, Ehresmann B, Ehresmann C. 1994. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc. Natl. Acad. Sci. U.S.A. 91:4945-4949. http://dx.doi.org/10.1073/pnas.91.11.4945.
26. Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J. 2004. Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol. 2:461-472. http://dx.doi.org/10.1038/nrmicro903.
27. Fu W, Gorelick RJ, Rein A. 1994. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and proteasedefective virions. J. Virol. 68:5013-5018.
28. Song R, Kafaie J, Yang L, Laughrea M. 2007. HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step proteasedependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J. Mol. Biol. 371:1084-1098. http://dx.doi.org/10.1016/j.jmb.2007.06.010.
29. Ohishi M, Nakano T, Sakuragi S, Shioda T, Sano K, Sakuragi J. 2011. The relationship between HIV-1 genome RNA dimerization, virion maturation and infectivity. Nucleic Acids Res. 39:3404-3417. http://dx.doi.org/10.1093/nar/gkq1314.
30. Hill MK, Shehu-Xhilaga M, Campbell SM, Poumbourios P, Crowe SM, Mak J. 2003. The dimer initiation sequence stem-loop of human immunodeficiency virus type 1 is dispensable for viral replication in peripheral blood mononuclear cells. J. Virol. 77:8329-8335. http://dx.doi.org/10.1128/JVI.77.15.8329-8335.2003.
31. Berkhout B, van Wamel JL. 1996. Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol. 70:6723-6732.
32. Jones KL, Sonza S, Mak J. 2008. Primary T-lymphocytes rescue the replication of HIV-1 DIS RNA mutants in part by facilitating reverse transcription. Nucleic Acids Res. 36:1578-1588. http://dx.doi.org/10.1093/nar/gkm1149.
33. Purcell DF, Martin MA. 1993. Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol. 67:6365-6378.
34. Abbink TE, Berkhout B. 2008. RNA structure modulates splicing efficiency at the human immunodeficiency virus type 1 major splice donor. J. Virol. 82:3090-3098. http://dx.doi.org/10.1128/JVI.01479-07.
35. Sakuragi J, Ueda S, Iwamoto A, Shioda T. 2003. Possible role of dimerization in human immunodeficiency virus type 1 genome RNA packaging. J. Virol. 77:4060-4069. http://dx.doi.org/10.1128/JVI.77.7.4060-4069.2003.
36. Heng X, Kharytonchyk S, Garcia EL, Lu K, Divakaruni SS, LaCotti C, Edme K, Telesnitsky A, Summers MF. 2012. Identification of a minimal region of the HIV-1 5'-leader required for RNA dimerization, NC binding, and packaging. J. Mol. Biol. 417:224-239. http://dx.doi.org/10.1016/j.jmb.2012.01.033.
37. Sakuragi J, Shioda T, Panganiban AT. 2001. Duplication of the primary encapsidation and dimer linkage region of human immunodeficiency virus type 1 RNA results in the appearance of monomeric RNA in virions. J. Virol. 75:2557-2565. http://dx.doi.org/10.1128/JVI.75.6.2557-2565.2001.
38. D'Souza V, Summers MF. 2004. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431:586-590. http://dx.doi.org/10.1038/nature02944.
39. Dirac AM, Huthoff H, Kjems J, Berkhout B. 2002. Regulated HIV-2 RNA dimerization by means of alternative RNA conformations. Nucleic Acids Res. 30:2647-2655. http://dx.doi.org/10.1093/nar/gkf381.
40. Huthoff H, Berkhout B. 2001. Two alternating structures of the HIV-1 leader RNA. RNA 7:143-157. http://dx.doi.org/10.1017/S1355838201001881.
41. Huthoff H, Berkhout B. 2002. Multiple secondary structure rearrangements during HIV-1 RNA dimerization. Biochemistry 41:10439-10445. http://dx.doi.org/10.1021/bi025993n.
42. Kenyon JC, Tanner SJ, Legiewicz M, Phillip PS, Rizvi TA, Le Grice SF, Lever AM. 2011. SHAPE analysis of the FIV leader RNA reveals a structural switch potentially controlling viral packaging and genome dimerization. Nucleic Acids Res. 39:6692-6704. http://dx.doi.org/10.1093/nar/gkr252.
43. Maurel S, Mougel M. 2010. Murine leukemia virus RNA dimerization is coupled to transcription and splicing processes. Retrovirology 7:64. http://dx.doi.org/10.1186/1742-4690-7-64.
44. Miyazaki Y, Garcia EL, King SR, Iyalla K, Loeliger K, Starck P, Syed S, Telesnitsky A, Summers MF. 2010. An RNA structural switch regulates diploid genome packaging by Moloney murine leukemia virus. J. Mol. Biol. 396:141-152. http://dx.doi.org/10.1016/j.jmb.2009.11.033.
45. Tounekti N, Mougel M, Roy C, Marquet R, Darlix JL, Paoletti J, Ehresmann B, Ehresmann C. 1992. Effect of dimerization on the conformation of the encapsidation Psi domain of Moloney murine leukemia virus RNA. J. Mol. Biol. 223:205-220. http://dx.doi.org/10.1016/0022-2836(92)90726-Z.
46. Abbink TE, Ooms M, Haasnoot PC, Berkhout B. 2005. The HIV-1 leader RNA conformational switch regulates RNA dimerization but does not regulate mRNA translation. Biochemistry 44:9058-9066. http://dx.doi.org/10.1021/bi0502588.
47. Berkhout B, van Wamel JL. 2000. The leader of the HIV-1 RNA genome forms a compactly folded tertiary structure.RNA6:282-295. http://dx.doi.org/10.1017/S1355838200991684.
48. Berkhout B, Ooms M, Beerens N, Huthoff H, Southern E, Verhoef K. 2002. In vitro evidence that the untranslated leader of the HIV-1 genome is an RNA checkpoint that regulates multiple functions through conformational changes. J. Biol. Chem. 277:19967-19975. http://dx.doi.org/10.1074/jbc.M200950200.
49. Ooms M, Huthoff H, Russell R, Liang C, Berkhout B. 2004. A riboswitch regulates RNA dimerization and packaging in human immunodeficiency virus type 1 virions. J. Virol. 78:10814-10819. http://dx.doi.org/10.1128/JVI.78.19.10814-10819.2004.
50. Sakuragi JI, Ode H, Sakuragi S, Shioda T, Sato H. 2012. A proposal for a new HIV-1 DLS structural model. Nucleic Acids Res. 40:5012-5022. http://dx.doi.org/10.1093/nar/gks156.
51. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6:e96. http://dx.doi.org/10.1371/journal.pbio.0060096.
52. Lu K, Heng X, Garyu L, Monti S, Garcia EL, Kharytonchyk S, Dorjsuren B, Kulandaivel G, Jones S, Hiremath A, Divakaruni SS, LaCotti C, Barton S, Tummillo D, Hosic A, Edme K, Albrecht S, Telesnitsky A, Summers MF. 2011. NMR detection of structures in the HIV-1 5'-leader RNA that regulate genome packaging. Science 334:242-245. http://dx.doi.org/10.1126/science.1210460.
53. Berkhout B, Klaver B. 1993. In vivo selection of randomly mutated retroviral genomes. Nucleic Acids Res. 21:5020-5024. http://dx.doi.org/10.1093/nar/21.22.5020.
54. Doria-Rose NA, Vogt VM. 1998. In vivo selection of Rous sarcoma virus mutants with randomized sequences in the packaging signal. J. Virol. 72: 8073-8082.
55. Das AT, Zhou X, Vink M, Klaver B, Verhoef K, Marzio G, Berkhout B. 2004. Viral evolution as a tool to improve the tetracycline-regulated gene expression system. J. Biol. Chem. 279:18776-18782. http://dx.doi.org/10.1074/jbc.M313895200.
56. Das AT, Harwig A, Berkhout B. 2011. The HIV-1 Tat protein has a versatile role in activating viral transcription. J. Virol. 85:9506-9516. http://dx.doi.org/10.1128/JVI.00650-11.
57. Das AT, Klaver B, Klasens BI, van Wamel JL, Berkhout B. 1997. A conserved hairpin motif in the R-U5 region of the human immunodeficiency virus type 1 RNA genome is essential for replication. J. Virol. 71:2346-2356.
58. Das AT, Klaver B, Berkhout B. 1999. A hairpin structure in the R region of the human immunodeficiency virus type 1 RNA genome is instrumental in polyadenylation site selection. J. Virol. 73:81-91.
59. van Opijnen T, Kamoschinski J, Jeeninga RE, Berkhout B. 2004. The human immunodeficiency virus type 1 promoter contains a CATA box instead of a TATA box for optimal transcription and replication. J. Virol. 78:6883-6890. http://dx.doi.org/10.1128/JVI.78.13.6883-6890.2004.
60. Reuter JS, Mathews DH. 2010. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11:129. http://dx.doi.org/10.1186/1471-2105-11-129.
61. Peden K, Emerman M, Montagnier L. 1991. Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI. Virology 185:661-672. http://dx.doi.org/10.1016/0042-6822(91)90537-L.
62. Koken SE, van Wamel JL, Goudsmit J, Berkhout B, Geelen JL. 1992. Natural variants of the HIV-1 long terminal repeat: analysis of promoters with duplicated DNA regulatory motifs. Virology 191:968-972. http://dx.doi.org/10.1016/0042-6822(92)90274-S.
63. Verhoef K, Bauer M, Meyerhans A, Berkhout B. 1998. On the role of the second coding exon of the HIV-1 Tat protein in virus replication and MHC class I downregulation. AIDS Res. Hum. Retroviruses 14:1553-1559. http://dx.doi.org/10.1089/aid.1998.14.1553.
64. van Hemert FJ, van der Kuyl AC, Berkhout B. 2013. The A-nucleotide preference of HIV-1 in the context of its structured RNA genome. RNA Biol. 10:211-215. http://dx.doi.org/10.4161/rna.22896.
65. Berkhout B, van Hemert FJ. 1994. The unusual nucleotide content of the HIV RNAgenomeresults inabiasedaminoacidcompositionofHIVproteins.Nucleic Acids Res. 22:1705-1711. http://dx.doi.org/10.1093/nar/22.9.1705.
66. Clever J, Sassetti C, Parslow TG. 1995. RNA secondary structure and binding sites for gag gene products in the 5' packaging signal of human immunodeficiency virus type 1. J. Virol. 69:2101-2109.
67. Darlix JL, Godet J, Ivanyi-Nagy R, Fosse P, Mauffret O, Mely Y. 2011. Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J. Mol. Biol. 410:565-581. http://dx.doi.org/10.1016/j.jmb.2011.03.037.
68. Gorelick RJ, Nigida SM, Jr, Bess JW, Jr, Arthur LO, Henderson LE, Rein A. 1990. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J. Virol. 64:3207-3211.
69. Gorelick RJ, Chabot DJ, Rein A, Henderson LE, Arthur LO. 1993. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. J. Virol. 67:4027-4036.
70. Muriaux D, De RH, Roques BP, Paoletti J. 1996. NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J. Biol. Chem. 271:33686-33692. http://dx.doi.org/10.1074/jbc.271.52.33686.
71. Rist MJ, Marino JP. 2002. Mechanism of nucleocapsid protein catalyzed structural isomerization of the dimerization initiation site of HIV-1. Biochemistry 41:14762-14770. http://dx.doi.org/10.1021/bi0267240.
72. Darlix JL, Gabus C, Nugeyre MT, Clavel F, Barre-Sinoussi F. 1990. Cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J. Mol. Biol. 216:689-699. http://dx.doi.org/10.1016/0022-2836(90)90392-Y.
73. Gallego J, Greatorex J, Zhang H, Yang B, Arunachalam S, Fang J, Seamons J, Lea S, Pomerantz RJ, Lever AM. 2003. Rev binds specifically to a purine loop in the SL1 region of the HIV-1 leader RNA. J. Biol. Chem. 278:40385-40391. http://dx.doi.org/10.1074/jbc.M301041200.
74. Brandt S, Blissenbach M, Grewe B, Konietzny R, Grunwald T, Uberla K. 2007. Rev proteins of human and simian immunodeficiency virus enhance RNA encapsidation. PLoS Pathog. 3:518-525. http://dx.doi.org/10.1371/journal.ppat.0030054.
75. Asang C, Erkelenz S, Schaal H. 2012. The HIV-1 major splice donor D1 is activated by splicing enhancer elements within the leader region and the p17-inhibitory sequence. Virology 432:133-145. http://dx.doi.org/10.1016/j.virol.2012.06.004.
76. Song R, Kafaie J, Laughrea M. 2008. Role of the 5' TAR stem-loop and the U5-AUG duplex in dimerization of HIV-1 genomic RNA. Biochemistry 47:3283-3293. http://dx.doi.org/10.1021/bi7023173.
77. Shen N, Jette L, Wainberg MA, Laughrea M. 2001. Role of stem B, loop B, and nucleotides next to the primer binding site and the kissing-loop domain in human immunodeficiency virus type 1 replication and genomic-RNA dimerization. J. Virol. 75:10543-10549. http://dx.doi.org/10.1128/JVI.75.21.10543-10549.2001.
78. van der Kuyl AC, Berkhout B. 2012. The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus. Retrovirology 9:92. http://dx.doi.org/10.1186/1742-4690-9-92.
79. Kuiken C, Foley B, Leitner T, Apetrei C, Hahn B, Mizrachi I, Mullins J, Rambaut A, Wolinsky S, Korber B. 2010. HIV sequence compendium 2010. LA-UR 10-03684. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, NM.