Dimeric RNA Recognition Regulates HIV-1 Genome Packaging

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Nikolaitchik, Olga A ^a   Dilley, Kari A ^a   Fu, William ^b   Gorelick, Robert J ^c   Tai, S H Sheldon ^a   Soheilian, Ferri ^c   Ptak, Roger G ^b   Nagashima, Kunio ^c   Pathak, Vinay K ^a   Hu, Wei Shau ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SOUTHERN RESEARCH INSTITUTE   (United States)

^c SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; REV PROTEIN; TRANSACTIVATOR PROTEIN; VIRUS RNA;

ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DIMERIZATION; DNA PACKAGING; GENE EXPRESSION; GENOME SIZE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR RECOGNITION; MS2 VIRUS; NONHUMAN; NORTHERN BLOTTING; REAL TIME POLYMERASE CHAIN REACTION; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY;

DIMERIZATION; DNA COPY NUMBER VARIATIONS; GENOME, VIRAL; HIV-1; HUMANS; KIDNEY; RNA, VIRAL; VIRION; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84875992709     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003249     Document Type: Article

References (56)

1. Temin HM, (1976) The DNA provirus hypothesis. Science 192: 1075-1080.
2. Duesberg PH, (1968) Physical properties of Rous Sarcoma Virus RNA. Proc Natl Acad Sci U S A 60: 1511-1518.
3. Kung HJ, Hu S, Bender W, Bailey JM, Davidson N, et al. (1976) RD-114, baboon, and woolly monkey viral RNA's compared in size and structure. Cell 7: 609-620.
4. Fu W, Gorelick RJ, Rein A, (1994) Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J Virol 68: 5013-5018.
5. Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J, (2004) Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2: 461-472.
6. Moore MD, Hu WS, (2009) HIV-1 RNA dimerization: It takes two to tango. AIDS Rev 11: 91-102.
7. Luban J, Goff SP, (1991) Binding of human immunodeficiency virus type 1 (HIV-1) RNA to recombinant HIV-1 gag polyprotein. Journal of virology 65: 3203-3212.
8. Aldovini A, Young RA, (1990) Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. Journal of virology 64: 1920-1926.
9. Lever AM, (2007) HIV-1 RNA packaging. Adv Pharmacol 55: 1-32.
10. Lever A, Gottlinger H, Haseltine W, Sodroski J, (1989) Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. Journal of virology 63: 4085-4087.
11. McBride MS, Panganiban AT, (1996) The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol 70: 2963-2973.
12. 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.
13. D'Souza V, Summers MF, (2005) How retroviruses select their genomes. Nat Rev Microbiol 3: 643-655.
14. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, et al. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6: e96.
15. Moore MD, Nikolaitchik OA, Chen J, Hammarskjold ML, Rekosh D, et al. (2009) Probing the HIV-1 genomic RNA trafficking pathway and dimerization by genetic recombination and single virion analyses. PLoS Pathog 5: e1000627.
16. Chen J, Nikolaitchik O, Singh J, Wright A, Bencsics CE, et al. (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.
17. Moore MD, Fu W, Nikolaitchik O, Chen J, Ptak RG, et al. (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.
18. 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.
19. Muriaux D, Fosse P, Paoletti J, (1996) A kissing complex together with a stable dimer is involved in the HIV-1Lai RNA dimerization process in vitro. Biochemistry 35: 5075-5082.
20. Paillart JC, Skripkin E, Ehresmann B, Ehresmann C, Marquet R, (1996) A loop-loop "kissing" complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc Natl Acad Sci U S A 93: 5572-5577.
21. Clever JL, Wong ML, Parslow TG, (1996) Requirements for kissing-loop-mediated dimerization of human immunodeficiency virus RNA. J Virol 70: 5902-5908.
22. Hussein IT, Ni N, Galli A, Chen J, Moore MD, et al. (2010) Delineation of the preferences and requirements of the human immunodeficiency virus type 1 dimerization initiation signal by using an in vivo cell-based selection approach. J Virol 84: 6866-6875.
23. St Louis DC, Gotte D, Sanders-Buell E, Ritchey DW, Salminen MO, et al. (1998) Infectious molecular clones with the nonhomologous dimer initiation sequences found in different subtypes of human immunodeficiency virus type 1 can recombine and initiate a spreading infection in vitro. J Virol 72: 3991-3998.
24. Sakalian M, Wills JW, Vogt VM, (1994) Efficiency and selectivity of RNA packaging by Rous sarcoma virus Gag deletion mutants. Journal of virology 68: 5969-5981.
25. Vogt VM (1997) Retroviral Virions and Genomes. In: Coffin JM, Hughes, S.H, Varmus, H.E., editor. Retroviruses. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp. 27-69.
26. Gelinas C, Temin HM, (1986) Nondefective spleen necrosis virus-derived vectors define the upper size limit for packaging reticuloendotheliosis viruses. Proceedings of the National Academy of Sciences of the United States of America 83: 9211-9215.
27. Terwilliger EF, Godin B, Sodroski JG, Haseltine WA, (1989) Construction and use of a replication-competent human immunodeficiency virus (HIV-1) that expresses the chloramphenicol acetyltransferase enzyme. Proceedings of the National Academy of Sciences of the United States of America 86: 3857-3861.
28. Swanstrom R, and Wills J.W. (1997) Synthesis, Assembly, and Processing of Viral Proteins. In: Coffin JM, Hughes, S.H, Varmus, H.E., editor. Retroviruses. Cold Spring Harbor: Cold Spring Harbor Press. pp. 263-334.
29. Shin NH, Hartigan-O'Connor D, Pfeiffer JK, Telesnitsky A, (2000) Replication of lengthened Moloney murine leukemia virus genomes is impaired at multiple stages. Journal of virology 74: 2694-2702.
30. Kumar M, Keller B, Makalou N, Sutton RE, (2001) Systematic determination of the packaging limit of lentiviral vectors. Hum Gene Ther 12: 1893-1905.
31. Larson DR, Johnson MC, Webb WW, Vogt VM, (2005) Visualization of retrovirus budding with correlated light and electron microscopy. Proc Natl Acad Sci U S A 102: 15453-15458.
32. 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.
33. Swain A, Coffin JM, (1992) Mechanism of transduction by retroviruses. Science 255: 841-845.
34. Goff SP, Gilboa E, Witte ON, Baltimore D, (1980) Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell 22: 777-785.
35. Herman SA, Coffin JM, (1987) Efficient packaging of readthrough RNA in ALV: implications for oncogene transduction. Science 236: 845-848.
36. D'Souza V, Summers MF, (2004) Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431: 586-590.
37. Gherghe C, Lombo T, Leonard CW, Datta SA, Bess JW Jr, et al. (2010) Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc Natl Acad Sci U S A 107: 19248-19253.
38. Lu K, Heng X, Garyu L, Monti S, Garcia EL, et al. (2011) NMR detection of structures in the HIV-1 5′-leader RNA that regulate genome packaging. Science 334: 242-245.
39. Hill MK, Shehu-Xhilaga M, Campbell SM, Poumbourios P, Crowe SM, et al. (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.
40. Rulli SJ Jr, Hibbert CS, Mirro J, Pederson T, Biswal S, et al. (2007) Selective and nonselective packaging of cellular RNAs in retrovirus particles. J Virol 81: 6623-6631.
41. Nikolaitchik OA, Galli A, Moore MD, Pathak VK, Hu WS, (2011) Multiple barriers to recombination between divergent HIV-1 variants revealed by a dual-marker recombination assay. Journal of molecular biology 407: 521-531.
42. Kent RB, Emanuel JR, Ben Neriah Y, Levenson R, Housman DE, (1987) Ouabain resistance conferred by expression of the cDNA for a murine Na+, K+-ATPase alpha subunit. Science 237: 901-903.
43. Nikolenko GN, Svarovskaia ES, Delviks KA, Pathak VK, (2004) Antiretroviral drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase increase template-switching frequency. J Virol 78: 8761-8770.
44. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, et al. (2003) Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr Biol 13: 161-167.
45. Kotsopoulou E, Kim VN, Kingsman AJ, Kingsman SM, Mitrophanous KA, (2000) A Rev-independent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gag-pol gene. J Virol 74: 4839-4852.
46. Burdick R, Smith JL, Chaipan C, Friew Y, Chen J, et al. (2010) P body-associated protein Mov10 inhibits HIV-1 replication at multiple stages. Journal of virology 84: 10241-10253.
47. Peterlin BM, Luciw PA, Barr PJ, Walker MD, (1986) Elevated levels of mRNA can account for the trans-activation of human immunodeficiency virus. Proceedings of the National Academy of Sciences of the United States of America 83: 9734-9738.
48. Lewis N, Williams J, Rekosh D, Hammarskjold ML, (1990) Identification of a cis-acting element in human immunodeficiency virus type 2 (HIV-2) that is responsive to the HIV-1 rev and human T-cell leukemia virus types I and II rex proteins. Journal of virology 64: 1690-1697.
49. Rhodes TD, Nikolaitchik O, Chen J, Powell D, Hu WS, (2005) Genetic recombination of human immunodeficiency virus type 1 in one round of viral replication: effects of genetic distance, target cells, accessory genes, and lack of high negative interference in crossover events. J Virol 79: 1666-1677.
50. Tobin GJ, Nagashima K, Gonda MA, (1996) Immunologic and Ultrastructural Characterization of HIV Pseudovirions Containing Gag and Env Precursor Proteins Engineered in Insect Cells. Methods 10: 208-218.
51. Fu W, Rein A, (1993) Maturation of dimeric viral RNA of Moloney murine leukemia virus. J Virol 67: 5443-5449.
52. Gorelick RJ, Benveniste RE, Gagliardi TD, Wiltrout TA, Busch LK, et al. (1999) Nucleocapsid protein zinc-finger mutants of simian immunodeficiency virus strain mne produce virions that are replication defective in vitro and in vivo. Virology 253: 259-270.
53. Gorelick RJ, Nigida SM Jr, Bess JW Jr, Arthur LO, Henderson LE, et al. (1990) Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. Journal of virology 64: 3207-3211.
54. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, et al. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
55. Cheevers WP, Archer BG, Crawford TB, (1977) Characterization of RNA from equine infectious anemia virus. Journal of virology 24: 489-497.
56. Buckman JS, Bosche WJ, Gorelick RJ, (2003) Human immunodeficiency virus type 1 nucleocapsid zn(2+) fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J Virol 77: 1469-1480.