The relationship between HIV-1 genome RNA dimerization, virion maturation and infectivity

Nucleic Acids Research

Volumn 39, Issue 8, 2011, Pages 3404-3417

  Ohishi, Masahisa ^a   Nakano, Takashi ^b   Sakuragi, Sayuri ^a   Shioda, Tatsuo ^a   Sano, Kouichi ^b   Sakuragi, Jun Ichi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; VIRUS RNA;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; GENE CONSTRUCT; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; RNA TRANSLATION; STOICHIOMETRY; VIRION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; WESTERN BLOTTING;

CELL LINE; DIMERIZATION; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENOME, VIRAL; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; MUTATION; PROTEIN PRECURSORS; RNA, VIRAL; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79955603835     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1314     Document Type: Article

References (60)

1. Hu, W.S. and Temin, H.M. (1990) Retroviral recombination and reverse transcription. Science, 250, 1227-1233. (Pubitemid 120031830)
2. Paillart, J.C., Shehu-Xhilaga, M., Marquet, R. and Mak, J. (2004) Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol., 2, 461-472. (Pubitemid 39200013)
3. Greatorex, J.S., Laisse, V., Dockhelar, M.C. and Lever, A.M. (1996) Sequences involved in the dimerisation of human T cell leukaemia virus type-1 RNA. Nucleic Acids Res., 24, 2919-2923. (Pubitemid 26257158)
4. Darlix, J.L., Gabus, C., Nugeyre, M.T., Clavel, F. and 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. (Pubitemid 120037399)
5. Prats, A.C., Roy, C., Wang, P.A., Erard, M., Housset, V., Gabus, C., Paoletti, C. and Darlix, J.L. (1990) cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol., 64, 774-783. (Pubitemid 20032694)
6. Roy, C., Tounekti, N., Mougel, M., Darlix, J.L., Paoletti, C., Ehresmann, C., Ehresmann, B. and Paoletti, J. (1990) An analytical study of the dimerization of in vitro generated RNA of Moloney murine leukemia virus MoMuLV. Nucleic Acids Res., 18, 7287-7292. (Pubitemid 120006029)
7. Marquet, R., Baudin, F., Gabus, C., Darlix, J.L., Mougel, M., Ehresmann, C. and Ehresmann, B. (1991) Dimerization of human immunodeficiency virus (type 1) RNA: stimulation by cations and possible mechanism. Nucleic Acids Res., 19, 2349-2357. (Pubitemid 21902970)
8. Darlix, J.L., Gabus, C. and Allain, B. (1992) Analytical study of avian reticuloendotheliosis virus dimeric RNA generated in vivo and in vitro. J. Virol., 66, 7245-7252.
9. Marquet, R., Paillart, J.C., Skripkin, E., Ehresmann, C. and Ehresmann, B. (1994) Dimerization of human immunodeficiency virus type 1 RNA involves sequences located upstream of the splice donor site. Nucleic Acids Res., 22, 145-151. (Pubitemid 24160928)
10. Adamson, C.S., Salzwedel, K. and Freed, E.O. (2009) Virus maturation as a new HIV-1 therapeutic target. Expert Opin. Ther. Targets, 13, 895-908.
11. Feng, Y.X., Campbell, S., Harvin, D., Ehresmann, B., Ehresmann, C. and Rein, A. (1999) The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. J. Virol., 73, 4251-4256. (Pubitemid 29189870)
12. Feng, Y.X., Copeland, T.D., Henderson, L.E., Gorelick, R.J., Bosche, W.J., Levin, J.G and Rein, A. (1996) HIV-1 nucleocapsid protein induces "maturation" of dimeric retroviral RNA in vitro. Proc. Natl Acad. Sci. USA, 93, 7577-7581.
13. Fu, W., Gorelick, R.J. and Rein, A. (1994) Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J. Virol., 68, 5013-5018. (Pubitemid 24226568)
14. Fu, W. and Rein, A. (1993) Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol., 67, 5443-5449. (Pubitemid 23241379)
15. Pettit, S.C., Sheng, N., Tritch, R., Erickson-Viitanen, S. and Swanstrom, R. (1998) The regulation of sequential processing of HIV-1 Gag by the viral protease. Adv. Exp. Med. Biol., 436, 15-25. (Pubitemid 28201260)
16. Wiegers, K., Rutter, G., Kottler, H., Tessmer, U., Hohenberg, H. and Krausslich, H.G (1998) Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol., 72, 2846-2854. (Pubitemid 28175521)
17. Shehu-Xhilaga, M., Kraeusslich, H.G, Pettit, S., Swanstrom, R., Lee, JY., Marshall, JA., Crowe, S.M. and Mak, J. (2001) Proteolytic processing of the p2/nucleocapsid cleavage site is critical for human immunodeficiency virus type 1 RNA dimer maturation. J. Virol., 75, 9156-9164. (Pubitemid 32851920)
18. Kafaie, J., Dolatshahi, M., Ajamian, L., Song, R., Mouland, A.J., Rouiller, I. and Laughrea, M. (2009) Role of capsid sequence and immature nucleocapsid proteins p9 and p15 in Human Immunodeficiency Virus type 1 genomic RNA dimerization. Virology, 385, 233-244.
19. Fu, W., Dang, Q., Nagashima, K., Freed, E.O., Pathak, V.K. and Hu, W.S. (2006) Effects of Gag mutation and processing on retroviral dimeric RNA maturation. J. Virol., 80, 1242-1249. (Pubitemid 43134081)
20. Jalalirad, M. and Laughrea, M. (2010) Formation of immature and mature genomic RNA dimers in wild-type and protease-inactive HIV-1: differential roles of the Gag polyprotein, nucleocapsid proteins NCp15, NCp9, NCp7, and the dimerization initiation site. Virology, 407, 225-236.
21. Sakuragi, J., Ueda, S., Iwamoto, A. and Shioda, T. (2003) Possible role of dimerization in human immunodeficiency virus type 1 genome RNA packaging. J. Virol., 77, 4060-4069. (Pubitemid 36350946)
22. Adachi, A., Gendelman, H.E., Koenig, S., Folks, T., Willey, R., Rabson, A. and Martin, MA. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol., 59, 284-291. (Pubitemid 16013975)
23. Pettit, S.C., Henderson, GJ., Schiffer, CA. and Swanstrom, R. (2002) Replacement of the P1 amino acid of human immunodeficiency virus type 1 Gag processing sites can inhibit or enhance the rate of cleavage by the viral protease. J. Virol., 76, 10226-10233.
24. Ohishi, M., Shioda, T. and Sakuragi, J.i. (2007) Retro-transduction by virus pseudotyped with glycoprotein of vesicular stomatitis virus. Virology, 362, 131-138. (Pubitemid 46617697)
25. Sakuragi, J., Iwamoto, A. and Shioda, T. (2002) Dissociation of genome dimerization from packaging functions and virion maturation of human immunodeficiency virus type 1. J. Virol., 76, 959-967. (Pubitemid 34066401)
26. DuBridge, R.B., Tang, P., Hsia, H.C., Leong, P.M., Miller, J.H. and Calos, M.P. (1987) Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell Biol., 7, 379-387. (Pubitemid 17230421)
27. Aldovini, A. and Walker, B.D. (1990) Techniques in HIV Research. Stockton Press, New York.
28. Koh, K.B., Fujita, M. and Adachi, A. (2000) Elimination of HIV-1 plasmid DNA from virus samples obtained from transfection by calcium-phosphate co-precipitation. J. Virol. Methods, 90, 99-102.
29. Ota, A., Liu, X., Fujio, H., Sakato, N. and Ueda, S. (1998) Random expression of human immunodeficiency virus-1 (HIV-1) p17 (epitopes) on the surface of the HIV-1-infected cell. Hybridoma, 17, 73-75. (Pubitemid 28120022)
30. Campbell, S. and Rein, A. (1999) In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol., 73, 2270-2279. (Pubitemid 29098132)
31. Sakuragi, J.I. and Panganiban, A.T. (1997) Human immunodeficiency virus type 1 RNA outside the primary encapsidation and dimer linkage region affects RNA dimer stability in vivo. J. Virol., 71, 3250-3254. (Pubitemid 27119973)
32. Masuda, T., Planelles, V., Krogstad, P. and Chen, I.S. (1995) Genetic analysis of human immunodeficiency virus type 1 integrase and the U3 att site: unusual phenotype of mutants in the zinc finger-like domain. J. Virol., 69, 6687-6696.
33. Nagao, T., Yoshida, A., Sakurai, A., Piroozmand, A., Jere, A., Fujita, M., Uchiyama, T. and Adachi, A. (2004) Determination of HIV-1 infectivity by lymphocytic cell lines with integrated luciferase gene. Int. J. Mol. Med., 14, 1073-1076.
34. Harada, S., Koyanagi, Y. and Yamamoto, N. (1985) Infection of HTLV-III/LAV in HTLV-I-carrying cells MT-2 and MT-4 and application in a plaque assay. Science, 229, 563-566. (Pubitemid 16239336)
35. Sakuragi, J., Sakuragi, S. and Shioda, T. (2007) Minimal region sufficient for genome dimerization in the human immunodeficiency virus type 1 virion and its potential roles in the early stages of viral replication. J. Virol., 81, 7985-7992. (Pubitemid 47101483)
36. Julias, J.G., Ferris, A.L., Boyer, P.L. and Hughes, S.H. (2001) Replication of phenotypically mixed human immunodeficiency virus type 1 virions containing catalytically active and catalytically inactive reverse transcriptase. J. Virol., 75, 6537-6546. (Pubitemid 32578173)
37. Dulude, D., Theberge-Julien, G., Brakier-Gingras, L. and Heveker, N. (2008) Selection of peptides interfering with a ribosomal frameshift in the human immunodeficiency virus type 1. RNA, 14, 981-991. (Pubitemid 351574919)
38. Pettit, S.C., Moody, M.D., Wehbie, R.S., Kaplan, A.H., Nantermet, P.V., Klein, CA. and Swanstrom, R. (1994) The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol., 68, 8017-8027. (Pubitemid 24362690)
39. Kaplan, A.H., Manchester, M. and Swanstrom, R. (1994) The activity of the protease of human immunodeficiency virus type 1 is initiated at the membrane of infected cells before the release of viral proteins and is required for release to occur with maximum efficiency. J. Virol., 68, 6782-6786.
40. Bukrinskaya, A.G (2004) HIV-1 assembly and maturation. Arch. Virol., 149, 1067-1082. (Pubitemid 38791655)
41. Peng, C., Ho, B.K., Chang, T.W. and Chang, N.T. (1989) Role of human immunodeficiency virus type 1-specific protease in core protein maturation and viral infectivity. J. Virol., 63, 2550-2556. (Pubitemid 19137530)
42. Nakayama, E.E. and Shioda, T. (2010) Anti-retroviral activity of TRIM5 alpha. Rev. Med. Virol., 20, 77-92.
43. Muriaux, D., De Rocquigny, H., Roques, B.P. and 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.
44. Moore, M.D., Fu, W., Soheilian, F., Nagashima, K., Ptak, R.G, Pathak, V.K. and Hu, W.S. (2008) Suboptimal inhibition of protease activity in human immunodeficiency virus type 1: effects on virion morphogenesis and RNA maturation. Virology, 379, 152-160.
45. Paillart, J.C., Dettenhofer, M., Yu, X.F., Ehresmann, C., Ehresmann, B. and Marquet, R. (2004) First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem., 279, 48397-48403. (Pubitemid 39540996)
46. Johnson, S.F. and Telesnitsky, A. (2010) Retroviral RNA dimerization and packaging: the what, how, when, where, and why. PLoS Pathog., 6, e1001007.
47. Weiss, S., Konig, B., Morikawa, Y. and Jones, I. (1992) Recombinant HIV-1 nucleocapsid protein p15 produced as a fusion protein with glutathione S-transferase in Escherichia coli mediates dimerization and enhances reverse transcription of retroviral RNA. Gene, 121, 203-212.
48. Barat, C., Lullien, V., Schatz, O., Keith, G, Nugeyre, M.T., Gruninger-Leitch, F., Barre-Sinoussi, F., LeGrice, S.F. and Darlix, J.L. (1989) HIV-1 reverse transcriptase specifically interacts with the anticodon domain of its cognate primer tRNA. EMBO J., 8, 3279-3285. (Pubitemid 19273554)
49. Cruceanu, M., Urbaneja, MA., Hixson, C.V., Johnson, D.G, Datta, SA., Fivash, M.J., Stephen, A.G, Fisher, R.J., Gorelick, R.J., Casas-Finet, J.R. et al. (2006) Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res., 34, 593-605. (Pubitemid 43240247)
50. Muriaux, D., Mirro, J., Harvin, D. and Rein, A. (2001) RNA is a structural element in retrovirus particles. Proc Natl Acad. Sci. USA, 98, 5246-5251. (Pubitemid 32397114)
51. Rulli, S.J. Jr, Hibbert, C.S., Mirro, J., Pederson, T., Biswal, S. and Rein, A. (2007) Selective and non-selective packaging of cellular RNAs in retrovirus particles. J. Virol., 81, 6623-6631. (Pubitemid 46878066)
52. Song, R., Kafaie, J., Yang, L. and Laughrea, M. (2007) HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step protease-dependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J. Mol. Biol., 371, 1084-1098. (Pubitemid 47101821)
53. Rein, A., Henderson, L.E. and Levin, J.G (1998) Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci., 23, 297-301. (Pubitemid 28461895)
54. Freed, E.O. (2001) HIV-1 replication. Somat Cell Mol. Genet., 26, 13-33. (Pubitemid 35332977)
55. Shvadchak, V.V., Klymchenko, A.S., de Rocquigny, H. and Mely Y. (2009) Sensing peptide-oligonucleotide interactions by a two-color fluorescence label: application to the HIV-1 nucleocapsid protein. Nucleic Acids Res., 37, e25.
56. Briggs, JA., Johnson, M.C., Simon, M.N., Fuller, S.D. and Vogt, V.M. (2006) Cryo-electron microscopy reveals conserved and divergent features of gag packing in immature particles of Rous sarcoma virus and human immunodeficiency virus. J. Mol. Biol., 355, 157-168. (Pubitemid 41782004)
57. Briggs, JA., Simon, M.N., Gross, I., Krausslich, H.G, Fuller, S.D., Vogt, V.M. and Johnson, M.C. (2004) The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol., 11, 672-675. (Pubitemid 38823535)
58. Tchenio, T. and Heidmann, T. (1995) The dimerization/packaging sequence is dispensable for both the formation of high-molecular-weight RNA complexes within retroviral particles and the synthesis of proviruses ofnormal structure. J. Virol., 69, 1079-1084.
59. Ortiz-Conde, BA. and Hughes, S.H. (1999) Studies of the genomic RNA of leukosis viruses: implications for RNA dimerization. J. Virol., 73, 7165-7174. (Pubitemid 29383197)
60. Mirambeau, G, Lyonnais, S., Coulaud, D., Hameau, L., Lafosse, S., Jeusset, J., Borde, I., Reboud-Ravaux, M., Restle, T., Gorelick, R.J. et al. (2007) HIV-1 protease and reverse transcriptase control the architecture of their nucleocapsid partner. PLoS One, 2, e669.