Mechanisms of human immunodeficiency virus type 2 RNA Packaging: Efficient trans packaging and selection of RNA copackaging partners

Journal of Virology

Volumn 85, Issue 15, 2011, Pages 7603-7612

  Ni, Na ^a   Nikolaitchik, Olga A ^a   Dilley, Kari A ^a   Chen, Jianbo ^a   Galli, Andrea ^a   Fu, William ^b   Prasad, V V S P ^a   Ptak, Roger G ^b   Pathak, Vinay K ^a   Hu, Wei Shau ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SOUTHERN RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; FLUORESCENT PROTEIN; GAG PROTEIN; MONOMER; PEPTIDES AND PROTEINS; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA; VIRUS VECTOR;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GAG POL GENE; GENE CONSTRUCT; GENE FUNCTION; GENE SEQUENCE; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN MOTIF; PROVIRUS; RNA PACKAGING; RNA TRANSLATION; STRUCTURAL GENE; VIRION; VIROGENESIS; VIRUS GENOME; VIRUS PARTICLE;

CELL LINE; FLOW CYTOMETRY; HIV-2; HUMANS; RNA, VIRAL; VIRION; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

EID: 79960395678     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00562-11     Document Type: Article

References (50)

1. Anderson, J. A., E. H. Bowman, and W. S. Hu. 1998. Retroviral recombination rates do not increase linearly with marker distance and are limited by the size of the recombining subpopulation. J. Virol. 72:1195-1202.
2. Arya, S. K., M. Zamani, and P. Kundra. 1998. Human immunodeficiency virus type 2 lentivirus vectors for gene transfer: expression and potential for helper virus-free packaging. Hum. Gene Ther. 9:1371-1380.
3. Baig, T. T., J. M. Lanchy, and J. S. Lodmell. 2007. HIV-2 RNA dimerization is regulated by intramolecular interactions in vitro. RNA 13:1341-1354.
4. Baig, T. T., J. M. Lanchy, and J. S. Lodmell. 2009. Randomization and in vivo selection reveal a GGRG motif essential for packaging human immunodeficiency virus type 2 RNA. J. Virol. 83:802-810.
5. Butsch, M., and K. Boris-Lawrie. 2002. Destiny of unspliced retroviral RNA: ribosome and/or virion? J. Virol. 76:3089-3094.
6. Butsch, M., and K. Boris-Lawrie. 2000. Translation is not required To generate virion precursor RNA in human immunodeficiency virus type 1-infected T cells. J. Virol. 74:11531-11537.
7. Chen, J., 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.
8. Chen, J., D. Powell, and W. S. Hu. 2006. High frequency of genetic recombination is a common feature of primate lentivirus replication. J. Virol. 80:9651-9658.
9. Chin, M. P., J. Chen, O. A. Nikolaitchik, and W. S. Hu. 2007. Molecular determinants of HIV-1 intersubtype recombination potential. Virology 363: 437-446.
10. Chin, M. P., T. D. Rhodes, J. Chen, W. Fu, and W. S. Hu. 2005. Identification of a major restriction in HIV-1 intersubtype recombination. Proc. Natl. Acad. Sci. U. S. A. 102:9002-9007.
11. Delviks, K. A., W. S. Hu, and V. K. Pathak. 1997. Psi- vectors: murine leukemia virus-based self-inactivating and self-activating retroviral vectors. J. Virol. 71:6218-6224.
12. Delviks, K. A., and V. K. Pathak. 1999. Effect of distance between homologous sequences and 3' homology on the frequency of retroviral reverse transcriptase template switching. J. Virol. 73:7923-7932.
13. Dirac, A. M., H. Huthoff, J. Kjems, and B. Berkhout. 2001. The dimer initiation site hairpin mediates dimerization of the human immunodeficiency virus, type 2 RNA genome. J. Biol. Chem. 276:32345-32352.
14. Dorman, N., and A. Lever. 2000. Comparison of viral genomic RNA sorting mechanisms in human immunodeficiency virus type 1 (HIV-1), HIV-2, and Moloney murine leukemia virus. J. Virol. 74:11413-11417.
15. D'Souza, V., A. Dey, D. Habib, and M. F. Summers. 2004. NMR structure of the 101-nucleotide core encapsidation signal of the Moloney murine leukemia virus. J. Mol. Biol. 337:427-442.
16. D'Souza, V., and M. F. Summers. 2004. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431:586-590.
17. Flynn, J. A., W. An, S. R. King, and A. Telesnitsky. 2004. Nonrandom dimerization of murine leukemia virus genomic RNAs. J. Virol. 78:12129-12139.
18. Flynn, J. A., and A. Telesnitsky. 2006. Two distinct Moloney murine leukemia virus RNAs produced from a single locus dimerize at random. Virology 344:391-400.
19. Fusco, D., et al. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr. Biol. 13:161-167.
20. Gao, F., et al. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436-441.
21. Gao, F., et al. 1992. Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358:495-499.
22. Gherghe, C., 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.
23. Griffin, S. D., J. F. Allen, and A. M. Lever. 2001. The major human immunodeficiency virus type 2 (HIV-2) packaging signal is present on all HIV-2 RNA species: cotranslational RNA encapsidation and limitation of Gag protein confer specificity. J. Virol. 75:12058-12069.
24. Hirsch, V. M., R. A. Olmsted, M. Murphey-Corb, R. H. Purcell, and P. R. Johnson. 1989. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339:389-392.
25. Hu, W. S., E. H. Bowman, K. A. Delviks, and V. K. Pathak. 1997. Homologous recombination occurs in a distinct retroviral subpopulation and exhibits high negative interference. J. Virol. 71:6028-6036.
26. Hussein, I. T., 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.
27. Kaye, J. F., and A. M. Lever. 1999. Human immunodeficiency virus types 1 and 2 differ in the predominant mechanism used for selection of genomic RNA for encapsidation. J. Virol. 73:3023-3031.
28. Kharytonchyk, S. A., A. I. Kireyeva, A. B. Osipovich, and I. K. Fomin. 2005. Evidence for preferential copackaging of Moloney murine leukemia virus genomic RNAs transcribed in the same chromosomal site. Retrovirology 2:3.
29. Lanchy, J. M., and J. S. Lodmell. 2002. Alternate usage of two dimerization initiation sites in HIV-2 viral RNA in vitro. J. Mol. Biol. 319:637-648.
30. Lanchy, J. M., and J. S. Lodmell. 2007. An extended stem-loop 1 is necessary for human immunodeficiency virus type 2 replication and affects genomic RNA encapsidation. J. Virol. 81:3285-3292.
31. Lanchy, J. M., C. A. Rentz, J. D. Ivanovitch, and J. S. Lodmell. 2003. Elements located upstream and downstream of the major splice donor site influence the ability of HIV-2 leader RNA to dimerize in vitro. Biochemistry 42:2634-2642.
32. Leitner, T., et al. 1993. Analysis of heterogeneous viral populations by direct DNA sequencing. Biotechniques 15:120-127.
33. Lemey, P., et al. 2003. Tracing the origin and history of the HIV-2 epidemic. Proc. Natl. Acad. Sci. U. S. A. 100:6588-6592.
34. Levin, J. G., P. M. Grimley, J. M. Ramseur, and I. K. Berezesky. 1974. Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D. J. Virol. 14:152-161.
35. Levin, J. G., and M. J. Rosenak. 1976. Synthesis of murine leukemia virus proteins associated with virions assembled in actinomycin D-treated cells: evidence for persistence of viral messenger RNA. Proc. Natl. Acad. Sci. U. S. A. 73:1154-1158.
36. L'Hernault, A., J. S. Greatorex, R. A. Crowther, and A. M. Lever. 2007. Dimerisation of HIV-2 genomic RNA is linked to efficient RNA packaging, normal particle maturation and viral infectivity. Retrovirology 4:90.
37. McCutchan, F. E. 2006. Global epidemiology of HIV. J. Med. Virol. 78(Suppl. 1):S7-S12.
38. Moore, M. D., 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.
39. Moore, M. D., and W. S. Hu. 2009. HIV-1 RNA dimerization: it takes two to tango. AIDS Rev. 11:91-102.
40. Naldini, L., et al. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
41. Nikolaitchik, O., T. D. Rhodes, D. Ott, and W. S. Hu. 2006. Effects of mutations in the human immunodeficiency virus type 1 Gag gene on RNA packaging and recombination. J. Virol. 80:4691-4697.
42. Paillart, J. C., M. Shehu-Xhilaga, R. Marquet, and J. Mak. 2004. Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol. 2:461-472.
43. Poeschla, E., et al. 1998. Identification of a human immunodeficiency virus type 2 (HIV-2) encapsidation determinant and transduction of nondividing human cells by HIV-2-based lentivirus vectors. J. Virol. 72:6527-6536.
44. Rasmussen, S. V., and F. S. Pedersen. 2006. Co-localization of gammaretroviral RNAs at their transcription site favours co-packaging. J. Gen. Virol. 87:2279-2289.
45. Rhodes, T. D., O. Nikolaitchik, J. Chen, D. Powell, and W. S. Hu. 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.
46. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Santiago, M. L., et al. 2005. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J. Virol. 79:12515-12527.
48. St. Louis, D. C., 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.
49. Van Heuverswyn, F., et al. 2006. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444:164.
50. Yee, J. K., et al. 1994. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 91:9564-9568.