Secondary structure of the mature ex virio moloney murine leukemia virus genomic RNA dimerization domain

Journal of Virology

Volumn 84, Issue 2, 2010, Pages 898-906

  Gherghe, Cristina ^a   Leonard, Christopher W ^a   Gorelick, Robert J ^b   Weeks, Kevin M ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; GENOMICS; IN VITRO STUDY; MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS; RNA ISOLATION; RNA STRUCTURE; VIRION; VIRUS MORPHOLOGY;

ANIMALS; BASE SEQUENCE; CELL LINE; DIMERIZATION; GENOME, VIRAL; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLONEY MURINE LEUKEMIA VIRUS; NUCLEIC ACID CONFORMATION; RNA, VIRAL; VIRION;

MOLONEY MURINE LEUKEMIA VIRUS; MURINAE;

EID: 73849110514     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01602-09     Document Type: Article

References (51)

1. Adam, M. A., and A. D. Miller. 1988. Identification of a signal in a murine retrovirus that is sufficient for packaging of nonretroviral RNA into virions. J. Virol. 62:3802-3806.
2. Alford, R. L., S. Honda, C. B. Lawrence, and J. W. Belmont. 1991. RNA secondary structure analysis of the packaging signal for Moloney murine leukemia virus. Virology 183:611-619.
3. Anderson, J. A., V. K. Pathak, and W. S. Hu. 2000. Effect of the murine leukemia virus extended packaging signal on the rates and locations of retroviral recombination. J. Virol. 74:6953-6963.
4. Badorrek, C. S., C. M. Gherghe, and K. M. Weeks. 2006. Structure of an RNA switch enforces stringent retroviral genomic RNA dimerization. Proc. Natl. Acad. Sci. U. S. A. 103:13640-13645.
5. Badorrek, C. S., and K. M. Weeks. 2006. Architecture of a gamma retroviral genomic RNA dimer. Biochemistry 45:12664-12672.
6. Badorrek, C. S., and K. M. Weeks. 2005. RNA flexibility in the dimerization domain of a gamma retrovirus. Nature Chem. Biol. 1:104-111.
7. Banks, J. D., A. Yeo, K. Green, F. Cepeda, and M. L. Linial. 1998. A minimal avian retroviral packaging sequence has a complex structure. J. Virol. 72: 6190-6194.
8. Bender, W., Y. H. Chien, S. Chattopadhyay, P. K. Vogt, M. B. Gardner, and N. Davidson. 1978. High-molecular-weight RNAs of AKR, NZB, and wild mouse viruses and avian reticuloendotheliosis virus all have similar dimer structures. J. Virol. 25:888-896.
9. Berkowitz, R., J. Fisher, and S. P. Goff. 1996. RNA packaging. Curr. Top. Microbiol. Immunol. 214:177-218.
10. Bess, J. W. J., P. J. Powell, H. J. Issaq, L. J. Schumack, M. K. Grimes, L. E. Henderson, and L. O. Arthur. 1992. Tightly bound zinc in human immunodeficiency virus type 1, human T-cell leukemia virus type I, and other retroviruses. J. Virol. 66:840-847.
11. Coffin, J. M., S. H. Hughes, and H. E. Varmus. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
12. Deigan, K. E., T. W. Li, D. H. Mathews, and K. M. Weeks. 2009. Accurate SHAPE-directed RNA structure determination. Proc. Natl. Acad. Sci. U. S. A. 106:97-102.
13. D'Souza, V., and M. F. Summers. 2004. Structural basis for packaging the dimeric genome of Moloney murine leukemia virus. Nature 431:586-590.
14. 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.
15. D'Souza, V., and M. F. Summers. 2005. How retroviruses select their genomes. Nat. Rev. Microbiol. 3:643-655.
16. Evans, M. J., E. Bacharach, and S. P. Goff. 2004. RNA sequences in the Moloney murine leukemia virus genome bound by the Gag precursor protein in the yeast three-hybrid system. J. Virol. 78:7677-7684.
17. Fischinger, P. J., C. O. Moore, and T. E. O'Connor. 1969. Isolation and identification of a helper virus found in the Moloney sarcoma-leukemia virus complex. J. Natl. Cancer Inst. 42:605-622.
18. Fu, W., Q. Dang, K. Nagashima, E. O. Freed, V. K. Pathak, and W.-S. Hu. 2006. Effects of Gag mutation and processing on retroviral dimeric RNA maturation. J. Virol. 80:1242-1249.
19. Fu, W., R. J. Gorelick, and A. Rein. 1994. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and proteasedefective virions. J. Virol. 68:5013-5018.
20. Fu, W., and A. Rein. 1993. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 67:5443-5449.
21. Ganser-Pornillos, B. K., M. Yeager, and W. I. Sundquist. 2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203-217.
22. Gherghe, C., and K. M. Weeks. 2006. The SL1-SL2 (stem loop) domain is the primary determinant for stability of the gamma retroviral genomic RNA dimer. J. Biol. Chem. 281:37952-37961.
23. Gherghe, C. M., Z. Shajani, K. A. Wilkinson, G. Varani, and K. M. Weeks. 2008. Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA. J. Am. Chem. Soc. 130:12244-12245.
24. Girard, P. M., B. Bonnet-Mathoniere, D. Muriaux, and J. Paoletti. 1995. A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry 34:9785-9794.
25. Gorelick, R. J., L. E. Henderson, J. P. Hanser, and A. Rein. 1988. Point mutants of Moloney murine leukemia virus that fail to package viral RNA: Evidence for specific RNA recognition by a "zinc finger-like" protein sequence. Proc. Natl. Acad. Sci. U. S. A. 85:8420-8424.
26. Hibbert, C. S., J. Mirro, and A. Rein. 2004. mRNA molecules containing murine leukemia virus packaging signals are encapsidated as dimers. J. Virol. 78:10927-10938.
27. Hoglund, S., A. Ohagen, J. Goncalves, A. T. Panganiban, and D. Gabuzda. 1997. Ultrastructure of HIV-1 genomic RNA. Virology 233:271-279.
28. Kim, C., and I. Tinoco. 2000. A retroviral RNA kissing complex containing only two GC base pairs. Proc. Natl. Acad. Sci. U. S. A. 97:9396-9401.
29. Konings, D. A. M., M. A. Nash, J. V. Maizel, and R. B. Arlinghaus. 1992. Novel GACG-hairpin pair motif in the 5′ untranslated region of type C retroviruses related to murine leukemia virus. J. Virol. 66:632-640.
30. Lee, E., A. Yeo, B. Kraemer, M. Wickens, and M. L. Linial. 1999. The Gag domains required for avian retroviral RNA encapsidation determined by using two independent assays. J. Virol. 73:6282-6292.
31. Levin, J. G., J. Guo, I. Rouzina, and K. Musier-Forsyth. 2005. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol. 80:217-286.
32. Ly, H., and T. G. Parslow. 2002. Bipartite signal for genomic RNA dimerization in Moloney murine leukemia virus. J. Virol. 76:3135-3144.
33. Mangel, W. F., H. Delius, and P. H. Duesberg. 1974. Structure and molecular weight of the 60-70S RNA and the 30-40S RNA of the Rous sarcoma virus. Proc. Natl. Acad. Sci. U. S. A. 71:4541-4545.
34. Mathews, D. H., M. D. Disney, J. L. Childs, S. J. Schroeder, M. Zuker, and D. H. Turner. 2004. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. U. S. A. 101:7287-7292.
35. Merino, E. J., K. A. Wilkinson, J. L. Coughlan, and K. M. Weeks. 2005. RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127:4223-4231.
36. Moore, M. D., W. Fu, O. Nikolaitchik, J. Chen, R. G. Ptak, and W. S. Hu. 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.
37. Mortimer, S. A., and K. M. Weeks. 2007. A fast acting reagent for accurate analysis of RNA secondary and tertiary structure for SHAPE chemistry. J. Am. Chem. Soc. 129:4144-4145.
38. Murti, K. G., M. Bondurant, and A. Tereba. 1981. Secondary structural features in the 70S RNAs of Moloney murine leukemia and Rous sarcoma viruses as observed by electron microscopy. J. Virol. 37:411-419.
39. Oroudjev, E. M., P. C. E. Kang, and L. A. Kohlstaedt. 1999. An additional dimer linkage structure in Moloney murine leukemia virus RNA. J. Mol. Biol. 291:603-613.
40. Paillart, J.-C., M. Dettenhofer, X.-F. Yu, C. Ehresmann, B. Ehresmann, and R. Marquet. 2004. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem. 279:48397-48403.
41. 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.
42. Prats, A. C., C. Roy, P. A. Wang, M. Erard, V. Housset, C. Gabus, C. Paoletti, and J. L. Darlix. 1990. cis Elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64:774-783.
43. Rein, A., L. E. Henderson, and J. G. Levin. 1998. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci. 23:297-301.
44. Sakuragi, J., A. Iwamoto, and T. Shioda. 2002. Dissociation of genome dimerization from packaging functions and virion maturation of human immunodeficiency virus type 1. J. Virol. 76:959-967.
45. Sakuragi, J., T. Shioda, and A. T. Panganiban. 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.
46. Thomas, J. A., T. D. Gagliardi, W. G. Alvord, M. Lubomirski, W. J. Bosche, and R. J. Gorelick. 2006. Human immunodeficiency virus type 1 nucleocapsid zinc-finger mutations cause defects in reverse transcription and integration. Virology 353:41-51.
47. Tounekti, N., M. Mougel, C. Roy, R. Marquet, J. Darlix, J. Paoletti, B. Ehresmann, and C. Ehresmann. 1992. Effect of dimerization on the conformation of the encapsidation psi domain of the Moloney murine leukemia virus. J. Mol. Biol. 223:205-220.
48. Vasa, S. M., N. Guex, K. A. Wilkinson, K. M. Weeks, and M. C. Giddings. 2008. ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. RNA 14:1979-1990.
49. Wilkinson, K. A., R. J. Gorelick, S. Vasa, N. Guex, A. Rein, D. H. Matthews, M. C. Giddings, and K. M. Weeks. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6:e96.
50. Wilkinson, K. A., E. J. Merino, and K. M. Weeks. 2006. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc. 1:1610-1616.
51. Yeager, M., E. M. Wilson-Kubalek, S. G. Weiner, P. O. Brown, and A. Rein. 1998. Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: Implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. U. S. A. 95:7299-7304.