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J Virol. 1993 September; 67(9): 5443-5449

Maturation of dimeric viral RNA of Moloney murine leukemia virus.

W Fu and A Rein

Laboratory of Molecular Virology and Carcinogenesis, NCI-Frederick Cancer Research and Development Center, Maryland 21702.

ABSTRACT

We have analyzed the dimeric RNA present in Moloney murine leukemia virus (MoMuLV) particles. We found that the RNA in newly released virions is in a conformation different from that in mature virions, since it has a different electrophoretic mobility in nondenaturing agarose gels and dissociates into monomers at a lower temperature. On the basis of these results, we suggest that the RNA initially packaged into nascent virions is already dimeric but that the dimer undergoes a maturation process after the virus is released from the cell. In further experiments, we tested the possibility that this maturation event is linked to the maturation cleavage of the virion proteins, which is catalyzed by the viral protease (PR). We found that the dimeric RNA isolated from PR- mutant virions resembles that from immature virions: it has a lower electrophoretic mobility and a lower sedimentation rate, and it also dissociates at a lower temperature than does RNA from mature wild-type virions. When Kirsten sarcoma virus is rescued by a PR- mutant or by a somewhat leaky cysteine array mutant of MoMuLV, its RNA also exhibits a electrophoretic mobility lower than that in the wild-type pseudotype. These results suggest that the maturation of dimeric RNA in released virus particles requires the cleavage of the Gag precursor and the presence of an intact cysteine array in the released nucleocapsid protein.


J Virol. 1993 September; 67(9): 5443-5449




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  • Ortiz-Conde, B. A., Hughes, S. H. (1999). Studies of the Genomic RNA of Leukosis Viruses: Implications for RNA Dimerization. J. Virol. 73: 7165-7174 [Abstract] [Full Text]  
  • Ly, H., Nierlich, D. P., Olsen, J. C., Kaplan, A. H. (1999). Moloney Murine Sarcoma Virus Genomic RNAs Dimerize via a Two-Step Process: a Concentration-Dependent Kissing-Loop Interaction Is Driven by Initial Contact between Consecutive Guanines. J. Virol. 73: 7255-7261 [Abstract] [Full Text]  
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  • Bowzard, J. B., Bennett, R. P., Krishna, N. K., Ernst, S. M., Rein, A., Wills, J. W. (1998). Importance of Basic Residues in the Nucleocapsid Sequence for Retrovirus Gag Assembly and Complementation Rescue. J. Virol. 72: 9034-9044 [Abstract] [Full Text]  
  • Pal, B. K., Scherer, L., Zelby, L., Bertrand, E., Rossi, J. J. (1998). Monitoring Retroviral RNA Dimerization In Vivo via Hammerhead Ribozyme Cleavage. J. Virol. 72: 8349-8353 [Abstract] [Full Text]  
  • Yeager, M., Wilson-Kubalek, E. M., Weiner, S. G., Brown, P. O., Rein, A. (1998). Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: Implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. USA 95: 7299-7304 [Abstract] [Full Text]  
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  • Risco, C, Menendez-Arias, L, Copeland, T., Pinto da Silva, P, Oroszlan, S (1995). Intracellular transport of the murine leukemia virus during acute infection of NIH 3T3 cells: nuclear import of nucleocapsid protein and integrase. J. Cell Sci. 108: 3039-3050 [Abstract]  
  • Balakrishnan, M., Fay, P. J., Bambara, R. A. (2001). The Kissing Hairpin Sequence Promotes Recombination within the HIV-I 5' Leader Region. J. Biol. Chem. 276: 36482-36492 [Abstract] [Full Text]  
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