Murine Leukemia Virus Particle Assembly Quantitated by Fluorescence Microscopy: Role of Gag-Gag Interactions and Membrane Association

Journal of Virology

Volumn 77, Issue 21, 2003, Pages 11651-11660

  Andrawiss, Mariam ^a   Takeuchi, Yasuhiro ^a   Hewlett, Lindsay ^a   Collins, Mary ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Windeyer Institute   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CHIMERIC PROTEIN; GAG FLUORESCENT FUSION PROTEIN; GAG PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN P133L; PROTEIN P150L; PROTEIN R119C; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BUDDING; CHANNEL GATING; CHIMERA; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE MUTATION; INHIBITION KINETICS; MEMBRANE BINDING; MEMBRANE FILTER; MURINE LEUKEMIA VIRUS; MYRISTYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SEDIMENTOLOGY; VELOCITY; VIRUS PARTICLE; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CAPSID; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; COS CELLS; GENE PRODUCTS, GAG; HUMANS; LEUKEMIA VIRUS, MURINE; LUMINESCENT PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT FUSION PROTEINS; SPODOPTERA; VIRION; VIRUS ASSEMBLY;

EID: 0142060842     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.21.11651-11660.2003     Document Type: Article

References (52)

1. Alin, K., and S. P. Goff. 1996. Mutational analysis of interactions between the Gag precursor proteins of murine leukemia viruses. Virology 216:418-424.
2. Alin, K., and S. P. Goff. 1996. Amino acid substitutions in the CA protein of Moloney murine leukemia virus that block early events in infection. Virology 222:339-351.
3. Barklis, E., J. McDermott, S. Wilkens, E. Schabtach, M. F. Schmid, S. Fuller, S. Karanjia, Z. Love, R. Jones, Y. Rui, X. Zhao, and D. Thompson. 1997. Structural analysis of membrane-bound retrovirus capsid proteins. EMBO J. 16:1199-1213.
4. Bennett, R. P., and J. W. Wills. 1999. Conditions for copackaging Rous sarcoma virus and murine leukemia virus Gag proteins during retroviral budding. J. Virol. 73:2045-2051.
5. Bowzard, J. B., R. P. Bennett, N. K. Krishna, S. M. Ernst, A. Rein, and J. W. Wills. 1998. Importance of basic residues in the nucleocapsid sequence for retrovirus Gag assembly and complementation rescue. J. Virol. 72:9034-9044.
6. Buchschacher, G. L., L. Yu, F. Murai, T. Friedman, and A. Miyanohara. 1999. Association of murine leukemia virus Pol with virions, independent of Gag-Pol expression. J. Virol. 73:9632-9637.
7. Campbell, S., and V. M. Vogt. 1997. In vitro assembly of virus-like particles with Rous sarcoma virus Gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles. J. Virol. 71:4425-4435.
8. Carriere, C., B. Gay, N. Chazal, N. Morin, and P. Boulanger. 1995. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles. J. Virol. 69:2366-2377.
9. Chiu, C. S., E. Kartalov, M. Unger, S. Quake, and H. A. Lester. 2001. Single-molecule measurements calibrate green fluorescent protein surface densities on transparent beads for use with 'knock-in' animals and other expression systems. J. Neurosci. Methods 105:55-63.
10. Chiu, H. C., F. D. Wang, S. Y. Yao, and C. T. Wang. 2002. Effects of gag mutations on human immunodeficiency virus type 1 particle assembly, processing, and cyclophilin A incorporation. J. Med. Virol. 68:156-163.
11. Cimarelli, A., S. Sandin, S. Hoglund, and J. Luban. 2000. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J. Virol. 74:3046-3057.
12. Cosset, F. L., F. J. Morling, Y. Takeuchi, R. A. Weiss, M. K. Collins, and S. J. Russell. 1995. Retroviral retargeting by envelopes expressing an N-terminal binding domain. J. Virol. 69:6314-6322.
13. Craven, R. C., A. E. Leure-duPree, R. A. Weldon, Jr., and J. W. Wills. 1995. Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J. Virol. 69:4213-4227.
14. Dawson, L., and X. F. Yu. 1998. The role of nucleocapsid of HIV-1 in virus assembly. Virology 251:141-157.
15. Dorfman, T., A. Bukovsky, A. Ohagen, S. Hoglund, and H. G. Gottlinger. 1994. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68:8180-8187.
16. Felsenstein, K. M., and S. P. Goff. 1988. Expression of the Gag-Pol fusion protein of Moloney murine leukemia virus without the Gag protein does not induce virion formation or proteolytic processing. J. Virol. 62:2179-2182.
17. Ganser, B. K., S. Li, V. Y. Klishko, J. T. Finch, and W. I. Sundquist. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-83.
18. Gottlinger, H. G., J. G. Sodroski, and W. A. Haseltine. 1989. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:5778-5815.
19. Hansen, M., L. Jelinek, S. Whiting, and E. Barklis. 1990. Transport and assembly of Gag proteins into Moloney murine leukemia virus. J. Virol. 64:5306-5316.
20. Hansen, M. S., and E. Barklis. 1995. Structural interactions between retroviral Gag proteins examined by cysteine cross-linking. J. Virol. 69:1150-1159.
21. Hartley, J. W., and W. P. Rowe. 1976. Naturally occurring murine leukemia viruses in wild mice: characterization of a new "amphotropic" class. J. Virol. 19:19-25.
22. Jones, T. A., G. Blaug, M. Hansen, and E. Barklis. 1990. Assembly of Gag-β-galactosidase proteins into retrovirus particles. J. Virol. 64:2265-2279.
23. Kingston, R. L., T. Fitzon-Ostendorp, E. Z. Eisenmesser, G. W. Schatz, V. M. Vogt, C. B. Post, and M. G. Rossmann. 2000. Structure and self-association of the Rous sarcoma virus capsid protein. Struct. Fold Des. 8:617-628.
24. Luban, J., K. B. Alin, K. L. Bossolt, T. Humaran, and S. P. Goff. 1992. Genetic assay for multimerization of retroviral Gag polyproteins. J. Virol. 66:5157-5160.
25. McDonald, D., M. A. Vodicka, G. Lucero, T. M. Svitkina, G. G. Borisy, M. Emerman, and T. J. Hope. 2002. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159:441-452.
26. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-982, 984-986, 989-990.
27. Morikawa, Y., S. Hinata, H. Tomoda, T. Goto, M. Nakai, C. Aizawa, H. Tanaka, and S. Omura. 1996. Complete inhibition of human immunodeficiency virus Gag myristoylation is necessary for inhibition of particle budding. J. Biol. Chem. 271:2868-2873.
28. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
29. Nermut, M. V., H. Frank, and W. Schafer. 1972. Properties of mouse leukemia viruses. 3. Electron microscopic appearance as revealed after conventional preparation techniques as well as freeze-drying and freeze-etching. Virology 49:345-358.
30. Nermut, M. V., D. J. Hockley, J. B. Jowett, I. M. Jones, M. Garreau, and D. Thomas. 1994. Fullerene-like organization of HIV gag-protein shell in virus-like particles produced by recombinant baculovirus. Virology 198:288-296.
31. Ono, A., and E. O. Freed. 1999. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73:4136-4144.
32. Paillart, J. C., and H. G. Gottlinger. 1999. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of Gag membrane targeting. J. Virol. 73:2604-2612.
33. gag and is incorporated into viruslike particles. J. Virol. 66:6304-6313.
34. Pizzato, M., S. A. Marlow, E. D. Blair, and Y. Takeuchi. 1999. Initial binding of murine leukemia virus particles to cells does not require specific Env-receptor interaction. J. Virol. 73:8599-8611.
35. Relcin, A. S., S. Paik, R. D. Berkowitz, J. Luban, I. Lowy, and S. P. Goff. 1995. Linker insertion mutations in the human immunodeficiency virus type 1 gag gene: effects on virion particle assembly, release, and infectivity. J. Virol. 69:642-650.
36. Rein, A., M. R. McClure, N. R. Rice, R. B. Luftig, and A. M. Schultz. 1986. Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proc. Natl. Acad. Sci. USA 83:7246-7250.
37. Rhee, S. S., and E. Hunter. 1987. Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J. Virol. 61:1045-1053.
38. Schultz, A. M., and S. Oroszlan. 1983. In vivo modification of retroviral gag gene-encoded polyproteins by myristic acid. J. Virol. 46:355-361.
39. gag is excluded from virus assembly and maturation events. J. Virol. 63:2370-2373.
40. Schwartzberg, P., J. Colicelli, M. L. Gordon, and S. P. Goff. 1984. Mutations in the gag gene of Moloney murine leukemia virus: effects on production of virions and reverse transcriptase. J. Virol. 49:918-924.
41. Shields, A., W. N. Witte, E. Rothenberg, and D. Baltimore. 1978. High frequency of aberrant expression of Moloney murine leukemia virus in clonal infections. Cell 14:601-609.
42. Simionescu, N., and M. Simionescu. 1976. Galloylglucoses of low molecular weight as mordant in electron microscopy. II. The moiety and functional groups possibly involved in the mordanting effect. J. Cell Biol. 70:622-633.
43. Soneoka, Y., P. M. Cannon, E. E. Ramsdale, J. C. Griffiths, G. Romano, S. M. Kingsman, and A. J. Kingsman. 1995. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23:628-633.
44. Soneoka, Y., S. M. Kingsman, and A. J. Kingsman. 1997. Mutagenesis analysis of the murine leukemia virus matrix protein: identification of regions important for membrane localization and intracellular transport. J. Virol. 71:5549-5559.
45. Spearman, P., R. Horton, L. Ratner, and I. Kuli-Zade. 1997. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism. J. Virol. 71:6582-6592.
46. Spearman, P., J. J. Wang, N. Vander Heyden, and L. Ratner. 1994. Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol. 68:3232-3242.
47. Swanstrom, R., and J. W. Wills. 1997. Synthesis, processing and assembly of viral proteins, p. 263-334. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Tsien, R. Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544.
49. Wills, J. W., C. E. Cameron, C. B. Wilson, Y. Xiang, R. P. Bennett, and J. Leis. 1994. An assembly domain of the Rous sarcoma virus Gag protein required late in budding. J. Virol. 68:6605-6618.
50. Yuan, B., X. Li, and S. P. Goff. 1999. Mutations altering the moloney murine leukemia virus p12 Gag protein affect virion production and early events of the virus life cycle. EMBO J. 18:4700-4710.
51. Zhang, Y., and E. Barklis. 1997. Effects of nucleocapsid mutations on human immunodeficiency virus assembly and RNA encapsidation. J. Virol. 71:6765-6776.
52. Zhang, Y., H. Qian, Z. Love, and E. Barklis. 1998. Analysis of the assembly function of the human immunodeficiency virus type 1 Gag protein nucleocapsid domain. J. Virol. 72:1782-1789.