Capsid is an important determinant for functional complementation of murine leukemia virus and spleen necrosis virus Gag proteins

Virology

Volumn 360, Issue 2, 2007, Pages 388-397

  Lee, Sook Kyung ^a   Boyko, Vitaly ^a   Hu, Wei Shau ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Capsid; Coassembly; Complementation; Infectivity; Phenotypic mixing; Retroviruses

Indexed keywords

GAG PROTEIN; VIRUS PROTEIN;

ARTICLE; FLUORESCENCE ANALYSIS; GENETIC COMPLEMENTATION; MURINE LEUKEMIA VIRUS; NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RETROVIRUS; SPLEEN; SPLEEN NECROSIS ONCOVIRUS; VIRUS CAPSID; VIRUS REPLICATION;

ANIMALS; CAPSID PROTEINS; CELL LINE; CELLS; DOGS; GENE PRODUCTS, GAG; GENETIC COMPLEMENTATION TEST; HUMANS; LEUKEMIA VIRUS, MURINE; MICROSCOPY, CONFOCAL; PROTEIN STRUCTURE, TERTIARY; TRAGER DUCK SPLEEN NECROSIS VIRUS; VIRUS REPLICATION;

MIRIDAE; MURINE LEUKEMIA VIRUS; SPLEEN NECROSIS VIRUS;

EID: 33947579105     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.10.038     Document Type: Article

References (62)

1. Ako-Adjei D., Johnson M.C., and Vogt V.M. The retroviral capsid domain dictates virion size, morphology, and coassembly of gag into virus-like particles. J. Virol. 79 21 (2005) 13463-13472
2. Alin K., and Goff S.P. Amino acid substitutions in the CA protein of Moloney murine leukemia virus that block early events in infection. Virology 222 2 (1996) 339-351
3. Bennett R.P., and Wills J.W. Conditions for copackaging rous sarcoma virus and murine leukemia virus Gag proteins during retroviral budding. J. Virol. 73 3 (1999) 2045-2051
4. Bennett R.P., Nelle T.D., and Wills J.W. Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus gag proteins. J. Virol. 67 11 (1993) 6487-6498
5. Berkowitz R.D., Ohagen A., Hoglund S., and Goff S.P. Retroviral nucleocapsid domains mediate the specific recognition of genomic viral RNAs by chimeric Gag polyproteins during RNA packaging in vivo. J. Virol. 69 10 (1995) 6445-6456
6. Boyko V., Leavitt M., Gorelick R., Fu W., Nikolaitchik O., Pathak V.K., Nagashima K., and Hu W.S. Coassembly and complementation of gag proteins from HIV-1 and HIV-2, two distinct human pathogens. Mol. Cell 23 2 (2006) 281-287
7. Buckman J.S., Bosche W.J., and Gorelick R.J. Human immunodeficiency virus type 1 nucleocapsid zn(2+) fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J. Virol. 77 2 (2003) 1469-1480
8. Cairns T.M., and Craven R.C. Viral DNA synthesis defects in assembly-competent Rous sarcoma virus CA mutants. J. Virol. 75 1 (2001) 242-250
9. Campbell S., and Rein A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73 3 (1999) 2270-2279
10. Campbell S., and Vogt V.M. 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 6 (1997) 4425-4435
11. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., and Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 99 12 (2002) 7877-7882
12. Certo J.L., Shook B.F., Yin P.D., Snider J.T., and Hu W.S. Nonreciprocal pseudotyping: murine leukemia virus proteins cannot efficiently package spleen necrosis virus-based vector RNA. J. Virol. 72 7 (1998) 5408-5413
13. Certo J.L., Kabdulov T.O., Paulson M.L., Anderson J.A., and Hu W.S. The nucleocapsid domain is responsible for the ability of spleen necrosis virus (SNV) Gag polyprotein to package both SNV and murine leukemia virus RNA. J. Virol. 73 11 (1999) 9170-9177
14. Chalfie M., Tu Y., Euskirchen G., Ward W.W., and Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 263 5148 (1994) 802-805
15. Chen B.K., Rousso I., Shim S., and Kim P.S. Efficient assembly of an HIV-1/MLV Gag-chimeric virus in murine cells. Proc. Natl. Acad. Sci. U.S.A. 98 26 (2001) 15239-15244
16. Cheslock S.R., Anderson J.A., Hwang C.K., Pathak V.K., and Hu W.S. Utilization of nonviral sequences for minus-strand DNA transfer and gene reconstitution during retroviral replication. J. Virol. 74 20 (2000) 9571-9579
17. Cheslock S.R., Poon D.T., Fu W., Rhodes T.D., Henderson L.E., Nagashima K., McGrath C.F., and Hu W.S. Charged assembly helix motif in murine leukemia virus capsid: an important region for virus assembly and particle size determination. J. Virol. 77 12 (2003) 7058-7066
18. Craven R.C., and Parent L.J. Dynamic interactions of the Gag polyprotein. Curr. Top. Microbiol. Immunol. 214 (1996) 65-94
19. Deminie C.A., and Emerman M. Incorporation of human immunodeficiency virus type 1 Gag proteins into murine leukemia virus virions. J. Virol. 67 11 (1993) 6499-6506
20. Demirov D.G., Ono A., Orenstein J.M., and Freed E.O. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. U.S.A. 99 2 (2002) 955-960
21. DuBridge R.B., Tang P., Hsia H.C., Leong P.M., Miller J.H., and Calos M.P. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7 1 (1987) 379-387
22. Dupraz P., and Spahr P.F. Specificity of Rous sarcoma virus nucleocapsid protein in genomic RNA packaging. J. Virol. 66 8 (1992) 4662-4670
23. Embretson J.E., and Temin H.M. Lack of competition results in efficient packaging of heterologous murine retroviral RNAs and reticuloendotheliosis virus encapsidation-minus RNAs by the reticuloendotheliosis virus helper cell line. J. Virol. 61 9 (1987) 2675-2683
24. Forshey B.M., von Schwedler U., Sundquist W.I., and Aiken C. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76 11 (2002) 5667-5677
25. Freed E.O. Viral late domains. J. Virol. 76 10 (2002) 4679-4687
26. Fu W., and Hu W.S. Functional replacement of nucleocapsid flanking regions by heterologous counterparts with divergent primary sequences: effects of chimeric nucleocapsid on the retroviral replication cycle. J. Virol. 77 1 (2003) 754-761
27. Fu W., Dang Q., Nagashima K., Freed E.O., Pathak V.K., and Hu W.S. Effects of Gag mutation and processing on retroviral dimeric RNA maturation. J. Virol. 80 3 (2006) 1242-1249
28. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Cote M., Rich R.L., Myszka D.G., and Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 1 (2001) 55-65
29. Gheysen D., Jacobs E., de Foresta F., Thiriart C., Francotte M., Thines D., and De Wilde M. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59 1 (1989) 103-112
30. Gorelick R.J., Chabot D.J., Rein A., Henderson L.E., and Arthur L.O. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. J. Virol. 67 7 (1993) 4027-4036
31. Gorelick R.J., Fu W., Gagliardi T.D., Bosche W.J., Rein A., Henderson L.E., and Arthur L.O. Characterization of the block in replication of nucleocapsid protein zinc finger mutants from Moloney murine leukemia virus. J. Virol. 73 10 (1999) 8185-8195
32. Gottlinger H.G. The HIV-1 assembly machine. AIDS 15 Suppl. 5 (2001) S13-S20
33. Gritz L., and Davies J. Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 25 2-3 (1983) 179-188
34. Hansen M.S., and Barklis E. Structural interactions between retroviral Gag proteins examined by cysteine cross-linking. J. Virol. 69 2 (1995) 1150-1159
35. Hu C.D., and Kerppola T.K. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21 5 (2003) 539-545
36. Kikonyogo A., Bouamr F., Vana M.L., Xiang Y., Aiyar A., Carter C., and Leis J. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. U.S.A. 98 20 (2001) 11199-11204
37. Landau N.R., Page K.A., and Littman D.R. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65 1 (1991) 162-169
38. Lee S.K., Nagashima K., and Hu W.S. Cooperative effect of gag proteins p12 and capsid during early events of murine leukemia virus replication. J. Virol. 79 7 (2005) 4159-4169
39. Martinez I., and Dornburg R. Improved retroviral packaging lines derived from spleen necrosis virus. Virology 208 1 (1995) 234-241
40. Miller A.D., and Buttimore C. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell. Biol. 6 8 (1986) 2895-2902
41. Moody A.M., Chui D., Reche P.A., Priatel J.J., Marth J.D., and Reinherz E.L. Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell 107 4 (2001) 501-512
42. Morikawa Y., Goto T., and Sano K. In vitro assembly of human immunodeficiency virus type 1 Gag protein. J. Biol. Chem. 274 39 (1999) 27997-82002
43. Mortuza G.B., Haire L.F., Stevens A., Smerdon S.J., Stoye J.P., and Taylor I.A. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 431 7007 (2004) 481-485
44. Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., and Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20 1 (2002) 87-90
45. Oshima M., Muriaux D., Mirro J., Nagashima K., Dryden K., Yeager M., and Rein A. Effects of blocking individual maturation cleavages in murine leukemia virus gag. J. Virol. 78 3 (2004) 1411-1420
46. Parent L.J., Bennett R.P., Craven R.C., Nelle T.D., Krishna N.K., Bowzard J.B., Wilson C.B., Puffer B.A., Montelaro R.C., and Wills J.W. Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 69 9 (1995) 5455-5460
47. Pornillos O., Garrus J.E., and Sundquist W.I. Mechanisms of enveloped RNA virus budding. Trends Cell Biol. 12 12 (2002) 569-579
48. Riggs J.L., McAllister R.M., and Lennette E.H. Immunofluorescent studies of RD-114 virus replication in cell culture. J. Gen. Virol. 25 1 (1974) 21-29
49. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
50. Schultz A.M., and Rein A. Unmyristylated Moloney murine leukemia virus Pr65gag is excluded from virus assembly and maturation events. J. Virol. 63 5 (1989) 2370-2373
51. Swanstrom R., and Wills J.W. Synthesis, assembly, and processing of viral proteins. In: Coffin J.M., Hughes S.H., and Varmus H.E. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 263-334
52. Tang S., Murakami T., Agresta B.E., Campbell S., Freed E.O., and Levin J.G. Human immunodeficiency virus type 1 N-terminal capsid mutants that exhibit aberrant core morphology and are blocked in initiation of reverse transcription in infected cells. J. Virol. 75 19 (2001) 9357-9366
53. Temin H.M., and Mizutani S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226 5252 (1970) 1211-1213
54. Thomas J.A., Gagliardi T.D., Alvord W.G., Lubomirski M., Bosche W.J., and Gorelick R.J. Human immunodeficiency virus type 1 nucleocapsid zinc-finger mutations cause defects in reverse transcription and integration. Virology 353 1 (2006) 41-51
55. von Schwedler U.K., Stray K.M., Garrus J.E., and Sundquist W.I. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77 9 (2003) 5439-5450
56. Weaver T.A., and Panganiban A.T. N myristoylation of the spleen necrosis virus matrix protein is required for correct association of the Gag polyprotein with intracellular membranes and for particle formation. J. Virol. 64 8 (1990) 3995-4001
57. Wills J.W., and Craven R.C. Form, function, and use of retroviral gag proteins. AIDS 5 6 (1991) 639-654
58. Yamashita M., and Emerman M. Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J. Virol. 78 11 (2004) 5670-5678
59. Yuan B., Li X., and Goff S.P. Mutations altering the Moloney murine leukemia virus p12 Gag protein affect virion production and early events of the virus life cycle. EMBO J. 18 17 (1999) 4700-4710
60. Yuan B., Fassati A., Yueh A., and Goff S.P. Characterization of Moloney murine leukemia virus p12 mutants blocked during early events of infection. J. Virol. 76 21 (2002) 10801-10810
61. Zhang Y., and Barklis E. Nucleocapsid protein effects on the specificity of retrovirus RNA encapsidation. J. Virol. 69 9 (1995) 5716-5722
62. Zhang W.H., Hwang C.K., Hu W.S., Gorelick R.J., and Pathak V.K. Zinc finger domain of murine leukemia virus nucleocapsid protein enhances the rate of viral DNA synthesis in vivo. J. Virol. 76 15 (2002) 7473-7484