Mutations in the spacer peptide and adjoining sequences in rous sarcoma virus gag lead to tubular budding

Journal of Virology

Volumn 82, Issue 14, 2008, Pages 6788-6797

  Keller, Paul W ^a   Johnson, Marc C ^b   Vogt, Volker M ^a  

^a Department of Obstetrics Gynecology   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GAG PROTEIN P19, ROUS SARCOMA VIRUS;

ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE OVEREXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; INSECT CELL; MURINE LEUKEMIA VIRUS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; ROUS SARCOMA ONCOVIRUS; VIRUS EXPRESSION; AMINO ACID SUBSTITUTION; ANIMAL; ARMYWORM; CELL LINE; CHEMISTRY; CHICKEN; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRION; VIRUS ASSEMBLY;

HEXAPODA; HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; MURINE LEUKEMIA VIRUS; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CHICKENS; GENE PRODUCTS, GAG; GENETIC COMPLEMENTATION TEST; HIV-1; LEUKEMIA VIRUS, MURINE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINATION, GENETIC; ROUS SARCOMA VIRUS; SPODOPTERA; VIRION; VIRUS ASSEMBLY;

EID: 47049101458     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00213-08     Document Type: Article

References (75)

1. Accola, M. A., S. Hoglund, and H. G. Gottlinger. 1998. A putative alphabetical structure which overlaps the capsid-p2 boundary in the human immunodeficiency virus type 1 Gag precursor is crucial for viral particle assembly. J. Virol. 72:2072-2078.
2. Accola, M. A., B. Strack, and H. G. Gottlinger. 2000. Efficient particle production by minimal Gag constructs which retain the carboxy-terminal domain of human immunodeficiency virus type 1 capsid-p2 and a late assembly domain. J. Virol. 74:5395-5402.
3. Adamson, C. S., S. D. Ablan, I. Boeras, R. Goila-Gaur, F. Soheilian, K. Nagashima, F. Li, K. Salzwedel, M. Sakalian, C. T. Wild, and E. O. Freed. 2006. In vitro resistance to the human immunodeficiency virus type 1 maturation inhibitor PA-457 (Bevirimat). J. Virol. 80:10957-10971.
4. Ako-Adjei, D., M. C. Johnson, and V. M. Vogt. 2005. The retroviral capsid domain dictates virion size, morphology, and coassembly of Gag into virus-like particles. J. Virol. 79:13463-13472.
5. Briggs, J. A. G., M. C. Johnson, M. N. Simon, S. D. Fuller, and V. M. Vogt. 2006. Cryo-electron microscopy reveals conserved and divergent features of Gag packing in immature particles of Rous sarcoma virus and human immunodeficiency virus. J. Mol. Biol. 355:157-168.
6. Briggs, J. A. G., M. N. Simon, I. Gross, H. G. Krausslich, S. D. Fuller, V. M. Vogt, and M. C. Johnson. 2004. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11:672-675.
7. Briggs, J. A. G., T. Wilk, R. Welker, H. G. Krausslich, and S. D. Fuller. 2003. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22:1707-1715.
8. Campbell, S., R. J. Fisher, E. M. Towler, S. Fox, H. J. Issaq, T. Wolfe, L. R. Phillips, and A. Rein. 2001. Modulation of HIV-like particle assembly in vitro by inositol phosphates. Proc. Natl. Acad. Sci. USA 98:10875-10879.
9. 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.
10. Campos-Olivas, R., J. L. Newman, and M. F. Summers. 2000. Solution structure and dynamics of the Rous sarcoma virus capsid protein and comparison with capsid proteins of other retroviruses. J. Mol. Biol. 296:633-649.
11. Cheslock, S. R., D. T. K. Poon, W. Fu, T. D. Rhodes, L. E. Henderson, K. Nagashima, C. F. McGrath, and W. S. Hu. 2003. Charged assembly helix motif in murine leukemia virus capsid: an important region for virus assembly and particle size determination. J. Virol. 77:7058-7066.
12. Craven, R., A. E. Leure-DuPree, C. R. Erdie, C. B. Wilson, and J. W. Wills. 1993. Necessity of the spacer peptide between CA and NC in the Rous sarcoma virus Gag protein. J. Virol. 67:6246-6252.
13. Ehrlich, L. S., T. B. Liu, S. Scarlata, B. Chu, and C. A. Carter. 2001. HIV-1 capsid protein forms spherical (immature-like) and tubular (mature-like) particles in vitro: structure switching by pH-induced conformational changes. Biophys. J. 81:586-594.
14. Gamble, T. R., S. H. Yoo, F. F. Vajdos, U. K. von Schwedler, D. K. Worthylake, H. Wang, J. P. McCutcheon, W. I. Sundquist, and C. P. Hill. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
15. Ganser, B. K., A. Cheng, W. I. Sundquist, and M. Yeager. 2003. Three-dimensional structure of the M-MuLV CA protein on a lipid monolayer: a general model for retroviral capsid assembly. EMBO J. 22:2886-2892.
16. 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.
17. Ganser-Pornillos, B. K., A. Cheng, and M. Yeager. 2007. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131:70-79.
18. Ganser-Pornillos, B. K., U. K. von Schwedler, K. M. Stray, C. Aiken, and W. I. Sundquist. 2004. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78:2545-2552.
19. Garrus, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, K. M. Stray, M. Cote, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
20. Gay, B., J. Tournier, N. Chazal, C. Carriere, and P. Boulanger. 1998. Morphopoietic determinants of HIV-1 Gag particles assembled in baculovirus-infected cells. Virology 247:160-169.
21. Gross, I., H. Hohenberg, and H. G. Krausslich. 1997. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249:592-600.
22. Gross, I., H. Hohenberg, T. Wilk, K. Wiegers, M. Grattinger, B. Muller, S. Fuller, and H. G. Krausslich. 2000. A conformational switch controlling HIV-1 morphogenesis. EMBO J. 19:103-113.
23. Guo, X. F., J. Hu, J. B. Whitney, R. S. Russell, and C. Liang. 2004. Important role for the CA-NC spacer region in the assembly of bovine immunodeficiency virus Gag protein. J. Virol. 78:551-560.
24. Guo, X. F., and C. Liang. 2005. Opposing effects of the M368A point mutation and deletion of the SP1 region on membrane binding of human immunodeficiency virus type 1 Gag. Virology 335:232-241.
25. Guo, X. F., A. Roldan, J. Hu, M. A. Wainberg, and C. Liang. 2005. Mutation of the SP1 sequence impairs both multimerization and membrane-binding activities of human immunodeficiency virus type 1 Gag. J. Virol. 79:1803-1812.
26. Guo, X. F., B. B. Roy, J. Hu, A. Roldan, M. A. Wainberg, and C. Liang. 2005. The R362A mutation at the C-terminus of CA inhibits packaging of human immunodeficiency virus type 1 RNA. Virology 343:190-200.
27. Ivanov, D., J. R. Stone, J. L. Maki, T. Collins, and G. Wagner. 2005. Mammalian SCAN domain dimer is a domain-swapped homolog of the HIV capsid C-terminal domain. Mol. Cell 17:137-143.
28. Ivanov, D., O. V. Tsodikov, J. Kasanov, T. Ellenberger, G. Wagner, and T. Collins. 2007. Domain-swapped dimerization of the HIV-1 capsid C-terminal domain. Proc. Natl. Acad. Sci. USA 104:4353-4358.
29. Johnson, M. C., H. M. Scobie, Y. M. Ma, and V. M. Vogt. 2002. Nucleic acid-independent retrovirus assembly can be driven by dimerization. J. Virol. 76:11177-11185.
30. Johnson, M. C., H. M. Scobie, and V. M. Vogt. 2001. PR domain of Rous sarcoma virus Gag causes an assembly/budding defect in insect cells. J. Virol. 75:4407-4412.
31. Jouvenet, N., S. J. Neil, C. Bess, M. C. Johnson, C. A. Virgen, S. M. Simon, and P. D. Bieniasz. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4:e435.
32. Kanamoto, T., Y. Kashiwada, K. Kanbara, K. Gotoh, M. Yoshimori, T. Goto, K. Sano, and H. Nakashima. 2001. Anti-human immunodeficiency virus activity of YK-FH312 (a betulinic acid derivative), a novel compound blocking viral maturation. Antimicrob. Agents Chemother. 45:1225-1230.
33. Kaye, J. F., and A. M. L. Lever. 1998. Nonreciprocal packaging of human immunodeficiency virus type 1 and type 2 RNA: a possible role for the p2 domain of Gag in RNA encapsidation. J. Virol. 72:5877-5885.
34. 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. Structure 8:617-628.
35. Krausslich, H. G., M. Facke, A. M. Heuser, J. Konvalinka, and H. Zentgraf. 1995. The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J. Virol. 69:3407-3419.
36. Krishna, N. K., S. Campbell, V. M. Vogt, and J. W. Wills. 1998. Genetic determinants of Rous sarcoma virus particle size. J. Virol. 72:564-577.
37. Lanman, J., T. T. Lam, S. Barnes, M. Sakalian, M. R. Emmett, A. G. Marshall, and P. E. Prevelige, Jr. 2003. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325:759-772.
38. Lanman, J., T. T. Lam, M. R. Emmett, A. G. Marshall, M. Sakalian, and P. E. Prevelige, Jr. 2004. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol 11:676-677.
39. Larson, D. R., M. C. Johnson, W. W. Webb, and V. M. Vogt. 2005. Visualization of retrovirus budding with correlated light and electron microscopy. Proc. Natl. Acad. Sci. USA 102:15453-15458.
40. Lee, S. K., V. Boyko, and W. S. Hu. 2007. Capsid is an important determinant for functional complementation of murine leukemia virus and spleen necrosis virus Gag proteins. Virology 360:388-397.
41. Lee, S. K., K. Nagashima, and W. S. Hu. 2005. Cooperative effect of gag proteins p12 and capsid during early events of murine leukemia virus replication. J. Virol. 79:4159-4169.
42. Li, F., R. Goila-Gaur, K. Salzwedel, N. R. Kilgore, M. Reddick, C. Matallana, A. Castillo, D. Zoumplis, D. E. Martin, J. M. Orenstein, G. P. Allaway, E. O. Freed, and C. T. Wild. 2003. PA-457: a potent HIV inhibitor that disrupts core condensation by targeting a late step in Gag processing. Proc. Natl. Acad. Sci. USA 100:13555-13560.
43. Li, F., D. Zoumplis, C. Matallana, N. R. Kilgore, M. Reddick, A. S. Yunus, C. S. Adamson, K. Salzwedel, D. E. Martin, G. P. Allaway, E. O. Freed, and C. T. Wild. 2006. Determinants of activity of the HIV-1 maturation inhibitor PA-457. Virology 356:217-224.
44. Li, S., C. P. Hill, W. I. Sundquist, and J. T. Finch. 2000. Image reconstructions of helical assemblies of the HIV-1CA protein. Nature 407:409-413.
45. Liang, C., J. Hu, R. S. Russell, A. Roldan, L. Kleiman, and M. A. Wainberg. 2002. Characterization of a putative alpha-helix across the capsid-SP1 boundary that is critical for the multimerization of human immunodeficiency virus type 1 gag. J. Virol. 76:11729-11737.
46. Liang, C., J. Hu, J. B. Whitney, L. Kleiman, and M. A. Wainberg. 2003. A structurally disordered region at the C terminus of capsid plays essential roles in multimerization and membrane binding of the Gag protein of human immunodeficiency virus type 1. J. Virol. 77:1772-1783.
47. Ma, Y. M., and V. M. Vogt. 2004. Nucleic acid binding-induced gag dimerization in the assembly of Rous sarcoma virus particles in vitro. J. Virol. 78:52-60.
48. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2003. Role of ESCRT-I in retroviral budding. J. Virol. 77:4794-4804.
49. Mayo, K., J. McDermott, and E. Barklis. 2002. Hexagonal organization of Moloney murine leukemia virus capsid proteins. Virology 298:30-38.
50. Medina, G., Y. Zhang, Y. Tang, E. Gottwein, M. L. Vana, F. Bouamr, J. Leis, and C. A. Carter. 2005. The functionally exchangeable L domains in RSV and HIV-1 Gag direct particle release through pathways linked by Tsg101. Traffic 6:880-894.
51. Melamed, D., M. Mark-Danieli, M. Kenan-Eichler, O. Kraus, A. Castiel, N. Laham, T. Pupko, F. Glaser, N. Ben-Tal, and E. Bacharach. 2004. The conserved carboxy terminus of the capsid domain of human immunodeficiency virus type 1 Gag protein is important for virion assembly and release. J. Virol. 78:9675-9688.
52. Morellet, N., S. Druillennec, C. Lenoir, S. Bouaziz, and B. P. Roques. 2005. Helical structure determined by NMR of the HIV-1 (345-392)Gag sequence, surrounding p2: implications for particle assembly and RNA packaging. Protein Sci. 14:375-386.
53. Morikawa, Y., D. J. Hockley, M. V. Nermut, and I. M. Jones. 2000. Roles of matrix, p2, and N-terminal myristoylation in human immunodeficiency virus type 1 Gag assembly. J. Virol. 74:16-23.
54. Mortuza, G. B., L. F. Haire, A. Stevens, S. J. Smerdon, J. P. Stoye, and I. A. Taylor. 2004. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 431:481-485.
55. Newman, J. L., E. W. Butcher, D. T. Patel, Y. Mikhaylenko, and M. F. Summers. 2004. Flexibility in the P2 domain of the HIV-1 Gag polyprotein. Protein Sci. 13:2101-2107.
56. Pepinsky, R. B., I. A. Papayannopoulos, E. P. C. Chow, N. K. Krishna, R. C. Craven, and V. M. Vogt. 1995. Differential proteolytic processing leads to multiple forms of the CA protein in avian-sarcoma and leukemia viruses. J. Virol. 69:6430-6438.
57. Pettit, S. C., M. D. Moody, R. S. Wehbie, A. H. Kaplan, P. V. Nantermet, C. A. Klein, and R. Swanstrom. 1994. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol. 68:8017-8027.
58. Phillips, J. M., P. S. Murray, D. Murray, and V. M. Vogt. 10 April 2008. A molecular switch required for retrovirus assembly participates in the hexagonal immature lattice. EMBO J. [Epub ahead of print.] doi:10.1038/emboj. 2008.71.
59. Reil, H., A. A. Bukovsky, H. R. Gelderblom, and H. G. Gottlinger. 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 17:2699-2708.
60. Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:208-212.
61. Roldan, A., R. S. Russell, B. Marchand, M. Gotte, C. Liang, and M. A. Wainberg. 2004. In vitro identification and characterization of an early complex linking HIV-1 genomic RNA recognition and Pr55Gag multimerization. J. Biol. Chem. 279:39886-39894.
62. Russell, R. S., A. Roldan, M. Detorio, J. Hu, M. A. Wainberg, and C. Liang. 2003. Effects of a single amino acid substitution within the p2 region of human immunodeficiency virus type 1 on packaging of spliced viral RNA. J. Virol. 77:12986-12995.
63. Sakalian, M., C. P. McMurtrey, F. J. Deeg, C. W. Maloy, F. Li, C. T. Wild, and K. Salzwedel. 2006. 3-O-(3′,3′-dimethysuccinyl) betulinic acid inhibits maturation of the human immunodeficiency virus type 1 Gag precursor assembled in vitro. J. Virol. 80:5716-5722.
64. Shehu-Xhilaga, M., S. Ablan, D. G. Demirov, C. Chen, R. C. Montelaro, and E. O. Freed. 2004. Late domain-dependent inhibition of equine infectious anemia virus budding. J. Virol. 78:724-732.
65. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43.
66. von Schwedler, U. K., T. L. Stemmler, V. Y. Klishko, S. Li, K. H. Albertine, D. R. Davis, and W. I. Sundquist. 1998. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17:1555-1568.
67. von Schwedler, U. K., K. M. Stray, J. E. Garrus, and W. I. Sundquist. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
68. Wiegers, K., G. Rutter, H. Kottler, U. Tessmer, H. Hohenberg, and H. G. Krausslich. 1998. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72:2846-2854.
69. Worthylake, D. K., H. Wang, S. H. Yoo, W. I. Sundquist, and C. P. Hill. 1999. Structures of the HIV-1 capsid protein dimerization domain at 2.6 angstrom resolution. Acta Crystallogr. D 55:85-92.
70. Wright, E. R., J. B. Schooler, H. J. Ding, C. Kieffer, C. Fillmore, W. I. Sundquist, and G. J. Jensen. 2007. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26:2218-2226.
71. Xiang, Y., R. Thorick, M. L. Vana, R. Craven, and J. Leis. 2001. Proper processing of avian sarcoma/leukosis virus capsid proteins is required for infectivity. J. Virol. 75:6016-6021.
72. Yu, F., S. M. Joshi, Y. M. Ma, R. L. Kingston, M. N. Simon, and V. M. Vogt. 2001. Characterization of Rous sarcoma virus Gag particles assembled in vitro. J. Virol. 75:2753-2764.
73. Zhang, Y. Q., H. Y. 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.
74. Zhou, J., L. Huang, D. L. Hachey, C. H. Chen, and C. Aiken. 2005. Inhibition of HIV-1 maturation via drug association with the viral Gag protein in immature HIV-1 particles. J. Biol. Chem. 280:42149-42155.
75. Zhou, J., X. Yuan, D. Dismuke, B. M. Forshey, C. Lundquist, K. H. Lee, C. Aiken, and C. H. Chen. 2004. Small-molecule inhibition of human immunodeficiency virus type 1 replication by specific targeting of the final step of virion maturation. J. Virol. 78:922-929.