Retroviral Capsid Assembly: A Role for the CA Dimer in Initiation

Journal of Molecular Biology

Volumn 389, Issue 2, 2009, Pages 438-451

  Purdy, John G ^a   Flanagan, John M ^a   Ropson, Ira J ^a   Craven, Rebecca C ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

CA protein; electrostatic control of assembly; nucleation of capsid assembly; retrovirus maturation; Rous sarcoma virus

Indexed keywords

ACTIVATED PROTEIN C; ANION; DIMER; MONOMER; TRYPTOPHAN;

ARTICLE; DIMERIZATION; ELECTRICITY; FLUORESCENCE; IN VITRO STUDY; KINETICS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; ROUS SARCOMA ONCOVIRUS; VIRION; VIRUS CAPSID;

MIRIDAE; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS;

EID: 65549092017     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.006     Document Type: Article

References (79)

1. Swanstrom R., and Wills J.W. Synthesis, assembly, and processing of viral proteins. In: Coffin J.M., Hughes S.H., and Varmus H. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Woodbury, NY 263-334
2. Benjamin J., Ganser-Pornillos B.K., Tivol W.F., Sundquist W.I., and Jensen G.J. Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J. Mol. Biol. 346 (2005) 577-588
3. Briggs J.A., Grunewald K., Glass B., Forster F., Krausslich H.G., and Fuller S.D. The mechanism of HIV-1 core assembly: insights from three-dimensional reconstructions of authentic virions. Structure 14 (2006) 15-20
4. Butan C., Winkler D.C., Heymann J.B., Craven R.C., and Steven A.C. RSV capsid polymorphism correlates with polymerization efficiency and envelope glycoprotein content: implications that nucleation controls morphogenesis. J. Mol. Biol. 376 (2008) 1168-1181
5. Briggs J.A., Wilk T., Welker R., Krausslich H.G., and Fuller S.D. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22 (2003) 1707-1715
6. Briggs J.A., Simon M.N., Gross I., Krausslich H.G., Fuller S.D., Vogt V.M., and Johnson M.C. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11 (2004) 672-675
7. Lanman J., Lam T.T., Barnes S., Sakalian M., Emmett M.R., Marshall A.G., and Prevelige P.E. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325 (2003) 759-772
8. Lanman J., Lam T.T., Emmett M.R., Marshall A.G., Sakalian M., and Prevelige Jr. P.E. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11 (2004) 676-677
9. Lanman J., and Prevelige Jr. P.E. Kinetic and mass spectrometry-based investigation of human immunodeficiency virus type 1 assembly and maturation. Adv. Virus Res. 64 (2005) 285-309
10. 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 (2005) 13463-13472
11. Briggs J.A.G., Johnson M.C., Simon M.N., Fuller S.D., and Vogt V.M. 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 (2006) 157-168
12. Ivanov D., Tsodikov O.V., Kasanov J., Ellenberger T., Wagner G., and Collins T. Domain-swapped dimerization of the HIV-1 capsid C-terminal domain. Proc. Natl Acad. Sci. USA 104 (2007) 4353-4358
13. Nandhagopal N., Simpson A.A., Johnson M.C., Francisco A.B., Schatz G.W., Rossmann M.G., and Vogt V.M. Dimeric Rous sarcoma virus capsid protein structure relevant to immature gag assembly. J. Mol. Biol. 335 (2004) 275-282
14. Phillips J.M., Murray P.S., Murray D., and Vogt V.M. A molecular switch required for retrovirus assembly participates in the hexagonal immature lattice. EMBO J. 27 (2008) 1411-1420
15. Wilk T., Gross I., Gowen B.E., Rutten T., de Haas F., Welker R., et al. Organization of immature human immunodeficiency virus type 1. J. Virol. 75 (2001) 759-771
16. Wright E.R., Schooler J.B., Ding H.J., Kieffer C., Fillmore C., Sundquist W.I., and Jensen G.J. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26 (2007) 2218-2226
17. Barrera F.N., del Alamo M., Mateu M.G., and Neira J.L. Envelope lipids regulate the in vitro assembly of the HIV-1 capsid. Biophys. J. 94 (2008) L8-L10
18. Purdy J.G., Flanagan J.M., Ropson I.J., Rennoll-Bankert K.E., and Craven R.C. Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J. Virol. 82 (2008) 5951-5961
19. Douglas C.C., Thomas D., Lanman J., and Prevelige P.E. Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1CA. Biochemistry 43 (2004) 10435-10441
20. Ganser-Pornillos B.K., Cheng A., and Yeager M. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131 (2007) 70-79
21. Li S., Hill C.P., Sundquist W.I., and Finch J.T. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407 (2000) 409-413
22. Ganser-Pornillos B.K., von Schwedler U.K., Stray K.M., Aiken C., and Sundquist W.I. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78 (2004) 2545-2552
23. Ganser B.K., Li S., Klishko V.Y., Finch J.T., and Sundquist W.I. Assembly and analysis of conical models for the HIV-1 core. Science 283 (1999) 80-83
24. Heymann J.B., Butan C., Winkler D.C., Craven R.C., and Steven A.C. Irregular and semi-regular polyhedral models for Rous sarcoma virus cores. Comput. Math. Methods Med. 9 (2008) 197-210
25. Nguyen T.T., Bruinsma R.F., and Gelbart W.M. Continuum theory of retroviral capsids. Phys. Rev. Lett. 96 (2006) 0781021-0781024
26. Ganser B.K., Cheng A., Sundquist W.I., and Yeager M. Three-dimensional structure of the M-MuLV CA protein on a lipid monolayer: a general model for retroviral capsid assembly. EMBO J. 22 (2003) 2886-2892
27. Mayo K., McDermott J., and Barklis E. Hexagonal organization of Moloney murine leukemia virus capsid proteins. Virology 298 (2002) 30-38
28. Mayo K., Huseby D., McDermott J., Arvidson B., Finlay L., and Barklis E. Retrovirus capsid protein assembly arrangements. J. Mol. Biol. 325 (2003) 225-237
29. 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 (2004) 481-485
30. Mortuza G.B., Dodding M.P., Goldstone D.C., Haire L.F., Stoye J.P., and Taylor I.A. Structure of B-MLV capsid amino-terminal domain reveals key features of viral tropism, gag assembly and core formation. J. Mol. Biol. 376 (2008) 1493-1508
31. Cardone G., Purdy J.G., Cheng N., Craven R.C., and Steven A.C. Visualization of a missing link in retrovirus capsid assembly. Nature 457 (2009) 694-698
32. Alcaraz L.A., del Alamo M., Barrera F.N., Mateu M.G., and Neira J.L. Flexibility in HIV-1 assembly subunits: solution structure of the monomeric C-terminal domain of the capsid protein. Biophys. J. 93 (2007) 1264-1276
33. Berthet-Colominas C., Monaco S., Novelli A., Sibai G., Mallet F., and Cusack S. Head-to-tail dimers and interdomain flexibility revealed by the crystal structure of HIV-1 capsid protein (p24) complexed with a monoclonal antibody Fab. EMBO J. 18 (1999) 1124-1136
34. Gamble T.R., Yoo S., Vajdos F.F., von Schwedler U.K., Worthylake D.K., Wang H., et al. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278 (1997) 849-853
35. Gitti R.K., Lee B.M., Walker J., Summers M.F., Yoo S., and Sundquist W.I. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273 (1996) 231-235
36. Jin Z., Jin L., Peterson D.L., and Lawson C.L. Model for lentivirus capsid core assembly based on crystal dimers of EIAV p26. J. Mol. Biol. 286 (1999) 83-93
37. Khorasanizadeh S., Campos-Olivas R., and Summers M.F. Solution structure of the capsid protein from the human T-cell leukemia virus type-I. J. Mol. Biol. 291 (1999) 491-505
38. Kingston R.L., Fitzon-Ostendorp T., Eisenmesser E.Z., Schatz G.W., Vogt V.M., Post C.B., and Rossmann M.G. Structure and self-association of the Rous sarcoma virus capsid protein. Structure 8 (2000) 617-628
39. Momany C., Kovari L.C., Prongay A.J., Keller W., Gitti R.K., Lee B.M., et al. Crystal structure of dimeric HIV-1 capsid protein. Nat. Struct. Biol. 3 (1996) 763-770
40. Mortuza G.B., Goldstone D.C., Pashley C., Haire L.F., Palmarini M., Taylor W.R., et al. Structure of the capsid amino-terminal domain from the betaretrovirus, Jaagsiekte sheep retrovirus. J. Mol. Biol. 386 (2008) 1179-1192
41. Ternois F., Sticht J., Duquerroy S., Krausslich H.G., and Rey F.A. The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat. Struct. Mol. Biol. 12 (2005) 678-682
42. Wong H.C., Shin R., and Krishna N.R. Solution structure of a double mutant of the carboxy-terminal dimerization domain of the HIV-1 capsid protein. Biochemistry 47 (2008) 2289-2297
43. Worthylake D.K., Wang H., Yoo S., Sundquist W.I., and Hill C.P. Structures of the HIV-1 capsid protein dimerization domain at 2.6 Å resolution. Acta Crystallogr. Sect. D 55 (1999) 85-92
44. Bowzard J.B., Wills J.W., and Craven R.C. Second-site suppressors of Rous sarcoma virus CA mutations: evidence for interdomain interactions. J. Virol. 75 (2001) 6850-6856
45. Kelly B.N., Kyere S., Kinde I., Tang C., Howard B.R., Robinson H., et al. Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J. Mol. Biol. 373 (2007) 355-366
46. Sticht J., Humbert M., Findlow S., Bodem J., Muller B., Dietrich U., et al. A peptide inhibitor of HIV-1 assembly in vitro. Nat. Struct. Mol. Biol. 12 (2005) 671-677
47. Tang C., Loeliger E., Kinde I., Kyere S., Mayo K., Barklis E., et al. Antiviral inhibition of the HIV-1 capsid protein. J. Mol. Biol. 327 (2003) 1013-1020
48. Gross I., Hohenberg H., and Krausslich H.G. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249 (1997) 592-600
49. Lanman J., Sexton J., Sakalian M., and Prevelige P.E. Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro. J. Virol. 76 (2002) 6900-6908
50. Frieden C. Protein aggregation processes: in search of the mechanism. Protein Sci. 16 (2007) 2334-2344
51. Kovari L.C., Momany C.A., Miyagi F., Lee S., Campbell S., Vuong B., et al. Crystals of Rous sarcoma virus capsid protein show a helical arrangement of protein subunits. Virology 238 (1997) 79-84
52. Baldwin R.L. How Hofmeister ion interactions affect protein stability. Biophys. J. 71 (1996) 2056-2063
53. Kingston R.L., Olson N.H., and Vogt V.M. The organization of mature Rous sarcoma virus as studied by cryoelectron microscopy. J. Struct. Biol. 136 (2001) 67-80
54. Oosawa F., and Kasai M. A theory of linear and helical aggregations of macromolecules. J. Mol. Biol. 4 (1962) 10-21
55. Prevelige Jr. P.E., Thomas D., and King J. Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells. Biophys. J. 64 (1993) 824-835
56. Campos-Olivas R., Newman J.L., and Summers M.F. Solution structure and dynamics of the Rous sarcoma virus capsid protein and comparison with capsid proteins of other retroviruses. J. Mol. Biol. 296 (2000) 633-649
57. Studier F.W. Protein production by auto-induction in high-density shaking cultures. Protein Expression Purif. 41 (2005) 207-234
58. Wyatt P.J. Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 272 (1993) 1-40
59. Utepbergenov D.I., Fanning A.S., and Anderson J.M. Dimerization of the scaffolding protein ZO-1 through the second PDZ domain. J. Biol. Chem. 281 (2006) 24671-24677
60. Yamaguchi T., and Adachi K. Hemoglobin equilibrium analysis by the multiangle laser light-scattering method. Biochem. Biophys. Res. Commun. 290 (2002) 1382-1387
61. Vivian J.T., and Callis P.R. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80 (2001) 2093-2109
62. Cairns T.M., and Craven R.C. Viral DNA synthesis defects in assembly-competent Rous sarcoma virus CA mutants. J. Virol. 75 (2001) 242-250
63. Craven R.C., Leuredupree A.E., Weldon R.A., and Wills J.W. Genetic-analysis of the major homology region of the Rous-sarcoma virus Gag protein. J. Virol. 69 (1995) 4213-4227
64. Lokhandwala P.M., Nguyen T.L., Bowzard J.B., and Craven R.C. Cooperative role of the MHR and the CA dimerization helix in the maturation of the functional retrovirus capsid. Virology 376 (2008) 191-198
65. von Schwedler U.K., Stemmler T.L., Klishko V.Y., Li S., Albertine K.H., Davis D.R., and Sundquist W.I. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17 (1998) 1555-1568
66. Kainov D.E., Butcher S.J., Bamford D.H., and Tuma R. Conserved intermediates on the assembly pathway of double-stranded RNA bacteriophages. J. Mol. Biol. 328 (2003) 791-804
67. Salunke D.M., Caspar D.L., and Garcea R.L. Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys. J. 56 (1989) 887-900
68. Zlotnick A., Aldrich R., Johnson J.M., Ceres P., and Young M.J. Mechanism of capsid assembly for an icosahedral plant virus. Virology 277 (2000) 450-456
69. Nicholls A., Sharp K.A., and Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11 (1991) 281-296
70. del Alamo M., Neira J.L., and Mateu M.G. Thermodynamic dissection of a low affinity protein-protein interface involved in human immunodeficiency virus assembly. J. Biol. Chem. 278 (2003) 27923-27929
71. del Alamo M., and Mateu M.G. Electrostatic repulsion, compensatory mutations, and long-range non-additive effects at the dimerization interface of the HIV capsid protein. J. Mol. Biol. 345 (2005) 893-906
72. Ehrlich L.S., Agresta B.E., and Carter C.A. Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J. Virol. 66 (1992) 4874-4883
73. Ehrlich L.S., Liu T., Scarlata S., Chu B., and Carter C.A. 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 (2001) 586-594
74. Rose S., Hensley P., O'Shannessy D.J., Culp J., Debouck C., and Chaiken I. Characterization of HIV-1 p24 self-association using analytical affinity chromatography. Proteins 13 (1992) 112-119
75. 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 (2003) 5439-5450
76. Yoo S., Myszka D.G., Yeh C., McMurray M., Hill C.P., and Sundquist W.I. Molecular recognition in the HIV-1 capsid/cyclophilin A complex. J. Mol. Biol. 269 (1997) 780-795
77. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., and Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31 (2003) 3784-3788
78. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
79. Zwietering M.H., Jongenburger I., Rombouts F.M., and van't Riet K. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56 (1990) 1875-1881