In vitro assembly of retroviruses

Annual Review of Virology

Volumn 1, Issue 1, 2014, Pages 561-580

  Bush, Di L ^a   Vogt, Volker M ^b  

^a University of Alabama at Birmingham   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

CA; Capsid; Gag; HIV 1; MPMV; RSV

Indexed keywords

GAG PROTEIN; GENOMIC RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DIMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MASON-PFIZER MONKEY VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RETROVIRIDAE; RNA BINDING; ROUS SARCOMA VIRUS; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS RELEASE;

HUMAN IMMUNODEFICIENCY VIRUS 1; MASON-PFIZER MONKEY VIRUS; MIRIDAE; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS;

EID: 85016962662     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-031413-085427     Document Type: Article

References (77)

1. Fuller SD, Wilk T,GowenBE, KrausslichHG,VogtVM.1997. Cryo-electronmicroscopy reveals ordered domains in the immature HIV-1 particle. Curr. Biol. 7:729-38
2. Yeager M, Wilson-Kubalek EM, Weiner SG, Brown PO, 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 95:7299-304
3. Wright ER, Schooler JB, Ding HJ, Kieffer C, Fillmore C, et al. 2007. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26:2218-26
4. Bharat TA, Davey NE, Ulbrich P, Riches JD, de Marco A, et al. 2012. Structure of the immature retroviral capsid at 8A resolution by cryo-electron microscopy. Nature 487:385-89
5. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Krausslich HG. 2009. Structure and assembly of immature HIV. Proc. Natl. Acad. Sci. USA 106:11090-95
6. de Marco A, Davey NE, Ulbrich P, Phillips JM, Lux V, et al. 2010. Conserved and variable features of Gag structure and arrangement in immature retrovirus particles. J. Virol. 84:11729-36
7. Briggs JA, Simon MN, Gross I, Krausslich HG, Fuller SD, et al. 2004. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11:672-75
8. Benjamin J,Ganser-PornillosBK, TivolWF, Sundquist WI, Jensen GJ. 2005. Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J. Mol. Biol. 346:577-88
9. Keller PW, Huang RK, EnglandMR, Waki K, Cheng N, et al. 2013. A two-pronged structural analysis of retroviral maturation indicates that core formation proceeds by a disassembly-reassembly pathway rather than a displacive transition. J. Virol. 87:13655-64
10. Ganser-Pornillos BK, von Schwedler UK, Stray KM, Aiken C, Sundquist WI. 2004. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78:2545-52
11. Butan C,Winkler DC, Heymann JB, Craven RC, Steven AC. 2008. RSV capsid polymorphism correlates with polymerization efficiency and envelope glycoprotein content: implications that nucleation controls morphogenesis. J. Mol. Biol. 376:1168-81
12. de Marco A, Muller B, Glass B, Riches JD, Krausslich HG, Briggs JA. 2010. Structural analysis of HIV-1 maturation using cryo-electron tomography. PLoS Pathog. 6:e1001215
13. Wiegers K, Rutter G, Kottler H, Tessmer U, Hohenberg H, Krausslich HG. 1998. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72:2846-54
14. Campbell S, Vogt VM. 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. 71:4425-35
15. Campbell S, Fisher RJ, Towler EM, Fox S, Issaq HJ, et al. 2001. Modulation of HIV-like particle assembly in vitro by inositol phosphates. Proc. Natl. Acad. Sci. USA 98:10875-79
16. Ehrlich LS, Agresta BE, Carter CA. 1992. Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J. Virol. 66:4874-83
17. Gross I,Hohenberg H, Krausslich HG. 1997. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249:592-600
18. Klikova M, Rhee SS, Hunter E, Ruml T. 1995. Efficient in vivo and in vitro assembly of retroviral capsids from Gag precursor proteins expressed in bacteria. J. Virol. 69:1093-98
19. Campbell S, Vogt VM. 1995. Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol. 69:6487-97
20. Affranchino JL, Gonzalez SA. 2010. In vitro assembly of the feline immunodeficiency virus Gag polyprotein. Virus Res. 150:153-57
21. Datta SA, Zuo X, Clark PK, Campbell SJ,Wang YX, Rein A. 2011. Solution properties ofmurine leukemia virus Gag protein: differences from HIV-1 Gag. J. Virol. 85:12733-41
22. Yu F, Joshi SM, Ma YM, Kingston RL, Simon MN, Vogt VM. 2001. Characterization of Rous sarcoma virus Gag particles assembled in vitro. J. Virol. 75:2753-64
23. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-83
24. Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, et al. 2013. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497:643-46
25. Li S, Hill CP, Sundquist WI, Finch JT. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407:409-13
26. Butan C, Lokhandwala PM, Purdy JG, Cardone G, Craven RC, Steven AC. 2010. Suppression of a morphogenic mutant in Rous sarcoma virus capsid protein by a second-site mutation: a cryoelectron tomography study. J. Virol. 84:6377-86
27. Lanman J, Sexton J, Sakalian M, Prevelige PE Jr. 2002. Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro. J. Virol. 76:6900-8
28. Gross I, Hohenberg H, Huckhagel C, Krausslich HG. 1998. N-terminal extension of human immunodeficiency virus capsid protein converts the in vitro assembly phenotype from tubular to spherical particles. J. Virol. 72:4798-810
29. Campbell S, Rein A. 1999. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73:2270-79
30. Datta SA, Curtis JE, RatcliffW, Clark PK, Crist RM, et al. 2007. Conformation of theHIV-1 Gag protein in solution. J. Mol. Biol. 365:812-24
31. Gross I,Hohenberg H, Wilk T, WiegersK,Grattinger M, et al. 2000. A conformational switch controlling HIV-1 morphogenesis. EMBO J. 19:103-13
32. Menendez-Arias L, Risco C, Pinto da Silva P, Oroszlan S. 1992. Purification of immature cores of mouse mammary tumor virus and immunolocalization of protein domains. J. Virol. 66:5615-20
33. Rumlova-KlikovaM,Hunter E,NermutMV, Pichova I, Ruml T. 2000. Analysis ofMason-Pfizer monkey virus Gag domains required for capsid assembly in bacteria: role of the N-terminal proline residue of CA in directing particle shape. J. Virol. 74:8452-59
34. Ulbrich P, Haubova S, NermutMV, Hunter E, RumlovaM, Ruml T. 2006. Distinct roles for nucleic acid in in vitro assembly of purified Mason-Pfizer monkey virus CANC proteins. J. Virol. 80:7089-99
35. Phillips JM, Murray PS, Murray D, Vogt VM. 2008. A molecular switch required for retrovirus assembly participates in the hexagonal immature lattice. EMBO J. 27:1411-20
36. Ma YM, Vogt VM. 2002. Rous sarcoma virus Gag protein-oligonucleotide interaction suggests a critical role for protein dimer formation in assembly. J. Virol. 76:5452-62
37. Ma YM, Vogt VM. 2004. Nucleic acid binding-induced Gag dimerization in the assembly of Rous sarcoma virus particles in vitro. J. Virol. 78:52-60
38. Purdy JG, Flanagan JM, Ropson IJ, Rennoll-Bankert KE, Craven RC. 2008. Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J. Virol. 82:5951-61
39. Bailey GD, Hyun JK, Mitra AK, Kingston RL. 2009. Proton-linked dimerization of a retroviral capsid protein initiates capsid assembly. Structure 17:737-48
40. Purdy JG, Flanagan JM, Ropson IJ, Craven RC. 2009. Retroviral capsid assembly: a role for the CA dimer in initiation. J. Mol. Biol. 389:438-51
41. Cardone G, Purdy JG, Cheng N, Craven RC, Steven AC. 2009. Visualization of a missing link in retrovirus capsid assembly. Nature 457:694-98
42. Ganser BK, Cheng A, Sundquist WI, YeagerM. 2003. Three-dimensional structure of the M-MuLV CA protein on a lipid monolayer: a general model for retroviral capsid assembly. EMBO J. 22:2886-92
43. Mayo K, McDermott J, Barklis E. 2002. Hexagonal organization ofMoloney murine leukemia virus capsid proteins. Virology 298:30-38
44. Pornillos O, Ganser-Pornillos BK, Yeager M. 2011. Atomic-level modelling of the HIV capsid. Nature 469:424-27
45. Briggs JA, Wilk T, Welker R, Krausslich HG, Fuller SD. 2003. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22:1707-15
46. Gamble TR, Vajdos FF, Yoo S,Worthylake DK, Houseweart M, et al. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-94
47. Gitti RK, Lee BM,Walker J, Summers MF, Yoo S, Sundquist WI. 1996. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273:231-35
48. Momany C, Kovari LC, Prongay AJ, KellerW, Gitti RK, et al. 1996. Crystal structure of dimeric HIV-1 capsid protein. Nat. Struct. Biol. 3:763-70
49. Gamble TR, Yoo S, Vajdos FF, von Schwedler UK,WorthylakeDK, et al. 1997. Structure of the carboxylterminal dimerization domain of the HIV-1 capsid protein. Science 278:849-53
50. Worthylake DK, Wang H, Yoo S, Sundquist WI, Hill CP. 1999. Structures of the HIV-1 capsid protein dimerization domain at 2.6A resolution. Acta Crystallogr. D 55:85-92
51. Kingston RL, Fitzon-Ostendorp T, Eisenmesser EZ, Schatz GW, Vogt VM, et al. 2000. Structure and self-association of the Rous sarcoma virus capsid protein. Structure 8:617-28
52. Mortuza GB, Haire LF, Stevens A, Smerdon SJ, Stoye JP, Taylor IA. 2004. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 431:481-85
53. Mortuza GB, Dodding MP, Goldstone DC, Haire LF, Stoye JP, Taylor IA. 2008. Structure of B-MLV capsid amino-terminal domain reveals key features of viral tropism, Gag assembly and core formation. J. Mol. Biol. 376:1493-508
54. Mortuza GB, Goldstone DC, Pashley C, Haire LF, Palmarini M, et al. 2009. Structure of the capsid amino-terminal domain from the betaretrovirus, Jaagsiekte sheep retrovirus. J. Mol. Biol. 386:1179-92
55. NandhagopalN, Simpson AA, Johnson MC, Francisco AB, SchatzGW, et al. 2004. Dimeric Rous sarcoma virus capsid protein structure relevant to immature Gag assembly. J. Mol. Biol. 335:275-82
56. Ganser-Pornillos BK, Cheng A, Yeager M. 2007. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131:70-79
57. Campos-Olivas R, Newman JL, Summers MF. 2000. Solution structure and dynamics of the Rous sarcoma virus capsid protein and comparison with capsid proteins of other retroviruses. J. Mol. Biol. 296:633-49
58. Macek P, Chmelik J, Krizova I, Kaderavek P, Padrta P, et al. 2009. NMR structure of the N-terminal domain of capsid protein from the Mason-Pfizer monkey virus. J. Mol. Biol. 392:100-14
59. Lanman J, Lam TT, Barnes S, Sakalian M, Emmett MR, et al. 2003. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325:759-72
60. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-50
61. Lanman J, Lam TT, Emmett MR, Marshall AG, Sakalian M, Prevelige PE Jr. 2004. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11:676-77
62. Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, et al. 2009. X-ray structures of the hexameric building block of the HIV capsid. Cell 137:1282-92
63. Bailey GD, Hyun JK,Mitra AK, Kingston RL. 2012. A structural model for the generation of continuous curvature on the surface of a retroviral capsid. J. Mol. Biol. 417:212-23
64. Byeon IJ, Meng X, Jung J, Zhao G, Yang R, et al. 2009. Structural convergence between cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function. Cell 139:780-90
65. Hyun JK, Radjainia M, Kingston RL,Mitra AK. 2010. Proton-driven assembly of the Rous sarcoma virus capsid protein results in the formation of icosahedral particles. J. Biol. Chem. 285:15056-64
66. Joshi SM, Vogt VM. 2000. Role of the Rous sarcoma virus p10 domain in shape determination of Gag virus-like particles assembled in vitro and within Escherichia coli. J. Virol. 74:10260-68
67. de Marco A, Heuser AM, Glass B, Krausslich HG, Muller B, Briggs JA. 2012. Role of the SP2 domain and its proteolytic cleavage in HIV-1 structural maturation and infectivity. J. Virol. 86:13708-16
68. Accola MA,Hoglund S, GottlingerHG. 1998. A putative α-helical structure which overlaps the capsid-p2 boundary in the human immunodeficiency virus type 1 Gag precursor is crucial for viral particle assembly. J. Virol. 72:2072-78
69. Keller PW, Johnson MC, Vogt VM. 2008. Mutations in the spacer peptide and adjoining sequences in Rous sarcoma virus Gag lead to tubular budding. J. Virol. 82:6788-97
70. Bush DL, Monroe EB, Bedwell GJ, Prevelige PE, Phillips JM, Vogt VM. 2014. Higher-order structure of the Rous sarcoma virus SP assembly domain. J. Virol. 88:5617-29
71. Datta SA, Temeselew LG, Crist RM, Soheilian F, Kamata A, et al. 2011. On the role of the SP1 domain in HIV-1 particle assembly: a molecular switch? J. Virol. 85:4111-21
72. Datta SA,Heinrich F, Raghunandan S,Krueger S, Curtis JE, et al. 2011. HIV-1Gag extension: Conformational changes require simultaneous interaction with membrane and nucleic acid. J. Mol. Biol. 406:205-14
73. Zhang Y, Qian H, Love Z, Barklis E. 1998. Analysis of the assembly function of the human immunodeficiency virus type 1 Gag protein nucleocapsid domain. J. Virol. 72:1782-89
74. Accola MA, Strack B, GottlingerHG. 2000. Efficient particle production by minimalGag constructs which retain the carboxy-terminal domain of human immunodeficiency virus type 1 capsid-p2 and a late assembly domain. J. Virol. 74:5395-402
75. Johnson MC, Scobie HM, Ma YM, Vogt VM. 2002. Nucleic acid-independent retrovirus assembly can be driven by dimerization. J. Virol. 76:11177-85
76. Crist RM, Datta SA, Stephen AG, Soheilian F, Mirro J, et al. 2009. Assembly properties of human immunodeficiency virus type 1 Gag-leucine zipper chimeras: implications for retrovirus assembly. J. Virol. 83:2216-25
77. Briggs JA, Johnson MC, Simon MN, Fuller SD, Vogt VM. 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. 355:157-68