Biophysical Characterization of the Feline Immunodeficiency Virus p24 Capsid Protein Conformation and In Vitro Capsid Assembly

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Serrière, Jennifer ^a   Fenel, Daphna ^b,c,d   Schoehn, Guy ^b,c,d,e   Gouet, Patrice ^a   Guillon, Christophe ^a  

^a INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^b CEA GRENOBLE   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d UNIV GRENOBLE ALPES   (France)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GAG PROTEIN;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DYNAMIC LIGHT SCATTERING; FELINE IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; IONIC STRENGTH; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

BIOPHYSICAL PROCESSES; CAPSID; GENE PRODUCTS, GAG; IMMUNODEFICIENCY VIRUS, FELINE; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SALTS; TEMPERATURE;

EID: 84874065989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056424     Document Type: Article

References (65)

1. Dickson C, Eisenman R, Fan H, Hunter E, Teich N (1984) Protein Biosynthesis and assembly. In: R. Weiss NT, H, Varmus aJC, editors. Molecular biology of tumor viruses: RNA tumor viruses. Cold Spring Harbor Laboratory ed. Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory. 513-648.
2. Willett BJ, Flynn JN, Hosie MJ, (1997) FIV infection of the domestic cat: an animal model for AIDS. Immunol Today 18: 182-189.
3. Bendinelli M, Pistello M, Lombardi S, Poli A, Garzelli C, et al. (1995) Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev 8: 87-112.
4. Ganser-Pornillos BK, Yeager M, Pornillos O, (2012) Assembly and architecture of HIV. Adv Exp Med Biol 726: 441-465.
5. Vogt VM, Simon MN, (1999) Mass determination of rous sarcoma virus virions by scanning transmission electron microscopy. J Virol 73: 7050-7055.
6. Fuller SD, Wilk T, Gowen BE, Krausslich HG, Vogt VM, (1997) Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle. Curr Biol 7: 729-738.
7. Wilk T, Gross I, Gowen BE, Rutten T, de Haas F, et al. (2001) Organization of immature human immunodeficiency virus type 1. J Virol 75: 759-771.
8. Krausslich HG, Welker R, (1996) Intracellular transport of retroviral capsid components. Curr Top Microbiol Immunol 214: 25-63.
9. Vogt VM (1997) Retroviral virions and genomes. In: Coffin JM, Hughes, S. H aV, H E., editors. Retroviruses. Plainview, NY: Cold Spring Harbor. Laboratory Press. 27-69.
10. Briggs JA, Wilk T, Welker R, Krausslich HG, Fuller SD, (2003) Structural organization of authentic, mature HIV-1 virions and cores. EMBO J 22: 1707-1715.
11. Li S, Hill CP, Sundquist WI, Finch JT, (2000) Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407: 409-413.
12. Nermut MV, Hockley DJ, Jowett JB, Jones IM, Garreau M, et al. (1994) Fullerene-like organization of HIV gag-protein shell in virus-like particles produced by recombinant baculovirus. Virology 198: 288-296.
13. Gelderblom HR, Hausmann EH, Ozel M, Pauli G, Koch MA, (1987) Fine structure of human immunodeficiency virus (HIV) and immunolocalization of structural proteins. Virology 156: 171-176.
14. 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.
15. Briggs JA, Grunewald K, Glass B, Forster F, Krausslich HG, et al. (2006) The mechanism of HIV-1 core assembly: insights from three-dimensional reconstructions of authentic virions. Structure 14: 15-20.
16. Ehrlich LS, Agresta BE, Carter CA, (1992) Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J Virol 66: 4874-4883.
17. 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: 2545-2552.
18. Garzon MT, Lidon-Moya MC, Barrera FN, Prieto A, Gomez J, et al. (2004) The dimerization domain of the HIV-1 capsid protein binds a capsid protein-derived peptide: a biophysical characterization. Protein Sci 13: 1512-1523.
19. Hoglund S, Su J, Reneby SS, Vegvari A, Hjerten S, et al. (2002) Tripeptide interference with human immunodeficiency virus type 1 morphogenesis. Antimicrob Agents Chemother 46: 3597-3605.
20. Niedrig M, Gelderblom HR, Pauli G, Marz J, Bickhard H, et al. (1994) Inhibition of infectious human immunodeficiency virus type 1 particle formation by Gag protein-derived peptides. J Gen Virol 75 (Pt 6): 1469-1474.
21. Sticht J, Humbert M, Findlow S, Bodem J, Muller B, et al. (2005) A peptide inhibitor of HIV-1 assembly in vitro. Nat Struct Mol Biol 12: 671-677.
22. Tang C, Loeliger E, Kinde I, Kyere S, Mayo K, et al. (2003) Antiviral inhibition of the HIV-1 capsid protein. J Mol Biol 327: 1013-1020.
23. Bocanegra R, Nevot M, Domenech R, Lopez I, Abian O, et al. (2011) Rationally designed interfacial peptides are efficient in vitro inhibitors of HIV-1 capsid assembly with antiviral activity. PLoS One 6: 23877.
24. Dorfman T, Bukovsky A, Ohagen A, Hoglund S, Gottlinger HG, (1994) Functional domains of the capsid protein of human immunodeficiency virus type 1. J Virol 68: 8180-8187.
25. Reicin AS, Paik S, Berkowitz RD, Luban J, Lowy I, et al. (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.
26. von Schwedler UK, Stemmler TL, Klishko VY, Li S, Albertine KH, et al. (1998) Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J 17: 1555-1568.
27. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI, (2003) Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 77: 5439-5450.
28. Gamble TR, Yoo S, Vajdos FF, von Schwedler UK, Worthylake DK, et al. (1997) Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278: 849-853.
29. Worthylake DK, Wang H, Yoo S, Sundquist WI, Hill CP, (1999) Structures of the HIV-1 capsid protein dimerization domain at 2.6 A resolution. Acta Crystallogr D Biol Crystallogr 55: 85-92.
30. 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: 6900-6908.
31. Chen B, Tycko R, (2010) Structural and dynamical characterization of tubular HIV-1 capsid protein assemblies by solid state nuclear magnetic resonance and electron microscopy. Protein Sci 19: 716-730.
32. 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: 4798-4810.
33. Gross I, Hohenberg H, Wilk T, Wiegers K, Grattinger M, et al. (2000) A conformational switch controlling HIV-1 morphogenesis. EMBO J 19: 103-113.
34. 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: 15056-15064.
35. Wilkins DK, Grimshaw SB, Receveur V, Dobson CM, Jones JA, et al. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38: 16424-16431.
36. Affranchino JL, Gonzalez SA, (2010) In vitro assembly of the feline immunodeficiency virus Gag polyprotein. Virus Res 150: 153-157.
37. 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: 6487-6497.
38. 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.
39. 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: 1782-1789.
40. Campbell S, Rein A, (1999) In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J Virol 73: 2270-2279.
41. Grattinger M, Hohenberg H, Thomas D, Wilk T, Muller B, et al. (1999) In vitro assembly properties of wild-type and cyclophilin-binding defective human immunodeficiency virus capsid proteins in the presence and absence of cyclophilin A. Virology. 257: 247-260.
42. Ehrlich LS, Liu T, Scarlata S, Chu B, Carter CA, (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.
43. Mayo K, Huseby D, McDermott J, Arvidson B, Finlay L, et al. (2003) Retrovirus capsid protein assembly arrangements. J Mol Biol 325: 225-237.
44. Benjamin J, Ganser-Pornillos BK, Tivol WF, Sundquist WI, Jensen GJ, (2005) Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J Mol Biol 346: 577-588.
45. Del Alamo M, Rivas G, Mateu MG, (2005) Effect of macromolecular crowding agents on human immunodeficiency virus type 1 capsid protein assembly in vitro. J Virol 79: 14271-14281.
46. Barklis E, Alfadhli A, McQuaw C, Yalamuri S, Still A, et al. (2009) Characterization of the in vitro HIV-1 capsid assembly pathway. J Mol Biol 387: 376-389.
47. Adamson CS, Freed EO, (2007) Human immunodeficiency virus type 1 assembly, release, and maturation. Adv Pharmacol 55: 347-387.
48. Bailey GD, Hyun JK, Mitra AK, Kingston RL, (2009) Proton-linked dimerization of a retroviral capsid protein initiates capsid assembly. Structure 17: 737-748.
49. 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: 617-628.
50. 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: 5951-5961.
51. Purdy JG, Flanagan JM, Ropson IJ, Craven RC, (2009) Retroviral capsid assembly: a role for the CA dimer in initiation. J Mol Biol 389: 438-451.
52. Bharat TA, Davey NE, Ulbrich P, Riches JD, de Marco A, et al. (2012) Structure of the immature retroviral capsid at 8 A resolution by cryo-electron microscopy. Nature.
53. Rose S, Hensley P, O'Shannessy DJ, Culp J, Debouck C, et al. (1992) Characterization of HIV-1 p24 self-association using analytical affinity chromatography. Proteins 13: 112-119.
54. Sundquist WI, Krausslich H-G:, (2012) HIV-1 Assembly, Budding, and Maturation. Cold Spring Harb Perspect Med 2: a006924.
55. Manrique ML, Celma CC, Gonzalez SA, Affranchino JL, (2001) Mutational analysis of the feline immunodeficiency virus matrix protein. Virus Res 76: 103-113.
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. Cortines JR, Monroe EB, Kang S, Prevelige PE Jr, (2011) A retroviral chimeric capsid protein reveals the role of the N-terminal beta-hairpin in mature core assembly. J Mol Biol 410: 641-652.
58. Yelamos B, Nunez E, Gomez-Gutierrez J, Datta M, Pacheco B, et al. (1999) Circular dichroism and fluorescence spectroscopic properties of the major core protein of feline immunodeficiency virus and its tryptophan mutants. Assignment of the individual contribution of the aromatic sidechains. Eur J Biochem 266: 1081-1089.
59. Bartonova V, Igonet S, Sticht J, Glass B, Habermann A, et al. (2008) Residues in the HIV-1 capsid assembly inhibitor binding site are essential for maintaining the assembly-competent quaternary structure of the capsid protein. J Biol Chem 283: 32024-32033.
60. Monaco-Malbet S, Berthet-Colominas C, Novelli A, Battai N, Piga N, et al. (2000) Mutual conformational adaptations in antigen and antibody upon complex formation between an Fab and HIV-1 capsid protein p24. Structure 8: 1069-1077.
61. Ternois F, Sticht J, Duquerroy S, Krausslich HG, Rey FA, (2005) The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat Struct Mol Biol 12: 678-682.
62. Kelly BN, Kyere S, Kinde I, Tang C, Howard BR, et al. (2007) Structure of the antiviral assembly inhibitor CAP-1 complex with the HIV-1 CA protein. J Mol Biol 373: 355-366.
63. Zhang H, Zhao Q, Bhattacharya S, Waheed AA, Tong X, et al. (2008) A cell-penetrating helical peptide as a potential HIV-1 inhibitor. J Mol Biol 378: 565-580.
64. Bhattacharya S, Zhang H, Debnath AK, Cowburn D, (2008) Solution structure of a hydrocarbon stapled peptide inhibitor in complex with monomeric C-terminal domain of HIV-1 capsid. J Biol Chem 283: 16274-16278.
65. Abdurahman S, Vegvari A, Youssefi M, Levi M, Hoglund S, et al. (2008) Activity of the small modified amino acid alpha-hydroxy glycineamide on in vitro and in vivo human immunodeficiency virus type 1 capsid assembly and infectivity. Antimicrob Agents Chemother 52: 3737-3744.