On the effect of thermodynamic equilibrium on the assembly efficiency of complex multi-layered virus-like particles (VLP): The case of rotavirus VLP

PLoS Computational Biology

Volumn 8, Issue 2, 2012, Pages

  Roldão, António ^a,b   Mellado, Maria Candida M ^a,b   Lima, J C ^c   Carrondo, Manuel J T ^a,b,c   Alves, Paula M ^a,b   Oliveira, R ^b,c  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^c UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; GIBBS FREE ENERGY; LIGHT SCATTERING; VIRUSES;

ASSEMBLY YIELDS; ASSEMBLY-DISASSEMBLY; IN-VITRO; MASS COMPOSITION; MULTI-LAYERED; RECOMBINANT HOSTS; ROTAVIRUSES; THERMODYNAMIC EQUILIBRIA; VIRUS-LIKE PARTICLES; VITRO ASSEMBLY;

PROTEINS;

VIRUS PROTEIN;

ARTICLE; COMPLEX FORMATION; COMPUTER MODEL; IN VITRO STUDY; IONIC STRENGTH; LIGHT SCATTERING; MATHEMATICAL MODEL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; ROTAVIRUS; TEMPERATURE SENSITIVITY; THERMODYNAMICS; VIRUS ASSEMBLY; VIRUS LIKE AGENT; ANIMAL; BIOLOGY; BIOSYNTHESIS; CHEMISTRY; INSECT; KINETICS; LIGHT; METHODOLOGY; PHYSIOLOGY; RADIATION SCATTERING; STATISTICAL MODEL; TEMPERATURE; THEORETICAL MODEL; VIRUS CAPSID;

ROTAVIRUS;

ANIMALS; CAPSID; COMPUTATIONAL BIOLOGY; INSECTS; KINETICS; LIGHT; MODELS, STATISTICAL; MODELS, THEORETICAL; ROTAVIRUS; SCATTERING, RADIATION; TEMPERATURE; THERMODYNAMICS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84861122841     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002367     Document Type: Article

References (49)

1. Zlotnick A, Johnson JM, Wingfield PW, Stahl SJ, Endres D, (1999) A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 38: 14644-14652.
2. Zlotnick A, (1994) To build a virus capsid. An equilibrium model of the self assembly of polyhedral protein complexes. J Mol Biol 241: 59-67.
3. Endres D, Miyahara M, Moisant P, Zlotnick A, (2005) A reaction landscape identifies the intermediates critical for self-assembly of virus capsids and other polyhedral structures. Protein Sci 14: 1518-1525.
4. Zeng CQY, Labbe M, Cohen J, Prasad BVV, Chen DY, et al. (1994) Characterization of Rotavirus Vp2 Particles. Virology 201: 55-65.
5. Zlotnick A, Aldrich R, Johnson JM, Ceres P, Young MJ, (2000) Mechanism of capsid assembly for an icosahedral plant virus. Virology 277: 450-456.
6. Zlotnick A, Ceres P, Singh S, Johnson JM, (2002) A small molecule inhibits and misdirects assembly of hepatitis B virus capsids. J Virol 76: 4848-4854.
7. Endres D, Zlotnick A, (2002) Model-based analysis of assembly kinetics for virus capsids or other spherical polymers. Biophys J 83: 1217-1230.
8. Mukherjee S, Thorsteinsson MV, Johnston LB, DePhillips PA, Zlotnick A, (2008) A quantitative description of in vitro assembly of human papillomavirus 16 virus-like particles. J Mol Biol 381: 229-237.
9. Zlotnick A, (2007) Distinguishing reversible from irreversible virus capsid assembly. J Mol Biol 366: 14-18.
10. Reddy VS, Giesing HA, Morton RT, Kumar A, Post CB, et al. (1998) Energetics of quasiequivalence: computational analysis of protein-protein interactions in icosahedral viruses. Biophys J 74: 546-558.
11. Rapaport DC, Johnson JE, Skolnick J, (1999) Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation. Comput Phys Commun 121-122: 231-235.
12. Bruinsma RF, Gelbart WM, Reguera D, Rudnick J, Zandi R, (2003) Viral self-assembly as a thermodynamic process. Phys Rev Lett 90: 248101.
13. Berger B, Shor PW, Tucker-Kellogg L, King J, (1994) Local rule-based theory of virus shell assembly. Proc Natl Acad Sci U S A 91: 7732-7736.
14. Kerner R, (2005) A stochastic model of icosahedral capsid growth. Comput Math Methods Med 6: 95-97.
15. Andrews JM, Roberts CJ, (2007) A Lumry-Eyring nucleated polymerization model of protein aggregation kinetics: 1. Aggregation with pre-equilibrated unfolding. J Phys Chem B 111: 7897-7913.
16. Hagan MF, Chandler D, (2006) Dynamic pathways for viral capsid assembly. Biophys J 91: 42-54.
17. Twarock R, (2004) A tiling approach to virus capsid assembly explaining a structural puzzle in virology. J Theor Biol 226: 477-482.
18. Labbe M, Charpilienne A, Crawford SE, Estes MK, Cohen J, (1991) Expression of rotavirus VP2 produces empty corelike particles. J Virol 65: 2946-2952.
19. Prasad BV, Wang GJ, Clerx JP, Chiu W, (1988) Three-dimensional structure of rotavirus. J Mol Biol 199: 269-275.
20. Vieira H, Estêvão C, Roldão A, Peixoto C, Sousa M, et al. (2005) Triple layered rotavirus VLP assembly: kinetics of vector replication, mRNA stability and recombinant protein production. J Biotechnol 120: 72-82.
21. Mellado MCM, Mena JA, Lopes A, Ramírez OT, Carrondo MJT, et al. (2009) Impact of Physicochemical Parameters on In Vitro Assembly and Disassembly Kinetics of Recombinant Triple-Layered Rotavirus-Like Particles. Biotechnol Bioeng 104: 674-686.
22. Peixoto C, Sousa MF, Silva AC, Carrondo MJ, Alves PM, (2007) Downstream processing of triple layered rotavirus like particles. J Biotechnol 127: 452-461.
23. Chen JZ, Settembre EC, Aoki ST, Zhang X, Bellamy AR, et al. (2009) Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc Natl Acad Sci USA 106: 10644-10648.
24. Zlotnick A, (2003) Are weak protein-protein interactions the general rule in capsid assembly? Virology 315: 269-274.
25. Madore HP, Estes MK, Zarley CD, Hu B, Parsons S, et al. (1999) Biochemical and immunologic comparison of virus-like particles for a rotavirus subunit vaccine. Vaccine 17: 2461-2471.
26. Mena JA, Ramirez OT, Palomares LA, (2006) Intracellular distribution of rotavirus structural proteins and virus-like particles expressed in the insect cell-baculovirus system. J Biotechnol 122: 443-452.
27. Caspar DL, Klug A, (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27: 1-24.
28. Charpilienne A, Lepault J, Rey F, Cohen J, (2002) Identification of rotavirus VP6 residues located at the interface with VP2 that are essential for capsid assembly and transcriptase activity. J Virol 76: 7822-7831.
29. Gorziglia M, Larrea C, Liprandi F, Esparza J, (1985) Biochemical evidence for the oligomeric (possibly trimeric) structure of the major inner capsid polypeptide (45 K) of rotaviruses. J Gen Virol 66: 1889-1900.
30. Lepault J, Petitpas I, Erk I, Navaza J, Bigot D, et al. (2001) Structural polymorphism of the major capsid protein of rotavirus. EMBO J 20: 1498-1507.
31. Dormitzer PR, Greenberg HB, Harrison SC, (2000) Purified recombinant rotavirus VP7 forms soluble, calcium-dependent trimers. Virology 277: 420-428.
32. Stirzaker SC, Poncet D, Both GW, (1990) Sequences in rotavirus glycoprotein VP7 that mediate delayed translocation and retention of the protein in the endoplasmic reticulum. J Cell Biol 111: 1343-1350.
33. Au KS, Mattion NM, Estes MK, (1993) A subviral particle binding domain on the rotavirus nonstructural glycoprotein NS28. Virology 194: 665-673.
34. Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, et al. (2009) Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 324: 1444-1447.
35. Lawton JA, Zeng CQ, Mukherjee SK, Cohen J, Estes MK, et al. (1997) Three-dimensional structural analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer. J Virol 71: 7353-7360.
36. McClain B, Settembre E, Temple BR, Bellamy AR, Harrison SC, (2010) X-ray crystal structure of the rotavirus inner capsid particle at 3.8 A resolution. J Mol Biol 397: 587-599.
37. Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, et al. (1998) The atomic structure of the bluetongue virus core. Nature 395: 470-478.
38. Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, et al. (2001) Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. Embo J 20: 1485-1497.
39. Hu Y-C, Bentley WE, (2000) A kinetic and statistical-thermodynamic model for baculovirus infection and virus-like particle assembly in suspended insect cells. Chem Eng Sci 55: 3991-4008.
40. Grimes JM, Jakana J, Ghosh M, Basak AK, Roy P, et al. (1997) An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure 5: 885-893.
41. Limn CK, Roy P, (2003) Intermolecular interactions in a two-layered viral capsid that requires a complex symmetry mismatch. J Virol 77: 11114-11124.
42. Pesavento JB, Crawford SE, Estes MK, Prasad BV, (2006) Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 309: 189-219.
43. Li Z, Baker ML, Jiang W, Estes MK, Prasad BV, (2009) Rotavirus architecture at subnanometer resolution. J Virol 83: 1754-1766.
44. Hu Y-C, Bentley W E, (2000) A kinetic and statistical-thermodynamic model for baculovirus infection and virus-like particle assembly in suspended insect cells. Chem Eng Sci 55: 3991-4008.
45. Sano Y, Inoue H, Kajiwara K, Urakawa H, Hiragi Y, (1994) Self-assembling process of cylindrical virus coat proteins as observed by synchrotron small-angle X-ray scattering. J Biochem 115: 1058-1063.
46. Mellado MC, Franco C, Coelho A, Alves PM, Simplicio AL, (2008) Sodium dodecyl sulfate-capillary gel electrophoresis analysis of rotavirus-like particles. J Chromatogr A 1192: 166-172.
47. Mellado MC, Peixoto C, Cruz PE, Carrondo MJ, Alves PM, (2008) Purification of recombinant rotavirus VP7 glycoprotein for the study of in vitro rotavirus-like particles assembly. J Chromatogr B Analyt Technol Biomed Life Sci 874: 89-94.
48. Tosser G, Labbe M, Bremont M, Cohen J, (1992) Expression of the major capsid protein VP6 of group C rotavirus and synthesis of chimeric single-shelled particles by using recombinant baculoviruses. J Virol 66: 5825-5831.
49. Cruz PE, Cunha A, Peixoto CC, Clemente J, Moreira JL, et al. (1998) Optimization of the production of virus-like particles in insect cells. Biotechnol Bioeng 60: 408-418.