Virus assembly occurs following a pH- or Ca2+-triggered switch in the thermodynamic attraction between structural protein capsomeres

Journal of the Royal Society Interface

Volumn 7, Issue 44, 2010, Pages 409-421

  Chuan, Yap P ^a   Fan, Yuan Y ^a   Lua, Linda H L ^a   Middelberg, Anton P J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Conformation; Cooperative; Second virial coefficient; Self assembly; Virus

Indexed keywords

AMMONIUM COMPOUNDS; CALCIUM; COMPLEXATION; CONFORMATIONS; EQUATIONS OF STATE; SELF ASSEMBLY; THERMODYNAMICS; VIRUSES;

AMMONIUM SULPHATE CONCENTRATION; ANTIVIRALS; CHEMICAL CHANGE; CONFORMATIONAL CHANGE; IN-VITRO; MOLECULAR ATTRACTION; PHYSICO-CHEMICALS; POLYOMAVIRUS; REGULATORY MECHANISM; SALTING-OUT; SECOND VIRIAL COEFFICIENT; SECOND VIRIAL COEFFICIENTS; SELF-ASSEMBLING; STRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS CAPSID;

PROTEINS;

CALCIUM ION; PROTEIN CAPSOMERE; PROTEIN VP1; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYOMA VIRUS; PROTEIN PROTEIN INTERACTION; THERMODYNAMICS; VIRUS ASSEMBLY; VIRUS CAPSID;

MIRIDAE; POLYOMAVIRUS;

EID: 76049094891     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0175     Document Type: Article

References (77)

1. Alber, T., Hartman, F. C., Johnson, R. M., Petsko, G. A. & Tsernoglou, D. 1981 Crystallization of yeast triose phosphate isomerase from polyethylene-glycol: protein crystal-formation following phase-separation. J. Biol. Chem. 256, 1356-1361.
2. Alberts, B. 2008 Molecular biology of the cell, 5th edn, pp. 3-190. New York, NY: Garland Science.
3. Bajaj, H., Sharma, V. K. & Kalonia, D. S. 2004 Determination of second virial coeficient of proteins using a dual-detector cell for simultaneous measurement of scattered light intensity and concentration in SEC-HPLC. Biophys. J. 87, 4048-4055. (doi:10.1529/biophysj.104.048686)
4. Berger, B., Shor, P. W., Tuckerkellogg, L. & King, J. 1994 Local rule-based theory of virus shell assembly. Proc. Natl Acad. Sci. USA 91, 7732-7736. (doi:10.1073/pnas.91.16.7732)
5. Bloustine, J., Berejnov, V. & Fraden, S. 2003 Measurements of protein - protein interactions by size exclusion chromatography. Biophys. J. 85, 2619-2623. (doi:10.1016/S0006-3495(03)74684-0)
6. Bonnete, F. & Vivares, D. 2002 Interest of the normalized second virial coefficient and interaction potentials for crystallizing large macromolecules. Acta Crystallogr. D Biol. Crystallogr. 58, 1571-1575. (doi:10.1107/S090744490201418X)
7. Casini, G. L., Graham, D., Heine, D., Garcea, R. L. & Wu, D. T. 2004 In vitro papillomavirus capsid assembly analyzed by light scattering. Virology 325, 320-327. (doi:10.1016/j.virol.2004.04.034)
8. Casjens, S. & King, J. 1975 Virus assembly. Annu. Rev. Biochem. 44, 555-611. (doi:10.1146/annurev.bi.44.070175.003011)
9. Caspar, D. L. D. 1963 Assembly and stability of the tobacco mosaic virus particle. Adv. Protein Chem. 18, 37-121. (doi:10.1016/S0065- 3233(08)60268-5)
10. Caspar, D. L. D. 1980 Movement and self-control in protein assemblies: quasi-equivalence revisited. Biophys. J. 32, 103-138. (doi:10.1016/S0006-3495(80)84929-0)
11. Caspar, D. L. D. & Klug, A. 1962 Physical principles in construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27, 1-24.
12. Chi, E. Y., Krishnan, S., Randolph, T. W. & Carpenter, J. F. 2003 Physical stability of proteins in aqueous solution: mechanism and driving forces in non-native protein aggregation. Pharm. Res. 20, 1325-1336. (doi:10.1023/A:1025771421906)
13. Chuan, Y. P., Fan, Y. Y., Lua, L. & Middelberg, A. P. J. 2008a Quantitative analysis of virus-like particle size and distribution by field-flow fractionation. Biotechnol. Bioeng. 99, 1425-1433. (doi:10.1002/bit.21710)
14. Chuan, Y. P., Lua, L. H. L. & Middelberg, A. P. J. 2008b High-level expression of soluble viral structural protein in Escherichia coli. J. Biotechnol. 134, 64-71. (doi:10.1016/j.jbiotec.2007.12.004)
15. Citkowicz, A., Petry, H., Harkins, R. N., Ast, O., Cashion, L., Goldmarm, C., Bringmarm, P., Plummer, K. & Larsen, B. R. 2008 Characterization of virus-like particle assembly for DNA delivery using asymmetrical flow field-flow fractionation and light scattering. Anal. Biochem. 376, 163-172. (doi:10.1016/j.ab.2008.02.011)
16. Coen, C. J., Blanch, H. W. & Prausnitz, J. M. 1995 Salting-out of aqueous proteins: phase-equilibria and intermolecular potentials. AIChE J. 41, 996-1004. (doi:10.1002/aic.690410430)
17. Crick, F. H. C. & Watson, J. D. 1956 Structure of small viruses. Nature 177, 473-475. (doi:10.1038/177473a0)
18. Curtis, R. A. & Lue, L. 2006 A molecular approach to bioseparations: protein-protein and protein-salt interactions. Chem. Eng. Sci. 61, 907-923. (doi:10.1016/j.ces.2005.04.007)
19. Curtis, R. A., Montaser, A., Prausnitz, J. M. & Blanch, H. W. 1998 Protein-protein and protein-salt interactions in aqueous protein solutions containing concentrated electrolytes. Biotechnol. Bioeng. 58, 451. (doi:10.1002/(SICI)1097-0290(19980520)58:4,<451::AID-BIT13>3.0.CO;2-E)
20. Dumetz, A. C., Chockla, A. M., Kaler, E.W. & Lenhoff, A. M. 2008 Protein phase behavior in aqueous solutions: crystallization, liquid-liquid phase separation, gels, and aggregates. Biophys. J. 94, 570-583. (doi:10.1529/biophysj.107.116152)
21. Durham, A. C., Hendry, D. A. & Von Wechmar, M. B. 1977 Does calcium ion binding control plant virus disassembly? Virology 77, 524-533. (doi:10.1016/0042-6822(77)90478-0)
22. Fraenkel-Conrat, H. & Williams, R. C. 1955 Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc. Natl Acad. Sci. USA 41, 690-698. (doi:10.1073/pnas.41.10. 690)
23. Garcea, R. L. & Gissmann, L. 2004 Virus-like particles as vaccines and vessels for the delivery of small molecules. Curr. Opin. Biotechnol. 15, 513-517. (doi:10.1016/j.copbio.2004.10.002)
24. Garcea, R. L., Salunke, D. M. & Caspar, D. L. D. 1987 Site-directed mutation affecting polyomavirus capsid self-assembly in vitro. Nature 329, 86-88. (doi:10.1038/329086a0)
25. George, A. & Wilson, W. W. 1994 Predicting protein crystallization from a dilute-solution property. Acta Crystallogr. D Biol. Crystallogr. 50, 361-365. (doi:10.1107/S0907444994001216)
26. Haas, C. & Drenth, J. 1998 The protein-water phase diagram and the growth of protein crystals from aqueous solution. J. Phys. Chem. B 102, 4226-4232. (doi:10.1021/jp980296j)
27. Haas, C. & Drenth, J. 1999 Understanding protein crystallization on the basis of the phase diagram. J. Cryst. Growth 196, 388-394. (doi:10.1016/S0022-0248(98)00831-8)
28. Harrison, S. C. 1980 Virus crystallography comes of age. Nature 286, 558-559. (doi:10.1038/286558a0)
29. Haynes, C. A., Carson, J., Blanch, H. W. & Prausnitz, J. M. 1991 Electrostatic potentials and protein partitioning in aqueous two-phase systems. AIChE J. 37, 1401-1409. (doi:10.1002/aic.690370912)
30. Ho, J. G. S., Middelberg, A. P. J., Ramage, P. & Kocher, H. P. 2003 The likelihood of aggregation during protein renaturation can be assessed using the second virial coefficient. Protein Sci. 12, 708-716. (doi:10.1110/ps.0233703)
31. Huglin, M. B. 1972 Light scattering from polymer solutions, p. 165. London, UK: Academic Press.
32. Johnson, J. M., Tang, J. H., Nyame, Y., Willits, D., Young, M. J. & Zlotnick, A. 2005 Regulating self-assembly of spherical oligomers. Nano Lett. 5, 765-770. (doi:10.1021/nl050274q)
33. Kataoka, M., Head, J. F., Seaton, B. A. & Engelman, D. M. 1989 Melittin binding causes a large calcium-dependent conformational change in calmodulin. Proc. Natl Acad. Sci. USA 86, 6944-6948. (doi:10.1073/pnas.86.18.6944)
34. Kim, J. H., Johannes, L., Goud, B., Antony, C., Lingwood, C. A., Daneman, R. & Grinstein, S. 1998 Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl Acad. Sci. USA 95, 2997-3002. (doi:10.1073/pnas.95.6.2997)
35. Klug, A. 1983 From macromolecules to biological assemblies. Angew. Chem. Int. Ed. Engl. 22, 565-582. (doi:10.1002/anie.198305653)
36. Knipe, D. M., Fields, B. N., Howley, P. M. & Griffin, D. E. 2001 Fields' virology, 4th edn, pp. 2263-2354. Philadelphia, PA: Lippincott Williams & Wilkins.
37. Lang, R., Winter, G., Vogt, L., Zurcher, A., Dorigo, B. & Schimmele, B. 2009 Rational design of a stable, freeze-dried virus-like particle-based vaccine formulation. Drug Dev. Ind. Pharm. 35, 83-97. (doi:10.1080/03639040802192806)
38. Liddington, R. C., Yan, Y., Moulai, J., Sahli, R., Benjamin, T. L. & Harrison, S. C. 1991 Structure of simian virus-40 at 3.8 angstrom resolution. Nature 354, 278-284. (doi:10.1038/354278a0)
39. Lindsey, J. S. 1991 Self-assembly in synthetic routes to molecular devices - biological principles and chemical perspectives - a review. New J. Chem. 15, 153-180.
40. Lipin, D. I., Chuan, Y. P., Lua, L. H. L. & Middelberg, A. P. J. 2008a Encapsulation of DNA and non-viral protein changes the structure of murine polyomavirus virus-like particles. Arch. Virol. 153, 2027-2039. (doi:10.1007/s00705-008-0220-9)
41. Lipin, D. I., Lua, L. H. L. & Middelberg, A. P. J. 2008b Quaternary size distribution of soluble aggregates of glutathione-S-transferase-purified viral protein as determined by asymmetrical flow field flow fractionation and dynamic light scattering. J. Chromatogr. A 1190, 204-214. (doi:10. 1016/j.chroma.2008.03.032)
42. Litzen, A. & Wahlund, K. G. 1991 Effects of temperature, carrier composition and sample load in asymmetrical flow field-flow fractionation. J. Chromatogr. A 548, 393-406. (doi:10.1016/S0021-9673(01)88622-2)
43. Magnuson, B., Rainey, E. K., Benjamin, T., Baryshev, M., Mkrtchian, S.&Tsai, B. 2005ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol. Cell 20, 289-300. (doi:10.1016/j.molcel.2005.08.034)
44. Malkin, A. J. & Mcpherson, A. 1993 Light-scattering investigations of protein and virus crystal growth: ferritin, apoferritin and satellite tobacco mosaic virus. J. Cryst. Growth 128, 1232-1235. (doi:10.1016/S0022-0248(07)80128-X)
45. 2+-dependent interactions of calmodulin with target sequences. Protein Sci. 9, 2477-2488. (doi:10.1110/ps.9.12.2477)
46. Melander, W. & Horvath, C. 1977 Salt effects on hydrophobic interactions in precipitation and chromatography of proteins: interpretation of lyotropic series. Arch. Biochem. Biophys. 183, 200-215. (doi:10.1016/0003-9861(77)90434-9)
47. Montross, L., Watkins, S., Moreland, R. B., Mamon, H., Caspar, D. L. D. & Garcea, R. L. 1991 Nuclear assembly of polyomavirus capsids in insect cells expressing the major capsid protein VP1. J. Virol. 65, 4991-4998.
48. Neal, B. L., Asthagiri, D. & Lenhoff, A. M. 1998 Molecular origins of osmotic second virial coefficients of proteins. Biophys. J. 75, 2469-2477. (doi:10.1016/S0006-3495(98)77691-X)
49. Oberholzer, M. R. & Lenhoff, A. M. 1999 Protein adsorption isotherms through colloidal energetics. Langmuir 15, 3905-3914. (doi:10.1021/la981199k)
50. Patro, S. Y. & Przybycien, T. M. 1996 Self-interaction chromatography: a tool for the study of protein-protein interactions in bioprocessing environments. Biotechnol. Bioeng. 52, 193-203. (doi:10.1002/(SICI)1097-0290(19961020)52:2,<193::AID-BIT2>3.0.CO;2-L)
51. Pattenden, L. K., Middelberg, A. P. J., Niebert, M. & Lipin, D. I. 2005 Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol. 23, 523-529. (doi:10.1016/j. tibtech.2005.07.011)
52. Piazza, R. 2000 Interactions and phase transitions in protein solutions. Curr. Opin. Colloid Interface Sci. 5, 38-43. (doi:10.1016/S1359- 0294(00)00034-0)
53. Prausnitz, J. M. 2003 Molecular thermodynamics for some applications in biotechnology. J. Chem. Thermodyn. 35, 22-39. (doi:10.1016/S0021- 9614(02)00305-1)
54. Rayment, I., Baker, T. S., Caspar, D. L. D. & Murakami, W. T. 1982 Polyoma-virus capsid structure at 22.5 angstrom resolution. Nature 295, 110-115. (doi:10.1038/295110a0)
55. Rosenbaum, D. F. & Zukoski, C. F. 1996 Protein interactions and crystallization. J. Cryst. Growth 169, 752-758. (doi:10.1016/S0022-0248(96)00455-1)
56. Rossmann, M. G., Abadzapatero, C., Hermodson, M. A. & Erickson, J. W. 1983 Subunit interactions in southern bean mosaic-virus. J. Mol. Biol. 166, 73. (doi:10.1016/ S0022-2836(83)80050-3)
57. Salunke, D. M., Caspar, D. L. D. & Garcea, R. L. 1986 Self-assembly of purified polyomavirus capsid protein VP1. Cell 46, 895-904. (doi:10.1016/0092-8674(86)90071-1)
58. Salunke, D. M., Caspar, D. L. D. & Garcea, R. L. 1989 Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys. J. 56, 887-900. (doi:10.1016/S0006-3495(89)82735-3)
59. Sayle, R. A. & Milnerwhite, E. J. 1995 Rasmol: biomolecular graphics for all. Trends Biochem. Sci. 20, 374-376. (doi:10.1016/S0968- 0004(00)89080-5)
60. Schwaller, B., Pauls, T. L. & Celio, M. R. 1996 Guidebook to the calcium-binding proteins, p. 1. Oxford, UK: Sambrook and Tooze
61. Seksek, O. & Bolard, J. 1996 Nuclear pH gradient in mammalian cells revealed by laser microspectro.uorimetry. J. Cell Sci. 109, 257-262.
62. Shi, L., Sanyal, G., Ni, A., Luo, Z., Doshna, S., Wang, B., Graham, T. L., Wang, N. & Volkin, D. B. 2005 Stabilization of human papillomavirus virus-like particles by non-ionic surfactants. J. Pharm. Sci. 94, 1538-1551. (doi:10.1002/jps.20377)
63. Silva, J. J. R. F. & Williams, R. J. P. 2001 The biological chemistry of the elements: the inorganic chemistry of life, 2nd edn, pp. 279-312. New York, NY: Oxford University Press.
64. Stehle, T. & Harrison, S. C. 1997 High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J. 16, 5139-5148. (doi:10.1093/emboj/16.16.5139)
65. Stehle, T., Yan, Y.W., Benjamin, T. L. & Harrison, S. C. 1994 Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 369, 160-163. (doi:10.1038/369160a0)
66. Tessier, P. M., Lenhoff, A. M. & Sandler, S. I. 2002a Rapid measurement of protein osmotic second virial coefficients by self-interaction chromatography. Biophys. J. 82, 1620-1631. (doi:10.1016/S0006- 3495(02)75513-6)
67. Tessier, P. M., Vandrey, S. D., Berger, B. W., Pazhianur, R., Sandler, S. I. & Lenhoff, A. M. 2002b Self-interaction chromatography: a novel screening method for rational protein crystallization. Acta Crystallogr. D Biol. Crystallogr. 58, 1531-1535. (doi:10.1107/S0907444902012775)
68. Trainoff, S. P. & Wyatt, P. J. 2002 Method for determining average solution properties of macromolecules by the injection method. Santa Barbara, CA: Wyatt Technology Corporation.
69. Tsai, B., Gilbert, J. M., Stehle, T., Lencer, W., Benjamin, T. L. & Rapoport, T. A. 2003 Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 22, 4346-4355. (doi:10.1093/emboj/cdg439)
70. Velev, O. D., Kaler, E. W. & Lenhoff, A. M. 1998 Protein interactions in solution characterized by light and neutron scattering: comparison of lysozyme and chymotrypsinogen. Biophys. J. 75, 2682-2697. (doi:10.1016/S0006-3495(98)77713-6)
71. Vivares, D., Kaler, E. W. & Lenhoff, A. M. 2005 Quantitative imaging by confocal scanning .uorescence microscopy of protein crystallization via liquid-liquid phase separation. Acta Crystallogr. D Biol. Crystallogr. 61, 819-825. (doi:10.1107/S090744490402949X)
72. Vliegenthart, G. A. & Lekkerkerker, H. N.W. 2000 Predicting the gas-liquid critical point from the second virial coefficient. J. Chem. Phys. 112, 5364-5369. (doi:10.1063/1.481106)
73. Wen, J., Arakawa, T. & Philo, J. S. 1996 Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal. Biochem. 240, 155-166. (doi:10.1006/abio.1996.0345)
74. Wyatt, P. J. 1993 Light scattering and the absolute characterization of macromolecules. Anal. Chim. Acta 272, 1-40. (doi:10.1016/0003- 2670(93)80373-S)
75. Zhang, S. J., McNees, A. L. & Butel, J. S. 2005 Quantification of vertical transmission of murine polyomavirus by real-time quantitative PCR. J. Gen. Virol. 86, 2721-2729. (doi:10.1099/vir.0.81168-0)
76. 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. (doi:10.1006/jmbi.1994.1473)
77. Zlotnick, A., Lee, A., Bourne, C. R., Johnson, J. M., Domanico, P. L. & Stray, S. J. 2007 In vitro screening for molecules that affect virus capsid assembly (and other protein association reactions). Nat. Protoc. 2, 490-498. (doi:10.1038/nprot.2007.60)