Understanding the concentration dependence of viral capsid assembly kinetics - The origin of the lag time and identifying the critical nucleus size

Biophysical Journal

Volumn 98, Issue 6, 2010, Pages 1065-1074

  Hagan, Michael F ^a   Elrad, Oren M ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MIRIDAE;

EID: 77949633781     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.11.023     Document Type: Article

References (45)

1. Prevelige, Jr., P. E., D. Thomas, and J. King. 1993. Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells. Biophys. J. 64: 824-835.
2. Zlotnick, A., J. M. Johnson, ..., D. Endres. 1999. A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry. 38: 14644-14652.
3. Zlotnick, A., R. Aldrich, ..., M. J. Young. 2000. Mechanism of capsid assembly for an icosahedral plant virus. Virology. 277: 450-456.
4. Casini, G. L., D. Graham, ..., D. T. Wu. 2004. In vitro papillomavirus capsid assembly analyzed by light scattering. Virology. 325: 320-327.
5. Johnson, J. M., J. H. Tang, ..., A. Zlotnick. 2005. Regulating selfassembly of spherical oligomers. Nano Lett. 5: 765-770.
6. Chen, C., C. C. Kao, and B. Dragnea. 2008. Self-assembly of brome mosaic virus capsids: insights from shorter time-scale experiments. J. Phys. Chem. A. 112: 9405-9412.
7. Berthet-Colominas, C., M. Cuillel, ..., B. Jacrot. 1987. Kinetic-study of the self-assembly of brome mosaic-virus capsid. Eur. Biophys. J. Biophys. Lett. 15: 159-1.68.
8. 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.
9. Endres, D., and A. Zlotnick. 2002. Model-based analysis of assembly kinetics for virus capsids or other spherical polymers. Biophys. J. 83: 1217-1.230.
10. Morozov, A. Y., R. F. Bruinsma, and J. Rudnick. 2009. Assembly of viruses and the pseudo law of mass action. J. Chem. Phys. 131: 155101.
11. Ceres, P., and A. Zlotnick. 2002. Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry. 41: 11525-11531.
12. Kegel, W. K., and P. Schoot Pv. 2004. Competing hydrophobic and screened-Coulomb interactions in hepatitis B virus capsid assembly. Biophys. J. 86: 3905-3913.
13. Bar-Haim, A., and J. Klafter. 1998. On mean residence and first passage times in finite one-dimensional systems. J. Chem. Phys. 109: 5187-5193.
14. Hagan, M. F. 2008. Controlling viral capsid assembly with templating. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 77: 051904.
15. Schwartz, R., P. W. Shor, ..., B. Berger. 1998. Local rules simulation of the kinetics of virus capsid self-assembly. Biophys. J. 75: 2626-2636.
16. Hagan, M. F., and D. Chandler. 2006. Dynamic pathways for viral capsid assembly. Biophys. J. 91: 42-54.
17. Nguyen, H. D., V. S. Reddy, and C. L. Brooks, 3rd. 2007. Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids. Nano Lett. 7: 338-344.
18. Wilber, A. W., J. P. K. Doye, ..., P. Wong. 2007. Reversible selfassembly of patchy particles into monodisperse icosahedral clusters. J. Chem. Phys. 127: 085106.
19. Hicks, S. D., and C. L. Henley. 2006. Irreversible growth model for virus capsid assembly. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 74: 031912.
20. Elrad, O. M., and M. F. Hagan. 2008. Mechanisms of size control and polymorphism in viral capsid assembly. Nano Lett. 8: 3850-3857.
21. Rapaport, D. C. 2008. Role of reversibility in viral capsid growth: a paradigm for self-assembly. Phys. Rev. Lett. 101: 186101.
22. Nguyen, H. D., V. S. Reddy, and C. L. Brooks. 2009. Invariant polymorphism in virus capsid assembly. J. Am. Chem. Soc. 131: 2606-2614.
23. Endres, D., M. Miyahara, ..., A. Zlotnick. 2005. A reaction landscape identifies the intermediates critical for self-assembly of virus capsids and other polyhedral structures. Protein Sci. 14: 1518-1525.
24. Zhang, T. Q., and R. Schwartz. 2006. Simulation study of the contribution of oligomer/oligomer binding to capsid assembly kinetics. Biophys. J. 90: 57-64.
25. Sweeney, B., T. Zhang, and R. Schwartz. 2008. Exploring the parameter space of complex self-assembly through virus capsid models. Biophys. J. 94: 772-783.
26. Maibaum, L. 2008. Phase transformation near the classical limit of stability. Phys. Rev. Lett. 101: 256102.
27. Ceres, P., S. J. Stray, and A. Zlotnick. 2004. Hepatitis B virus capsid assembly is enhanced by naturally occurring mutation F97L. J. Virol. 78: 9538-9543.
28. Zlotnick, A. 2007. Distinguishing reversible from irreversible virus capsid assembly. J. Mol. Biol. 366: 14-18.
29. Reference deleted in proof.
30. Sorger, P. K., P. G. Stockley, and S. C. Harrison. 1986. Structure and assembly of turnip crinkle virus. II. Mechanism of reassembly in vitro. J. Mol. Biol. 191: 639-658.
31. Zandi, R., P. van der Schoot, ..., H. Reiss. 2006. Classical nucleation theory of virus capsids. Biophys. J. 90: 1939-1948.
32. Wu, D. T. 1992. The time-lag in nucleation theory. J. Chem. Phys. 97: 2644-2650.
33. Whitelam, S., E. H. Feng, ..., P. L. Geissler. 2009. The role of collective motion, in examples of coarsening and self-assembly. Soft Matter. 5: 1251-1262.
34. Jouvenet, N., P. D. Bieniasz, and S. M. Simon. 2008. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature. 454: 236-240.
35. Hagan, M. F. 2009. A theory for viral capsid assembly around electrostatic cores. J. Chem. Phys. 130: 114902.
36. Johnson, J. M., D. A. Willits, ..., A. Zlotnick. 2004. Interaction with capsid protein alters RNA structure and the pathway for in vitro assembly of cowpea chlorotic mottle virus. J. Mol. Biol. 335: 455-464.
37. Sikkema, F. D., M. Cornelias-Aragonès, ..., R. J. Nolte. 2007. Monodisperse polymer-virus hybrid nanoparticles. Org. Biomol. Chem. 5: 54-57.
38. Hu, Y., R. Zandi, ..., W. M. Gelbart. 2008. Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys. J. 94: 1428-1436.
39. Sun, J., C. DuFort, ..., B. Dragnea. 2007. Core-controlled polymorphism, in virus-like particles. Proc. Natl. Acad. Sci. USA. 104: 1354-1359.
40. Parent, K. N., S. M. Doyle, ..., C. M. Teschke. 2005. Electrostatic interactions govern both nucleation and elongation during phage P22 procapsid assembly. Virology. 340: 33-45.
41. Parent, K. N., A. Zlotnick, and C. M. Teschke. 2006. Quantitative analysis of multi-component spherical virus assembly: scaffolding protein contributes to the global stability of phage P22 procapsids. J. Mol. Biol. 359: 1097-1106.
42. Tuma, R., H. Tsuruta, ..., P. E. Prevelige. 2008. Detection of intermediates and kinetic control during assembly of bacteriophage P22 procapsid. J. Mol. Biol. 381: 1395-1406.
43. McPherson, A. 2005. Micelle formation and crystallization as paradigms for virus assembly. Bioessays. 27: 447-458.
44. Misra, N., D. Lees, ..., R. Schwartz. 2008. Pathway complexity of model virus capsid assembly systems. Comput. Math. Method Med. 9: 277-293.
45. Parent, K. N., M. M. Suhanovsky, and C. M. Teschke. 2007. Phage P22 procapsids equilibrate with free coat protein, subunits. J. Mol. Biol. 365: 513-522.