Interrogating viral capsid assembly with ion mobility-mass spectrometry

Nature Chemistry

Volumn 3, Issue 2, 2011, Pages 126-132

  Uetrecht, Charlotte ^a,b   Barbu, Ioana M ^a,b   Shoemaker, Glen K ^a,b,c   Van Duijn, Esther ^a,b   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; HEPATITIS B VIRUS; HUMAN; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; NOROVIRUS; PROTEIN CONFORMATION; VIRUS ASSEMBLY; VIRUS CAPSID;

CAPSID; CAPSID PROTEINS; HEPATITIS B VIRUS; HUMANS; MASS SPECTROMETRY; MODELS, MOLECULAR; NOROVIRUS; PROTEIN CONFORMATION; VIRUS ASSEMBLY;

EID: 79251613176     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.947     Document Type: Article

References (52)

1. Alberts, B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92, 291-294 (1998).
2. Robinson, C. V., Sali, A. & Baumeister, W. The molecular sociology of the cell. Nature 450, 973-982 (2007).
3. van Duijn, E., Barendregt, A., Synowsky, S., Versluis, C. & Heck, A. J. Chaperonin complexes monitored by ion mobility mass spectrometry. J. Am. Chem. Soc. 131, 1452-1459 (2009).
4. Sykes, M. T. & Williamson, J. R. A complex assembly landscape for the 30S ribosomal subunit. Annu. Rev. Biophys. 38, 197-215 (2009).
5. Besche, H. C., Peth, A. & Goldberg, A. L. Getting to first base in proteasome assembly. Cell 138, 25-28 (2009).
6. Sharon, M., Witt, S., Glasmacher, E., Baumeister, W. & Robinson, C. V. Mass spectrometry reveals the missing links in the assembly pathway of the bacterial 20 S proteasome. J. Biol. Chem. 282, 18448-18457 (2007).
7. Caspar, D. L. & Klug, A. Physical principles in the construction of regular viruses. Cold. Spring Harb. Symp. Quant. Biol. 27, 1-24 (1962).
8. Zlotnick, A. Theoretical aspects of virus capsid assembly. J. Mol. Recogn. 18, 479-490 (2005).
9. Stockley, P. G. et al. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T=3 viral capsid. J. Mol. Biol. 369, 541-552 (2007).
10. Prasad, B. V. et al. X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287-290 (1999).
11. Zlotnick, A., Johnson, J. M., Wingfield, P. W., Stahl, S. J. & Endres, D. A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 38, 14644-14652 (1999).
12. Glass, R. I., Parashar, U. D. & Estes, M. K. Norovirus gastroenteritis. N. Engl. J. Med. 361, 1776-1785 (2009).
13. Sarin, S. K. et al. Consensus on extra-hepatic portal vein obstruction. Liver Int. 26, 512-519 (2006).
14. Prasad, B. V., Hardy, M. E., Jiang, X. & Estes, M. K. Structure of Norwalk virus. Arch. Virol. 12(Suppl.), 237-242 (1996).
15. Wynne, S. A., Crowther, R. A. & Leslie, A. G. The crystal structure of the human hepatitis B virus capsid. Mol. Cell. 3, 771-780 (1999).
16. Crowther, R. A. et al. Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 77, 943-950 (1994).
17. Hutson, A. M., Atmar, R. L., Marcus, D. M. & Estes, M. K. Norwalk virus-like particle hemagglutination by binding to H histo-blood broup antigens. J. Virol. 77, 405-415 (2003).
18. Steven, A. C. et al. Structure, assembly, and antigenicity of hepatitis B virus capsid proteins. Adv. Virus Res. 64, 125-164 (2005).
19. Zlotnick, A. et al. Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 35, 7412-7421 (1996).
20. Uetrecht, C. et al. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids. Proc. Natl Acad. Sci. USA 105, 9216-9220 (2008).
21. Dryden, K. A. et al. Native hepatitis B virions and capsids visualized by electron cryomicroscopy. Mol. Cell. 22, 843-850 (2006).
22. Duda, R. L., Martincic, K., Xie, Z. & Hendrix, R. W. Bacteriophage HK97 head assembly. FEMS Microbiol. Rev. 17, 41-46 (1995).
23. Ceres, P. & Zlotnick, A.Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry 41, 11525-11531 (2002).
24. Heck, A. J. Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5, 927-933 (2008).
25. Morton, V. L., Stockley, P. G., Stonehouse, N. J. & Ashcroft, A. E. Insights into virus capsid assembly from non-covalent mass spectrometry. Mass Spectrom. Rev. 27, 575-595 (2008).
26. Uetrecht, C. et al. Stability and shape of hepatitis B virus capsids in vacuo. Angew. Chem. Int. Ed. Engl. 47, 6247-6251 (2008).
27. Shoemaker, G. K. et al. Norwalk virus assembly and stability monitored by mass spectrometry. Mol. Cell. Proteomics 9, 1742-1751 (2010).
28. Uetrecht, C., Rose, R. J., Duijn, E. V., Lorenzen, K. & Heck, A. J. R. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39, 1633-1655 (2010).
29. Lorenzen, K., Olia, A. S., Uetrecht, C., Cingolani, G. & Heck, A. J. Determination of stoichiometry and conformational changes in the first step of the P22 tail assembly. J. Mol. Biol. 379, 385-396 (2008).
30. Ruotolo, B. T. et al. Evidence for macromolecular protein rings in the absence of bulk water. Science 310, 1658-1661 (2005).
31. Mesleh, M. F., Hunter, J. M., Shvartsburg, A. A., Schatz, G. C. & Jarrold, M. F. Structural information from ion mobility measurements: effects of the longrange potential. J. Phys. Chem. 100, 16082-16086 (1996).
32. Shvartsburg, A. A. & Jarrold, M. F. An exact hard-spheres scattering model for the mobilities of polyatomic ions. Chem. Phys. Lett. 261, 86-91 (1996).
33. Derewenda, Z. S. The use of recombinant methods and molecular engineering in protein crystallization. Methods 34, 354-363 (2004).
34. Jarrold, M. F. Peptides and proteins in the vapor phase. Annu. Rev. Phys. Chem. 51, 179-207 (2000).
35. Packianathan, C., Katen, S. P., Dann, C. E.III & Zlotnick, A. Conformational changes in the hepatitis B virus core protein are consistent with a role for allostery in virus assembly. J. Virol. 84, 1607-1615 (2010).
36. Hsu, C. et al. Characterization of polymorphism displayed by the coat protein mutants of tomato bushy stunt virus. Virology 349, 222-229 (2006).
37. Dokland, T. Freedom and restraint: themes in virus capsid assembly. Structure 8, R157-R162 (2000).
38. Hilmer, J. K., Zlotnick, A. & Bothner, B. Conformational equilibria and rates of localized motion within hepatitis B virus capsids. J. Mol. Biol. 375, 581-594 (2008).
39. Parent, K. N., Suhanovsky, M. M. & Teschke, C. M. Phage P22 procapsids equilibrate with free coat protein subunits. J. Mol. Biol. 365, 513-522 (2007).
40. Rabe, B. et al. Nuclear entry of hepatitis B virus capsids involves disintegration to protein dimers followed by nuclear reassociation to capsids. PLoS Pathog. 5, e1000563 (2009).
41. Zlotnick, A. Distinguishing reversible from irreversible virus capsid assembly. J. Mol. Biol. 366, 14-18 (2007).
42. Pringle, S. D. et al. An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Int. J. Mass Spectrom. 261, 1-12 (2007).
43. van den Heuvel, R. H. et al. Improving the performance of a quadrupole time-offlight instrument for macromolecular mass spectrometry. Anal. Chem. 78, 7473-7483 (2006).
44. van Duijn, E. et al. Tandem mass spectrometry of intact GroEL-substrate complexes reveals substrate-specific conformational changes in the trans ring. J. Am. Chem. Soc. 128, 4694-4702 (2006).
45. Lorenzen, K., Versluis, C., van Duijn, E., van den Heuvel, R. H. H. & Heck, A. J. R. Optimizing macromolecular tandem mass spectrometry of large non-covalent complexes using heavy collision gases. Int. J. Mass Spectrom. 268, 198-206 (2007).
46. Sobott, F., Hernandez, H., McCammon, M. G., Tito, M. A. & Robinson, C. V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74, 1402-1407 (2002).
47. Tahallah, N., Pinkse, M., Maier, C. S. & Heck, A. J. The effect of the source pressure on the abundance of ions of noncovalent protein assemblies in an electrospray ionization orthogonal time-of-flight instrument. Rapid Commun. Mass Spectrom. 15, 596-601 (2001).
48. Jiang, X.,Wang, M., Graham, D. Y. & Estes, M. K. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66, 6527-6532 (1992).
49. Wingfield, P. T., Stahl, S. J., Williams, R. W. & Steven, A. C. Hepatitis core antigen produced in Escherichia coli: subunit composition, conformational analysis, and in vitro capsid assembly. Biochemistry 34, 4919-4932 (1995).
50. Ruotolo, B. T., Benesch, J. L., Sandercock, A. M., Hyung, S. J. & Robinson, C. V. Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc. 3, 1139-1152 (2008).
51. Smith, D. P. et al. Deciphering drift time measurements from travelling wave ion mobility spectrometry-mass spectrometry studies. Eur. J. Mass Spectrom. 15, 113-130 (2009).
52. Roos, W. H. et al. Squeezing protein shells: how continuum elastic models, molecular dynamics simulations and experiments coalesce at the nanoscale. Biophys. J. 99, 1175-1181 (2010).