Disulfide linkage and structure of highly stable yeastderived virus-like particles of murine polyomavirus

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10411-10418

  Simon, Claudia ^a   Klose, Thomas ^b   Herbst, Sabine ^a   Han, Bong Gyoon ^c   Sinz, Andrea ^a   Glaeser, Robert M ^c   Stubbs, Milton T ^a   Lilie, Hauke ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COVALENT BONDS; VIRUSES;

ACTIVATION ENTHALPIES; CELLULAR COMPONENTS; CLAMP STRUCTURE; CRYO-ELECTRON MICROSCOPY; DISULFIDE LINKAGES; RECOMBINANT PROTEIN PRODUCTIONS; STRUCTURAL FEATURE; VIRUS-LIKE PARTICLES;

SULFUR COMPOUNDS;

CYSTEINE; RECOMBINANT PROTEIN; TRYPSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENTHALPY; FUNGAL STRAIN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN STRUCTURE; VIRUS LIKE AGENT;

PROTEIN SELF-ASSEMBLY; PROTEIN STABILITY; VIRAL PROTEIN; VIRUS ASSEMBLY; YEAST;

AMINO ACID SEQUENCE; CAPSID; CAPSID PROTEINS; CROSS-LINKING REAGENTS; CRYOELECTRON MICROSCOPY; CYSTEINE; DISULFIDES; HOT TEMPERATURE; KINETICS; KLUYVEROMYCES; MOLECULAR SEQUENCE DATA; PEPTIDES; POLYOMAVIRUS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RIBONUCLEASE, PANCREATIC; TRYPSIN; ULTRACENTRIFUGATION; VIRION; VIRUS ASSEMBLY;

EID: 84898655869     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.484162     Document Type: Article

References (34)

1. Stehle, T., and Harrison, S. C. (1996) Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure 4, 183-194
2. Bird, G., O'Donnell, M., Moroianu, J., and Garcea, R. L. (2008) Possible role for cellular karyopherins in regulating polyomavirus and papillomavirus capsid assembly. J. Virol. 82, 9848-9857
3. Erickson, K. D., Bouchet-Marquis, C., Heiser, K., Szomolanyi-Tsuda, E., Mishra, R., Lamothe, B., Hoenger, A., and Garcea, R. L. (2012) Virion assembly factories in the nucleus of polyomavirus-infected cells. PLoS Pathog. 8, e1002630
4. Walczak, C. P., and Tsai, B. (2011) A PDI family network acts distinctly and coordinately with ERp29 to facilitate polyomavirus infection. J. Virol. 85, 2386-2396
5. Richterová, Z., Liebl, D., Horák, M., Palková, Z., Stokrová, J., Hozák, P., Korb, J., and Forstová, J. (2001) Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J. Virol. 75, 10880-10891
6. Inoue, T., and Tsai, B. (2011)Alarge and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol. PLoS Pathog. 7, e1002037
7. Mannová, P., and Forstová, J. (2003) Mouse polyomavirus utilizes recycling endosomes for a traffic pathway independent of COPI vesicle transport. J. Virol. 77, 1672-1681
8. Leavitt, A. D., Roberts, T. M., and Garcea, R. L. (1985) Polyoma virus major capsid protein, VP1. Purification after high level expression in Escherichia coli. J. Biol. Chem. 260, 12803-12809
9. Liew, M. W., Rajendran, A., and Middelberg, A. P. (2010) Microbial production of virus-like particle vaccine protein at gram-per-litre levels. J. Biotechnol. 150, 224-231
10. Salunke, D. M., Caspar, D. L., and Garcea, R. L. (1986) Self-assembly of purified polyomavirus capsid protein VP1. Cell 46, 895-904
11. Montross, L., Watkins, S., Moreland, R. B., Mamon, H., Caspar, D. L., and Garcea, R. L. (1991) Nuclear assembly of polyomavirus capsids in insect cells expressing the major capsid protein VP1. J. Virol. 65, 4991-4998
12. Palková, Z., Adamec, T., Liebl, D., Stokrová, J., and Forstová, J. (2000) Production of polyomavirus structural protein VP1 in yeast cells and its interaction with cell structures. FEBS Lett. 478, 281-289
13. Sasnauskas, K., Buzaite, O., Vogel, F., Jandrig, B., Razanskas, R., Staniulis, J., Scherneck, S., Krüger, D. H., and Ulrich, R. (1999) Yeast cells allow high-level expression and formation of polyomavirus-like particles. Biol. Chem. 380, 381-386
14. Simon, C., Schaepe, S., Breunig, K., and Lilie, H. (2013) Production of polyomavirus-like particles in a kLGAL80 knockout strain of the yeast Kluyveromyces lactis. Prep. Biochem. Biotechnol. 43, 217-235
15. Salunke, D. M., Caspar, D. L., and Garcea, R. L. (1989) Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys. J. 56, 887-900
16. Götze, M., Pettelkau, J., Schaks, S., Bosse, K., Ihling, C. H., Krauth, F., Fritzsche, R., Kühn, U., and Sinz, A. (2012) StavroX-A software for analyzing cross-linked products in protein interaction studies. J. Am. Soc. Mass. Spectrom. 23, 76-87
17. Typke, D., Nordmeyer, R. A., Jones, A., Lee, J., Avila-Sakar, A., Downing, K. H., and Glaeser, R. M. (2005) High-throughput film-densitometry: An efficient approach to generate large data sets. J. Struct. Biol. 149, 17-29
18. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97
19. Frank, J. (2006) Three-dimensional Electron Microscopy of Macromolecular Assemblies-Visualization of Biology Cal Molecules in Their Native State, 2 Ed., pp. 71-145, Oxford University Press, New York
20. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
21. DeLano, W. L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific LLC, San Carlos, CA
22. Jao, C. C., Weidman, M. K., Perez, A. R., and Gharakhanian, E. (1999) Cys9, Cys104 and Cys207 of simian virus 40 Vp1 are essential for interpentamer disulfide-linkage and stabilization in cell-free lysates. J. Gen. Virol. 80, 2481-2489
23. Liddington, R. C., Yan, Y., Moulai, J., Sahli, R., Benjamin, T. L., and Harrison, S. C. (1991) Structure of simian virus 40 at 3.8-A resolution. Nature 354, 278-284
24. Schelhaas, M., Malmström, J., Pelkmans, L., Haugstetter, J., Ellgaard, L., Grünewald, K., and Helenius, A. (2007) Simian virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131, 516-529
25. Sasnauskas, K., Bulavaite, A., Hale, A., Jin, L., Knowles, W. A., Gedvilaite, A., Dargeviciute, A., Bartkeviciute, D., Zvirbliene, A., Staniulis, J., Brown, D. W., and Ulrich, R. (2002) Generation of recombinant virus-like particles of human and non-human polyomaviruses in yeast Saccharomyces cerevisiae. Intervirology 45, 308-317
26. Ashcroft, A. E., Lago, H., Macedo, J. M., Horn, W. T., Stonehouse, N. J., and Stockley, P. G. (2005) Engineering thermal stability in RNA phage capsids via disulphide bonds. J. Nanosci. Nanotechnol. 5, 2034-2041
27. Bundy, B. C., and Swartz, J. R. (2011) Efficient disulfide bond formation in virus-like particles. J. Biotechnol. 154, 230-239
28. Li, P. P., Nakanishi, A., Tran, M. A., Salazar, A. M., Liddington, R. C., and Kasamatsu, H. (2000) Role of simian virus 40 Vp1 cysteines in virion infectivity. J. Virol. 74, 11388-11393
29. Chang, D., Fung, C. Y., Ou, W. C., Chao, P. C., Li, S. Y., Wang, M., Huang, Y. L., Tzeng, T. Y., and Tsai, R. T. (1997) Self-assembly of the JC virus major capsid protein, VP1, expressed in insect cells. J. Gen. Virol. 78, 1435-1439
30. Stehle, T., and Harrison, S. C. (1997) High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J. 16, 5139-5148
31. Schmidt, U., Rudolph, R., and Böhm, G. (2000) Mechanism of assembly of recombinant murine polyomavirus-like particles. J. Virol. 74, 1658-1662
32. Cripe, T. P., Delos, S. E., Estes, P. A., and Garcea, R. L. (1995) In vivo and in vitro association of hsc70 with polyomavirus capsid proteins. J. Virol. 69, 7807-7813
33. Chromy, L. R., Pipas, J. M., and Garcea, R. L. (2003) Chaperone-mediated in vitro assembly of polyomavirus capsids. Proc. Natl. Acad. Sci. U.S.A. 100, 10477-10482
34. Palková, Z., Spanielová, H., Gottifredi, V., Hollanderová, D., Forstová, J., and Amati, P. (2000) The polyomavirus major capsid protein VP1 interacts with the nuclear matrix regulatory protein YY1. FEBS Lett. 467, 359-364