In vitro assembly of Tobacco mosaic virus coat protein variants derived from fission yeast expression clones or plants

Journal of Virological Methods

Volumn 166, Issue 1-2, 2010, Pages 77-85

  Mueller, Anna ^a   Kadri, Anan ^a   Jeske, Holger ^a   Wege, Christina ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

Coat protein mutants; Fission yeast; Nanotechnology; Schizosaccharomyces pombe; Self assembly; Tobacco mosaic virus

Indexed keywords

COAT PROTEIN; HEXAHISTIDINE; NANOMATERIAL; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENRICHMENT CULTURE; GENE CONSTRUCT; GENETIC ENGINEERING; GENETIC VARIABILITY; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; MOLECULAR CLONING; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SCHIZOSACCHAROMYCES POMBE; TOBACCO MOSAIC VIRUS; VIRION; WILD TYPE; YEAST;

CAPSID PROTEINS; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; GENE EXPRESSION; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ELECTRON, TRANSMISSION; MUTANT PROTEINS; NANOPARTICLES; PLANTS; RECOMBINANT FUSION PROTEINS; SCHIZOSACCHAROMYCES; TOBACCO MOSAIC VIRUS; VIROSOMES;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE; TOBACCO MOSAIC VIRUS;

EID: 77952674391     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2010.02.026     Document Type: Article

References (78)

1. Aberle H.J., Rutz M.L., Karayavuz M., Frischmuth S., Wege C., Hulser D., Jeske H. Localizing the movement proteins of Abutilon mosaic geminivirus in yeast by subcellular fractionation and freeze-fracture immuno-labelling. Arch. Virol. 2002, 147:103-117.
2. Amor-Mahjoub M., Suppini J.-P., Gomez-Vrielyunck N., Ladjimi M. The effect of the hexahistidine-tag in the oligomerization of HSC70 constructs. J. Chromatogr. B 2006, 844:328-334.
3. Arnold F.H., Haymore B.L. Engineered metal-binding proteins: purification to protein folding. Science 1991, 252:1796-1797.
4. Balci S., Leinberger D., Knez M., Bittner A.M., Boes F., Wege C., Jeske H., Kern K. Printing and aligning mesoscale patterns of Tobacco mosaic virus on surfaces. Adv. Mater. 2008, 20:2195-2200.
5. Balci S., Noda K., Bittner A.M., Kadri A., Wege C., Jeske H., Kern K. Self-assembly of metal-virus nanodumbbells. Angew. Chem. Int. Ed. 2007, 46:3149-3151.
6. Banerjee I.A., Yu L., Matsui H. Cu nanocrystal growth on peptide nanotubes by biomineralization: size control of Cu nanocrystals by tuning peptide conformation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14678-14682.
7. Basi G., Schmid E., Maundrell K. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene 1993, 123:131-136.
8. Bendahmane M., Chen I., Asurmendi S., Bazzini A.A., Szecsi J., Beachy R.N. Coat protein-mediated resistance to TMV infection of Nicotiana tabacum involves multiple modes of interference by coat protein. Virology 2007, 366:107-116.
9. Bendahmane M., Koo M., Karrer E., Beachy R.N. Display of epitopes on the surface of tobacco mosaic virus: impact of charge and isoelectric point of the epitope on virus-host interactions. J. Mol. Biol. 1999, 290:9-20.
10. Blum H., Beier H., Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8:93-99.
11. Boston R.S., Viitanen P.V., Vierling E. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 1996, 32:191-222.
12. Buning H., Gartner U., von Schack D., Baeuerle P.A., Zorbas H. The histidine tail of recombinant DNA binding proteins may influence the quality of interaction with DNA. Anal. Biochem. 1996, 234:227-230.
13. Busso D., Kim R., Kim S.-H. Expression of soluble recombinant proteins in a cell-free system using a 96-well format. J. Biochem. Biophys. Met. 2003, 55:233-240.
14. Butler P.J. Self-assembly of tobacco mosaic virus: the role of an intermediate aggregate in generating both specificity and speed. Philos. Trans. R. Soc., Lond. B. Biol. Sci. 1999, 354:537-550.
15. Chatterji A., Ochoa W.F., Ueno T., Lin T., Johnson J.E. A virus-based nanoblock with tunable electrostatic properties. Nano Lett. 2005, 5:597-602.
16. Culver J.N., Dawson W.O., Plonk K., Stubbs G. Site-directed mutagenesis confirms the involvement of carboxylate groups in the disassembly of tobacco mosaic virus. Virology 1995, 206:724-730.
17. Demir M., Stowell H.B. A chemoselective biomolecular template for assembling diverse nanotubular materials. Nanotechnology 2002, 13:541-544.
18. Devash Y., Hauschner A., Sela I., Chakraburtty K. The antiviral factor (AVF) from virus-infected plants induces discharge of histidinyl-TMV-RNA. Virology 1981, 111:103-112.
19. Durham A.C., Finch J.T. Structure and roles of the polymorphic forms of Tobacco mosaic virus protein. II. Electron microscope observations of the larger polymers. J. Mol. Biol. 1972, 67:307-314.
20. Durham A.C., Finch J.T., Klug A. States of aggregation of Tobacco mosaic virus protein. Nat. New Biol. 1971, 229:37-42.
21. Durham A.C., Klug A. Polymerization of Tobacco mosaic virus protein and its control. Nat. New Biol. 1971, 229:42-46.
22. Eckart M.R., Bussineau C.M. Quality and authenticity of heterologous proteins synthesized in yeast. Curr. Opin. Biotechnol. 1996, 7:525-530.
23. Endo M., Wang H., Fujitsuka M., Majima T. Pyrene-stacked nanostructures constructed in the recombinant Tobacco mosaic virus rod scaffold. Chemistry 2006, 12:3735-3740.
24. Forsburg S.L. The best yeast?. Trends Genet. 1999, 15:340-344.
25. Forsburg S.L., Rhind N. Basic methods for fission yeast. Yeast 2006, 23:173-183.
26. Fraenkel-Conrat H. Degradation of Tobacco mosaic virus with acetic acid. Virology 1957, 4:1-4.
27. Frischmuth S., Wege C., Hulser D., Jeske H. The movement protein BC1 promotes redirection of the nuclear shuttle protein BV1 of Abutilon mosaic geminivirus to the plasma membrane in fission yeast. Protoplasma 2007, 230:117-123.
28. Halliwell C.M., Morgan G., Ou C.-P., Cass A.E.G. Introduction of a (poly)histidine tag in lactate dehydrogenase produces a mixture of active and inactive molecules. Anal. Biochem 2001, 295:257-261.
29. Hamacher J., Wettern M., Schulz M. Ubiquitination of TMV coat protein aggregates in infected tobacco leaves. J. Phytopathol. 2003, 151:652-659.
30. Hwang D.J., Roberts I.M., Wilson T.M. Expression of Tobacco mosaic virus coat protein and assembly of pseudovirus particles in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:9067-9071.
31. Hwang D.J., Tumer N.E., Wilson T.M. Chaperone protein GrpE and the GroEL/GroES complex promote the correct folding of Tobacco mosaic virus coat protein for ribonucleocapsid assembly in vivo. Arch. Virol. 1998, 143:2203-2214.
32. Jockusch H., Wiegand C. Misfolded plant virus proteins: elicitors and targets of ubiquitylation. FEBS Lett. 2003, 545:229-232.
33. Jockusch H., Wiegand C., Mersch B., Rajes D. Mutants of Tobacco mosaic virus with temperature-sensitive coat proteins induce heat shock response in tobacco leaves. Mol. Plant-Microbe Interact. 2001, 14:914-917.
34. Kadri, A., 2007. Maßgeschneiderte Tabakmosaikviren für die Nanotechnologie. PhD Thesis, Molekularbiologie und Virologie der Pflanzen, Universität Stuttgart.
35. Kittelmann K., Rau P., Gronenborn B., Jeske H. Plant geminivirus Rep protein induces re-replication in fission yeast. J. Virol. 2009, 83:6769-6778.
36. Kleinow T., Holeiter G., Nischang M., Stein M., Karayavuz M., Wege C., Jeske H. Post-translational modifications of Abutilon mosaic virus movement protein (BC1) in fission yeast. Virus Res. 2008, 131:86-94.
37. Kleinow T., Nischang M., Beck A., Kratzer U., Tanwir F., Preiss W., Kepp G., Jeske H. Three C-terminal phosphorylation sites in the Abutilon mosaic virus movement protein affect symptom development and viral DNA accumulation. Virology 2009, 390:89-101.
38. Klug A. The Tobacco mosaic virus particle: structure and assembly. Philos. Trans. R. Soc., Lond. B. Biol. Sci. 1999, 354:531-535.
39. Knez M., Bittner A.M., Boes F., Wege C., Jeske H., Mai E., Kern K. Biotemplate synthesis of 3-nm nickel and cobalt nanowires. Nano Lett. 2003, 3:1079-1082.
40. Knez M., Kadri A., Wege C., Gösele U., Jeske H., Nielsch K. Atomic layer deposition on biological macromolecules: metal oxide coating of Tobacco mosaic virus and ferritin. Nano Lett. 2006, 6:1172-1177.
41. Knez M., Sumser M., Bittner A.M., Wege C., Jeske H., Martin T.P., Kern K. Spatially selective nucleation of metal clusters on the Tobacco mosaic virus. Adv. Funct. Mater. 2004, 14:116-124.
42. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
43. Lee S.Y., Choi J., Royston E., Janes D.B., Culver J.N., Harris M.T. Deposition of platinum clusters on surface-modified Tobacco mosaic virus. J. Nanosci. Nanotechnol. 2006, 6:974-981.
44. Lewandowski D.J. Genus Tobamovirus. Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses 2005, 1009-1014. Elsevier/Academic Press, London. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
45. Li Q., Jiang L., Li M., Li P., Zhang Q., Song R., Xu Z. Morphology and stability changes of recombinant TMV particles caused by a cysteine residue in the foreign peptide fused to the coat protein. J. Virol. Met. 2007, 140:212-217.
46. Lu B., Stubbs G., Culver J.N. Carboxylate interactions involved in the disassembly of tobacco mosaic tobamovirus. Virology 1996, 225:11-20.
47. Lu B., Taraporewala F., Stubbs G., Culver J.N. Intersubunit interactions allowing a carboxylate mutant coat protein to inhibit tobamovirus disassembly. Virology 1998, 244:13-19.
48. Maree H.J., van der Walt E., Tiedt F.A.C., Hanzlik T.N., Appel M. Surface display of an internal His-tag on virus-like particles of Nudaurelia capensis [omega] virus (N[omega]V) produced in a baculovirus expression system. J. Virol. Methods 2006, 136:283-288.
49. Matsuyama A., Shirai A., Yoshida M. A series of promoters for constitutive expression of heterologous genes in fission yeast. Yeast 2008, 25:371-376.
50. Maundrell K. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 1993, 123:127-130.
51. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
52. McCormick A.A., Corbo T.A., Wykoff-Clary S., Nguyen L.V., Smith M.L., Palmer K.E., Pogue G.P. TMV-peptide fusion vaccines induce cell-mediated immune responses and tumor protection in two murine models. Vaccine 2006, 24:6414-6423.
53. Milne R.G., Lesemann D.E. Immunosorbent electron microscopy in plant virus studies. Methods in Virology 1984, Academic Press, Inc, Orlando, San Diego, New York, London. K. Koprowski (Ed.).
54. Mohanty A.K., Wiener M.C. Membrane protein expression and production: effects of polyhistidine tag length and position. Prot. Expr. Purif. 2004, 33:311-325.
55. Mutombo K., Michels B., Ott H., Cerf R., Witz J. Scanning calorimetric studies of the stability of Tobacco mosaic virus and aggregates of its coat protein. Eur. Biophys. J. 1992, 21:77-83.
56. Namba K., Pattanayek R., Stubbs G. Visualization of protein-nucleic acid interactions in a virus. Refined structure of intact Tobacco mosaic virus at 2.9A resolution by X-ray fiber diffraction. J. Mol. Biol. 1989, 208:307-325.
57. Nicolaieff A., Lebeurier G. Polar uncoating of Tobacco mosaic virus (TMV) with dimethylsulfoxide (DMSO) and subsequent reassembly of partially stripped TMV. Mol. Genet. Genomics 1979, 171:327-333.
58. Okada Y. Molecular assembly of Tobacco mosaic virus in vitro. Adv. Biophys. 1986, 22:95-149.
59. Perham R.N., Wilson T.M.A. The characterization of intermediates formed during the disassembly of Tobacco mosaic virus at alkaline pH. Virology 1978, 84:293-302.
60. Pietzsch M., Wiese A., Ragnitz K., Wilms B., Altenbuchner J., Mattes R., Syldatk C. Purification of recombinant hydantoinase and -N-carbamoylase from Arthrobacter aurescens expressed in Escherichia coli: comparison of wild-type and genetically modified proteins. J. Chromatogr. B 2000, 737:179-186.
61. Renzi F., Panetta G., Vallone B., Brunori M., Arceci M., Bozzoni I., Laneve P., Caffarelli E. Large-scale purification and crystallization of the endoribonuclease XendoU: troubleshooting with His-tagged proteins. Acta Crystallogr. F 2006, 62:298-301.
62. Richards K.E., Williams R.C. Assembly of Tobacco mosaic virus in vitro: effect of state of polymerization of the protein component. Proc. Natl. Acad. Sci. U.S.A. 1972, 69:1121-1124.
63. Royston E., Ghosh A., Kofinas P., Harris M.T., Culver J.N. Self-assembly of virus-structured high surface area nanomaterials and their application as battery electrodes. Langmuir 2008, 24:906-912.
64. Sachse C., Chen J.Z., Coureux P.-D., Stroupe M.E., Fändrich M., Grigorieff N. High-resolution electron microscopy of helical specimens: a fresh look at Tobacco mosaic virus. J. Mol. Biol. 2007, 371:812-835.
65. Sambrook S., Russell D.W. Molecular Cloning. A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
66. Schlick T.L., Ding Z., Kovacs E.W., Francis M.B. Dual-surface modification of the Tobacco mosaic virus. J. Am. Chem. Soc. 2005, 127:3718-3723.
67. Shibagaki Y., Holmes M.L., Appa R.S., Chow S.A. Characterization of feline immunodeficiency virus integrase and analysis of functional domains. Virology 1997, 230:1-10.
68. Shire S.J., McKay P., Leung D.W., Cachianes G.J., Jackson E., Wood W.I., Raghavendra K., Khairallah L., Schuster T.M. Preparation and properties of recombinant DNA derived tobacco mosaic virus coat protein. Biochemistry 1990, 29:5119-5126.
69. Slocik J.M., Moore J.T., Wright D.W. Monoclonal antibody recognition of histidine-rich peptide encapsulated nanoclusters. Nano Lett. 2002, 2:169-173.
70. Smith M.L., Lindbo J.A., Dillard-Telm S., Brosio P.M., Lasnik A.B., McCormick A.A., Nguyen L.V., Palmer K.E. Modified Tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology 2006, 348:475-488.
71. Sullivan C.S., Pipas J.M. The virus-chaperone connection. Virology 2001, 287:1-8.
72. Terpe K. Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 2003, 60:523-533.
73. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:4350-4354.
74. Wilson T.M., Perham R.N., Finch J.T., Butler P.J.G. Polarity of the RNA in the Tobacco mosaic virus particle and the direction of protein stripping in sodium dodecyl sulphate. FEBS Lett. 1976, 64:285-289.
75. Woestenenk E.A., Hammarstrom M., van den Berg S., Hard T., Berglund H. His tag effect on solubility of human proteins produced in Escherichia coli: a comparison between four expression vectors. J. Struct. Funct. Genom. 2004, 5:217-229.
76. Wu J., Filutowicz M. Hexahistidine (His6)-tag dependent protein dimerization: a cautionary tale. Acta Biochim. Pol. 1999, 46:591-599.
77. Yi H., Nisar S., Lee S.Y., Powers M.A., Bentley W.E., Payne G.F., Ghodssi R., Rubloff G.W., Harris M.T., Culver J.N. Patterned assembly of genetically modified viral nanotemplates via nucleic acid hybridization. Nano Lett. 2005, 5:1931-1936.
78. Zayakina O., Arkhipenko M., Smirnov A., Rodionova N., Karpova O., Atabekov J. Restoration of potato virus X coat protein capacity for assembly with RNA after His-tag removal. Arch. Virol. 2009, 154:337-341.