publication . Article . 2017

Combining high-resolution cryo-electron microscopy and mutagenesis to develop cowpea mosaic virus for bionanotechnology

Meshcheriakova, Y; Durrant, A; Hesketh, EL; Ranson, NA; Lomonossoff, GP;
Open Access English
  • Published: 01 Dec 2017 Journal: Biochemical Society Transactions, volume 45, issue 6, pages 1,263-1,269 (issn: 0300-5127, eissn: 1470-8752, Copyright policy)
  • Publisher: Portland Press Ltd.
  • Country: United Kingdom
Abstract
Particles of cowpea mosaic virus (CPMV) have enjoyed considerable success as nanoparticles. The development of a system for producing empty virus-like particles (eVLPs) of the virus, which are non-infectious and have the potential to be loaded with heterologous material, has increased the number of possible applications for CPMV-based particles. However, for this potential to be realised, it was essential to demonstrate that eVLPs were accurate surrogates for natural virus particles, and this information was provided by high-resolution cryo-EM studies of eVLPs. This demonstration has enabled the approaches developed for the production of modified particles devel...
Subjects
Medical Subject Headings: viruses
free text keywords: Review Articles, Review Article, 52, 4, 37, cowpea mosaic virus, cryo-electron microscopy, mutagenesis, transient expression, virus-like particle
29 references, page 1 of 2

1 Sainsbury F., Cañizares M.C. and Lomonossoff G.P. (2010) Cowpea mosaic virus: the plant virus-based biotechnology workhorse. Annu. Rev. Phytopathol. 48, 437–455 10.1146/annurev-phyto-073009-114242 20455698 [OpenAIRE] [PubMed] [DOI]

2 Steinmetz N.F., Lin T., Lomonossoff G.P. and Johnson J.E. (2009) Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology. Curr. Top. Microbiol. Immunol. 327, 23–58 PMID:1919856 9 [PubMed]

3 Lomonossoff G.P. and Evans D.J. (2014) Applications of plant viruses in bionanotechnology. Curr. Top. Microbiol. Immunol. 375, 61–87 10.1007/82_2011_184 22038411 [OpenAIRE] [PubMed] [DOI]

4 Steele J.F.C., Peyret H., Saunders K., Castells-Graells R., Marsian,J., Meshcheriakova Y.et al. (2017) Synthetic plant virology for nanobiotechnology and nanomedicine. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 9, e1447 10.1002/wnan.1447 [OpenAIRE] [DOI]

5 Rae C.S., Khor I.W., Wang Q., Destito G., Gonzalez M.J., Singh P.et al. (2005) Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 343, 224–235 10.1016/j.virol.2005.08.017 16185741 [OpenAIRE] [PubMed] [DOI]

6 Singh P., Prasuhn D., Yeh R.M., Destito G., Rae C.S., Osborn K.et al. (2007) Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J. Control. Release 120, 41–50 10.1016/j.jconrel.2007.04.003 17512998 [OpenAIRE] [PubMed] [DOI]

7 Saunders K., Sainsbury F. and Lomonossoff G.P. (2009) Efficient generation of Cowpea Mosaic Virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 393, 329–337 10.1016/j.virol.2009.08.023 19733890 [OpenAIRE] [PubMed] [DOI]

8 Hesketh,E.L., Meshcheriakova,Y., Dent,K.C., Saxena,P., Thompson,R.F., Cockburn,J.J.et al. (2015) Mechanisms of assembly and genome packaging in an RNA virus revealed by high-resolution cryo-EM. Nat. Commun. 6, 10113 10.1038/ncomms10113 26657148 [OpenAIRE] [PubMed] [DOI]

9 Huynh N.T., Hesketh,E.L., Saxena,P., Meshcheriakova,Y., Ku,Y.-C., Hoang,L.T.et al. (2016) Crystal structure and proteomics analysis of empty virus-like particles of cowpea mosaic virus. Structure 24, 567–575 10.1016/j.str.2016.02.011 27021160 [OpenAIRE] [PubMed] [DOI]

10 Lin T., Chen Z., Usha R., Stauffacher C.V., Dai J.-B., Schmidt T.et al. (1999) The refined crystal structure of cowpea mosaic virus at 2.8 Å resolution. Virology 265, 20–34 10.1006/viro.1999.0038 10603314 [OpenAIRE] [PubMed] [DOI]

11 Hesketh E.L., Meshcheriakova Y., Thompson R.F., Lomonossoff G.P. and Ranson N.A. (2017) The structures of a naturally empty cowpea mosaic virus particle and its genome-containing counterpart by cryo-electron microscopy. Sci. Rep. 7, 539 10.1038/s41598-017-00533-w 28373698 [OpenAIRE] [PubMed] [DOI]

12 Montague N.P., Thuenemann E.C., Saxena P., Saunders K., Lenzi,P. and Lomonossoff G.P. (2011) Recent advances of cowpea mosaic virus-based particle technology. Hum. Vaccines 7, 383–390 10.4161/hv.7.3.14989 [OpenAIRE] [DOI]

13 Sainsbury F., Saxena P., Aljabali A.A.A., Saunders K., Evans D.J. and Lomonossoff G.P. (2014) Genetic engineering and characterization of cowpea mosaic virus empty virus-like particles. Methods Mol. Biol. 1108, 139–153 10.1007/978-1-62703-751-8_11 24243247 [OpenAIRE] [PubMed] [DOI]

14 Usha R., Rohll J.B., Spall V.E., Shanks M., Maule A.J., Johnson J.E.et al. (1993) Expression of an animal virus antigenic site on the surface of a plant virus particle. Virology 197, 366–374 10.1006/viro.1993.1598 7692669 [OpenAIRE] [PubMed] [DOI]

15 Porta C., Spall V.E., Loveland J., Johnson J.E., Barker P.J. and Lomonossoff G.P. (1994) Development of cowpea mosaic virus as a high-yielding system for the presentation of foreign peptides. Virology 202, 949–955 10.1006/viro.1994.1417 8030255 [OpenAIRE] [PubMed] [DOI]

29 references, page 1 of 2
Abstract
Particles of cowpea mosaic virus (CPMV) have enjoyed considerable success as nanoparticles. The development of a system for producing empty virus-like particles (eVLPs) of the virus, which are non-infectious and have the potential to be loaded with heterologous material, has increased the number of possible applications for CPMV-based particles. However, for this potential to be realised, it was essential to demonstrate that eVLPs were accurate surrogates for natural virus particles, and this information was provided by high-resolution cryo-EM studies of eVLPs. This demonstration has enabled the approaches developed for the production of modified particles devel...
Subjects
Medical Subject Headings: viruses
free text keywords: Review Articles, Review Article, 52, 4, 37, cowpea mosaic virus, cryo-electron microscopy, mutagenesis, transient expression, virus-like particle
29 references, page 1 of 2

1 Sainsbury F., Cañizares M.C. and Lomonossoff G.P. (2010) Cowpea mosaic virus: the plant virus-based biotechnology workhorse. Annu. Rev. Phytopathol. 48, 437–455 10.1146/annurev-phyto-073009-114242 20455698 [OpenAIRE] [PubMed] [DOI]

2 Steinmetz N.F., Lin T., Lomonossoff G.P. and Johnson J.E. (2009) Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology. Curr. Top. Microbiol. Immunol. 327, 23–58 PMID:1919856 9 [PubMed]

3 Lomonossoff G.P. and Evans D.J. (2014) Applications of plant viruses in bionanotechnology. Curr. Top. Microbiol. Immunol. 375, 61–87 10.1007/82_2011_184 22038411 [OpenAIRE] [PubMed] [DOI]

4 Steele J.F.C., Peyret H., Saunders K., Castells-Graells R., Marsian,J., Meshcheriakova Y.et al. (2017) Synthetic plant virology for nanobiotechnology and nanomedicine. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 9, e1447 10.1002/wnan.1447 [OpenAIRE] [DOI]

5 Rae C.S., Khor I.W., Wang Q., Destito G., Gonzalez M.J., Singh P.et al. (2005) Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 343, 224–235 10.1016/j.virol.2005.08.017 16185741 [OpenAIRE] [PubMed] [DOI]

6 Singh P., Prasuhn D., Yeh R.M., Destito G., Rae C.S., Osborn K.et al. (2007) Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J. Control. Release 120, 41–50 10.1016/j.jconrel.2007.04.003 17512998 [OpenAIRE] [PubMed] [DOI]

7 Saunders K., Sainsbury F. and Lomonossoff G.P. (2009) Efficient generation of Cowpea Mosaic Virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 393, 329–337 10.1016/j.virol.2009.08.023 19733890 [OpenAIRE] [PubMed] [DOI]

8 Hesketh,E.L., Meshcheriakova,Y., Dent,K.C., Saxena,P., Thompson,R.F., Cockburn,J.J.et al. (2015) Mechanisms of assembly and genome packaging in an RNA virus revealed by high-resolution cryo-EM. Nat. Commun. 6, 10113 10.1038/ncomms10113 26657148 [OpenAIRE] [PubMed] [DOI]

9 Huynh N.T., Hesketh,E.L., Saxena,P., Meshcheriakova,Y., Ku,Y.-C., Hoang,L.T.et al. (2016) Crystal structure and proteomics analysis of empty virus-like particles of cowpea mosaic virus. Structure 24, 567–575 10.1016/j.str.2016.02.011 27021160 [OpenAIRE] [PubMed] [DOI]

10 Lin T., Chen Z., Usha R., Stauffacher C.V., Dai J.-B., Schmidt T.et al. (1999) The refined crystal structure of cowpea mosaic virus at 2.8 Å resolution. Virology 265, 20–34 10.1006/viro.1999.0038 10603314 [OpenAIRE] [PubMed] [DOI]

11 Hesketh E.L., Meshcheriakova Y., Thompson R.F., Lomonossoff G.P. and Ranson N.A. (2017) The structures of a naturally empty cowpea mosaic virus particle and its genome-containing counterpart by cryo-electron microscopy. Sci. Rep. 7, 539 10.1038/s41598-017-00533-w 28373698 [OpenAIRE] [PubMed] [DOI]

12 Montague N.P., Thuenemann E.C., Saxena P., Saunders K., Lenzi,P. and Lomonossoff G.P. (2011) Recent advances of cowpea mosaic virus-based particle technology. Hum. Vaccines 7, 383–390 10.4161/hv.7.3.14989 [OpenAIRE] [DOI]

13 Sainsbury F., Saxena P., Aljabali A.A.A., Saunders K., Evans D.J. and Lomonossoff G.P. (2014) Genetic engineering and characterization of cowpea mosaic virus empty virus-like particles. Methods Mol. Biol. 1108, 139–153 10.1007/978-1-62703-751-8_11 24243247 [OpenAIRE] [PubMed] [DOI]

14 Usha R., Rohll J.B., Spall V.E., Shanks M., Maule A.J., Johnson J.E.et al. (1993) Expression of an animal virus antigenic site on the surface of a plant virus particle. Virology 197, 366–374 10.1006/viro.1993.1598 7692669 [OpenAIRE] [PubMed] [DOI]

15 Porta C., Spall V.E., Loveland J., Johnson J.E., Barker P.J. and Lomonossoff G.P. (1994) Development of cowpea mosaic virus as a high-yielding system for the presentation of foreign peptides. Virology 202, 949–955 10.1006/viro.1994.1417 8030255 [OpenAIRE] [PubMed] [DOI]

29 references, page 1 of 2
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