Display of whole proteins on inner and outer surfaces of grapevine fanleaf virus-like particles

Plant Biotechnology Journal

Volumn 14, Issue 12, 2016, Pages 2288-2299

  Belval, Lorène ^a,b   Hemmer, Caroline ^a,b   Sauter, Claude ^b   Reinbold, Catherine ^a   Fauny, Jean Daniel ^b   Berthold, François ^b   Ackerer, Léa ^a,b,c   Schmitt Keichinger, Corinne ^b   Lemaire, Olivier ^a   Demangeat, Gérard ^a   Ritzenthaler, Christophe ^b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Institut Français de la Vigne et du Vin Pôle Val de Loire   (France)

Author keywords

nanocarrier; nanoparticles; nepovirus; virus; virus like particles

Indexed keywords

CAPSID PROTEIN; NANOPARTICLE; PLANT PROTEIN; RECOMBINANT PROTEIN;

GENETICS; METABOLISM; NEPOVIRUS; PHYSIOLOGY; VIROLOGY; VITIS;

CAPSID PROTEINS; NANOPARTICLES; NEPOVIRUS; PLANT PROTEINS; RECOMBINANT PROTEINS; VITIS;

EID: 84979753521     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12582     Document Type: Article

References (57)

1. Alonso, J., Górzny, M. and Bittner, A. (2013) The physics of tobacco mosaic virus and virus-based devices in biotechnology. Trends Biotechnol. 31, 530–538.
2. Amari, K., Boutant, E., Hofmann, C., Schmitt-Keichinger, C., Fernandez-Calvino, L., Didier, P., Lerich, A. et al. (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog. 6, e1001119–e1001119.
3. Arcangeli, C., Circelli, P., Donini, M., Aljabali, A.A., Benvenuto, E., Lomonossoff, G.P. and Marusic, C. (2014) Structure-based design and experimental engineering of a plant virus nanoparticle for the presentation of immunogenic epitopes and as a drug carrier. J. Biomol. Struct. Dyn. 32, 630–647.
4. Barbier, P., Demangeat, G., Perrin, M., Cobanov, P., Jacquet, C. and Walter, B. (1997) Grapevine genetically transformed with the coat protein gene of grapevine fanleaf virus: an analysis of transformants. In: Proceedings of the 12th Meeting of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine, Lisbon, Portugal, p.131, http://icvg.org/general-assembly/.
5. Bertioli, D., Harris, R., Edwards, M., Cooper, J. and Hawes, W. (1991) Transgenic plants and insect cells expressing the coat protein of arabis mosaic virus produce empty virus-like particles. J. Gen. Virol. 72, 1801–1809.
6. Bruckman, M.A., Hern, S., Jiang, K., Flask, C.A., Yu, X. and Steinmetz, N.F. (2013) Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. J. Mater. Chem. B 1, 1482–1490.
7. Brumfield, S., Willits, D., Tang, L., Johnson, J.E., Douglas, T. and Young, M. (2004) Heterologous expression of the modified coat protein of Cowpea chlorotic mottle bromovirus results in the assembly of protein cages with altered architectures and function. J. Gen. Virol. 85, 1049–1053.
8. Cardinale, D., Carette, N. and Michon, T. (2012) Virus scaffolds as enzyme nano-carriers. Trends Biotechnol. 30, 369–376.
9. Carrillo-Tripp, M., Shepherd, C.M., Borelli, I.A., Venkataraman, S., Lander, G., Natarajan, P., Johnson, J.E. et al. (2009) VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic. Acids. Res. 37, D436–D442.
10. Chandrasekar, V. and Johnson, J.E. (1998) The structure of tobacco ringspot virus: a link in the evolution of icosahedral capsids in the picornavirus superfamily. Structure, 6, 157–171.
11. Chatterji, A., Ochoa, W., Shamieh, L., Salakian, S.P., Wong, S.M., Clinton, G., Ghosh, P. et al. (2004) Chemical conjugation of heterologous proteins on the surface of cowpea mosaic virus. Bioconjug. Chem. 15, 807–813.
12. Chen, Q. and Lai, H. (2013) Plant-derived virus-like particles as vaccines. Hum. Vaccin. Immunother. 9, 26–49.
13. Demangeat, G., Hemmer, O., Reinbolt, J., Mayo, M. and Fritsch, C. (1992) Virus-specific proteins in cells infected with tomato black ring nepovirus: evidence for proteolytic processing in vivo. J. Gen. Virol. 73, 1609–1614.
14. Gaire, F., Schmitt, C., Stussi-Garaud, C., Pinck, L. and Ritzenthaler, C. (1999) Protein 2A of grapevine fanleaf nepovirus is implicated in RNA2 replication and colocalizes to the replication site. Virology, 264, 25–36.
15. Glasgow, J. and Tullman-Ercek, D. (2014) Production and applications of engineered viral capsids. Appl. Microbiol. Biotechnol. 98, 5847–5858.
16. Hassani-Mehraban, A., Creutzburg, S., van Heereveld, L. and Kormelink, R. (2015) Feasibility of cowpea chlorotic mottle virus-like particles as scaffold for epitope presentations. BMC Biotechnol. 15, 80.
17. Hesketh, E.L., Meshcheriakova, Y., Dent, K.C., Saxena, P., Thompson, R.F., Cockburn, J.J., Lomonossoff, G.P. et al. (2015) Mechanisms of assembly and genome packaging in an RNA virus revealed by high-resolution cryo-EM. Nat. Commun. 6, 10113. doi:10.1038/ncomms10113.
18. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51–59.
19. Kratz, P.A., Böttcher, B. and Nassal, M. (1999) Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl. Acad. Sci. U S A. 96, 1915–1920.
20. Lai-Kee-Him, J., Schellenberger, P., Dumas, C., Richard, E., Trapani, S., Komar, V., Demangeat, G. et al. (2013) The backbone model of the arabis mosaic virus reveals new insights into functional domains of nepovirus capsid. J. Struct. Biol. 182, 1–9.
21. Lee, E.J., Lee, N.K. and Kim, I.-S. (2016) Bioengineered protein-based nanocage for drug delivery. Adv. Drug Deliv. Rev. doi: 10.1016/j.addr.2016.03.002.
22. Lewis, J.D., Destito, G., Zijlstra, A., Gonzalez, M.J., Quigley, J.P., Manchester, M. and Stuhlmann, H. (2006) Viral nanoparticles as tools for intravital vascular imaging. Nat. Med. 12, 354–360.
23. Li, F. and Wang, Q. (2014) Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small, 10, 230–245.
24. Liu, Z., Qiao, J., Niu, Z. and Wang, Q. (2012) Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem. Soc. Rev. 41, 6178–6194.
25. Lua, L.H., Connors, N.K., Sainsbury, F., Chuan, Y.P., Wibowo, N. and Middelberg, A.P. (2014) Bioengineering virus-like particles as vaccines. Biotechnol. Bioeng. 111, 425–440.
26. Marmonier, A., Schellenberger, P., Esmenjaud, D., Schmitt-Keichinger, C., Ritzenthaler, C., Andret-Link, P., Lemaire, O. et al. (2010) The coat protein determines the specificity of virus transmission by Xiphinema diversicaudatum. J. Plant. Pathol. 92, 275–279.
27. Merzlyak, E.M., Goedhart, J., Shcherbo, D., Bulina, M.E., Shcheglov, A.S., Fradkov, A.F., Gaintzeva, A., et al. (2007) Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4, 555–557.
28. Minten, I.J., Hendriks, L.J., Nolte, R.J. and Cornelissen, J.J. (2009) Controlled encapsulation of multiple proteins in virus capsids. J. Am. Chem. Soc. 131, 17771–17773.
29. 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. Vaccin. 7, 383–390.
30. Mueller, A., Eber, F.J., Azucena, C., Petershans, A., Bittner, A.M., Gliemann, H., Jeske, H. et al. (2011) Inducible site-selective bottom-up assembly of virus-derived nanotube arrays on RNA-equipped wafers. ACS Nano 5, 4512–4520.
31. 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.
32. Peyret, H., Gehin, A., Thuenemann, E.C., Blond, D., El Turabi, A., Beales, L., Clarke, D. et al. (2015) Tandem fusion of hepatitis B core antigen allows assembly of virus-like particles in bacteria and plants with enhanced capacity to accommodate foreign proteins. PLoS ONE, 10, e0120751.
33. Pokorski, J.K. and Steinmetz, N.F. (2010) The art of engineering viral nanoparticles. Mol. Pharm. 8, 29–43.
34. Porta, C., Spall, V.E., Findlay, K.C., Gergerich, R.C., Farrance, C.E. and Lomonossoff, G.P. (2003) Cowpea mosaic virus-based chimaeras: effects of inserted peptides on the phenotype, host range, and transmissibility of the modified viruses. Virology, 310, 50–63.
35. Quacquarelli, A., Gallitelli, D., Savino, V. and Martelli, G. (1976) Properties of grapevine fanleaf virus. J. Gen. Virol. 32, 349–360.
36. Rhee, J.-K., Hovlid, M., Fiedler, J.D., Brown, S.D., Manzenrieder, F., Kitagishi, H., Nycholat, C. et al. (2011) Colorful virus-like particles: fluorescent protein packaging by the Qβ capsid. Biomacromolecules, 12, 3977–3981.
37. Ritzenthaler, C. and Hofmann, C.(2007) Tubule-guided movement of plant viruses. In Viral Transport in Plants, Plant Cell Monographs, (Waigmann, E. and Heinlein, M., eds), Heidelberg: Springer. 7 63–83.
38. Sainsbury, F., Thuenemann, E.C. and Lomonossoff, G.P. (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant. Biotechnol. J. 7, 682–693.
39. 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.
40. Sainsbury, F., Saxena, P., Aljabali, 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.
41. Sanfaçon, H., Wellink, J., Le Gall, O., Karasev, A., Van der Vlugt, R. and Wetzel, T. (2009) Secoviridae: a proposed family of plant viruses within the order Picornavirales that combines the families Sequiviridae and Comoviridae, the unassigned genera Cheravirus and Sadwavirus, and the proposed genus Torradovirus. Arch. Virol. 154, 899–907.
42. Saunders, K. and Lomonossoff, G.P. (2013) Exploiting plant virus-derived components to achieve in planta expression and for templates for synthetic biology applications. New Phytol. 200, 16–26.
43. 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.
44. Schellenberger, P., Andret-Link, P., Schmitt-Keichinger, C., Bergdoll, M., Marmonier, A., Vigne, E., Lemaire, O. et al. (2010) A stretch of 11 amino acids in the βB-βC loop of the coat protein of grapevine fanleaf virus is essential for transmission by the nematode Xiphinema index. J. Virol. 84, 7924–7933.
45. Schellenberger, P., Demangeat, G., Lemaire, O., Ritzenthaler, C., Bergdoll, M., Oliéric, V., Sauter, C. et al. (2011a) Strategies for the crystallization of viruses: using phase diagrams and gels to produce 3D crystals of grapevine fanleaf virus. J. Struct. Biol. 174, 344–351.
46. Schellenberger, P., Sauter, C., Lorber, B., Bron, P., Trapani, S., Bergdoll, M., Marmonier, A. et al. (2011b) Structural Insights into viral determinants of nematode mediated Grapevine fanleaf virus transmission. PLoS Pathog. 7, e1002034.
47. Schiller, J.T. and Lowy, D.R. (2012) Understanding and learning from the success of prophylactic human papillomavirus vaccines. Nat. Rev. Microbiol. 10, 681–692.
48. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH image to imagej: 25 years of image analysis. Nat. Methods 9, 671–675.
49. Seitsonen, J.J., Susi, P., Lemmetty, A. and Butcher, S.J. (2008) Structure of the mite-transmitted blackcurrant reversion nepovirus using electron cryo-microscopy. Virology, 378, 162–168.
50. Servid, A., Jordan, P., O'Neil, A., Prevelige, P. and Douglas, T. (2013) Location of the bacteriophage P22 coat protein C-terminus provides opportunities for the design of capsid-based materials. Biomacromolecules, 14, 2989–2995.
51. Shriver, L.P., Plummer, E.M., Thomas, D.M., Ho, S. and Manchester, M. (2013) Localization of gadolinium-loaded CPMV to sites of inflammation during central nervous system autoimmunity. J. Mat. Chem. B. 1, 5256–5263.
52. Singh, S., Rothnagel, R., Prasad, B.V. and Buckley, B. (1995) Expression of tobacco ringspot virus capsid protein and satellite RNA in insect cells and three-dimensional structure of tobacco ringspot virus-like particles. Virology, 213, 472–481.
53. Steinmetz, N.F., Ablack, A.L., Hickey, J.L., Ablack, J., Manocha, B., Mymryk, J.S., Luyt, L.G. et al. (2011) Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing peptide receptors. Small, 7, 1664–1672.
54. Suci, P.A., Varpness, Z., Gillitzer, E., Douglas, T. and Young, M. (2007) Targeting and photodynamic killing of a microbial pathogen using protein cage architectures functionalized with a photosensitizer. Langmuir, 23, 12280–12286.
55. Takahashi, R.-U., Kanesashi, S.-N., Inoue, T., Enomoto, T., Kawano, M.-A., Tsukamoto, H., Takeshita, F. et al. (2008) Presentation of functional foreign peptides on the surface of SV40 virus-like particles. J. Biotechnol. 135, 385–392.
56. Vigne, E., Gottula, J., Schmitt-Keichinger, C., Komar, V., Ackerer, L., Belval, L., Rakotomalala, L. et al. (2013) A strain-specific segment of the RNA-dependent RNA polymerase of Grapevine fanleaf virus determines symptoms in Nicotiana species. J. Gen. Virol. 94, 2803–2813.
57. Zilian, E. and Maiss, E. (2011) An optimized mRFP-based bimolecular fluorescence complementation system for the detection of protein–protein interactions in planta. J. Virol. Methods 174, 158–165.