Overexpression and self-assembly of virus-like particles in Nicotiana benthamiana by a single-vector DNA replicon system

Applied Microbiology and Biotechnology

Volumn 98, Issue 19, 2014, Pages 8281-8290

  Moon, Ki Beom ^a   Lee, Jisu ^b   Kang, Sebyung ^b   Kim, Moonil ^a   Mason, Hugh S ^c   Jeon, Jae Heung ^a   Kim, Hyun Soon ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Ulsan National Institute of Science and Technology   (South Korea)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Bionanomaterial; pBYR2fp viral vector; Plant virus; Self assembly; Virus like particle

Indexed keywords

ASSEMBLY; BIOSYNTHESIS; CLONING; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; PROTEINS; SELF ASSEMBLY; VIRUSES;

BIONANOMATERIAL; CUCUMBER MOSAIC VIRUS; HETEROLOGOUS PROTEINS; NICOTIANA BENTHAMIANA; PLANT VIRUS; TRANSIENT EXPRESSION; VIRAL VECTORS; VIRUS-LIKE PARTICLES;

PLANTS (BOTANY);

CAPSID PROTEIN;

BIOTECHNOLOGY; BROMOVIRUS; CUCUMOVIRUS; GENE EXPRESSION; GENE VECTOR; GENETICS; METABOLISM; NICOTIANA; REPLICON; TYMOVIRIDAE; VIRION;

BIOTECHNOLOGY; BROMOVIRUS; CAPSID PROTEINS; CUCUMOVIRUS; GENE EXPRESSION; GENETIC VECTORS; NICOTIANA; REPLICON; TYMOVIRIDAE; VIRION;

EID: 84920249951     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5901-6     Document Type: Article

References (47)

1. Annamalai P, Rao A (2005) Replication-independent expression of genome components and capsid protein of brome mosaic virus in planta: a functional role for viral replicase in RNA packaging. Virology 338(1):96–111. doi:10.1016/j.virol.2005.05.013
2. Bally J, Nadai M, Vitel M, Rolland A, Dumain R, Dubald M (2009) Plant physiological adaptations to the massive foreign protein synthesis occurring in recombinant chloroplasts. Plant Physiol 150(3):1474–1481. doi:10.1104/pp. 109.139816
3. Cañizares MC, Nicholson L, Lomonossoff GP (2005) Use of viral vectors for vaccine production in plants. Immunol Cell Biol 83(3):263–270. doi:10.1111/j.1440-1711.2005.01339.x
4. Chen B, Randles JW, Francki R (1995) Mixed-subunit capsids can be assembled in vitro with coat protein subunits from two cucumoviruses. J Gen Virol 76(Pt 4):971–973
5. Chen C, Kwak E-S, Stein B, Kao CC, Dragnea B (2005) Packaging of gold particles in viral capsids. J Nanosci Nanotechnol 5(12):2029–2033. doi:10.1166/jnn.2005.506
6. Chen Q, He J, Phoolcharoen W, Mason HS (2011) Geminiviral vectors based on bean yellow dwarf virus for production of vaccine antigens and monoclonal antibodies in plants. Hum Vaccin 7(3):331–338. doi:10.4161/hv.7.3.14262
7. Douglas T, Young M (2006) Viruses: making friends with old foes. Science 312(5775):873–875. doi:10.1126/science.1123223
8. Falk B, Tsai J (1986) The two capsid proteins of maize rayado fino virus contain common peptide sequences. Intervirology 25(2):111–116
9. Gopinath K, Dragnea B, Kao C (2005) Interaction between brome mosaic virus proteins and RNAs: effects on RNA replication, protein expression, and RNA stability. J Virol 79(22):14222–14234. doi:10.1128/JVI.79.22.14222-14234.2005
10. Hammond RW, Hammond J (2010) Maize rayado fino virus capsid proteins assemble into virus-like particles in Escherichia coli. Virus Res 147(2):208–215. doi:10.1016/j.virusres.2009.11.002
11. Hassan S, Van Dolleweerd CJ, Ioakeimidis F, Keshavarz‐Moore E, Ma JKC (2008) Considerations for extraction of monoclonal antibodies targeted to different subcellular compartments in transgenic tobacco plants. Plant Biotechnol J 6(7):733–748. doi:10.1111/j.1467-7652.2008.00354.x
12. Hassan S, Colgan R, Paul MJ, Atkinson CJ, Sexton AL, van Dolleweerd CJ, Keshavarz-Moore E, Ma JK (2012) Recombinant monoclonal antibody yield in transgenic tobacco plants is affected by the wounding response via an ethylene dependent mechanism. Transgenic Res 21(6):1221–1232. doi:10.1007/s11248-012-9595-1
13. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218. doi:10.1007/BF01977351
14. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H (2009) A DNA replicon system for rapid high‐level production of virus‐like particles in plants. Biotechnol Bioeng 103(4):706–714. doi:10.1002/bit.22299
15. Huang Z, Phoolcharoen W, Lai H, Piensook K, Cardineau G, Zeitlin L, Whaley KJ, Arntzen CJ, Mason HS, Chen Q (2010) High‐level rapid production of full‐size monoclonal antibodies in plants by a single‐vector DNA replicon system. Biotechnol Bioeng 106(1):9–17. doi:10.1002/bit.22652
16. Kadri A, Wege C, Jeske H (2013) In vivo self-assembly of TMV-like particles in yeast and bacteria for nanotechnological applications. J Virol Methods 189(2):328–340. doi:10.1016/j.jviromet.2013.02.017
17. Kao CC, Sivakumaran K (2000) Brome mosaic virus, good for an RNA virologist’s basic needs. Mol Plant Pathol 1(2):91–97. doi:10.1046/j.1364-3703.2000.00017.x
18. Koprowski H, Yusibov V (2001) The green revolution: plants as heterologous expression vectors. Vaccine 19(17):2735–2741. doi:10.1016/S0264-410X(00)00511-9
19. Korban SS (2002) Targeting and expression of antigenic proteins in transgenic plants for production of edible oral vaccines. Vitro Cell Dev Biol-Plan 38(3):231–236. doi:10.1079/IVP2002292
20. Lico C, Chen Q, Santi L (2008) Viral vectors for production of recombinant proteins in plants. J Cell Physiol 216(2):366–377. doi:10.1002/jcp.21423
21. Lu X, Thompson JR, Perry KL (2012) Encapsidation of DNA, a protein and a fluorophore into virus-like particles by the capsid protein of cucumber mosaic virus. J Gen Virol 93(Pt 5):1120–1126. doi:10.1099/vir.0.040170-0
22. Lucas RW, Larson SB, McPherson A (2002) The crystallographic structure of brome mosaic virus. J Mol Biol 317(1):95–108. doi:10.1006/jmbi.2001.5389
23. Mallory AC, Parks G, Endres MW, Baulcombe D, Bowman LH, Pruss GJ, Vance VB (2002) The amplicon-plus system for high-level expression of transgenes in plants. Nat Biotechnol 20(6):622–625. doi:10.1038/nbt0602-622
24. Manchester M, Singh P (2006) Virus-based nanoparticles (VNPs): platform technologies for diagnostic imaging. Adv Drug Deliv Rev 58(14):1505–1522. doi:10.1016/j.addr.2006.09.014
25. Moon KB, Jeon JH, Lee WS, Kim HS (2012) Transient erythropoietin overexpression with cucumber mosaic virus suppressor 2b in Nicotiana benthamiana. Hort Environ Biotechnol 53(5):434–440. doi:10.1007/s13580-012-0971-9
26. Mor TS, Moon YS, Palmer KE, Mason HS (2003) Geminivirus vectors for high‐level expression of foreign proteins in plant cells. Biotechnol Bioeng 81(4):430–437. doi:10.1002/bit.10483
27. Natilla A, Hammond RW (2011) Maize rayado fino virus virus-like particles expressed in tobacco plants: a new platform for cysteine selective bioconjugation peptide display. J Virol Methods 178(1):209–215. doi:10.1016/j.jviromet.2011.09.013
28. Nuzzaci M, Bochicchio I, De Stradis A, Vitti A, Natilla A, Piazzolla P, Tamburro A (2009) Structural and biological properties of cucumber mosaic virus particles carrying hepatitis C virus-derived epitopes. J Virol Methods 155(2):118–121. doi:10.1016/j.jviromet.2008.10.005
29. Palmer KE, Rybicki EP (1998) The molecular biology of mastreviruses. Adv Virus Res 50:183–234
30. Ramírez P, Bonilla J, Moreno E, León P (1983) Electrophoretic transfer of viral proteins to nitrocellulose sheets and detection with peroxidase-bound lectins and protein A. J Immunol Methods 62(1):15–22. doi:10.1016/0022-1759(83)90105-9
31. Rybicki EP (2010) Plant‐made vaccines for humans and animals. Plant Biotechnol J 8(5):620–637. doi:10.1111/j.1467-7652.2010.00507.x
32. Saunders K, Lomonossoff GP (2013) Exploiting plant virus‐derived components to achieve in planta expression and for templates for synthetic biology applications. New Phytol 200(1):16–26. doi:10.1111/nph.12204
33. Scholthof HB, Scholthof K, Jackson AO (1995) Identification of tomato bushy stunt virus host-specific symptom determinants by expression of individual genes from a potato virus X vector. Plant Cell 7(8):1157–1172. doi:10.1105/tpc.7.8.1157
34. Stevens LH, Stoopen GM, Elbers IJ, Molthoff JW, Bakker HA, Lommen A, Bosch D, Jordi W (2000) Effect of climate conditions and plant developmental stage on the stability of antibodies expressed in transgenic tobacco. Plant Physiol 124(1):173–182. doi:10.1104/pp. 124.1.173
35. Streatfield SJ, Jilka JM, Hood EE, Turner DD, Bailey MR, Mayor JM, Woodard SL, Beifuss KK, Horn ME, Delaney DE (2001) Plant-based vaccines: unique advantages. Vaccine 19(17):2742–2748. doi:10.1016/S0264-410X(00)00512-0
36. Streatfield SJ, Lane JR, Brooks CA, Barker DK, Poage ML, Mayor JM, Lamphear BJ, Drees CF, Jilka JM, Hood EE (2003) Corn as a production system for human and animal vaccines. Vaccine 21(7):812–815. doi:10.1016/S0264-410X(02)00605-9
37. Thanavala Y, Huang Z, Mason HS (2006) Plant-derived vaccines: a look back at the highlights and a view to the challenges on the road ahead. Expert Rev Vaccines 5(2):249–260. doi:10.1586/14760584.5.2.249
38. Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol 21(12):570–578. doi:10.1016/j.tibtech.2003.10.002
39. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33(5):949–956. doi:10.1046/j.1365-313X.2003.01676.x
40. Wang Q, Kaltgrad E, Lin T, Johnson JE, Finn M (2002a) Natural supramolecular building blocks: wild-type cowpea mosaic virus. Chem Biol 9(7):805–811. doi:10.1016/S1074-5521(02)00165-5
41. Wang Q, Lin T, Johnson JE, Finn M (2002b) Natural supramolecular building blocks: cysteine-added mutants of cowpea mosaic virus. Chem Biol 9(7):813–819. doi:10.1016/S1074-5521(02)00166-7
42. Wikoff WR, Tsai CJ, Wang G, Baker TS, Johnson JE (1997) The structure of cucumber mosaic virus: cryoelectron microscopy, X-ray crystallography, and sequence analysis. Virology 232(1):91–97. doi:10.1006/viro.1997.8543
43. Wu Y, Yang H, Shin H-J (2011) Expression and self assembly of cowpea chlorotic mottle virus capsid proteins in Pichia pastoris and encapsulation of fluorescent myoglobin. In: MRS Proceedings, vol 1317. Cambridge Univ Press, p 6-14
44. Yusibov V, Rabindran S, Commandeur U, Twyman RM, Fischer R (2006) The potential of plant virus vectors for vaccine production. Drugs R D 7(4):203–217. doi:10.2165/00126839-200607040-00001
45. Zaitlin M (2000) Tobacco mosaic virus. AAB Descr Plant Viruses 370:1–13
46. Zeng Q, Wen H, Wen Q, Chen X, Wang Y, Xuan W, Liang J, Wan S (2013) Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 34(19):4632–4642. doi:10.1016/j.biomaterials.2013.03.017
47. Zhang X, Mason H (2006) Bean yellow dwarf virus replicons for high‐level transgene expression in transgenic plants and cell cultures. Biotechnol Bioeng 93(2):271–279. doi:10.1002/bit.20695