Efficient production of chimeric Human papillomavirus 16 L1 protein bearing the M2e influenza epitope in Nicotiana benthamiana plants

BMC Biotechnology

Volumn 11, Issue , 2011, Pages

  Matić, Slavica ^a   Rinaldi, Riccardo ^a   Masenga, Vera ^a   Noris, Emanuela ^a  

^a INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEINS; CODON USAGE; ECTODOMAIN; EFFICIENT PRODUCTION; EXPRESSION VECTORS; HIGHER-ORDER STRUCTURE; HUMAN PAPILLOMAVIRUS; INFLUENZA A; INFLUENZA A VIRUS; N-TERMINALS; NICOTIANA BENTHAMIANA; SELF-ASSEMBLE; TRANSIENT EXPRESSION; VACCINE PRODUCTION; VIRUS-LIKE PARTICLES;

ANTIGENS; GENES; PROTEINS; VIRUSES;

PLANTS (BOTANY);

CHIMERIC PROTEIN; EPITOPE; FOREIGN EPITOPE; MONOCLONAL ANTIBODY; PROTEIN M2; RIBOSOMAL PROTEIN L1; SCAFFOLD PROTEIN; SYNTHETIC DNA; UNCLASSIFIED DRUG;

ARTICLE; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC CODE; HUMAN PAPILLOMAVIRUS TYPE 16; INFLUENZA A; NICOTIANA BENTHAMIANA; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; VIRUS LIKE AGENT;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CAPSID PROTEINS; CLONING, MOLECULAR; COMOVIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; GENETIC VECTORS; HUMAN PAPILLOMAVIRUS 16; HUMANS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TOBACCO; VIRAL MATRIX PROTEINS;

COWPEA MOSAIC VIRUS; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16; INFLUENZA A VIRUS; NICOTIANA BENTHAMIANA;

EID: 81055134740     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-11-106     Document Type: Article

References (43)

1. Seedorf K, Krammer G, Durst M, Suhai S, Rowekamp WG. Human papillomavirus type 16 DNA sequence. Virology 1985, 145:181-185. 10.1016/0042-6822(85)90214-4, 2990099.
2. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006, 118:3030-3044. 10.1002/ijc.21731, 16404738.
3. Bosch FX, Manos MM, Muñoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer I 1995, 87:796-802.
4. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML, Daniel RW, Viglione M, Symer DE, Shah KV, Sidransky D. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer I 2000, 92:709-720.
5. Steenbergen RD, de Wilde J, Wilting SM, Brink AA, Snijders PJ, Meijer CJ. HPV-mediated transformation of the anogenital tract. J Clin Virol 2005, 32:S25-S33.
6. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus Li major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 1992, 89:12180-12184. 10.1073/pnas.89.24.12180, 50722, 1334560.
7. Modis Y, Trus BL, Harrison SC. Atomic model of the papillomavirus capsid. EMBO J 2002, 21:4754-4762. 10.1093/emboj/cdf494, 126290, 12234916.
8. Baker TS, Newcomb WW, Olson NH, Cowsert LM, Olson C, Brown JC. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys J 1991, 60:1445-1456. 10.1016/S0006-3495(91)82181-6, 1260204, 1663794.
9. Chen X, Garcea R, Goldberg I, Casini G, Harrison SC. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell 2000, 5:557-567. 10.1016/S1097-2765(00)80449-9, 10882140.
10. Chen XS, Casini G, Harrison SC, Garcea RL. Papillomavirus capsid protein expression in Escherichia coli: purification and assembly of HPV11 and HPV16 L1. J Mol Biol 2001, 307:173-182. 10.1006/jmbi.2000.4464, 11243812.
11. Bishop B, Dasgupta J, Chen XS. Structure-based engineering of papillomavirus major capsid L1: controlling particle assembly. Virol J 2007, 4:3. 10.1186/1743-422X-4-3, 1781933, 17210082.
12. Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Müller M. Production of human papillomavirus type 16 virus-like particles in transgenic plants. J Virol 2003, 77:9211-9220. 10.1128/JVI.77.17.9211-9220.2003, 187377, 12915537.
13. Varsani A, Williamson AL, Rose RC, Jaffer M, Rybicki EP. Expression of human papillomavirus type 16 major capsid protein in transgenic Nicotiana tabacum cv. Xanthi. Arch Virol 2003, 148:1771-1786. 10.1007/s00705-003-0119-4, 14505089.
14. Maclean J, Koekemoer M, Olivier AJ, Stewart D, Hitzeroth II, Rademacher T, Fischer R, Williamson AL, Rybicki EP. Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J Gen Virol 2007, 88:1460-1469. 10.1099/vir.0.82718-0, 17412974.
15. Giorgi C, Franconi R, Rybicki EP. Human papillomavirus vaccines in plants. Expert Rev Vaccines 2010, 9:913-924. 10.1586/erv.10.84, 20673013.
16. Xu YF, Zhang YQ, Xu XM, Song GX. Papillomavirus virus-like particles as vehicles for the delivery of epitopes or genes. Arch Virol 2006, 151:2133-2148. 10.1007/s00705-006-0798-8, 16791442.
17. Nieland JD, Da Silva DM, Velders MP, de Visser KE, Schiller JT, Müller M, Kast WM. Chimeric papillomavirus virus-like particles induce a murine self-antigen-specific protective and therapeutic antitumor immune response. J Cell Biochem 1999, 73:145-152. 10.1002/(SICI)1097-4644(19990501)73:2<145::AID-JCB1>3.0.CO;2-5, 10227378.
18. Slupetzky K, Shafti-Keramat S, Lenz P, Brandt S, Grassauer A, Sara M, Kirnbauer R. Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops. J Gen Virol 2001, 82:2799-2804.
19. Sadeyen JR, Tourne S, Shkreli M, Sizaret PY, Coursaget P. Insertion of a foreign sequence on capsid surface loops of human papillomavirus type 16 virus-like particles reduces their capacity to induce neutralizing antibodies and delineates a conformational neutralizing epitope. Virology 2003, 309:32-40. 10.1016/S0042-6822(02)00134-4, 12726724.
20. Varsani A, Williamson AL, de Villiers D, Becker I, Christensen ND, Rybicki EP. Chimeric human papillomavirus type 16 (HPV-16) L1 particles presenting the common neutralizing epitope for the L2 minor capsid protein of HPV-6 and HPV-16. J Virol 2003, 77:8386-8393. 10.1128/JVI.77.15.8386-8393.2003, 165259, 12857908.
21. Murata Y, Lightfoote PM, Rose RC, Walsh EE. Antigenic presentation of heterologous epitopes engineered into the outer surface-exposed helix 4 loop region of human papillomavirus L1 capsomeres. Virol J 2009, 6:81. 10.1186/1743-422X-6-81, 2702290, 19538743.
22. Paz De la Rosa G, Monroy-García A, Mora-García Mde L, Peña CGR, Hernández-Montes J, Weiss-Steider B, Lim MAG. An HPV 16 L1-based chimeric human papilloma virus-like particles containing a string of epitopes produced in plants is able to elicit humoral and cytotoxic T-cell activity in mice. Virol J 2009, 6:2. 10.1186/1743-422X-6-2, 2639544, 19126233.
23. Lenzi P, Scotti N, Alagna F, Tornesello ML, Pompa A, Vitale A, De Stradis A, Monti L, Grillo S, Buonaguro FM, Maliga P, Cardi T. Translational fusion of chloroplast-expressed human papillomavirus type 16 L1 capsid protein enhances antigen accumulation in transplastomic tobacco. Transgenic Res 2008, 17:1091-1102. 10.1007/s11248-008-9186-3, 18491213.
24. Waheed MT, Thönes N, Müller M, Hassan SW, Gottschamel J, Lössl E, Kaul HP, Lössl AG. Plastid expression of a double-pentameric vaccine candidate containing human papillomavirus-16 L1 antigen fused with LTB as adjuvant: transplastomic plants show pleiotropic phenotypes. Plant Biotechnol J 2011, 9:651-660. 10.1111/j.1467-7652.2011.00612.x, 21447051.
25. Waheed MT, Thönes N, Müller M, Hassan SW, Razavi NM, Lössl E, Kaul HP, Lössl AG. Transplastomic expression of a modified human papillomavirus L1 protein leading to the assembly of capsomeres in tobacco: a step towards cost-effective second-generation vaccines. Transgenic Res 2011, 20:271-282. 10.1007/s11248-010-9415-4, 20563641.
26. White WI, Wilson SD, Palmer-Hill FJ, Woods RM, Ghim SJ, Hewitt LA, Goldman DM, Burke SJ, Jenson AB, Koenig S, Suzich JA. Characterization of major neutralizing epitope on human papillomavirus type 16 L1. J Virol 1999, 73:4882-4889. 112531, 10233949.
27. Christensen ND, Cladel NM, Reed CA, Budgeon LR, Embers ME, Skulsky DM, McClements WL, Ludmerer SW, Jansen KU. Hybrid papillomavirus L1 molecules assemble into virus-like particles that reconstitute conformational epitopes and induce neutralizing antibodies to distinct HPV types. Virology 2001, 291:324-334. 10.1006/viro.2001.1220, 11878901.
28. Christensen ND, Dillner J, Eklund C, Carter JJ, Wipf GC, Reed CA, Cladel NM, Galloway DA. Surface conformational and linear epitopes on HPV-16 and HPV-18 L1 virus-like particles as defined by monoclonal antibodies. Virology 1996, 223:174-184. 10.1006/viro.1996.0466, 8806551.
29. Zhou J, Doorbar J, Sun XY, Crawford LV, McLean CS, Frazer IH. Identification of the nuclear localization signal of human papillomavirus type 16 L1 protein. Virology 1991, 185:625-632. 10.1016/0042-6822(91)90533-H, 1660197.
30. Sainsbury F, Thuenemann EC, Lomonossoff GP. pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 2009, 7:682-693. 10.1111/j.1467-7652.2009.00434.x, 19627561.
31. Luisoni E, Milne RG, Vecchiati M. Purification of tomato yellow leaf curl geminivirus. Microbiologica 1995, 18:253-260.
32. Cañizares MC, Nicholson L, Lomonossoff GP. Use of viral vectors for vaccine production in plants. Immunol Cell Biol 2005, 83:263-270. 10.1111/j.1440-1711.2005.01339.x, 15877604.
33. Giritch A, Marillonnet S, Engler C, van Eldik G, Botterman J, Klimyuk V, Gleba Y. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci USA 2006, 103:14701-14706. 10.1073/pnas.0606631103, 1566189, 16973752.
34. Lindbo JA. TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector. Plant Physiol 2007, 145:1232-1240. 10.1104/pp.107.106377, 2151719, 17720752.
35. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 1999, 5:1157-1163. 10.1038/13484, 10502819.
36. Fan J, Liang X, Horton MS, Perry HC, Citron MP, Heidecker GJ, Fu TM, Joyce J, Przysiecki CT, Keller PM, Garsky VM, Ionescu R, Rippeon Y, Shi L, Chastain MA, Condra JH, Davies ME, Liao J, Emini EA, Shiver JW. Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 2004, 22:2993-3003. 10.1016/j.vaccine.2004.02.021, 15297047.
37. Zhao G, Lin Y, Du L, Guan J, Sun S, Sui H, Kou Z, Chan CCS, Guo Y, Jiang S, Zheng BJ, Zhou Y. An M2e-based multiple antigenic peptide vaccine protects mice from lethal challenge with divergent H5N1 influenza viruses. Virol J 2010, 7:9. 10.1186/1743-422X-7-9, 2823673, 20082709.
38. Wang Y, Zhou L, Shi H, Xu H, Yao H, Xi XG, Toyoda T, Wang X, Wang T. Monoclonal antibody recognizing SLLTEVET epitope of M2 protein potently inhibited the replication of influenza A viruses in MDCK cells. Biochem Bioph Res Co 2009, 385:118-122.
39. Roden RB, Armstrong A, Haderer P, Christensen ND, Hubbert NL, Lowy DR, Schiller JT, Kirnbauer R. Characterization of a human papillomavirus type 16 variant-dependent neutralizing epitope. J Virol 1997, 71:6247-6252. 191893, 9223527.
40. Varsani A, Williamson AL, Stewart D, Rybicki EP. Transient expression of Human papillomavirus type 16 L1 protein in Nicotiana benthamiana using an infectious tobamovirus vector. Virus Res 2006, 120:91-96. 10.1016/j.virusres.2006.01.022, 16530873.
41. Thönes N, Herreiner A, Schädlich L, Piuko K, Müller M. A direct comparison of human papillomavirus type 16 L1 particles reveals a lower immunogenicity of capsomeres than viruslike particles with respect to the induced antibody response. J Virol 2008, 82:5472-5485. 10.1128/JVI.02482-07, 2395182, 18385253.
42. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
43. Bates PA, Kelley LA, MacCallum RM, Sternberg MJE. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Protien Struct Funct Genet 2001, (Suppl 5):39-46.