Plant-based vaccines: Novel and low-cost possible route for mediterranean innovative vaccination strategies

Advances in Virus Research

Volumn 89, Issue , 2014, Pages 1-37

  Aboul Ata, Aboul Ata E ^a   Vitti, Antonella ^b   Nuzzaci, Maria ^b   El Attar, Ahmad K ^a   Piazzolla, Giuseppina ^c   Tortorella, Cosimo ^c   Harandi, Ali M ^d   Olson, Olof ^e   Wright, Sandra A ^f   Piazzolla, Pasquale ^b  

^a Agricultural Research Center   (Egypt)

^b UNIVERSITY OF BASILICATA   (Italy)

^c UNIVERSITY OF BARI   (Italy)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e LUND UNIVERSITY   (Sweden)

^f UNIVERSITY OF GÄVLE   (Sweden)

Author keywords

AlMV viral vector; Chimeric virus; CMV viral vector; HCV HVR1 expressed protein; HSV 2 gD and HSV 2 VP16 expressed proteins; Plant based vaccine; TMV viral vector

Indexed keywords

EDIBLE VACCINE; VIRUS VACCINE;

BIOTECHNOLOGY; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; PHARMACEUTICS; PROCEDURES; TRANSGENIC PLANT; VACCINATION;

BIOTECHNOLOGY; HUMANS; PLANTS, GENETICALLY MODIFIED; TECHNOLOGY, PHARMACEUTICAL; VACCINATION; VACCINES, EDIBLE; VIRAL VACCINES;

EID: 84898925463     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800172-1.00001-X     Document Type: Chapter

References (147)

1. Arazi T., Huang P.L., Huang P., Zhang L., Shiboleth Y.M., Gal-On A., et al. Production of antiviral and antitumor proteins MAP30 and GAP31 in cucurbits using the plant virus vector ZYMV-AGII. Biochemical and Biophysical Research Communications 2002, 292:441-448.
2. Baldo V., Baldovin T., Trivello R., Floreani A. Epidemiology of HCV infection. Current Pharmaceutical Design 2008, 14:1646-1654.
3. Bally M., Murgier M., Lazdunski A. Cloning and orientation of the gene encoding aminopeptidase N in Escherichia coli. Molecular and General Genetics: MGG 1984, 195:507-510.
4. Bantel H., Schulze-Osthoff K. Apoptosis in hepatitis C virus infection. Cell Death and Differentiation 2003, 10:S48-S58.
5. Berg T., Mas Marques A., Höhne M., Wiedenmann B., Hopf U., Schreier E. Mutations in the E2-PePHD and NS5A region of hepatitis C virus type 1 and the dynamics of hepatitis C viremia decline during interferon alfa treatment. Hepatology 2000, 32:1386-1395.
6. Bhasin M., Raghava G.P.S. Prediction of CTL epitopes using QM, SVM and ANN techniques. Vaccine 2004, 22:3195-3204.
7. Biet F., Kremer L., Wolowczuk I., Delacre M., Locht C. Immune response induced by recombinant Mycobacterium bovis BCG producing the cholera toxin B subunit. Infection and Immunity 2003, 71:2933-2937.
8. Bol J.F. Alfalfa mosaic virus and ilarviruses: Involvement of coat protein in multiple steps of the replication cycle. Journal of General Virology 1999, 80:1089-1102.
9. Bol J.F., van Vloten-Doting L., Jaspars E.M.A. Functional equivalence of top component a RNA and coat protein in the initiation of infection by alfalfa mosaic virus. Virology 1971, 46:73-85.
10. Brederode F.T., Koper-Zwarthoff E.C., Bol J.F. Complete nucleotide sequence of alfalfa mosaic virus RNA 4. Nucleic Acids Research 1980, 8:2213-2223.
11. Bregenholt S., Wang M., Wolfe M., Bærentzen H., Dyrberg T., Herrathz J.V., et al. The cholera toxin B subunit is a mucosal adjuvant for oral tolerance induction in type 1 diabetes. Scandinavian Journal of Immunology 2003, 57:432-438.
12. Brennan F.R., Gilleland L.B., Staczek J., Bendig M.M., Hamilton W.O., Gilleland H.E. A chimeric plant virus vaccine protects mice against a bacterial infection. Microbiology 1999, 145:2061-2067.
13. Browning D.F., Busby S.J. The regulation of bacterial transcription initiation. Nature Reviews. Microbiology 2004, 2:57-65.
14. Brunak S., Buus S. Identifying cytotoxic T cell epitopes from genomic and proteomic information: "The human MHC project". Reviews in Immunogenetics 2000, 2:477-491.
15. Carrère I., Tepfer M., Jacquemond M. Recombinants of cucumber mosaic virus (CMV): Determinants of host range and symptomatology. Archives of Virology 1999, 144:365-379.
16. Chiou H.L., Hsieh Y.S., Hsieh M.R., Chen T.Y. HCV E2 may induce apoptosis of Huh-7 cells via a mitochondrial-related caspase pathway. Biochemical and Biophysical Research Communications 2006, 345:453-458.
17. Chou A.H., Tsai H.F., Wu Y.Y., Hu C.Y., Hwang L.H., Hsu P.I., et al. Hepatitis C virus core protein modulates TRAIL-mediated apoptosis by enhancing Bid cleavage and activation of mitochondria apoptosis signaling pathway. Journal of Immunology 2005, 174:2160-2166.
18. Creager A.N.A., Scholthof K.-B.J., Citovsky V., Scholthof H.B. Tobacco mosaic virus: Pioneering research for a century. The Plant Cell 1999, 11:301-308.
19. Crescenzi A., Barbarossa L., Cillo F., Di Franco A., Vovlas N., Gallitelli D. Role of cucumber mosaic virus and its satellite RNA in the etiology of tomato fruit necrosis in Italy. Arch. Virol. 1993, 131:321-333.
20. Daniel H., Streatfield S.J., Wyckoff K. Medical molecular farming: Production of antibiotics, biopharmaceuticals and edible vaccines in plants. Trends in Plant Science 2001, 6:219-226.
21. deGraaff M., Man in't Veld M.R., Jaspars E.M. In vitro evidence that the coat protein of alfalfa mosaic virus plays a direct role in the regulation of plus and minus RNA synthesis: Implications for the life cycle of alfalfa mosaic virus. Virology 1995, 208:583-589.
22. Dhama K., Wani M.Y., Deb R., Karthik K., Tiwari R., Barathidasan R., et al. Plant based oral vaccines for human and animal pathogens-A new era of prophylaxis: Current and future perspectives. Journal of Experimental Biology and Agricultural Sciences 2013, 1:1-12.
23. Donson J., Kearney C.M., Hilf M.E., Dawson W.O. Systemic expression of bacterial gene by tobacco mosaic virus-based vector. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:7204-7208.
24. El-Attara A.K., Aboul-Ataa A.E., Mazyada H.M., Harandi A.M., Olsson O. Recombinant-TMV vector for plant-based vaccine induction against HSV-2gD and VP16 subunits. Journal of Virological Methods 2014, submitted in Feb. 2014 [reviewing].
25. El-Attar A.K., Shamloul A.M., Shalaby A.A., Riad B.Y., Saad A., Mazyad H.M., et al. Expression of chimeric HCV peptide in transgenic tobacco plants infected with recombinant alfalfa mosaic virus for development of a plant-derived vaccine against HCV. African Journal of Biotechnology 2004, 11:588-594.
26. El-Sayed Zaki M., Goda H. Relevance of parvovirus B19, herpes simplex virus 2, and cytomegalovirus virologic markers in maternal serum for diagnosis of unexplained recurrent abortions. Archives of Pathology & Laboratory Medicine 2007, 131(6):956-960.
27. El-Zanaty F., Way A. Egypt demographic and health survey 2008 2009, Ministry of Health, Cairo, Egypt.
28. Erny C., Schoumacher F., Jung C., Gagey M.-J., Godeefroy-Colburn T., Stussi-Garaud C., et al. An N-proximal sequence of the alfalfa mosaic virus movement protein is necessary for association with cell walls in transgenic plants. Journal of General Virology 1992, 73:2115-2119.
29. Farci P., Shimoda A., Wong D., Cabezon T., De Gioannis D., Strazzera A., et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:15394-15399.
30. Fernàndez-Fernàndez M.R., Martinez-Torrecuadrada J.L., Casal J.I., Garcia J.A. Development of an antigen presentation system based on plum pox potyvirus. FEBS Letters 1998, 427:229-235.
31. Ferrari C., Valli A., Galati L., Penna A., Scaccaglia P., Giuberti T., et al. T-cell response to structural and nonstructural Hepatitis C virus antigens in persistent and self-limited Hepatitis C virus infections. Hepatology 1994, 19:286-295.
32. Fischer R., Baumert T., Blum H.E. Hepatitis C virus infection and apoptosis. World Journal of Gastroenterology 2007, 13:4865-4872.
33. Fischer R., Stoger E., Schillberg S., Christou P., Twyman R.M. Plant-based production of biopharmaceuticals. Current Opinion in Plant Biology 2004, 7:152-158.
34. Francis M.J. Peptide vaccines for viral diseases. Science Progress 1990, 74:115-130.
35. Fujita T., Ishido S., Muramatsu S., Itoh M., Hotta H. Suppression of actinomycin D-induced apoptosis by the NS3 protein of hepatitis C virus. Biochemical and Biophysical Research Communications 1996, 229:825-831.
36. Gellért A., Salánki K., Náray-Szabó G., Balázs E. Homology modelling and protein structure based functional analysis of five cucumovirus coat proteins. Journal of Molecular Graphics & Modelling 2006, 24:319-327.
37. Goelet P., Lomonossoff G.P., Butler P.J.G., Akam M.E., Gait M.J., Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proceedings of the National Academy of Sciences of the United States of America 1982, 79:5818-5822.
38. Gough K.C., Cockburn W., Whitelam G.C. Selection of phage-display peptides that bind to cucumber mosaic virus coat protein. Journal of Virological Methods 1999, 79:169-180.
39. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modelling. Electrophoresis 1997, 18:2714-2723.
40. Guicciardi M.E., Gores G.J. Apoptosis: A mechanism of acute and chronic liver injury. Gut 2005, 54:1024-1033.
41. Gunn M.R., Symons R.H. Sequence homology at the 3'-termini of the four RNAs of Alfalfa mosaic virus. FEBS Letters 1980, 109:145-150.
42. Han M., Su T., Zu Y.G., An Z.G. Research advances of transgenic plant vaccines. Acta Genetica Sinica 2006, 33:285-293.
43. He X., Liu S., Perry K.L. Identification of epitopes in cucumber mosaic virus using a phage-displayed random peptide library. Journal of General Virology 1998, 79:3145-3153.
44. Henderson A., Propsta K., Kedlc R., Dowa S. Mucosal immunization with liposome-nucleic acid adjuvants generates effective humoral and cellular immunity. Vaccine 2011, 29:5304-5312.
45. Honda M., Kaneko S., Shimazaki T., Matsushita E., Kobayashi K., Ping L.H., et al. Hepatitis C virus core protein induces apoptosis and impairs cell-cycle regulation in stably transformed Chinese hamster ovary cells. Hepatology 2000, 31:1351-1359.
46. Hong-Ge J., Yong-Qi P., Rong-Xiang F. Agroinoculation as a simple way to deliver tobacco mosaic virus-based expression vector. Acta Botanica Sinica 2003, 45(7):770-773.
47. Hooper D.C. Plant vaccines: An immunological perspective. Plant-produced microbial vaccines. Current Topics in Microbiology and Immunology 2009, 332:1-11.
48. Houghton M. Strategies and prospects for vaccination against the hepatitis C virus. Current Topics in Microbiology and Immunology 2000, 242:327-329.
49. Ishii S., Koziel M.J. Immune responses during acute and chronic infection with hepatitis C virus. Clinical Immunology 2008, 128:133-147.
50. Jiskoot W., Kersten G.F.A., Beuvery E.C. Vaccines. Pharmaceutical biotechnology: An introduction for pharmacists and pharmaceutical scientists 2002, 259-281. Taylor & Francis, London. 2nd ed. D.J.A. Crommelin, R.D. Sindelar (Eds.).
51. Joelson T., Akerblom L., Oxelfelt P., Strandberg B., Tomenius K., Morris T.J. Presentation of a foreign peptide on the surface of tomato bushy stunt virus. Journal of General Virology 1997, 78:1213-1217.
52. Johnson J., Lin T., Lomonossoff G. Presentation of heterologous peptides on plant viruses: Genetics, structure and function. Annual Review of Phytopathology 1997, 35:67-86.
53. Joshi S., Pleij C.W.A., Haenni A.L., Chapeville F., Bosch L. The nature of the tobacco mosaic virus intermediate length RNA-2 and its translation. Virology 1983, 127:100-111.
54. Kagale S., Uzuhashi S., Wigness M., Bender T., Yang W., Borhan H., et al. TMV-gate vectors: Gateway compatible tobacco mosaic virus based expression vectors for functional analysis of proteins. Scientific Reports 2012, 2:874.
55. Kaper J.M., Waterworth H.E. Cucumoviruses. Handbook of plant virus infections and comparative diagnosis 1981, 257-332. Elsevier/North-Holland Biomedical Press, Amsterdam. E. Kurstak (Ed.).
56. Konecny R., Trylska J., Tama F., Zhang D., Baker N.A., Brooks C.L., et al. Electrostatic properties of cowpea chlorotic mottle virus and cucumber mosaic virus capsids. Biopolymers 2006, 82:106-120.
57. Koo M., Bendahmane M., Lettieri G.A., Paoletti A.D., Lane T.E., Fitchen J.H., et al. Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carries an MHV epitope. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:7774-7779.
58. Kountouras J., Zavos C., Chatzopoulos D. Apoptosis in hepatitis C. Journal of Viral Hepatitis 2003, 10:335-342.
59. Kumar S., Ganapathi T.R., Bapat V.A. Production of hepatitis B surface antigen in recombinant plant systems: An update. Biotechnology Progress 2007, 23:532-539.
60. Langereis K., Mugnier M.-A., Cornelissen B.J.C., Pink L., Bol J.F. Variable repeats and poly (A)-stretches in the leader sequence of Alfalfa mosaic virus RNA 3. Virology 1986, 154:409-414.
61. Larsen J.E.P., Lund O., Nielsen M. Improved method for predicting linear B-cell epitopes. Immunome Research 2006, 2:2.
62. Lechmann M., Ihlenfeldt H.G., Braunschweiger I., Giers G., Jung G., Matz B., et al. T- and B-cell responses to different hepatitis C virus antigens in patients with chronic hepatitis C infection and in healthy anti-hepatitis C virus-positive blood donors without viremia. Hepatology 1996, 24:790-795.
63. Lechmann M., Liang T.J. Vaccine development for hepatitis C. Seminars in Liver Disease 2000, 20:211-226.
64. Lechner F., Gruener N.H., Urbani S., Uggeri J., Santantonio T., Kammer A.R. CD8+ T lymphocyte responses are induced during acute hepatitis C virus infection but are not sustained. European Journal of Immunology 2000, 30:2479-2487.
65. Lechner S., Rispeter K., Meisel H., Kraas W., Jung G., Roggendorf M., et al. Antibodies directed to envelope proteins of hepatitis C virus outside of hypervariable region 1. Virology 1998, 243:313-321.
66. Lechner F., Wong D., Dunbar P., Chapman R., Chung R., Dohrenwend P., et al. Analysis of a successful immune response in persons infected with hepatitis C virus. Journal of Experimental Medicine 2000, 191:1499-1512.
67. Lee S.H., Kim Y.K., Kim C.S., Seol S.K., Kim J., Cho S., et al. E2 of hepatitis C virus inhibits apoptosis. Journal of Immunology 2005, 175:8226-8235.
68. Leroux-Roels G., Esquivel C.A., DeLeys R., Stuyver L., Elewaut A., Philippe J., et al. Lymphoproliferative responses to hepatitis C virus core, E1, E2, and NS3 in patients with chronic hepatitis C infection treated with interferon α. Hepatology 1996, 23:8-16.
69. Lico C., Chen Q., Santi L. Viral vectors for production of recombinant proteins in plants. Journal of Cellular Physiology 2008, 216:366-377.
70. Lico C., Santi L., Twyman R.M., Pezzotti M., Avesani L. The use of plants for the production of therapeutic human peptides. Plant Cell Reports 2012, 31:439-451.
71. Liljeqvist S., Stahl S., Andreoni C., Binz H., Uhlen M., Murby M. Fusions to the cholera toxin B subunit: Influence on pentamerization and GM1 binding. Journal of Immunological Methods 1997, 210:125-135.
72. Lot H., Marrou J., Quiot J.B., Esvan C. Contribution 'a l'D́etude du virus de la mosaique du concombre (CMV). I. Methode de purification rapide du virus. Annals of Phytopathology 1972, 14:25-38.
73. Mahmoud Y.A., Mumtaz G.R., Riome S., Miller D., Abu-Raddad L.J. The epidemiology of hepatitis C virus in Egypt: A systematic review and data synthesis. BMC Infectious Diseases 2013, 13:288-329.
74. Major M.E., Mihalik K., Fernandez J., Seidman J., Kleiner D., Kolykhalov A.A., et al. Long-term follow-up of chimpanzees inoculated with the first infectious clone for hepatitis C virus. Journal of Virology 1999, 73(4):3317-3325.
75. Mani A., Gelmann E.P. The ubiquitin-proteasome pathway and its role in cancer. Journal of Clinical Oncology 2005, 23:4776-4789.
76. Manns M.P., McHutchinson J.C., Gordon S.C., Rustgi V.K., Shiffman M.L., Reindollar R., et al. Peginterferonα-2b plus ribavirin compared with interferon α-2b plus ribavirin for initial treatment of chronic hepatitis C: A randomised trial. Lancet 2001, 358:958-965.
77. Marusic C., Rizza P., Lattanzi L., Mancini C., Spada M., Belardelli F., et al. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. Journal of Virology 2001, 75:8434-8439.
78. Mason H.S., Lam D.M., Harntzen C.J. Expression of hepatitis B surface antigen in transgenic plants. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:11745-11749.
79. McLain L., Durrani Z., Wisniewski L.A., Porta C., Lomonossoff G.P., Dimmock N.J. Stimulation of neutralizing antibodies to human immunodeficiency virus type 1 in three strains of mice immunized with a 22 amino acid peptide of gp41 expressed on the surface of a plant virus. Vaccine 1996, 14:799-810.
80. McLain L., Porta C., Lomonossoff G.P., Durrani Z., Dimmock N.J. Human immunodeficiency virus type 1 neutralizing antibodies raised to a gp41 peptide expressed on the surface of a plant virus. AIDS Research and Human Retroviruses 1995, 11:327-334.
81. Mekalanos J.J., Swartz D.J., Pearson G.D., Harford N., Groyne F., deWilde M. Cholera toxin genes: Nucleotide sequence, deletion analysis and vaccine development. Nature 1983, 306:551-557.
82. Memon M.L., Memon M.A. Hepatitis C: An epidemiological review. Journal of Viral Hepatology 2002, 9:84-100.
83. Missale G., Bertoni R., Lamonaca V., Valli A., Massari M., Mori C., et al. Different clinical behaviours of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. Journal of Clinical Investigation 1996, 98:706-714.
84. Natilla A., Piazzolla G., Nuzzaci M., Saldarelli P., Tortorella C., Antonaci S., et al. Cucumber mosaic virus as carrier of a Hepatitis C viru-derived epitope. Archives of Virology 2004, 149:137-154.
85. Neeleman L., van der Kuyl A.C., Bol J.F. Role of alfalfa mosaic virus coat protein gene in symptom formation. Virology 1991, 181:687-693.
86. Nemchinov L.G., Liang T.J., Rifaat M.M., Mazyad H.M., Hadidi A., Keith J.M. Development of a plant-derived subunit vaccine candidate against hepatitis C virus. Archives of Virology 2000, 145:2557-2573.
87. Nicholas B.L., Brennan F.R., Martinez-Torrecuadrada J.L., Casal J.I., Hamilton W.D., Wakeln D. Characterization of the immune response to canine parvovirus induced by vaccination with chimeric plant viruses. Vaccine 2002, 20:2727-2734.
88. Nomura-Takigawa Y., Nagano-Fujii M., Deng L., Kitazawa S., Ishido S., Sada K., et al. Non-structural protein 4A of hepatitis C virus accumulates on mitochondria and renders the cells prone to undergoing mitochondria-mediated apoptosis. Journal of General Virology 2006, 87:1935-1945.
89. Nuzzaci M., Bochicchio I., De Stradis A., Vitti A., Natilla A., Piazzolla P., et al. Structural and biological properties of Cucumber mosaic virus particles carrying hepatitis C virus-derived epitopes. Journal of Virological Methods 2009, 155:118-121.
90. Nuzzaci M., Piazzolla G., Vitti A., Lapelosa M., Tortorella C., Stella I., et al. Cucumber mosaic virus as a presentation system for a double hepatitis C virus-derived epitope. Archives of Virology 2007, 152:915-928.
91. Nuzzaci M., Vitti A., Condelli V., Lanorte M.T., Tortorella C., Boscia D., et al. In vitro stability of Cucumber mosaic virus nanoparticles carrying a Hepatitis C virus-derived epitope under simulated gastrointestinal conditions and in vivo efficacy of an edible vaccine. Journal of Virological Methods 2010, 165:211-215.
92. Pacios L.F., Garcia-Arenal F. Comparison of properties of particles of Cucumber mosaic virus and Tomato aspermy virus based on the analysis of molecular surfaces of capsids. Journal of General Virology 2006, 87:2073-2083.
93. Palukaitis P., Zaitlin M. Tobacco mosaic virus: Infectivity and replication. Plant viruses. Vol. 2. The rod-shaped plant viruses 1986, 105-131. Plenum Press, New York. M.H.V. Van Regenmortel, H. Fraenkel-Conrat (Eds.).
94. Pavio N., Lai M.M.C. The hepatitis C virus persistence: How to evade the immune system?. Journal of Biosciences 2003, 28:287-304.
95. Pelham H.R.B. Leaky UAG termination codon in tobacco mosaic virus RNA. Nature 1978, 272:469-471.
96. Perry K.L., Zhang L., Shintaku M.H., Palukaitis P. Mapping determinants in cucumber mosaic virus for transmission by Aphis gossypii. Virology 1994, 205:591-595.
97. Piazzolla G., Nuzzaci M., Tortorella C., Panella E., Natilla A., Boscia D., et al. Immunogenic properties of a chimeric plant virus expressing a hepatitis C virus (HCV)-derived epitope: New prospects for an HCV vaccine. Journal of Clinical Immunology 2005, 25:142-152.
98. Piazzolla G., Nuzzaci M., Vitti A., Napoli N., Schiavone M., Piazzolla P., et al. Apoptotic effects of a chimeric plant virus carrying a mimotope of the Hepatitis C virus hypervariable region 1: Role of caspases and endoplasmic reticulum-stress. Journal of Clinical Immunology 2012, 32:866-876.
99. Pnieweski T. The twenty-year story of a plant-based vaccine against hepatitis B: Stagnation or promising prospects?. International Journal of Molecular Sciences 2013, 14:1978-1998.
100. Porta C., Lomonossoff G. Viruses as vectors for expression of foreign sequences in plants. Biotechnology and Genetic Engineering Reviews 2002, 19:245-292.
101. Porta C., Spall V.E., Loveland J., Johnson J.E., Barker P.J. Development of cowpea mosaic virus as a high-yielding system for the presentation of foreign peptides. Virology 1994, 202:949-955.
102. Puntoriero G., Meola A., Lahm A., Zucchelli S., Ercole B.B., Tafi R., et al. Towards a solution for hepatitis C virus hypervariability: Mimotopes of the hypervariable region 1 can induce antibodies cross-reacting with a large number of viral variants. EMBO Journal 1998, 17:3521-3533.
103. Rehermann B., Chisari F.V. Cell mediated immune response to the hepatitis C virus. Current Topics in Microbiology and Immunology 2000, 242:299-325.
104. Rehermann B., Nascimbeni M. Immunology of Hepatitis B virus and Hepatitis C virus infection. Nature Reviews Immunology 2005, 5(3):215-229.
105. Reusken C.B., Neeleman L., Brederode F.T., Bol J.F. Mutations in coat protein binding sites of alfalfa mosaic virus RNA 3 affect subgenomic RNA 4 accumulation and encapsidation of viral RNAs. Journal of Virology 1997, 71:8385-8391.
106. Robertson B., Myers G., Howard C., Brettin T., Bukh J., Gaschen B., et al. Classification, nomenclature and database development for hepatitis C virus (HCV) and related viruses: Proposals for standardization. International Committee on Virus Taxonomy. Archives of Virology 1998, 143:2493-2503.
107. Roggero P., Ciuffo M., Benvenuto E., Franconi R. The expression of a single-chain Fv antibody fragment in different plant hosts and tissues by using potato virus X as a vector. Protein Expression and Purification 2001, 22:70-74.
108. Rosenberg S. Recent advances in the molecular biology of hepatitis C virus. Journal of Molecular Biology 2001, 313:451-464.
109. Rust C., Gores G.J. Apoptosis and liver disease. American Journal of Medicine 2000, 108:567-574.
110. Saha S., Raghava G.P.S. BcePred: Prediction of continuous B-cell epitopes in antigenic sequences using physico-chemical properties. ICARIS 2004, LNCS 3239 2004, 197-204. Springer, Berlin. G. Nicosia, V. Cutello, P.J. Bentley, J. Timis (Eds.).
111. Saha S., Raghava G.P.S. Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins: Structure, Function, and Bioinformatics 2006, 65:40-48.
112. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning: A laboratory manual 1989, Cold Spring Harbor Laboratory Press, New York. 2nd ed.
113. Sanchez A.E., Aquino G., Ostoa-Saloma P., Laclette J.P., Rocha-Zavaleta L. Cholera toxin B-subunit gene enhances mucosal immunoglobulin A, Th1-type, and CD8 cytotoxic responses when coadministered intradermally with a DNA vaccine. Clinical and Diagnostic Laboratory Immunology 2004, 11(4):711-719.
114. Sanchez J., Johansson S., Lowenadler B., Svennerholm A.M., Holmgren J. Recombinant cholera toxin B subunit and gene fusion proteins for oral vaccination. Research in Microbiology 1990, 141:971-979.
115. Savelyeva N., Munday R., Spellerberg M.B., Lomonossoff G.P., Stevenson F.K. Plant viral genes in DNA idiotypic vaccines activate linked CD4+ T-cell mediated immunity against B-cell malignancies. Nature Biotechnology 2001, 19:760-764.
116. Scholthof K.-B.G. Tobacco mosaic virus: A model system for plant biology. Annual Review of Phytopathology 2004, 42:13-34.
117. Schouten A., Roosien J., van Engelen F.A., de Jong G.A., Borst-Vrenssen A.W., Zilverentant J.F., et al. The C-terminal KDEL sequence increases the expression level of a single-chain antibody designed to be targeted to both the cytosol and the secretory pathway in transgenic tobacco. Plant Molecular Biology 1996, 30:781-793.
118. Shimizu Y.K., Igarashi H., Kiyohara T., Cabezon T., Farci P., Purcell R.H., et al. A hyperimmune serum against a synthetic peptide corresponding to the hypervariable region 1 of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996, 223:409-412.
119. Shivprasad S., Pogue G.P., Lewandowski D.J., Hidalgo J., Donson J., Grill L.K., et al. Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. Virology 1999, 255:312-323.
120. Siavoshian S., Abraham J.D., Thumann C., Kieny M.P., Schuster C. Hepatitis C virus core, NS3, NS5A, NS5B proteins induce apoptosis in mature dendritic cells. Journal of Medical Virology 2005, 75:402-411.
121. Siler C.A., McGettigan J.P., Dietzschold B., Herrine S.K., Dubuisson J., Pomerantz R.J., et al. Live and killed rhabdovirus-based vectors as potential hepatitis C vaccines. Virology 2002, 292:24-34.
122. Smith T.J., Chase E., Schmidt T., Perry K.L. The structure of cucumber mosaic virus and comparison to cowpea chlorotic mottle virus. Journal of Virology 2000, 74:7578-7686.
123. Sweredoski M.J., Baldi P. Cobepro: A novel system for predicting continuous B-cell epitopes. Protein Engineering, Design & Selection: PEDS 2008, 22(3):113-120.
124. Tacket C.O., Mason H.S. A review of oral vaccination with transgenic vegetables. Microbes and Infection 1999, 1:777-783.
125. Tacket C.O., Sztein M.B., Losonsky G.A., Wasserman S.S., Estes M.K. Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clinical Immunology 2003, 108:241-247.
126. Takaki A., Wiese M., Maertens G., Depla E., Seifert U., Liebetrau A. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nature Medicine 2000, 6:578-582.
127. Tengvall S., Josefsson A., Holmgren J., Harandi A.M. CpGoxynucleotideoligode augments HSV-2 glycoprotein D DNA vaccine efficacy to generate T helper 1 response and subsequent protection against primary genital herpes infection in mice. Journal of Reproductive Immunology 2005, 68:53-69.
128. Tenllado F., Bol J.F. Genetic detection of the multiple functions of Alfalfa mosaic virus coat protein in viral RNA replication, encapsidation, and movement. Virology 2000, 268:29-40.
129. Thanavala Y., Mahoney M., Pal S., Scott A., Richter L., Natarajan N., et al. Immunogenicity in humans of an edible vaccine for hepatitis B. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3378-3382.
130. Tiwari S., Verma P.C., Singh P.K., Tuli R. Plants as bioreactors for the production of vaccine antigens. Biotechnology Advances 2009, 27:449-467.
131. Turpen T.H., Reini S.J., Charoenvit Y., Hoffman S.L., Fallarme V., Grill L.K. Malarial epitopes expressed on the surface of recombinant tobacco mosaic virus. Biotechnology (NY) 1995, 13:53-57.
132. Tyulkina L.G., Skurat E.V., Frolova O.Yu., Komarova T.V., Karger E.M., Atabekov I.G. New viral vector for superproduction of epitopes of vaccine proteins in plants. Acta Nature 2011, 3(4):73-82.
133. van der Kuyl A.C., Neeleman L., Bol J.F. Role of alfalfa mosaic virus coat protein in regulation of the balance between viral plus and minus strand RNA synthesis. Virology 1991, 185:496-499.
134. van der Vossen E.A.G., Neeleman L., Bol J.F. Early and late functions of Alfalfa mosaic virus coat protein can be mutated separately. Virology 1994, 202:891-903.
135. Vitti A., Nuzzaci M., Condelli V., Piazzolla P. Protocol of simulated digestion for testing the stability of edible vaccine, Cucumber mosaic virus (CMV) chimeric particle display Hepatitis C virus (HCV) peptide. Virus hybrids as nanomaterials: Methods and protocols. Series: Methods in molecular biology: Vol. 1108 2013, 41-56. Springer Science+Business Media 2014, New York, Chapter 3. L. Baochuan, R. Banahalli (Eds.).
136. Vitti A., Piazzolla G., Condelli V., Nuzzaci M., Lanorte M.T., Boscia D., et al. Cucumber mosaic virus as the expression system for a potential vaccine against Alzheimer's disease. Journal of Virological Methods 2010, 69:332-340.
137. Watanabe Y., Emori Y., Ooshika I., Meshi T., Ohno T., Okada Y. Synthesis of TMV-specific RNAs and proteins at the early stage of infection in tobacco protoplasts: Transient expression of the 30K protein and its RNA. Virology 1984, 133:18-24.
138. Webster D.E., Thomas D.E., Strugnell R.A., Dry I.B., Wesselingh S.L. Appetizing solutions: An edible vaccine for measles. Medical Journal of Australia 2002, 176:434-437.
139. Wikoff W.R., Tsai C.J., Wang G., Baker T.S., Johnson J.E. The structure of cucumber mosaic virus: Cryoelectron microscopy, X-ray crystallography, and sequence analysis. Virology 1997, 232:91-97.
140. Yang S.H., Lee C.G., Lee C.W., Choi E.J., Yoon S.K., Ahn K.S., et al. Hepatitis C virus core inhibits the Fas-mediated p38 mitogen activated kinase signalling pathway in hepatocytes. Molecules and Cells 2002, 13:452-462.
141. Yerly D., Heckerman D., Allen T.M., Chisholm J.V., Faircloth K., Linde C.H., et al. Increased cytotoxic T-lymphocyte epitope variant cross-recognition and functional avidity are associated with hepatitis C virus clearance. Journal of Virology 2008, 82:3147-3153.
142. Yusibov V., Hoopera D.C., Spitsina S.V., Fleysha N., Keana R.B., Mikheevaa T., et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 2002, 20:3155-3164.
143. Yusibov V., Loesch-Fries L.S. N-terminal basic amino acids of alfalfa mosaic virus coat protein involved in the initiation of infection. Virology 1995, 208:405-407.
144. Yusibov V., Loesch-Fries L.S. Functional significance of three basic N-terminal amino acids of alfalfa mosaic virus coat protein. Virology 1998, 242:1-5.
145. Yusibov V., Modelska A., Steplewski K., Agadjanyan M., Weiner D., Craig Hooper D.C., et al. Antigens produced in plants by infection with chimeric plant viruses immunize against rabies virus and HIV-1. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:5784-5788.
146. Yusibov V., Rabindran S. Recent progress of development of plant-derived vaccines. Expert Review of Vaccines 2008, 7(8):1173-1183.
147. Zhu N., Ware C.F., Lai M.M. Hepatitis C virus core protein enhances FADD-mediated apoptosis and suppresses TRADD signalling of tumor necrosis factor receptor. Virology 2001, 283:178-187.