Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Recent Studies of Edible Plant Vaccine for Prophylactic Medicine against Virus-mediated Diseases

바이러스 질병 예방을 위한 식물 경구 백신 연구 동향

  • 한범수 (농업생명공학연구원 신기능소재개발팀) ;
  • 박종석 (농업생명공학연구원 신기능소재개발팀) ;
  • 김형국 (농업생명공학연구원 신기능소재개발팀) ;
  • 하선화 (농업생명공학연구원 신기능소재개발팀) ;
  • 조강진 (농업생명공학연구원 신기능소재개발팀) ;
  • 김용환 (농업생명공학연구원 신기능소재개발팀) ;
  • 김종범 (농업생명공학연구원 신기능소재개발팀)
  • Published : 2004.06.01
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Abstract

Transgenic plants have been studied as delivery system for edible vaccine against various diseases. Edible plant vaccines have several potential advantages as follows: an inexpensive source of antigen, easy administration, reduced need for medical personnel, economical to mass produce and easy transport, heat-stable vaccine without refrigerator, generation of systemic and mucosal immunity and safe antigen without fetal animal-virus contaminants. The amount of recombinant antigens in transgenic plants ranged from 0.002 to 0.8％ in total soluble protein, depending on promoters for the expression of interested genes and plants to be used for transformation. Throughout the last decade, edible plant vaccine made notable progresses that protect from challenges against virus or bacteria. However edible plant vaccines have still problems that could be solved. First, the strong promoter or inducible promoter or strategy of protein targeting could be solved to improve the low expression of antigens in transgenic plants. Second, the transformation technique of target plant should be developed to be able to eat uncooked. Third, marker-free vector could be constructed to be more safety. In this review we describe advances of edible plant vaccines, focusing on the yields depending on plants/promoters employed and the results of animal/clinical trials, and consider further research for the development of a new plant-derived vaccine.

Keywords

References

  1. Arntzen CJ (1998) Pharmaceutical foodstuffs-oral immunization with transgenic plants. Nat Med 4: 502-503 https://doi.org/10.1038/nm0598supp-502
  2. Avendano P, Matson DO, Long J, Whitney S, Matson CC, Pickering LK (1993) Costs associated with office visits for diarrhea in infants and toddlers. Pediatr Infect Dis J 12: 897-902 https://doi.org/10.1097/00006454-199311000-00001
  3. Barrett T, Rossiter PB (1999) Rinderpest: the disease and its impact on humans and animals. Adv Virus Res 53: 89-110 https://doi.org/10.1016/S0065-3527(08)60344-9
  4. Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Muller M (2003) Production of human papillomavirus type 16 virus-like particles in transgenic plants. J Virol 77: 9211-9220 https://doi.org/10.1128/JVI.77.17.9211-9220.2003
  5. Bouche FB, Marquet-Blouin E, Yanagi Y, Steinmetz A, Muller CP (2003) Neutralising immunogenicity of a polyepitope antigen expressed in a transgenic food plant: a novel antigen to protect against measles. Vaccine 21: 2065-2072 https://doi.org/10.1016/S0264-410X(02)00747-8
  6. Carrillo C, Wigdorovitz A, Oliveros JC, Zamorano PI, Sadir AM, Gomez N, Salinas J, Escribano JM, Borca MV (1998) Protective immune response to foot-and-mouth disease virus with VP1 expressed in transgenic plants. J Virol 72: 1688-1690
  7. Carrillo C, Wigdorovitz A, Trono K, Dus Santos MJ, Castanon S, Sadir AM, Ordas R, Escribano JM, Borca MV (2001) Induction of a virus-specific antibody response to foot and mouth disease virus using the structural protein VP1 expressed in transgenic potato plants. Viral Immunol 14: 49-57 https://doi.org/10.1089/08828240151061383
  8. Castanon S, Martin-alonso JM, Martin MS, Boga JA, Alonso P, Parra F, Ordas RJ (2002) The effect of the promoter on expression of VP 60 gene from rabbit hemorrhagic disease virus in potato plants. Plant Sci 162: 87-95 https://doi.org/10.1016/S0168-9452(01)00535-0
  9. Castanon S, Marin MS, Martin-Alonso JM, Boga JA, Casais R, Humara JM, Ordas RJ, Parra F (1999) Immunization with potato plants expressing VP60 protein protects against rabbit hemorrhagic disease virus. J Virol 73: 4452-4455
  10. Chikwamba R, Cunnick J, Hathaway D, McMurray J, Mason H, Wang K (2002) A functional antigen in a practical crop: LT-B producing maize protects mice against Escherichia coli heat labile enterotoxin (LT) and cholera toxin (CT). Transgenic Res 11: 479-493 https://doi.org/10.1023/A:1020393426750
  11. Davies G (2002) Foot and mouth disease. Res Vet Sci 73: 195-199 https://doi.org/10.1016/S0034-5288(02)00105-4
  12. Fotisch K, Vieths S (2001) N- and O-linked oligosaccharides of allergenic glycoproteins. Glycoconj J 18: 373-390 https://doi.org/10.1023/A:1014860030380
  13. Gao Y, Ma Y, Li M, Cheng T, Li SW, Zhang J, Xia NS (2003) Oral immunization of animals with transgenic cherry tomatillo expressing HBsAg. World J Gastroenterol 9: 996-1002 https://doi.org/10.3748/wjg.v9.i5.996
  14. Gil F, Brun A, Wigdorovitz A, Catala R, Martinez-Torrecuadrada JL, Casal I, Salinas J, Borca MV, Escribano JM (2001) High-yield expression of a viral peptide vaccine in transgenic plants. FEBS Lett 488: 13-17 https://doi.org/10.1016/S0014-5793(00)02405-4
  15. Gomez N, Carrillo C, Salinas J, Parra F, Borca MV, Escribano JM (1998) Expression of immunogenic glycoprotein S polypeptides from transmissible gastroenteritis coronavirus in transgenic plants. Virology 249: 352-358 https://doi.org/10.1006/viro.1998.9315
  16. Gomez N, Wigdorovitz A, Castanon S, Gil F, Ordas R, Borca MV, Escribano JM (2000) Oral immunogenicity of the plant derived spike protein from swine-transmissible gastroenteritis coronavirus. Arch Virol 145: 1725-1732 https://doi.org/10.1007/s007050070087
  17. Hajdukiewicz PT, Gilbertson L, Staub JM (2001) Multiple pathways for Cre/lox-mediated recombination in plastids. Plant J 27: 161-170 https://doi.org/10.1046/j.1365-313x.2001.01067.x
  18. Haq TA, Mason HS, Clements JD, Arntzen CJ (1995) Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 268: 714-715 https://doi.org/10.1126/science.7732379
  19. Hein MB, Yeo TC, Wang F, Sturtevant A (1996) Expression of cholera toxin subunits in plants. Ann N Y Acad Sci 792: 50-56 https://doi.org/10.1111/j.1749-6632.1996.tb32490.x
  20. Huang Z, Dry I, Webster D, Strugnell R, Wesselingh S (2001) Plant-derived measles virus hemagglutinin protein induces neutralizing antibodies in mice. Vaccine 19: 2163-2171 https://doi.org/10.1016/S0264-410X(00)00390-X
  21. Jackson AC (2002) Update on rabies. Curr Opin Neurol 15: 327-331 https://doi.org/10.1097/00019052-200206000-00017
  22. Kao JH, Chen DS (2002) Global control of hepatitis B virus infection. Lancet Infect Dis 2: 395-403 https://doi.org/10.1016/S1473-3099(02)00315-8
  23. Kapikian AZ, Estes MK, Chanock RM (1996) Norwalk group of viruses. In Fields Virology, eds. Fields BN, Knipe, DM, Howley PM, Chanock RM, Melnick JL, Monath TP, Roizman B, Straus SE (Raven, New York): 783-810
  24. Kapusta J, Modelska A, Figlerowicz M, Pniewski T, Letellier M, Lisowa O, Yusibov V, Koprowski H, Plucienniczak A, Legocki AB (1999) A plant-derived edible vaccine against hepatitis B virus. FASEB J 13: 1796-1799 https://doi.org/10.1096/fasebj.13.13.1796
  25. Khandelwal A, Sita G L, Shaila MS (2003) Expression of hemagglutinin protein of rinderpest virus in transgenic tobacco and immunogenicity of plant-derived protein in a mouse model. Virology 308: 207-215 https://doi.org/10.1016/S0042-6822(03)00010-2
  26. Kim HS, Jeon JH, Kim CJ, Joung H (2002) Introduction of hog cholera virus gene into potato plants by Agrobacterium- mediated transformation and the analysis of its expression. J Plant Biotechnol 4: 155-161
  27. Kong Q, Richter L, Yang YF, Arntzen CJ, Mason HS, Thanavala Y (2001) Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci USA 98: 11539-11544 https://doi.org/10.1073/pnas.191617598
  28. Lee YS, Hwang CH (2002) Development of transgenic carrot oral vaccine to project against diarrhea of piglets. Korean J Plant Biotechnol 29: 287-293 https://doi.org/10.5010/JPB.2002.29.4.287
  29. Lerouge P, Bardor M, Pagny S, Gomord V, Faye L (2000) N-glycosylation of recombinant pharmaceutical glycoproteins produced in transgenic plants: towards an humanisation of plant N-glycans. Curr Pharm Biotechnol 1: 347-354 https://doi.org/10.2174/1389201003378843
  30. Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Laine AC, Gomord V, Faye L (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38: 31-48 https://doi.org/10.1023/A:1006012005654
  31. Liu SJ, Xue HP, Pu BQ, Quian NH (1984) A new viral disease in rabbits. Anim Hubs Vet Med 16: 253-255
  32. Loeffler F, Frosch P (1897) Summarischer bericht/uber der ergebnisse der untersuchungen zur erforschung der maul-und klauenseuche. Zentralblatt Bakt Abt Orig 22: 257-259
  33. Ma Y, Lin SQ, Gao Y, Li M, Luo WX, Zhang J, Xia NS (2003) Expression of ORF2 partial gene of hepatitis E virus in tomatoes and immunoactivity of expression products. World J Gastroenterol 9: 2211-2215 https://doi.org/10.3748/wjg.v9.i10.2211
  34. Mackie PL (2003) The classification of viruses infecting the respiratory tract. Paediatr Respir Rev 4: 84-90 https://doi.org/10.1016/S1526-0542(03)00031-9
  35. Markowitz LE, Preblud SR, Fine PE, Orenstein WA (1990) Duration of live measles vaccine-induced immunity. Pediatr Infect Dis J 9: 101-110 https://doi.org/10.1097/00006454-199002000-00008
  36. Marquet-Blouin E, Bouche FB, Steinmetz A, Muller CP (2003) Neutralizing immunogenicity of transgenic carrot (Daucus carota L.)-derived measles virus hemagglutinin. Plant Mol Biol 51: 459-469 https://doi.org/10.1023/A:1022354322226
  37. Martin-Alonso JM, Castanon S, Alonso P, Parra F, Ordas R (2003) Oral immunization using tuber extracts from transgenic potato plants expressing rabbit hemorrhagic disease virus capsid protein. Transgenic Res 12: 127-130 https://doi.org/10.1023/A:1022112717331
  38. Mason HS, Ball JM, Shi JJ, Jiang X, Estes MK, Arntzen CJ (1996) Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc Natl Acad Sci USA 93: 5335-5340 https://doi.org/10.1073/pnas.93.11.5335
  39. Mason HS, Lam DM, Arntzen CJ (1992) Expression of hepatitis B surface antigen in transgenic plants. Proc Natl Acad Sci USA 89: 11745-11749 https://doi.org/10.1073/pnas.89.24.11745
  40. Mason PW, Grubman MJ, Baxt B (2003) Molecular basis of pathogenesis of FMDV. Virus Res 91: 9-32 https://doi.org/10.1016/S0168-1702(02)00257-5
  41. Matsumura T, Itchoda N, Tsunemitsu H (2002) Production of immunogenic VP6 protein of bovine group A rotavirus in transgenic potato plants. Arch Virol 147: 1263-1270 https://doi.org/10.1007/s00705-002-0808-4
  42. Modelska A, Dietzschold B, Sleysh N, Fu ZF, Steplewski K, Hooper DC, Koprowski H, Yusibov V (1998) Immunization against rabies with plant-derived antigen. Proc Natl Acad Sci USA 95: 2481-2485 https://doi.org/10.1073/pnas.95.5.2481
  43. Pan American Health Organization (2000) Global measles efforts. In: EPI newsletter. 22: 5
  44. Parra F, Boga JA, Marin MS, Casais R (1993) The amino terminal sequence of VP60 from rabbit hemorrhagic disease virus supports its putative subgenomic origin. Virus Res 27: 219-228 https://doi.org/10.1016/0168-1702(93)90034-K
  45. Richter LJ, Thanavala Y, Arntzen CJ, Mason HS (2000) Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol 18: 1167-1171 https://doi.org/10.1038/81153
  46. Ribeiro RM, Lo A, Perelson AS (2002) Dynamics of hepatitis B virus infection. Microbes Infect 4: 829-835 https://doi.org/10.1016/S1286-4579(02)01603-9
  47. Sagi L, Panis B, Remy S, Schoofs H, De Smet K, Swennen R, Cammue BP (1995) Genetic transformation of banana and plantain (Musa spp.) via particle bombardment. Biotechnology (NY) 13: 481-485 https://doi.org/10.1038/nbt0595-481
  48. Sandhu JS, Krasnyanski SF, Domier LL, Korban SS, Osadjan MD, Buetow DE (2000) Oral immunization of mice with transgenic tomato fruit expressing respiratory syncytial virus-F protein induces a systemic immune response. Transgenic Res 9: 127-135 https://doi.org/10.1023/A:1008979525909
  49. Sandhu JS, Osadjan MD, Krasnyanski SF, Domier LL, Korban, SS, Buetow DE (1999) Enhanced expression of the humn respiratory syncytial virus-F gene in apple leaf protoplasts. Plant Cell Rep 18: 394-397 https://doi.org/10.1007/s002990050592
  50. Satyavathi VV, Prasad V, Khandelwal A, Shaila MS, Sita GL (2003) Expression of hemagglutinin protein of Rinderpest virus in transgenic pigeon pea [Cajanus cajan (L.) Millsp.] plants. Plant Cell Rep 21: 651-658
  51. Smith ML, Richter L, Arntzen CJ, Shuler ML, Mason HS (2003) Structural characterization of plant-derived hepatitis B surface antigen employed in oral immunization studies. Vaccine 21: 4011-4021 https://doi.org/10.1016/S0264-410X(03)00268-8
  52. Sojikul P, Buehner N, Mason HS (2003) A plant signal peptide-hepatitis B surface antigen fusion protein with enhanced stability and immunogenicity expressed in plant cells. Proc Natl Acad Sci USA 100: 2209-2214 https://doi.org/10.1073/pnas.0438037100
  53. Tacket CO, Mason HS, Losonsky G, Clements JD, Levine MM, Arntzen CJ (1998) Immunogenicity in humans of a recombinant bacterial antigen delivered in a transgenic potato. Nat Med 4: 607-609 https://doi.org/10.1038/nm0598-607
  54. Tacket CO, Mason HS, Losonsky G, Estes MK, Levine MM, Arntzen CJ (2000) Human immune responses to a novel norwalk virus vaccine delivered in transgenic potatoes. J Infect Dis 182: 302-305 https://doi.org/10.1086/315653
  55. Taraporewala ZF, Patton JT (2004) Nonstructural proteins involved in genome packaging and replication of rotaviruses and other members of the Reoviridae. Virus Res 101: 57-66 https://doi.org/10.1016/j.virusres.2003.12.006
  56. Thanavala Y, Yang YF, Lyons P, Mason HS, Arntzen C (1995) Immunogenicity of transgenic plant-derived hepatitis B surface antigen. Proc Natl Acad Sci USA 92: 3358-3361 https://doi.org/10.1073/pnas.92.8.3358
  57. Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S, Bowe F, Fairweather N, Ytterberg J, van Wijk KJ, Dougan G, Maliga P (2003) Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Res 31: 1174-1179 https://doi.org/10.1093/nar/gkg221
  58. Tuboly T, Yu W, Bailey A, Degrandis S, Du S, Erickson L, Nagy E (2000) Immunogenicity of porcine transmissible gastroenteritis virus spike protein expressed in plants. Vaccine 18: 2023-2028 https://doi.org/10.1016/S0264-410X(99)00525-3
  59. Turpen TH, Reinl SJ, Charoenvit Y, Hoffman SL, Fallarme V, Grill LK (1995) Malarial epitopes expressed on the surface of recombinant tobacco mosaic virus. Biotechnology 13: 53-57 https://doi.org/10.1038/nbt0195-53
  60. Wang XG, Zhang GH, Liu CX, Zhang YH, Xiao CZ, Fang RX (2001) Purified cholera toxin B subunit from transgenic tobacco plants possesses authentic antigenicity. Biotechnol Bioeng 72: 490-494 https://doi.org/10.1002/1097-0290(20010220)72:4<490::AID-BIT1011>3.0.CO;2-0
  61. Warzecha H, Mason HS, Lane C, Tryggvesson A, Rybicki E, Williamson AL, Clements JD, Rose RC (2003) Oral immunogenicity of human papillomavirus-like particles expressed in potato. J Virol 77: 8702-8711 https://doi.org/10.1128/JVI.77.16.8702-8711.2003
  62. Webster DE, Cooney ML, Huang Z, Drew DR, Ramshaw IA, Dry IB, Strugnell RA, Martin JL, Wesselingh SL (2002) Successful boosting of a DNA measles immunization with an oral plant-derived measles virus vaccine. J Virol 76: 7910-7912 https://doi.org/10.1128/JVI.76.15.7910-7912.2002
  63. WHO (2000) Supplementary information on vaccine safety. Genova, World Health Organization (WHO/v&B/00.36)
  64. Wigdorovitz A, Carrillo C, Dus Santos MJ, Trono K, Peralta A, Gomez MC, Rios RD, Franzone PM, Sadir AM, Escribano JM, Borca MV (1999) Induction of a protective antibody response to foot and mouth disease virus in mice following oral or parenteral immunization with alfalfa transgenic plants expressing the viral structural protein VP1. Virology 255: 347-353 https://doi.org/10.1006/viro.1998.9590
  65. Woldehiwet Z (2002) Rabies: recent developments. Res Vet Sci 73: 17-25 https://doi.org/10.1016/S0034-5288(02)00046-2
  66. Wu YZ, Li JT, Mou ZR, Fei L, Ni B, Geng M, Jia ZC, Zhou W, Zou LY, Tang Y (2003) Oral immunization with rotavirus VP7 expressed in transgenic potatoes induced high titers of mucosal neutralizing IgA. Virology 313: 337-342 https://doi.org/10.1016/S0042-6822(03)00280-0
  67. Yusibov V, Hooper DC, Spitsin SV, Fleysh N, Kean RB, Mikheeva T, Deka D, Karasev A, Cox S, Randall J, Koprowski H (2002) Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 20: 3155-3164 https://doi.org/10.1016/S0264-410X(02)00260-8
  68. Yusibov V, Modelska A, Steplewski K, Agadjanyan M, Weiner D, Hooper DC, Koprowski H (1997) Antigens produced in plants by infection with chimeric plant viruses immunize against rabies virus and HIV-1. Proc Natl Acad Sci USA 94: 5784-5788 https://doi.org/10.1073/pnas.94.11.5784
  69. Zhou JY, Wu JX, Cheng LQ, Zheng XJ, Gong H, Shang SB, Zhou EM (2003) Expression of immunogenic S1 glycoprotein of infectious bronchitis virus in transgenic potatoes. J Virol 77: 9090-9093 https://doi.org/10.1128/JVI.77.16.9090-9093.2003
  70. Zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2: 342-350 https://doi.org/10.1038/nrc798

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