Oral immunization with a lettuce-derived Escherichia coli heat-labile toxin B subunit induces neutralizing antibodies in mice

Plant Cell, Tissue and Organ Culture

Volumn 107, Issue 3, 2011, Pages 441-449

  Martínez González, Luzmila ^a   Rosales Mendoza, Sergio ^a,c   Soria Guerra, Ruth Elena ^a,c   Moreno Fierros, Leticia ^b   López Revilla, Rubén ^a   Korban, Schuyler S ^d   Guevara Arauza, Juan C ^c   Alpuche Solís, Ángel Gabriel ^a  

^a INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Enteric diseases; Oral immunization; Plant based vaccine

Indexed keywords

AGROBACTERIUM MEDIATED TRANSFORMATIONS; ANTIBODY RESPONSE; ATTRACTIVE SYSTEMS; BALB/C MICE; CHOLERA TOXIN; EDIBLE PLANTS; ENTEROTOXIGENIC ESCHERICHIA COLI; IMMUNOLOGICAL CHARACTERIZATION; INTESTINAL FLUID; NEUTRALIZING ANTIBODIES; QUATERNARY STRUCTURE; SUBUNIT VACCINE; TOTAL SOLUBLE PROTEIN; TRANSGENIC LINES; TRANSGENIC PLANTS;

ANTIBODIES; ESCHERICHIA COLI; MAMMALS; TISSUE; TOXIC MATERIALS; VACCINES;

IMMUNIZATION;

AGROBACTERIUM; ESCHERICHIA COLI; LACTUCA; MUS; RHIZOBIUM;

EID: 81155134002     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-011-9994-7     Document Type: Article

References (37)

1. Black RE (1993) Epidemiology of diarrheal disease: implications for control by vaccines. Vaccine 11: 100-106.
2. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
3. 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.
4. Clements JD, Sack DA, Harris JR, Chakraborty J, Neogy PK, Stanton B, Huda N, Khan MU, Kay BA, Khan MR (1988) Crossprotection by B subunit-whole cell cholera vaccine against diarrhea associated with heat-labile toxin-producing enterotoxigenic Escherichia coli: results of a large-scale field trial. J Infect Dis 158: 372-377.
5. Clements JD, van Loon F, Sack DA (1991) Field trial of oral cholera vaccines in Bangladesh: serum vibriocidal and antitoxic antibodies as markers of the risk of cholera. J Infect Dis 163: 1235-1242.
6. Curtis IS, Power JB, Blackhall NW, de Laat AMM, Davey MR (1994) Genotype-independent transformation of lettuce using Agrobacterium tumefaciens. J Exp Bot 45: 1441-1449.
7. Giudice EL, Campbell JD (2006) Needle-free vaccine delivery. Adv Drug Deliv Rev 58: 68-89.
8. Haq TA, Mason HS, Clements JD, Arntzen CJ (1995) Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 268: 714-716.
9. Hirst TR (1991) Assembly and secretion of oligomerictoxins in gram negative bacteria. In: Alouf JE, Freer JH (eds) A source book of bacterial protein toxins. Academic Press, London.
10. Hoffmeisterová H, Čeřovská N, Tomáš Moravec T, Helena Plchová H, Folwarczna J, J Velemínsky (2008) Transient expression of fusion gene coding for the HPV-16 epitopes fused to the sequence of potyvirus coat protein using different means of inoculation of Nicotiana benthamiana and Brassica rapa, cv. Rapa plants. Plant Cell Tiss Organ Cult 94: 261-267.
11. Kang TJ, Han SC, Kim MY, Kim YS, Yang MS (2004) Expression of non-toxic mutant of Escherichia coli heat-labile enterotoxin in tobacco chloroplasts. Protein Expr Purif 38: 123-128.
12. Kang TJ, Lee WS, Choi EG, Kim JW, Kim BG, Yang MS (2006) Mass production of somatic embryos expressing Escherichia coli heat-labile enterotoxin B subunit in Siberian ginseng. J Biotechnol 121: 124-133.
13. Kapusta J, Modelska A, Pniewski T, Figlerowicz M, Jankowski K, Lisowa O, Plucienniczak A, Koprowski H, Legocki AB (2001) Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Adv Exp Med Biol 495: 299-303.
14. Kim YS, Kim B-G, Kim T-G, Kang T-J, Yang M-S (2006) Expression of a cholera toxin B subunit in transgenic lettuce (Lactuca sativa L.) using Agrobacterium-mediated transformation system. Plant Cell Tiss Organ Cult 87: 203-210.
15. Kim TG, Kim MY, Kim BG, Kang TJ, Kim YS, Jang YS, Arntzen CJ, Yang MS (2007) Synthesis and assembly of Escherichia coli heat-labile enterotoxin B subunit in transgenic lettuce (Lactuca sativa). Protein Expr Purif 51: 22-27.
16. Kim TG, Kim BG, Kim MY, Choi JK, Jung ES, Yang MS (2010) Expression and immunogenicity of enterotoxigenic Escherichia coli heat-labile toxin B subunit in transgenic rice callus. Mol Biotechnol 44: 14-21.
17. Kim MY, Kim T-G, Yoo H-S, Yang M-S (2011) Expression and assembly of ApxIIA toxin of Actinobacillus pleuropneumoniae fused with the enterotoxigenic E. coli heat-labile toxin B subunit in transgenic tobacco. Plant Cell Tiss Organ Cult. doi: 10. 1007/s11240-010-9877-3.
18. Klipstein FA, Engert RF, Clements JD, Houghten RA (1984) Differences in cross-protection in rats immunized with the B subunits of cholera toxin and Escherichia coli heat-labile toxin. Infect Immun 43: 811-816.
19. Landell FGC, Rivera GG, Flores TJO, Martínez MB, Orozco EO (2008) Expression and functional analysis of an Entamoeba histolytica truncated adhesin in tomato plants. Plant Cell Tiss Organ Cult 94: 1-9.
20. 3 generation of transgenic tomato plants. Plant Cell Tiss Organ Cult 96: 335-342.
21. Lee JY, Yu J, Henderson D, Langridge WH (2004) Plant-synthesized E. coli CFA/I fimbrial protein protects Caco-2 cells from bacterial attachment. Vaccine 23: 222-231.
22. Loc NH, Song NV, Tien NQD, Minh TT, Nga PTQ, Kim T-G, Yang M-S (2011) Expression of the Escherichia coli heat-labile enterotoxin B subunit in transgenic watercress (Nasturtium officinale L.). Plant Cell Tiss Organ Cult. doi: 10. 1007/s11240-010-9835-0.
23. Mason HS, Haq TA, Clements JD, Arntzen CJ (1998) Edible vaccine protects mice against Escherichia coli heat-labile enterotoxin (LT): potatoes expressing a synthetic LT-B gene. Vaccine 16: 1336-1343.
24. Mason H, Warzecha H, Mor T, Arntzen C (2002) Edible plant vaccines: applications for prophylactic and therapeutic molecular medicine. Trends Mol Med 8: 324-329.
25. Michiels A, van den Ende W, Tucker M, van Riet L, van Laere A (2003) Extraction of high-quality genomic DNA from latex-containing plants. Anal Biochem 315: 85-89.
26. Moravec T, Schmidt MA, Herman EM, Woodford-Thomas T (2007) Production of Escherichia coli heat labile toxin (LT) B subunit in soybean seed and analysis of its immunogenicity as an oral vaccine. Vaccine 25: 1647-1657.
27. Peltola H, Siitonen A, Kyronseppa H, Simula I, Mattila L, Oksanen P, Kataja MJ, Cadoz M (1991) Prevention of travellers' diarrhoea by oral B-subunit/whole-cell cholera vaccine. Lancet 338: 1285-1289.
28. Qadri F, Wenneras C, Ahmed F, Azaduzzamar M, Saha D, Albert MJ, Sack RB, Svennerholm AM (2000) Safety and immunogenicity of an oral, inactivated enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine in Bangladeshi adults and children. Vaccine 18: 2704-2712.
29. Rezaee MA, Rezaee A, Moazzeni SM, Salmanian AH, Yasuda Y, Tochikubo K, Pirayeh SN, Arzanlou M (2005) Expression of Escherichia coli heat-labile enterotoxin B subunit (LTB) in Saccharomyces cerevisiae. J Microbiol 43: 354-360.
30. Richardson SH, Giles JC, Kruger KS (1984) Sealed adult mice: new model for enterotoxin evaluation. Infect Immun 43: 482-486.
31. Rosales-Mendoza S, Soria-Guerra RE, de Jesus Olivera-Flores MT, Lopez-Revilla R, Arguello-Astorga GR, Jimenez-Bremont JF, Garcia-de la Cruz RF, Loyola-Rodriguez JP, Alpuche-Solis AG (2007) Expression of Escherichia coli heat-labile enterotoxin b subunit (LTB) in carrot (Daucus carota L.). Plant Cell Rep 26: 969-976.
32. Rosales-Mendoza S, Soria-Guerra RE, López-Revilla R, Moreno-Fierros L, Alpuche-Solís A (2008) Ingestion of transgenic carrots expressing the Escherichia coli heat-labile enterotoxin B subunit protects mice against cholera toxin challenge. Plant Cell Rep 27: 79-84.
33. Sack RB, Gorbach SL, Banwell JG, Jacobs B, Chatterjee BD, Mitra RC (1971) Enterotoxigenic Escherichia coli isolated from patients with severe cholera-like disease. J Infect Dis 123: 378-385.
34. Spangler BD (1992) Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 56: 622-647.
35. Spira WM, Sack RB, Froehlich JL (1981) Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect Immun 32: 739-747.
36. Webster DE, Smith SD, Pickering RJ, Strugnell RA, Dry IB, Wesselingh SL (2006) Measles virus hemagglutinin protein expressed in transgenic lettuce induces neutralising antibodies in mice following mucosal vaccination. Vaccine 24: 3538-3544.
37. Yu J, Langridge WH (2001) A plant-based multicomponent vaccine protects mice from enteric diseases. Nat Biotechnol 19: 548-552.