B subunit of Escherichia coli heat-labile enterotoxin as adjuvant of humoral immune response in recombinant BCG vaccination

Canadian Journal of Microbiology

Volumn 54, Issue 8, 2008, Pages 677-686

  Da Silva Ramos Rocha, Andréa ^a   Conceição, Fabricio Rochedo ^a   Grassmann, André Alex ^a   Lagranha, Valeska Lizzi ^a   Dellagostin, Odir Antônio ^a  

^a FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

Author keywords

Adjuvant; Humoral immune response; LTB; Recombinant BCG

Indexed keywords

ANTIGENS; ESCHERICHIA COLI; IMMUNIZATION;

ADJUVANT; BIOLOGICAL PROPERTIES; HEAT-LABILE ENTEROTOXIN; HUMORAL IMMUNE RESPONSE; IMMUNE RESPONSES; LTB; MEAN RATIO; RECOMBINANT BCG;

IMMUNOLOGY;

ADHESIN; ADJUVANT; BCG VACCINE; ENTEROTOXIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; PROTEIN P97; PROTEIN SUBUNIT; RECOMBINANT VACCINE;

ANTIGEN; BACTERIUM; GENE EXPRESSION; IMMUNE RESPONSE; RECOMBINATION; TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; HEATING; HUMORAL IMMUNITY; IMMUNOMODULATION; MOLECULAR CLONING; MOUSE; MYCOPLASMA HYOPNEUMONIAE; MYCOPLASMA PNEUMONIA; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TH1 CELL; TH2 CELL; WESTERN BLOTTING;

ADHESINS, BACTERIAL; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODY FORMATION; BACTERIAL TOXINS; BCG VACCINE; CLONING, MOLECULAR; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; FEMALE; MICE; MICE, INBRED BALB C; MYCOPLASMA HYOPNEUMONIAE; TUBERCULOSIS; VACCINATION; VACCINES, SYNTHETIC;

ESCHERICHIA COLI; MUS; MYCOPLASMA HYOPNEUMONIAE;

EID: 49449095824     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W08-056     Document Type: Article

References (45)

1. Bastos, R.G., Dellagostin, O.A., Barletta, R.G., Doster, A.R., Nelson, E., Zuckermann, F., and Osório, F.A. 2004. Immune response of pigs inoculated with Mycobacterium bovis BCG expressing a truncated form of GP5 and M protein of porcine reproductive and respiratory syndrome virus. Vaccine, 22: 467-474. doi:10.1016/S0264-410X(03)00572-3. PMID:14670329.
2. Biet, F., Kremer, L., Wolowczuk, I., Delacre, M., and Locht, C. 2003. Immune response induced by recombinant Mycobacterium bovis BCG producing the cholera toxin B subunit. Infect. Immun. 71: 2933-2937. doi:10.1128/IAI.71.5.2933-2937.2003. PMID:12704173.
3. Carter, J.E., Yu, J., Choi, N.W., Hough, J., Henderson, D., He, D., and Langridge, W.H. 2006. Bacterial and plant enterotoxin B subunit-autoantigen fusion proteins suppress diabetes insulitis. Mol. Biotechnol. 32: 1-15. doi:10.1385/MB:32:1:001. PMID:16382177.
4. Chen, A.Y., Fry, S.R., Forbes-Faulkner, J., Daggard, G., and Mukkur, T.K. 2006. Evaluation of the immunogenicity of the P97R1 adhesin of Mycoplasma hyopneumoniae as a mucosal vaccine in mice. J. Med. Microbiol. 55: 923-929. doi:10.1099/jmm.0.46088-0. PMID:16772421.
5. Chen, J.R., Liao, C.W., Mao, C.N.W., and Weng, C.N. 2001. A recombinant chimera composed of repeat region RR1 of Mycoplasma hyopneumoniae adhesin with Pseudomonas exotoxin: in vivo evaluation of specific IgG response in mice and pigs. Vet. Microbiol. 80: 347-357. doi:10.1016/S0378-1135(01)00315-7. PMID:11348771.
6. Conceição, F.R., Moreira, A.N., and Dellagostin, O.A. 2006. A recombinant chimera composed of R1 repeat region of Mycoplasma hyopneumoniae P97 adhesin with Escherichia coli heat-labile enterotoxin B subunit elicits immune response in mice. Vaccine, 24: 5734-5743. doi:10.1016/j.vaccine.2006.04.036. PMID:16730864.
7. Cruz, F.W., McBride, A.J., Conceição, F.R., Dale, J.W., McFadden, J., and Dellagostin, O.A. 2001. Expression of the B-cell and T-cell epitopes of the rabies virus nucleoprotein in Mycobacterium bovis BCG and induction of a humoral response in mice. Vaccine, 20: 731-736. doi:10.1016/S0264-410X(01)00414-5. PMID:11738736.
8. De Haan, L., Verweij, W.R., Feil, I.K., Holtrop, M., Hol, W.G.J., Agsteribbe, E., and Wilschut, J. 1998. Role of GM1 binding in the mucosal immunogenicity and adjuvant activity of the Escherichia coli heat-labile enterotoxin and its B subunit. Immunology, 94: 424-430. doi:10.1046/j.1365-2567.1998.00535.x. PMID:9767427.
9. Dellagostin, O.A., Esposito, G., Eales, L.J., Dale, J.W., and McFadden, J. 1995. Activity of mycobacterial promoters during intracellular and extracellular growth. Microbiology, 141: 1785-1792. PMID:7551043.
10. Ferreira, D.M., Darrieux, M., Oliveira, M.L., Leite, L.C., and Miyaji, E.N. 2008. Optimized immune response elicited by a DNA vaccine expressing pneumococcal surface protein A is characterized by a balanced immunoglobulin G1 (IgG1)/IgG2a ratio and pro-inflammatory cytokine production. Clin. Vaccine Immunol. 15: 499-505. doi:10.1128/CVI.00400-07. PMID:18184825.
11. Fingerut, E., Gutter, B., Goldway, M., Eliahoo, D., and Pitcovski, J. 2006. B subunit of E. coli enterotoxin as adjuvant and carrier in oral and skin vaccination. Vet. Immunol. Immunopathol. 112: 253-263. doi:10.1016/j.vetimm.2006.03.005. PMID:16701905.
12. Fischer, G., Conceição, F.R., Leite, F.P.L., Dummer, L.A., Vargas, G.D., Hübner, S.O., et al. 2007. Immunomodulation produced by a green propolis extract on humoral and cellular responses of mice immunized with SuHV-1. Vaccine, 25: 1250-1256. doi:10.1016/j.vaccine.2006.10.005. PMID:17084001.
13. Fukuta, S., Magnani, J.L., Twiddy, E.M., Holmes, R.K., and Ginsburg, V. 1988. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 56: 1748-1753. PMID:3290106.
14. Green, E.A., Botting, C., Webb, H.M., Hirst, T.R., and Randall, R.E. 1996. Construction, purification and immunogenicity of antigen antibody-LTB complexes. Vaccine, 14: 949-958. doi:10.1016/0264-410X(96)00039-4. PMID:8873387.
15. Habjanec, L., Halassy, B., and Tomasić, J. 2008. Immunomodulatory activity of novel adjuvant formulations based on Montanide ISA oil-based adjuvants and peptidoglycan monomer. Int. Immunopharmacol. 8: 717-724. doi:10.1016/j.intimp.2008.01.017. PMID:18387514.
16. Hayward, C.M.M., O'Gaorab, P., Young, D.B., Griffin, G.E., Thole, J., Hirst, T.R., et al. 1999. Construction and murine immunogenicity of recombinant Bacille Calmette Guérin vaccines expressing the B subunit of Escherichia coli heat labile enterotoxin. Vaccine, 17: 1272-1281. doi:10.1016/S0264-410X(98)00350-8. PMID:10195640.
17. Kim, P.H., Eckmann, L., Lee, W.J., Han, W., and Kagnoff, M.F. 1998. Cholera toxin and cholera toxin B subunit induce IgA switching through the action of TGF-beta 1. J. Immunol. 160: 1198-1203. PMID:9570534.
18. Langermann, S., Palaszynski, S., Sadziene, A., Stover, C., and Koenig, S. 1994. Systemic and mucosal immunity induced by BCG vector expressing outer surface protein A of Borrelia burgdorferi. Nature (Lond.), 372: 552-555. doi:10.1038/372552a0. PMID:7990928.
19. Lebens, M., Shahabi, V., Backstrom, M., Houze, T., Lindblad, M., and Holmgren, J. 1996. Synthesis of hybrid molecules between heat-labile enterotoxin and cholera toxin B subunits: potential for use in a broad-spectrum vaccine. Infect. Immun. 64: 2144-2150. PMID:8675319.
20. Leclerc, C. 2003. New approaches in vaccine development. Comp. Immunol. Microbiol. Infect. Dis. 26: 329-341. doi:10.1016/S0147-9571(03)00018-3. PMID:12818620.
21. Maassen, C.B., Boersma, W.J., van Holten-Neelen, C., Claassen, E., and Laman, J.D. 2003. Growth phase of orally administered Lactobacillus strains differentially affects IgG1/IgG2a ratio for soluble antigens: implications for vaccine development. Vaccine, 21: 2751-2757. doi:10.1016/S0264-410X(03)00220-2. PMID:12798614.
22. Mazzantini, R.P., Miyaji, E.N., Dias, W.O., Sakauchi, D., Nascimento, A.O., Raw, I., et al. 2004. Adjuvant activity of Mycobacterium bovis BCG expressing CRM197 on the immune response induced by BCG expressing tetanus toxin fragment C. Vaccine, 22: 740-746. doi:10.1016/j.vaccine.2003.08.017. PMID:14741167.
23. Michelon, A., Conceição, F.R., Binsfeld, P.C., da Cunha, C.W., Moreira, A.N., Argondizzo, A.P., et al. 2006. Immunogenicity of Mycobacterium bovis BCG expressing Anaplasma marginale MSP1a antigen. Vaccine, 24: 6332-6339. doi:10.1016/j.vaccine.2006.05.028. PMID:16781025.
24. Millar, D.G., Hirst, T.R., and Snider, D.P. 2001. Escherichia coli heat labile enterotoxin B subunit is a more potent mucosal adjuvant than its closely related homologue, the B subunit of cholera toxin. Infect. Immun. 69: 3476-3482. doi:10.1128/IAI.69.5.3476-3482.2001. PMID:11292779.
25. Mosmann, T.R., and Coffman, R.I. 1989. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7: 145-173. doi:10.1146/annurev.iy.07.040189.001045. PMID:2523712.
26. Murray, A., Winter, N., Lagranderie, M., Hill, D.F., Rauzier, J., Timm, J., et al. 1992. Expression of Escherichia coli beta-galactosidase in Mycobacterium bovis BCG using an expression system isolated from Mycobacterium paratuberculosis which induced humoral and cellular immune responses. Mol. Microbiol. 6: 3331-3342. doi:10.1111/j.1365-2958.1992. tb02201.x. PMID:1336563.
27. Nascimento, I.P., Dias, W.O., Mazzantini, R.P., Miyaji, E.N., Gamberini, M., Quintilio, W., et al. 2000. Recombinant Mycobacterium bovis BCG expressing pertussis toxin subunit S1 induces protection against an intracerebral challenge with live Bordetella pertussis in mice. Infect. Immun. 68: 4877-4883. doi:10.1128/IAI.68.9.4877-4883.2000. PMID:10948100.
28. Nashar, T.O., Hirst, T.R., and Williams, N.A. 1997. Modulation of B-cell activation by the B subunit of Escherichia coli enterotoxin: receptor interaction up regulates MHC class II, B7, CD40, CD25 and ICAM-1. Immunology, 91: 572-578. doi:10.1046/j.1365-2567.1997.00291.x. PMID:9378497.
29. Ohara, N., and Yamada, T. 2001. Recombinant BCG vaccines. Vaccine, 19: 4089-4098. doi:10.1016/S0264-410X(01)00155-4. PMID:11457532.
30. Pitcovski, J., Bazak, Z., Wasserman, E., Elias, O., Levy, A., Peretz, T., et al. 2006. Heat labile enterotoxin of E. coli: a potential adjuvant for transcutaneous cancer immunotherapy. Vaccine, 24: 636-643. PMID:16157421.
31. Ranallo, R.T., Fonseka, C.P., Cassels, F., Srinivasan, J., and Venkatesan, M.M. 2005. Construction and characterization of bivalent Shigella flexneri 2a vaccine strains SC608 (pCFAI) and SC608 (pCFAI/LTB) that express antigens from enterotoxigenic Escherichia coli. Infect. Immun. 73: 258-267. doi:10.1128/IAI.73.1.258-267.2005. PMID:15618162.
32. Richards, C.M., Amon, A.T., Hirst, T.R., Hill, T.J., and Williams, N.A. 2001. Protective immunity to ocular herpes simplex virus type-1 infection in mice using Escherichia coli heat-labile enterotoxin. J. Virol. 75: 1664-1671. doi:10.1128/JVI.75.4.1664-1671.2001. PMID:11160664.
33. Ruddock, L.W., Ruston, S.P., Kelly, S.M., Price, N.C., Freedman, R.B., and Hirst, T.R. 1995. Kinetics of acid-mediated disassembly of the B subunit pentamer of Escherichia coli heat-labile enterotoxin. Molecular basis of pH stability. J. Biol. Chem. 270: 29953-29959. doi:10.1074/jbc.270.50. 29953. PMID:8530395.
34. Sambrook, J., and Russell, D.W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
35. Schödel, F., and Will, H. 1989. Construction of a plasmid for expression of foreign epitopes as fusion protein with subunit B of Escherichia coli heat-labile enterotoxin. Infect. Immun. 57: 1347-1350. PMID:2647637.
36. Shimoji, Y., Oishi, E., Kitajima, T., Muneta, Y., Shimizu, S., and Mori, Y. 2002. Erysipelothrix rhusiopathiae YS-1 as a live vaccine vehicle for heterologous protein expression and intranasal immunization of pigs. Infect. Immun. 70: 226-232. doi:10.1128/IAI.70.1.226-232.2002. PMID:11748187.
37. Snoeck, V., Peters, I.R., and Cox, E. 2006. The IgA system: a comparison of structure and function in different species. Vet. Res. 37: 455-467. doi:10.1051/vetres:2006010. PMID:16611558.
38. Stover, C.K., Bansal, G.P., Hanson, M.S., Burlein, J.E., Palaszynski, S.R., Young, J.F., et al. 1993. Protective immunity elicited by recombinant bacille Calmette-Guérin (BCG) expressing outer surface protein A (OspA) lipoprotein: a candidate Lyme disease vaccine. J. Exp. Med. 178: 197-209. doi:10.1084/jem.178.1.197. PMID:8315378.
39. Tamura, S., Hatori, E., Tsuruhara, T., Aizawa, C., and Kurata, T. 1997. Suppression of delayed type hypersensitivity and IgE antibody responses to ovalbumin by intranasal administration of Escherichia coli heat-labile enterotoxin B subunit-conjugated ovalbumin. Vaccine, 15: 225-229. doi:10.1016/S0264-410X(96)00135-1. PMID:9066042.
40. Truitt, R.L., Hanke, C., Radke, J., Mueller, R., and Barbieri, J.T. 1998. Glycosphingolipids as novel targets for T-cell suppression by the B subunit of recombinant heat-labile enterotoxin. Infect. Immun. 66: 1299-1308. PMID:9529046.
41. Varaldo, P.B., Leite, L.C., Dias, W.O., Miyaji, E.N., Torres, F.I., Gebara, V.C., et al. 2004. Recombinant Mycobacterium bovis BCG expressing the Sm14 antigen of Schistosoma mansoni protects mice from cercarial challenge. Infect. Immun. 72: 3336-3343. doi:10.1128/IAI.72.6.3336-3343. 2004. PMID:15155638.
42. Weltzin, R., Guy, B., Thomas, W.D., Giannasca, P.J., and Monath, T.P. 2000. Parenteral adjuvant activities of Escherichia coli heat-labile toxin and its B subunit for immunization of mice against Helicobacter pylori infection. Infect. Immun. 68: 2775-2782. doi:10.1128/IAI.68.5. 2775-2782.2000. PMID:10768972.
43. Williams, N.A. 2000. Immune modulation by the cholera-like enterotoxin B-subunits: from adjuvant to immunotherapeutic. Int. J. Med. Microbiol. 290: 447-453. PMID:11111925.
44. Winter, N., Lagranderie, M., Gangloff, S., Leclerc, C., Gheorghiu, M., and Gicquel, B. 1995. Recombinant BCG strains expressing the SIV mac 251 nef gene induce proliferative and CTL responses against nef synthetic peptides in mice. Vaccine, 13: 471-478. doi:10.1016/0264- 410X(94)00001-4. PMID:7543715.
45. Yamamoto, M., McGhee, J.R., Hagiwara, Y., Otake, S., and Kiyono, H. 2001. Genetically manipulated bacterial toxin as a new generation mucosal adjuvant. Scand. J. Immunol. 53: 211-217. doi:10.1046/j.1365-3083.2001.00883.x. PMID:11251876.