Immune responses to new vaccine candidates constructed by a live attenuated Salmonella typhimurium delivery system expressing Escherichia coli F4, F5, F6, F41 and intimin adhesin antigens in a murine model

Journal of Veterinary Medical Science

Volumn 73, Issue 10, 2011, Pages 1265-1273

  Hur, Jin ^a   Lee, John Hwa ^a  

^a Chonbuk National University   (South Korea)

Author keywords

Adhesin; Expression and secretion plasmid; Neonatal piglet diarrhea; Pathogenic escherichia coli; Salmonella delivery system

Indexed keywords

ADHESIN; ANTIGEN 987P, E COLI; BACTERIAL ANTIGEN; BACTERIAL TOXIN; EAEA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; ESCHERICHIA COLI VACCINE; F41 ANTIGEN, E COLI; FIMBRIA PROTEIN; K88 ANTIGEN, E COLI; K99 ANTIGEN; LIVE VACCINE; MEMBRANE ANTIGEN; RECOMBINANT VACCINE;

ANIMAL; ANIMAL DISEASE; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; DRUG DELIVERY SYSTEM; ESCHERICHIA COLI INFECTION; FEMALE; GENETIC TRANSFORMATION; IMMUNOLOGY; MOUSE; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASE;

ADHESINS, BACTERIAL; ADHESINS, ESCHERICHIA COLI; ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; BACTERIAL TOXINS; DRUG DELIVERY SYSTEMS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; FEMALE; FIMBRIAE PROTEINS; MICE; MICE, INBRED BALB C; MODELS, ANIMAL; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASES; TRANSFORMATION, GENETIC; VACCINES, ATTENUATED; VACCINES, SYNTHETIC;

ESCHERICHIA COLI; MURINAE; MUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 80055074933     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.11-0087     Document Type: Article

References (48)

1. Ascón, M., Hone, D. H., Walters, N. and Pascual, D. W. 1998. Oral immunization with a Salmonella typhimurium vaccine vector expressing recombinant enterotoxigenic Escherichia coli K99 fimbriae elicits elevated antibody titers for protective immunity. Infect. Immun. 66: 5470-5476.
2. Branger, C. G., Torres-Escobar, A., Sun, W., Perry, R., Fetherston, J., Roland, K. L. and Curtiss, III R. 2009. Oral vaccination with LcrV from Yersinia pestis KIM delivered by live attenuated Salmonella enterica serovar Typhimurium elicits a protective immune response against challenge with Yersinia pseudotuberculosis and Yersinia enterocolitica. Vaccine 27: 5363-5370.
3. Carvajal, B. G., Methner, U., Pieper, J. and Berndt, A. 2008. Effects of Salmonella enterica serovar Enteritidis on cellular recruitment and cytokine gene expression in caecum of vaccinated chickens. Vaccine 26: 5423-5433.
4. Causey, R. C., Artiushin, S. C., Crowley, I. F., Weber, J. A., Homola, A. D., Kelley, A., Stephenson, L. A., Opitz, H. M., Guilmain, S. and Timoney, J. F. 2010. Immunisation of the equine uterus against Streptococcus equi subspecies zooepidemicus using an intranasal attenuated Salmonella vector. Vet. J. 184: 156-161.
5. Chen, X., Gao, S., Jiao, X. and Liu, X. F. 2004. Prevalence of serogroups and virulence factors of Escherichia coli strains isolated from pigs with postweaning diarrhoea in eastern China. Vet. Microbiol. 103: 13-20.
6. Chen, H. and Schifferli, D. M. 2000. Mucosal and systemic immune responses to chimeric fimbriae expressed by Salmonella enterica serovar Typhimurium vaccine strains. Infect. Immun. 68: 3129-3139.
7. Gaastra, W. and de Graaf, F. K. 1982. Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiol. Rev. 46: 129-161.
8. Galan, J. E., Nakayama, K. and Curtiss, III, R. 1990. Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene 94: 29-35.
9. Gentschev, I., Glaser, I., Goebel, W., McKeever, D. J., Musoke, A. and Heussler, V. T. 1998. Delivery of the p67 sporozoite antigen of Theileria parva by using recombinant Salmonella dublin: secretion of the product enhances specific antibody responses in cattle. Infect. Immun. 66: 2060-2064.
10. Gentschev, I., Mollenkopf, H., Sololovic, Z., Hess, J., Kaufmann, S. H. and Goebel, W. 1996. Development of antigen- delivery systems, based on the Escherichia coli hemolysin secretion pathway. Gene 179:133-140.
11. Guinee, P. A. and Jansen, W. H. 1979. Behavior of Escherichia coli K antigens K88ab, K88ac, and K88ad in immunoelectrophoresis, double diffusion, and hemagglutination. Infect. Immun. 23: 700-705.
12. Haesebrouck, F., Pasmans, F., Chiers, K., Maes, D., Ducatelle, R. and Decostere, A. 2004. Efficacy of vaccines against bacterial diseases in swine: what can we expect? Vet. Microbiol. 100: 255-268.
13. Hajishengallis, G., Arce, S., Gockel, C. M., Connell, T. D. and Russell, M. W. 2005. Immunomodulation with enterotoxins for the generation of secretory immunity or tolerance: applications for oral infections. J. Dent. Res. 84: 1104-1116.
14. Harmsen, M. M., van Solt, C. B., Hoogendoorn, A., van Zijderveld, F. G., Niewold, T. A. and van der Meulen, J. 2005. Escherichia coli F4 fimbriae specific llsma single-domain antibody fragments effectively inhibit bacterial adhesion in vitro but poorly protect against diarrhorea. Vet. Microbiol. 111: 89-98.
15. Holmgren, J. and Czerkinsky, C. 2005. Mucosal immunity and vaccines. Nat. Med. 11: 545-553.
16. Hur, J. and Lee, J. H. 2010. Immunization of pregnant sows with a novel virulence gene deleted live Salmonella vaccine and protection of their suckling piglets against salmonellosis. Vet. Microbiol. 143: 270-276.
17. Hur, J., Kim, M. Y. and Lee, J. H. 2011. Evaluation of efficacy of a new live Salmonella Typhimurium vaccine candidate in a murine model. Comp. Immunol. Microbiol. Infect. Dis. 34: 171-177.
18. Hur, J., Song, S. O., Lim, J. S., Chung, I. G. and Lee, J. H. 2011. Efficacy of a novel virulence gene-deleted Salmonella Typhimurium vaccine for protection against Salmonella infections in growing piglets. Vet. Immunol. Immunopathol. 139: 250-256.
19. Janeway, C. A. and Medzhitov, R. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
20. Kang, H. Y., Srinivasan, J. and Curtiss, R. 3rd. 2002. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect. Immun. 70: 1739-1749.
21. Khare, S., Alali, W., Zhang, S., Hunter, D., Pugh, R., Fang, F. C., Libby, S. J. and Adams, L. G. 2010. Vaccination with attenuated Salmonella enterica Dublin expressing E. coli O157:H7 outer membrane protein Intimin induces transient reduction of fecal shedding of E. coli O157:H7 in cattle. BMC Vet. Res. 6: 35.
22. Kim, S. W., Kim, Y. H., Yoo, A. Y., Yu, J. E., Hur, J., Lee, J. H., Cha, J. and Kang, H. Y. 2007. Development of a protein secretion system with the application of Sec-dependent protein secretion components. J. Microbiol. Biotechnol. 17: 1316-1323.
23. Kohler, J. J., Pathangey, L. B. and Brown, T. A. 1998. Oral immunization with recombinant Salmonella typhimurium expressing a cloned Porphyromonas gingivalis hemagglutinin: effect of boosting on mucosal, systemic and immunoglobulin G subclass response. Oral Microbiol. Immunol. 13: 81-88.
24. Krause, G., Zimmermann, S. and Beutin, L. 2005. Investigation of domestic animals and pets as a reservoir for intimin-(eae) gene positive Escherichia coli types. Vet. Microbiol. 106: 87-95.
25. Lee, S. H., Jung, B. Y., Rayamahji, N., Lee, H. S., Jeon, W. J., Choi, K. S., Kweon, C. H. and Yoo, H. S. 2009. A multiplex real-time PCR for differential detection and quantification of Salmonella spp., Salmonella enterica serovar Typhimurium and Enteritidis in meats. J. Vet. Sci. 10: 43-51.
26. Liao, C. W., Lin, S. H., Lin, P. Y., Chiou, H. Y., Chang, W. F. and Weng, C. N. 2004. Orally administrable enterotoxigenic Escherichia coli vaccine encapsulated by ethylcellulose powder dispersion. Appl. Microbiol. Biotechnol. 65: 295-300.
27. Malik, A., Tóth, I., Beutin, L., Schmidt, H., Taminiau, B., Dow, M. A., Marabito, S., Oswald, E., Mainil, J. and Nagy, B. 2006. Serotypes and intimin types of intestinal and faecal strains of eae+ Escherichia coli from weaned pigs. Vet. Microbiol. 114: 82-93.
28. Matic, J. N., Terry, T. D., Van Bockel, D., Maddocks, T., Tinworth, D., Jennings, M. P., Dordjevic, S. P. and Walker, M. J. 2009. Development of non-antibiotic-resistant, chromosomally based, constitutive and inducible expression systems for aroAattenuated Salmonella enterica serovar Typhimurium. Infect. Immun. 7: 1817-1826.
29. Mestecky, J., Nguyen, H., Czerkinsky, C. and Kiyono, H. 2008. Oral immunization: an update. Curr. Opin. Gastroenterol. 24: 713-719.
30. Morgan, R. L., Isaacson, R. E., Moon, H. W., Brinton, C. C. and To, C. C. 1978. Immunization of suckling pigs against enterotoxigenic E. coli-induced diarrhoeal disease by vaccinating dams with purified 987 or K99 pili. Infect. Immun. 22: 771-777.
31. Nagy, B. and Fekete, P. Z. 1999. Enterotoxigenic Escherichia coli in farm animals. Vet. Res. 30: 259-284.
32. O'Garra, A. and Arai, N. 2000. The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell Biol. 10: 542-550.
33. Osek, J. 1999. Prevalence of virulence factors of Escherichia coli strains isolated from diarrheic and healthy piglets after weaning. Vet. Microbiol. 68: 209-217.
34. Osek, K. 2003. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 (EAST1) gene and its relationship with fimbrial and enterotoxin markers in E. coli isolates from pigs with diarrhoea. Vet. Microbiol. 91: 65-72.
35. Pathangey, L., Kohler, J. J., Isoda, R. and Brown, T. A. 2009. Effect of expression level on immune responses to recombinant oral Salmonella enterica serovar Typhimurium vaccines. Vaccine 27: 2707-2711.
36. Puiprom, O., Chantaroj, S., Gangnonngiw, W., Okada, K., Honda, T., Taniguchi, T. and Sawanpanyalert, P. 2010. Identification of colonization factors of enterotoxigenic Escherichia coli with PCR-based technique. Epidemiol. Infect. 138: 519-524.
37. Remer, K. A., Barttrow, M., Roeger, B., Moll, H., Sonnenborn, U. and Oelschlaeger, T. A. 2009. Split immune response after oral vaccination of mice with recombinant Escherichia coli Nissle 1917 expressing fimbrial adhesin K88. Int. J. Med. Microbiol. 299: 467-478.
38. Riising, H. J., Murmans, M. and Witvliet, M. 2005. Protection against neonatal Escherichia coli diarrhoea in pigs by vaccination of sows with a new vaccine that contains purified enterotoxic E. coli virulence factors F4ac, F4ab, F5 and F6 fimbrial antigens and heat-labile E. coli enterotoxin (LT) toxoid. J. Vet. Med. B Infect. Dis. Vet. Public Health 52: 296-300.
39. Rojas, R. L., Gomes, P. A., Bentancor, L. V., Sbrogio-Almeida, M. E., Costa, S. O., Massis, L. M., Ferreira, R. C., Palermo, M. S. and Ferreira, L. C. 2010. Salmonella enterica serovar Typhimurium vaccine strains expressing a nontoxic shiga-like toxin 2 derivative induce partial protective immunity to the toxin expressed by enterohemorrhagic Escherichia coli. Clin. Vaccine Immunol. 17: 529-536.
40. Snoeck, V., Huyghebaert, N., Cox, E., Vermeire, A., Vancaeneghem, S., Remon, J. P. and Goddeeris, B. M. 2003. Entericcoated pellets of F4 fimbriae for oral vaccination of suckling piglets against enterotoxigenic Escherichia coli infections. Vet. Immunol. Immunopathol. 96: 219-227.
41. Spellberg, B. and Edwards, J. E. Jr. 2001. Type 1/type 2 immunity in infectious diseases. Clin. Infect. Dis. 32: 76-102.
42. VanCott, J. L., Staats, H. F., Pascual, D. W., Roberts, M., Chatfield, S. N., Yamamoto, M, Coste, M., Carter, P. B., Kiyono, H. and McGhee, J. R. 1996. Regulation of mucosal and systemic antibody responses by T helper cell subsets, macrophages, and derived cytokines following oral immunization with live recombinant Salmonella. J. Immunol. 156: 1504-1514.
43. Vázquez, F., González, E. A., Garabal, J. I. and Blanco, J. 2006. Characherization of fimbriae extracts from porcine enterotoxigenic Escherichia coli strains carrying F6 (987P) antigen. Int. Microbiol. 9: 241-246.
44. Verdonck, F., Cox, E., van Gog, K., Van der Stede, Y., Duchateau, L., Deprez, P. and Goddeeris, B. M. 2002. Different kinetic of antibody responses following infection of newly weaned pigs with an F4 enterotoxigenic Escherichia coli strain or an F18 verotoxigenic Escherichia coli strain. Vaccine 20: 2995-3004.
45. Verdonck, F., Snoeck, V., Goddeeris, B. M. and Cox, E. 2005. Cholera toxin improves the F4(K88)-specific immune response following oral immunization of pigs with recombinant FaeG. Vet. Immunol. Immunopathol. 103: 21-29.
46. Vu-Khac, H., Holoda, E., Pilipcinec, E., Blanco, M., Blanco, J. E., Dahbi, G., Mora, A., López, C., González, E. A. and Blanco, J. 2007. Serotypes, virulence genes, intimin types and PFGE profiles of Escherichia coli isolated from piglets with diarrhea in Slovakia. Vet. Microbiol. 174: 176-187.
47. Zhang, W., Fang, Y. and Francis, D. H. 2009. Characterization of the binding specificity of K88ac and K88ad fimbriae of Enterotoxigenic Escherichia coli by constructing K88ac/K88ad chimeric major subnuits. Infect. Immun. 77: 699-706.
48. Zhu, C., Harel, J., Jacques, M., Desautels, C., Donnenberg, M. S., Beaudry, M. and Fairbrother, J. M. 1994. Virulence properties and attaching-effacing activity of E. coli O45 from swine postweaning diarrhea. Infect. Immun. 62: 4153-4159.