Enhancement of immune responses by an attenuated Salmonella enterica serovar Typhimurium strain secreting an Escherichia coli heat-labile enterotoxin B subunit protein as an adjuvant for a live Salmonella vaccine candidate

Clinical and Vaccine Immunology

Volumn 18, Issue 2, 2011, Pages 203-209

  Hur, Jin ^a   Lee, John Hwa ^a  

^a Chonbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI HEAT LABILE ENTEROTOXIN B; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; LIVE VACCINE; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOBLOTTING; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLOSIS; WESTERN BLOTTING; WILD TYPE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL TOXINS; DISEASE MODELS, ANIMAL; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; FEMALE; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; PLASMIDS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; SURVIVAL ANALYSIS; VACCINATION; VACCINES, ATTENUATED;

EID: 79551473978     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00407-10     Document Type: Article

References (53)

1. Abd El Ghany, M., et al. 2007. Candidate live, attenuated Salmonella enterica serotype Typhimurium vaccines with reduced fecal shedding are immunogenic and effective oral vaccines. Infect. Immun. 75:1835-1842.
2. Alvarez, J., et al. 2004. Development of a multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples. J. Clin. Microbiol. 42:1734-1738.
3. Bessa, M. C., et al. 2007. Phenotypic and genetic characterization of Salmonella enterica subsp. enterica serovar Typhimurium isolated from pigs in Rio Grande do Sul, Brazil. Res. Vet. Sci. 83:302-310.
4. Boyen, F., et al. 2008. Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. Vet. Microbiol. 130:1-19.
5. Brumme, S., et al. 2007. Impact of Salmonella Typhimurium DT104 virulence factors invC and sseD on the onset, clinical course, colonization patterns and immune response of porcine salmonellosis. Vet. Microbiol. 124: 274-285.
6. Chen, H., and D. M. Schifferli. 2003. Construction, characterization, and immunogenicity of an attenuated Salmonella enterica serovar Typhimurium pgtE vaccine expressing fimbriae with integrated viral epitopes from the spiC promoter. Infect. Immun. 71:4664-4673.
7. Donaldson, D. S., K. K. Tong, and N. A. Williams. 2010. Mucosal administration of the B subunit of E. coli heat-labile enterotoxin promotes the development of Foxp3-expressing regulatory T cells. Mucosal Immunol. doi: 10.1038/mi.2010.65.
8. Fingerut, E., B. Gutter, M. Goldway, D. Eliahoo, and J. Pitcovski. 2006. B subunit of E. coli enterotoxin as adjuvant and carrier in oral and skin vaccination. Vet. Immunol. Immunopathol. 112:253-263.
9. Freytag, L. C., and J. D. Clements. 2005. Mucosal adjuvants. Vaccine 23: 1804-1813.
10. Garmory, H. S., et al. 2003. The use of live attenuated bacteria as a delivery system for heterologous antigens. J. Drug Target. 11:471-479.
11. Hajishengallis, G., S. Arce, C. M. Gockel, T. D. Connell, and M. W. Russell. 2005. Immunomodulation with enterotoxins for the generation of secretory immunity or tolerance: application for oral infections. J. Dent. Res. 84:1104-1116.
12. Holmgren, J., M. Lindblad, P. Fredman, L. Svennerholm, and H. Myrvold. 1985. Comparison of receptors for cholera and Escherichia coli enterotoxins in human intestine. Gastroenterology 89:27-35. (Pubitemid 15057910)
13. Kadonaga, J. T., A. Plückthun, and J. R. Knowles. 1985. Signal sequence mutants of β-lactamase. J. Biol. Chem. 260:16192-16199.
14. Kang, H. Y., J. Srinivasan, and R. Curtiss III. 2002. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect. Immun. 70:1739-1749.
15. Kim, S. W., et al. 2009. Changes of physiological and biochemical properties of Salmonella enterica serovar Typhimurium by deletion of cpxR and lon genes using allelic exchange method. J. Microbiol. Methods 79:314-320.
16. Kodama, C., et al. 2005. Evaluation of the Lon-deficient Salmonella strain as an oral vaccine candidate. Microbiol. Immunol. 49:1035-1045.
17. Koshland, D., and D. Botstein. 1980. Secretion of beta-lactamase requires the carboxy end of the protein. Cell 20:749-760. (Pubitemid 10078554)
18. Kwon, Y. M., M. M. Cox, and L. N. Calhoun. 2007. Salmonella-based vaccines for infectious diseases. Expert Rev. Vaccines 6:147-152.
19. Lim, J. U., et al. 2009. Expression of functional pentameric heat-labile enterotoxin B subunit of Escherichia coli in Saccharomyces cerevisiae. J. Microbiol. Biotechnol. 19:502-510.
20. Liu, D., X. Wang, J. Ge, S. Liu, and Y. Li. 2010. Comparison of the immune responses induced by oral immunization of mice with Lactobacillus casei-expressing porcine parvovirus VP2 and VP2 fused to Escherichia coli heatlabile enterotoxin B subunit protein. Comp. Immunol. Microbiol. Infect. Dis. doi:10.1016/j.cimid. 2010.02.004.
21. + T cells. Arthritis Rheum. 46: 1671-1682.
22. Ma, X., B. Yao, W. Zheng, and L. Li. 2010. Comparative study on characterization of recombinant B subunit of E. coli heat-labile enterotoxin (rLTB) prepared from E. coli and P. patoris. J. Microbiol. Biotechnol. 20:550-557.
23. Mastroeni, P., J. A. Chabalgoity, S. J. Dunstan, D. J. Maskell, and G. Dougan. 2001. Salmonella: immune responses and vaccines. Vet. J. 161:132-164.
24. Matic, J. N., et al. 2009. Development of non-antibiotic-resistant, chromosomally based, constitutive and inducible expression systems for aroA-attenuated Salmonella enterica serovar Typhimurium. Infect. Immun. 77:1817-1826.
25. 32- Medited negative regulation of Salmonella pathogenicity island 1 expression. J. Bacteriol. 190: 6636-6645.
26. McSorley, S. J., and M. K. Jenkins. 2000. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infect. Immun. 68:3344-3348.
27. Mead, P. S., et al. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-624.
28. Moyle, P. M., R. P. McGeary, J. T. Blanchfield, and I. Toth. 2004. Mucosal immunization: adjuvants and delivery system. Curr. Drug Deliv. 1:385-396.
29. Nagarajan, A. G., et al. 2009. sopB of Salmonella enterica serovar Typhimurium is a potential DNA vaccine candidate in conjugation with live attenuated bacteria. Vaccine 27:2804-2811.
30. Norimatsu, M., V. Chance, G. Dougan, C. J. Howard, and B. Villarreal-Ramos. 2004. Live Salmonella enterica serovar Typhimurium (S. Typhimurium) elicit dendritic cell responses that differ from those induced by killed S. Typhimurium. Vet. Immunol. Immunopathol. 98:193-201.
31. O'Garra, A., and N. Arai. 2000. The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell. Biol. 10:542-550.
32. Ogra, P. L., H. Faden, and R. C. Welliver. 2001. Vaccination strategies for mucosal immune responses. Clin. Microbiol. Rev. 14:430-445.
33. Ola, T. O., and N. A. Williams. 2006. Protection of non-obese diabetic mice from autoimmune diabetes by Escherichia coli heat-labile enterotoxin B subunit. Immunology 117:262-270.
34. Olsen, S. J., L. C. MacKinnon, J. S. Goulding, N. H. Bean, and L. Slutsker. 2000. Surveillance for foodborne-disease outbreaks - United States, 1993-1997. MMWR CDC Surveill. Summ. 49:1-62.
35. Plückthun, A., and J. R. Knowles. 1987. The consequences of stepwise deletion from the signal-processing site of β-lactamase. J. Biol. Chem. 262: 3951-3957.
36. Qiao, X., et al. 2009. Recombinant porcine rotavirus VP4 and VP4-LTB expressed in Lactobacillus casei induced mucosal and systemic antibody responses in mice. BMC Microbiol. doi:10.1186/1471-2180-9-249.
37. Raveney, B. J., et al. 2008. The B subunit of Escherichia coli heat-labile enterotoxin inhibits Th1 but not Th17 cell responses in established experimental autoimmune uveoretinitis. Invest. Ophthalmol. Vis. Sci. 49:4008-4017.
38. Richards, C. M., A. T. Aman, T. R. Hirst, T. J. Hill, and N. A. Williams. 2001. Protective mucosal immunity to ocular herpes simplex virus type 1 infection in mice by using Escherichia coli heat-labile enterotoxin B subunit as an adjuvant. J. Virol. 75:1664-1671.
39. Roesler, U., P. Heller, K. H. Waldmann, U. Truyen, and A. Hensel. 2006. Immunization of sows in an integrated pig-breeding herd using a homologous inactivated Salmonella vaccine decreases the prevalence of Salmonella Typhimurium infection in the offspring. J. Vet. Med. B Infect. Dis. Public Health 53:224-228.
40. Roland, K. L., S. A. Tinge, K. P. Killeen, and S. K. Kochi. 2005. Recent advances in the development of live, attenuated bacterial vectors. Curr. Opin. Mol. Ther. 7:62-72.
41. Ruitenberg, K. M., J. R. Gilkerson, J. E. Wellington, D. N. Love, and J. M. Whalley. 2001. Equine herpesvirus 1 glycoprotein D expressed in Pichia pastoris is hyperglycosylated and elicits a protective immune response in the mouse model of EHV-1 disease. Virus Res. 79:125-135.
42. Sagt, C. M., et al. 2000. Introduction of an N-glycosylation site increases secretion of heterologous proteins in yeasts. Appl. Environ. Microbiol. 66: 4940-4944.
43. Spellberg, B., and J. E. Edwards, Jr. 2001. Type 1/type 2 immunity in infectious diseases. Clin. Infect. Dis. 32:76-102.
44. Summers, R. G., and J. R. Knowles. 1989. Illicit secretion of a cytoplasmic protein into the periplasm of Escherichia coli requires a signal peptide plus a portion of the cognate secreted protein. J. Biol. Chem. 264:20074-20081.
45. Sun, J. B., C. Czerkinsky, and J. Holmgren. 2010. Mucosally induced immunological tolerance, regulatory T cells and the adjuvant effect by cholera toxin B subunit. Scand. J. Immunol. 71:1-11.
46. Sun, J. B., J. Holmegren, and C. Czerkinsky. 1994. Cholera toxin B subunit: an efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. Proc. Natl. Acad. Sci. U. S. A. 91:10795-10799.
47. Swanenburg, M., H. A. P. Urlings, and J. M. A. Snijders. 2001. Salmonella in slaughter pigs: prevalence, serotypes and critical control points during slaughter in two slaughterhouses. Int. J. Food Microbiol. 70:243-254.
48. Vasserman, Y., and J. Pitcovski. 2006. Genetic detoxification and adjuvant-activity retention of Escherichia coli enterotoxin LT. Avian Pathol. 35:134-140.
49. Wagner, B., et al. 2004. Expression of the B subunit of the heat-labile enterotoxin of Escherichia coli in tobacco mosaic virus-infected Nicotiana benthamiana plants and its characterization as mucosal immunogen and adjuvant. J. Immunol. Methods 287:203-215.
50. Weening, E. H., et al. 2005. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in Mice. Infect. Immun. 73:3358-3366.
51. Weltzin, R., B. Guy, W. D. Thomas, Jr., P. J. Giannasca, and T. P. Monath. 2000. Parenteral adjuvant activities of Escherichia coli heat-labile toxin and its B subunit for immunization of mice against gastric Helicobacter pylori infection. Infect. Immun. 68:2775-2782.
52. Williams, N. A. 2000. Immune modulation by the cholera-like enterotoxins B-subunits: from adjuvant to immunotherapeutic. Int. J. Med. Microbiol. 290:447-453.
53. Yoon, H. A., et al. 2007. Correlation between the nature of immunity induced by different immunogens and the establishment of latent infection by wild-type pseudorabies virus. Res. Vet. Sci. 83:73-81.