Oral immunization with attenuated Salmonella vaccine expressing Escherichia coli O157: H7 intimin gamma triggers both systemic and mucosal humoral immunity in mice

Microbiology and Immunology

Volumn 56, Issue 8, 2012, Pages 513-522

  Ferreira Oliveira, Aline ^a,b,c   Almeida Cardoso, Silvia ^b,c   Bruno dos Reis Almeida, Fausto ^b   Licursi de Oliveira, Leandro ^d   Pitondo Silva, André ^b   Gomes Soares, Sandro ^c   Seixas Hanna, Ebert ^b,c  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Invent Biotecnologia Ltd   (Brazil)

^d FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

Escherichia coli; Salmonella enterica Typhimurium; Vaccines

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTIMIN; INTIMIN GAMMA; LIVE VACCINE; RECOMBINANT VACCINE; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; EAE GENE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI O157; EXPRESSION VECTOR; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; MICROBIAL ATTENUATION; MOUSE; NONHUMAN; PROTEIN SYNTHESIS; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

ADHESINS, BACTERIAL; ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, BACTERIAL; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; FEMALE; GENETIC VECTORS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; PLASMIDS; SALMONELLA TYPHIMURIUM; VACCINES, ATTENUATED; VACCINES, SYNTHETIC;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MUS; SALMONELLA; SALMONELLA ENTERICA;

EID: 84864349515     PISSN: 03855600     EISSN: 13480421     Source Type: Journal    
DOI: 10.1111/j.1348-0421.2012.00477.x     Document Type: Article

References (49)

1. Goldwater P.N. (2007). Treatment and prevention of enterohemorrhagic Escherichia coli infection and hemolytic uremic syndrome. Expert Rev Anti Infect Ther 5(4): 653-63.
2. La Ragione R.M., Best A., Woodward M.J., Wales A.D. (2009). Escherichia coli O157:H7 colonization in small domestic ruminants. FEMS Microbiol Rev 33(2): 394-410.
3. Tarr P.I., Gordon C.A., Chandler W.L. (2005). Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365(9464): 1073-86.
4. Wong C.S., Jelacic S., Habeeb R.L., Watkins S.L., Tarr PI. (2000). The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 342(26): 1930-6.
5. Clarke S.C. (2001). Diarrhoeagenic Escherichia coli- an emerging problem? Diagn Microbiol Infect Dis 41(3): 93-8.
6. Judge N.A., Mason H.S., O'Brien A.D. (2004). Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect Immun 72(1): 168-75.
7. Agin T.S., Zhu C., Johnson L.A., Thate T.E., Yang Z., Boedeker E.C. (2005). Protection against hemorrhagic colitis in an animal model by oral immunization with isogeneic rabbit enteropathogenic Escherichia coli attenuated by truncating intimin. Infect Immun 73(10): 6608-19.
8. Berard N.C., Holley R.A., McAllister T.A., Ominski K.H., Wittenberg K.M., Bouchard K.S., Bouchard J.J., Krause D.O. (2009). Potential to reduce Escherichia coli shedding in cattle feces by using sainfoin (Onobrychis viciifolia) forage, tested in vitro and in vivo. Appl Environ Microbiol 75(4): 1074-9.
9. Smith D.R., Moxley R.A., Peterson R.E., Klopfenstein T.J., Erickson G.E., Bretschneider G., Berberov E.M., Clowser S. (2009). A two-dose regimen of a vaccine against type III secreted proteins reduced Escherichia coli O157:H7 colonization of the terminal rectum in beef cattle in commercial feedlots. Foodborne Pathog Dis 6(2): 155-61.
10. Khare S., Alali W., Zhang S., Hunter D., Pugh R., Fang F.C., Libby S.J., 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.
11. Gu J, Ning Y, Wang H, Xiao D, Tang B, Luo P, Cheng Y, Jiang M, Li N, Zou Q, Mao X. (2011). Vaccination of attenuated EIS-producing Salmonella induces protective immunity against enterohemorrhagic Escherichia coli in mice. Vaccine Jul 30. [Epub ahead of print.
12. Phillips A.D., Navabpour S., Hicks S., Dougan G., Wallis T., Frankel G. (2000). Enterohaemorrhagic Escherichia coli O157:H7 target Peyer's patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut 47: 377-81.
13. Ramachandran V., Brett K., Hornitzky M.A., Dowton M., Bettelheim K.A., Walker, M.J., Djordjevic S.P. (2003). Distribution of intimin subtypes among Escherichia coli isolates from ruminant and human sources. J Clin Microbiol 41: 5022-32.
14. Frankel G., Candy D.C., Everest P., and Dougan G. (1994). Characterization of the C-terminal domains of intimin-like proteins of enteropathogenic and enterohemorrhagic Escherichia coli, Citrobacter freundii, and Hafnia alvei. Infec Immun 62: 1835-42.
15. Frankel G., Candy D.C., Fabiani E., Adu-Bobie J., Gil S., Novakova M., Phillips A.D., and Dougan G. (1995). Molecular characterization of a carboxy-terminal eukaryotic-cell-binding domain of intimin from enteropathogenic Escherichia coli. Infect Immun 63: 4323-8.
16. Sinclair J.F., and O'Brien A.D. (2002). Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J Biol Chem 277: 2876-85.
17. Van Diemen P.M., Dziva F., Abu-Median A., Wallis T.S., van den Bosch H., Dougan G., Chanter N., Frankel G., Stevens M.P. (2007). Subunit vaccines based on intimin and Efa-1 polypeptides induce humoral immunity in cattle but do not protect against intestinal colonisation by enterohaemorrhagic Escherichia coli O157:H7 or O26:H. Vet Immunol Immunopathol 116(1-2): 47-58.
18. Gu J., Liu Y., Yu S., Wang H., Wang Q., Yi Y., Zhu F., Yu X.J., Zou Q., Mao X. (2009). Enterohemorrhagic Escherichia coli trivalent recombinant vaccine containing EspA, intimin and Stx2 induces strong humoral immune response and confers protection in mice. Microbes Infect 11(10-11): 835-41.
19. Li Y., Frey E., Mackenzie A.M., Finlay B.B. (2000). Human response to Escherichia coli O157:H7 infection: antibodies to secreted virulence factors. Infect Immun 68(9): 5090-5.
20. Oliveira A.F., Ferraz L.C., Brocchi M., Roque-Barreira M.C. (2007). Oral administration of a live attenuated Salmonella vaccine strain expressing the VapA protein induces protection against infection by Rhodococcus equi. Microbes Infect 9: 382-90.
21. Oliveira A.F., Ruas L.P., Cardoso S.A., Soares S.G., Roque-Barreira M.C. (2010). Vaccination of mice with Salmonella expressing VapA: mucosal and systemic Th1 responses provide protection against Rhodococcus equi infection. PlosOne 5(1): 1-12.
22. Shiau A.L., Chen C.C., Yo Y.T., Chu C.Y., Wang S.Y., Wu, C.L. (2005). Enhancement of humoral and cellular immune responses by an oral Salmonella choleraesuis vaccine expressing porcine prothymosin alpha. Vaccine 23: 5563-71.
23. Wyszyńska A., Raczko A., Lis M., Jagusztyn-Krynicka E.K. (2004). Oral immunization of chickens with avirulent Salmonella vaccine strain carrying C. jejuni 72Dz/92 cjaA gene elicits specific humoral immune response associated with protection against challenge with wild-type Campylobacter. Vaccine 22(11-12): 1379-1389.
24. Yang X., Hinnebusch B.J., Trunkle T., Bosio C.M., Suo Z., Tighe M., Harmsen A., Becker T., Crist K., Walters N., Avci R., Pascual D.W. (2007). Oral vaccination with Salmonella simultaneously expressing Yersinia pestis F1 and V antigens protects against bubonic and pneumonic plague. J Immunol 178(2): 1059-67.
25. Pasetti M.F., Levine M.M., Sztein M.B. (2003). Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 21: 401-18.
26. Kotton C.N., Hohmann E.L. (2004). Enteric pathogens as vaccine vectors for foreign antigen delivery. Infect Immun 72: 5535-47.
27. Hegazy W.A., Hensel M.(2012). Salmonella enterica as a vaccine carrier. Future Microbiol 7: 111-27.
28. Dougan G., Hormaeche C.E., Maskell D.J. (1987). Live oral Salmonella vaccines: potential use of attenuated strains as carriers of heterologous antigens to the immune system. Parasite Immunol 9: 151-60.
29. Covone M.G., Brocchi M., Palla E., Dias da Silveira W., Rappuoli R., Galeotti C.L. (1998). Levels of expression and immunogenicity of attenuated Salmonella enterica serovar Typhimurium strains expressing Escherichia coli mutant heat-labile enterotoxin. Infect Immun 66(1): 224-31.
30. Nakayama K., Kelly S.M., Curtiss 3rd R. (1988). Construction of an ASD +expression-cloning vector: Stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Nature Biotechnol 6: 693-697.
31. Galan J.E., Nakayama K., Curtiss 3rd 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(1): 29-35.
32. Curtiss R.III., and Kelly, S.M. (1987). Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun 55: 3035-43.
33. Maloy S.R., Stewart V.J., Taylor R.K. (1996). Generalized transduction with phage P22. In: Genetic Analysis of Pathogenic Bacteria. New York, Cold Spring Harbor Laboratory Press, pp. 473-92.
34. Dean-Nystrom E.A., Gansheroff L.J., Mills M., Moon H.W., O'Brien A.D. (2002). Vaccination of pregnant dams with intimin (O157) protects suckling piglets from Escherichia coli O157:H7 infection. Infect Immun 70(5): 2414-18.
35. Son W.G., Graham T.A., Gannon V.P. (2002). Immunological characterization of Escherichia coli O157:H7 intimin gamma1. Clin Diagn Lab Immunol 9(1): 46-53.
36. Diez-Gonzalez F., Callaway T.R., Kizoulis M.G., Russell J.B. (1998). Grain feeding and the dissemination of acid-resistant Escherichia coli from cattle. Science 281(5383): 1666-8.
37. Zhao T., Doyle M.P., Harmon B.G., Brown C.A., Mueller P.O., Parks A.H. (1998). Reduction of carriage of enterohemorrhagic Escherichia coli O157:H7 in cattle by inoculation with probiotic bacteria. J Clin Microbiol 36(3): 641-7.
38. Stevens M.P., van Diemen P.M., Dziva F., Jones P.W., Wallis T.S. (2002). Options for the control of enterohaemorrhagic Escherichia coli in ruminants. Microbiology 148(12): 3767-78.
39. Potter A.A., Klashinsky S., Li Y., Frey E., Townsend H., Rogan D., Erickson G., Hinkley S., Klopfenstein T., Moxley R.A., Smith D.R., Finlay B.B. (2004). Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 22(3-4): 362-9.
40. Van Donkersgoed J., Hancock D., Rogan D., S A.A. (2005). Escherichia coli O157:H7 vaccine field trial in 9 feedlots in Alberta and Saskatchewan. Can Vet J 46(8): 724-8.
41. Hackett J. (1990). Salmonella-based vaccines. Vaccine 8(1): 5-11.
42. Leary S.E.C., Griffin K.F., Garmory H.S., Williamson E.D., and Titball R.W. (1997). Expression of an F1/V fusion protein in attenuated Salmonella typhimurium and protection of mice against plague. Microb. Pathog 23: 167-79.
43. Garmory H.S., Griffin K.F., Brown K.A., Titball R.W. (2003). Oral immunization with live aroA attenuated Salmonella enterica serovar Typhimurium expressing the Yersinia pestis V antigen protects mice against plague. Vaccine 21: 3051-7.
44. Dunstan S.J., Simmons C.P., Strugnell R.A. (2003). In vitro and in vivo stability of recombinant plasmids in a vaccine strain of Salmonella enterica var. Typhimurium. FEMS Immunol Med Microbiol 37: 111-9.
45. Loureiro I., Frankel G., Adu-Bobie J., Dougan G., Trabulsi LR, Carneiro-Sampaio M.M. (1998). Human colostrum contains IgA antibodies reactive to enteropathogenic Escherichia coli virulence-associated proteins: intimin, BfpA, EspA, and EspB. J Pediatr Gastroenterol Nutr 27(2): 166-71.
46. Zapata-Quintanilla L.B., Tino-De-Franco M., Nunez S.P., Carbonare C.B., Vulcano A.B., Carbonare S.B. (2009). Seric and secretory antibodies reactive to alpha, beta and gamma intimins of Escherichia coli in healthy Brazilian adults. FEMS Immunol Med Microbiol 57(1): 32-9.
47. Conlan J.W., KuoLee R., Webb A., Perry M.B. (1999). Salmonella landau as a live vaccine against Escherichia coli O157:H7 investigated in a mouse model of intestinal colonization. Can J Microbiol 45(9): 723-31.
48. Sargeant J.M., Amezcua M.R., Rajic A., Waddell L. (2007). Pre-harvest interventions to reduce the shedding of E. coli O157 in the faeces of weaned domestic ruminants: a systematic review. Zoonoses Public Health. 54(6-7): 260-77.
49. Canadian Food Inspection Agency. In: "List of Veterinary Biological Products licensed in Canada". [Cited 24 Apr 2012] Available from URL: