Immunogenicity of a Salmonella Enteritidis mutant as vaccine candidate and its protective efficacy against salmonellosis in chickens

Veterinary Immunology and Immunopathology

Volumn 144, Issue 3-4, 2011, Pages 299-311

  Nandre, Rahul M ^a   Chaudhari, Atul A ^a   Matsuda, Kiku ^a   Lee, John Hwa ^a  

^a Chonbuk National University   (South Korea)

Author keywords

Chickens; Immune responses; Protection; Salmonellosis; Vaccination

Indexed keywords

CD45 ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; JOL 860; JOL 917; JOL 918; JOL 919; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG;

ANIMAL SALMONELLOSIS; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BIRD DISEASE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INVASION; CELLULAR IMMUNITY; CHICKEN; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DRUG EFFICACY; FEMALE; GENETIC MANIPULATION; HELPER CELL; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; INTESTINE SECRETION; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MUCOSAL IMMUNITY; NEWBORN; NONHUMAN; SALMONELLA ENTERITIDIS; SUSPENSION; T LYMPHOCYTE ACTIVATION; VACCINATION;

ANIMALS; CHICKENS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC ENGINEERING; IMMUNOGLOBULIN A, SECRETORY; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MACROPHAGES; POULTRY DISEASES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA VACCINES;

BACTERIA (MICROORGANISMS); GALLUS GALLUS; SALMONELLA ENTERITIDIS;

EID: 81555197071     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2011.08.015     Document Type: Article

References (82)

1. Adriaensen C., Greve H.D., Tian J.Q., Craeye S.D., Gubbels E., Eeckhaut V., Immerseel F.V., Ducatelle R., Kumar M., Hernalsteens J.P. A live Salmonella enterica serovar Enteritidis vaccine allows serological differentiation between vaccinated and infected animals. Infect. Immun. 2007, 75(5):2461-2468.
2. Altekruse S.F., Bauer N., Chanlongbutra A., DeSagun R., Naugle A., Schlosser W., Umholtz R., White P. Salmonella Enteritidis in broiler chickens, United States, 2000-2005. Emerg. Infect. Dis. 2006, 12:1848-1852.
3. Alvarez J., Sota M., Vivanco A.B., Perales I., Cisterna R., Rementeria A., Garaizar J. Development of a multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples. J. Clin. Microbiol. 2004, 42:1734-1738.
4. Babu U., Scott M., Myers M.J., Okamura M.D., Gaines D., Yancy H.F., Lillehoj H., Heckert R.A., Raybourne R.B. Effects of live attenuated and killed Salmonella vaccine on T-lymphocyte mediated immunity in laying hens. Vet. Immunol. Immunopathol. 2003, 91(1):39-44.
5. Babu U., Dalloul R.A., Okamura M., Lillehoj H.S., Xie H., Raybourne R.B., Gaines D., Heckert R.A. Salmonella Enteritidis clearance and immune responses in chickens following Salmonella vaccination and challenge. Vet. Immunol. Immunopathol. 2004, 101:251-257.
6. Badovinac V.P., Messingham K.A.N., Jabbari A., Haring J.S., Harty J.T. Accelerated CD8+ T-cell memory and prime-boost response after dendritic-cell vaccination. Nat. Med. 2005, 11(7):748-756.
7. Bäumler A.J., Hargis B.M., Tsolis R.M. Tracing the origins of Salmonella outbreaks. Science 2000, 287(5450):50-52.
8. Beal R.K., Powers C., Davison T.F., Barrow P.A., Smith A.L. Clearance of enteric Salmonella enterica serovar Typhimurium in chickens is independent of B-cell function. Infect. Immun. 2006, 74:1442-1444.
9. Beal R.K., Wigley P., Powers C., Barrow P.A., Smith A.L. Cross-reactive cellular and humoral immune responses to Salmonella enterica serovars Typhimurium and Enteritidis are associated with protection to heterologous re-challenge. Vet. Immunol. Immunopathol. 2006, 114:84-93.
10. Berndt A., Methner U. Gamma/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella Typhimurium strains. Vet. Immunol. Immunopathol. 2001, 78:143-161.
11. Berthelot-Herault F., Mompart F., Zygmunt M.S., Dubray G., Duchet-Suchaux M. Antibody responses in the serum and gut of chicken lines differing in ceacal carriage of Salmonella Enteritidis. Vet. Immunol. Immunopathol. 2003, 96:43-52.
12. Betancor L., Schelotto F., Fernandez M., Pereira M., Rial A., Chabalgoity J.A. An attenuated Salmonella Enteritidis strain derivative of the main genotype circulating in Uruguay is an effective vaccine for chickens. Vet. Microbiol. 2005, 25:81-89.
13. Bleackley R.C. Cytotoxic T lymphocytes. Fundamental Immunology 2008, 1079-1095. Lippincott Williams & Wikins, Philadelphia, PA, USA. 6th edition. W.E. Paul (Ed.).
14. Boddicker J.D., Jones B.D. Lon protease activity causes down-regulation of Salmonella pathogenicity island 1 invasion gene expression after infection of epithelial cells. Infect. Immun. 2004, 72:2002-2013.
15. Boyen F., Haesebrouck F., Maes D., Immerseel F.V., Ducatelle R., Pasmans F. Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. Vet. Microbiol. 2008, 130:1-19.
16. Brumme S., Arnold T., Sigmarsson H., Lehmann J., Scholz H.C., Hardt W.D., Hensel A., Truyen U., Roesler U. 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. 2007, 124:274-285.
17. Carvajal B.G., Methner U., Piepera J., Bernd A. Effects of Salmonella enterica serovar Enteritidis on cellular recruitment and cytokine gene expression in caecum of vaccinated chicken. Vaccine 2008, 26:5423-5433.
18. Chong C., Bost K.L., Clements J.D. Differential production of interleukin-12 mRNA by murine macrophages in response to viable or killed Salmonella spp. Infect. Immun. 1996, 64(4):1154-1160.
19. Cooper G.L., Venables L.M., Nicholas R.A.J., Cullen G.A., Hormaeche C.E. Vaccination of chickens with-chicken derived. Salmonella Enteritidis phage type 4 aroA-live oral Salmonella vaccines. Vaccine 1992, 10:247-254.
20. Crouch S.P., Kozlowski R., Slater K.J., Fletcher J. The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J. Immunol. Methods 1993, 160:81-88.
21. Curtiss R., Kelly S.M., Hassan J.O. Live oral avirulent Salmonella vaccines. Vet. Microbiol. 1993, 37:397-405.
22. Dutton R.W., Bradley L.M., Swain S.L. T cell memory. Annu. Rev. Immunol. 1998, 16:201-223.
23. Flanagan J., Bewley M. Protein quality control in bacterial cells: integrated networks of chaperones and ATP-dependent proteases. Genet. Eng. 2002, 24:17-47.
24. Gast R.K. Invited review. Serotype-specific and serotype independent strategies for pre-harvest control of food-borne Salmonella in poultry. Avian Dis. 2007, 51:817-828.
25. Gast R.K., Stone H.D., Holt P.S. Evaluation of the efficacy of oil-emulsion bacterin for reducing faecal shedding of Salmonella Enteritidis by laying hens. Avian Dis. 1993, 37(4):1085-1091.
26. Godinez I., Haneda T., Raffatellu M., George M.D., Paixao T.A., Rolan H.G., Santos R.L., Dandekar S., Tsolis R.M., Bäumler A.J. T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect. Immun. 2008, 76:2008-2017.
27. Gogal R.M., Ahmed S.A., Larsen C.T. Analysis of avian lymphocyte proliferation by a new, simple, nonradioactive assay (lympho-pro). Avian Dis. 1997, 41:714-725.
28. Hahn I. A contribution to consumer protection: TAD Salmonella vac1 E-a new live vaccine for chickens against Salmonella Enteritidis. Lohmann Information 2000, 23:29-32.
29. Higgins S.E., Erf G.F., Higgins J.P., Henderson S.N., Wolfenden A.D., Gaona-Ramirez G., Hargis B.M. Effect of probiotic treatment in broiler chicks on intestinal macrophage numbers and phagocytosis of Salmonella Enteritidis by abdominal exudate cells. Poult. Sci. 2007, 86:2315-2321.
30. Humphreys S., Rowley G., Stevenson A., Anjum M.F., Woodward M.J., Gilbert S., Kormanec J., Roberts M. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect. Immun. 2004, 72(8):4654-4661.
31. Humphrey T.J. Are happy chickens safer chickens? Poultry welfare and disease susceptibility. Braz. Poult. Sci. 2006, 47:379-391.
32. Hur J., Lee J.H. Immunization of pregnant sows with a novel virulence gene deleted live Salmonella vaccine and protection of their suckling piglets against salmonellosis. Vet. Microbiol. 2010, 143:270-276.
33. Janeway C.A., Travers P., Walport M., Sholmchick M. Immunobiology 2001, Garland Science.
34. Jones B.D., Falkow S. Salmonellosis: host immune responses and bacterial virulence determinants. Annu. Rev. Immunol. 1996, 14:533-561.
35. Jones M.A., Wigley P., Page K.L., Hulme S.D., Barrow P.A. Salmonella enterica serovar Gallinarum requires the Salmonella pathogenicity island 2 type III secretion system but not the Salmonella pathogenicity island 1 type III secretion system for virulence in chickens. Infect. Immun. 2001, 69:5471-5476.
36. Kim S.W., Moon K.H., Baik H.S., Kang H.Y., Kim S.K., Bahk J.D., Hur J., Lee J.H. 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 2009, 79:314-320.
37. Lebacq-Verheyden A.M., Vaerman J.P., Heremans J.F. A possible homologue of mammalian IgA in chicken serum and secretions. Immunology 1972, 22:165-175.
38. Lena S., Malin F., Ingvar S. Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine 2004, 22(27-28):3797-3808.
39. Leslie G.A., Martin L.N. Studies on the secretory immunologic system of fowl. Part 3. Serum and secretory IgA of the chicken. J. Immunol. 1973, 110:1-9.
40. Lindberg A.A., Robertsson J.A. Salmonella Typhimurium infection in calves: cell-mediated and humoral immune reactions before and after challenge with live virulent bacteria in calves given live or inactivated vaccines. Infect. Immun. 1983, 41(2):751-757.
41. Linde K., Hahn I., Vielitz E. Development of live Salmonella vaccines optimally attenuated for chickens. Lohmann Information 1997, 20:23-31.
42. Maloy S.R., Stewar V.J., Taylor R.K. Genetic Analysis of Pathogenic Bacteria 1996, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
43. Mastroeni P., Villarreal-Ramos B., Hormaeche C.E. Adoptive transfer of immunity to oral challenge with virulent Salmonella in innately susceptible BALB/c mice requires both immune serum and T cells. Infect. Immun. 1993, 61:3981-3984.
44. Mastroeni P., Chabalgoity J.A., Dunstan S.J., Maskell D.J., Dougan G. Salmonella: immune responses and vaccines. Vet. J. 2001, 161:132-164.
45. Matsuda K., Chaudhari A.A., Kim S.W., Lee K.M., Lee J.H. Physiology, pathogenicity and immunogenicity of lon and/or cpxR deleted mutants of Salmonella Gallinarum as vaccine candidates for fowl typhoid. Vet. Res. 2010, 41:59.
46. Matsui H., Suzuki M., Isshiki Y., Kodama C., Eguchi M., Kikuchi Y., Motokawa K., Takaya A., Tomoyasu T., Yamamoto T. Oral immunization with ATP-dependent protease-deficient mutants protects mice against subsequent oral challenge with virulent Salmonella enterica serovar Typhimurium. Infect. Immun. 2003, 71:30-39.
47. Meyer H., Koch H., Methner U., Steinbach G. Vaccines in salmonellosis control in animals. Zentralblatt Bakteriologie 1993, 278:407-415.
48. Mittrucker H.W., Kohler A., Kaufmann S.H. Characterization of the murine T lymphocyte response to Salmonella enterica serovar Typhimurium infection. Infect. Immun. 2002, 70:199-203.
49. Okamura M., Tachizaki H., Kubo T., Kikuchi S., Suzuki A., Takehara K., Nakamura M. Comparative evaluation of a bivalent killed Salmonella vaccine to prevent egg contamination with Salmonella enterica serovars Enteritidis, Typhimurium, and Gallinarum biovar Pullorum, using 4 different challenge models. Vaccine 2007, 25:4837-4844.
50. Pantin-Jackwood M.J., Brown T.P., Huff G.R. Proventriculitis in broiler chickens: immunohistochemical characterization of the lymphocytes infiltrating the proventricular glands. Vet. Pathol. 2004, 41:641-648.
51. Pirofski L.A., Casadevall A. Use of licensed vaccines for active immunization of the immunocompromised host. Clin. Microbiol. Rev. 1998, 11(1):1-26.
52. Porter R.E., Holt P.S. Use of a pilocarpine-based lavage procedure to study secretory immunoglobulin concentration in the alimentary tract of White Leghorn chickens. Avian Dis. 1992, 36(3):529-536.
53. Qureshi M.A., Dietert R.R., Bacon L.D. Genetic variation in the recruitment and activation of chicken peritoneal macrophages. Proc. Soc. Exp. Biol. Med. 1986, 181:560-568.
54. Rafael A.C.P.F., Jacqueline B.P., Mariana D.S., Adriana M.A., Angelo B. Control of Salmonella Enteritidis and Salmonella Gallinarum in birds by using live vaccine candidate containing attenuated Salmonella Gallinarum mutant strain. Vaccine 2010, 28(16):2853-2859.
55. Rana N., Kulshreshtha R.C. Cell-mediated and humoral immune responses to a virulent plasmid-cured mutant strain of Salmonella enterica serotype Gallinarum in broiler chickens. Vet. Microbiol. 2006, 115:156-162.
56. Rodrigue D.C., Tauxe R.V., Rowe B. International increase in Salmonella Enteritidis: a new pandemic?. Epidemiol. Infect. 1990, 105:21-27.
57. Roesler U., Heller P., Waldmann K.H., Truyen U., Hensel A. 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. 2006, 53:224-228.
58. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York. 2nd edition.
59. Saskia V.H., Arjan J.W.H., Mari A.S., Johanna M.J.R. Immunological and gene expression responses to a Salmonella infection in the chicken intestine. Vet. Res. 2007, 38:51-63.
60. Scharek L., Tedin K. The porcine immune system-differences compared to man and mouse possible consequences for infections by Salmonella enterica serovars. Berl. Münch. Tierärztl. Wochenschr. 2007, 120:347-354.
61. Schoemaker J., Gayda R., Markovitz A. Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death. J. Bacteriol. 1984, 158:551-561.
62. Schmidt R., Decatur A., Rather P., Moran C., Losick R. Bacillus Subtilis lon protease prevents inappropriate transcription of genes under the control of the sporulation transcription factor sigma G. J. Bacteriol. 1994, 176:6528-6537.
63. Silva E.N., Snoeyenbos G.H., Weinack O.M., Smyser C.F. Studies on the use of 9R strain of Salmonella Gallinarum as a vaccine in chickens. Avian Dis. 1981, 25:38-52.
64. Singh, B.R., 2005. Project CGP III-327 Report. Development of double defined deletion mutant vaccine for control of Salmonella Abortusequi infection in equines. IVRI, Izatnagar, India.
65. Stewart B., Enos-Berlage J., McCarter L. The lonS gene regulates swarmer cell differentiation of Vibrio Parahaemolyticus. J. Bacteriol. 1997, 179:107-114.
66. Stocker B.A.D., Hoiseth S.K., Smith B.P. Aromatic dependent Salmonella sp. as live vaccine in mice and calves. Dev. Biol. Standard. 1983, 53:47-59.
67. Takaya A., Kubota Y., Isogai E., Yamamoto T. Degradation of the HilC and HilD regulator proteins by ATP dependent Lon protease leads to downregulation of Salmonella pathogenicity island 1 gene expression. Mol. Microbiol. 2005, 55(3):839-852.
68. Takaya A., Suzuki M., Matsui H., Tomoyasu T., Sashinami H., Nakane A., Yamamoto T. Lon, a stress-induced ATP-dependent protease, is critically important for systemic Salmonella enterica serovar Typhimurium infection of mice. Infect. Immun. 2003, 71:690-696.
69. Takaya A., Tomoyasu T., Tokumitsu A., Morioka M., Yamamoto T. The ATP-dependent lon protease of Salmonella enterica serovar Typhimurium regulates invasion and expression of genes carried on Salmonella pathogenicity island 1. J. Bacteriol. 2002, 184:224-232.
70. Tan S., Gyles C.L., Wilkie B.N. Evaluation of an aroA mutant Salmonella Typhimurium vaccine in chickens using modified semisolid Rappaport Vassiliadis medium to monitor fecal shedding. Vet. Microbiol. 1997, 54:247-254.
71. Tchilian E.Z., Gil J., Navarro M.L., Fernandez-Cruz E., Chapel H., Misbah S., Ferry B., Renz H., Schwinzer R., Beverley P.C.L. Unusual case presentations associated with the CD45 C77G polymorphism. Clin. Exp. Immunol. 2006, 146(3):448-454.
72. Titball R.W. Vaccines against intracellular bacterial pathogens. Drug. Discov. Today 2008, 13:596-600.
73. Torres-Cabassa A., Gottesman S. Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J. Bacteriol. 1987, 169:981-989.
74. Toshi N., Yukio K. Induction of specific CD8+ T cells against intracellular bacteria by CD8+ T-cell-oriented immunization approaches. J. Biomed. Biotechnol. 2010, 2010:764542.
75. Trebichavsky I., Splichalova A., Rychlik I., Hojna H., Muneta Y., Mori Y., Splichal I. Attenuated aroA Salmonella enterica serovar Typhimurium does not induce inflammatory response and early protection of gnotobiotic pigs against parental virulent LT2 strain. Vaccine 2006, 24:4285-4289.
76. Vainio O., Lassila O. Chicken T cells: differentiation antigens and cell-cell interactions. Crit. Rev. Poult. Biol. 1989, 2:97-102.
77. Van Immerseel F., De Buck J., De Smet I., Mast J., Haesebrouck F., Ducatelle R. The effect of vaccination with a Salmonella Enteritidis aroA mutant on early cellular responses in caecal lamina propria of newly-hatched chickens. Vaccine 2002, 20:3034-3041.
78. Vielitz E., Conrad C., Voss M., Löhren U., Bachmeier J., Hahn I. Immunization against Salmonella-infections using live and inactivated vaccine preparations. Deutsche Tierärztliche Wochenschrift 1992, 99:483-485.
79. Wigley P., Hulme S., Powers C., Beal R., Smith A., Barrow P. Oral infection with the Salmonella enterica serovar Gallinarum 9R attenuated live vaccine as a model to characterise immunity to fowl typhoid in the chicken. BMC Vet. Res. 2005, 1:2.
80. Wolfe A.J., Parikh N., Lima B.P., Zemaitaitis B. Signal integration by the two-competent signal transduction response regulator CpxR. J. Bacteiol. 2008, 190(7):2314-2322.
81. Wright R., Stephens C., Zweiger G., Shapiro L., Alley M. Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev. 1996, 10:1532-1542.
82. Xie D., Wang Z.X., Dong Y.L., Cao J., Wang J.F., Chen J.L., Chen Y.X. Effects of monochromatic light on immune response of broilers. Poult. Sci. 2008, 87(8):1535-1539.