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Comparative evaluation of the murine immune responses to Salmonella enterica serovars Enteritidis, Gallinarum and Typhimurium infection

Salmonella enterica serovars Enteritidis, Gallinarum 및 Typhimurium의 마우스 면역반응의 비교평가

  • Kim, Kiju (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University) ;
  • Kim, Dooree (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University) ;
  • Sun, Jisun (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University) ;
  • Park, Soyeon (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University) ;
  • Cho, Youngjae (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University) ;
  • Ko, Hyun-Jeong (College of Pharmacy, Kangwon National University) ;
  • Joo, Hong-Gu (College of Veterinary Medicine, Jeju National University) ;
  • Hahn, Tae-Wook (College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University)
  • 김기주 (강원대학교 수의과대학 및 동물의학종합연구소) ;
  • 김두리 (강원대학교 수의과대학 및 동물의학종합연구소) ;
  • 선지선 (강원대학교 수의과대학 및 동물의학종합연구소) ;
  • 박소연 (강원대학교 수의과대학 및 동물의학종합연구소) ;
  • 조영재 (강원대학교 수의과대학 및 동물의학종합연구소) ;
  • 고현정 (강원대학교 약학대학) ;
  • 주홍구 (제주대학교 수의과대학) ;
  • 한태욱 (강원대학교 수의과대학 및 동물의학종합연구소)
  • Received : 2013.02.28
  • Accepted : 2013.05.15
  • Published : 2013.06.30

Abstract

The study was carried out to evaluate and compare the immune responses in mice experimentally infected with either wild-type or isogenic mutants of Salmonella enterica serovars Enteritidis (SE), Salmonella Typhimurium (ST) and Gallinarum (SG). The mutant strains were constructed by allelic replacement of some virulence-associated genes in the wild-type strains. Seven-week-old female BALB/c mice were orally or intraperitoneally inoculated by injecting bacterial suspension. To evaluate the immune responses, enzyme-linked immunosorbent assay (ELISA) and enzyme-linked immunospot (ELISPOT) assay were conducted with serum and fecal samples. As a result, the mice group infected orally with the SE mutant strain showed the highest level of specific IgA-secreting splenocytes, compared to the other groups. The peritoneally injected groups showed the greater levels of IgG1 than the orally injected groups, which was in a good agreement with the previous studies. In addition, the mutant infected groups had the similar secretion levels of antibodies with the wild-type infected groups. These results demonstrated that the SE mutant strain elicited humoral immune response as much as wild-type, implying that it can be useful as a delivery vehicle as well as a candidate of a live attenuated vaccine.

Keywords

References

  1. Blondel CJ, Yang HJ, Castro B, Chiang S, Toro CS, Zaldivar M, Contreras I, Andrews-Polymenis HL, Santiviago CA. Contribution of the Type VI Secretion System Encoded in SPI-19 to Chicken Colonization by Salmonella enterica Serotypes Gallinarum and Enteritidis. PLoS One 2010, 5, e11724. https://doi.org/10.1371/journal.pone.0011724
  2. Chung Y, Cho J, Chang YS, Cho SH, Kang CY. Preventive and therapeutic effects of oral tolerance in a murine model of asthma. Immunobiology 2002, 206, 408-423. https://doi.org/10.1078/0171-2985-00190
  3. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000, 97, 6640-6645. https://doi.org/10.1073/pnas.120163297
  4. Dunstan SJ, Simmons CP, Strugnell RA. Comparison of the abilities of different attenuated Salmonella typhimurium strains to elicit humoral immune responses against a heterologous antigen. Infect Immun 1998, 66, 732-740.
  5. Gast RK, Stone HD, Holt PS. Evaluation of the efficacy of oil-emulsion bacterins for reducing fecal shedding of Salmonella enteritidis by laying hens. Avian Dis 1993, 37, 1085-1091. https://doi.org/10.2307/1591918
  6. Herberich E, Sikorski J, Hothorn T. A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS One 2010, 5, e9788. https://doi.org/10.1371/journal.pone.0009788
  7. Hindle Z, Chatfield SN, Phillimore J, Bentley M, Johnson J, Cosgrove CA, Ghaem-Maghami M, Sexton A, Khan M, Brennan FR, Everest P, Wu T, Pickard D, Holden DW, Dougan G, Griffin GE, House D, Santangelo JD, Khan SA, Shea JE, Feldman RG, Lewis DJ. Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun 2002, 70, 3457-3467. https://doi.org/10.1128/IAI.70.7.3457-3467.2002
  8. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ. Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog 2012, 8, e1002933. https://doi.org/10.1371/journal.ppat.1002933
  9. Kang HY, Srinivasan J, Curtiss R 3rd. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect Immun 2002, 70, 1739-1749. https://doi.org/10.1128/IAI.70.4.1739-1749.2002
  10. Kantele A, Arvilommi H, Iikkanen K, Savilahti E, Makela HP, Herzog C, Furer E, Kantele JM. Unique characteristics of the intestinal immune system as an inductive site after antigen reencounter. J Infect Dis 2005, 191, 312-317. https://doi.org/10.1086/426943
  11. Ko SY, Ko HJ, Chang WS, Park SH, Kweon MN, Kang CY. ${\alpha}$-Galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J Immunol 2005, 175, 3309-3317. https://doi.org/10.4049/jimmunol.175.5.3309
  12. Kotton CN, Lankowski AJ, Scott N, Sisul D, Chen LM, Raschke K, Borders G, Boaz M, Spentzou A, Galan JE, Hohmann EL. Safety and immunogenicity of attenuated Salmonella enterica serovar Typhimurium delivering an HIV-1 Gag antigen via the Salmonella Type III secretion system. Vaccine 2006, 24, 6216-6224. https://doi.org/10.1016/j.vaccine.2006.05.094
  13. Li Y, Wang S, Xin W, Scarpellini G, Shi Z, Gunn B, Roland KL, Curtiss R 3rd. A sopB deletion mutation enhances the immunogenicity and protective efficacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Infect Immun 2008, 76, 5238-5246. https://doi.org/10.1128/IAI.00720-08
  14. Muotiala A, Hovi M, Makela PH. Protective immunity in mouse salmonellosis: comparison of smooth and rough live and killed vaccines. Microb Pathog 1989, 6, 51-60. https://doi.org/10.1016/0882-4010(89)90007-7
  15. Nyeleti C, Cogan TA, Humphrey TJ. Effect of sunlight on the survival of Salmonella on surfaces. J Appl Microbiol 2004, 97, 617-620. https://doi.org/10.1111/j.1365-2672.2004.02335.x
  16. Piao HH, Tam VTM, Na HS, Kim HJ, Ryu PY, Kim SY, Rhee JH, Choy HE, Kim SW, Hong Y. Immunological responses induced by asd and wzy/asd mutant strains of Salmonella enterica serovar Typhimurium in BALB/c mice. J Microbiol 2010, 48, 486-495. https://doi.org/10.1007/s12275-010-0023-z
  17. Salerno-Goncalves R, Pasetti MF, Sztein MB. Characterization of $CD8^+$ effector T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J Immunol 2002, 169, 2196-2203. https://doi.org/10.4049/jimmunol.169.4.2196
  18. Seo KY, Han SJ, Cha HR, Seo SU, Song JH, Chung SH, Kweon MN. Eye mucosa: an efficient vaccine delivery route for inducing protective immunity. J Immunol 2010, 185, 3610-3619. https://doi.org/10.4049/jimmunol.1000680
  19. Shata MT, Reitz Jr MS, DeVico AL, Lewis GK, Hone DM. Mucosal and systemic HIV-1 Env-specific $CD8^+$ T-cells develop after intragastric vaccination with a Salmonella Env DNA vaccine vector. Vaccine 2002, 20, 623-629.
  20. Simon R, Tennant SM, Galen JE, Levine MM. Mouse models to assess the efficacy of non-typhoidal Salmonella vaccines: revisiting the role of host innate susceptibility and routes of challenge. Vaccine 2011, 29, 5094-5106. https://doi.org/10.1016/j.vaccine.2011.05.022
  21. Strindelius L, Wikingsson LD, Sjoholm I. Extracellular antigens from Salmonella enteritidis induce effective immune response in mice after oral vaccination. Infect Immun 2002, 70, 1434-1442. https://doi.org/10.1128/IAI.70.3.1434-1442.2002
  22. Tizard IR. Veterinary immunology: an introduction. 7th ed. pp. 145-153, Saunders, Philadelphia, 2004.
  23. Tsolis RM, Young GM, Solnick JV, Baumler AJ. From bench to bedside: stealth of enteroinvasive pathogens. Nat Rev Microbiol 2008, 6, 883-892. https://doi.org/10.1038/nrmicro2012