Invasive behavior of Campylobacter jejuni in immunosuppressed chicken

Mahdi M. Vaezirad, A.M. Keestra-Gounder, Marcel R. de Zoete, Miriam G. Koene, Jaap A. Wagenaar, Jos P.M. van Putten

Research output: Contribution to journalArticleAcademicpeer-review

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Abstract

Campylobacter jejuni is a predominant cause of gastroenteritis in humans but rather harmless in chickens. The basis of this difference is unknown. We investigated the effect of the chicken immune defense on the behavior of C. jejuni using glucocorticoid (GC)-treated and mock-treated 17-day old Ross 308 chicken bearing in mind that GCs have immunosuppressive effects and dampen the innate immune response. The effect of GC administration on the behavior of C. jejuni was compared with that on infection with Salmonella Enteritidis to address possible microbe-associated differences. Our results revealed that GC treatment fastened the intestinal colonization of C. jejuni (p <0.001) and enhanced its dissemination to the liver (p = 0.007). The effect of GC on intestinal colonization of S. Enteritidis was less pronounced (p = 0.033) but GC did speed up the spread of this pathogen to the liver (p <0.001). Cytokine transcript analysis showed an up to 30-fold reduction in baseline levels of IL-8 mRNA in the cecal (but not spleen) tissue at Day 1 after GC treatment (p <0.005). Challenge with C. jejuni strongly increased intestinal IL-8, IL-6, and iNOS transcript levels in the non-GC treated animals but not in the GC-treated birds (P <0.005). In vitro assays with chicken macrophages showed that GC dampened the TLR agonist- and C. jejuni induced-inflammatory gene transcription and production of nitric oxide (P <0.005). Together, the results support the hypothesis that C. jejuni has the intrinsic ability to invade chicken tissue and that an effective innate immune response may limit its invasive behavior.
Original languageEnglish
Pages (from-to)248-260
JournalVirulence
Volume8
Issue number3
DOIs
Publication statusPublished - 2017

Fingerprint

Campylobacter jejuni
Glucocorticoids
Chickens
Salmonella enteritidis
Interleukin-8
Innate Immunity
Aptitude
Liver
Gastroenteritis
Immunosuppressive Agents
Birds
Interleukin-6
Nitric Oxide
Spleen
Macrophages
Cytokines
Messenger RNA
Infection

Keywords

  • Campylobacter
  • chicken
  • colonization
  • glucocorticoids
  • innate immunity
  • invasion
  • Toll-like receptor

Cite this

Vaezirad, M. M., Keestra-Gounder, A. M., de Zoete, M. R., Koene, M. G., Wagenaar, J. A., & van Putten, J. P. M. (2017). Invasive behavior of Campylobacter jejuni in immunosuppressed chicken. Virulence, 8(3), 248-260. https://doi.org/10.1080/21505594.2016.1221559
Vaezirad, Mahdi M. ; Keestra-Gounder, A.M. ; de Zoete, Marcel R. ; Koene, Miriam G. ; Wagenaar, Jaap A. ; van Putten, Jos P.M. / Invasive behavior of Campylobacter jejuni in immunosuppressed chicken. In: Virulence. 2017 ; Vol. 8, No. 3. pp. 248-260.
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Vaezirad, MM, Keestra-Gounder, AM, de Zoete, MR, Koene, MG, Wagenaar, JA & van Putten, JPM 2017, 'Invasive behavior of Campylobacter jejuni in immunosuppressed chicken' Virulence, vol. 8, no. 3, pp. 248-260. https://doi.org/10.1080/21505594.2016.1221559

Invasive behavior of Campylobacter jejuni in immunosuppressed chicken. / Vaezirad, Mahdi M.; Keestra-Gounder, A.M.; de Zoete, Marcel R.; Koene, Miriam G.; Wagenaar, Jaap A.; van Putten, Jos P.M.

In: Virulence, Vol. 8, No. 3, 2017, p. 248-260.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Vaezirad, Mahdi M.

AU - Keestra-Gounder, A.M.

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AU - Wagenaar, Jaap A.

AU - van Putten, Jos P.M.

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AB - Campylobacter jejuni is a predominant cause of gastroenteritis in humans but rather harmless in chickens. The basis of this difference is unknown. We investigated the effect of the chicken immune defense on the behavior of C. jejuni using glucocorticoid (GC)-treated and mock-treated 17-day old Ross 308 chicken bearing in mind that GCs have immunosuppressive effects and dampen the innate immune response. The effect of GC administration on the behavior of C. jejuni was compared with that on infection with Salmonella Enteritidis to address possible microbe-associated differences. Our results revealed that GC treatment fastened the intestinal colonization of C. jejuni (p <0.001) and enhanced its dissemination to the liver (p = 0.007). The effect of GC on intestinal colonization of S. Enteritidis was less pronounced (p = 0.033) but GC did speed up the spread of this pathogen to the liver (p <0.001). Cytokine transcript analysis showed an up to 30-fold reduction in baseline levels of IL-8 mRNA in the cecal (but not spleen) tissue at Day 1 after GC treatment (p <0.005). Challenge with C. jejuni strongly increased intestinal IL-8, IL-6, and iNOS transcript levels in the non-GC treated animals but not in the GC-treated birds (P <0.005). In vitro assays with chicken macrophages showed that GC dampened the TLR agonist- and C. jejuni induced-inflammatory gene transcription and production of nitric oxide (P <0.005). Together, the results support the hypothesis that C. jejuni has the intrinsic ability to invade chicken tissue and that an effective innate immune response may limit its invasive behavior.

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KW - chicken

KW - colonization

KW - glucocorticoids

KW - innate immunity

KW - invasion

KW - Toll-like receptor

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Vaezirad MM, Keestra-Gounder AM, de Zoete MR, Koene MG, Wagenaar JA, van Putten JPM. Invasive behavior of Campylobacter jejuni in immunosuppressed chicken. Virulence. 2017;8(3):248-260. https://doi.org/10.1080/21505594.2016.1221559