Comparative in vivo infection models yield insights on early host immune response to Campylobacter in chickens

Abstract

Salmonella typhimurium and Campylobacter jejuni pose significant risks to human health and poultry are a major vector for infection. Comparative in vivo infection models were performed to compare the avian host immune response to both bacterial species. Forty-five commercial broiler chickens were orally challenged with either C. jejuni or S. typhimurium whilst 60 similar control birds were mock challenged in parallel. Birds were sacrificed at 0, 6, 20 and 48 h post-infection and cloacal swabs, blood and tissue samples taken. Peripheral blood leukocytes were isolated for flow cytometric analyses and RNA was extracted for gene expression profiling. Colonisation patterns were markedly different between the two bacterial species, with systemic colonisation of Campylobacter outside the gastrointestinal tract. Salmonella infection induced significant changes in circulating heterophil and monocyte/macrophage populations, whilst Campylobacter infection had no effect on the heterophil numbers but caused a significant early increase in circulating monocytes/macrophages. Toll-like receptor 1 (TLR1) gene expression was decreased, and avian beta-defensin (AvBD) gene expression (AvBD3, AvBD10 and AvBD12) was significantly increased in response to Salmonella infection (P < 0.05). In contrast, Campylobacter infection induced increased TLR21 gene expression but significantly reduced expression of seven antimicrobial peptide (AMP) genes (AvBD3, AvBD4, AvBD8, AvBD13, AvBD14, CTHL2 and CTHL3; P < 0.05). Considered together, microbiological, cellular and gene expression profiles indicate that the innate immune system responds differently to Salmonella and to Campylobacter infection. Furthermore, reduction in the expression of AMPs may play a role in the persistence of high level colonisation of the host by Campylobacter.

Different effect of doxycycline and enrofloxacin on cathelicidin-3 mRNA expression in chickens with or without probiotics supplementation

“…Thus they do not provoke changes in the expression levels of CATH3 antimicrobial peptide. In contrast, the pathogenic bacteria such as Salmonella enterica serovar Typhimurium up-regulated CATH3 mRNA (Akbari et al, 2008;Meade et al, 2009). These changes were neutralised by probiotics administration, an effect attributed to their properties for inhibition of Salmonella enterica and of its adhesion to the intestinal cells of the host (Akbari et al, 2008;Meade et al, 2009).…”

“…In contrast, the pathogenic bacteria such as Salmonella enterica serovar Typhimurium up-regulated CATH3 mRNA (Akbari et al, 2008;Meade et al, 2009). These changes were neutralised by probiotics administration, an effect attributed to their properties for inhibition of Salmonella enterica and of its adhesion to the intestinal cells of the host (Akbari et al, 2008;Meade et al, 2009). Microorganisms such as Campylobacter jejuni provoke downregulation of CATH3 mRNA and -defensins which leads to successful colonisation of the gastro-intestinal tract of chickens by this pathogen (Meade et al, 2009).…”

“…These changes were neutralised by probiotics administration, an effect attributed to their properties for inhibition of Salmonella enterica and of its adhesion to the intestinal cells of the host (Akbari et al, 2008;Meade et al, 2009). Microorganisms such as Campylobacter jejuni provoke downregulation of CATH3 mRNA and -defensins which leads to successful colonisation of the gastro-intestinal tract of chickens by this pathogen (Meade et al, 2009). Co-administration of probiotic strains L. brevis, L. plantarum and L. bulgaricus with broad spectrum antibiotics such as enrofloxacin and doxycycline does not have a negative impact on innate immunity as determined by CATH3 mRNA levels.…”

Integrated Genomic Approaches to Enhance Genetic Resistance in Chickens

“…Because antimicrobial peptides are an important component of the innate immune response to pathogens, the rapid expression of avian b-defensin (AvBD) genes after infection is likely important in resistance. Expression of AvBD genes in leukocytes was increased significantly within 6 h in response to Salmonella Typhimurium infection of broilers (100). Inbred chicken lines differing in cecal bacterial carriage showed marked differences in expression of AvBD1 and AvBD2, with higher expression in the line with the lower bacterial carriage (91).…”

Strong Concordance Between Transcriptomic Patterns of Spleen and Peripheral Blood Leukocytes in Response to Avian Pathogenic Escherichia coli Infection

“…This difference may demonstrate that tissues respond at different times to infection, or may reflect differences in the flow of cascading signals over time and between tissues. Time-course experiments of other bacterial infections have shown increasing rates of colonization over the first 48 hr after infection (16). Many reports of spleen colonization of APEC are measured 48 hr or more after infection (4,6,17), whereas APEC has been shown to gain access to the bloodstream within hours after intra-air sac inoculation (20,24).…”