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Transcriptional responses of PBMC in psychosocially stressed animals indicate an alerting of the immune system in female but not in castrated male pigs.

Oster M, Muráni E, Ponsuksili S, D'Eath RB, Turner SP, Evans G, Thölking L, Kurt E, Klont R, Foury A, Mormède P, Wimmers K - BMC Genomics (2014)

Bottom Line: Relevant stress-dependent alterations were found only between female samples, but not between castrated male samples.Molecular routes related to TREM 1 signalling, dendritic cell maturation, IL-6 signalling, Toll-like receptor signalling, and IL-8 signalling were increased in high stressed females compared to low stressed females.This indicates a launch of immune effector molecules as a direct response.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute for Farm Animal Biology (FBN), Institute for Genome Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany. wimmers@fbn-dummerstorf.de.

ABSTRACT

Background: Brain and immune system are linked in a bi-directional manner. To date, it remained largely unknown why immune components become suppressed, enhanced, or remain unaffected in relation to psychosocial stress. Therefore, we mixed unfamiliar pigs with different levels of aggressiveness. We separated castrated male and female pigs into psychosocially high- and low- stressed animals by skin lesions, plasma cortisol level, and creatine kinase activity obtained from agonistic behaviour associated with regrouping. Peripheral blood mononuclear cells (PBMC) were collected post-mortem and differential gene expression was assessed using the Affymetrix platform (n = 16).

Results: Relevant stress-dependent alterations were found only between female samples, but not between castrated male samples. Molecular routes related to TREM 1 signalling, dendritic cell maturation, IL-6 signalling, Toll-like receptor signalling, and IL-8 signalling were increased in high stressed females compared to low stressed females. This indicates a launch of immune effector molecules as a direct response. According to the shifts of transcripts encoding cell surface receptors (e.g. CD14, TLR2, TLR4, TREM1) the study highlights processes acting on pattern recognition, inflammation, and cell-cell communication.

Conclusions: The transcriptional response partly affected the degree of 'stress responsiveness', indicating that the high stressed females altered their signal transduction due to potential infections and injuries while fighting.

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Related in: MedlinePlus

Experimental design used to analyse transcriptional responses due to different levels of psychosocial stress. The origin and composition of the profiled sampling groups is shown regarding their parental genetics, affiliation to skin lesion group, and resulted stress levels. LR - Landrace; LW – Large White; D – Duroc; P – Pietrain; H – High lesion score; L – Low lesion score; HS – High stress; LS – Low stress.
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Fig1: Experimental design used to analyse transcriptional responses due to different levels of psychosocial stress. The origin and composition of the profiled sampling groups is shown regarding their parental genetics, affiliation to skin lesion group, and resulted stress levels. LR - Landrace; LW – Large White; D – Duroc; P – Pietrain; H – High lesion score; L – Low lesion score; HS – High stress; LS – Low stress.

Mentions: In order to identify pigs differing in their stress level, a mixing experiment was conducted which was described recently in detail by D’Eath et al.[5]. Animal care and tissue collection procedures followed the guidelines of the German Law of Animal Protection, and the experimental protocol was approved by the Institutional Animal Care and Use Committee (IACUC) of the Leibniz Institute for Farm Animal Biology (FBN). This study was based on phenotypic records and gene expression profiling done with castrated male and female finishing pigs. In fact, progeny (n = 271) derived from a crossbreed including Landrace, Large White, Duroc (sows) and Pietrain (boars) was bred (Figure 1) and reared commercially on slatted floors. Male animals were castrated at 4 days post-natum. At approximately 10 weeks of age, the pigs were assigned to new single-sex groups of eight or ten animals (Figure 1: MIXING 1). These groups were balanced for weight and unfamiliarity in order to minimize these determinants of aggressiveness in pigs[19, 20]. Thereby, standardized weight and unfamiliarity did likely contribute to uncover aggressive behaviour to a larger extent. Animals were housed in standardized conditions. Immediately before and at 24 hrs after mixing, skin lesions were counted. Thereby, the body was divided into front (head, neck, shoulder, and front legs), middle (flanks, and back) and rear (rump, hind legs, and tail) sections[9]. Changes in skin lesions pre- to post-mixing reflect the involvement in fighting and aggressive behaviour[9, 10]. For each mixing group the cut-off criteria for the total lesion score was individually calculated (pre- to post-mixing). Thereby, also the distribution of skin lesion scores in each group was estimated. Half of the pigs were designated as high skin lesion score group (H) (those with front lesions above average; mean in H: 60.6 ± 23.4) and the remaining half was designated as low skin lesion score group (L) (those with front lesions below average, mean in L: 27.5 ± 12.4), respectively. The first mixing revealed a mean total skin lesion score (mean ± SEM) of 140.9 ± 57.5 in H animals and of 98.6 ± 39.2 in L animals, respectively. The pigs remained in the established mixing groups until they reached 110 kg live weight corresponding to approximately 27 weeks of age. Here, the pigs were assigned to mixing groups based on their previous skin lesion score group (Figure 1: MIXING 2), as they were loaded onto a vehicle for a 270 km transport to the abattoir. In detail, single-sex groups were built by mixing four pigs from one rearing group and four pigs from another rearing group. Thus, H pigs were mixed with H pigs resulting in a HH batch, H pigs were mixed with L pigs resulting in a HL batch, or L pigs were mixed with L pigs resulting in a LL batch. Skin lesions were counted before mixing and after slaughter on the carcass and the skin lesion score was calculated (Table 1). In all these batches animals with high and low lesion scores were observed. Apparently, high and low levels of psychosocial stress (HS – High stress; LS – Low stress) were induced independently from the initial mixing group. In detail, the second mixing revealed a skin lesion score (mean ± SEM) on HS and LS animals originated from the HH mixing of 164.3 ± 42.7 and 34.5 ± 17.6, respectively, and a skin lesion score on HS and LS animals originating from LL mixing of 99.8 ± 44.1 and 24.0 ± 4.1, respectively. In order to limit bias due to circadian fluctuation of cortisol levels, pigs were slaughtered between 0600 and 0800 h in the next morning. Pigs were moved from lairage pens and stunned by means of CO2 gas and exsanguinated. Trunk blood was collected and stored on ice. Based on parameters of stress levels (Table 1), those animals were selected for gene expression profiling which represented extremes within mixing groups (Figure 1: ANALYSIS). Overall, the experimental design covered four slaughter days. Animals selected for microarray analyses were balanced for slaughter day. Each sampling group was represented by 4 castrates and 4 females.Figure 1


Transcriptional responses of PBMC in psychosocially stressed animals indicate an alerting of the immune system in female but not in castrated male pigs.

Oster M, Muráni E, Ponsuksili S, D'Eath RB, Turner SP, Evans G, Thölking L, Kurt E, Klont R, Foury A, Mormède P, Wimmers K - BMC Genomics (2014)

Experimental design used to analyse transcriptional responses due to different levels of psychosocial stress. The origin and composition of the profiled sampling groups is shown regarding their parental genetics, affiliation to skin lesion group, and resulted stress levels. LR - Landrace; LW – Large White; D – Duroc; P – Pietrain; H – High lesion score; L – Low lesion score; HS – High stress; LS – Low stress.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4233077&req=5

Fig1: Experimental design used to analyse transcriptional responses due to different levels of psychosocial stress. The origin and composition of the profiled sampling groups is shown regarding their parental genetics, affiliation to skin lesion group, and resulted stress levels. LR - Landrace; LW – Large White; D – Duroc; P – Pietrain; H – High lesion score; L – Low lesion score; HS – High stress; LS – Low stress.
Mentions: In order to identify pigs differing in their stress level, a mixing experiment was conducted which was described recently in detail by D’Eath et al.[5]. Animal care and tissue collection procedures followed the guidelines of the German Law of Animal Protection, and the experimental protocol was approved by the Institutional Animal Care and Use Committee (IACUC) of the Leibniz Institute for Farm Animal Biology (FBN). This study was based on phenotypic records and gene expression profiling done with castrated male and female finishing pigs. In fact, progeny (n = 271) derived from a crossbreed including Landrace, Large White, Duroc (sows) and Pietrain (boars) was bred (Figure 1) and reared commercially on slatted floors. Male animals were castrated at 4 days post-natum. At approximately 10 weeks of age, the pigs were assigned to new single-sex groups of eight or ten animals (Figure 1: MIXING 1). These groups were balanced for weight and unfamiliarity in order to minimize these determinants of aggressiveness in pigs[19, 20]. Thereby, standardized weight and unfamiliarity did likely contribute to uncover aggressive behaviour to a larger extent. Animals were housed in standardized conditions. Immediately before and at 24 hrs after mixing, skin lesions were counted. Thereby, the body was divided into front (head, neck, shoulder, and front legs), middle (flanks, and back) and rear (rump, hind legs, and tail) sections[9]. Changes in skin lesions pre- to post-mixing reflect the involvement in fighting and aggressive behaviour[9, 10]. For each mixing group the cut-off criteria for the total lesion score was individually calculated (pre- to post-mixing). Thereby, also the distribution of skin lesion scores in each group was estimated. Half of the pigs were designated as high skin lesion score group (H) (those with front lesions above average; mean in H: 60.6 ± 23.4) and the remaining half was designated as low skin lesion score group (L) (those with front lesions below average, mean in L: 27.5 ± 12.4), respectively. The first mixing revealed a mean total skin lesion score (mean ± SEM) of 140.9 ± 57.5 in H animals and of 98.6 ± 39.2 in L animals, respectively. The pigs remained in the established mixing groups until they reached 110 kg live weight corresponding to approximately 27 weeks of age. Here, the pigs were assigned to mixing groups based on their previous skin lesion score group (Figure 1: MIXING 2), as they were loaded onto a vehicle for a 270 km transport to the abattoir. In detail, single-sex groups were built by mixing four pigs from one rearing group and four pigs from another rearing group. Thus, H pigs were mixed with H pigs resulting in a HH batch, H pigs were mixed with L pigs resulting in a HL batch, or L pigs were mixed with L pigs resulting in a LL batch. Skin lesions were counted before mixing and after slaughter on the carcass and the skin lesion score was calculated (Table 1). In all these batches animals with high and low lesion scores were observed. Apparently, high and low levels of psychosocial stress (HS – High stress; LS – Low stress) were induced independently from the initial mixing group. In detail, the second mixing revealed a skin lesion score (mean ± SEM) on HS and LS animals originated from the HH mixing of 164.3 ± 42.7 and 34.5 ± 17.6, respectively, and a skin lesion score on HS and LS animals originating from LL mixing of 99.8 ± 44.1 and 24.0 ± 4.1, respectively. In order to limit bias due to circadian fluctuation of cortisol levels, pigs were slaughtered between 0600 and 0800 h in the next morning. Pigs were moved from lairage pens and stunned by means of CO2 gas and exsanguinated. Trunk blood was collected and stored on ice. Based on parameters of stress levels (Table 1), those animals were selected for gene expression profiling which represented extremes within mixing groups (Figure 1: ANALYSIS). Overall, the experimental design covered four slaughter days. Animals selected for microarray analyses were balanced for slaughter day. Each sampling group was represented by 4 castrates and 4 females.Figure 1

Bottom Line: Relevant stress-dependent alterations were found only between female samples, but not between castrated male samples.Molecular routes related to TREM 1 signalling, dendritic cell maturation, IL-6 signalling, Toll-like receptor signalling, and IL-8 signalling were increased in high stressed females compared to low stressed females.This indicates a launch of immune effector molecules as a direct response.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute for Farm Animal Biology (FBN), Institute for Genome Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany. wimmers@fbn-dummerstorf.de.

ABSTRACT

Background: Brain and immune system are linked in a bi-directional manner. To date, it remained largely unknown why immune components become suppressed, enhanced, or remain unaffected in relation to psychosocial stress. Therefore, we mixed unfamiliar pigs with different levels of aggressiveness. We separated castrated male and female pigs into psychosocially high- and low- stressed animals by skin lesions, plasma cortisol level, and creatine kinase activity obtained from agonistic behaviour associated with regrouping. Peripheral blood mononuclear cells (PBMC) were collected post-mortem and differential gene expression was assessed using the Affymetrix platform (n = 16).

Results: Relevant stress-dependent alterations were found only between female samples, but not between castrated male samples. Molecular routes related to TREM 1 signalling, dendritic cell maturation, IL-6 signalling, Toll-like receptor signalling, and IL-8 signalling were increased in high stressed females compared to low stressed females. This indicates a launch of immune effector molecules as a direct response. According to the shifts of transcripts encoding cell surface receptors (e.g. CD14, TLR2, TLR4, TREM1) the study highlights processes acting on pattern recognition, inflammation, and cell-cell communication.

Conclusions: The transcriptional response partly affected the degree of 'stress responsiveness', indicating that the high stressed females altered their signal transduction due to potential infections and injuries while fighting.

Show MeSH
Related in: MedlinePlus