Heat Stress Reduces Intestinal Barrier Integrity and Favors Intestinal Glucose Transport in Growing Pigs

Pearce, Sarah; Mani, Venkatesh; Boddicker, Rebecca L.; Johnson, Jay S; Weber, Thomas; Ross, Jason W.; Rhoads, Robert P.; Baumgard, Lance H.; Gabler, Nicholas K.

doi:10.1371/journal.pone.0070215

Cited by 248 publications

(228 citation statements)

References 59 publications

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“…We speculated this increase resulted from early changes in inflammatory signaling or migration from vasculature since TNF α blood content decreased following 12 and 24 h of heat stress (Pearce et al. 2013b, 2015) while muscle transcript expression was not elevated (Montilla et al. 2014; Ganesan et al.…”

Section: Discussionmentioning

confidence: 99%

Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle

et al. 2017

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Despite well‐studied clinical manifestations, intracellular mechanisms of prolonged hyperthermic injury remain unclear, especially in skeletal muscle. Given muscle's large potential to impact systemic inflammation and metabolism, the response of muscle cells to heat‐mediated injury warrants further investigation. We have previously reported increased activation of NF‐κB signaling and increased NF‐κB and AP‐1‐driven transcripts in oxidative skeletal muscle following 12 h of heat stress. The purpose of this investigation was to examine early heat stress‐induced inflammatory signaling in skeletal muscle. We hypothesized that heat stress would increase NF‐κB and AP‐1 signaling in oxidative skeletal muscle. To address this hypothesis, 32 gilts were randomly assigned to one of four treatment groups (n = 8/group): control (0 h: 21°C) or exposed to heat stress conditions (37°C) for 2 h (n = 8), 4 h (n = 8), or 6 h (n = 8). Immediately following environmental exposure pigs were euthanized and the red portion of the semitendinosus muscle (STR) was harvested. We found evidence of NF‐κB pathway activation as indicated by increased protein abundance of NF‐κB activator IKK‐α following 4 h and increased total NF‐κB protein abundance following 6 h of heat stress. Heat stress also stimulated AP‐1 signaling as AP‐1 protein abundance was increased in nuclear fractions following 4 h of heat stress. Interleukin‐6 protein abundance and activation of the JAK/STAT pathway were decreased in heat stressed muscle. These data indicate that heat stress activated inflammatory signaling in the porcine STR muscle via the AP‐1 pathway and early activation of the NF‐κB pathway.

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Section: Discussionmentioning

confidence: 99%

Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle

et al. 2017

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“…Whole sections from both the proximal ileum (1.5 m proximal to the ileal-cecal junction) and distal colon (0.5 m proximal to the rectum) were harvested immediately following euthanasia. Intestinal segments were flushed of luminal contents, and placed immediately into Krebs-Henseleit buffer (KHBB; containing 25 mM NaHCO 3 , 120 mM NaCl, 1 mM MgSO 4 , 6.3 mM KCl, 2 mM CaCl and 0.2 mM NaH 2 PO 4 ; pH 7.4) under constant aeration, and transported to the laboratory for mounting into modified Ussing chambers as previously described (Pearce et al, 2013b). In addition, ileal sections were fixed in 10% formalin for histological analysis.…”

Section: Methodsmentioning

confidence: 99%

“…Ussing chambers Ileal and colonic segments of each animal were mounted into modified Ussing chambers (Physiological Instruments, San Diego, CA, USA) for determination of intestinal integrity and active nutrient transport as described by Pearce et al (2013b). Briefly, intestinal samples were placed into the chambers, connected to dual channel current and voltage electrodes.…”

Section: Methodsmentioning

confidence: 99%

“…After 30 min of stabilization, ileal nutrient transport was measured for glucose, lysine, glutamine and methionine. Additionally, intestinal segments were tested for permeability to the macromolecule fluorescein isothiocyanate-labeled dextran (FITC-Dextran; 4.4 kDa; Sigma ® , St. Louis, MO, USA) and FITC-labeled LPS (FITC-LPS, Sigma ® , St. Louis, MO, USA); and apparent permeability coefficients (APP) were calculated as follows (Pearce et al, 2013b):…”

Section: Methodsmentioning

confidence: 99%

“…For instance, the small intestine is highly sensitive to heat damage (Kregel, 2002), and is one of the first tissues up-regulating heat shock proteins during hyperthermia (Flanagan et al, 1995). HS increases intestinal permeability (Lambert et al, 2002;Pearce et al, 2013b) and leads to increasing concentrations of lipopolysaccharide (LPS) in portal and systemic blood (Hall et al, 2001). Further, endotoxemia is common among heat stroke patients (Leon, 2007) and it is thought to play a central role in heat stroke pathophysiology, as survival increases when intestinal bacterial load is reduced (Bynum et al, 1979) or when plasma LPS is neutralized (Gathiram et al, 1987).…”

Section: Introductionmentioning

confidence: 99%

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Effects of supplemental zinc amino acid complex on gut integrity in heat-stressed growing pigs

Fernández

Pearce

Gabler

et al. 2014

Animal

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Heat stress (HS) jeopardizes livestock health and productivity and both may in part be mediated by reduced intestinal integrity. Dietary zinc improves a variety of bowel diseases, which are characterized by increased intestinal permeability. Study objectives were to evaluate the effects of supplemental zinc amino acid complex (ZnAA) on intestinal integrity in heat-stressed growing pigs. Crossbred gilts (43 ± 6 kg BW) were ad libitum fed one of three diets: (1) control (ZnC; 120 ppm Zn as ZnSO 4 ; n = 13), (2) control + 100 ppm Zn as ZnAA (Zn220; containing a total of 220 ppm Zn; n = 14), and (3) control + 200 ppm Zn as ZnAA (Zn320; containing a total of 320 ppm Zn; n = 16). After 25 days on their respective diets, all pigs were exposed to constant HS conditions (36°C, ∼50% humidity) for either 1 or 7 days. At the end of the environmental exposure, pigs were euthanized and blood and intestinal tissues were harvested immediately after sacrifice. As expected, HS increased rectal temperature ( P ⩽ 0.01; 40.23°C v. 38.93°C) and respiratory rate ( P ⩽ 0.01; 113 v. 36 bpm). Pigs receiving ZnAA tended to have increased rectal temperature (P = 0.07; +0.27°C) compared with ZnC-fed pigs. HS markedly reduced feed intake (FI; P ⩽ 0.01; 59%) and caused BW loss (2.10 kg), but neither variable was affected by dietary treatment. Fresh intestinal segments were assessed ex vivo for intestinal integrity. As HS progressed from days 1 to 7, both ileal and colonic transepithelial electrical resistance (TER) decreased ( P ⩽ 0.05; 34% and 22%, respectively). This was mirrored by an increase in ileal and colonic permeability to the macromolecule dextran ( P ⩽ 0.01; 13-and 56-fold, respectively), and increased colonic lipopolysaccharide permeability ( P ⩽ 0.05; threefold) with time. There was a quadratic response ( P ⩽ 0.05) to increasing ZnAA on ileal TER, as it was improved ( P ⩽ 0.05; 56%) in Zn220-fed pigs compared with ZnC. This study demonstrates that HS progressively compromises the intestinal barrier and supplementing ZnAA at the appropriate dose can improve aspects of small intestinal integrity during severe HS.

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Selenium exerts protective effects against heat stress‐induced barrier disruption and inflammation response in jejunum of growing pigs

Liu

Tang

et al. 2021

J Sci Food Agric

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BACKGROUND Heat stress (HS) has a negative impact on the intestinal barrier and immune function of pigs. Selenium (Se) may improve intestinal health through affecting selenoproteins. Thus we investigate the protective effect of new organic Se (2‐hydroxy‐4‐methylselenobutanoic acid, HMSeBA) on jejunal damage in growing pigs upon HS and integrate potential roles of corresponding selenoproteins. RESULTS HS decreased the villus height and increased (P < 0.05) the protein abundance of HSP70, and downregulated (P < 0.05) protein levels of tight junction‐related proteins (CLDN‐1 and OCLD). HS‐induced jejunal damage was associated with the upregulation of four inflammation‐related genes and ten selenoprotein‐encoding genes, downregulation (P < 0.05) of four selenoprotein‐encoding genes and decreased (P < 0.05) the protein abundance of GPX4 and SELENOS. Compared with the HS group, HMSeBA supplementation not only elevated the villus height and the ratio of V/C (P < 0:05), but also reduced (P < 0.05) the protein abundance of HSP70 and MDA content, and increased (P < 0.05) the protein abundance of OCLD. HMSeBA supplementation downregulated the expression of seven inflammation‐related genes, changed the expression of 12 selenoprotein‐encoding genes in jejunum mucosa affected by HS, and increased the protein abundance of GPX4, TXNRD1 and SELENOS. CONCLUSION Organic Se supplementation beyond nutritional requirement alleviates the negative effect of HS on the jejunum of growing pigs, and its protective effect is related to the response of corresponding selenoproteins. © 2021 Society of Chemical Industry.

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Heat Stress Reduces Intestinal Barrier Integrity and Favors Intestinal Glucose Transport in Growing Pigs

Cited by 248 publications

References 59 publications

Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle

Acute heat stress activated inflammatory signaling in porcine oxidative skeletal muscle

Effects of supplemental zinc amino acid complex on gut integrity in heat-stressed growing pigs

Selenium exerts protective effects against heat stress‐induced barrier disruption and inflammation response in jejunum of growing pigs

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