Heat stress directly impairs gut integrity and recruits distinct immune cell populations into the bovine intestine

Abstract

High ambient temperature has multiple potential effects on the organism such as hyperthermia, endotoxemia, and/or systemic inflammation. However, it is often difficult to discriminate between cause and consequence of phenotypic effects, such as the indirect influence of heat stress via reduced food intake. Lactating dairy cows are a particularly sensitive model to examine the effects of heat stress due to their intensive metabolic heat production and small surface:volume ratio. Results from this model show heat stress directly induced a so-far unknown infiltration of yet uncategorized cells into the mucosa and submucosa of the jejunum. Due to a pair-feeding design, we can exclude this effect being a consequence of the concurrent heat-induced reduction in feed intake. Isolation and characterization of the infiltrating cells using laser capture microdissection and RNA sequencing indicated a myeloic origin and macrophage-like phenotype. Furthermore, targeted transcriptome analyses provided evidence of activated immune- and phagocytosis-related pathways with LPS and cytokines as upstream regulators directly associated with heat stress. Finally, we obtained indication that heat stress may directly alter jejunal tight junction proteins suggesting an impaired intestinal barrier. The penetration of toxic and bacterial compounds during heat stress may have triggered a modulated immune repertoire and induced an antioxidative defense mechanism to maintain homeostasis between commensal bacteria and the jejunal immune system. Our bovine model indicates direct effects of heat stress on the jejunum of mammals already at moderately elevated ambient temperature. These results need to be considered when developing concepts to combat the negative consequences of heat stress.

Intestinal Barrier Integrity in Heat-Stressed Modern Broilers and Their Ancestor Wild Jungle Fowl

“…Recent study has shown that heat stress increases FITC-D levels in chicken serum indicating an increased intestinal permeability and leacky gut syndrome (22). Koch and co-workers have shown that heat stress directly impairs gut integrity and disturbs the immune cell populations in bovine intestine (23). This breakdown of the intestinal barrier has been shown to allow opportuinistic bacteria to enter circulation resulting in infections such necrotic enteritis (24), femoral head necrosis, and bacterial chondronecrosis with osteomyelitis (25).…”

Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers

“…Tight junctions act as selective barriers that regulate paracellular transport. Heat stress can compromise the integrity of the tight junctions and thereby increase the permeability of the intestinal mucosa, disturbing its function as a selective barrier that absorbs nutrients while keeping pathogens at bay [9]. Heat stress was also reported to reduce the performance of broilers, increase viable counts of coliforms and Clostridium, downregulate the protein levels of occludin and zonula occludens-1, increase intestinal permeability and injure jejunal morphology [10].…”

Effects of dietary zinc source on the metabolic and immunological response to lipopolysaccharide in lactating Holstein dairy cows

“…Uterine, mammary, and intestinal epithelial integrity can become compromised due to a variety of stressors (Khafipour et al, 2009;Kvidera et al, 2017c;Koch et al, 2019), and hyperpermeability of these barriers permits pathogen infiltration and, ultimately, immune stimulation (van Miert and Frens, 1968). Regardless of the pathogen's origin, a robust and transient immune response is imperative to successful pathogen clearance, resolution of inflammation, and return to optimal production (i.e., milk production, growth, and reproduction; Bertoni et al, 2008;Bradford et al, 2015;Trevisi and Minuti, 2018).…”