Downregulation of Cellular Protective Factors of Rumen Epithelium in Goats Fed High Energy Diet

Hollmann, M.; Miller, Ingrid; Hummel, Karin Anna; Sabitzer, Sonja; Metzler‐Zebeli, Barbara U.; Razzazi-Fazeli, Ebrahim; Zebeli, Qendrim

doi:10.1371/journal.pone.0081602

Cited by 31 publications

(24 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The mechanism(s) of translocation for toxic compounds may be favoured by impairment of the barrier function of the rumen epithelium (Emmanuel et al, 2007), depletion of protective factors (Hollmann et al, 2013) and increased luminal osmolality (Owens et al, 1998). Also, the chronic exposure to ethanol can increase the epithelial permeability and portal vein translocation of endotoxin (Enomoto et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

Review: Enhancing gastrointestinal health in dairy cows

Plaizier

Mesgaran

Derakhshani

et al. 2018

Animal

153

144

View full text Add to dashboard Cite

Due to their high energy requirements, high-yielding dairy cows receive high-grain diets. This commonly jeopardises their gastrointestinal health by causing subacute ruminal acidosis (SARA) and hindgut acidosis. These disorders can disrupt nutrient utilisations, impair the functionalities of gastrointestinal microbiota, and reduce the absorptive and barrier capacities of gastrointestinal epithelia. They can also trigger inflammatory responses. The symptoms of SARA are not only due to a depressed rumen pH. Hence, the diagnosis of this disorder based solely on reticulo-rumen pH values is inaccurate. An accurate diagnosis requires a combination of clinical examinations of cows, including blood, milk, urine and faeces parameters, as well as analyses of herd management and feed quality, including the dietary contents of NDF, starch and physical effective NDF. Grain-induced SARA increases acidity and shifts availabilities of substrates for microorganisms in the reticulo-rumen and hindgut and can result in a dysbiotic microbiota that are characterised by low richness, diversity and functionality. Also, amylolytic microorganisms become more dominant at the expense of proteolytic and fibrolytic ones. Opportunistic microorganisms can take advantage of newly available niches, which, combined with reduced functionalities of epithelia, can contribute to an overall reduction in nutrient utilisation and increasing endotoxins and pathogens in digesta and faeces. The reduced barrier function of epithelia increases translocation of these endotoxins and other immunogenic compounds out of the digestive tract, which may be the cause of inflammations. This needs to be confirmed by determining the toxicity of these compounds. Cows differ in their susceptibility to poor gastrointestinal health, due to variations in genetics, feeding history, diet adaptation, gastrointestinal microbiota, metabolic adaptation, stress and infections. These differences may also offer opportunities for the management of gastrointestinal health. Strategies to prevent SARA include balancing the diet for physical effective fibre, non-fibre carbohydrates and starch, managing the different fractions of non-fibre carbohydrates, and consideration of the type and processing of grain and forage digestibility. Gastrointestinal health disorders due to high grain feeding may be attenuated by a variety of feed supplements and additives, including buffers, antibiotics, probiotics/direct fed microbials and yeast products. However, the efficacy of strategies to prevent these disorders must be improved. This requires a better understanding of the mechanisms through which these strategies affect the functionality of gastrointestinal microbiota and epithelia, and the immunity, inflammation and 'gastrointestinal-health robustness' of cows. More representative models to induce SARA are also needed.

show abstract

Section: Discussionmentioning

confidence: 99%

Review: Enhancing gastrointestinal health in dairy cows

Plaizier

Mesgaran

Derakhshani

et al. 2018

Animal

153

144

View full text Add to dashboard Cite

show abstract

“…In a human colon adenocarcinoma cell line, acetate treatment in the pH range of 6.0 to 7.0 induced cell apoptosis rather than necrosis, while acetate treatment at pH 5.5 caused cell necrosis [7] . Additionally, a recent study conducted in growing goats showed that after feeding high grain diet for 6 wks, several chaperone proteins with important cellular protective functions were collectively down-regulated in ruminal epithelium, indicating an attenuated cell defense system [26] .…”

Section: Discussionmentioning

confidence: 99%

“…Several studies conducted in goat and dairy cattle showed that a high grain diet impaired barrier functions of the rumen epithelium [23] , [24] , inflammation and caused other health problems in host animals [25] . Several chaperone proteins with important cellular protective functions in epithelial tissues were collectively down-regulated in response to high dietary energy supply, which indicates that energy-rich diets and the resulting acidotic insult may facilitate the impairment of rumen barrier function by attenuating their cell defense system [26] . However, no information exists about the underlying mechanism behind the disruption of protective functions of the hindgut epithelium in response to high grain diet to ruminants.…”

Section: Introductionmentioning

confidence: 99%

High Concentrate Diet Induced Mucosal Injuries by Enhancing Epithelial Apoptosis and Inflammatory Response in the Hindgut of Goats

et al. 2014

View full text Add to dashboard Cite

PurposeIt is widely accepted that lipopolysaccharide and volatile fatty acids (VFA) accumulate in the digestive tract of ruminants fed diets containing high portions of grain. Compared to the ruminal epithelium, the hindgut epithelium is composed of a monolayer structure that is more “leaky” for lipopolysaccharide and susceptible to organic acid-induced damage. The aim of this study was to investigate changes in epithelial structure, apoptosis and inflammatory response in the hindgut of goats fed a high-concentrate diet for 6 weeks.Experimental DesignEight local Chinese goats with rumen cannulas were randomly assigned to two groups: one group was fed a high-concentrate diet (65% concentrate of dry matter, HC) and the other group was fed a low-concentrate diet (35% concentrate of dry matter, LC) for 6 wks. Ruminal fluid, plasma, and hindgut mucosa tissues were collected. Histological techniques, real-time PCR and western blotting were used to evaluate the tissues structure, cell apoptosis and local inflammation in the hindguts.ResultsFeeding HC diet for 6 wks resulted in a significant decrease of ruminal pH (p<0.01), and ruminal lipopolysaccharide concentrations were significantly increased in HC goats (p<0.05). Obvious damage was observed to mucosal epithelium of the hindgut and the intercellular tight junctions in HC, but not in LC, goats. The expression of MyD88 and caspase-8 mRNA was increased in colonic epithelium of HC goats compared to LC (p<0.05), and the expression of TLR-4 and caspase-3 showed a tendency to increase. In the cecum, interleukin-1β mRNA expression was decreased (p<0.05), and caspase-3 showed a potential increase (p = 0.07) in HC goats. The level of NF-κB protein was increased in colonic epithelium of HC goats. Caspase-3 activity was elevated in both colon and cecum, whereas caspase-8 activity was statistically increased only in colon.ConclusionsFeeding a high-concentrate diet to goats for 6 wks led to hindgut mucosal injuries via activating epithelial cells apoptosis and local inflammatory response.

show abstract

“…Although excess oxidative stress is inferred from the literatures [22][23][24] , the responses of rumen epithelial cells to oxidative stress might be depressed during the first period in contrast to a short-term (17 days) SARA challenge in dairy cows 21 . These results also imply www.nature.com/scientificreports www.nature.com/scientificreports/ mitochondrial metabolic dysfunction (i.e., handling oxidative stress), suggesting greater rumen epithelial cell vulnerability to cellular damage by acidotic insult 25 .…”

Section: Discussionmentioning

confidence: 90%

Long-term high-grain diet alters ruminal pH, fermentation, and epithelial transcriptomes, leading to restored mitochondrial oxidative phosphorylation in Japanese Black cattle

Ogata

Makino

Ishizuka

et al. 2020

Sci Rep

View full text Add to dashboard Cite

to increase intramuscular fat accumulation, Japanese Black beef cattle are commonly fed a high-grain diet from 10 to 30 months of age. Castrated and fistulated cattle (n = 9) were fed a high-concentrate diets during the early, middle, and late stages consecutively (10-14, 15-22, 23-30 months of age, respectively). Ruminal pH was measured continuously, and rumen epithelium and fluid samples were collected on each stage. The 24-h mean ruminal pH during the late stage was significantly lower than that during the early stage. Total volatile fatty acid (VFA) and lactic acid levels during the late stage were significantly lower and higher, respectively, than those during the early and middle stages. In silico analysis of differentially expressed genes showed that "Oxidative Phosphorylation" was the pathway inhibited most between the middle and early stages in tandem with an inhibited upstream regulator (PPARGC1A, also called PGC-1α) but the most activated pathway between the late and middle stages. these results suggest that mitochondrial dysfunction and thereby impaired cell viability due to acidic irritation under the higher VFA concentration restored stable mitochondrial oxidative phosphorylation and cell viability by higher lactic acid levels used as cellular oxidative fuel under a different underlying mechanism in subacute ruminal acidosis. A high-grain diet promotes the growth, productivity, and quality of meat or milk production in beef and dairy cattle. On a high-grain diet, organic acids such as volatile fatty acids (VFAs) and lactic acid accumulate in the rumen 1,2. Ruminal pH is critical in the maintenance of normal, stable fermentation, microbial populations, and absorptive function 2-4 , and is determined by the balance between acid production by microbes and acid removal by absorption, neutralization, and clearance 1,5,6 , in a host-microbiome interaction 7. The occurrence of subacute ruminal acidosis (SARA) defined by a rumen pH <5.6 is due to the non-physiological accumulation of VFAs, while ruminal acidosis defined by a rumen pH <5.0 is associated with accumulated lactic acid in the rumen 2. Several short-(days) or mid-term (weeks) studies have shown that SARA or rumen acidosis challenges affected the rumen epithelial structure, gene expression, and transcriptomes 8-10. For example, in one study, 3 weeks of a high-grain diet (65% grain) compromised the structural integrity and led to the appearance of undifferentiated cells near the stratum corneum of the rumen papillae in non-lactating dairy cattle 8. In another, the rumen papillae in dairy cattle fed a total mixed ration had increased epithelial desquamation and sloughing scores during early lactation, as well as upregulation of genes encoding desmosome assembly (despoglein1 and corneodesmosin), epidermal growth factor (EGF) signaling (epiregulin), transforming growth factor β (TGFB)

show abstract

Downregulation of Cellular Protective Factors of Rumen Epithelium in Goats Fed High Energy Diet

Cited by 31 publications

References 48 publications

Review: Enhancing gastrointestinal health in dairy cows

Review: Enhancing gastrointestinal health in dairy cows

High Concentrate Diet Induced Mucosal Injuries by Enhancing Epithelial Apoptosis and Inflammatory Response in the Hindgut of Goats

Long-term high-grain diet alters ruminal pH, fermentation, and epithelial transcriptomes, leading to restored mitochondrial oxidative phosphorylation in Japanese Black cattle

Contact Info

Product

Resources

About