Short-term feed restriction induces inflammation and an antioxidant response via cystathionine-β-synthase and glutathione peroxidases in ruminal epithelium from Angus steers

Abstract Decreased intake is induced by stressors such as parturition, transportation, dietary transitions, and disease. An important function of one-carbon metabolism (OCM) is to produce the antioxidant glutathione to help reduce oxidative stress. Although various components of OCM are expressed in...

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Published in:Journal of animal science 2024-08
Main Authors: Jiang, Qianming, Galvão, Matheus Castilho, Thanh, Lam P, Aboragah, Ahmad A, Mauck, John, Gionbelli, Mateus P, Alhidary, Ibrahim A, McCann, Joshua C, Loor, Juan J
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creator Jiang, Qianming
Galvão, Matheus Castilho
Thanh, Lam P
Aboragah, Ahmad A
Mauck, John
Gionbelli, Mateus P
Alhidary, Ibrahim A
McCann, Joshua C
Loor, Juan J
description Abstract Decreased intake is induced by stressors such as parturition, transportation, dietary transitions, and disease. An important function of one-carbon metabolism (OCM) is to produce the antioxidant glutathione to help reduce oxidative stress. Although various components of OCM are expressed in the bovine rumen and small intestine, the relationship among reduced feed intake, one-carbon metabolism, and antioxidant mechanisms in gut tissues is unknown. This study aimed to assess alterations in immune and antioxidant pathways in ruminal epithelium due to acute feed restriction (FR). Seven group-housed ruminally-cannulated Angus steers (663 ± 73 kg body weight, 2-year old) had ad libitum access to a finishing diet (dry-rolled corn, corn silage, modified wet distiller’s grains) during 15 days of a pre-FR period (PRE). Subsequently, steers were moved to a metabolism barn with tie-stalls and individually-fed at 25% of estimated intake in PRE for 3 days (FR period, FRP). This was followed by 15-days of recovery (POST) during which steers had ad libitum access to the same diet as in PRE and FRP. Plasma and ruminal tissue biopsies were collected during each period. Plasma free fatty acid and IL1-β concentrations were higher (P ≤ 0.03) in FRP than PRE or POST. The mRNA abundance of the pro-inflammatory genes TNF, TLR2, and TLR4 in ruminal epithelium peaked (P < 0.05) at FRP and remained higher at POST. These responses agreed with the higher (P < 0.05) abundance of phosphorylated (p)-MAPK (an inflammation activator) and p-EEF2 (translational repressor) in FRP than PRE and POST. Although ruminal GPX enzyme activity did not increase at FRP compared with PRE and POST, protein abundance of GPX1 and GPX3 along with the antioxidant response regulator NFE2L2 were highest (P < 0.01) and the activity of cystathione-beta synthase tended (P = 0.06) to be highest during FR. Although FR had minimal negative effects on tissue integrity-related genes (only filamin A was downregulated), it led to a systemic inflammatory response and triggered inflammation and antioxidant mechanisms within ruminal epithelium. Thus, deploying anti-inflammatory and antioxidant mechanisms via molecules that feed into OCM (e.g., dietary methyl donors such as methionine, choline, betaine, folate) could potentially counteract the stressors associated with FR.
doi_str_mv 10.1093/jas/skae257
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An important function of one-carbon metabolism (OCM) is to produce the antioxidant glutathione to help reduce oxidative stress. Although various components of OCM are expressed in the bovine rumen and small intestine, the relationship among reduced feed intake, one-carbon metabolism, and antioxidant mechanisms in gut tissues is unknown. This study aimed to assess alterations in immune and antioxidant pathways in ruminal epithelium due to acute feed restriction (FR). Seven group-housed ruminally-cannulated Angus steers (663 ± 73 kg body weight, 2-year old) had ad libitum access to a finishing diet (dry-rolled corn, corn silage, modified wet distiller’s grains) during 15 days of a pre-FR period (PRE). Subsequently, steers were moved to a metabolism barn with tie-stalls and individually-fed at 25% of estimated intake in PRE for 3 days (FR period, FRP). This was followed by 15-days of recovery (POST) during which steers had ad libitum access to the same diet as in PRE and FRP. Plasma and ruminal tissue biopsies were collected during each period. Plasma free fatty acid and IL1-β concentrations were higher (P ≤ 0.03) in FRP than PRE or POST. The mRNA abundance of the pro-inflammatory genes TNF, TLR2, and TLR4 in ruminal epithelium peaked (P &lt; 0.05) at FRP and remained higher at POST. These responses agreed with the higher (P &lt; 0.05) abundance of phosphorylated (p)-MAPK (an inflammation activator) and p-EEF2 (translational repressor) in FRP than PRE and POST. Although ruminal GPX enzyme activity did not increase at FRP compared with PRE and POST, protein abundance of GPX1 and GPX3 along with the antioxidant response regulator NFE2L2 were highest (P &lt; 0.01) and the activity of cystathione-beta synthase tended (P = 0.06) to be highest during FR. 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Although FR had minimal negative effects on tissue integrity-related genes (only filamin A was downregulated), it led to a systemic inflammatory response and triggered inflammation and antioxidant mechanisms within ruminal epithelium. 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title Short-term feed restriction induces inflammation and an antioxidant response via cystathionine-β-synthase and glutathione peroxidases in ruminal epithelium from Angus steers
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