Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells

Yak is a special free-ranging cattle breed in the plateau areas of Qinghai and Tibet. Pasture withering in cold-season pastures results in energy deficiency in yaks, which undermines the rumen epithelial barrier. However, the leading factor causing rumen epithelial injury remains unknown. Glutamine...

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Main Authors: Ziqi Yue, Junmei Wang, Rui Hu, Quanhui Peng, Hongrui Guo, Huawei Zou, Jianxin Xiao, Yahui Jiang, Zhisheng Wang
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Animals
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Online Access:https://www.mdpi.com/2076-2615/14/22/3232
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author Ziqi Yue
Junmei Wang
Rui Hu
Quanhui Peng
Hongrui Guo
Huawei Zou
Jianxin Xiao
Yahui Jiang
Zhisheng Wang
author_facet Ziqi Yue
Junmei Wang
Rui Hu
Quanhui Peng
Hongrui Guo
Huawei Zou
Jianxin Xiao
Yahui Jiang
Zhisheng Wang
author_sort Ziqi Yue
collection DOAJ
description Yak is a special free-ranging cattle breed in the plateau areas of Qinghai and Tibet. Pasture withering in cold-season pastures results in energy deficiency in yaks, which undermines the rumen epithelial barrier. However, the leading factor causing rumen epithelial injury remains unknown. Glutamine (Gln), a conditionally essential amino acid, is insufficient under pathological conditions. Glucose (GLU) is an important energy source. Thus, we explored the effects of Gln or GLU deprivation on the barrier function of yak rumen epithelial cells and investigated the underlying mechanisms, as well as the differences in rumen epithelial barrier function between Gln deprivation (Gln-D) and GLU deprivation (GLU-D). In previous work, we constructed the yak rumen epithelial cells (YRECs) line by transferring the human telomerase reverse transcriptase gene (hTERT) and simian virus 40 large T antigen (SV40T) into primary YRECs. The YRECs were exposed to normal, Gln-D, GLU-D, and serum replacement (SR) media for 6, 12, and 24 h. Our data displayed that cell viability and tight junction protein expression in the SR group were not significantly changed compared to the normal group. Whereas, compared with the SR group, Gln-D treated for more than 12 h reduced cell viability and proliferation, and GLU-D treated for more than 12 h damaged the cell morphology and reduced cell viability and proliferation. The cell proliferation and cell viability were decreased more in GLU-D than in Gln-D. In addition, Gln-D treated for more than 12 h disrupted YREC cellular partially tight junctions by inducing oxidative stress and inflammation, and GLU-D treated for more than 12 h disrupted YREC cellular tight junctions by inducing apoptosis, oxidative stress, and inflammation. Compared with Gln-D, GLU-D more significantly induced cell injury and reduced tight junction protein levels. Our results provided evidence that GLU-D induced damage through the p38 mitogen-activated protein kinase (p38 MAPK)/c-junN-terminal kinase (JNK) signaling pathway, which was more serious than Gln-D treated for more than 12 h.
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publishDate 2024-11-01
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spelling doaj-art-f3e4d2b5ad674e91857f5e16baba439d2024-11-26T17:45:50ZengMDPI AGAnimals2076-26152024-11-011422323210.3390/ani14223232Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial CellsZiqi Yue0Junmei Wang1Rui Hu2Quanhui Peng3Hongrui Guo4Huawei Zou5Jianxin Xiao6Yahui Jiang7Zhisheng Wang8Low Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaKey Laboratory of Animal Diseases and Environmental Hazards of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaLow Carbon Breeding Cattle and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, ChinaYak is a special free-ranging cattle breed in the plateau areas of Qinghai and Tibet. Pasture withering in cold-season pastures results in energy deficiency in yaks, which undermines the rumen epithelial barrier. However, the leading factor causing rumen epithelial injury remains unknown. Glutamine (Gln), a conditionally essential amino acid, is insufficient under pathological conditions. Glucose (GLU) is an important energy source. Thus, we explored the effects of Gln or GLU deprivation on the barrier function of yak rumen epithelial cells and investigated the underlying mechanisms, as well as the differences in rumen epithelial barrier function between Gln deprivation (Gln-D) and GLU deprivation (GLU-D). In previous work, we constructed the yak rumen epithelial cells (YRECs) line by transferring the human telomerase reverse transcriptase gene (hTERT) and simian virus 40 large T antigen (SV40T) into primary YRECs. The YRECs were exposed to normal, Gln-D, GLU-D, and serum replacement (SR) media for 6, 12, and 24 h. Our data displayed that cell viability and tight junction protein expression in the SR group were not significantly changed compared to the normal group. Whereas, compared with the SR group, Gln-D treated for more than 12 h reduced cell viability and proliferation, and GLU-D treated for more than 12 h damaged the cell morphology and reduced cell viability and proliferation. The cell proliferation and cell viability were decreased more in GLU-D than in Gln-D. In addition, Gln-D treated for more than 12 h disrupted YREC cellular partially tight junctions by inducing oxidative stress and inflammation, and GLU-D treated for more than 12 h disrupted YREC cellular tight junctions by inducing apoptosis, oxidative stress, and inflammation. Compared with Gln-D, GLU-D more significantly induced cell injury and reduced tight junction protein levels. Our results provided evidence that GLU-D induced damage through the p38 mitogen-activated protein kinase (p38 MAPK)/c-junN-terminal kinase (JNK) signaling pathway, which was more serious than Gln-D treated for more than 12 h.https://www.mdpi.com/2076-2615/14/22/3232yak rumen epithelial cellsglutamine deprivationglucose deprivationinflammationtight junction
spellingShingle Ziqi Yue
Junmei Wang
Rui Hu
Quanhui Peng
Hongrui Guo
Huawei Zou
Jianxin Xiao
Yahui Jiang
Zhisheng Wang
Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
Animals
yak rumen epithelial cells
glutamine deprivation
glucose deprivation
inflammation
tight junction
title Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
title_full Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
title_fullStr Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
title_full_unstemmed Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
title_short Effects of Glutamine or Glucose Deprivation on Inflammation and Tight Junction Disruption in Yak Rumen Epithelial Cells
title_sort effects of glutamine or glucose deprivation on inflammation and tight junction disruption in yak rumen epithelial cells
topic yak rumen epithelial cells
glutamine deprivation
glucose deprivation
inflammation
tight junction
url https://www.mdpi.com/2076-2615/14/22/3232
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