Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway

Abstract Current measures mainly focus on how melatonin reduces physiological heat stress in animals, but its effects on reproductive damage to male dairy goats have been neglected. This study aimed to determine the protective effect of melatonin on male reproduction during heat stress in dairy goat...

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Main Authors: Yundie Liu, Hui Cai, Xinrui Guo, Aili Aierken, Jinlian Hua, Baohua Ma, Sha Peng
Format: Article
Language:English
Published: Springer 2022-11-01
Series:Stress Biology
Subjects:
Online Access:https://doi.org/10.1007/s44154-022-00068-9
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author Yundie Liu
Hui Cai
Xinrui Guo
Aili Aierken
Jinlian Hua
Baohua Ma
Sha Peng
author_facet Yundie Liu
Hui Cai
Xinrui Guo
Aili Aierken
Jinlian Hua
Baohua Ma
Sha Peng
author_sort Yundie Liu
collection DOAJ
description Abstract Current measures mainly focus on how melatonin reduces physiological heat stress in animals, but its effects on reproductive damage to male dairy goats have been neglected. This study aimed to determine the protective effect of melatonin on male reproduction during heat stress in dairy goats and to further explore its mechanisms. A natural heat stress model of Saanen dairy goats was used to assess testicular tissue damage 7 days after heat stress and to examine semen quality changes during a spermatogenic cycle. RNA-seq, Western blot, RT–qPCR, and immunofluorescence staining were used to explore the mechanism by which melatonin protects against heat stress-induced reproductive damage and to validate the results. The data suggested that melatonin significantly alleviated the heat stress-induced decrease in sperm quality, protected varicose tubule structure, reduced the levels of heat shock proteins and apoptotic proteins and protected the spermatocytes and round spermatozoa, which are mainly affected by heat stress. RNA-seq results suggest that melatonin inhibits the PI3K/AKT signaling pathway, reduces the level of p-AKT, and promotes elevated BCL-2. In addition, melatonin treatment could upregulate the gene expression of MT2 which was downregulated by heat stress and improve the change in extracellular matrix components and restore serum testosterone levels. Our results suggest that melatonin can protect against testicular and spermatogenic cell damage and improve semen quality in male dairy goats under heat stress. This study provides an important reference for subsequent studies on the molecular mechanisms of melatonin in protecting male reproductive processes under heat stress and using exogenous melatonin to prevent heat stress.
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spelling doaj.art-4df7d6d2a1d74337a5cd2b292bdcdda02022-12-22T03:43:02ZengSpringerStress Biology2731-04502022-11-012111610.1007/s44154-022-00068-9Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathwayYundie Liu0Hui Cai1Xinrui Guo2Aili Aierken3Jinlian Hua4Baohua Ma5Sha Peng6College of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyCollege of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering & Technology, Northwest Agriculture and Forestry University of Science and TechnologyAbstract Current measures mainly focus on how melatonin reduces physiological heat stress in animals, but its effects on reproductive damage to male dairy goats have been neglected. This study aimed to determine the protective effect of melatonin on male reproduction during heat stress in dairy goats and to further explore its mechanisms. A natural heat stress model of Saanen dairy goats was used to assess testicular tissue damage 7 days after heat stress and to examine semen quality changes during a spermatogenic cycle. RNA-seq, Western blot, RT–qPCR, and immunofluorescence staining were used to explore the mechanism by which melatonin protects against heat stress-induced reproductive damage and to validate the results. The data suggested that melatonin significantly alleviated the heat stress-induced decrease in sperm quality, protected varicose tubule structure, reduced the levels of heat shock proteins and apoptotic proteins and protected the spermatocytes and round spermatozoa, which are mainly affected by heat stress. RNA-seq results suggest that melatonin inhibits the PI3K/AKT signaling pathway, reduces the level of p-AKT, and promotes elevated BCL-2. In addition, melatonin treatment could upregulate the gene expression of MT2 which was downregulated by heat stress and improve the change in extracellular matrix components and restore serum testosterone levels. Our results suggest that melatonin can protect against testicular and spermatogenic cell damage and improve semen quality in male dairy goats under heat stress. This study provides an important reference for subsequent studies on the molecular mechanisms of melatonin in protecting male reproductive processes under heat stress and using exogenous melatonin to prevent heat stress.https://doi.org/10.1007/s44154-022-00068-9Natural heat stressMelatoninPI3K/AKT signaling pathwaySpermatocytesApoptosis
spellingShingle Yundie Liu
Hui Cai
Xinrui Guo
Aili Aierken
Jinlian Hua
Baohua Ma
Sha Peng
Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
Stress Biology
Natural heat stress
Melatonin
PI3K/AKT signaling pathway
Spermatocytes
Apoptosis
title Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
title_full Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
title_fullStr Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
title_full_unstemmed Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
title_short Melatonin alleviates heat stress-induced testicular damage in dairy goats by inhibiting the PI3K/AKT signaling pathway
title_sort melatonin alleviates heat stress induced testicular damage in dairy goats by inhibiting the pi3k akt signaling pathway
topic Natural heat stress
Melatonin
PI3K/AKT signaling pathway
Spermatocytes
Apoptosis
url https://doi.org/10.1007/s44154-022-00068-9
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