Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis
As a novel gasotransmitter, hydrogen sulfide (H2S) elicits various physiological actions including smooth muscle relaxation and promotion of transepithelial ion transport. However, the pro-secretory function of H2S in the male reproductive system remains largely unclear. The aim of this study is to...
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doaj-45632bbb1e7b49279967a64e1cfa1ee02020-11-24T21:14:24ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-01-01910.3389/fphys.2018.01886423498Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat EpididymisDong-Dong Gao0Jia-Wen Xu1Wei-Bing Qin2Lei Peng3Zhuo-Er Qiu4Long-Long Wang5Chong-Feng Lan6Xiao-Nian Cao7Jian-Bang Xu8Yun-Xin Zhu9Yun-Ge Tang10Yi-Lin Zhang11Wen-Liang Zhou12School of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaKey Laboratory of Male Reproductive and Genetics, National Health and Family Planning Commission, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaKey Laboratory of Male Reproductive and Genetics, National Health and Family Planning Commission, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaAs a novel gasotransmitter, hydrogen sulfide (H2S) elicits various physiological actions including smooth muscle relaxation and promotion of transepithelial ion transport. However, the pro-secretory function of H2S in the male reproductive system remains largely unclear. The aim of this study is to elucidate the possible roles of H2S in modulating rat epididymal intraluminal ionic microenvironment essential for sperm storage. The results revealed that endogenous H2S-generating enzymes cystathionine β-synthetase (CBS) and cystathionine γ-lyase (CSE) were both expressed in rat epididymis. CBS located predominantly in epithelial cells whilst CSE expressed primarily in smooth muscle cells. The relative expression level of CBS and CSE escalated from caput to cauda regions of epididymis, which was paralleled to the progressively increasing production of endogenous H2S. The effect of H2S on epididymal epithelial ion transportation was investigated using short-circuit current (ISC), measurement of intracellular ion concentration and in vivo rat epididymal microperfusion. Our data showed that H2S induced transepithelial K+ secretion via adenosine triphosphate-sensitive K+ (KATP) channel and large conductance Ca2+-activated K+ (BKCa) channel. Transient receptor potential vanilloid 4 (TRPV4) channel-mediated Ca2+ influx was implicated in the activation of BKCa channel. In vivo studies further demonstrated that H2S promoted K+ secretion in rat epididymal epithelium. Inhibition of endogenous H2S synthesis caused a significant decrease in K+ concentration of cauda epididymal intraluminal fluid. Moreover, our data demonstrated that high extracellular K+ concentration actively depressed the motility of cauda epididymal sperm in a pH-independent manner. Collectively, the present study demonstrated that H2S was vital to the formation of high K+ concentration in epididymal intraluminal fluid by promoting the transepithelial K+ secretion, which might contribute to the maintenance of the cauda epididymal sperm in quiescent dormant state before ejaculation.https://www.frontiersin.org/article/10.3389/fphys.2018.01886/fullH2SK+ secretionepididymal epitheliumKATP channelBKCa channel |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Dong-Dong Gao Jia-Wen Xu Wei-Bing Qin Lei Peng Zhuo-Er Qiu Long-Long Wang Chong-Feng Lan Xiao-Nian Cao Jian-Bang Xu Yun-Xin Zhu Yun-Ge Tang Yi-Lin Zhang Wen-Liang Zhou |
spellingShingle |
Dong-Dong Gao Jia-Wen Xu Wei-Bing Qin Lei Peng Zhuo-Er Qiu Long-Long Wang Chong-Feng Lan Xiao-Nian Cao Jian-Bang Xu Yun-Xin Zhu Yun-Ge Tang Yi-Lin Zhang Wen-Liang Zhou Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis Frontiers in Physiology H2S K+ secretion epididymal epithelium KATP channel BKCa channel |
author_facet |
Dong-Dong Gao Jia-Wen Xu Wei-Bing Qin Lei Peng Zhuo-Er Qiu Long-Long Wang Chong-Feng Lan Xiao-Nian Cao Jian-Bang Xu Yun-Xin Zhu Yun-Ge Tang Yi-Lin Zhang Wen-Liang Zhou |
author_sort |
Dong-Dong Gao |
title |
Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis |
title_short |
Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis |
title_full |
Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis |
title_fullStr |
Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis |
title_full_unstemmed |
Cellular Mechanism Underlying Hydrogen Sulfide Mediated Epithelial K+ Secretion in Rat Epididymis |
title_sort |
cellular mechanism underlying hydrogen sulfide mediated epithelial k+ secretion in rat epididymis |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Physiology |
issn |
1664-042X |
publishDate |
2019-01-01 |
description |
As a novel gasotransmitter, hydrogen sulfide (H2S) elicits various physiological actions including smooth muscle relaxation and promotion of transepithelial ion transport. However, the pro-secretory function of H2S in the male reproductive system remains largely unclear. The aim of this study is to elucidate the possible roles of H2S in modulating rat epididymal intraluminal ionic microenvironment essential for sperm storage. The results revealed that endogenous H2S-generating enzymes cystathionine β-synthetase (CBS) and cystathionine γ-lyase (CSE) were both expressed in rat epididymis. CBS located predominantly in epithelial cells whilst CSE expressed primarily in smooth muscle cells. The relative expression level of CBS and CSE escalated from caput to cauda regions of epididymis, which was paralleled to the progressively increasing production of endogenous H2S. The effect of H2S on epididymal epithelial ion transportation was investigated using short-circuit current (ISC), measurement of intracellular ion concentration and in vivo rat epididymal microperfusion. Our data showed that H2S induced transepithelial K+ secretion via adenosine triphosphate-sensitive K+ (KATP) channel and large conductance Ca2+-activated K+ (BKCa) channel. Transient receptor potential vanilloid 4 (TRPV4) channel-mediated Ca2+ influx was implicated in the activation of BKCa channel. In vivo studies further demonstrated that H2S promoted K+ secretion in rat epididymal epithelium. Inhibition of endogenous H2S synthesis caused a significant decrease in K+ concentration of cauda epididymal intraluminal fluid. Moreover, our data demonstrated that high extracellular K+ concentration actively depressed the motility of cauda epididymal sperm in a pH-independent manner. Collectively, the present study demonstrated that H2S was vital to the formation of high K+ concentration in epididymal intraluminal fluid by promoting the transepithelial K+ secretion, which might contribute to the maintenance of the cauda epididymal sperm in quiescent dormant state before ejaculation. |
topic |
H2S K+ secretion epididymal epithelium KATP channel BKCa channel |
url |
https://www.frontiersin.org/article/10.3389/fphys.2018.01886/full |
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