Abstract
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.
Highlights
Epididymis, a well-organized mass of compactly coiled tubes, acts as the last programmed differentiation reservoir for male gametes in mammals (Cornwall, 2009; Bedford, 2015; Sullivan and Mieusset, 2016)
Using real-time quantitative PCR, the relative mRNA level of the endogenous H2S-generating enzymes CBS and cystathionine γ-lyase (CSE) was found to be highly expressed in corpus and cauda regions compared with caput region of the rat epididymis (Figure 1A)
The synthesis of H2S was significantly suppressed when pretreated the tissue homogenate with AOAA (1 mM), the inhibitor of CBS, or/and PAG (10 mM), the inhibitor of CSE (Aydinoglu et al, 2017). These results indicated that the epididymis possessed increasing ability to generate the endogenous H2S from caput to cauda regions
Summary
Epididymis, a well-organized mass of compactly coiled tubes, acts as the last programmed differentiation reservoir for male gametes in mammals (Cornwall, 2009; Bedford, 2015; Sullivan and Mieusset, 2016). Over the past few decades, several K+ channels have been identified in epididymal epithelium of various species including the adenosine triphosphate-sensitive K+ channel (KATP) channel (Lybaert et al, 2008), the Ca2+-activated K+ channel (KCa channel) (Huang et al, 1999) and an outwardly rectifying K+ channel (Chan et al, 1995). The existence of these K+ channels suggests that epididymal epithelial cells may play a vital role in maintaining the high K+ level along the epididymal intraluminal fluid
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