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24 May 2018 Mouse quiescin sulfhydryl oxidases exhibit distinct epididymal luminal distribution with segment-specific sperm surface associations
Tse-En Wang, Sheng-Hsiang Li, Shiori Minabe, Amanda L Anderson, Matthew D Dun, Kei-Ichiro Maeda, Fuko Matsuda, Hui-Wen Chang, Brett Nixon, Pei-Shiue Jason Tsai
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Abstract

Sulfhydryl oxidation is part of the sperm maturation process essential for the acquisition of sperm fertilization competency and its structural stabilization; however, the specific sulfhydryl oxidases that fulfill these roles have yet to be identified. In this study, we investigate the potential involvement of one atypical thiol oxidase family called quiescin Q6/sulfhydryl oxidase (QSOX) using the mouse epididymis as our model system. With multidisciplinary approaches, we show that QSOX isoform 1 and 2 exhibit complementary distribution throughout the epididymal duct, but that each variant possesses distinct subcellular localization within the epididymal principal cells. While QSOX2 was exclusively present in the Golgi apparatus of the caput and corpus epididymis, QSOX1c, the most profusely express QSOX1 variant, was abundantly present in the cauda luminal fluids. Moreover, immunohistochemistry studies together with proteomic identification in isolated epididymosomes provided evidence substantiating the release of QSOX2, but not QSOX1c, via an apocrine secretory pathway. Furthermore, we demonstrate for the first time, distinct association of QSOX1c and QSOX2 with the sperm acrosome and implantation fossa, during different stages of their epididymal maturation. In conclusion, our study provides the first comprehensive comparisons between QSOX1 and QSOX2 in the mouse epididymis, revealing their distinct epididymal distribution, cellular localization, mechanisms of secretion and sperm membrane association. Together, these data suggest that QSOX1 and QSOX2 have discrete biological functions in male germ cell development.

Summary Sentence

Mouse epididymal sulfhydryl oxidases exhibit complementary tissue distribution with disparate cellular localization, the distinct secretory mechanism and sperm membrane association suggesting their participation in different sperm maturation processes.

© The Author(s) 2018. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
Tse-En Wang, Sheng-Hsiang Li, Shiori Minabe, Amanda L Anderson, Matthew D Dun, Kei-Ichiro Maeda, Fuko Matsuda, Hui-Wen Chang, Brett Nixon, and Pei-Shiue Jason Tsai "Mouse quiescin sulfhydryl oxidases exhibit distinct epididymal luminal distribution with segment-specific sperm surface associations," Biology of Reproduction 99(5), 1022-1033, (24 May 2018). https://doi.org/10.1093/biolre/ioy125
Received: 11 February 2018; Accepted: 22 May 2018; Published: 24 May 2018
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KEYWORDS
acrosome
epididymis
fertility
implantation fossa
quiescin sulfhydryl oxidase
sperm maturation
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