Testosterone regulation on quiescin sulfhydryl oxidase 2 synthesis in the epididymis

in Reproduction
Authors:
Tse-En Wang Department of Veterinary Medicine, National Taiwan University, Taipei, Taiwan
Graduate Institute of Veterinary Medicine, National Taiwan University, Taipei, Taiwan

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Shiori Minabe Department of Veterinary Medical Sciences, Graduate School of Agriculture and Life Sciences, The University of Tokyo, Tokyo, Japan

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Fuko Matsuda Department of Veterinary Medical Sciences, Graduate School of Agriculture and Life Sciences, The University of Tokyo, Tokyo, Japan

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Sheng-Hsiang Li Department of Medical Research, Mackay Memorial Hospital, Tamshui, Taiwan

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Hiroko Tsukamura Graduate School of Bioagriculture Sciences, Nagoya University, Nagoya, Japan

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Kei-Ichiro Maeda Department of Veterinary Medical Sciences, Graduate School of Agriculture and Life Sciences, The University of Tokyo, Tokyo, Japan

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Lee Smith MRC Centre for Reproductive Health, University of Edinburgh, Edinburgh, UK
Faculty of Science, University of Newcastle, Callaghan, Australia

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Laura O’Hara Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, UK

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Bart M Gadella Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands

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Pei-Shiue Tsai Department of Veterinary Medicine, National Taiwan University, Taipei, Taiwan
Graduate Institute of Veterinary Medicine, National Taiwan University, Taipei, Taiwan
Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei, Taiwan

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https://orcid.org/0000-0001-8217-6285

Correspondence should be addressed to P-S Tsai; Email: psjasontsai@ntu.edu.tw
DOI:
https://doi.org/10.1530/REP-20-0629
Volume/Issue:
Volume 161: Issue 5
Page Range:
593–602
Article Type:
Research Article
Online Publication Date:
20 Apr 2021
Copyright:
© 2021 Society for Reproduction and Fertility 2021
Restricted access
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The epididymis is an androgen-responsive organ, whose structure and functions are modulated by the coordination between androgen and epididymal cues. Highly regulated molecular interaction within the epididymis is required to support viable sperm development necessary for subsequent fertilization. In the present study, we extended our earlier findings on a promising epididymal protein, quiescin sulfhydryl oxidase 2 (QSOX2), and demonstrated a positive correlation between testosterone and QSOX2 protein synthesis through the use of loss- and restore-of-function animal models. Moreover, based on transcriptomic analyses and 2D culture system, we determined that an additional polarized effect of glutamate is indispensable for the regulatory action of testosterone on QSOX2 synthesis. In conclusion, we propose noncanonical testosterone signaling supports epididymal QSOX2 protein synthesis, providing a novel perspective on the regulation of sperm maturation within the epididymis.

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Sept 2018 onwards Past Year Past 30 Days
Full Text Views 603 20 2
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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Araki Y, Suzuki K, Matusik RJ, Obinata M & Orgebin-Crist MC 2002 Immortalized epididymal cell lines from transgenic mice overexpressing temperature-sensitive simian virus 40 large T-antigen gene. Journal of Andrology 23 854–869.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bhutia YD & Ganapathy V 2016 Glutamine transporters in mammalian cells and their functions in physiology and cancer. Biochimica et Biophysica Acta 1863 2531–2539. (https://doi.org/10.1016/j.bbamcr.2015.12.017)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Breton S, Nair AV & Battistone MA 2019 Epithelial dynamics in the epididymis: role in the maturation, protection, and storage of spermatozoa. Andrology 7 631–643. (https://doi.org/10.1111/andr.12632)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bulldan A, Malviya VN, Upmanyu N, Konrad L & Scheiner-Bobis G 2017 Testosterone/bicalutamide antagonism at the predicted extracellular androgen binding site of ZIP9. Biochimica et Biophysica Acta: Molecular Cell Research 1864 2402–2414. (https://doi.org/10.1016/j.bbamcr.2017.09.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Calvin HI & Bedford JM 1971 Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. Journal of Reproduction and Fertility: Supplement 13 65–75.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cornwall GA 2009 New insights into epididymal biology and function. Human Reproduction Update 15 213–227. (https://doi.org/10.1093/humupd/dmn055)

  • Dacheux JL, Castella S, Gatti JL & Dacheux F 2005 Epididymal cell secretory activities and the role of proteins in boar sperm maturation. Theriogenology 63 319–341. (https://doi.org/10.1016/j.theriogenology.2004.09.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heckler EJ, Rancy PC, Kodali VK & Thorpe C 2008 Generating disulfides with the Quiescin-sulfhydryl oxidases. Biochimica et Biophysica Acta 1783 567–577. (https://doi.org/10.1016/j.bbamcr.2007.10.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heinlein CA & Chang C 2002 The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Molecular Endocrinology 16 2181–2187. (https://doi.org/10.1210/me.2002-0070)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hinton BT 1990 The testicular and epididymal luminal amino acid microenvironment in the rat. Journal of Andrology 11 498–505.

  • Ijiri TW, Vadnais ML, Huang AP, Lin AM, Levin LR, Buck J & Gerton GL 2014 Thiol changes during epididymal maturation: a link to flagellar angulation in mouse spermatozoa? Andrology 2 65–75. (https://doi.org/10.1111/j.2047-2927.2013.00147.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meistrich ML & Hess RA 2013 Assessment of spermatogenesis through staging of seminiferous tubules. Methods in Molecular Biology 927 299–307. (https://doi.org/10.1007/978-1-62703-038-0_27)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mital P, Hinton BT & Dufour JM 2011 The blood-testis and blood-epididymis barriers are more than just their tight junctions. Biology of Reproduction 84 851–858. (https://doi.org/10.1095/biolreprod.110.087452)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ng KM, Catalano MG, Pinós T, Selva DM, Avvakumov GV, Munell F & Hammond GL 2006 Evidence that fibulin family members contribute to the steroid-dependent extravascular sequestration of sex hormone-binding globulin. Journal of Biological Chemistry 281 15853–15861. (https://doi.org/10.1074/jbc.M512370200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • O’Hara L & Smith LB 2016 Development and characterization of cell-specific androgen receptor knockout mice. Methods in Molecular Biology 1443 219–248. (https://doi.org/10.1007/978-1-4939-3724-0_14)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • O’Hara L, Welsh M, Saunders PT & Smith LB 2011 Androgen receptor expression in the caput epididymal epithelium is essential for development of the initial segment and epididymal spermatozoa transit. Endocrinology 152 718–729. (https://doi.org/10.1210/en.2010-0928)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pholpramool C, White RW & Setchell BP 1982 Influence of androgens on inositol secretion and sperm transport in the epididymis of rats. Journal of Reproduction and Fertility 66 547–553. (https://doi.org/10.1530/jrf.0.0660547)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pi M, Parrill AL & Quarles LD 2010 GPRC6A mediates the non-genomic effects of steroids. Journal of Biological Chemistry 285 39953–39964. (https://doi.org/10.1074/jbc.M110.158063)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rigaudière N, Pelardy G, Robert A & Delost P 1976 Changes in the concentrations of testosterone and androstenedione in the plasma and testis of the guinea-pig from birth to death. Journal of Reproduction and Fertility 48 291–300. (https://doi.org/10.1530/jrf.0.0480291)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Robaire B & Hamzeh M 2011 Androgen action in the epididymis. Journal of Andrology 32 592–599. (https://doi.org/10.2164/jandrol.111.014266)

  • Robaire B & Henderson NA 2006 Actions of 5alpha-reductase inhibitors on the epididymis. Molecular and Cellular Endocrinology 250 190–195. (https://doi.org/10.1016/j.mce.2005.12.044)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Robaire B, Seenundun S, Hamzeh M & Lamour SA 2007 Androgenic regulation of novel genes in the epididymis. Asian Journal of Andrology 9 545–553. (https://doi.org/10.1111/j.1745-7262.2007.00316.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sedlacek RL, Carlin RW, Singh AK & Schultz BD 2001 Neurotransmitter-stimulated ion transport by cultured porcine vas deferens epithelium. American Journal of Physiology: Renal Physiology 281 F557–F570. (https://doi.org/10.1152/ajprenal.2001.281.3.F557)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shum WW, da Silva N, Brown D & Breton S 2009 Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk. Journal of Experimental Biology 212 1753–1761. (https://doi.org/10.1242/jeb.027284)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Skorupskaite K, George JT & Anderson RA 2014 The kisspeptin-GnRH pathway in human reproductive health and disease. Human Reproduction Update 20 485–500. (https://doi.org/10.1093/humupd/dmu009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tan MH, Li J, Xu HE, Melcher K & Yong EL 2015 Androgen receptor: structure, role in prostate cancer and drug discovery. Acta Pharmacologica Sinica 36 3–23. (https://doi.org/10.1038/aps.2014.18)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thomas P, Pang Y, Dong J & Berg AH 2014 Identification and characterization of membrane androgen receptors in the ZIP9 zinc transporter subfamily: II. Role of human ZIP9 in testosterone-induced prostate and breast cancer cell apoptosis. Endocrinology 155 4250–4265. (https://doi.org/10.1210/en.2014-1201)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Turner TT, Ewing LL, Jones CE, Howards SS & Zegeye B 1985 Androgens in male rat reproductive tract fluids: hypophysectomy and steroid replacement. American Journal of Physiology 248 E274–E280. (https://doi.org/10.1152/ajpendo.1985.248.3.E274)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Uenoyama Y, Nakamura S, Hayakawa Y, Ikegami K, Watanabe Y, Deura C, Minabe S, Tomikawa J, Goto T & Ieda N et al.2015 Lack of pulse and surge modes and glutamatergic stimulation of luteinising hormone release in Kiss1 knockout rats. Journal of Neuroendocrinology 27 187–197. (https://doi.org/10.1111/jne.12257)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Viger RS & Robaire B 1992 Expression of 4-ene steroid 5 alpha-reductase messenger ribonucleic acid in the rat epididymis during postnatal development. Endocrinology 131 1534–1540. (https://doi.org/10.1210/endo.131.3.1505481)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wagenfeld A, Yeung CH, Lehnert W, Nieschlag E & Cooper TG 2002 Lack of glutamate transporter EAAC1 in the epididymis of infertile c-ros receptor tyrosine-kinase deficient mice. Journal of Andrology 23 772–782.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wang C, Liu Y & Cao JM 2014 G protein-coupled receptors: extranuclear mediators for the non-genomic actions of steroids. International Journal of Molecular Sciences 15 15412–15425. (https://doi.org/10.3390/ijms150915412)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wang TE, Li SH, Minabe S, Anderson AL, Dun MD, Maeda KI, Matsuda F, Chang HW, Nixon B & Tsai PJ 2018 Mouse quiescin sulfhydryl oxidases exhibit distinct epididymal luminal distribution with segment-specific sperm surface associations. Biology of Reproduction 99 1022–1033. (https://doi.org/10.1093/biolre/ioy125)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu TS & Hammond GL 2014 Naturally occurring mutants inform SHBG structure and function. Molecular Endocrinology 28 1026–1038. (https://doi.org/10.1210/me.2014-1058)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yang R, Browne JA, Eggener SE, Leir SH & Harris A 2018 A novel transcriptional network for the androgen receptor in human epididymis epithelial cells. Molecular Human Reproduction 24 433–443. (https://doi.org/10.1093/molehr/gay029)

    • PubMed
    • Search Google Scholar
    • Export Citation