Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis

Yuichi Ozaki, Masato Higuchi, Chiemi Miura, Sonoko Yamaguchi, Yuzuru Tozawa, Takeshi Miura

Research output: Contribution to journalArticle

58 Citations (Scopus)

Abstract

In fish spermatogenesis, the main action of progestins is generally regarded as the induction of sperm maturation. Our previous in vitro study demonstrated that a progestin, 17α,20β-dihydroxy-4-pregnen-3-one (DHP), induced the initiation of meiosis in spermatogenesis in the Japanese eel (Anguilla japonica). In the present study, to elucidate the molecular mechanisms underlying the action of DHP, we attempted to clone cDNAs encoding genes whose expression was induced by DHP in eel testis, using cDNA subtraction. One of the cDNAs we isolated encodes eel 11β-hydroxysteroid dehydrogenase short form (e11β-HSDsf), and Northern blot and RT-PCR analysis showed that transcripts of e11β-HSDsf in testis were induced by DHP. The recombinant e11β-HSDsf had 11β-dehydrogenase activity, metabolizing cortisol to cortisone, and 11β-hydroxytestosterone to 11-ketotestosterone (11-KT). In vitro experiments revealed that eel immature testis had 11β-dehydrogenase activity, and DHP treatment enhanced the activity. To understand the role of 11β-HSD in spermatogenesis, we examined the direct effects of cortisol on eel spermatogenesis using an organ culture system. Cortisol induced DNA replication in spermatogonia and enhanced the spermatogonial proliferation induced by 11-KT. However, excess cortisol inhibited proliferation. In addition, 11-KT production was induced in testicular fragments incubated with cortisol. These results suggest that optimal levels of cortisol induced spermatogonial mitosis by increasing 11-KT production. Furthermore, two possible roles of DHP on spermatogenesis, via the up-regulation of 11β-HSD expression, are suggested: positive feedback control of 11-KT production and the modulation of cortisol levels to protect testes from excess circulating cortisol.

Original languageEnglish
Pages (from-to)5139-5146
Number of pages8
JournalEndocrinology
Volume147
Issue number11
DOIs
Publication statusPublished - 2006
Externally publishedYes

Fingerprint

11-beta-Hydroxysteroid Dehydrogenases
Eels
Spermatogenesis
Hydrocortisone
Fishes
Testis
Complementary DNA
Progestins
Oxidoreductases
Sperm Maturation
Anguilla
Spermatogonia
Organ Culture Techniques
Cortisone
Meiosis
DNA Replication
Mitosis
Northern Blotting
17,20-dihydroxy-4-pregnen-3-one
Up-Regulation

ASJC Scopus subject areas

  • Endocrinology
  • Endocrinology, Diabetes and Metabolism

Cite this

Ozaki, Y., Higuchi, M., Miura, C., Yamaguchi, S., Tozawa, Y., & Miura, T. (2006). Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis. Endocrinology, 147(11), 5139-5146. https://doi.org/10.1210/en.2006-0391

Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis. / Ozaki, Yuichi; Higuchi, Masato; Miura, Chiemi; Yamaguchi, Sonoko; Tozawa, Yuzuru; Miura, Takeshi.

In: Endocrinology, Vol. 147, No. 11, 2006, p. 5139-5146.

Research output: Contribution to journalArticle

Ozaki, Y, Higuchi, M, Miura, C, Yamaguchi, S, Tozawa, Y & Miura, T 2006, 'Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis', Endocrinology, vol. 147, no. 11, pp. 5139-5146. https://doi.org/10.1210/en.2006-0391
Ozaki Y, Higuchi M, Miura C, Yamaguchi S, Tozawa Y, Miura T. Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis. Endocrinology. 2006;147(11):5139-5146. https://doi.org/10.1210/en.2006-0391
Ozaki, Yuichi ; Higuchi, Masato ; Miura, Chiemi ; Yamaguchi, Sonoko ; Tozawa, Yuzuru ; Miura, Takeshi. / Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis. In: Endocrinology. 2006 ; Vol. 147, No. 11. pp. 5139-5146.
@article{9268a35875884e05a8ba9f66389b6e6c,
title = "Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis",
abstract = "In fish spermatogenesis, the main action of progestins is generally regarded as the induction of sperm maturation. Our previous in vitro study demonstrated that a progestin, 17α,20β-dihydroxy-4-pregnen-3-one (DHP), induced the initiation of meiosis in spermatogenesis in the Japanese eel (Anguilla japonica). In the present study, to elucidate the molecular mechanisms underlying the action of DHP, we attempted to clone cDNAs encoding genes whose expression was induced by DHP in eel testis, using cDNA subtraction. One of the cDNAs we isolated encodes eel 11β-hydroxysteroid dehydrogenase short form (e11β-HSDsf), and Northern blot and RT-PCR analysis showed that transcripts of e11β-HSDsf in testis were induced by DHP. The recombinant e11β-HSDsf had 11β-dehydrogenase activity, metabolizing cortisol to cortisone, and 11β-hydroxytestosterone to 11-ketotestosterone (11-KT). In vitro experiments revealed that eel immature testis had 11β-dehydrogenase activity, and DHP treatment enhanced the activity. To understand the role of 11β-HSD in spermatogenesis, we examined the direct effects of cortisol on eel spermatogenesis using an organ culture system. Cortisol induced DNA replication in spermatogonia and enhanced the spermatogonial proliferation induced by 11-KT. However, excess cortisol inhibited proliferation. In addition, 11-KT production was induced in testicular fragments incubated with cortisol. These results suggest that optimal levels of cortisol induced spermatogonial mitosis by increasing 11-KT production. Furthermore, two possible roles of DHP on spermatogenesis, via the up-regulation of 11β-HSD expression, are suggested: positive feedback control of 11-KT production and the modulation of cortisol levels to protect testes from excess circulating cortisol.",
author = "Yuichi Ozaki and Masato Higuchi and Chiemi Miura and Sonoko Yamaguchi and Yuzuru Tozawa and Takeshi Miura",
year = "2006",
doi = "10.1210/en.2006-0391",
language = "English",
volume = "147",
pages = "5139--5146",
journal = "Endocrinology",
issn = "0013-7227",
publisher = "The Endocrine Society",
number = "11",

}

TY - JOUR

T1 - Roles of 11β-hydroxysteroid dehydrogenase in fish spermatogenesis

AU - Ozaki, Yuichi

AU - Higuchi, Masato

AU - Miura, Chiemi

AU - Yamaguchi, Sonoko

AU - Tozawa, Yuzuru

AU - Miura, Takeshi

PY - 2006

Y1 - 2006

N2 - In fish spermatogenesis, the main action of progestins is generally regarded as the induction of sperm maturation. Our previous in vitro study demonstrated that a progestin, 17α,20β-dihydroxy-4-pregnen-3-one (DHP), induced the initiation of meiosis in spermatogenesis in the Japanese eel (Anguilla japonica). In the present study, to elucidate the molecular mechanisms underlying the action of DHP, we attempted to clone cDNAs encoding genes whose expression was induced by DHP in eel testis, using cDNA subtraction. One of the cDNAs we isolated encodes eel 11β-hydroxysteroid dehydrogenase short form (e11β-HSDsf), and Northern blot and RT-PCR analysis showed that transcripts of e11β-HSDsf in testis were induced by DHP. The recombinant e11β-HSDsf had 11β-dehydrogenase activity, metabolizing cortisol to cortisone, and 11β-hydroxytestosterone to 11-ketotestosterone (11-KT). In vitro experiments revealed that eel immature testis had 11β-dehydrogenase activity, and DHP treatment enhanced the activity. To understand the role of 11β-HSD in spermatogenesis, we examined the direct effects of cortisol on eel spermatogenesis using an organ culture system. Cortisol induced DNA replication in spermatogonia and enhanced the spermatogonial proliferation induced by 11-KT. However, excess cortisol inhibited proliferation. In addition, 11-KT production was induced in testicular fragments incubated with cortisol. These results suggest that optimal levels of cortisol induced spermatogonial mitosis by increasing 11-KT production. Furthermore, two possible roles of DHP on spermatogenesis, via the up-regulation of 11β-HSD expression, are suggested: positive feedback control of 11-KT production and the modulation of cortisol levels to protect testes from excess circulating cortisol.

AB - In fish spermatogenesis, the main action of progestins is generally regarded as the induction of sperm maturation. Our previous in vitro study demonstrated that a progestin, 17α,20β-dihydroxy-4-pregnen-3-one (DHP), induced the initiation of meiosis in spermatogenesis in the Japanese eel (Anguilla japonica). In the present study, to elucidate the molecular mechanisms underlying the action of DHP, we attempted to clone cDNAs encoding genes whose expression was induced by DHP in eel testis, using cDNA subtraction. One of the cDNAs we isolated encodes eel 11β-hydroxysteroid dehydrogenase short form (e11β-HSDsf), and Northern blot and RT-PCR analysis showed that transcripts of e11β-HSDsf in testis were induced by DHP. The recombinant e11β-HSDsf had 11β-dehydrogenase activity, metabolizing cortisol to cortisone, and 11β-hydroxytestosterone to 11-ketotestosterone (11-KT). In vitro experiments revealed that eel immature testis had 11β-dehydrogenase activity, and DHP treatment enhanced the activity. To understand the role of 11β-HSD in spermatogenesis, we examined the direct effects of cortisol on eel spermatogenesis using an organ culture system. Cortisol induced DNA replication in spermatogonia and enhanced the spermatogonial proliferation induced by 11-KT. However, excess cortisol inhibited proliferation. In addition, 11-KT production was induced in testicular fragments incubated with cortisol. These results suggest that optimal levels of cortisol induced spermatogonial mitosis by increasing 11-KT production. Furthermore, two possible roles of DHP on spermatogenesis, via the up-regulation of 11β-HSD expression, are suggested: positive feedback control of 11-KT production and the modulation of cortisol levels to protect testes from excess circulating cortisol.

UR - http://www.scopus.com/inward/record.url?scp=33751238803&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33751238803&partnerID=8YFLogxK

U2 - 10.1210/en.2006-0391

DO - 10.1210/en.2006-0391

M3 - Article

C2 - 16887910

AN - SCOPUS:33751238803

VL - 147

SP - 5139

EP - 5146

JO - Endocrinology

JF - Endocrinology

SN - 0013-7227

IS - 11

ER -