Role of ovarian thecal and granulosa layers in gonadotropin-induced synthesis of a salmonid maturation-inducing substance (17α,20β-dihydroxy-4-pregnen-3-one)

In vertebrates, sperm development and maturation are directly regulated by gonadal steroid hormone secretion. The relationships among the expression of genes encoding steroidogenic proteins and receptors for gonadotropins, and testicular steroid production have not yet been comprehensively determined in male teleosts. In this study, the changes in levels of mRNAs encoding follicle-stimulating hormone (FSH) receptor, luteinizing hormone (LH) receptor, steroidogenic acute regulatory protein (StAR), cytochrome P450 cholesterol side-chain cleavage, 3 -hydroxysteroid dehydrogenase/n5-4-isomerase, cytochrome P450 17 -hydroxylase/17,20-lyase, cytochrome P450 11 -hydroxylase, 11 -hydroxysteroid dehydrogenase and 20 -hydroxysteroid dehydrogenase were determined by real-time, quantitative PCR assays and related to changes in serum steroid levels throughout the reproductive cycle in male rainbow trout. Serum 11-ketotestosterone and 17 ,20 -dihydroxy-4-pregnen-3-one levels were measured by RIA. Although the pattern of change in the mRNA levels for the enzymes was variable, the increases in steroidogenic enzyme mRNAs started prior to a significant increase of serum steroid levels. The patterns of transcript levels of FSH and LH receptors suggest that changes in StAR and steroidogenic enzyme transcripts are largely mediated by the FSH receptor during early and mid-spermatogenesis and by the LH receptor during late spermatogenesis and spermiation. Levels of StAR (10-fold) and P450 17 -hydroxylase/ 17,20-lyase (sevenfold) transcripts changed with the greatest magnitude and were closely related to the changes in serum steroids, suggesting that changes in StAR and P450 17 -hydroxylase/17,20-lyase abundance are likely to be the major influences on overall steroidogenic output during the reproductive cycle in male rainbow trout.

show abstract

“…Levels of 11-KT and 17 ,20 -P were measured by RIA, as previously described (Kagawa et al 1981, Ueda et al 1985, Young et al 1986). …”

Section: Serum Sex Steroidsmentioning

confidence: 99%

Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes

Kusakabe¹,

Nakamura²,

Evans³

et al. 2006

Journal of Endocrinology

110

View full text Add to dashboard Cite

show abstract

“…The in vitro studies also demonstrated that isolated theca layers produced a substantial amount of 17OHP in response to partially purified chinook salmon gonadotropin (SG-G100; see 16) exposure, but granulosa layers did not (12). Furthermore, the studies found that both theca and granulosa layers are incapable of producing DHP by themselves; however, a co-culture of both layers can be induced to produce DHP by SG-G100, and a substantial amount of DHP can be synthesized from 17OHP by isolated granulosa layers incubated with SG-G100 (12). These findings clearly indicate that DHP is synthesized in the granulosa layer from 17OHP that is produced and delivered from the theca layer.…”

Section: Introductionmentioning

confidence: 97%

“…In salmonid fish, including the masu salmon (Oncorhynchus masou), a sharp increase in serum DHP occurs around FOM and during the subsequent ovulation period (8)(9)(10), and in the 1980s, a series of in vitro studies using salmonid ovarian follicles demonstrated the hormonal control of DHP production (8,(11)(12)(13)(14)(15). Those studies reported that ovarian follicles (comprised of oocytes, granulosa layers, and theca layers) acquired the ability to produce DHP after completion of vitellogenic growth in response to the release of gonadotropin (8) or exposure to dibutyryl cAMP (13).…”

Section: Introductionmentioning

confidence: 99%

“…Those studies reported that ovarian follicles (comprised of oocytes, granulosa layers, and theca layers) acquired the ability to produce DHP after completion of vitellogenic growth in response to the release of gonadotropin (8) or exposure to dibutyryl cAMP (13). The in vitro studies also demonstrated that isolated theca layers produced a substantial amount of 17OHP in response to partially purified chinook salmon gonadotropin (SG-G100; see 16) exposure, but granulosa layers did not (12). Furthermore, the studies found that both theca and granulosa layers are incapable of producing DHP by themselves; however, a co-culture of both layers can be induced to produce DHP by SG-G100, and a substantial amount of DHP can be synthesized from 17OHP by isolated granulosa layers incubated with SG-G100 (12).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon¹²

et al. 2016

Self Cite

View full text Add to dashboard Cite

Abbreviated title: 17β-HSD12-like responsible for DHP production Key terms: 17α,20β-dihydroxy-4-pregnen-3-one, 20β-hydroxysteroid dehydrogenase, 17β-hydroxysteroid dehydrogenase, Oocyte maturation, Granulosa, Masu salmon, Oncorhynchus masou AbstractThe maturation-inducing hormone 17α,20β-dihydroxy-4-pregnen-3-one (DHP) was first identified in the amago salmon. However, although carbonyl reductase-like 20β-hydroxysteroid dehydrogenase (CR/20β-HSD) was reported to convert 17α-hydroxyprogesterone (17OHP) to DHP in rainbow trout, we previously found that CR/20β-HSD mRNA was not up-regulated in stimulated granulosa cells from masu salmon, which suggested that DHP is synthesized by a different enzyme. Accordingly, the present study aimed to identify the specific 20β-hydroxysteroid dehydrogenase (20β-HSD) responsible for DHP production by granulosa cells during final oocyte maturation in masu salmon. RNA-sequencing was performed on granulosa layers that were isolated from ovarian follicles at one month before ovulation and incubated with or without forskolin, which was used to mimic luteinizing hormone, and ~12 million reads were obtained, which yielded 71,062 contigs of > 100 bp. tBlastx analysis identified one contig (#f103496) as similar to 17β-hydroxysteroid dehydrogenase type 12 (hsd17β12); however, because the fulllength #f103496 sequence was different from hsd17β12, it was termed to hsd17β12-like (hsd17β12l). We found that mammalian cells transfected with full-length hsd17β12l exhibited considerable 20β-HSD activity, as indicated by efficient conversion of exogenous 17OHP to DHP. In addition, we found that hsd17β12l mRNA levels were consistently low in follicles during vitellogenic growth; however, the levels increased significantly during final oocyte maturation. The levels of hsd17β12l mRNA were also considerably increased in granulosa layers in which 20β-HSD activity was induced by salmon pituitary extract. Therefore, we suggest that hsd17β12l, not CR/20β-HSD, is the 20β-HSD responsible for DHP production by granulosa cells in masu salmon during final oocyte maturation.

show abstract

“…Elevated concentrations of plasma T were observed in black porgy by injection of DAla 6 , des-Gly 10 LH-RH ethylamide (without microencapsulation) during the prespawning season (Chang ef al, 1991 The effects of prolonged stimulation by the released LH-RH analog might affect the production of gonadal steroids in black porgy. T, 11-KT, 17a-OH P and 17a, 20p-dihydroxy-4-pregnen-3-one (17a, 20p-diOH P) are involved in spermatogenesis, spermiation and oocyte maturation in fish (Billard et al, 1982;Young et al, 1986). Because of the unavailability of assays for 17a, 20p-diOH P, 11-KT and black porgy gonadotropin, only T, E2 and 17a-OH P were measured in the present study.…”

Section: Introductionmentioning

confidence: 90%

A microencapsulated analog of LH-RH accelerates maturation but without stimulating sex reversal in the protandrous black porgy, Acanthopagrus schlegeli

Chang¹,

Yueh²,

Lee³

et al. 1995

Reprod. Nutr. Dev.

View full text Add to dashboard Cite

Summary ― The objective of this study was to regulate the reproduction and levels of gonadal steroids in 3-year-old protandrous black porgy (Acanthopagrus schlegeli) by treatment with microencapsulated o-Trp s -luteinizing hormone-releasing hormone (LH-RH analog) during the prespawning season. Twenty-four previously male black porgy were equally divided into 2 groups and injected with vehicle (control group) or with microencapsulated LH-RH analog (LH-RH analog group), respectively. Spermiation and plasma levels of testosterone (T), estradiol-1 7p (E2) and 17a-hydroxyprogesterone (17a-OH P) were measured, after treatment, at intervals of 1-2 weeks for 4 months. Oocyte diameters were also measured after 4, 10, 12, 14 and 16 weeks of treatment. The microencapsulated LH-RH analog accelerated the onset of spermiation by at least 5 weeks. Oocyte diameters were also significantly increased in the LH-RH analog group. The microencapsulated LH-RH analog did not increase the number of sex-reversing females compared with the number in the control group. High levels of plasma E2 were found in the sex-reversing females in the LH-RH analog and control groups during the prespawning and spawning season. Low levels of plasma E2 were observed in the non-reversed males in both the LH-RH analog and the control groups. Similar profiles of plasma T levels were detected in male and in reversing female black porgy in the LH-RH analog and control groups. Plasma 17a-OH P levels were low and constant throughout the experimental period in fish in each group. These findings indicate that the microencapsulated LH-RH analog accelerated gonadal maturation in the black porgy during the prespawning season. Plasma levels of E2 seem to be closely related to the occurrence of natural sex reversal in the protandrous black porgy, A schlegeli.

show abstract

Role of ovarian thecal and granulosa layers in gonadotropin-induced synthesis of a salmonid maturation-inducing substance (17α,20β-dihydroxy-4-pregnen-3-one)

Cited by 83 publications

References 23 publications

Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes

Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes

17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon¹²

A microencapsulated analog of LH-RH accelerates maturation but without stimulating sex reversal in the protandrous black porgy, Acanthopagrus schlegeli

Contact Info

Product

Resources

About

Role of ovarian thecal and granulosa layers in gonadotropin-induced synthesis of a salmonid maturation-inducing substance (17α,20β-dihydroxy-4-pregnen-3-one)

Cited by 83 publications

References 23 publications

Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes

Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes

17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon12

A microencapsulated analog of LH-RH accelerates maturation but without stimulating sex reversal in the protandrous black porgy, Acanthopagrus schlegeli

Contact Info

Product

Resources

About

17β-HSD type 12-like is responsible for maturation-inducing hormone synthesis during oocyte maturation in masu salmon¹²