Localization of Two Gonadotropin Receptors in the Salmon Gonad by in Vitro Ligand Autoradiography1

Miwa, Satoshi; Yan, Liguang; Swanson, Penny

doi:10.1095/biolreprod50.3.629

Cited by 130 publications

(63 citation statements)

References 51 publications

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“…This observation is in agreement with the expression of the gonadotropin receptor genes in the somatic testicular cells described previously in different teleostean fish species including zebrafish, catfish, eel, and coho salmon (Miwa et al 1994, Ohta et al 2007, Garcia-Lopez et al 2009. We further identified a number of genes upregulated in vitro by both Fsh and Lh that are also found to be naturally and strongly increased at the end of the reproductive cycle, when both gonadotropins and their receptors reach their maximum secretion and expression levels, respectively (Gomez et al 1999).…”

Section: Discussionsupporting

confidence: 91%

“…Among the genes preferentially regulated by Fsh, we found the transcripts that were previously shown to be expressed in the Sertoli cells, such as amh in fish (Skaar et al 2011) and Wisp1, Abca1, Smtn, Krt18, Slc40a1, Col1a1, Ccnd1, and Fstl3 in mice (Chalmel et al 2007). This is in agreement with the fact that the Fsh receptor would be the only gonadotropin receptor expressed in the salmonid Sertoli cells (Miwa et al 1994). The known or putative function of the Fsh-dependent genes will be detailed below.…”

Section: Discussionsupporting

confidence: 89%

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Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis

Sambroni¹,

Rolland²,

Lareyre³

et al. 2012

Journal of Molecular Endocrinology

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The general rules established from mammalian species for the regulation of spermatogenesis by gonadotropins may not be fully relevant in fish. Particularly, Fsh is as potent as Lh to stimulate steroidogenesis and the Fsh receptor is expressed in Leydig cells. In seasonal breeders, Fsh is likely the major gonadotropin involved in spermatogenesis onset and Lh is required to support spermatogenesis progression and gamete release. However, the genes that relay the action of Fsh and Lh have been poorly investigated in fish. The present study was aimed at identifying gonadotropin-dependent genes expressed in the testis during fish puberty. We cultured pubertal trout testicular explants for 96 h, with or without gonadotropin, and analyzed transcriptome variations using microarrays. Fsh and Lh had similar effects on a large group of genes while other genes were preferentially regulated by one or the other gonadotropin. We showed that most of the responsive genes were expressed in somatic cells and exhibited relevant patterns during the seasonal reproductive cycle. Some genes preferentially modulated by Lh could be involved in testicular cell fate (pvrl1 and bty) or sperm maturation (ehmt2 and racgap1) and will deserve further examination. Besides Fsh's effects on the steroidogenic pathway, our study demonstrates that Fsh coordinates relevant stimulatory and inhibitory paracrine factors known to regulate early germ cell proliferation and differentiation. Some of these genes belong to major regulatory pathways including the Igf pathway (igf1b/igf3 and igfbp6), the Tgfb pathway (amh, inha, inhba, and fstl3), the Wnt pathway (wisp1), and pleiotrophin (mdka).

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 89%

Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis

Sambroni¹,

Rolland²,

Lareyre³

et al. 2012

Journal of Molecular Endocrinology

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“…In contrast to the high specificity of r-mtFSH and r-mtLH for their receptors, purified chum salmon FSH activated both types of GTH receptors with a slight preference for FSH-R, while LH did only LH-R (Oba et al 1999a,b). In in vitro ligand autoradiography, coho salmon FSH showed a specific interaction with FSH-R, whereas LH interacted with both FSH-R and LH-R (Miwa et al 1994), which is a similar situation in African catfish , channel catfish (Zmora et al 2003), and zebrafish ). Although we have no clear explanation for these different observations, these results may be attributed to high plasticity of gonadotropin-receptor interaction in teleosts and the use of heterologous GTHs from a different species.…”

Section: (B)mentioning

confidence: 62%

“…This is the first report on production of biologically active recombinant GTHs in salmonids, although pioneering researches on the fish GTHs and GTH receptors were carried out using salmon species (Suzuki et al 1988a,b, Yan et al 1992, Miwa et al 1994, Oba et al 1999a. In order to produce heterodimeric and biologically active recombinant GTHs, single-chain mtFSH and mtLH were constructed in which the carboxyl terminus of the mtFSHb or mtLHb subunit was fused to the amino terminus of the mature mtGTHa subunit with an intermediate polypeptide sequence (NCS).…”

Section: Discussionmentioning

confidence: 99%

Biological activities of recombinant Manchurian trout FSH and LH: their receptor specificity, steroidogenic and vitellogenic potencies

Ko¹,

Park²,

Kim³

et al. 2007

Journal of Molecular Endocrinology

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Gonadotropins (GTHs), FSH and LH, play central roles in vertebrate reproduction. Here, we report the production of biologically-active recombinant FSH (r-mtFSH) and LH (r-mtLH) of an endangered salmon species, Manchurian trout (Brachymystax lenok), by baculovirus in silkworm (Bombyx mori) larvae. The biological activities of the recombinant hormones were analyzed using COS-7 cell line transiently expressing either amago salmon FSH or LH receptor. The steroidogenic potency of the r-mtFSH and r-mtLH was examined by a culture system using rainbow trout follicles in vitro. In vivo, bioactivity was assessed by measuring ovarian weight, oocyte diameter, and plasma steroid hormone levels in female rainbow trout. Moreover, inducing potency of milt production were examined in vivo using goldfish. Our results demonstrated that the r-mtFSH and r-mtLH were successfully produced in the baculovirus-silkworm system and recognized by their cognate receptors specifically in vitro. The production of estradiol-17b (E2) and testosterone (T) was stimulated by the r-mtFSH and r-mtLH respectively, from the full-grown follicles of rainbow trout, whereas both E2 and T were increased by relatively higher doses of the recombinant hormones from the follicles of the maturing stage. In in vivo assay, injection of the r-mtFSH but not r-mtLH increased ovarian weight, oocyte diameter, and plasma E2 levels in immature rainbow trout. Injection of both r-mtFSH and r-mtLH induced milt production in male goldfish. In conclusion, the present study strongly suggests that the r-mtFSH and r-mtLH have distinct biological properties, such as a specific responsiveness for the cognate receptor, steroidogenic, and vitellogenic activities for ovarian follicles in salmonids. These recombinant FSH and LH may be applied for future studies on the gonadal development and maturation in fishes as well as the endangered salmon species.

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“…Few data are available on specific functions of FSH in spermatogenesis in fish; however, studies suggest that FSH stimulates spermatogonial proliferation in trout (Loir 1999) and 11-KT production in vitro (Planas & Swanson 1995). Furthermore, autoradiography studies in salmon localized FSH-R to presumed Sertoli cells, but could not determine whether Leydig cells contained FSH-R (Miwa et al 1994). More recently, Schulz et al (2003) reported that FSH also stimulates proliferation of Sertoli cells in African catfish.…”

Section: -Kt 1720 -P Fsh-r Lh-rmentioning

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

109

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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.

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Localization of Two Gonadotropin Receptors in the Salmon Gonad by in Vitro Ligand Autoradiography1

Cited by 130 publications

References 51 publications

Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis

Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis

Biological activities of recombinant Manchurian trout FSH and LH: their receptor specificity, steroidogenic and vitellogenic potencies

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

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