Receptor-selective determinants in catfish gonadotropin seat-belt loops

Vischer, Henry F.; Marques, Rute B.; Granneman, J.C.M.; Linskens, Maarten H.K.; Schulz, Rüdiger; Bogerd, Jan

doi:10.1016/j.mce.2004.06.011

Cited by 17 publications

(13 citation statements)

References 34 publications

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“…These results confirm previous data obtained using Xenopus laevis oocytes expressing Senegalese sole Fshra and Lhcgrba and European sea bass recombinant gonadotropins [6]. The promiscuous activation of the Fshra by Lh has also been reported in some salmonids [7], catfish [8][9][10], and cyprinids [11,12], but in other teleosts, such as the rainbow trout [15], Manchurian trout [16], and European sea bass [17,18], each gonadotropin seems to exclusively activate specific cognate receptors. Our observations suggest that the cross-activation of the Fshra by Lh is a conserved mechanism in acanthomorph teleosts such as the Senegalese sole.…”

Section: Discussionsupporting

confidence: 90%

“…By using highly purified gonadotropin preparations or homologous recombinant hormones, it has also been shown that the role of gonadotropins in teleost spermatogenesis seems to be more complex than in mammals. Ligandbinding studies indicate that teleost Fshra shows a preference for Fsh, but it can also be activated by Lh [7][8][9][10][11][12][13][14]. However, such receptor promiscuity is apparently not found in the rainbow trout (Onchorynchus mykiss) [15], the Manchurian trout (Brachymystax lenok) [16], or the European sea bass (Dicentrarchus labrax) [17,18].…”

Section: Introductionmentioning

confidence: 99%

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Follicle-Stimulating Hormone and Luteinizing Hormone Mediate the Androgenic Pathway in Leydig Cells of an Evolutionary Advanced Teleost1

Chauvigné

Verdura

Mazón

et al. 2012

Biology of Reproduction

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The endocrine pathways controlling vertebrate spermatogenesis are well established in mammals where the pituitary gonadotropins follicle-stimulating hormone (FSH) and luteinizing hormone (LH) exclusively activate the FSH receptor (FSHR) in Sertoli cells and the LH/choriogonadotropin receptor (LHCGR) in Leydig cells, respectively. In some teleosts, however, it has been shown that Lh can cross-activate the Fshra ortholog, and that Leydig cells coexpress the Lhcgrba and Fshra paralogs, thus mediating the androgenic function of Fsh in the testis. Here, we investigated whether these proposed mechanisms are conserved in an evolutionary advanced pleuronectiform teleost, the Senegalese sole (Solea senegalensis). Transactivation assays using sole Fshra- and Lhcgrba-expressing cells and homologous single-chain recombinant gonadotropins (rFsh and rLh) showed that rFsh exclusively activated Fshra, whereas rLh stimulated both Lhcgrba and Fshra. The latter cross-activation of Fshra by rLh occurred with an EC(50) 4-fold higher than for rFsh. Both recombinant gonadotropins elicited a significant androgen release response in vitro and in vivo, which was blocked by protein kinase A (PKA) and 3beta-hydroxysteroid dehydrogenase inhibitors, suggesting that activation of steroidogenesis through the cAMP/PKA pathway is the major route for both Lh- and Fsh-stimulated androgen secretion. Combined in situ hybridization and immunocytochemistry using cell-specific molecular markers and antibodies specifically raised against sole Fshra and Lhcgrba demonstrated that both receptors are expressed in Leydig cells, whereas Sertoli cells only express Fshra. These data suggest that Fsh-mediated androgen production through the activation of cognate receptors in Leydig cells is a conserved pathway in Senegalese sole.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Follicle-Stimulating Hormone and Luteinizing Hormone Mediate the Androgenic Pathway in Leydig Cells of an Evolutionary Advanced Teleost1

Chauvigné

Verdura

Mazón

et al. 2012

Biology of Reproduction

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“…The promiscuous response of the sbsLhr to mammalian FSHs (hFSH and bFSH) but not to sea bass Fsh could have its basis in the higher similarity in sequence and structure of mammalian FSHs to sea bass Lh than to sea bass Fsh, as we previously proposed [20]. On the other hand, the very weak response of sbsFshr to hFSH, together with the fact that many residues described as important for hFSH/hFSHR binding [53] are lacking in sea bass [20], or that specificity determinants in fish b subunits are not related to charge differences as in mammals [54], would recommend caution when using mammalian models to explain fish Fsh-receptor interactions.…”

Section: Discussionmentioning

confidence: 84%

Receptor Specificity and Functional Comparison of Recombinant Sea Bass (Dicentrarchus labrax) Gonadotropins (Fsh and Lh) Produced in Different Host Systems1

Molés

Zanuy

Muñoz

et al. 2011

Biology of Reproduction

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Different yields, biopotency, and in vivo pharmacokinetics are obtained for recombinant sea bass gonadoltropins depending on the production system and DNA construct, but they show specific activation of their corresponding receptors. Gonadotropins (GTHs) are glycoprotein hormones that play a major role in the regulation of gonadal functions. Recently, we succeeded in isolating the native sea bass Fsh from sea bass pituitaries, but to ensure the availability of bioactive GTHs and no cross-contamination with other related glycoproteins, recombinant sea bass GTHs were produced using two expression systems-insect and mammalian cells-and different constructs that yielded tethered or noncovalently bound dimers. Their production levels, binding specificity to their homologous cognate receptors, and bioactivity were investigated and compared. Both expression systems were successful in the generation of bioactive recombinant GTHs, but insect Sf9 cells yielded higher amounts of recombinant proteins than mammalian Chinese Hamster Ovary (CHO) stable clones. All recombinant GTHs activated their cognate receptors without cross-ligand binding and were able to stimulate sea bass gonadal steroidogenesis in vitro, although with different biopotencies. To assess their use for in vivo applications, their half-life in sea bass plasma was evaluated. Sf9-GTHs had a lower in vivo stability compared with CHO-GTHs due to their rapid clearance from the blood circulation. Cell-dependent glycosylation could be contributing to the final in vivo stability and biopotency of these recombinant glycoproteins. In conclusion, both insect and mammalian expression systems produced bioactive sea bass recombinant gonadotropins, although with particular features useful for different proposes (e.g., antibody production or in vivo studies, respectively).

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“…The selectivity of gonadotropin ligand/receptor interaction in mammals is well defined: FSH and LH bind to their respective cognate receptors specifically and show little cross-reactivity (0.01%-0.1%) (61,62). In contrast, the bioactivity of fish gonadotropins seems to be less well separated as a result of promiscuous ligand-receptor interactions (26,27,(63)(64)(65)(66). Most of the evidence has suggested that the wider but still limited functional selectivity of FSHR for both FSH and LH may depend on the fish species or taxa, whereas fish LHR, like its mammalian counterpart, seems to be more specific for its ligand (1).…”

Section: Discussionmentioning

confidence: 99%

Targeted Gene Disruption in Zebrafish Reveals Noncanonical Functions of LH Signaling in Reproduction

Chu

Liu

et al. 2014

Molecular Endocrinology

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The pivotal role of gonadotropin signaling in regulating gonadal development and functions has attracted much research attention in the past 2 decades. However, the precise physiological role of gonadotropin signaling is still largely unknown in fish. In this study, we have established both LH β-subunit (lhb) and LH receptor (lhr) knockout zebrafish lines by transcription activator-like effector nucleases. Intriguingly, both homozygous lhb and lhr mutant male fish are fertile. The fertilization rate, sperm motility, and histological structure of the testis were not affected in either lhb or lhr mutant males. On the contrary, homozygous lhb mutant females are infertile, whereas homozygous lhr mutant females are fertile. Folliculogenesis was not affected in either lhb or lhr mutants, but oocyte maturation and ovulation were disrupted in lhb mutant, whereas only ovulation was affected in lhr mutant. Differential expression of genes in the ovary involved in steroidogenesis, oocyte maturation, and ovulation was found between the lhb and lhr mutants. These data demonstrate the essential role of LH signaling in oocyte maturation and ovulation, and support the notion that LH acts through the FSH receptor in the absence of LH receptor. Moreover, the defects of lhb mutant could be partially restored by administration of human chorionic gonadotropin. This in vivo evidence in the present study demonstrates, for the first time in any vertebrate species, that LH signaling is indispensable in female reproduction but not in male reproduction. LH signaling is demonstrated to control oocyte maturation and ovulation in the ovary.

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Receptor-selective determinants in catfish gonadotropin seat-belt loops

Cited by 17 publications

References 34 publications

Follicle-Stimulating Hormone and Luteinizing Hormone Mediate the Androgenic Pathway in Leydig Cells of an Evolutionary Advanced Teleost1

Follicle-Stimulating Hormone and Luteinizing Hormone Mediate the Androgenic Pathway in Leydig Cells of an Evolutionary Advanced Teleost1

Receptor Specificity and Functional Comparison of Recombinant Sea Bass (Dicentrarchus labrax) Gonadotropins (Fsh and Lh) Produced in Different Host Systems1

Targeted Gene Disruption in Zebrafish Reveals Noncanonical Functions of LH Signaling in Reproduction

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