Functional and developmental heterogeneity of pituitary lactotropes in medaka

Royan, Muhammad Rahmad; Siddique, Khadeeja; Nourizadeh-Lillabadi, Rasoul; Weltzien, Finn‐Arne; Henkel, Christiaan V.; Fontaine, Romain

doi:10.1016/j.ygcen.2022.114144

Cited by 3 publications

(1 citation statement)

References 74 publications

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“…RNAscope was performed as previously described (85). After euthanasia, the blood was removed by cardiac perfusion as described previously (86) with 4% PFA (PBS).…”

Section: Identification Of the Cells Expressing Tsh Receptors With Rn...mentioning

confidence: 99%

Photoperiod regulates gonadotrope cell division in medaka via melatonin, Tsh and folliculostellate cells

Royan,

Hodne,

Nourizadeh-lillabadi

et al. 2023

Preprint

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In vertebrates, pituitary gonadotropins (follicle-stimulating and luteinizing hormones: FSH and LH) regulate gonadal development and maturation, therefore playing an essential role in reproduction. The seasonal regulation of gonadotropins has been widely studied in mammals and birds, and in these taxa thyroid-stimulating hormone (TSH) was found to play a critical role. By contrast, the seasonal regulation of gonadotropins remains unclear in teleost fish. In addition, the seasonal regulation of gonadotrope (gonadotropin-producing cell) proliferation has not been elucidated in any vertebrate group. Using the teleost fish medaka as a model, we show for the first time that long photoperiod enables reproduction by stimulating gonadotropin mRNA synthesis and gonadotrope cell proliferation. In female medaka, this proliferation is achieved by gonadotrope mitosis. We then demonstrate that in female medaka, photoperiod stimulates gonadotropin mRNA production and mitosis via an indirect intra-pituitary pathway, involving pituitary Tsh cells. We show that non-endocrine folliculostellate cells in the pituitary mediate the Tsh signal regulating gonadotrope activity and proliferation, as they are the only pituitary cells to express Tsh receptors and send projections to gonadotropes. Finally, we show that melatonin suppresses pituitary tshba expression in fish exposed to long photoperiod, suggesting that short photoperiod inhibits gonadotropin synthesis via melatonin in both fish and mammals. This study therefore demonstrates that in fish, photoperiod regulates gonadotrope cell activity and mitosis via a melatonin-Tsh pathway. It also reveals the existence of a novel intra-pituitary pathway for seasonal regulation of gonadotropes, involving folliculostellate cells, which we propose might also exist in other vertebrates.

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“…RNAscope was performed as previously described (85). After euthanasia, the blood was removed by cardiac perfusion as described previously (86) with 4% PFA (PBS).…”

Section: Identification Of the Cells Expressing Tsh Receptors With Rn...mentioning

confidence: 99%

Photoperiod regulates gonadotrope cell division in medaka via melatonin, Tsh and folliculostellate cells

Royan,

Hodne,

Nourizadeh-lillabadi

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

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Day length regulates gonadotrope proliferation and reproduction via an intra-pituitary pathway in the model vertebrate Oryzias latipes

Royan,

Hodne,

Nourizadeh-Lillabadi

et al. 2024

Commun Biol

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In seasonally breeding mammals and birds, the production of the hormones that regulate reproduction (gonadotropins) is controlled by a complex pituitary-brain-pituitary pathway. Indeed, the pituitary thyroid-stimulating hormone (TSH) regulates gonadotropin expression in pituitary gonadotropes, via dio2-expressing tanycytes, hypothalamic Kisspeptin, RFamide-related peptide, and gonadotropin-releasing hormone neurons. However, in fish, how seasonal environmental signals influence gonadotropins remains unclear. In addition, the seasonal regulation of gonadotrope (gonadotropin-producing cell) proliferation in the pituitary is, to the best of our knowledge, not elucidated in any vertebrate group. Here, we show that in the vertebrate model Japanese medaka (Oryzias latipes), a long day seasonally breeding fish, photoperiod (daylength) not only regulates hormone production by the gonadotropes but also their proliferation. We also reveal an intra-pituitary pathway that regulates gonadotrope cell number and hormone production. In this pathway, Tsh regulates gonadotropes via folliculostellate cells within the pituitary. This study suggests the existence of an alternative regulatory mechanism of seasonal gonadotropin production in fish.

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Sexually Dimorphic Regulation of Gonadotrope Cell Hyperplasia in Medaka Pituitary via Mitosis and Transdifferentiation

et al. 2023

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The two pituitary gonadotropins, FSH and LH, regulate the reproductive function in all vertebrates. While many studies have investigated the regulation of gonadotropin production and release by the sex steroid feedback, its role on the regulation of gonadotrope cell number remains unclear. Using medaka as a model and an optimized protocol to restore physiological sex steroids levels following gonadectomy, we show that gonadal sex steroids not only decrease fshb transcript levels, but also Fsh cell number in both sexes. We then investigated the origin of the Fsh cell hyperplasia induced by gonadectomy. In both sexes, BrdU incubation shows that this is achieved via Fsh cell mitosis. In situ hybridization reveals that new Fsh cells also originate from transdifferentiating Tsh cells in females, but not in males. Both phenomena are inhibited by sex steroid supplementation via feeding. In males (but not females), gonadectomy (without recovery with sex steroid supplementation) also reduces sox2 transcript levels and Sox2-immunopositive population size, suggesting that sox2-progenitors may be recruited to produce new Fsh cells. Opposite to Fsh cells, gonadectomy decreases lhb levels in both sexes, and levels are not restored by sex steroid supplementation. In addition, the regulation of Lh cell number also seems to be sex dependent. Removal of gonadal sex steroids stimulates Lh cell mitosis in male (like Fsh cells), but not in females. To conclude, our study provides the first evidence on sexually dimorphic mechanisms used in the fish pituitary to remodel gonadotrope populations in response to sex steroids.

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Functional and developmental heterogeneity of pituitary lactotropes in medaka

Cited by 3 publications

References 74 publications

Photoperiod regulates gonadotrope cell division in medaka via melatonin, Tsh and folliculostellate cells

Photoperiod regulates gonadotrope cell division in medaka via melatonin, Tsh and folliculostellate cells

Day length regulates gonadotrope proliferation and reproduction via an intra-pituitary pathway in the model vertebrate Oryzias latipes

Sexually Dimorphic Regulation of Gonadotrope Cell Hyperplasia in Medaka Pituitary via Mitosis and Transdifferentiation

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