Differential Regulation of Gonadotropins as Revealed by Transcriptomes of Distinct LH and FSH Cells of Fish Pituitary

Abstract

From mammals to fish, reproduction is driven by luteinizing hormone (LH) and follicle-stimulating hormone (FSH) temporally secreted from the pituitary gland. Teleost fish are an excellent model for addressing the unique regulation and function of each gonadotropin cell since, unlike mammals, they synthesize and secrete LH and FSH from distinct cells. Only very distant vertebrate classes (such as fish and birds) demonstrate the mono-hormonal strategy, suggesting a potential convergent evolution. Cell-specific transcriptome analysis of double-labeled transgenic tilapia expressing GFP and RFP in LH or FSH cells, respectively, yielded genes specifically enriched in each cell type, revealing differences in hormone regulation, receptor expression, cell signaling, and electrical properties. Each cell type expresses a unique GPCR signature that reveals the direct regulation of metabolic and homeostatic hormones. Comparing these novel transcriptomes to that of rat gonadotrophs revealed conserved genes that might specifically contribute to each gonadotropin activity in mammals, suggesting conserved mechanisms controlling the differential regulation of gonadotropins in vertebrates.

Pituitary Gonadotropin Gene Expression During Induced Onset of Postsmolt Maturation in Male Atlantic Salmon: In Vivo and Tissue Culture Studies

“…Previous work suggests that, different from mammals, gonadotropic hormones are produced and secreted by distinct endocrine cells in the teleost pituitary ( 60 , 61 ). Studies using transgenic zebrafish and tilapia ( Oreochromis niloticus ) expressing fluorescence-tagged gonadotropes ( 62 ) and single-cell RNAseq of tilapia pituitaries ( 63 ) confirmed that Fsh and Lh are synthesized and secreted from distinct cells. However, a study in medaka that combined multi-color in situ hybridization (ISH) and single-cell RNAseq analyses revealed the existence of a small fraction (4%) among the gonadotrophs co-expressing fshb and lhb ( 64 ).…”

“…Despite the essential role of androgens, such as T and 11-KT in male reproductive physiology also in fish ( 101 – 103 ), not a single gene annotated as being androgen-specific, was significantly regulated in our RNAseq study. Literature describing cell type-specific androgen receptor expression at the pituitary level is not available in salmonids to date, but in tilapia three different androgen receptor paralogs were enriched specifically in Fsh cells ( 63 ). Evidence for a direct effect of androgens comes from studies, in which non-aromatizable, 11-oxygenated androgens increased lhb transcript levels in three teleost species [Atlantic salmon parr ( 15 ), African catfish ( 99 ) or stickleback ( 100 )].…”

Screening and Validation of p38 MAPK Involved in Ovarian Development of Brachymystax lenok

“…However, no serious tissue damage was caused to the hypothalamus. FSH and LH are secreted by the anterior pituitary gland, and FSH binds to specific receptors and stimulates the formation of LH receptors ( 77 , 78 ). In addition, FSH acts synergistically with LH to promote follicle maturation and stimulate E2 synthesis and secretion in the ovary ( 79 , 80 ).…”

Transcriptomes of testis and pituitary from male Nile tilapia (O. niloticus L.) in the context of social status

“…A recent study by Hollander-Cohen et al . [ 66 ] further showed that Gnrhr3 is enriched in Lh-cells from tilapia pituitaries while Gnrhr1 is enriched in Fsh-cells.…”

“…In non-reproducing fish however, Prl decreased Lh induced testosterone secretion. Recently, it was further reported that prolactin transcripts were enriched in the Lh secreting gonadotrophs of male Nile tilapia [ 66 ]. In summary, our present study adds another clue as for the involvement of prolactin in modulating hormone levels in dominant and subordinate fish.…”