Abstract
The gonadotropins, follicle-stimulating hormone (FSH) and luteinizing hormone (LH), are secreted from the pituitary and bind to the FSH receptor (FSHR) and LH receptor (LHR) to regulate gonadal development in vertebrates. Previously, using fshr-knockout (KO) medaka (Oryzias latipes), we demonstrated that FSH regulates ovarian development by elevating estrogen levels. However, the lhr-KO phenotype in medaka is poorly characterized. Here, we generated lhr-KO medaka using the transcription activator-like effector nuclease (TALEN) technique. We analyzed its phenotype and that of fshr-KO, lhr;fshr double-heterozygotes (double-hetero), and double-KO fish. All genetically male medaka displayed normal testes and were fertile, whereas fshr-KO and double-KO genetically female fish displayed small ovaries containing many early pre-vitellogenic oocytes and were infertile. Although lhr-KO genetically female fish had normal ovaries with full-grown oocytes, ovulation did not occur. Levels of 17α,20β-dihydroxy-4-pregnen-3-one, which is required for meiotic maturation of oocytes and sperm maturation in teleost fish, were significantly decreased in all KO female medaka ovaries except for double-heteros. Further, 17β-estradiol levels in fshr-KO and double-KO ovaries were significantly lower than those in double-heteros. These findings indicate that LH is necessary for oocyte maturation and FSH is necessary for follicle development, but that neither are essential for spermatogenesis in medaka.
Highlights
Gonadotropin-releasing hormone (GnRH) released from the hypothalamus stimulates the pituitary gland to secrete follicle-stimulating hormone (FSH) and luteinizing hormone (LH), two gonadotropins responsible for gonadal development [1,2]
Using fshr single-KO (fshr-KO) medaka (Oryzias latipes), we have recently demonstrated that FSH regulates ovarian development and maintenance, mainly by elevating estrogen levels [15]. fshr-KO male medaka show normal testes and are fertile, whereas female medaka display small ovaries and are infertile
The present results show that folliculogenesis in fshr-KO and lhr;fshr doubleKO females was halted at the previtellogenic stage (Figure 2G,H)
Summary
Gonadotropin-releasing hormone (GnRH) released from the hypothalamus stimulates the pituitary gland to secrete follicle-stimulating hormone (FSH) and luteinizing hormone (LH), two gonadotropins responsible for gonadal development [1,2]. Fshr-KO male medaka show normal testes and are fertile, whereas female medaka display small ovaries and are infertile. These results indicate that the FSH signal via FSHR/Fshr is necessary for ovarian development but is not important for spermatogenesis in mammals and fish. By generating KOs of the gonadotropin receptors in medaka, which are phylogenetically distant from Zebrafish, and analyzing their phenotypes, we can better understand FSH and LH signaling in sexual development and reproduction. To reveal gonadotropin receptor function in the sexual development of medaka, we first generated lhr single-KO (lhr-KO) medaka using the TALEN technique and analyzed its phenotype and sex steroid hormone expression pattern. We generated lhr;fshr double-heterozygotes (double-hetero), lhr heterozygote;fshr single-KO (fshr-KO), and lhr;fshr double-KO (double-KO) medaka to investigate the function of the two gonadotropin receptors in gonadal development and reproduction
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