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19 pages, 4593 KiB

Open AccessArticle

Morphological and Molecular Gonadal Sex Differentiation in the Wild Japanese eel Anguilla japonica

by Moemi Horiuchi, Seishi Hagihara, Manabu Kume, Daichi Chushi, Yuya Hasegawa, Hikaru Itakura, Yoh Yamashita, Shinji Adachi and Shigeho Ijiri

Cells 2022, 11(9), 1554; https://doi.org/10.3390/cells11091554 - 5 May 2022

Cited by 6 | Viewed by 3985

Abstract

Most cultured Japanese eels (Anguilla japonica) show male sex differentiation; however, natural gonadal sex differentiation has not been evaluated. In this study, this process was characterized in wild eels. Differentiated ovaries and testes were observed after the eels grew to 320 [...] Read more.

Most cultured Japanese eels (Anguilla japonica) show male sex differentiation; however, natural gonadal sex differentiation has not been evaluated. In this study, this process was characterized in wild eels. Differentiated ovaries and testes were observed after the eels grew to 320 and 300 mm in total length, respectively. The youngest ovary and testis appeared at 3 and 4 years old, respectively; however, undifferentiated gonads were found up to 7 years, suggesting that sex differentiation was triggered by growth rather than aging. gsdf, amh, foxl2b and foxl3b were highly expressed in the testes, whereas figla, sox3, foxn5, zar1, and zp3 were highly expressed in the ovaries. The expression of cyp19a1a and foxl2a did not differ significantly between the testis and ovary. In the ovaries, the cyp19a1a and foxl2a levels were highest in the early stages, suggesting that their function is limited to early ovarian differentiation. The foxn5, zar1 and zp3 levels tended to increase in the later stages, suggesting that they function after the initiation of ovarian differentiation. In undifferentiated gonads, dimorphic gene expression was not observed, suggesting that the molecular sex differentiation phase is short and difficult to detect. These findings provide the first demonstration of the whole course of natural gonadal sex differentiation in eels at molecular and morphological levels. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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19 pages, 1967 KiB

Open AccessArticle

Are Cell Junctions Implicated in the Regulation of Vitellogenin Uptake? Insights from an RNAseq-Based Study in Eel, Anguilla australis

by Lucila Babio, P. Mark Lokman, Erin L. Damsteegt and Ludovic Dutoit

Cells 2022, 11(3), 550; https://doi.org/10.3390/cells11030550 - 4 Feb 2022

Cited by 1 | Viewed by 3048

Abstract

At the onset of puberty, ovarian follicles become competent to incorporate large amounts of vitellogenin (Vtg). Using an RNAseq-based approach, transcriptomes from pre-vitellogenic (PV) and early vitellogenic (EV) ovaries from wild-caught eel, Anguilla australis, were compared to investigate the expression of specific [...] Read more.

At the onset of puberty, ovarian follicles become competent to incorporate large amounts of vitellogenin (Vtg). Using an RNAseq-based approach, transcriptomes from pre-vitellogenic (PV) and early vitellogenic (EV) ovaries from wild-caught eel, Anguilla australis, were compared to investigate the expression of specific genes encoding cell junction proteins that could be involved in regulating Vtg uptake. Partial support was found for the mechanical barrier hypothesis proposing that the access of Vtg to the oolemma is restricted by a tight junction (TJ) network within the granulosa cell layer, which changes between the PV and EV stage. Among 25 genes encoding TJ-constituting proteins, five were down-regulated and two were up-regulated. A chemical barrier hypothesis stating that gap junctions (GJs) are involved in modulating Vtg uptake was not supported, as only five GJs were found to be expressed in the ovary with no significant changes in expression between stages. Furthermore, the endocytic pathway was found to be up-regulated during the PV-EV transition. Finally, the study showed that gene expression patterns may help identify suitable candidates involved in the regulation of Vtg uptake, and provided novel sequence data for A. australis, including putative Vtg receptors corresponding to Lr8 and Lrp13 members of the low-density lipoprotein receptor family. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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15 pages, 2107 KiB

Open AccessArticle

Male Pheromones Induce Ovulation in Female Honeycomb Groupers (Epinephelus merra): A Comprehensive Study of Spawning Aggregation Behavior and Ovarian Development

by Takafumi Amagai, Daisuke Izumida, Ryosuke Murata and Kiyoshi Soyano

Cells 2022, 11(3), 484; https://doi.org/10.3390/cells11030484 - 30 Jan 2022

Cited by 5 | Viewed by 3160

Abstract

This study characterizes the spawning phenomena of the honeycomb grouper (Epinephelus merra), which is a lunar-synchronized spawner that spawns a few days after full moon. To elucidate the aggregation characteristics of wild honeycomb groupers, the numbers of males and females at [...] Read more.

This study characterizes the spawning phenomena of the honeycomb grouper (Epinephelus merra), which is a lunar-synchronized spawner that spawns a few days after full moon. To elucidate the aggregation characteristics of wild honeycomb groupers, the numbers of males and females at the spawning grounds were counted before and after the full moon. Approximately 20 males were consistently observed at the spawning grounds throughout the study period. Females appeared several days after full moon and rapidly increased in number, peaking four days after full moon (41 individuals). The maturation status of the females aggregating at the spawning grounds was investigated. The gonadosomatic index increased rapidly three days after full moon, and ovulation was confirmed. Individuals with ovulatory eggs were present for three days, after which the number of females at the spawning grounds decreased. Additionally, the role of males in final oocyte maturation (FOM) and ovulation in females during the spawning phase was investigated in captivity. FOM was induced in females reared in water with mature males, suggesting that male pheromones in the water induced FOM via activation of the hypothalamic–pituitary–gonadal axis. This suggests that spawning at the natural spawning grounds was the result of male–female interactions via pheromones. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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11 pages, 1676 KiB

Open AccessFeature PaperArticle

Roles of Gonadotropin Receptors in Sexual Development of Medaka

by Takeshi Kitano, Tomoaki Takenaka, Hisanori Takagi, Yasutoshi Yoshiura, Yukinori Kazeto, Toshiaki Hirai, Koki Mukai and Ryo Nozu

Cells 2022, 11(3), 387; https://doi.org/10.3390/cells11030387 - 24 Jan 2022

Cited by 12 | Viewed by 3814

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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15 pages, 2788 KiB

Open AccessArticle

Leptin Is an Important Endocrine Player That Directly Activates Gonadotropic Cells in Teleost Fish, Chub Mackerel

by Hirofumi Ohga, Kosuke Ito, Kohei Kakino, Hiroaki Mon, Takahiro Kusakabe, Jae Man Lee and Michiya Matsuyama

Cells 2021, 10(12), 3505; https://doi.org/10.3390/cells10123505 - 11 Dec 2021

Cited by 7 | Viewed by 2918

Abstract

Leptin, secreted by adipocytes, directly influences the onset of puberty in mammals. Our previous study showed that leptin stimulation could promote the secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from pituitary cells in primary culture and ovarian development in chub mackerel. [...] Read more.

Leptin, secreted by adipocytes, directly influences the onset of puberty in mammals. Our previous study showed that leptin stimulation could promote the secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from pituitary cells in primary culture and ovarian development in chub mackerel. This study aimed to elucidate the detailed mechanism of leptin-induced effects on gonadotropin hormone-producing cells. We produced recombinant leptin using silkworm pupae and investigated the effects of leptin on FSH and LH secretion and gene expression in the primary culture of pituitary cells from chub mackerel. The presence or absence of co-expression of lepr mRNA, FSH and LH b-subunit mRNA in gonadotropic cells was examined by double-labeled in situ hybridization. The addition of leptin significantly increased the secretion and gene expression of FSH and LH from male and female pituitary cells in primary culture. In contrast, gonadotropin-releasing hormone 1 affected neither FSH secretion in cells from females nor fshb and lhb expression in cells from males and females. The expression of lepr was observed in FSH- and LH-producing cells of both males and females. The results indicate that leptin directly regulates gonadotropin synthesis and secretion and plays an important role in the induction of puberty in teleost fish. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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17 pages, 3470 KiB

Open AccessArticle

Neurohypophysial Hormones Associated with Osmotic Challenges in the Brain and Pituitary of the Euryhaline Black Porgy, Acanthopagrus schlegelii

by Adimoolam Aruna, Chien-Ju Lin, Ganesan Nagarajan and Ching-Fong Chang

Cells 2021, 10(11), 3086; https://doi.org/10.3390/cells10113086 - 9 Nov 2021

Cited by 7 | Viewed by 2089

Abstract

Our study showed differential expression of the arginine vasotocin (avt)/isotocin (it) in the brain and pituitary gland of the euryhaline black porgy (Acanthopagrus schlegelii) during osmotic stress. A decrease in serum osmolality and increased cortisol levels [...] Read more.

Our study showed differential expression of the arginine vasotocin (avt)/isotocin (it) in the brain and pituitary gland of the euryhaline black porgy (Acanthopagrus schlegelii) during osmotic stress. A decrease in serum osmolality and increased cortisol levels were observed after acute transfer from seawater (SW) to freshwater (FW). The increased expressions of avt, avt receptor (avtr: v1a), and isotocin receptor (itr: itr1) transcripts on day 1 and it and itr transcripts on days 7 and 30 were found in the brains and pituitary glands of FW fish. Increased levels of avt mRNA in the diencephalon and avtr mRNA in the pituitary together with serum cortisol on day 1 of FW exposure indicated activation of the hypothalamic–pituitary–interrenal (HPI) axis. The expression levels of avtr and itr after FW transfer were increased in the pituitary on days 7 and 30. Furthermore, in situ hybridization demonstrated spatially differential expression of avt and itr transcripts in nucleus preopticus parvocellularis of pars gigantocellularis (PMgc), magnocellularis (PMmc), and parvocellularis (PMpc) of the preoptic area (POA). Positive signals for avt and it were highly abundant in PMpc after FW exposure. The data suggest involvement of neurohypophysial hormones in the brain (telencephalon and diencephalon) and pituitary for osmotic stress. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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29 pages, 5807 KiB

Open AccessArticle

Involvement of Transforming Growth Factor Beta Family Genes in Gonadal Differentiation in Japanese Eel, Anguilla japonica, According to Sex-Related Gene Expressions

by Chien-Ju Lin, Shan-Ru Jeng, Zhen-Yuan Lei, Wen-Shiun Yueh, Sylvie Dufour, Guan-Chung Wu and Ching-Fong Chang

Cells 2021, 10(11), 3007; https://doi.org/10.3390/cells10113007 - 4 Nov 2021

Cited by 8 | Viewed by 3302

Abstract

The gonochoristic feature with environmental sex determination that occurs during the yellow stage in the eel provides an interesting model to investigate the mechanisms of gonadal development. We previously studied various sex-related genes during gonadal sex differentiation in Japanese eels. In the present [...] Read more.

The gonochoristic feature with environmental sex determination that occurs during the yellow stage in the eel provides an interesting model to investigate the mechanisms of gonadal development. We previously studied various sex-related genes during gonadal sex differentiation in Japanese eels. In the present study, the members of transforming growth factor beta (TGF-β) superfamily were investigated. Transcript levels of anti-Müllerian hormone, its receptor, gonadal soma-derived factor (amh, amhr2, and gsdf, respectively) measured by real-time polymerase chain reaction (qPCR) showed a strong sexual dimorphism. Transcripts were dominantly expressed in the testis, and their levels significantly increased with testicular differentiation. In contrast, the expressions of amh, amhr2, and gsdf transcripts were low in the ovary of E2-feminized female eels. In situ hybridization detected gsdf (but not amh) transcript signals in undifferentiated gonads. amh and gsdf signals were localized to Sertoli cells and had increased significantly with testicular differentiation. Weak gsdf and no amh signals were detected in early ovaries of E2-feminized female eels. Transcript levels of amh and gsdf (not amhr2) decreased during human chorionic gonadotropin (HCG)-induced spermatogenesis in males. This study suggests that amh, amhr2, and especially gsdf might be involved in the gene pathway regulating testicular differentiation of Japanese eels. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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Review

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14 pages, 1774 KiB

Open AccessReview

Endocrine Regulation of Maturation and Sex Change in Groupers

by Kiyoshi Soyano, Takafumi Amagai, Tomofumi Yamaguchi, Yuji Mushirobira, Wen-Gang Xu, Nhan Thành Phạm and Ryosuke Murata

Cells 2022, 11(5), 825; https://doi.org/10.3390/cells11050825 - 27 Feb 2022

Cited by 16 | Viewed by 4713

Abstract

Groupers are widely distributed in tropical and subtropical areas worldwide, are key species to coastal ecosystems, and valuable fishery targets. To facilitate artificial seed production technology for grouper aquaculture, the mechanisms of reproduction and gonad development are being elucidated for these important species. [...] Read more.

Groupers are widely distributed in tropical and subtropical areas worldwide, are key species to coastal ecosystems, and valuable fishery targets. To facilitate artificial seed production technology for grouper aquaculture, the mechanisms of reproduction and gonad development are being elucidated for these important species. In addition, since groupers are sexually dimorphic fish with female-first maturity (protogynous hermaphrodite fish), research is being conducted to clarify the ecological mechanism of sex change and their reproductive physiology, focusing on the endocrine system. In recent years, research on groupers has also been conducted to understand changes in the coastal environment caused by ocean warming and man-made chemicals. However, due to difficulties associated with conducting research using wild populations for breeding experiments, knowledge of the physiology and ecology of these fish is lacking, especially their reproductive physiology. In this review, we present information on the reproductive physiology and endocrinology of groupers obtained to date, together with the characteristics of their life history. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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25 pages, 1072 KiB

Open AccessReview

Advances in Reproductive Endocrinology and Neuroendocrine Research Using Catfish Models

by Balasubramanian Senthilkumaran and Sonika Kar

Cells 2021, 10(11), 2807; https://doi.org/10.3390/cells10112807 - 20 Oct 2021

Cited by 16 | Viewed by 4161

Abstract

Catfishes, belonging to the order siluriformes, represent one of the largest groups of freshwater fishes with more than 4000 species and almost 12% of teleostean population. Due to their worldwide distribution and diversity, catfishes are interesting models for ecologists and evolutionary biologists. Incidentally, [...] Read more.

Catfishes, belonging to the order siluriformes, represent one of the largest groups of freshwater fishes with more than 4000 species and almost 12% of teleostean population. Due to their worldwide distribution and diversity, catfishes are interesting models for ecologists and evolutionary biologists. Incidentally, catfish emerged as an excellent animal model for aquaculture research because of economic importance, availability, disease resistance, adaptability to artificial spawning, handling, culture, high fecundity, hatchability, hypoxia tolerance and their ability to acclimate to laboratory conditions. Reproductive system in catfish is orchestrated by complex network of nervous, endocrine system and environmental factors during gonadal growth as well as recrudescence. Lot of new information on the molecular mechanism of gonadal development have been obtained over several decades which are evident from significant number of scientific publications pertaining to reproductive biology and neuroendocrine research in catfish. This review aims to synthesize key findings and compile highly relevant aspects on how catfish can offer insight into fundamental mechanisms of all the areas of reproduction and its neuroendocrine regulation, from gametogenesis to spawning including seasonal reproductive cycle. In addition, the state-of-knowledge surrounding gonadal development and neuroendocrine control of gonadal sex differentiation in catfish are comprehensively summarized in comparison with other fish models. Full article

(This article belongs to the Special Issue Fish: A Model for Endocrine Research)

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