Gonadal response of juvenile protogynous grouper (<i>Epinephelus fuscoguttatus</i>) to long-term recombinant follicle-stimulating hormone administration†

Palma, Peter; Nocillado, Josephine; Superio, Joshua; Ayson, Evelyn Grace de Jesus; Ayson, Felix G.; Bar, Ido; Elizur, Abigail

doi:10.1093/biolre/ioy228

Cited by 19 publications

(21 citation statements)

References 64 publications

(99 reference statements)

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“…It has also been reported in E. coioides that endogenous 11KT triggers their natural sex change from female to male 26 . Additionally, a novel experimental study on E. fuscoguttatus suggested that pituitary FSH is involved in the initiation of sex change as an upstream factor, which is consistent with our previous findings regarding the honeycomb grouper 17 , 27 . Considering these findings, we suggest that sex change in groupers is regulated by a common endocrine mechanism: 11KT, which is secreted from TIS cells in response to pituitary FSH, triggers the onset of sex change, as previously reported in the honeycomb grouper (Fig.…”

Section: Discussionsupporting

confidence: 91%

Testicular inducing steroidogenic cells trigger sex change in groupers

Murata

Nozu

Mushirobira

et al. 2021

Sci Rep

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Vertebrates usually exhibit gonochorism, whereby their sex is fixed throughout their lifetime. However, approximately 500 species (~ 2%) of extant teleost fishes change sex during their lifetime. Although phylogenetic and evolutionary ecological studies have recently revealed that the extant sequential hermaphroditism in teleost fish is derived from gonochorism, the evolution of this transsexual ability remains unclear. We revealed in a previous study that the tunica of the ovaries of several protogynous hermaphrodite groupers contain functional androgen-producing cells, which were previously unknown structures in the ovaries of gonochoristic fishes. Additionally, we demonstrated that these androgen-producing cells play critical roles in initiating female-to-male sex change in several grouper species. In the present study, we widened the investigation to include 7 genera and 18 species of groupers and revealed that representatives from most major clades of extant groupers commonly contain these androgen-producing cells, termed testicular-inducing steroidogenic (TIS) cells. Our findings suggest that groupers acquired TIS cells in the tunica of the gonads for successful sex change during their evolution. Thus, TIS cells trigger the evolution of sex change in groupers.

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Section: Discussionsupporting

confidence: 91%

Testicular inducing steroidogenic cells trigger sex change in groupers

Murata

Nozu

Mushirobira

et al. 2021

Sci Rep

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“…In orange-spotted grouper Epinephelus coioides, recombinant FSH injection resulted in the occurrence of primary oocytes in sexually immature individuals (Chen et al 2012). Similarly, our previous experiments showed that recombinant FSH injection advanced oocyte development into cortical alveolar stage in juvenile tiger grouper although prolonged treatment resulted in the initiation of female to male sex change (Palma et al 2019a). Female vitellogenic honeycomb grouper Epinephelus merra also sex reversed after receiving injection of bovine FSH (Kobayashi et al 2010).…”

Section: Introductionmentioning

confidence: 59%

Induction of Gonadal Development in Protogynous Grouper with Orally Delivered FSH DNA

et al. 2019

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The availability of sexually mature fish often dictates the success of its captive breeding. In this study, we induced reproductive development in juvenile protogynous tiger grouper through oral administration of a plasmid (p) containing an engineered folliclestimulating hormone (FSH). An expression construct (pcDNA3.1) was designed to express a single-chain FSH consisting of giant grouper FSH β-subunit and glycoprotein subunit-α (CGα), linked by the carboxy-terminal peptide (CTP) sequence from the human chorionic gonadotropin (hCG). Single oral delivery of pFSH encapsulated in liposome and chitosan to tiger grouper yielded a significant increase in plasma FSH protein level after 4 days. Weekly pFSH feeding of juvenile tiger groupers for 8 weeks stimulated ovarian development as indicated by a significant increase in oocyte diameter and progression of oocytes to cortical alveolar stage. As the pFSH treatment progressed from 20 to 38 weeks, female to male sex change was initiated, characterized by oocyte regression, proliferation of spermatogonial cells, and occurrence of spermatogenic cysts. It was also associated with significantly lower mRNA expression of steroidogenic genes (cyp11b, cyp19a1a, and foxl2) and basal plasma levels of sex steroid hormones 17β-estradiol (E 2 ), testosterone (T), and 11-ketotestosterone (11KT). Results suggest that pFSH stimulates ovarian development up to cortical alveolar stage and then initiates sex change in tiger grouper. These findings significantly contribute to our knowledge on the role of FSH in the development of protogynous hermaphroditic fish. This study is the first to demonstrate induction of reproductive development in fish through oral delivery of plasmid gonadotropin.

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“…For instance, after 60 days of treatment with injections at 10-day intervals of rFsh produced in P. pastoris (10 -20 µg kg-1) immature yellowtail kingfish oocytes developed to cortical alveoli stage (Sanchís-Benlloch et al, 2017). Weekly injections for 8 weeks at 100 µg kg-1 to juvenile grouper (Epinephelus fuscoguttatus) also induced development to the cortical alveoli stage (Palma et al, 2018). Recombinant Fsh produced in Drosophila S2 cell line (100 µg kg-1) induced early vitellogenesis in the Japanese eel after 56 days of treatment with a weekly administration (Kazeto et al, 2008) and rFsh (500 µg/kg) produced in HEK293 cells induced initial oil droplet stage in previtellogenic yellow shortfinned eels (Anguilla australis) after three weeks (Tuan Nguyen et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…An alternative strategy to control gametogenesis in mullet as in other teleost, which would not require the availability of endogenous Gths from the pituitary, is the long-term use of recombinant Fsh and Lh (rFsh and rLh, respectively). This approach is nowadays possible through the production of large amounts of species-specific rGths in heterologous expression systems, such as the Drosophila S2 cell line (Kazeto et al, 2008;Zmora et al, 2007), the yeast Pichia pastoris (Aizen et al, 2007;Chen et al, 2012;Kamei et al, 2003;Kasuto and Levavi-Sivan, 2005;Palma et al, 2018;Sanchís-Benlloch et al, 2017), baculovirus silkworm larvae (Cui et al, 2007;Glubokov et al, 1994;Ko et al, 2007;Kobayashi et al, 2010Kobayashi et al, , 2003Meri et al, 2000), HEK293 cells (Kazeto et al, 2019) and…”

Section: Introductionmentioning

confidence: 99%

Providing recombinant gonadotropin-based therapies that induce complete oogenesis and produce viable larvae from an immature teleost, flathead grey mullet (Mugil cephalus)

Ramos-Júdez

Chauvigné

González-López

et al. 2020

Preprint

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Under intensive captive conditions, wild-caught flathead grey mullet (Mugil cephalus) 12 females remain arrested at early gonad development and males do not produce sperm. With the aim to induce gametogenesis and obtain fertilized eggs, adult female and male 14 grey mullet were treated with M. cephalus single-chain recombinant gonadotropins (rGths), follicle-stimulating (rFsh) and luteinizing (rLh) hormones. In Experiment 1, a 16 weekly dose of rFsh (15 µg kg -1 ) significantly (P < 0.001) increased plasma concentration of 17β-estradiol in females and induced oocyte growth up to a maximum diameter of 425 18 ± 19 µm after 9 weeks of treatment. In males, spermiogenesis (> 75% motile spermatozoa) was induced after 5 weeks to produce low quantities (29.3 ± 6.1 µL) of 20 viscous sperm. However, the application of therapies based on human chorionic gonadotropin (hCG) or gonadotropin releasing hormone agonist (GnRHa) were 22 ineffective to complete oocyte maturation. In Experiment 2, fish were treated with weekly injections of both rFsh and rLh at different doses (from 2.5 to 12 µg kg -1 ). Oocyte 24 diameter reached 609 ± 5 µm prior to oocyte maturation and ovulation, which was induced with 30 µg kg -1 of rLh and 40 mg kg -1 of progesterone. Higher quantities of good 26 quality sperm (92.7 ± 24.7 µL) were obtained after rLh treatment of males and used to fertilise the eggs. Although the percentage of fertilisation was low (0.4 %), these eggs 28 were able to produce viable larvae (71% hatching rate). In comparison, control groups remained arrested as immature fish. The study demonstrated that both rGths are effective 30 to induce the entire process of gametogenesis in sexually immature male and female grey mullet, which confirmed the central roles of the Gths in teleost gametogenesis. This 32 advance provides the bases of a therapy for the use in the aquaculture of teleosts of commercial interest or the conservation of endangered species. 34 42 positive attributes of grey mullet culture have made this species a suitable option for aquaculture. Grey mullet has fast growth (0.75 -1 kg per year) [2], does not require 44 dietary fish meal and oil and can be reared in a wide range of salinities and culture systems including polyculture [3]. In addition, the final product marketed in various forms has 46 good texture, taste [4] and is an excellent source of omega-3 essential fatty acids [5].Although this species has a long history of culture, it exhibits different degrees of 48 reproductive dysfunctions in both genders under captive conditions. These dysfunctions have limited the possibility to close the life cycle and, thus, culture has been based on the 50 capture of wild juveniles [4] or induced spawning of wild breeders [6 -10]. Two types of reproductive dysfunction have been described and can be placed in two categories; arrest 52 in the late stages or early stages of gametogenesis. Arrest in late stages of gametogenesis (maturation and ovulation) has been observed in recently caught wild mullet or wild 54 mullet...

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Gonadal response of juvenile protogynous grouper (Epinephelus fuscoguttatus) to long-term recombinant follicle-stimulating hormone administration†

Cited by 19 publications

References 64 publications

Testicular inducing steroidogenic cells trigger sex change in groupers

Testicular inducing steroidogenic cells trigger sex change in groupers

Induction of Gonadal Development in Protogynous Grouper with Orally Delivered FSH DNA

Providing recombinant gonadotropin-based therapies that induce complete oogenesis and produce viable larvae from an immature teleost, flathead grey mullet (Mugil cephalus)

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