Cytological analysis of nuclear migration and dissolution during steroid‐induced meiotic maturation in vitro of follicle‐enclosed oocytes of the goldfish (<i>Carassius auratus</i>)

Lessman, Charles A.; Kavumpurath, Soosamma

doi:10.1002/mrd.1120100104

Cited by 31 publications

(18 citation statements)

References 12 publications

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“…Groups of 20 oocytes were washed in extraction buffer (0.1 M sodium ␤-glycerophos- Abbreviations: 17,17␣,…”

Section: Methodsmentioning

confidence: 99%

“…Immature oocytes were exposed in vitro by incubating ovarian fragments (each containing 2-10 oocytes) in 4 ml of zebrafish Ringer's solution containing each agent (from a 1,000-fold stock in ethanol) at room temperature with gentle agitation (40 rpm). To assess maturation processes, germinal vesicles in full-grown oocytes were examined under a binocular microscope (SMZ645, Nikon) after placing the oocytes in clearing solution (17). The nuclear state (%) at each time point was determined in Ͼ20 oocytes.…”

Section: Methodsmentioning

confidence: 99%

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Diethylstilbestrol induces fish oocyte maturation

Tokumoto

Horiguchi

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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O ocyte maturation in lower vertebrates is triggered by maturation-inducing hormone (MIH), which acts on receptors located on the oocyte membrane and induces the activation of maturation-promoting factor in the oocyte cytoplasm (1-4). During the course of maturation, oocytes undergo drastic morphological changes associated with progression of the meiotic cell cycle, in which breakdown of the oocyte nuclear envelope [germinal vesicle breakdown (GVBD)] occurring at the prophase͞metaphase transition is usually regarded as a hallmark of the progress of oocyte maturation. Two MIHs, 17␣,20␤-dihydroxy-4-pregnen-3-one (17,20␤-DHP) and 17␣,20␤,21-trihydroxy-4-pregnen-3-one (20␤-S), have been identified in several fish species (5, 6). In goldfish, 17,20␤-DHP has been shown to induce oocyte maturation by stimulating the de novo synthesis of cyclin B, a regulatory subunit of maturationpromoting factor (7). Although progestins including 17,20␤-DHP and 20␤-S are the most potent steroid inducers of oocyte maturation in fish, other hormones such as deoxycorticosterone and testosterone, but not estradiol or its analogs, are also effective (8).Several endocrine-disrupting chemicals, Kepon and dichlorodiphenyldichloroethane, have been reported to antagonize MIH-induced meiotic maturation of fish oocytes in vitro (9). One of the environmental endocrine-disrupting chemicals (EEDCs), diethylstilbestrol (DES) is a nonsteroidal substance that was prescribed from the late 1940s to the early 1970s to pregnant women to prevent abortion, preeclampsia, and other complications of pregnancy. Male and female offspring exposed in utero to DES may develop multiple and neoplastic lesions of the reproductive tract, along with other changes, during development (10). Here we show that exposing fish oocytes to DES at a dose within a range similar to that used in experimental exposure to 17,20␤-DHP induces oocyte maturation. Estradiol-17␤ has been reported to be ineffective in inducing fish oocyte maturation (11, 12) and even inhibitory in several teleost species (13-15). Thus, the stimulatory effect of DES to induce fish oocyte maturation observed in this study has not been published previously. This report shows that EEDC can potentially induce oocyte maturation like an endogenous MIH, 17,20␤-DHP. Materials and MethodsMaterials. Goldfish were purchased from a local supplier and maintained at 15°C until used. Zebrafish were maintained at 28.5°C on a 14-h light͞10-h dark cycle (16). 17,20␤-DHP, DES, DES dimethyl ether (DM-DES), DES dipropionate (DP-DES), and 17␤-estradiol were purchased from Sigma. Dimethylstilbestrol (DMS) was a generous gift from J. Katzenellenbogen (University of Illinois, Urbana). 17␣-Estradiol, ethynylestradiol, butyl benzyl phthalate, di(2-ethylhexyl)-phthalate, and pentachlorophenol were obtained from Wako Pure Chemical (Osaka). Other chemicals were purchased as follows: hexestrol (HEX; ICN); trans,trans-dienestrol(␣-dienestrol) (DIES; U.S. Pharmacopeia, Rockville, MD); resveratorol (Calbiochem); DDTs (AccuStandard, New Haven, ...

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“…Groups of 20 oocytes were washed in extraction buffer (0.1 M sodium ␤-glycerophos- Abbreviations: 17,17␣,…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Diethylstilbestrol induces fish oocyte maturation

Tokumoto

Horiguchi

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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“…The resultant complex (10 ml) was layered on oocytes in culture. Medium was replaced with fresh Ringer after 1 h. Oocyte viability was checked using Trypan blue and GVBD was monitored at 3 h following immersion in clearing solution (Lessman & Kavumpurath 1984) under an inverted microscope (Victory FL, Dewinter Optical, Inc., Italy) fitted with phasecontrast optics.…”

Section: Oocyte Preparation and In Vitro Culturementioning

confidence: 99%

Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1

Das¹,

Pal²,

Maitra³

2016

Reproduction

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Binding of 17b-estradiol (E 2 ) to novel G-protein coupled receptor, Gper1, promotes intra-oocyte adenylyl cyclase activity and transactivates epidermal growth factor receptor to ensure prophase-I arrest. Although involvement of either membrane progestin receptor (mPR) or Igf system has been implicated in regulation of meiosis resumption, possibility of concurrent activation and potential synergism between 17a,20b-dihydroxy-4-pregnen-3-one (DHP)-and Igf-mediated signalling cascades in alleviating E 2 inhibition of oocyte maturation (OM) has not been investigated. Here using zebrafish (Danio rerio) defolliculated oocytes, we examined the effect of DHP and Igf1, either alone or in combination, in presence or absence of E 2 , on OM in vitro. While priming of denuded oocytes with E 2 blocked spontaneous maturation, co-treatment with DHP (3 nM) and Igf1 (10 nM), but not alone, reversed E 2 inhibition and promoted a robust increase in germinal vesicle breakdown (GVBD). Although stimulation with either Igf1 or DHP promoted Akt phosphorylation, pharmacological inhibition of PI3K/Akt signalling prevented Igf1-induced GVBD but delayed DHP action till 4-5 h of incubation. Moreover, high intra-oocyte cAMP attenuates both DHP and Igf1-mediated OM and co-stimulation with DHP and Igf1 could effectively reverse E 2 action on PKA phosphorylation. Interestingly, data from in vivo studies reveal that heightened expression of igf1, igf3 transcripts in intact follicles corresponded well with elevated phosphorylation of Igf1r and Akt, mPRa immunoreactivity, PKA inhibition and accelerated GVBD response just prior to ovulation. This indicates potential synergism between maturational steroid and Igf1 which might have physiological relevance in overcoming E 2 inhibition of meiosis resumption in zebrafish oocytes.

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“…They include variations in ooplasmic fluidity (Elinson 1980(Elinson , 1983, chromosome configuration and condensation (Masui and Clarke 1979), migration of GV towards the animal pole (Brachet et al 1970;Imoh and Miyazaki 1984) or the micropyle (Lessman and Kavumpurath 1984), dissolution of the nuclear membrane, formation of the spindle and generation of the first polar body (Schuetz 1974;Masui and Clarke 1979). Variations in cytoplasmic firmness are associated with changes in cytoskeleton and microtubule polymerization in amphibians and echinoderms (Vacquier 1981;Elinson 1983;Schroeder and Otto 1984).…”

Section: Introductionmentioning

confidence: 98%

“…In amphibians it is difficult to dissociate between GVM and GVD since dissolution of nuclear membrane commences before complete migration of GV to animal pole (Imoh and Miyazaki 1984). In goldfish however, complete GVM to the micropyle apparently takes place before GVD, and the GVM process can be readily quantified in all oocytes (Lessman and Kavumpurath 1984). In addition, it is possible to induce GVM in the oocyte of goldfish without effecting GVD by administration of demecolcine (DE; a colchicine derivative also known as colcemid).…”

Section: Introductionmentioning

confidence: 98%

A study of goldfish oocyte meiosisin vitro: effects of 2,4-dinitrophenol and adenosine-5-triphosphate

Habibi

Lessman

1986

Fish Physiol Biochem

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Germinal vesicle migration (GVM) and/or dissolution (GVD) were measured in goldfish oocytes, treated with 17α, 20β dihydroxyprogesterone (DHP) and other compounds considered to effect the cytoskeleton and oxidative phosphorylation,in vitro. Administration of DHP reinitiated meiotic maturation, increasing GVM and GVD in goldfish oocytes. Addition of 2,4-dinitrophenol (DNP) to the incubation medium significantly inhibited DHP-induced GVM and GVD. The DNP effect was found to be partially reversible after 24 h and could be reversed fully after a further delay of approximately 24h. Treatment of goldfish oocytes with demecolcine (DE; a colchicine derivative also known as colcemid) induces GVM to the micropyle without effecting GVD; while Cytochalasin-B which inhibits microfilament polymerization impairs both GVM and GVD. Administration of DNP, significantly inhibited DE-induced GVM, suggesting that GVM as well as GVD are dependent upon the process of oxidative phosphorylation. Addition of adenosine-5' -triphosphate (ATP) at low concentrations (0.01-0.1 mM) did not effect DHP-induced or DNP-inhibited GVD in goldfish oocytes. The present results are consistent with the idea that migration of the oocyte nucleus during meiosis reinitiation has an energy requirement and involves participation by the cytoskeleton.

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Cytological analysis of nuclear migration and dissolution during steroid‐induced meiotic maturation in vitro of follicle‐enclosed oocytes of the goldfish (Carassius auratus)

Cited by 31 publications

References 12 publications

Diethylstilbestrol induces fish oocyte maturation

Diethylstilbestrol induces fish oocyte maturation

Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1

A study of goldfish oocyte meiosisin vitro: effects of 2,4-dinitrophenol and adenosine-5-triphosphate

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