Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: Temporal relationship and locus of action

Previous studies demonstrated that estrogen inhibited frog pituitary homogenate (FPH) and progesterone-induced oocyte maturation. In order to determine whether estrogen interfered with intrafollicular progesterone synthesis, experiments were designed to study the effect of exogenous estrogen (estrad...

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Veröffentlicht in:General and comparative endocrinology 1985-01, Vol.58 (3), p.421-435
Hauptverfasser: Peter Lin, Yu-Wai, Schuetz, Allen W.
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description Previous studies demonstrated that estrogen inhibited frog pituitary homogenate (FPH) and progesterone-induced oocyte maturation. In order to determine whether estrogen interfered with intrafollicular progesterone synthesis, experiments were designed to study the effect of exogenous estrogen (estradiol-17β) on FPH-induced progesterone production in amphibian ( Rana pipiens) ovarian follicles cultured in vitro. Intrafollicular progesterone concentrations were monitored directly using radioimmunoassay and the occurrence of germinal vesicle breakdown (GVBD) was used as a biological indicator of the action of steroids on oocyte maturation. FPH elicited a rapid and dramatic increase in follicular progesterone concentration (1000–3000 pg per follicle) which preceded germinal vesicle breakdown. Addition of estrogen to the culture medium inhibited FPH-induced progesterone production and the accompanying GVBD in a dose-dependent fashion. The presence of estrogen did not enhance the degradation of preloaded progesterone, suggesting estrogen impeded progesterone synthesis rather than enhanced progesterone metabolism. The temporal relationship between estrogen and FPH interaction was assessed by varying the relative time of hormone addition, after which intrafollicular progesterone concentration and GVBD were monitored. Progesterone production and GVBD were drastically inhibited when estrogen was added before or simultaneously with FPH. However, when addition of estrogen was delayed until after FPH simulation, a progressive loss of the inhibitory effect of the steroid on progesterone accumulation and GVBD was observed. Thus, the estrogensensitive phase was confined to the early portion of FPH stimulation. Continuous presence of estrogen in the culture system was not required to inhibit FPH-induced events. A short exposure (15 min) of follicles to estrogen was sufficient to inhibit oocyte maturation, whereas progesterone synthesis was not significantly affected. With longer exposure, however, FPH-induced progesterone production was impeded. Washing estrogen-treated follicles did not reverse the inhibitory effect of estrogen, however the follicles remained responsive to exogenous progesterone stimulation and exhibited GVBD. Results suggest that the inhibitory effects of estrogen on FPH action and progesterone production were not reversible under the in vitro culture conditions. To determine whether specific follicular components were involved in estrogen inhibition, pro
doi_str_mv 10.1016/0016-6480(85)90115-7
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In order to determine whether estrogen interfered with intrafollicular progesterone synthesis, experiments were designed to study the effect of exogenous estrogen (estradiol-17β) on FPH-induced progesterone production in amphibian ( Rana pipiens) ovarian follicles cultured in vitro. Intrafollicular progesterone concentrations were monitored directly using radioimmunoassay and the occurrence of germinal vesicle breakdown (GVBD) was used as a biological indicator of the action of steroids on oocyte maturation. FPH elicited a rapid and dramatic increase in follicular progesterone concentration (1000–3000 pg per follicle) which preceded germinal vesicle breakdown. Addition of estrogen to the culture medium inhibited FPH-induced progesterone production and the accompanying GVBD in a dose-dependent fashion. The presence of estrogen did not enhance the degradation of preloaded progesterone, suggesting estrogen impeded progesterone synthesis rather than enhanced progesterone metabolism. The temporal relationship between estrogen and FPH interaction was assessed by varying the relative time of hormone addition, after which intrafollicular progesterone concentration and GVBD were monitored. Progesterone production and GVBD were drastically inhibited when estrogen was added before or simultaneously with FPH. However, when addition of estrogen was delayed until after FPH simulation, a progressive loss of the inhibitory effect of the steroid on progesterone accumulation and GVBD was observed. Thus, the estrogensensitive phase was confined to the early portion of FPH stimulation. Continuous presence of estrogen in the culture system was not required to inhibit FPH-induced events. A short exposure (15 min) of follicles to estrogen was sufficient to inhibit oocyte maturation, whereas progesterone synthesis was not significantly affected. With longer exposure, however, FPH-induced progesterone production was impeded. Washing estrogen-treated follicles did not reverse the inhibitory effect of estrogen, however the follicles remained responsive to exogenous progesterone stimulation and exhibited GVBD. Results suggest that the inhibitory effects of estrogen on FPH action and progesterone production were not reversible under the in vitro culture conditions. To determine whether specific follicular components were involved in estrogen inhibition, progesterone production was assessed following selective removal of different follicle components by microdissection prior to being treated with FPH and estrogen. Removal of the follicular epithelium, theca layer, or the cytoplasm (yolk) of the oocyte did not interfere with estrogen inhibition of progesterone production. The data suggest that the locus of action of estrogen, within the ovarian follicle, is directed against the follicle cells and hence these cells may play a pivotal role in regulating the progesterone synthesis and oocyte meiotic maturation. 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Psychology ; Kinetics ; Non mammalian vertebrate reproduction ; Oocytes - drug effects ; Oocytes - growth &amp; development ; Ovarian Follicle - drug effects ; Ovarian Follicle - metabolism ; Ovary - physiology ; Pituitary Gland - physiology ; Progesterone - biosynthesis ; Progesterone - metabolism ; Rana pipiens ; Time Factors ; Tissue Extracts - pharmacology ; Vertebrates: reproduction</subject><ispartof>General and comparative endocrinology, 1985-01, Vol.58 (3), p.421-435</ispartof><rights>1985</rights><rights>1986 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c512t-93434e49033998f5c89bda66ec5fe28cef77fccd8455406ac7eac897e965f6f63</citedby><cites>FETCH-LOGICAL-c512t-93434e49033998f5c89bda66ec5fe28cef77fccd8455406ac7eac897e965f6f63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/0016648085901157$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=8410084$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/3874115$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Peter Lin, Yu-Wai</creatorcontrib><creatorcontrib>Schuetz, Allen W.</creatorcontrib><title>Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: Temporal relationship and locus of action</title><title>General and comparative endocrinology</title><addtitle>Gen Comp Endocrinol</addtitle><description>Previous studies demonstrated that estrogen inhibited frog pituitary homogenate (FPH) and progesterone-induced oocyte maturation. In order to determine whether estrogen interfered with intrafollicular progesterone synthesis, experiments were designed to study the effect of exogenous estrogen (estradiol-17β) on FPH-induced progesterone production in amphibian ( Rana pipiens) ovarian follicles cultured in vitro. Intrafollicular progesterone concentrations were monitored directly using radioimmunoassay and the occurrence of germinal vesicle breakdown (GVBD) was used as a biological indicator of the action of steroids on oocyte maturation. FPH elicited a rapid and dramatic increase in follicular progesterone concentration (1000–3000 pg per follicle) which preceded germinal vesicle breakdown. Addition of estrogen to the culture medium inhibited FPH-induced progesterone production and the accompanying GVBD in a dose-dependent fashion. The presence of estrogen did not enhance the degradation of preloaded progesterone, suggesting estrogen impeded progesterone synthesis rather than enhanced progesterone metabolism. The temporal relationship between estrogen and FPH interaction was assessed by varying the relative time of hormone addition, after which intrafollicular progesterone concentration and GVBD were monitored. Progesterone production and GVBD were drastically inhibited when estrogen was added before or simultaneously with FPH. However, when addition of estrogen was delayed until after FPH simulation, a progressive loss of the inhibitory effect of the steroid on progesterone accumulation and GVBD was observed. Thus, the estrogensensitive phase was confined to the early portion of FPH stimulation. Continuous presence of estrogen in the culture system was not required to inhibit FPH-induced events. A short exposure (15 min) of follicles to estrogen was sufficient to inhibit oocyte maturation, whereas progesterone synthesis was not significantly affected. With longer exposure, however, FPH-induced progesterone production was impeded. Washing estrogen-treated follicles did not reverse the inhibitory effect of estrogen, however the follicles remained responsive to exogenous progesterone stimulation and exhibited GVBD. Results suggest that the inhibitory effects of estrogen on FPH action and progesterone production were not reversible under the in vitro culture conditions. To determine whether specific follicular components were involved in estrogen inhibition, progesterone production was assessed following selective removal of different follicle components by microdissection prior to being treated with FPH and estrogen. Removal of the follicular epithelium, theca layer, or the cytoplasm (yolk) of the oocyte did not interfere with estrogen inhibition of progesterone production. The data suggest that the locus of action of estrogen, within the ovarian follicle, is directed against the follicle cells and hence these cells may play a pivotal role in regulating the progesterone synthesis and oocyte meiotic maturation. Intrafollicular estrogen levels may thus serve as a physiological regulator of follicular responsiveness to gonadotrophic hormones.</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Estradiol - administration &amp; dosage</subject><subject>Estradiol - pharmacology</subject><subject>Female</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Kinetics</subject><subject>Non mammalian vertebrate reproduction</subject><subject>Oocytes - drug effects</subject><subject>Oocytes - growth &amp; development</subject><subject>Ovarian Follicle - drug effects</subject><subject>Ovarian Follicle - metabolism</subject><subject>Ovary - physiology</subject><subject>Pituitary Gland - physiology</subject><subject>Progesterone - biosynthesis</subject><subject>Progesterone - metabolism</subject><subject>Rana pipiens</subject><subject>Time Factors</subject><subject>Tissue Extracts - pharmacology</subject><subject>Vertebrates: reproduction</subject><issn>0016-6480</issn><issn>1095-6840</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1985</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc-KFDEQxoMo6-zqGyjkILIeWpPpJJ3egyCLfxYWBFnPoTZdmY30JG2SXpjX8glNzwxz1EtyqN9X9VV9hLzi7D1nXH1g9WmU0OxSy3c941w23ROy4qyXjdKCPSWrE_KcnOf8izEmW8XPyFmrO1EFK_LnJpQELo6jt_MIiYItPgYaHcVcUtxgoD7QhJtaLT5s6OTL7AukXePDMFscaHyE5CHQacFzwRQD0rwL5QGzzxRCRaLdFaRbKHOC_YDa9AcEqO0mjyFf0TvcTjHBWGeNeyQ_-GkvHqOd8-Lo4O0FeeZgzPjy-F-Qn18-311_a26_f725_nTbWMnXpelb0QoUPWvbvtdOWt3fD6AUWulwrS26rnPWDlpIKZgC2yFUpsNeSaecai_I20PfutfvuS5mtj5bHEcIGOdsOsWVEl3_X5CLdXXEdAXFAbQp5pzQmSn5bT2l4cwsmZolMLMEZrQ0-0xNV2Wvj_3n-y0OJ9ExxFp_c6xDtjC6BMH6fMK04IxpUbGPBwzr0R49JpNtPX1N0Ce0xQzR_9vHX4L4wq4</recordid><startdate>19850101</startdate><enddate>19850101</enddate><creator>Peter Lin, Yu-Wai</creator><creator>Schuetz, Allen W.</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SQ</scope><scope>7X8</scope></search><sort><creationdate>19850101</creationdate><title>Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: Temporal relationship and locus of action</title><author>Peter Lin, Yu-Wai ; Schuetz, Allen W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c512t-93434e49033998f5c89bda66ec5fe28cef77fccd8455406ac7eac897e965f6f63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1985</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Estradiol - administration &amp; dosage</topic><topic>Estradiol - pharmacology</topic><topic>Female</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Kinetics</topic><topic>Non mammalian vertebrate reproduction</topic><topic>Oocytes - drug effects</topic><topic>Oocytes - growth &amp; development</topic><topic>Ovarian Follicle - drug effects</topic><topic>Ovarian Follicle - metabolism</topic><topic>Ovary - physiology</topic><topic>Pituitary Gland - physiology</topic><topic>Progesterone - biosynthesis</topic><topic>Progesterone - metabolism</topic><topic>Rana pipiens</topic><topic>Time Factors</topic><topic>Tissue Extracts - pharmacology</topic><topic>Vertebrates: reproduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Peter Lin, Yu-Wai</creatorcontrib><creatorcontrib>Schuetz, Allen W.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Endocrinology Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>General and comparative endocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Peter Lin, Yu-Wai</au><au>Schuetz, Allen W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: Temporal relationship and locus of action</atitle><jtitle>General and comparative endocrinology</jtitle><addtitle>Gen Comp Endocrinol</addtitle><date>1985-01-01</date><risdate>1985</risdate><volume>58</volume><issue>3</issue><spage>421</spage><epage>435</epage><pages>421-435</pages><issn>0016-6480</issn><eissn>1095-6840</eissn><coden>GCENA5</coden><abstract>Previous studies demonstrated that estrogen inhibited frog pituitary homogenate (FPH) and progesterone-induced oocyte maturation. In order to determine whether estrogen interfered with intrafollicular progesterone synthesis, experiments were designed to study the effect of exogenous estrogen (estradiol-17β) on FPH-induced progesterone production in amphibian ( Rana pipiens) ovarian follicles cultured in vitro. Intrafollicular progesterone concentrations were monitored directly using radioimmunoassay and the occurrence of germinal vesicle breakdown (GVBD) was used as a biological indicator of the action of steroids on oocyte maturation. FPH elicited a rapid and dramatic increase in follicular progesterone concentration (1000–3000 pg per follicle) which preceded germinal vesicle breakdown. Addition of estrogen to the culture medium inhibited FPH-induced progesterone production and the accompanying GVBD in a dose-dependent fashion. The presence of estrogen did not enhance the degradation of preloaded progesterone, suggesting estrogen impeded progesterone synthesis rather than enhanced progesterone metabolism. The temporal relationship between estrogen and FPH interaction was assessed by varying the relative time of hormone addition, after which intrafollicular progesterone concentration and GVBD were monitored. Progesterone production and GVBD were drastically inhibited when estrogen was added before or simultaneously with FPH. However, when addition of estrogen was delayed until after FPH simulation, a progressive loss of the inhibitory effect of the steroid on progesterone accumulation and GVBD was observed. Thus, the estrogensensitive phase was confined to the early portion of FPH stimulation. Continuous presence of estrogen in the culture system was not required to inhibit FPH-induced events. A short exposure (15 min) of follicles to estrogen was sufficient to inhibit oocyte maturation, whereas progesterone synthesis was not significantly affected. With longer exposure, however, FPH-induced progesterone production was impeded. Washing estrogen-treated follicles did not reverse the inhibitory effect of estrogen, however the follicles remained responsive to exogenous progesterone stimulation and exhibited GVBD. Results suggest that the inhibitory effects of estrogen on FPH action and progesterone production were not reversible under the in vitro culture conditions. To determine whether specific follicular components were involved in estrogen inhibition, progesterone production was assessed following selective removal of different follicle components by microdissection prior to being treated with FPH and estrogen. Removal of the follicular epithelium, theca layer, or the cytoplasm (yolk) of the oocyte did not interfere with estrogen inhibition of progesterone production. The data suggest that the locus of action of estrogen, within the ovarian follicle, is directed against the follicle cells and hence these cells may play a pivotal role in regulating the progesterone synthesis and oocyte meiotic maturation. Intrafollicular estrogen levels may thus serve as a physiological regulator of follicular responsiveness to gonadotrophic hormones.</abstract><cop>San Diego, CA</cop><pub>Elsevier Inc</pub><pmid>3874115</pmid><doi>10.1016/0016-6480(85)90115-7</doi><tpages>15</tpages></addata></record>
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subjects Animals
Biological and medical sciences
Estradiol - administration & dosage
Estradiol - pharmacology
Female
Fundamental and applied biological sciences. Psychology
Kinetics
Non mammalian vertebrate reproduction
Oocytes - drug effects
Oocytes - growth & development
Ovarian Follicle - drug effects
Ovarian Follicle - metabolism
Ovary - physiology
Pituitary Gland - physiology
Progesterone - biosynthesis
Progesterone - metabolism
Rana pipiens
Time Factors
Tissue Extracts - pharmacology
Vertebrates: reproduction
title Intrafollicular action of estrogen in regulating pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: Temporal relationship and locus of action
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