Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes
The developmental competence of IVM porcine oocytes is still low compared with that in their in vivo counterparts. Although many studies reported effects of glucose metabolism (GM) on oocyte nuclear maturation, few reported on cytoplasmic maturation. Previous studies could not differentiate whether...
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description | The developmental competence of IVM porcine oocytes is still low compared with that in their
in vivo
counterparts. Although many studies reported effects of glucose metabolism (GM) on oocyte nuclear maturation, few reported on cytoplasmic maturation. Previous studies could not differentiate whether GM of cumulus cells (CCs) or that of cumulus-denuded oocytes (DOs) supported oocyte maturation. Furthermore, species differences in oocyte GM are largely unknown. Our aim was to address these issues by using enzyme activity inhibitors, RNAi gene silencing and special media that could support nuclear but not cytoplasmic maturation when GM was inhibited. The results showed that GM in CCs promoted pig oocyte maturation by releasing metabolites from both pentose phosphate pathway and glycolysis. Both pyruvate and lactate were transferred into pig DOs by monocarboxylate transporter and pyruvate was further delivered into mitochondria by mitochondrial pyruvate carrier in both pig DOs and CCs. In both pig DOs and CCs, pyruvate and lactate were utilized through mitochondrial electron transport and LDH-catalyzed oxidation to pyruvate, respectively. Pig and mouse DOs differed in their CC dependency for glucose, pyruvate and lactate utilization. While mouse DOs could not, pig DOs could use the lactate-derived pyruvate. |
doi_str_mv | 10.1038/s41598-020-59709-6 |
format | Article |
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in vivo
counterparts. Although many studies reported effects of glucose metabolism (GM) on oocyte nuclear maturation, few reported on cytoplasmic maturation. Previous studies could not differentiate whether GM of cumulus cells (CCs) or that of cumulus-denuded oocytes (DOs) supported oocyte maturation. Furthermore, species differences in oocyte GM are largely unknown. Our aim was to address these issues by using enzyme activity inhibitors, RNAi gene silencing and special media that could support nuclear but not cytoplasmic maturation when GM was inhibited. The results showed that GM in CCs promoted pig oocyte maturation by releasing metabolites from both pentose phosphate pathway and glycolysis. Both pyruvate and lactate were transferred into pig DOs by monocarboxylate transporter and pyruvate was further delivered into mitochondria by mitochondrial pyruvate carrier in both pig DOs and CCs. In both pig DOs and CCs, pyruvate and lactate were utilized through mitochondrial electron transport and LDH-catalyzed oxidation to pyruvate, respectively. Pig and mouse DOs differed in their CC dependency for glucose, pyruvate and lactate utilization. While mouse DOs could not, pig DOs could use the lactate-derived pyruvate.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-020-59709-6</identifier><identifier>PMID: 32066834</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/136 ; 631/45 ; 631/80 ; Animals ; Cell differentiation ; Cell Nucleus - metabolism ; Coculture Techniques ; Cumulus Cells - metabolism ; Cytoplasm - metabolism ; Electron transport ; Enzymatic activity ; Female ; Gene silencing ; Glucose ; Glucose - metabolism ; Glycolysis ; Glycolysis - genetics ; Humanities and Social Sciences ; In Vitro Oocyte Maturation Techniques - methods ; Lactic acid ; Maturation ; Metabolism ; Metabolites ; Mice ; Mitochondria ; Mitochondria - metabolism ; multidisciplinary ; Oocytes ; Oocytes - growth & development ; Oocytes - metabolism ; Oxidation ; Oxidation-Reduction ; Pentose phosphate pathway ; Pentose Phosphate Pathway - genetics ; Pyruvic acid ; Pyruvic Acid - metabolism ; RNA-mediated interference ; Science ; Science (multidisciplinary) ; Swine</subject><ispartof>Scientific reports, 2020-02, Vol.10 (1), p.2782-2782, Article 2782</ispartof><rights>The Author(s) 2020</rights><rights>This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c577t-2aca77dba9af2bbc893a21178efa7849ab9d84d32d92007405c3dabb514658a73</citedby><cites>FETCH-LOGICAL-c577t-2aca77dba9af2bbc893a21178efa7849ab9d84d32d92007405c3dabb514658a73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7026050/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7026050/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27922,27923,41118,42187,51574,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32066834$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wen, Jing</creatorcontrib><creatorcontrib>Wang, Guo-Liang</creatorcontrib><creatorcontrib>Yuan, Hong-Jie</creatorcontrib><creatorcontrib>Zhang, Jie</creatorcontrib><creatorcontrib>Xie, Hong-Li</creatorcontrib><creatorcontrib>Gong, Shuai</creatorcontrib><creatorcontrib>Han, Xiao</creatorcontrib><creatorcontrib>Tan, Jing-He</creatorcontrib><title>Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>The developmental competence of IVM porcine oocytes is still low compared with that in their
in vivo
counterparts. Although many studies reported effects of glucose metabolism (GM) on oocyte nuclear maturation, few reported on cytoplasmic maturation. Previous studies could not differentiate whether GM of cumulus cells (CCs) or that of cumulus-denuded oocytes (DOs) supported oocyte maturation. Furthermore, species differences in oocyte GM are largely unknown. Our aim was to address these issues by using enzyme activity inhibitors, RNAi gene silencing and special media that could support nuclear but not cytoplasmic maturation when GM was inhibited. The results showed that GM in CCs promoted pig oocyte maturation by releasing metabolites from both pentose phosphate pathway and glycolysis. Both pyruvate and lactate were transferred into pig DOs by monocarboxylate transporter and pyruvate was further delivered into mitochondria by mitochondrial pyruvate carrier in both pig DOs and CCs. In both pig DOs and CCs, pyruvate and lactate were utilized through mitochondrial electron transport and LDH-catalyzed oxidation to pyruvate, respectively. Pig and mouse DOs differed in their CC dependency for glucose, pyruvate and lactate utilization. While mouse DOs could not, pig DOs could use the lactate-derived pyruvate.</description><subject>631/136</subject><subject>631/45</subject><subject>631/80</subject><subject>Animals</subject><subject>Cell differentiation</subject><subject>Cell Nucleus - metabolism</subject><subject>Coculture Techniques</subject><subject>Cumulus Cells - metabolism</subject><subject>Cytoplasm - metabolism</subject><subject>Electron transport</subject><subject>Enzymatic activity</subject><subject>Female</subject><subject>Gene silencing</subject><subject>Glucose</subject><subject>Glucose - metabolism</subject><subject>Glycolysis</subject><subject>Glycolysis - genetics</subject><subject>Humanities and Social Sciences</subject><subject>In Vitro Oocyte Maturation Techniques - methods</subject><subject>Lactic acid</subject><subject>Maturation</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Mice</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>multidisciplinary</subject><subject>Oocytes</subject><subject>Oocytes - growth & development</subject><subject>Oocytes - metabolism</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Pentose phosphate pathway</subject><subject>Pentose Phosphate Pathway - genetics</subject><subject>Pyruvic acid</subject><subject>Pyruvic Acid - metabolism</subject><subject>RNA-mediated interference</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Swine</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kUtP3TAQha2qqCDgD7BAlth0E_AztjdIFYIWCambsmJhTRznEpTEwXaK7r_Ht5dXu6g3tnS-OTPjg9ARJaeUcH2WBJVGV4SRShpFTFV_QnuMCFkxztjnD-9ddJjSAylHMiOo-YJ2OSN1rbnYQ3eXXeddTjh0eDUsLiSPR5-hCUOfRjxDvn-CdZEnPC1u8BAxTC126xzmAdLYOzxCXiLkviDFZO5XOISi-3SAdjoYkj98uffR7dXlr4sf1c3P79cX324qJ5XKFQMHSrUNGOhY0zhtODBKlfYdKC0MNKbVouWsNYwQJYh0vIWmkVTUUoPi--h86zsvzehb56ccYbBz7EeIaxugt38rU39vV-G3VYTVRJJi8PXFIIbHxadsxz45Pwww-bAky7hUoqZGb3qd_IM-hCVOZb0NVT61plwUim0pF0NK0Xdvw1BiN_HZbXy2xGf_xGfrUnT8cY23ktewCsC3QCrStPLxvfd_bJ8BeV-nWw</recordid><startdate>20200217</startdate><enddate>20200217</enddate><creator>Wen, Jing</creator><creator>Wang, Guo-Liang</creator><creator>Yuan, Hong-Jie</creator><creator>Zhang, Jie</creator><creator>Xie, Hong-Li</creator><creator>Gong, Shuai</creator><creator>Han, Xiao</creator><creator>Tan, Jing-He</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20200217</creationdate><title>Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes</title><author>Wen, Jing ; Wang, Guo-Liang ; Yuan, Hong-Jie ; Zhang, Jie ; Xie, Hong-Li ; Gong, Shuai ; Han, Xiao ; Tan, Jing-He</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c577t-2aca77dba9af2bbc893a21178efa7849ab9d84d32d92007405c3dabb514658a73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>631/136</topic><topic>631/45</topic><topic>631/80</topic><topic>Animals</topic><topic>Cell differentiation</topic><topic>Cell Nucleus - metabolism</topic><topic>Coculture Techniques</topic><topic>Cumulus Cells - metabolism</topic><topic>Cytoplasm - metabolism</topic><topic>Electron transport</topic><topic>Enzymatic activity</topic><topic>Female</topic><topic>Gene silencing</topic><topic>Glucose</topic><topic>Glucose - metabolism</topic><topic>Glycolysis</topic><topic>Glycolysis - genetics</topic><topic>Humanities and Social Sciences</topic><topic>In Vitro Oocyte Maturation Techniques - methods</topic><topic>Lactic acid</topic><topic>Maturation</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Mice</topic><topic>Mitochondria</topic><topic>Mitochondria - metabolism</topic><topic>multidisciplinary</topic><topic>Oocytes</topic><topic>Oocytes - growth & development</topic><topic>Oocytes - metabolism</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Pentose phosphate pathway</topic><topic>Pentose Phosphate Pathway - genetics</topic><topic>Pyruvic acid</topic><topic>Pyruvic Acid - metabolism</topic><topic>RNA-mediated interference</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Swine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wen, Jing</creatorcontrib><creatorcontrib>Wang, Guo-Liang</creatorcontrib><creatorcontrib>Yuan, Hong-Jie</creatorcontrib><creatorcontrib>Zhang, Jie</creatorcontrib><creatorcontrib>Xie, Hong-Li</creatorcontrib><creatorcontrib>Gong, Shuai</creatorcontrib><creatorcontrib>Han, Xiao</creatorcontrib><creatorcontrib>Tan, Jing-He</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wen, Jing</au><au>Wang, Guo-Liang</au><au>Yuan, Hong-Jie</au><au>Zhang, Jie</au><au>Xie, Hong-Li</au><au>Gong, Shuai</au><au>Han, Xiao</au><au>Tan, Jing-He</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2020-02-17</date><risdate>2020</risdate><volume>10</volume><issue>1</issue><spage>2782</spage><epage>2782</epage><pages>2782-2782</pages><artnum>2782</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>The developmental competence of IVM porcine oocytes is still low compared with that in their
in vivo
counterparts. Although many studies reported effects of glucose metabolism (GM) on oocyte nuclear maturation, few reported on cytoplasmic maturation. Previous studies could not differentiate whether GM of cumulus cells (CCs) or that of cumulus-denuded oocytes (DOs) supported oocyte maturation. Furthermore, species differences in oocyte GM are largely unknown. Our aim was to address these issues by using enzyme activity inhibitors, RNAi gene silencing and special media that could support nuclear but not cytoplasmic maturation when GM was inhibited. The results showed that GM in CCs promoted pig oocyte maturation by releasing metabolites from both pentose phosphate pathway and glycolysis. Both pyruvate and lactate were transferred into pig DOs by monocarboxylate transporter and pyruvate was further delivered into mitochondria by mitochondrial pyruvate carrier in both pig DOs and CCs. In both pig DOs and CCs, pyruvate and lactate were utilized through mitochondrial electron transport and LDH-catalyzed oxidation to pyruvate, respectively. Pig and mouse DOs differed in their CC dependency for glucose, pyruvate and lactate utilization. While mouse DOs could not, pig DOs could use the lactate-derived pyruvate.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32066834</pmid><doi>10.1038/s41598-020-59709-6</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 631/136 631/45 631/80 Animals Cell differentiation Cell Nucleus - metabolism Coculture Techniques Cumulus Cells - metabolism Cytoplasm - metabolism Electron transport Enzymatic activity Female Gene silencing Glucose Glucose - metabolism Glycolysis Glycolysis - genetics Humanities and Social Sciences In Vitro Oocyte Maturation Techniques - methods Lactic acid Maturation Metabolism Metabolites Mice Mitochondria Mitochondria - metabolism multidisciplinary Oocytes Oocytes - growth & development Oocytes - metabolism Oxidation Oxidation-Reduction Pentose phosphate pathway Pentose Phosphate Pathway - genetics Pyruvic acid Pyruvic Acid - metabolism RNA-mediated interference Science Science (multidisciplinary) Swine |
title | Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes |
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