Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway
In this study we tested the hypothesis that the pentose phosphate pathway (PPP) participates in the meiotic induction of mouse oocytes. The electron acceptors methylene blue, phenazine ethosulfate (PES), and pyrroline-5-carboxylate (P5C) oxidize NADPH to NADP and activate the NADP-dependent enzymes...
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| Veröffentlicht in: | Biology of reproduction 1998-04, Vol.58 (4), p.1084-1094 |
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| creator | DOWNS, S. M HUMPHERSON, P. G LEESE, H. J |
| description | In this study we tested the hypothesis that the pentose phosphate pathway (PPP) participates in the meiotic induction of mouse
oocytes. The electron acceptors methylene blue, phenazine ethosulfate (PES), and pyrroline-5-carboxylate (P5C) oxidize NADPH
to NADP and activate the NADP-dependent enzymes of the PPP. Each of these compounds triggered a dose-dependent increase in
meiotic maturation in hypoxanthine-arrested cumulus cell-enclosed oocytes during 17- to 18-h cultures. More than 96% of the
oocytes underwent germinal vesicle breakdown (GVB) at the highest concentrations of P5C and PES tested (250 and 1 microM,
respectively) as compared to only 45-52% of control oocytes. P5C was also stimulatory to denuded oocytes. Analysis of energy
substrates in microdrop cultures revealed a 3.6-fold increase in glucose consumption by PES-treated oocyte-cumulus cell complexes
that was associated with stimulation of GVB. On the other hand, 2-deoxyglucose, which interferes with glucose utilization,
prevented the induction of maturation brought about by P5C. Apocynin and diphenyleneiodonium, inhibitors of NADPH oxidase,
prevented meiotic maturation in the presence or absence of FSH. Gonadotropin-induced maturation was also prevented by 6-aminonicotinamide
(6-AN) and dehydroepiandrosterone (DHEA), inhibitors of the two NADP-dependent enzymes of the PPP, and this was accompanied
by suppression of glucose consumption. Phosphoribosyl-pyrophosphate (PRPP) is an important compound required in purine metabolism
and can be formed from the end product of the oxidative arm of the PPP, ribose-5-phosphate. Ribose, which can be metabolized
to PRPP, increased PRPP synthesis in complexes and induced meiotic maturation when added to hypoxanthine-arrested cumulus
cell-enclosed oocytes in glucose-free medium in both the presence and absence of FSH. PRPP levels within complexes were also
increased by glucose and FSH, but were reduced by hypoxanthine, 6-AN, and DHEA. In addition, exogenous PRPP stimulated maturation
in hypoxanthine-arrested oocytes. These results support the proposition that glucose metabolism through the PPP is important
in the meiotic induction mechanism and may involve the generation of PRPP that acts, at least in part, through the purine
metabolizing pathways. |
| doi_str_mv | 10.1095/biolreprod58.4.1084 |
| format | Article |
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oocytes. The electron acceptors methylene blue, phenazine ethosulfate (PES), and pyrroline-5-carboxylate (P5C) oxidize NADPH
to NADP and activate the NADP-dependent enzymes of the PPP. Each of these compounds triggered a dose-dependent increase in
meiotic maturation in hypoxanthine-arrested cumulus cell-enclosed oocytes during 17- to 18-h cultures. More than 96% of the
oocytes underwent germinal vesicle breakdown (GVB) at the highest concentrations of P5C and PES tested (250 and 1 microM,
respectively) as compared to only 45-52% of control oocytes. P5C was also stimulatory to denuded oocytes. Analysis of energy
substrates in microdrop cultures revealed a 3.6-fold increase in glucose consumption by PES-treated oocyte-cumulus cell complexes
that was associated with stimulation of GVB. On the other hand, 2-deoxyglucose, which interferes with glucose utilization,
prevented the induction of maturation brought about by P5C. Apocynin and diphenyleneiodonium, inhibitors of NADPH oxidase,
prevented meiotic maturation in the presence or absence of FSH. Gonadotropin-induced maturation was also prevented by 6-aminonicotinamide
(6-AN) and dehydroepiandrosterone (DHEA), inhibitors of the two NADP-dependent enzymes of the PPP, and this was accompanied
by suppression of glucose consumption. Phosphoribosyl-pyrophosphate (PRPP) is an important compound required in purine metabolism
and can be formed from the end product of the oxidative arm of the PPP, ribose-5-phosphate. Ribose, which can be metabolized
to PRPP, increased PRPP synthesis in complexes and induced meiotic maturation when added to hypoxanthine-arrested cumulus
cell-enclosed oocytes in glucose-free medium in both the presence and absence of FSH. PRPP levels within complexes were also
increased by glucose and FSH, but were reduced by hypoxanthine, 6-AN, and DHEA. In addition, exogenous PRPP stimulated maturation
in hypoxanthine-arrested oocytes. These results support the proposition that glucose metabolism through the PPP is important
in the meiotic induction mechanism and may involve the generation of PRPP that acts, at least in part, through the purine
metabolizing pathways.</description><identifier>ISSN: 0006-3363</identifier><identifier>EISSN: 1529-7268</identifier><identifier>DOI: 10.1095/biolreprod58.4.1084</identifier><identifier>PMID: 9546744</identifier><identifier>CODEN: BIREBV</identifier><language>eng</language><publisher>Madison, WI: Society for the Study of Reproduction</publisher><subject>Animals ; Biological and medical sciences ; Deoxyglucose - pharmacology ; Enzyme Inhibitors - pharmacology ; Female ; Follicle Stimulating Hormone - pharmacology ; Fundamental and applied biological sciences. Psychology ; Glucosephosphate Dehydrogenase - antagonists & inhibitors ; Glucosephosphate Dehydrogenase - metabolism ; Mammalian female genital system ; Meiosis ; Methylene Blue - pharmacology ; Mice ; Mice, Inbred C57BL ; Morphology. Physiology ; NADP - metabolism ; NADPH Oxidases - antagonists & inhibitors ; Oocytes - cytology ; Ovarian Follicle - physiology ; Oxidation-Reduction ; Pentose Phosphate Pathway - physiology ; Phenazines - pharmacology ; Phosphogluconate Dehydrogenase - antagonists & inhibitors ; Phosphogluconate Dehydrogenase - metabolism ; Pyrroles - pharmacology ; Vertebrates: reproduction</subject><ispartof>Biology of reproduction, 1998-04, Vol.58 (4), p.1084-1094</ispartof><rights>1998 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=2203138$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9546744$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>DOWNS, S. M</creatorcontrib><creatorcontrib>HUMPHERSON, P. G</creatorcontrib><creatorcontrib>LEESE, H. J</creatorcontrib><title>Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway</title><title>Biology of reproduction</title><addtitle>Biol Reprod</addtitle><description>In this study we tested the hypothesis that the pentose phosphate pathway (PPP) participates in the meiotic induction of mouse
oocytes. The electron acceptors methylene blue, phenazine ethosulfate (PES), and pyrroline-5-carboxylate (P5C) oxidize NADPH
to NADP and activate the NADP-dependent enzymes of the PPP. Each of these compounds triggered a dose-dependent increase in
meiotic maturation in hypoxanthine-arrested cumulus cell-enclosed oocytes during 17- to 18-h cultures. More than 96% of the
oocytes underwent germinal vesicle breakdown (GVB) at the highest concentrations of P5C and PES tested (250 and 1 microM,
respectively) as compared to only 45-52% of control oocytes. P5C was also stimulatory to denuded oocytes. Analysis of energy
substrates in microdrop cultures revealed a 3.6-fold increase in glucose consumption by PES-treated oocyte-cumulus cell complexes
that was associated with stimulation of GVB. On the other hand, 2-deoxyglucose, which interferes with glucose utilization,
prevented the induction of maturation brought about by P5C. Apocynin and diphenyleneiodonium, inhibitors of NADPH oxidase,
prevented meiotic maturation in the presence or absence of FSH. Gonadotropin-induced maturation was also prevented by 6-aminonicotinamide
(6-AN) and dehydroepiandrosterone (DHEA), inhibitors of the two NADP-dependent enzymes of the PPP, and this was accompanied
by suppression of glucose consumption. Phosphoribosyl-pyrophosphate (PRPP) is an important compound required in purine metabolism
and can be formed from the end product of the oxidative arm of the PPP, ribose-5-phosphate. Ribose, which can be metabolized
to PRPP, increased PRPP synthesis in complexes and induced meiotic maturation when added to hypoxanthine-arrested cumulus
cell-enclosed oocytes in glucose-free medium in both the presence and absence of FSH. PRPP levels within complexes were also
increased by glucose and FSH, but were reduced by hypoxanthine, 6-AN, and DHEA. In addition, exogenous PRPP stimulated maturation
in hypoxanthine-arrested oocytes. These results support the proposition that glucose metabolism through the PPP is important
in the meiotic induction mechanism and may involve the generation of PRPP that acts, at least in part, through the purine
metabolizing pathways.</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Deoxyglucose - pharmacology</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Female</subject><subject>Follicle Stimulating Hormone - pharmacology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Glucosephosphate Dehydrogenase - antagonists & inhibitors</subject><subject>Glucosephosphate Dehydrogenase - metabolism</subject><subject>Mammalian female genital system</subject><subject>Meiosis</subject><subject>Methylene Blue - pharmacology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Morphology. Physiology</subject><subject>NADP - metabolism</subject><subject>NADPH Oxidases - antagonists & inhibitors</subject><subject>Oocytes - cytology</subject><subject>Ovarian Follicle - physiology</subject><subject>Oxidation-Reduction</subject><subject>Pentose Phosphate Pathway - physiology</subject><subject>Phenazines - pharmacology</subject><subject>Phosphogluconate Dehydrogenase - antagonists & inhibitors</subject><subject>Phosphogluconate Dehydrogenase - metabolism</subject><subject>Pyrroles - pharmacology</subject><subject>Vertebrates: reproduction</subject><issn>0006-3363</issn><issn>1529-7268</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctu1TAQhi0EKofCEyAkLxC7tL4lttmhqlykVmzadTRxJsTIiUPsNDpvj484giWr-TX_p7kS8pazK85sfd35GFZc1tjX5kqVnFHPyIHXwlZaNOY5OTDGmkrKRr4kr1L6yRhXUsgLcmFr1WilDmS4Rx-zd9TP_eayj3NR1G3TFrZEHYZQ4exCTNjTKW4JaYzumDF9LNxTDE844ZxpHGgekS5FF5QuY0zLCLkoyOMOx9fkxQAh4ZtzvCSPn28fbr5Wd9-_fLv5dFeNwupcdb1kNQdutLW6R206Aa4G3g0MnB5AO95x1gzCDFBbobWBpukdaglaq7LnJfnwp265yq8NU24nn05bwIxl-lZbbTRj9r8gbxTjkp_Ad2dw6ybs22X1E6zH9nzB4r8_-5AchGGF2fn0FxOCSS7Nv36j_zHufsU2TRBCKSrbfd9r06r29ED5G4TikQc</recordid><startdate>19980401</startdate><enddate>19980401</enddate><creator>DOWNS, S. M</creator><creator>HUMPHERSON, P. G</creator><creator>LEESE, H. J</creator><general>Society for the Study of Reproduction</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>19980401</creationdate><title>Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway</title><author>DOWNS, S. M ; HUMPHERSON, P. G ; LEESE, H. J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-h297t-bd3051a187997de78b2ac5a1bf0ac7fa7c1b106f28fa592778a66dce73a774363</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Deoxyglucose - pharmacology</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Female</topic><topic>Follicle Stimulating Hormone - pharmacology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Glucosephosphate Dehydrogenase - antagonists & inhibitors</topic><topic>Glucosephosphate Dehydrogenase - metabolism</topic><topic>Mammalian female genital system</topic><topic>Meiosis</topic><topic>Methylene Blue - pharmacology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Morphology. Physiology</topic><topic>NADP - metabolism</topic><topic>NADPH Oxidases - antagonists & inhibitors</topic><topic>Oocytes - cytology</topic><topic>Ovarian Follicle - physiology</topic><topic>Oxidation-Reduction</topic><topic>Pentose Phosphate Pathway - physiology</topic><topic>Phenazines - pharmacology</topic><topic>Phosphogluconate Dehydrogenase - antagonists & inhibitors</topic><topic>Phosphogluconate Dehydrogenase - metabolism</topic><topic>Pyrroles - pharmacology</topic><topic>Vertebrates: reproduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>DOWNS, S. M</creatorcontrib><creatorcontrib>HUMPHERSON, P. G</creatorcontrib><creatorcontrib>LEESE, H. J</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>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Biology of reproduction</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>DOWNS, S. M</au><au>HUMPHERSON, P. G</au><au>LEESE, H. J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway</atitle><jtitle>Biology of reproduction</jtitle><addtitle>Biol Reprod</addtitle><date>1998-04-01</date><risdate>1998</risdate><volume>58</volume><issue>4</issue><spage>1084</spage><epage>1094</epage><pages>1084-1094</pages><issn>0006-3363</issn><eissn>1529-7268</eissn><coden>BIREBV</coden><abstract>In this study we tested the hypothesis that the pentose phosphate pathway (PPP) participates in the meiotic induction of mouse
oocytes. The electron acceptors methylene blue, phenazine ethosulfate (PES), and pyrroline-5-carboxylate (P5C) oxidize NADPH
to NADP and activate the NADP-dependent enzymes of the PPP. Each of these compounds triggered a dose-dependent increase in
meiotic maturation in hypoxanthine-arrested cumulus cell-enclosed oocytes during 17- to 18-h cultures. More than 96% of the
oocytes underwent germinal vesicle breakdown (GVB) at the highest concentrations of P5C and PES tested (250 and 1 microM,
respectively) as compared to only 45-52% of control oocytes. P5C was also stimulatory to denuded oocytes. Analysis of energy
substrates in microdrop cultures revealed a 3.6-fold increase in glucose consumption by PES-treated oocyte-cumulus cell complexes
that was associated with stimulation of GVB. On the other hand, 2-deoxyglucose, which interferes with glucose utilization,
prevented the induction of maturation brought about by P5C. Apocynin and diphenyleneiodonium, inhibitors of NADPH oxidase,
prevented meiotic maturation in the presence or absence of FSH. Gonadotropin-induced maturation was also prevented by 6-aminonicotinamide
(6-AN) and dehydroepiandrosterone (DHEA), inhibitors of the two NADP-dependent enzymes of the PPP, and this was accompanied
by suppression of glucose consumption. Phosphoribosyl-pyrophosphate (PRPP) is an important compound required in purine metabolism
and can be formed from the end product of the oxidative arm of the PPP, ribose-5-phosphate. Ribose, which can be metabolized
to PRPP, increased PRPP synthesis in complexes and induced meiotic maturation when added to hypoxanthine-arrested cumulus
cell-enclosed oocytes in glucose-free medium in both the presence and absence of FSH. PRPP levels within complexes were also
increased by glucose and FSH, but were reduced by hypoxanthine, 6-AN, and DHEA. In addition, exogenous PRPP stimulated maturation
in hypoxanthine-arrested oocytes. These results support the proposition that glucose metabolism through the PPP is important
in the meiotic induction mechanism and may involve the generation of PRPP that acts, at least in part, through the purine
metabolizing pathways.</abstract><cop>Madison, WI</cop><pub>Society for the Study of Reproduction</pub><pmid>9546744</pmid><doi>10.1095/biolreprod58.4.1084</doi><tpages>11</tpages></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0006-3363 |
| ispartof | Biology of reproduction, 1998-04, Vol.58 (4), p.1084-1094 |
| issn | 0006-3363 1529-7268 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_79787009 |
| source | MEDLINE; Oxford Journals Online; EZB Electronic Journals Library |
| subjects | Animals Biological and medical sciences Deoxyglucose - pharmacology Enzyme Inhibitors - pharmacology Female Follicle Stimulating Hormone - pharmacology Fundamental and applied biological sciences. Psychology Glucosephosphate Dehydrogenase - antagonists & inhibitors Glucosephosphate Dehydrogenase - metabolism Mammalian female genital system Meiosis Methylene Blue - pharmacology Mice Mice, Inbred C57BL Morphology. Physiology NADP - metabolism NADPH Oxidases - antagonists & inhibitors Oocytes - cytology Ovarian Follicle - physiology Oxidation-Reduction Pentose Phosphate Pathway - physiology Phenazines - pharmacology Phosphogluconate Dehydrogenase - antagonists & inhibitors Phosphogluconate Dehydrogenase - metabolism Pyrroles - pharmacology Vertebrates: reproduction |
| title | Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway |
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