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Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction

Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction
Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction
This study was performed to address the possible role of pyruvate in meiotic induction in mouse oocytes. Cumulus cell-enclosed oocytes from primed, immature mice were cultured in 7.5 μl microdrops under oil for 9 or 18 h in medium containing 4 mmol hypoxanthine l−1 plus 0.23 mmol pyruvate l−1, l mmol pyruvate l−1, or 1 mmol pyruvate l−1 plus 5.5 mmol glucose l−1. When compared with cultures containing 0.23 mmol pyruvate l−1, 1 mmol pyruvate l−1 induced germinal vesicle breakdown, and this was preceded by an increase in pyruvate utilization. Addition of glucose prevented both the increase in pyruvate consumption and the meiotic induction. When different combinations of pyruvate and glucose were tested on oocyte maturation in microdrop cultures, a high concentration of pyruvate or glucose alone was stimulatory to maturation. Addition of the complementary energy substrate prevented the induction of germinal vesicle breakdown and reduced the amount of substrate consumption. During spontaneous maturation in vitro, oocyte–cumulus cell complexes consumed glucose for the first 3 h; however, during the second 3 h period, which followed germinal vesicle breakdown, glucose consumption decreased and net pyruvate utilization was initiated. Treatment of hypoxanthine-arrested oocytes with dichloroacetate, an activator of pyruvate dehydrogenase, stimulated pyruvate consumption but had no effect on germinal vesicle breakdown. Although FSH stimulates meiotic resumption, no changes in pyruvate consumption were observed in response to this gonadotrophin. Measurement of oxygen consumption by hypoxanthine-treated complexes revealed no effect of high concentrations of pyruvate on respiration, and FSH treatment resulted in a suppression of oxygen utilization. These data indicate that, in mouse oocyte–cumulus cell complexes, pyruvate and glucose can each modulate metabolism of the other substrate, and this can significantly influence meiotic maturation of the oocyte. In addition, augmentation of pyruvate oxidation does not appear to play a mediating role in meiotic induction triggered by energy substrate manipulation or gonadotrophin treatment.
1-10
Downs, S.M.
11fa69d6-e877-48df-8863-1c55d490447f
Houghton, F.D.
53946041-127e-45a8-9edb-bf4b3c23005f
Humpherson, P.G.
bc23acf1-9272-4e71-812f-1988e82686cf
Leese, H.J.
1f369c23-4361-4534-a093-54699ec5eceb
Downs, S.M.
11fa69d6-e877-48df-8863-1c55d490447f
Houghton, F.D.
53946041-127e-45a8-9edb-bf4b3c23005f
Humpherson, P.G.
bc23acf1-9272-4e71-812f-1988e82686cf
Leese, H.J.
1f369c23-4361-4534-a093-54699ec5eceb

Downs, S.M., Houghton, F.D., Humpherson, P.G. and Leese, H.J. (1997) Substrate utilization and maturation of cumulus cell-enclosed mouse oocytes: evidence that pyruvate oxidation does not mediate meiotic induction. Journal of Reproduction and Fertility, 110 (1), 1-10. (doi:10.1530/jrf.0.1100001).

Record type: Article

Abstract

This study was performed to address the possible role of pyruvate in meiotic induction in mouse oocytes. Cumulus cell-enclosed oocytes from primed, immature mice were cultured in 7.5 μl microdrops under oil for 9 or 18 h in medium containing 4 mmol hypoxanthine l−1 plus 0.23 mmol pyruvate l−1, l mmol pyruvate l−1, or 1 mmol pyruvate l−1 plus 5.5 mmol glucose l−1. When compared with cultures containing 0.23 mmol pyruvate l−1, 1 mmol pyruvate l−1 induced germinal vesicle breakdown, and this was preceded by an increase in pyruvate utilization. Addition of glucose prevented both the increase in pyruvate consumption and the meiotic induction. When different combinations of pyruvate and glucose were tested on oocyte maturation in microdrop cultures, a high concentration of pyruvate or glucose alone was stimulatory to maturation. Addition of the complementary energy substrate prevented the induction of germinal vesicle breakdown and reduced the amount of substrate consumption. During spontaneous maturation in vitro, oocyte–cumulus cell complexes consumed glucose for the first 3 h; however, during the second 3 h period, which followed germinal vesicle breakdown, glucose consumption decreased and net pyruvate utilization was initiated. Treatment of hypoxanthine-arrested oocytes with dichloroacetate, an activator of pyruvate dehydrogenase, stimulated pyruvate consumption but had no effect on germinal vesicle breakdown. Although FSH stimulates meiotic resumption, no changes in pyruvate consumption were observed in response to this gonadotrophin. Measurement of oxygen consumption by hypoxanthine-treated complexes revealed no effect of high concentrations of pyruvate on respiration, and FSH treatment resulted in a suppression of oxygen utilization. These data indicate that, in mouse oocyte–cumulus cell complexes, pyruvate and glucose can each modulate metabolism of the other substrate, and this can significantly influence meiotic maturation of the oocyte. In addition, augmentation of pyruvate oxidation does not appear to play a mediating role in meiotic induction triggered by energy substrate manipulation or gonadotrophin treatment.

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More information

Published date: 1 May 1997
Additional Information: Copyright: 1997 Journals of Reproduction and Fertility

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Local EPrints ID: 457893
URI: http://eprints.soton.ac.uk/id/eprint/457893
PURE UUID: 7c2c9eae-9019-44df-ad12-197a3a75c196
ORCID for F.D. Houghton: ORCID iD orcid.org/0000-0002-5167-1694

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Date deposited: 21 Jun 2022 18:13
Last modified: 17 Mar 2024 03:05

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Contributors

Author: S.M. Downs
Author: F.D. Houghton ORCID iD
Author: P.G. Humpherson
Author: H.J. Leese

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