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Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion

Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion
Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion
Fertilization increases both cytosolic Ca(2+) concentration and oxygen consumption in the egg but the relationship between these two phenomena remains largely obscure. We have measured mitochondrial oxygen consumption and the mitochondrial NADH concentration on single ascidian eggs and found that they increase in phase with each series of meiotic Ca(2+) waves emitted by two pacemakers (PM1 and PM2). Oxygen consumption also increases in response to Ins(1,4,5)P(3)-induced Ca(2+) transients. Using mitochondrial inhibitors we show that active mitochondria sequester cytosolic Ca(2+) during sperm-triggered Ca(2+) waves and that they are strictly necessary for triggering and sustaining the activity of the meiotic Ca(2+) wave pacemaker PM2. Strikingly, the activity of the Ca(2+) wave pacemaker PM2 can be restored or stimulated by flash photolysis of caged ATP. Taken together our observations provide the first evidence that, in addition to buffering cytosolic Ca(2+), the egg's mitochondria are stimulated by Ins(1,4,5)P(3)-mediated Ca(2+) signals. In turn, mitochondrial ATP production is required to sustain the activity of the meiotic Ca(2+) wave pacemaker PM2
1477-9129
683-692
Dumollard, Remi
742f3baa-be31-4316-8b33-47052f851f82
Hammar, Katherine
c1706f67-2af6-4246-9c7f-341d48a693ec
Porterfield, Marshall
1d0bdeb0-1318-490b-a840-f2250667e70f
Smith, Peter J.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Cibert, Christian
8aad7550-fb92-4516-8865-7115ef66c3bd
Rouviere, Christian
1b0a2155-8821-45e1-9a07-0e4914df9a77
Sardet, Christian
74c5403f-c400-4acc-9f1d-7caee62b17a5
Dumollard, Remi
742f3baa-be31-4316-8b33-47052f851f82
Hammar, Katherine
c1706f67-2af6-4246-9c7f-341d48a693ec
Porterfield, Marshall
1d0bdeb0-1318-490b-a840-f2250667e70f
Smith, Peter J.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Cibert, Christian
8aad7550-fb92-4516-8865-7115ef66c3bd
Rouviere, Christian
1b0a2155-8821-45e1-9a07-0e4914df9a77
Sardet, Christian
74c5403f-c400-4acc-9f1d-7caee62b17a5

Dumollard, Remi, Hammar, Katherine, Porterfield, Marshall, Smith, Peter J., Cibert, Christian, Rouviere, Christian and Sardet, Christian (2003) Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development, 130 (4), 683-692. (doi:10.1242/dev.00296). (PMID:12505999)

Record type: Article

Abstract

Fertilization increases both cytosolic Ca(2+) concentration and oxygen consumption in the egg but the relationship between these two phenomena remains largely obscure. We have measured mitochondrial oxygen consumption and the mitochondrial NADH concentration on single ascidian eggs and found that they increase in phase with each series of meiotic Ca(2+) waves emitted by two pacemakers (PM1 and PM2). Oxygen consumption also increases in response to Ins(1,4,5)P(3)-induced Ca(2+) transients. Using mitochondrial inhibitors we show that active mitochondria sequester cytosolic Ca(2+) during sperm-triggered Ca(2+) waves and that they are strictly necessary for triggering and sustaining the activity of the meiotic Ca(2+) wave pacemaker PM2. Strikingly, the activity of the Ca(2+) wave pacemaker PM2 can be restored or stimulated by flash photolysis of caged ATP. Taken together our observations provide the first evidence that, in addition to buffering cytosolic Ca(2+), the egg's mitochondria are stimulated by Ins(1,4,5)P(3)-mediated Ca(2+) signals. In turn, mitochondrial ATP production is required to sustain the activity of the meiotic Ca(2+) wave pacemaker PM2

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Published date: February 2003
Organisations: University of Southampton

Identifiers

Local EPrints ID: 188765
URI: http://eprints.soton.ac.uk/id/eprint/188765
ISSN: 1477-9129
PURE UUID: 00cab44a-3364-4fc8-913f-e11252f1e644
ORCID for Peter J. Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 13 Jun 2011 14:43
Last modified: 17 Dec 2019 01:39

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Contributors

Author: Remi Dumollard
Author: Katherine Hammar
Author: Marshall Porterfield
Author: Peter J. Smith ORCID iD
Author: Christian Cibert
Author: Christian Rouviere
Author: Christian Sardet

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