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doi: 10.1242/10.1242/dev.00296

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

Rémi Dumollard^1,*,, Katherine Hammar², Marshall Porterfield², Peter J. Smith², Christian Cibert³, Christian Rouvière¹ and Christian Sardet¹

¹ BioMarCell, Unité de Biologie du Développement UMR 7009 CNRS/Paris VI, Observatoire, Station Zoologique, Villefranche sur Mer, 06230 France
² National Vibrating Probe Facility, Marine Biological Laboratory, Woods Hole, MA 02543-1015, USA
³ Laboratoire de Biologie du Développement, Institut Jacques Monod, CNRS, Universités Paris 6 et Paris 7, 2, place Jussieu, F-75251 Paris, France
^* Present address: Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK

Author for correspondence (e-mail: r.dumollard{at}ucl.ac.uk)

Accepted 15 November 2002

Fertilization increases both cytosolic Ca²⁺ 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 Ca²⁺ waves emitted by two pacemakers (PM1 and PM2). Oxygen consumption also increases in response to Ins(1,4,5)P₃-induced Ca²⁺ transients. Using mitochondrial inhibitors we show that active mitochondria sequester cytosolic Ca²⁺ during sperm-triggered Ca²⁺ waves and that they are strictly necessary for triggering and sustaining the activity of the meiotic Ca²⁺ wave pacemaker PM2. Strikingly, the activity of the Ca²⁺ 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 Ca²⁺, the egg's mitochondria are stimulated by Ins(1,4,5)P₃-mediated Ca²⁺ signals. In turn, mitochondrial ATP production is required to sustain the activity of the meiotic Ca²⁺ wave pacemaker PM2.

Key words: Fertilization, Respiration, Ca²⁺ waves, Mitochondria, Endoplasmic reticulum, ATP, Ca²⁺ wave pacemakers, Ascidian

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