{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T13:24:13Z","timestamp":1783689853575,"version":"3.55.0"},"reference-count":50,"publisher":"The Company of Biologists","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2003,2,15]]},"abstract":"<jats:p>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.<\/jats:p>","DOI":"10.1242\/dev.00296","type":"journal-article","created":{"date-parts":[[2003,1,6]],"date-time":"2003-01-06T23:32:07Z","timestamp":1041895927000},"page":"683-692","source":"Crossref","is-referenced-by-count":80,"title":["Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion"],"prefix":"10.1242","volume":"130","author":[{"given":"Re\u0301mi","family":"Dumollard","sequence":"first","affiliation":[{"name":"BioMarCell, Unite\u0301 de Biologie du De\u0301veloppement UMR 7009 CNRS\/Paris VI, Observatoire, Station Zoologique, Villefranche sur Mer, 06230 France"},{"name":"Present address: Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine","family":"Hammar","sequence":"additional","affiliation":[{"name":"National Vibrating Probe Facility, Marine Biological Laboratory, Woods Hole,MA 02543-1015, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marshall","family":"Porterfield","sequence":"additional","affiliation":[{"name":"National Vibrating Probe Facility, Marine Biological Laboratory, Woods Hole,MA 02543-1015, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter J.","family":"Smith","sequence":"additional","affiliation":[{"name":"National Vibrating Probe Facility, Marine Biological Laboratory, Woods Hole,MA 02543-1015, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Cibert","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie du De\u0301veloppement, Institut Jacques Monod, CNRS,Universite\u0301s Paris 6 et Paris 7, 2, place Jussieu, F-75251 Paris,France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Rouvie\u0300re","sequence":"additional","affiliation":[{"name":"BioMarCell, Unite\u0301 de Biologie du De\u0301veloppement UMR 7009 CNRS\/Paris VI, Observatoire, Station Zoologique, Villefranche sur Mer, 06230 France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Sardet","sequence":"additional","affiliation":[{"name":"BioMarCell, Unite\u0301 de Biologie du De\u0301veloppement UMR 7009 CNRS\/Paris VI, Observatoire, Station Zoologique, Villefranche sur Mer, 06230 France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042611485254300_REF1","doi-asserted-by":"crossref","unstructured":"Berridge, M. J. (1997). Elementary and global aspects of calcium signalling. J. Physiol.499,291-306.","DOI":"10.1113\/jphysiol.1997.sp021927"},{"key":"2021042611485254300_REF2","doi-asserted-by":"crossref","unstructured":"Boitier, E., Rea, R. and Duchen, M. (1999). Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes. J. Cell Biol.145,795-808.","DOI":"10.1083\/jcb.145.4.795"},{"key":"2021042611485254300_REF3","doi-asserted-by":"crossref","unstructured":"Bootman, M. D. and Lipp, P. (1999). Calcium signalling: ringing changes to the `bell-shaped curve'. Curr. Biol.9,R876-R878.","DOI":"10.1016\/S0960-9822(00)80072-X"},{"key":"2021042611485254300_","doi-asserted-by":"crossref","unstructured":"Brind, S., Swann, K. and Carroll, J. (2000). Inositol 1,4,5-trisphosphate receptors are downregulated in mouse oocytes in response to sperm or adenophostin A but not to increases in intracellular Ca2+ or egg activation. Dev. Biol.223,251-65.","DOI":"10.1006\/dbio.2000.9728"},{"key":"2021042611485254300_REF5","doi-asserted-by":"crossref","unstructured":"Duchen, M. (2000). Mitochondria and calcium:from cell signalling to cell death. J. Physiol.529.1,57-68.","DOI":"10.1111\/j.1469-7793.2000.00057.x"},{"key":"2021042611485254300_REF6","unstructured":"Dumollard, R. and Sardet, C. (2001). Three calcium wave pacemakers in the ascidian egg. J. Cell. Sci.114,2471-2481"},{"key":"2021042611485254300_REF7","doi-asserted-by":"crossref","unstructured":"Dumollard, R., Carroll, J., Dupont, G. and Sardet, C.(2002). Calcium wave pacemakers in eggs. J. Cell Sci.115,3557-3564.","DOI":"10.1242\/jcs.00056"},{"key":"2021042611485254300_REF8","doi-asserted-by":"crossref","unstructured":"Eisen, A. and Reynolds, G. T. (1985). Source and sinks for the calcium released during fertilization of single sea urchin eggs. J. Cell Biol.100,1522-1527.","DOI":"10.1083\/jcb.100.5.1522"},{"key":"2021042611485254300_REF9","doi-asserted-by":"crossref","unstructured":"Fissore, R. A., Longo, F. J., Anderson, E., Parys, J. B. and Ducibella, T. (1999). Differential distribution of inositol trisphosphate receptor isoforms in mouse oocytes. Biol. Reprod.60,49-57.","DOI":"10.1095\/biolreprod60.1.49"},{"key":"2021042611485254300_REF10","doi-asserted-by":"crossref","unstructured":"Fujiwara, A., Kamata, Y. and Yasumasu, I.(2001). Effects of Ca2+ on flavin-linked complex enzymes in mitochondria isolated from eggs and embryos of sea urchin.Dev. Growth Differ.43,213-221.","DOI":"10.1046\/j.1440-169X.2001.00559.x"},{"key":"2021042611485254300_REF11","doi-asserted-by":"crossref","unstructured":"Girard, J., Gillot, I., Renzis, G. D. and Payan, P.(1991). Calcium pools in sea urchin eggs: roles of endoplasmic reticulum mitochondria in relation to fertilization. Cell Calcium12,289-299.","DOI":"10.1016\/0143-4160(91)90003-W"},{"key":"2021042611485254300_REF12","doi-asserted-by":"crossref","unstructured":"Gunter, T., Gunter, K., Sheu, S. and Gavin, C.(1994). Mitochondrial calcium transport: physiological and pathological relevance. Am. J. Physiol.267,C313-C339.","DOI":"10.1152\/ajpcell.1994.267.2.C313"},{"key":"2021042611485254300_REF13","doi-asserted-by":"crossref","unstructured":"Hajnoczky, G., Robb-Gaspers, L., Seitz, M. B. and Thomas, A.(1995). Decoding of cytosolic calcium oscillations in the mitochondria. Cell82,415-424.","DOI":"10.1016\/0092-8674(95)90430-1"},{"key":"2021042611485254300_REF14","doi-asserted-by":"crossref","unstructured":"Hajnoczky, G., Csordas, G., Madesh, M. and Pacher, P.(2000). The machinery of local Ca2+ signalling between sarco-endoplasmic reticulum and mitochondria. J. Physiol.529,69-81.","DOI":"10.1111\/j.1469-7793.2000.00069.x"},{"key":"2021042611485254300_REF15","doi-asserted-by":"crossref","unstructured":"Hansford, R. (1994). Physiological role of mitochondrial Ca2+ transport. J. Bioenerg. Biomemb.26,495-508.","DOI":"10.1007\/BF00762734"},{"key":"2021042611485254300_REF16","doi-asserted-by":"crossref","unstructured":"He, Z., Stienen, G., Barends, J. and Ferenczi, M.(1998). Rate of phosphate release after photoliberation of adenosine 5\u2032-triphosphate in slow and fast skeletal muscle fibers.Biophys. J.75,2389-2401.","DOI":"10.1016\/S0006-3495(98)77683-0"},{"key":"2021042611485254300_REF17","doi-asserted-by":"crossref","unstructured":"Heinecke, J. and Shapiro, B. (1992). The respiratory burst oxydase of fertilization. J. Biol. Chem.267,7959-7962.","DOI":"10.1016\/S0021-9258(18)42390-3"},{"key":"2021042611485254300_REF18","unstructured":"Jones, K. (1998). Ca2+ oscillations in the activation of the egg and development of the embryo in mammals.Int. J. Dev. Biol.42,1-10."},{"key":"2021042611485254300_REF19","unstructured":"Kennedy, H., Pouli, A., Ainscow, E., Jouaville, L., Rizzuto, R. and Rutter, G. (1999). Glucose generates sub-plasma membrane ATP microdomains in single islet beta cells. Potential role for strategically located mitochondria. J. Biol. Chem.274,13281-13291."},{"key":"2021042611485254300_REF20","doi-asserted-by":"crossref","unstructured":"Land, S., Porterfield, D. and Smith, R. S.(1999). The self-referencing oxygen-selective microelectrode:detection of transmembrane oxygen flux from single cells. J. Exp. Biol.202,211-218.","DOI":"10.1242\/jeb.202.2.211"},{"key":"2021042611485254300_REF21","doi-asserted-by":"crossref","unstructured":"Landolfi, B., Curci, S., Debellis, L., Pozzan, T. and Hofer,A. (1998). Ca2+ homeostasis in the agonist-sensitive internal store: functional interactions between mitochondria and the ER measured in situ in intact cells. J. Cell Biol.142,1986-1995.","DOI":"10.1083\/jcb.142.5.1235"},{"key":"2021042611485254300_REF22","doi-asserted-by":"crossref","unstructured":"Liu, L., Hammar, K., Smith, P. J., Inoue, S. and Keefe, D. L. (2001). Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium.30,423-433.","DOI":"10.1054\/ceca.2001.0251"},{"key":"2021042611485254300_REF23","doi-asserted-by":"crossref","unstructured":"McDougall, A. and Levasseur, M. (1998). Sperm-triggered calcium oscillations during meiosis in ascidian oocytes first pause, restart, then stop: correlations with cell cycle kinase activity.Development125,4451-4459.","DOI":"10.1242\/dev.125.22.4451"},{"key":"2021042611485254300_REF24","doi-asserted-by":"crossref","unstructured":"Maes, K., Missiaen, L., Smet, P. D., Vanlingen, S., Callewaert,G., Parys, J. and Smedt, H. D. (2000). Differential modulation of inositol 1,4,5-triphosphate receptor type 1 and type 3 by ATP.Cell Calcium27,257-267.","DOI":"10.1054\/ceca.2000.0121"},{"key":"2021042611485254300_REF25","doi-asserted-by":"crossref","unstructured":"Mak, D., McBride, S. and Foskett, K. J. (1999). ATP regulation of type 1 inositol 1,4,5-trisphosphate receptor channel gating by allosteric tuning of Ca2+ activation. J. Biol. Chem.274,22231-22237.","DOI":"10.1074\/jbc.274.32.22231"},{"key":"2021042611485254300_REF26","doi-asserted-by":"crossref","unstructured":"Mak, D., McBride, S. and Foskett, K. J. (2001). ATP regulation of recombinant type 3 inositol 1,4,5-trisphosphate receptor gating. J. Gen. Physiol.117,447-456.","DOI":"10.1085\/jgp.117.5.447"},{"key":"2021042611485254300_REF27","unstructured":"Masters, B. and Chance, B. (1993). Redox confocal imaging: intrinsic fluorescent probes of cellular metabolism. InFluorescent and Luminescent Probes for Biological Activity (ed. W. Mason), pp. 44-56. London: DB Sattelle, London."},{"key":"2021042611485254300_REF28","doi-asserted-by":"crossref","unstructured":"McCormack, J. G., Halestrap, A. P. and Denton, R. M.(1990). Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev.70,391-425.","DOI":"10.1152\/physrev.1990.70.2.391"},{"key":"2021042611485254300_REF29","doi-asserted-by":"crossref","unstructured":"McDougall, A. and Levasseur, M. (1998). Sperm-triggered calcium oscillations during meiosis in ascidian oocytes first pause, restart, then stop: correlations with cell cycle kinase activity.Development125,4451-4459.","DOI":"10.1242\/dev.125.22.4451"},{"key":"2021042611485254300_REF30","doi-asserted-by":"crossref","unstructured":"McDougall, A. and Sardet, C. (1995). Function and characteristics of repetitive calcium waves associated with meiosis.Curr. Biol.5,318-328.","DOI":"10.1016\/S0960-9822(95)00062-5"},{"key":"2021042611485254300_REF31","doi-asserted-by":"crossref","unstructured":"Miyakawa, T., Maeda, A., Yamazawa, T., Hirose, K., Kurosaki, T. and Iino, M. (1999). Encoding of Ca2+ signals by differential expression of IP3 receptor subtypes. EMBO J.18,1303-1308.","DOI":"10.1093\/emboj\/18.5.1303"},{"key":"2021042611485254300_REF32","doi-asserted-by":"crossref","unstructured":"Nixon, V. L., McDougall, A. and Jones, K. T.(2000). Calcium oscillations and the cell cycle at fertilisation of mammalian and ascidian eggs. Biol. Cell,187-196.","DOI":"10.1016\/S0248-4900(00)01068-6"},{"key":"2021042611485254300_REF33","doi-asserted-by":"crossref","unstructured":"Ozil, J. and Huneau, D. (2001). Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development128,917-928.","DOI":"10.1242\/dev.128.6.917"},{"key":"2021042611485254300_REF34","doi-asserted-by":"crossref","unstructured":"Perry, G. and Epel, D. (1985). Characterization of a Ca2+-stimulated lipid peroxidizing system in the sea urchin egg. Dev. Biol.107,47-57.","DOI":"10.1016\/0012-1606(85)90374-4"},{"key":"2021042611485254300_REF35","doi-asserted-by":"crossref","unstructured":"Pralong, W. F., Spat, A. and Wollheim, C. B.(1994). Dynamic pacing of cell metabolism by intracellular calcium transients. J. Biol. Chem.269,27310-27314.","DOI":"10.1016\/S0021-9258(18)46986-4"},{"key":"2021042611485254300_REF36","doi-asserted-by":"crossref","unstructured":"Rizzuto, R., Bernardi, P. and Pozzan, T.(2000). Mitochondria as all-round players of the calcium game.J. Physiol.529.1,37-47.","DOI":"10.1111\/j.1469-7793.2000.00037.x"},{"key":"2021042611485254300_REF37","doi-asserted-by":"crossref","unstructured":"Roegiers, F., McDougall, A. and Sardet, C.(1995). The sperm entry point defines the orientation of the calcium-induced contraction wave that directs the first phase of cytoplasmic reorganization in the ascidian egg. Development121,3457-3466.","DOI":"10.1242\/dev.121.10.3457"},{"key":"2021042611485254300_REF38","doi-asserted-by":"crossref","unstructured":"Roegiers, F., Djediat, C., Dumollard, R., Rouviere, C. and Sardet, C. (1999). Phases of cytoplasmic and cortical reorganizations of the ascidian zygote between fertilization and first division. Development126,3101-3117.","DOI":"10.1242\/dev.126.14.3101"},{"key":"2021042611485254300_REF39","doi-asserted-by":"crossref","unstructured":"Runft, L. L. and Jaffe, L. F. (2000). Sperm extract injection into ascidian eggs signals Ca2+ release by the same pathway as fertilization. Development127,3227-3236","DOI":"10.1242\/dev.127.15.3227"},{"key":"2021042611485254300_REF40","doi-asserted-by":"crossref","unstructured":"Sardet, C., Roegiers, F., Dumollard, R., Rouviere, C. and McDougall, A. (1998). Calcium waves and oscillations in eggs.Biophys. Chem.72,131-140.","DOI":"10.1016\/S0301-4622(98)00129-X"},{"key":"2021042611485254300_","unstructured":"Sardet, C., Prodon, F., Dumollard, R., Chenevert, J. and Chang,P. (2002). Structure and function of the egg cortex.Dev. Biol.241,1-23."},{"key":"2021042611485254300_REF42","doi-asserted-by":"crossref","unstructured":"Schomer, B. and Epel, D. (1998). Redox changes during fertilization and maturation of marine invertebrates eggs.Dev. Biol.203,1-11.","DOI":"10.1006\/dbio.1998.9044"},{"key":"2021042611485254300_REF43","doi-asserted-by":"crossref","unstructured":"Speksnijder, J., Corson, D., Sardet, C. and Jaffe, L.(1989). Free calcium pulses following fertilization in the ascidian egg. Dev. Biol.135,182-190.","DOI":"10.1016\/0012-1606(89)90168-1"},{"key":"2021042611485254300_REF44","doi-asserted-by":"crossref","unstructured":"Stricker, S. (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals.Dev. Biol.211,157-176.","DOI":"10.1006\/dbio.1999.9340"},{"key":"2021042611485254300_REF45","unstructured":"Territo, P., Mootha, V., French, S. and Balaban, R.(2000). Calcium activation of heart mitochondrial oxidative phosphorylation: role of the F0\/F1-ATPase. Am. J. Physiol.278,C423-C435."},{"key":"2021042611485254300_REF46","doi-asserted-by":"crossref","unstructured":"Trimarchi, J., Liu, L., Porterfield, D., Smith, P. and Keefe,D. (2000). Oxydative phosphorylation-dependent and-independent oxygen consumption by individual preimplantation mouse embryos.Biol. Reprod.62,1866-1874.","DOI":"10.1095\/biolreprod62.6.1866"},{"key":"2021042611485254300_REF47","unstructured":"Warburg, O. (1908). Beobachtungen u\u0308eber die Oxydationsprozesse im Seeigelei. Hoppe-Seyler's Z. Physiol. Chem.57,1-16."},{"key":"2021042611485254300_REF48","doi-asserted-by":"crossref","unstructured":"Yang, Z. and Steele, D. S. (2000). Effect of cytosolic ATP on spontaneous and triggered Ca2+-induced Ca2+ release in permeabilised rat ventricular myocytes.J. Physiol.523,29-44.","DOI":"10.1111\/j.1469-7793.2000.00029.x"},{"key":"2021042611485254300_REF49","unstructured":"Yasumasu, I. (2000). Regulation of mitochondrial respiration in eggs and embryos of sea urchin.Zygote8 Suppl.,S3-S4."},{"key":"2021042611485254300_REF50","doi-asserted-by":"crossref","unstructured":"Yoshida, M., Sensui, N., Inoue, T., Morisawa, M. and Mikoshiba,K. (1998). Role of two series of Ca2+ oscillations in activation of ascidian eggs. Dev. Biol.203,122-133.","DOI":"10.1006\/dbio.1998.9037"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/130\/4\/683\/1499177\/683.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dev\/article-pdf\/130\/4\/683\/1499177\/683.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T18:45:24Z","timestamp":1704739524000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/130\/4\/683\/52098\/Mitochondrial-respiration-and-Ca2-waves-are-linked"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,2,15]]},"references-count":50,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2003,2,15]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.00296","relation":{},"ISSN":["1477-9129","0950-1991"],"issn-type":[{"value":"1477-9129","type":"electronic"},{"value":"0950-1991","type":"print"}],"subject":[],"published":{"date-parts":[[2003,2,15]]}}}