Seminars in Cell & Developmental Biology xxx (2006) xxx–xxx
Review
Calcium signals and mitochondria at fertilisation
Remi Dumollard
a,b,∗
, Michael Duchen
b
, Christian Sardet
a
a
Laboratoire de Biologie du D´ eveloppement, UMR 7009 CNRS/UPMC, Station Zoologique, Observatoire, 06230 Villefranche sur Mer, France
b
Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK
Abstract
At fertilisation, Ca
2+
signals activate embryonic development by stimulating metabolism, exocytosis and endocytosis, cytoskeletal remodelling,
meiotic resumption and recruitment of maternal RNAs. Mitochondria present in large number in eggs have long been thought to act as a relay
in Ca
2+
signalling at fertilisation. However, only recently have studies on ascidians and mouse proven that sperm-triggered Ca
2+
waves are
transduced into mitochondrial Ca
2+
signals that stimulate mitochondrial respiration. Mitochondrial Ca
2+
uptake can substantially buffer cytosolic
Ca
2+
concentration and the concerted action of heterogeneously distributed mitochondria in the mature egg may modulate the spatiotemporal
pattern of sperm-triggered Ca
2+
waves. Regulation of fertilisation Ca
2+
signals could also be achieved through mitochondrial ATP production
and mitochondrial oxidant activity but these hypotheses remain to be explored. A critically poised dynamic interplay between Ca
2+
signals and
mitochondrial metabolism is stimulated at fertilisation and may well determine whether the embryo can proceed further into development. The
monitoring of Ca
2+
signals and mitochondrial activity during fertilisation in living zygotes of diverse species should confirm the universality of the
role for sperm-triggered Ca
2+
waves in the activation of mitochondrial activity at fertilisation.
© 2006 Elsevier Ltd. All rights reserved.
Keywords: Fertilisation; Mitochondria; Ca
2+
oscillations; ATP; Oxidative stress
Contents
1. Introduction ............................................................................................................. 00
2. Mitochondrial biogenesis and inheritance in the oocyte ....................................................................... 00
3. Mitochondrial organisation, distribution and shapes in oocytes ................................................................ 00
4. Mitochondria take up Ca
2+
during the passage sperm-triggered Ca
2+
waves ..................................................... 00
5. Impact of sperm-triggered Ca
2+
waves on mitochondrial physiology ........................................................... 00
6. Modulation of sperm-triggered Ca
2+
waves by mitochondria .................................................................. 00
7. Perspectives ............................................................................................................. 00
Acknowledgements ....................................................................................................... 00
References .............................................................................................................. 00
Abbreviations: [Ca
2+
]
cyto
, cytosolic Ca
2+
concentration; [Ca
2+
]
mito
, mito-
chondrial Ca
2+
concentration; ATP, adenosine trisphosphate; ROS, reactive
oxygen species; mtDNA, mitochondrial DNA; GV, germinal vesicle; ER, endo-
plasmic reticulum; IP3, inositol 3,4,5 trisphosphate; IICR, IP3-induced Ca
2+
release; FCCP, carbonyl cyanide 4-(trifluoromethoxy)phenylhydrazone; PM1,
pacemaker 1; PM2, pacemaker 2; SERCA, sarco-endoplasmic Ca
2+
ATPase;
PMCA, plasma membrane Ca
2+
ATPase; GFP, green fluorescent protein; O
2
,
oxygen; O
2
-
, superoxide; H
2
O
2
, hydrogen peroxide; CN
-
, cyanide
∗
Corresponding author.
E-mail address: remi.dumollard@obs-vlfr.fr (R. Dumollard).
1. Introduction
Mitochondria were first described in 1890 as “bioblasts: a
cytoplasmic structure of ubiquitous occurrence, resembling bac-
teria and functioning as elementary organisms” [1]. Much later,
this idea was confirmed by the discovery that mitochondria pos-
sess their own DNA, a unique nucleic acid coding sequence
system and that they can replicate independently of the nuclear
cell cycle. Mitochondria contain the enzymes of the citric cycle,
fatty acid oxidation and oxidative phosphorylation making them
the major site for production of ATP in eukaryotic cells [1].
1084-9521/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.semcdb.2006.02.009
YSCDB-584; No. of Pages 10