Table Of ContentOogenesis
Oogenesis: The Universal Process Edited by Marie-Hélène Verlhac and Anne Villeneuve
© 2010 John Wiley & Sons Ltd. ISBN: 978-0-470-69682-8
Oogenesis: The Universal Process
Editors
(cid:1) (cid:3)
Marie-Helene Verlhac
CNRS/Universite´Pierre et Marie Curie, Paris, France
and
Anne Villeneuve
Stanford University School of Medicine, Stanford, CA, USA
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LibraryofCongressCataloguing-in-PublicationData
Oogenesis:theuniversalprocess/[editedby]Marie-He´le`neVerlhacandAnne
Villeneuve.
p.cm.
Includesindex.
ISBN978-0-470-69682-8
1.Oogenesis.I.Verlhac,Marie-He´le`ne.II.Villeneuve,Anne.
QL965.O6562010
571.8045–dc22
2009051040
ISBN:978-0-470-69682-8
AcataloguerecordforthisbookisavailablefromtheBritishLibrary.
Setin10.5/12.5TimesbyThomsonDigital,Noida,India.
PrintedinGreatBritainbyAntonyRoweLtd,Chippenham,Wiltshire.
FirstImpression 2010
Contents
List of Contributors vii
Foreword TimHunt xi
Section I: Oocyte Determination 1
Chapter1:TheSperm/OocyteDecision,aC.elegansPerspective 3
RonaldEllis
Chapter2:SexDeterminationandGonadalDevelopment 27
AlexanderCombes,CassySpillerandPeterKoopman
Chapter3:Clytiahemisphaerica:ACnidarianModelforStudyingOogenesis 81
AldineAmiel,PatrickChang,TsuyoshiMomoseandEvelynHouliston
Section II: Oocyte Growth 103
Chapter4:Soma–GermlineInteractionsintheOvary:anEvolutionary
Perspective 105
DavidAlbertiniandJohnBromfield
Section III: Homologous Chromosome Pairing and Recombination 115
Chapter5:HomologousChromosomePairingandSynapsisduringOogenesis 117
SusannaMlynarczyk-EvansandAnneVilleneuve
Chapter6:MeioticRecombinationinMammals 141
SabineSantucci-DarmaninandFre´de´ricBaudat
Section IV: Meiosis Resumption 179
Chapter7:InitiationoftheMeioticProphase-to-MetaphaseTransition
inMammalianOocytes 181
LaurindaA.JaffeandRachaelP.Norris
Chapter8:Oocyte-SpecificTranslationalControlMechanisms 199
IsabelNovoa,CarolinaEliscovich,Eula`liaBellocandRau´lMe´ndez
Chapter9:MPFandtheControlofMeioticDivisions:OldProblems,
NewConcepts 227
CatherineJessus
Section V: The Cytological Events of Meiotic Divisions 267
Chapter10:MeioticSpindleAssemblyandChromosomeSegregationinOocytes 269
JulienDumontandSte´phaneBrunet
vi CONTENTS
Chapter11:MechanismsofAsymmetricDivisioninMetazoanMeiosis 291
Marie-He´le`neVerlhacandKarenWingmanLee
Section VI: Biological Clocks Regulating Meiotic Divisions 311
Chapter12:TheControloftheMetaphase-to-AnaphaseTransitioninMeiosisI 313
M.EmilieTerret
Chapter13:MechanismsControllingMaintenanceandExitoftheCSFArrest 343
ThierryLorcaandAnnaCastro
Chapter14:CytostaticArrest:Post-ovulationArrestUntilFertilization
inMetazoanOocytes 357
TomokoNishiyama,KazunoriTachibanaandTakeoKishimoto
Section VII: Oocyte Ageing in Mammals 385
Chapter15:MammalianOocytePopulationthroughoutLife 387
RogerGosden,EujinKim,BoraLee,KatiaManovaandMalcolmFaddy
Section VIII: From Oocyte to Embryo 403
Chapter16:FertilizationandtheEvolutionofAnimalGameteProteins 405
JulianL.WongandGaryM.Wessel
Chapter17:RemodellingtheOocyteintoaTotipotentZygote:Degradation
ofMaternalProducts 423
Jose´-EduardoGomes,JorgeMerlet,JulienBurgerandLionelPintard
Chapter18:ChromatinRemodellinginMammalianOocytes 447
RabindranathDeLaFuente,ClaudiaBaumann,FeikunYangandMariaM.Viveiros
Chapter19:FolliclesandMedicallyAssistedReproduction 479
SusanL.BarrettandTeresaK.Woodruff
Index 490
List of contributors
David Albertini, Department of Molecular and Integrative Physiology and
Department of Anatomy and Cell Biology, University of Kansas Cancer Centre,
Kansas City, KS 66160, USA; Marine Biological Laboratory, Woods Hole, MA
02543, USA
Aldine Amiel, UMR 7009, UPMC-CNRS, Developmental Biology Unit, Observa-
toire Oce´anologique, 06230 Villefranche sur mer, France
Susan L. Barrett, Department of Obstetrics and Gynecology, Feinberg School of
MedicineandCenterforReproductiveScience,NorthwesternUniversity,Evanston,
IL 60208 USA; The Oncofertility Consortium, Chicago, IL 60611, USA
Fre´de´ric Baudat, CNRS UPR 1142,Institutde Ge´ne´tique Humaine, 141 rue de la
Cardonille, 34396 Montpellier CEDEX 5, France
ClaudiaBaumann, DepartmentofClinicalStudies,CenterforAnimalTransgenesis
andGermCellResearch,NewBoltonCenter,UniversityofPennsylvania,Schoolof
Veterinary Medicine, 382 West Street Road, Kennett Square, PA 19348 USA
Eula`liaBelloc, GeneRegulationProgram,Centre forGenomicRegulation(CRG),
C/Dr Aiguader, 88, 08003, Barcelona, Spain
JohnBromfield, DepartmentofMolecularandIntegrativePhysiology,Universityof
Kansas Cancer Centre, Kansas City KS 66160, USA
Ste´phaneBrunet, BiologieduDe´veloppement–UMR7622,UPMC-CNRS,9Quai
St Bernard, 75252 Paris CEDEX 05, France
JulienBurger, InstitutJacquesMonod,CNRSandUniversite´ParisDiderot,Buffon
Building, 15 rue He´le`ne Brion, 75205 Paris CEDEX 13, France
AnnaCastro, CNRSUMR5237,IFR122,Universite´sMontpellier2et1,Centrede
Recherche de Biochimie Macromole´culaire, 1919 Route de Mende, 34293
Montpellier CEDEX 5, France
Patrick Chang, UMR 7009, UPMC-CNRS, Developmental Biology Unit, Obser-
vatoire Oce´anologique, 06230 Villefranche sur mer, France
Alexander Combes, Institute for Molecular Biosciences, The University of
Queensland, Brisbane, QLD 4072, Australia
viii LISTOFCONTRIBUTORS
Rabindranath De La Fuente, Department of Clinical Studies, Center for Animal
Transgenesis and Germ Cell Research, New Bolton Center, University of
Pennsylvania,SchoolofVeterinaryMedicine,382WestStreetRoad,KennettSquare
PA 19348, USA
JulienDumont, DesaiLaboratory,DepartmentofCellularandMolecularMedecine,
LudwigInstituteforCancerResearch,UniversityofCalifornia,9500GilmanDrive,
La Jolla, CA 92093-0660, USA
Carolina Eliscovich, Gene Regulation Program, Centre for Genomic Regulation
(CRG), C/Dr Aiguader, 88, 08003, Barcelona, Spain
Ronald Ellis, Department of Molecular Biology, School of Osteopathic Medicine,
B303 Science Center, The University of Medicine and Dentistry of New Jersey, 2
Medical Center Drive, Stratford NJ 08084, USA
Malcolm Faddy, School of Mathematical Sciences, Queensland University of
Technology, Brisbane, QLD 4001, Australia
Jose´-EduardoGomes, InstitutJacquesMonod,CNRSandUniversite´ParisDiderot,
Buffon Building, 15 rue He´le`ne Brion, 75205 Paris CEDEX 13, France
Roger Gosden, Weill Medical College of Cornell University, 1305 York Avenue,
New York, NY 10021, USA
Evelyn Houliston, UMR 7009, UPMC-CNRS, Developmental Biology Unit,
Observatoire Oce´anologique, 06230 Villefranche sur mer, France
TimHunt, CancerResearchUK,ClareHallLaboratories,SouthMimms,Herts,UK
LaurindaA.Jaffe, DepartmentofCellBiology,L-5004,UniversityofConnecticut
Health Center, 263 Farmington Avenue, Farmington, CT 06032, USA
CatherineJessus, BiologieduDe´veloppement–UMR7622,UPMC-CNRS,9Quai
St Bernard, 75252 Paris CEDEX 05, France
Eujin Kim, Weill Medical College of Cornell University, 1305 York Avenue,
New York, NY 10021, USA
TakeoKishimoto, GraduateSchoolofBioscienceandBiotechnology,Laboratoryof
Cell and Developmental Biology, Tokyo Institute of Technology, Nagatsuta 4259,
Midoriku, Yokohama 226-8501, Japan
PeterKoopman, InstituteforMolecularBiosciencesandARCCentreofExcellence
inBiotechnologyandDevelopment,TheUniversityofQueensland,Brisbane,QLD
4072, Australia
Bora Lee, Weill Medical College of Cornell University 1305 York Avenue,
New York, NY 10021, USA
ThierryLorca, CNRSUMR5237,IFR122,Universite´sMontpellier2et1,Centrede
Recherche de Biochimie Macromole´culaire, 1919 Route de Mende, 34293
Montpellier CEDEX 5, France
LISTOFCONTRIBUTORS ix
Katia Manova, Memorial Sloan-Kettering Cancer Center, New York, NY 10065,
USA
Rau´l Me´ndez, Gene Regulation Program, Centre for Genomic Regulation (CRG),
C/Dr Aiguader, 88, 08003, Barcelona, Spain
Jorge Merlet, Institut Jacques Monod,CNRS and Universite´ Paris Diderot Buffon
Building, 15 rue He´le`ne Brion, 75205 Paris CEDEX 13, France
Susanna Mlynarczyk-Evans, Department of Developmental Biology, Stanford
University School of Medicine, Beckman Center, B300, 279 Campus Drive,
Stanford CA 94305-5329, USA
Tsuyoshi Momose, UMR 7009, UPMC-CNRS, Developmental Biology Unit,
Observatoire Oce´anologique, 06230 Villefranche sur mer, France
Tomoko Nishiyama, Institute of Molecular Pathology, Dr. Bohr-Gasse 7, 1030
Vienna, Austria
RachaelP.Norris, DepartmentofCellBiology,L-5004,UniversityofConnecticut
Health Center, 263 Farmington Avenue, Farmington CT 06032, USA
Isabel Novoa, Gene Regulation Program, Centre for Genomic Regulation (CRG),
C/Dr Aiguader, 88, 08003, Barcelona, Spain
LionelPintard, InstitutJacquesMonod,CNRSandUniversite´ParisDiderot, Buffon
Building, 15 rue He´le`ne Brion, 75205 Paris CEDEX 13, France
SabineSantucci-Darmanin, FRE3086,CNRS,Faculte´deMe´decine,Universite´de
Nice Sophia-Antipolis, Avenue de Valombrose, 06107 Nice CEDEX 2,
France
Cassy Spiller, Institute for Molecular Biosciences, The University of Queensland
andARCCentreofExcellenceinBiotechnologyandDevelopment,Brisbane QLD
4072, Australia
Kazunori Tachibana, Graduate School of Bioscience and Biotechnology, Labora-
toryofCellandDevelopmentalBiology,TokyoInstituteofTechnology,Nagatsuta
4259, Midoriku, Yokohama 226-8501, Japan
M. Emilie Terret, Molecular Biology Program, Memorial Sloan-Kettering Cancer
Center, Box # 97, 1275 York Avenue, New York, NY 10021, USA
Marie-He´le`neVerlhac, BiologieduDe´veloppement–UMR7622,UPMC-CNRS,
9 Quai St Bernard, 75252 Paris CEDEX 05, France
Anne Villeneuve, Department of Developmental Biology, Stanford University
School of Medicine, Beckman Center, B300, 279 Campus Drive, Stanford, CA
94305-5329, USA
MariaM.Viveiros, DepartmentofAnimalBiology,CenterforAnimalTransgenesis
andGermCellResearch,NewBoltonCenterUniversityofPennsylvania,Schoolof
Veterinary Medicine, 382 West Street Road, Kennett Square, PA 19348, USA
x LISTOFCONTRIBUTORS
GaryM.Wessel, DepartmentofMolecularBiology,CellBiology,andBiochemistry,
Brown University, Box G-L173, 185 Meeting Street, Providence RI 02912, USA
Karen Wingman Lee, Biologie du De´veloppement – UMR 7622, UPMC-CNRS
9 Quai St Bernard, 75252 Paris CEDEX 05, France
JulianL.Wong, DepartmentofMolecularBiology,CellBiology,andBiochemistry,
Brown University, Providence, RI 02912, USA
TeresaK.Woodruff, DepartmentofObstetricsandGynecologyFeinbergSchoolof
MedicineNorthwesternUniversityand TheOncofertilityConsortium,ChicagoIL
60611,USA;CenterforReproductiveScience,NorthwesternUniversity,Evanston
IL 60208, USA
FeikunYang, DepartmentofClinicalStudies,CenterforAnimalTransgenesisand
Germ Cell Research, New Bolton Center, University of Pennsylvania, School of
Veterinary Medicine, 382 West Street Road, Kennett Square, PA 19348, USA
Foreword
August Weissman dedicated his book, ‘The Germ-Plasm’ (1892) to the memory of
CharlesDarwin.Weissmanunderstoodtheurgentneedforapropertheoryofheredity,
knew that Darwin’s ideas on the subject were inadequate, and equally clearly recog-
nizedthat,unlike“theperishablebodyoftheindividual”something—the“hereditary
substance”—had to be passed from generation to generation in eggs and sperm and
hence,“thecontinuityofthegerm-plasm”.Ittookanother10–15yearsbeforeThomas
HuntMorganacceptedthatthebehaviourofchromosomesexplainedMendel’slaws(of
whichWeissmanwasunaware;indeed,neither‘chromosomes’nor‘nucleus’featurein
theindexofhisbook),andonemightsaythatittookthestructureofDNA,andtheidea
that“DNAmakesRNAmakesprotein”tobringbiologyintothemodernera.Wedon’t
thinktwice,thesedays,aboutthecontinuityoflifeonearth,andacceptwithoutquestion
thatcellsonlyarisefrompre-existingcells;thisisallsointegraltothebiologist’sworld
viewthatanumberofgreatmysterieshardlyevercometolight.Broadlyspeaking,these
underliethetopicofthiscollectionofessaysaboutoogenesis.Howdoesthegerm-plasm
manage to avoid the body’s mortality?
Quiteapartfromdeepquestionsofthiskind,thedetailsofhoweggscometobeeggs
arefascinatingandinstructivewellbeyondtherelativelynarrowfieldofreproductive
biology.Likewisetheeventsjustbeforeandafterfertilization,whentheeggmeetsthe
sperm and starts to become a new body. This book contains a series of essays,
authoritative and fascinating reviews of all aspects of oogenesis.
Thereviewsfollowakindofchronologicalordevelopmentalorderfromquestions
about sex determination in worms to assisted reproduction in humans. The simple-
soundingdecisionofwhatsextobecomeisanythingbut,andweareremindedthatitis
quitepossibletobeahermaphroditeandsurviveperfectlysuccessfully.Wediscussthe
setting-aside of germ cells from the soma early in development as well as the
surprisingly complicated decision-makingprocesses that lead to the differentation of
eggsorsperm.Meiosisisanecessarycommonprocessforbothkindsofgamete,andwe
have reviews of what is known about meiotic chromosome pairing and homologous
recombination.Inoocytes,themeioticdivisionsoftentakeplaceshortlybeforethecell
becomesafully-fledged,fertilizableegg,andissubjecttosomeelaboratecontrolsthat
are still far from completely understood.
The choice between becoming an egg or a sperm is one of the most complex of
development,anditismadelongbeforechangesincellmorphologytakeplace.This
fate decision depends on sex chromosomes and depends on interactions between
gonadalsomaticcelllineagesandthegermcellsthemselves.Indeed,metazoanshave
evolvedacomplexarrayofinteractionsbetweenthesomaandgermlinethatregulate
reproductive success. During the growth period of oogenesis, meiotically-arrested
