Swathi Arur Editor From Oogenesis to Oocyte-to-Embryo Development

296 Pages·2017·5.88 MB·English

Results and Problems in Cell Diff erentiation 59
Swathi Arur Editor
Signaling-
Mediated
Control of Cell
Division
From Oogenesis to Oocyte-to-Embryo
Development
Results and Problems in Cell Differentiation
Volume 59
Series editors
JacekZ.Kubiak,RennesCX,France
MalgorzataKloc,Houston,TX,USA
More information about this series at http://www.springer.com/series/400
Swathi Arur
Editor
Signaling-Mediated Control
of Cell Division
From Oogenesis to Oocyte-to-Embryo
Development
Editor
SwathiArur
Dept.ofGenetics,Genes&Dev.Program
UTMDAndersonCancerCenter
Houston,Texas
USA
ISSN0080-1844 ISSN1861-0412 (electronic)
ResultsandProblemsinCellDifferentiation
ISBN978-3-319-44819-0 ISBN978-3-319-44820-6 (eBook)
DOI10.1007/978-3-319-44820-6
LibraryofCongressControlNumber:2016961937
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Preface
Germcellssustainlifethroughgenerations.Germcellsaresetasidefromsomatic
cellsintheembryoandgothroughthespecializedcelldivisionprocessofmeiosis
toproducethegametes—theoocyteorthesperm.Theprocesswherebygermcells
developintogametesisgovernedviaseveraldevelopmental,nutritional,andother
environmental cues or signals. Unsurprisingly, due to a variety of causes, some-
times these signals are spatially and/or temporally anomalous during organismal
development, and such anomalies can manifest as birth defects in the progeny.
Thus, elucidating how a multitude of molecular mediators integrate the various
developmentalandenvironmentalsignalstocoordinategermcellformation,main-
tenance,andfunctionremainsanactiveareaofinvestigation.
Inbothinvertebrateandvertebrateanimals,environmentallyactivatedsignaling
pathwaysregulateproductionofgameteswithnutritionalavailability.Muchwork
has focused on understanding the mechanisms that regulate oocyte fitness and
quality in humans and other vertebrate model organisms such as mice. However,
in the mammalian female, germ cells enter and arrest in meiosis I during fetal
development, and initiation of meiosis II—ovulation—occurs after birth and only
when the progeny attains sexual maturity. In contrast, the invertebrate female
germlinestemcellsproduceoocytescontinuouslythroughoutdevelopment.There-
fore, understanding the cellular and molecular mechanisms that govern germline
stem cell populations and meiosis I is relatively more tractable using invertebrate
model organisms such as Caenorhabditis elegans and Drosophila melanogaster.
Together,studiesusingbothvertebrateandinvertebratesarebeginningtoprovide
insightsintothemechanismsthatensureoocytequalityandminimizeerrorsduring
meiosisandmeioticmaturation.Inthisvolume,expertsworkingondiversemodel
organismscometogethertodiscussthestate-of-the-artknowledgebaseontherole
of signaling pathways in regulating germline stem cell biology and meiotic pro-
gression of oocytes until fertilization and birth and identify exciting new avenues
andquestionsforfutureresearch.
WebeginwithadescriptionofepigeneticmechanismsthatregulateDrosophila
germline stem cell gene expression. Rangan and coauthors elaborate the role of
v
vi Preface
several histone variants and nucleosome remodeling complexes in maintaining
germline stem cells. They further provide insights into the interplay between
epigenetic and signaling mechanisms that drive differentiation into the meiotic
program.
The decision of a stem cell to differentiate or self-renew is of fundamental
importancetoorganismaldevelopmentandtissuemaintenance.SinghandHansen
discuss the signaling circuitry, including feedback loops between differentiated
cellsandstemcells,whichenablesagermlinestemcelltomaintainafinebalance
betweenself-renewal(enoughtomaintainapoolofstemcells)anddifferentiation
(tomaintainoocytenumbers).Theyalsodiscussthesimilaritiesanduniqueaspects
ofstemcellrenewalanddifferentiationinworms,flies,andmalemice.
Oocytequalityisinfluencedsignificantlybynutritionalandotherenvironmental
cuesorsignals.
Laws and Drummond-Barbosa elaborate on the strong influence of diet and
physiology on reproductive fitness. The authors critically review in vivo studies
in model organisms (worms, flies, and mice) and discuss how diet-dependent
signals can control the proliferation of germline stem cells and their maintenance
andsubsequentmeioticprogressionandproductionofoocytes.
I then provide a mechanistic view on how nutrition-induced signals regulate
oogenic meiosis I progression via the ERK/MAPK pathway in C. elegans and
signalingandsecondmessengerpathwaysthatregulateoocytemeioticmaturation
in C. elegans, Drosophila and mammals. Through detailed discussions of several
evolutionarily conserved signaling pathways, I synthesize common themes in the
regulationofkeymeioticeventsduringoocytegrowthandmaturation.
Meiosis-specific processes such as chromosomal pairing and recombination
generate diversity in a species. Failure in the coordinated regulation of these
meiotic processes also results in aneuploidy in the progeny. Smolikove and col-
leaguesexaminetheinterplayofsignalingwithmeiosisIthatiscriticalfornormal
oocyte development. They also examine the role of increasing maternal age on
oocytequality.
Oocytegrowth,development,andmaturationoccurunderamolecularenviron-
ment of transcriptional quiescence. Transcription is not reinitiated until embryo-
genesis. Thus, posttranscriptional and translational mechanisms are critical to
normaloocytedevelopment.Subramaniamandcolleaguesdiscussthetranslational
and posttranslational mechanisms that control the decision of stem cells to enter
meiosis,oocytedevelopment,andmaturation.
Mammalian oocytes undergo meiotic arrest intwo phases: meiotic Iarrest and
meiotic II arrest. The second meiotic arrest is coordinated with embryo develop-
ment by the activity of the cell division protein Cdc6. Kubiak and colleagues
discuss mechanisms utilized by Cdc6 to exquisitely coordinate DNA replication
after meiotic II arrest with that in the embryo. Yeste and colleagues weave in the
importance of sperm- and oocyte-derived factors that regulate meiosis II comple-
tion—after resumption from the meiotic II arrest—and prevent polyspermy,
thereby ensuring a normal zygote. They discuss the role of lipid signaling in
these processes and contemplate the impact of artificial oocyte activating factors
Preface vii
inclinicalsettingsdedicatedtohelpinghumanswithoocyteactivationdeficiency.
Theyalsodiscussoptionsforbetterandmoreendogenousalternativestoartificial
oocyteactivatingfactors.
HoangandMillerfocusonthespecificmechanismsthatenablespermguidance
in the female reproductive tract. They examine the role of pheromones and nutri-
tionalsignalsthataffectthespermguidancemachineryandimpactspermmotility
and fertility and discuss implications to human reproduction and oncologic
treatments.
Fassnacht and Ciosk analyze our current understanding on the critical
reprogrammingmechanismsthatunderlietheprogression ofanoocytetoasingle
totipotent embryo. They highlight the role of developmental reprogramming with
implicationstovariedaspectsofhumandevelopmentandregenerativemedicine.
The authors synthesize information derived from various different model sys-
temstoprovidecriticalinsightsintotheprogressionoffemalegermlinestemcells
throughmeioticmaturationanddevelopmentofahealthyembryo,highlightingthe
impact on human health. Additionally, we discuss the critical gaps in knowledge
and questions that remain to be addressed, understanding of which will influence
humanreproduction,development,andregenerativemedicine.
Houston,TX SwathiArur
2016
Contents
1 RoleofChromatinModificationsinDrosophilaGermlineStem
CellDifferentiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
PoojaFlora,AliciaMcCarthy,MaitreyiUpadhyay,
andPrashanthRangan
2 RegulationoftheBalanceBetweenProliferation
andDifferentiationinGermLineStemCells. . . . . . . . . . . . . . . . . 31
RamyaSinghandDaveHansen
3 ControlofGermlineStemCellLineagesbyDietandPhysiology. . . 67
KaitlinM.LawsandDanielaDrummond-Barbosa
4 Signaling-MediatedRegulationofMeioticProphaseI
andTransitionDuringOogenesis. . . . . . . . . . . . . . . . . . . . . . . . . . 101
SwathiArur
5 ProphaseI:PreparingChromosomesforSegregation
intheDevelopingOocyte. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
RachelReichman,BenjaminAlleva,andSaritSmolikove
6 TranslationalControlofGermCellDecisions. . . . . . . . . . . . . . . . 175
KumariPushpa,GangaAnilKumar,andKuppuswamySubramaniam
7 RoleofCdc6DuringOogenesisandEarlyEmbryoDevelopment
inMouseandXenopuslaevis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
EwaBorsuk,JoannaJachowicz,MalgorzataKloc,Jean-PierreTassan,
andJacekZ.Kubiak
8 OocyteActivationandFertilisation:CrucialContributors
fromtheSpermandOocyte. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213
MarcYeste,CelineJones,SitiNornadhirahAmdani,
andKevinCoward
9 SpermNavigationMechanismsintheFemaleReproductiveTract. . . 241
HieuD.HoangandMichaelA.Miller
ix
x Contents
10 CellFateMaintenanceandReprogrammingDuring
theOocyte-to-EmbryoTransition. . . . . . . . . . . . . . . . . . . . . . . . . . 269
ChristinaFassnachtandRafalCiosk
Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287