Genome Organization And Function In The Cell Nucleus

183 Pages·2012·10.779 MB·English

by  Karsten Rippe

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15.4 ConcludingsRemark 383
andH4K20hasbeendetectedduringthenextG1phase[189].Thissuggeststhat
restoration of global levels of these histone modi(cid:147)cations would occur mostly
justpriortothenextS-phase,whichcouldberegardedagainasananticipationof
the dilution event occurring during replication. Thus, our understanding of the
transmission of chromatin-based information in a replication-independent man-
ner concerning the histone H3 variants and speci(cid:147)c PTMs represents a general
themethatmayalsohelpustounderstandthefateofothermarks,likeassociation
ofnuclearRNA,Polycomb proteins,orotherchromatinproteins.
15.4
ConcludingRemarks
In eukaryotic cells, chromatin duplication entails a series of complex and coor-
dinated events. These include nucleosomal disruption, histone transfer, and
deposition,alongwithdynamichistonemodi(cid:147)cationsthatoccurinamannerthat
maintainsparticularmarksatde(cid:147)nedchromatinregions.Here,weemphasizethe
possiblerolesofchromatinremodelers,histonemodi(cid:147)ersandhistonechaperones
in chromatin duplication. These are discussed both at the level of histone
dynamicsandinthecontextofreestablishingmarksthatde(cid:147)nedistinctchromatin
states.Itshouldbenotedthatreplicationhasalsobeenconsideredasawindowof
opportunity important to induce changes in chromatin states [190]. In addition,
non-replicative chromatin dynamics can also promote the maintenance of parti-
cularmarks,asexempli(cid:147)edwiththecaseofthehistonevariantsH3.3andCENP-
A.Theassociated keyplayers inhistone dynamics andmodi(cid:147)cations(chromatin
remodelers, histone modi(cid:147)ers, histone chaperones) seem to be involved in other
DNA metabolic processes such as DNA repair (Chapter 16) and transcription
(Chapter10).Thus,itwillbeimportanttodeterminehowtheyaredirectedtoone
task or another. A better understanding of the (cid:147)ne-tuning of this system and its
network of partners will not only improve our basic knowledge of chromatin
duplication but will be informative with respect to functional conservation
betweenspeciesofkeyplayerssuchasINO80orAsf1.Furthermore,itwillhelpus
togaininsightinthepathologicalcasessuchasdevelopmentaldiseasesaswellas
cancer,inwhichthenetworkdisplaysaberrantactivities.
Acknowledgments
Weapologizetoauthorswhoseworkhasnotbeencitedowingtolimitedspace.We
thank A. Cook for input and D. Ray-Gallet for critical reading of the manuscript
and for providing Figure 15.2. This work was supported by la Ligue Nationale
contre le Cancer (Equipe labellis (cid:2)ee Ligue 2010), PIC Programs, the European
Commission Network of Excellence Epigenome ( LSHG-CT-2004-503433), the
European Commission ITN FP7-PEOPLE-2007 (cid:141)Image DDR(cid:142) and FP7-PEOPLE-
2008 (cid:141)Nucleosome 4D,(cid:142) ACI-2007-Canc (cid:2)eropo (cid:26) le IdF (cid:141)Breast cancer and Epige-
netics(cid:142),ANR(cid:141)ECenS(cid:142) ANR-09-BLAN-0257-01,INCa(cid:141)GepiG,(cid:142)andERCAdvanced
c15 29August2011;14:21:1
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382 15 DNAReplicationandInheritanceofticEpigeneStates
S-phase. This is consistent with the fact that replacement variant H3.3 accumu-
latesinactivelytranscribedchromatinregions,as(cid:147)rstshownin Drosophila [168],
and within chromatin enriched in (cid:141)active(cid:142) marks when compared to replicative
variants[99,169,170].HistoneH3.3accumulationatpromotersofactivegenesor
at regulatory elements could exploit a replication-independent mechanism invol-
vingthehistonechaperoneHIRA[57,171(cid:133)173].Whilethedilutionofactivemarks
on parental histones occurs during replication, the amount provided may be
suf(cid:147)cienttomaintainapermissivestatefortranscription,whichinturnwouldadd
more active marks. The presence of some H3.3 along with active marks would
thus act as a seeding event. According to this view, the memory of an active
transcriptional state could thus involve both the choice of the H3.3 variant com-
binedwithanactivemarksuchasH3K4methylation[174,175].However,H3.3is
notcon(cid:147)nedtositesofactivetranscriptionbutcanbeenrichedinothergenomic
regionsdependingonthedevelopmentalcontext.Thisisillustratedatthetimeof
fertilization with a massive and global accumulation of H3.3 onto sperm DNA
[176] and in ES cells with the detection of H3.3 accumulation at telomeres [177,
178].Howtheseeventsarecontrolledandwhichfactorsareinvolvedisbeginning
tobeunravelled(forareview,see[179]).Itisamazingthoughtobearinmindthat
H3.1,H3.2,andH3.3showverylittlesequencedifference;thushowspeci(cid:147)cityin
theirdeposition isachievedremainsafascinatingunresolvedissue.
Incontrast,CENP-A,alsocalleddeviantH3[180],ishighlydivergent.Itprovides
thebestexampleofahistoneH3variantthatspeci(cid:147)esafunctionalgenomelocus:
the site of centromere identity [181], which serves as a platform for kinetochore
assembly [182]. During replication of centromeric chromatin, CENP-A nucleo-
somesbecomedilutedtohalftheinitialconcentrationondaughterchromatin[29,
183]. It is not until the next G1 phase that new CENP-A gets incorporated again
[183, 184]. This case illustrates a situation in which the disruption during repli-
cationisclearlyseparatedfromthereassemblyeventoutsideS-phase.Withrespect
to theassociated mechanism, the identi(cid:147)cation of the Holliday junction recogni-
tionprotein(HJURP)isparticularlyenlightening.HJURPisaCENP-Achaperone
(localizedatcentromerespreciselyfromlatetelophasetoearlyG1)thatpromotes
the speci(cid:147)c targeting/incorporation and maintenance of CENP-A at centromeres
[185,186].Sofarwehaveconsideredthesituationfromthepointofviewofhowto
restore the initial chromatin state after a disruptive event such as replication.
However,thefollowingalternativeconsiderationisequallyvalid:incorporationof
CENP-AinG1maybeprogrammedinanticipationofthedisruptiveeventduring
replication,ratherthanbeingarestorationofhalfthepoolofCENP-A.Whichever
way one looks at this issue, it provides a general conceptual framework for the
mechanism by which chromatin marks can be dealt with during the cell cycle.
Thus,itisinformativetoconsiderhowandwhenhistonemarks,stablymarking
particular domains, are actually imposed given that parental nucleosomes
experience the disruption due to passage of the replication fork. Late steps in
chromatinrestorationmayawaitreinitiationoftranscriptionondaughterstrands
as recently proposed for H3K9me2 at heterochromatic repeats in -Schizosacchar
omycespombe [187,188].Similarly,inhumancells,di-ortrimethylationofH3K27
c15 29August2011;14:21:1
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15.3 ceMaintenanofEpigeneticMarksandslationalPost-tranModi(cid:147)cations 381
marksasinpericentricheterochromatinwhereH3K9me3isboundbyHP1proteins
[136, 137]. However, it cannot apply to regions in which particular marks are
restrictedtoonlyoneortwonucleosomes.Intheseregions,thesplittingoftetra-
mersasrecentlyobservedwithH3.3variants[67]wouldleadtothetransmissionof
histone marks through an intra-particle mechanism. With respect to facultative
heterochromatin regions, the process proposed for maintaining the H3K27me3
histone modi(cid:147)cation through cell division resembles the one put forward for
H3K9me3[160,161].Here,polycombrepressivecomplex2(PRC2),theveryenzyme
thatcatalyzesthismodi(cid:147)cation,directlybindstoH3K27me3.Accordingly,itcould
copy this methylation mark onto neighboring newly incorporated histones [160,
161].Polycombrepressivecomplex1(PRC1),whichremainsassociatedwithDNA
duringreplication invitro ,couldalsopotentiallyparticipateinthemaintenanceof
transcriptionalsilentstatesthroughcelldivision[162].However,itremainstobe
elucidatedwhetherPRC1remainsindirectcontactwithDNAduringDNArepli-
cationorwhetheritstransferinvolvescomponentofthereplicationmachinery.
Recent studies provide a (cid:147)rst glimpse of how H4K20 methylation could be
maintained duringDNAreplication. Several groupshave shown that Pr-Set7, an
H4K20histonemonomethyltransferasealsoknownasSet8(KMT5A),isrequired
for the progression through S-phase and is found at replication sites [163(cid:133)165].
Targeting to replication forks could exploit a direct interaction with PCNA via a
PCNA-interactingproteinbox((cid:141)PIPbox(cid:142))initsN-terminus[163,164].However,
thereportedlowlevelsofPr-Set7duringS-phasechallengethisview[166].Thus,it
needs to be further investigated whether Pr-Set7 reproduce H4K20 mono-
methylation patterns on daughter strands via its interaction with PCNA. Never-
theless,theessentialroleofPr-Set7formousedevelopment[163,166]associated
with its functions in cell division and genome stability [164, 165] points to an
importantfunctionofthisenzyme.
15.3.3
InheritanceofHistoneVariantsandPTMsOutsideReplication?
AnticipationorRestoration?
Given that histone variants can mark particular chromatin states, a challenging
question is to understand how this marking pass through replication, and if
maintenanceisensuredoverthecellcycle,howthisisachieved.Here,weillustrate
thispointforH3variantstoderivegeneralprinciplesthatcanpotentiallyapplyto
otherchromatinmarks.WhenconsideringthereplicativehistonevariantsH3.1or
H3.2 mainly deposited during replication, a genome-wide distribution could be
expected.Ofnote,however,isthefactthatincorporationofH3.1outsideS-phase
atsitesofUVdamage[167]canmarkasiteofexperienceddamageasascar.This
mayprovideamemoryofdamagesincenewlysynthesizedhistonescarrydifferent
PTMsthantheoriginalones.Furthermore,oligonucleosomescontainingH3.1are
moreprominentlyassociatedwithHP1 a andMBD1,suggestinganenrichmentof
H3.1 in constitutive pericentric heterochromatin [99]. These domains of con-
centrationscouldre(cid:148)ectadefaultstate,ifnoothervariantisincorporatedoutside
c15 29August2011;14:21:1
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384 15 DNAReplicationandInheritanceofticEpigeneStates
Grant 2009-AdG_20090506.A.C.wasfundedbyUniversityPierreetMarieCurie
(UPMC)andbyAssociationpourlaRecherchesurleCancer(ARC).
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