Centromeric DNA destabilizes H3 nucleosomes to promote CENP-A deposition during the cell cycle

Active centromeres are defined by the presence of nucleosomes containing CENP-A, a histone H3 variant, which alone is sufficient to direct kinetochore assembly. Once assembled at a location CENP-A chromatin and kinetochores are maintained at that location though a positive feedback loop where kineto...

Full description

Saved in:
Bibliographic Details
Published inbioRxiv
Main Authors Shukla, Manu, Tong, Pin, White, Sharon A, Singh, Puneet P, Reid, Angus M, Catania, Sandra, Pidoux, Alison L, Allshire, Robin C
Format Paper
LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 07.11.2017
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Active centromeres are defined by the presence of nucleosomes containing CENP-A, a histone H3 variant, which alone is sufficient to direct kinetochore assembly. Once assembled at a location CENP-A chromatin and kinetochores are maintained at that location though a positive feedback loop where kinetochore proteins recruited by CENP-A itself promote deposition of new CENP-A following replication. Although CENP-A chromatin itself is a heritable entity, it is normally associated with specific sequences. Intrinsic properties of centromeric DNA may favour the assembly of CENP-A rather than H3 nucleosomes. Here we investigate histone dynamics on centromeric DNA. We show that during S-phase histone H3 is deposited as a placeholder at fission yeast centromeres and is subsequently evicted in G2 when we detect deposition of the majority of new CENP-ACnp1. We also find that centromeric DNA has an innate property of driving high rates of turnover of H3 containing nucleosomes resulting in low nucleosome occupancy. When placed at an ectopic chromosomal location in the absence of any CENP-ACnp1 assembly, centromeric DNA retains its ability to impose S-phase deposition and G2 eviction of H3, suggesting that features within this DNA program H3 dynamics. As RNAPII occupancy on this centromere DNA coincides with H3 eviction in G2, we propose a model in which RNAPII-coupled chromatin remodelling promotes replacement of H3 with CENP-ACnp1 nucleosomes.
AbstractList Active centromeres are defined by the presence of nucleosomes containing CENP-A, a histone H3 variant, which alone is sufficient to direct kinetochore assembly. Once assembled at a location CENP-A chromatin and kinetochores are maintained at that location though a positive feedback loop where kinetochore proteins recruited by CENP-A itself promote deposition of new CENP-A following replication. Although CENP-A chromatin itself is a heritable entity, it is normally associated with specific sequences. Intrinsic properties of centromeric DNA may favour the assembly of CENP-A rather than H3 nucleosomes. Here we investigate histone dynamics on centromeric DNA. We show that during S-phase histone H3 is deposited as a placeholder at fission yeast centromeres and is subsequently evicted in G2 when we detect deposition of the majority of new CENP-ACnp1. We also find that centromeric DNA has an innate property of driving high rates of turnover of H3 containing nucleosomes resulting in low nucleosome occupancy. When placed at an ectopic chromosomal location in the absence of any CENP-ACnp1 assembly, centromeric DNA retains its ability to impose S-phase deposition and G2 eviction of H3, suggesting that features within this DNA program H3 dynamics. As RNAPII occupancy on this centromere DNA coincides with H3 eviction in G2, we propose a model in which RNAPII-coupled chromatin remodelling promotes replacement of H3 with CENP-ACnp1 nucleosomes.
Author Pidoux, Alison L
Reid, Angus M
White, Sharon A
Singh, Puneet P
Shukla, Manu
Catania, Sandra
Allshire, Robin C
Tong, Pin
Author_xml – sequence: 1
  givenname: Manu
  surname: Shukla
  fullname: Shukla, Manu
– sequence: 2
  givenname: Pin
  surname: Tong
  fullname: Tong, Pin
– sequence: 3
  givenname: Sharon
  surname: White
  middlename: A
  fullname: White, Sharon A
– sequence: 4
  givenname: Puneet
  surname: Singh
  middlename: P
  fullname: Singh, Puneet P
– sequence: 5
  givenname: Angus
  surname: Reid
  middlename: M
  fullname: Reid, Angus M
– sequence: 6
  givenname: Sandra
  surname: Catania
  fullname: Catania, Sandra
– sequence: 7
  givenname: Alison
  surname: Pidoux
  middlename: L
  fullname: Pidoux, Alison L
– sequence: 8
  givenname: Robin
  surname: Allshire
  middlename: C
  fullname: Allshire, Robin C
BookMark eNotj7tOwzAUhj3AAAWe4UjMAd_iOGMVCkWqChLMVIl9DEbBDrEzwNNjBNO_fP_tlByFGJCQC0avGKPsmrNacXlCXjoMeY4fOHsDN_s1WEy5H_zovzHBVkBYzIgxFSJBjjAVNmaEbrN_rH7pKSaffQxgl9mHV8hvCAbHEcxXMZ6RY9ePCc__dUWebjfP3bbaPdzdd-tdNSkqq16attXUMU2tFq4ZrKrdoBsllOES-1paN1g0sjW019zUGm0jW0WFU4ozsSKXf6ll3edSDhze4zKHUnjgtGFcUs5a8QMb_E3k
ContentType Paper
Copyright 2017. Notwithstanding the ProQuest Terms and conditions, you may use this content in accordance with the associated terms available at https://www.biorxiv.org/content/early/2017/11/07/215624
Copyright_xml – notice: 2017. Notwithstanding the ProQuest Terms and conditions, you may use this content in accordance with the associated terms available at https://www.biorxiv.org/content/early/2017/11/07/215624
DBID 8FE
8FH
AAFGM
AAMXL
ABOIG
ABUWG
ADZZV
AFKRA
AFLLJ
AFOLM
AGAJT
AQTIP
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
GNUQQ
HCIFZ
LK8
M7P
PIMPY
PQCXX
PQEST
PQQKQ
PQUKI
PRINS
DOI 10.1101/215624
DatabaseName ProQuest SciTech Collection
ProQuest Natural Science Collection
ProQuest Central Korea - hybrid linking
Natural Science Collection - hybrid linking
Biological Science Collection - hybrid linking
ProQuest Central (Alumni)
ProQuest Central (Alumni) - hybrid linking
ProQuest Central
SciTech Premium Collection - hybrid linking
ProQuest Central Student - hybrid linking
ProQuest Central Essentials - hybrid linking
ProQuest Women's & Gender Studies - hybrid linking
ProQuest Central Essentials
Biological Science Collection
AUTh Library subscriptions: ProQuest Central
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
ProQuest Central Student
SciTech Premium Collection
Biological Sciences
Biological Science Database
Publicly Available Content Database
ProQuest Central - hybrid linking
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
DatabaseTitle Publicly Available Content Database
ProQuest Central Student
ProQuest Biological Science Collection
ProQuest Central Essentials
ProQuest One Academic Eastern Edition
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
Biological Science Database
ProQuest SciTech Collection
ProQuest Central China
ProQuest Central
ProQuest One Academic UKI Edition
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest One Academic
DatabaseTitleList Publicly Available Content Database
Database_xml – sequence: 1
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Genre Working Paper/Pre-Print
GroupedDBID 8FE
8FH
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
GNUQQ
HCIFZ
LK8
M7P
PIMPY
PQEST
PQQKQ
PQUKI
PRINS
ID FETCH-LOGICAL-p604-a4c9980f180d83f7bd65fb87636c24ea54dfbdec49c0a82c58ed749603f66213
IEDL.DBID BENPR
IngestDate Thu Oct 10 16:25:47 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed false
IsScholarly false
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-p604-a4c9980f180d83f7bd65fb87636c24ea54dfbdec49c0a82c58ed749603f66213
OpenAccessLink https://www.proquest.com/docview/2071240219?pq-origsite=%requestingapplication%
PQID 2071240219
PQPubID 2050091
ParticipantIDs proquest_journals_2071240219
PublicationCentury 2000
PublicationDate 20171107
PublicationDateYYYYMMDD 2017-11-07
PublicationDate_xml – month: 11
  year: 2017
  text: 20171107
  day: 07
PublicationDecade 2010
PublicationPlace Cold Spring Harbor
PublicationPlace_xml – name: Cold Spring Harbor
PublicationTitle bioRxiv
PublicationYear 2017
Publisher Cold Spring Harbor Laboratory Press
Publisher_xml – name: Cold Spring Harbor Laboratory Press
Score 1.5584756
Snippet Active centromeres are defined by the presence of nucleosomes containing CENP-A, a histone H3 variant, which alone is sufficient to direct kinetochore...
SourceID proquest
SourceType Aggregation Database
SubjectTerms Cell cycle
Centromeres
Chromatin remodeling
Deoxyribonucleic acid
DNA
Evictions
Histone H3
Kinetochores
Nucleosomes
Nucleotide sequence
Title Centromeric DNA destabilizes H3 nucleosomes to promote CENP-A deposition during the cell cycle
URI https://www.proquest.com/docview/2071240219
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1LSwMxEA7aXrwpKj6q5OA1uJvXZk-itaUIluIDerLkedxdu_Wgv95MTBE8eM6EkCHMl3wz-QahqwCJ_1CIeHOzlPDKC6JB8NIZr2jtA-dJrulxLmev_GEplplw63NZ5TYmpkDtWgscOTAhJWQCyvqmeyfQNQqyq7mFxi4a0pIpNUDDu8l88ZSbCMXjdh0hTcJ39j-RNsHHdB8NF7rz6wO045tD9JYY1TalSvD9_Ba7aJ-Ebr98j2cMN6Ax3PbRosebFnepYs7jcVyTgPW20Ar__DHE8Q6HgYDH9jNOPELP08nLeEZymwPSyYITzW188hShVIVTLFTGSREMCMVJS7nXgrtgnLe8toVW1ArlXcXjw4MFKeOuj9GgaRt_grAN2lYlDzXzhutK1BGeudHUgoQ6o-wUjbZOWOWT2q9-_Xr2__A52qMAaUCpViM02Kw__EUE5I25zF7_BpMWjg0
link.rule.ids 780,784,21388,27925,33744,43805
linkProvider ProQuest
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV07T8MwED5BO8AGAsSjgAfWiMSPPCYEpVWANqqgSJ2oHD_GJDRlgF-Pz6RCYmD2WZZs677zd-fvAK4sJv5tKFzkpmjAEyMCiYKXujQpzYzl3Ms1TYs4f-WPC7HoCLe2K6vc-ETvqHWtkCNHJiTCTECU3TTvAXaNwuxq10JjG_qonC560L8bFbPnromQu27XDtJi_M7-x9N6-BjvQX8mG7Pahy1THcCbZ1Rrnyoh98Ut0c7eC91-mZbkjFSoMVy3zqIl65o0vmLOkKFbM0DrTaEV-fljSFwMR5CAJ-rTTTyEl_FoPsyDrs1B0MQhDyRX7skT2igNdcpsUupY2BKF4mJFuZGCa1tqo3imQplSJVKjE-4eHszGMY3YEfSqujLHQJSVKom4zZgpuUxE5uCZl5IqlFBnlJ3AYLMJy-6mtsvffT39f_gSdvL5dLKcPBRPZ7BLEd6QXk0G0FuvPsy5A-d1edGdwDdYO5D1
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Centromeric+DNA+destabilizes+H3+nucleosomes+to+promote+CENP-A+deposition+during+the+cell+cycle&rft.jtitle=bioRxiv&rft.au=Shukla%2C+Manu&rft.au=Tong%2C+Pin&rft.au=White%2C+Sharon+A&rft.au=Singh%2C+Puneet+P&rft.date=2017-11-07&rft.pub=Cold+Spring+Harbor+Laboratory+Press&rft_id=info:doi/10.1101%2F215624