Inheritance of CENP-A Nucleosomes during DNA Replication Requires HJURP

Ewelina Zasadzińska; Jiehuan Huang; Aaron O. Bailey; Lucie Y. Guo; Nancy S. Lee; Shashank Srivastava; Kelvin A. Wong; Bradley T. French; Ben E. Black; Daniel R. Foltz

doi:10.1016/j.devcel.2018.09.003

Inheritance of CENP-A Nucleosomes during DNA Replication Requires HJURP

Ewelina Zasadzińska, Jiehuan Huang, Aaron O. Bailey, Lucie Y. Guo, Nancy S. Lee, Shashank Srivastava, Kelvin A. Wong, Bradley T. French, Ben E. Black, Daniel R. Foltz^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

62 Scopus citations

Abstract

Centromeric chromatin defines the site of kinetochore formation and ensures faithful chromosome segregation. Centromeric identity is epigenetically specified by the incorporation of CENP-A nucleosomes. DNA replication presents a challenge for inheritance of centromeric identity because nucleosomes are removed to allow for replication fork progression. Despite this challenge, CENP-A nucleosomes are stably retained through S phase. We used BioID to identify proteins transiently associated with CENP-A during DNA replication. We found that during S phase, HJURP transiently associates with centromeres and binds to pre-existing CENP-A, suggesting a distinct role for HJURP in CENP-A retention. We demonstrate that HJURP is required for centromeric nucleosome inheritance during S phase. HJURP co-purifies with the MCM2-7 helicase complex and, together with the MCM2 subunit, binds CENP-A simultaneously. Therefore, pre-existing CENP-A nucleosomes require an S phase function of the HJURP chaperone and interaction with MCM2 to ensure faithful inheritance of centromere identity through DNA replication. Inheritance of centromere identity requires the transmission of CENP-A across DNA replication, when nucleosomes are disassembled ahead of the replication fork. Zasadzińska et al. demonstrate that CENP-A requires the dedicated CENP-A chaperone HJURP and interaction with the replicative helicase complex to retain and redeposit CENP-A following DNA replication.

Original language	English (US)
Pages (from-to)	348-362.e7
Journal	Developmental Cell
Volume	47
Issue number	3
DOIs	https://doi.org/10.1016/j.devcel.2018.09.003
State	Published - Nov 5 2018

Keywords

DNA replication
centromere
chromatin
chromosome
epigenetics
helicase
mitosis
nucleosome

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)
Molecular Biology
Cell Biology
Developmental Biology

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10.1016/j.devcel.2018.09.003

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@article{14ef250385934d5083fa9b0345c139f5,

title = "Inheritance of CENP-A Nucleosomes during DNA Replication Requires HJURP",

abstract = "Centromeric chromatin defines the site of kinetochore formation and ensures faithful chromosome segregation. Centromeric identity is epigenetically specified by the incorporation of CENP-A nucleosomes. DNA replication presents a challenge for inheritance of centromeric identity because nucleosomes are removed to allow for replication fork progression. Despite this challenge, CENP-A nucleosomes are stably retained through S phase. We used BioID to identify proteins transiently associated with CENP-A during DNA replication. We found that during S phase, HJURP transiently associates with centromeres and binds to pre-existing CENP-A, suggesting a distinct role for HJURP in CENP-A retention. We demonstrate that HJURP is required for centromeric nucleosome inheritance during S phase. HJURP co-purifies with the MCM2-7 helicase complex and, together with the MCM2 subunit, binds CENP-A simultaneously. Therefore, pre-existing CENP-A nucleosomes require an S phase function of the HJURP chaperone and interaction with MCM2 to ensure faithful inheritance of centromere identity through DNA replication. Inheritance of centromere identity requires the transmission of CENP-A across DNA replication, when nucleosomes are disassembled ahead of the replication fork. Zasadzi{\'n}ska et al. demonstrate that CENP-A requires the dedicated CENP-A chaperone HJURP and interaction with the replicative helicase complex to retain and redeposit CENP-A following DNA replication.",

keywords = "DNA replication, centromere, chromatin, chromosome, epigenetics, helicase, mitosis, nucleosome",

author = "Ewelina Zasadzi{\'n}ska and Jiehuan Huang and Bailey, {Aaron O.} and Guo, {Lucie Y.} and Lee, {Nancy S.} and Shashank Srivastava and Wong, {Kelvin A.} and French, {Bradley T.} and Black, {Ben E.} and Foltz, {Daniel R.}",

note = "Funding Information: We thank D. Burke, P.T. Stukenberg, Y. Wang, and members of the Foltz lab for helpful comments and A.F. Straight, P.T. Stukenberg, D. Matson, A. Holland, and I. Cheeseman for reagents. We also acknowledge G. Minasov for help with the structure comparison. D.R.F. was supported by NIH R01GM111907 and by a Zell Scholar grant from the Robert L. Lurie Cancer Center . E.Z. was supported by a pre-doctoral fellowship from the American Heart Association ( 15PRE25700271 ). We also acknowledge support by NIH R01GM082989 (B.E.B.) and NIH F30CA186430 (L.Y.G.). Publisher Copyright: {\textcopyright} 2018 Elsevier Inc.",

year = "2018",

month = nov,

day = "5",

doi = "10.1016/j.devcel.2018.09.003",

language = "English (US)",

volume = "47",

pages = "348--362.e7",

journal = "Developmental Cell",

issn = "1534-5807",

publisher = "Cell Press",

number = "3",

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TY - JOUR

T1 - Inheritance of CENP-A Nucleosomes during DNA Replication Requires HJURP

AU - Zasadzińska, Ewelina

AU - Huang, Jiehuan

AU - Bailey, Aaron O.

AU - Guo, Lucie Y.

AU - Lee, Nancy S.

AU - Srivastava, Shashank

AU - Wong, Kelvin A.

AU - French, Bradley T.

AU - Black, Ben E.

AU - Foltz, Daniel R.

N1 - Funding Information: We thank D. Burke, P.T. Stukenberg, Y. Wang, and members of the Foltz lab for helpful comments and A.F. Straight, P.T. Stukenberg, D. Matson, A. Holland, and I. Cheeseman for reagents. We also acknowledge G. Minasov for help with the structure comparison. D.R.F. was supported by NIH R01GM111907 and by a Zell Scholar grant from the Robert L. Lurie Cancer Center . E.Z. was supported by a pre-doctoral fellowship from the American Heart Association ( 15PRE25700271 ). We also acknowledge support by NIH R01GM082989 (B.E.B.) and NIH F30CA186430 (L.Y.G.). Publisher Copyright: © 2018 Elsevier Inc.

PY - 2018/11/5

Y1 - 2018/11/5

N2 - Centromeric chromatin defines the site of kinetochore formation and ensures faithful chromosome segregation. Centromeric identity is epigenetically specified by the incorporation of CENP-A nucleosomes. DNA replication presents a challenge for inheritance of centromeric identity because nucleosomes are removed to allow for replication fork progression. Despite this challenge, CENP-A nucleosomes are stably retained through S phase. We used BioID to identify proteins transiently associated with CENP-A during DNA replication. We found that during S phase, HJURP transiently associates with centromeres and binds to pre-existing CENP-A, suggesting a distinct role for HJURP in CENP-A retention. We demonstrate that HJURP is required for centromeric nucleosome inheritance during S phase. HJURP co-purifies with the MCM2-7 helicase complex and, together with the MCM2 subunit, binds CENP-A simultaneously. Therefore, pre-existing CENP-A nucleosomes require an S phase function of the HJURP chaperone and interaction with MCM2 to ensure faithful inheritance of centromere identity through DNA replication. Inheritance of centromere identity requires the transmission of CENP-A across DNA replication, when nucleosomes are disassembled ahead of the replication fork. Zasadzińska et al. demonstrate that CENP-A requires the dedicated CENP-A chaperone HJURP and interaction with the replicative helicase complex to retain and redeposit CENP-A following DNA replication.

AB - Centromeric chromatin defines the site of kinetochore formation and ensures faithful chromosome segregation. Centromeric identity is epigenetically specified by the incorporation of CENP-A nucleosomes. DNA replication presents a challenge for inheritance of centromeric identity because nucleosomes are removed to allow for replication fork progression. Despite this challenge, CENP-A nucleosomes are stably retained through S phase. We used BioID to identify proteins transiently associated with CENP-A during DNA replication. We found that during S phase, HJURP transiently associates with centromeres and binds to pre-existing CENP-A, suggesting a distinct role for HJURP in CENP-A retention. We demonstrate that HJURP is required for centromeric nucleosome inheritance during S phase. HJURP co-purifies with the MCM2-7 helicase complex and, together with the MCM2 subunit, binds CENP-A simultaneously. Therefore, pre-existing CENP-A nucleosomes require an S phase function of the HJURP chaperone and interaction with MCM2 to ensure faithful inheritance of centromere identity through DNA replication. Inheritance of centromere identity requires the transmission of CENP-A across DNA replication, when nucleosomes are disassembled ahead of the replication fork. Zasadzińska et al. demonstrate that CENP-A requires the dedicated CENP-A chaperone HJURP and interaction with the replicative helicase complex to retain and redeposit CENP-A following DNA replication.

KW - DNA replication

KW - centromere

KW - chromatin

KW - chromosome

KW - epigenetics

KW - helicase

KW - mitosis

KW - nucleosome

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DO - 10.1016/j.devcel.2018.09.003

M3 - Article

C2 - 30293838

AN - SCOPUS:85056256689

SN - 1534-5807

VL - 47

SP - 348-362.e7

JO - Developmental Cell

JF - Developmental Cell

IS - 3

ER -

Inheritance of CENP-A Nucleosomes during DNA Replication Requires HJURP

Abstract

Keywords

ASJC Scopus subject areas

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