Releasing Activity Disengages Cohesin’s Smc3/Scc1 Interface in a Process Blocked by Acetylation

Frederic Beckouët; Madhusudhan Srinivasan; Maurici Brunet Roig; Kok-Lung Chan; Johanna C. Scheinost; Paul Batty; Bin Hu; Naomi Petela; Thomas Gligoris; Alexandra C. Smith; Lana Strmecki; Benjamin D. Rowland; Kim Nasmyth

doi:10.1016/j.molcel.2016.01.026

Releasing Activity Disengages Cohesin’s Smc3/Scc1 Interface in a Process Blocked by Acetylation

Frederic Beckouët, Madhusudhan Srinivasan, Maurici Brunet Roig, Kok-Lung Chan, Johanna C. Scheinost, Paul Batty, Bin Hu, Naomi Petela, Thomas Gligoris, Alexandra C. Smith, Lana Strmecki, Benjamin D. Rowland , Kim Nasmyth^*

^*Corresponding author for this work

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

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Abstract

Sister chromatid cohesion conferred by entrapment of sister DNAs within a tripartite ring formed between cohesin’s Scc1, Smc1, and Smc3 subunits is created during S and destroyed at anaphase through Scc1 cleavage by separase. Cohesin’s association with chromosomes is controlled by opposing activities: loading by Scc2/4 complex and release by a separase-independent releasing activity as well as by cleavage. Coentrapment of sister DNAs at replication is accompanied by acetylation of Smc3 by Eco1, which blocks releasing activity and ensures that sisters remain connected. Because fusion of Smc3 to Scc1 prevents release and bypasses the requirement for Eco1, we suggested that release is mediated by disengagement of the Smc3/Scc1 interface. We show that mutations capable of bypassing Eco1 in Smc1, Smc3, Scc1, Wapl, Pds5, and Scc3 subunits reduce dissociation of N-terminal cleavage fragments of Scc1 (NScc1) from Smc3. This process involves interaction between Smc ATPase heads and is inhibited by Smc3 acetylation.

Original language	English
Pages (from-to)	563-574
Number of pages	13
Journal	Molecular Cell
Volume	61
Issue number	4
Early online date	18 Feb 2016
DOIs	https://doi.org/10.1016/j.molcel.2016.01.026
Publication status	Published - 18 Feb 2016
Externally published	Yes

Bibliographical note

ACKNOWLEDGMENTS
We are grateful to K. Shirahige for supplying anti-acetylated Smc3 antibody
and to all members of the Nasmyth group for valuable discussions. This
work was funded by the Wellcome Trust (091859/Z/10/Z to K.N.) and Cancer
Research UK (C573/A 12386 to K.N.).

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Beckouet_et_al_MC_ReleasingActivityDisengages_VoR
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Bin Hu
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Cite this

@article{0a47643692304c3781f6aa38060dc936,

title = "Releasing Activity Disengages Cohesin{\textquoteright}s Smc3/Scc1 Interface in a Process Blocked by Acetylation",

abstract = "Sister chromatid cohesion conferred by entrapment of sister DNAs within a tripartite ring formed between cohesin{\textquoteright}s Scc1, Smc1, and Smc3 subunits is created during S and destroyed at anaphase through Scc1 cleavage by separase. Cohesin{\textquoteright}s association with chromosomes is controlled by opposing activities: loading by Scc2/4 complex and release by a separase-independent releasing activity as well as by cleavage. Coentrapment of sister DNAs at replication is accompanied by acetylation of Smc3 by Eco1, which blocks releasing activity and ensures that sisters remain connected. Because fusion of Smc3 to Scc1 prevents release and bypasses the requirement for Eco1, we suggested that release is mediated by disengagement of the Smc3/Scc1 interface. We show that mutations capable of bypassing Eco1 in Smc1, Smc3, Scc1, Wapl, Pds5, and Scc3 subunits reduce dissociation of N-terminal cleavage fragments of Scc1 (NScc1) from Smc3. This process involves interaction between Smc ATPase heads and is inhibited by Smc3 acetylation.",

author = "Frederic Beckou{\"e}t and Madhusudhan Srinivasan and Roig, {Maurici Brunet} and Kok-Lung Chan and Scheinost, {Johanna C.} and Paul Batty and Bin Hu and Naomi Petela and Thomas Gligoris and Smith, {Alexandra C.} and Lana Strmecki and Rowland, {Benjamin D.} and Kim Nasmyth",

note = "ACKNOWLEDGMENTS We are grateful to K. Shirahige for supplying anti-acetylated Smc3 antibody and to all members of the Nasmyth group for valuable discussions. This work was funded by the Wellcome Trust (091859/Z/10/Z to K.N.) and Cancer Research UK (C573/A 12386 to K.N.).",

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day = "18",

doi = "10.1016/j.molcel.2016.01.026",

language = "English",

volume = "61",

pages = "563--574",

journal = "Molecular Cell",

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publisher = "Cell Press",

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T1 - Releasing Activity Disengages Cohesin’s Smc3/Scc1 Interface in a Process Blocked by Acetylation

AU - Beckouët, Frederic

AU - Srinivasan, Madhusudhan

AU - Roig, Maurici Brunet

AU - Chan, Kok-Lung

AU - Scheinost, Johanna C.

AU - Batty, Paul

AU - Hu, Bin

AU - Petela, Naomi

AU - Gligoris, Thomas

AU - Smith, Alexandra C.

AU - Strmecki, Lana

AU - Rowland , Benjamin D.

AU - Nasmyth, Kim

N1 - ACKNOWLEDGMENTS We are grateful to K. Shirahige for supplying anti-acetylated Smc3 antibody and to all members of the Nasmyth group for valuable discussions. This work was funded by the Wellcome Trust (091859/Z/10/Z to K.N.) and Cancer Research UK (C573/A 12386 to K.N.).

PY - 2016/2/18

Y1 - 2016/2/18

N2 - Sister chromatid cohesion conferred by entrapment of sister DNAs within a tripartite ring formed between cohesin’s Scc1, Smc1, and Smc3 subunits is created during S and destroyed at anaphase through Scc1 cleavage by separase. Cohesin’s association with chromosomes is controlled by opposing activities: loading by Scc2/4 complex and release by a separase-independent releasing activity as well as by cleavage. Coentrapment of sister DNAs at replication is accompanied by acetylation of Smc3 by Eco1, which blocks releasing activity and ensures that sisters remain connected. Because fusion of Smc3 to Scc1 prevents release and bypasses the requirement for Eco1, we suggested that release is mediated by disengagement of the Smc3/Scc1 interface. We show that mutations capable of bypassing Eco1 in Smc1, Smc3, Scc1, Wapl, Pds5, and Scc3 subunits reduce dissociation of N-terminal cleavage fragments of Scc1 (NScc1) from Smc3. This process involves interaction between Smc ATPase heads and is inhibited by Smc3 acetylation.

AB - Sister chromatid cohesion conferred by entrapment of sister DNAs within a tripartite ring formed between cohesin’s Scc1, Smc1, and Smc3 subunits is created during S and destroyed at anaphase through Scc1 cleavage by separase. Cohesin’s association with chromosomes is controlled by opposing activities: loading by Scc2/4 complex and release by a separase-independent releasing activity as well as by cleavage. Coentrapment of sister DNAs at replication is accompanied by acetylation of Smc3 by Eco1, which blocks releasing activity and ensures that sisters remain connected. Because fusion of Smc3 to Scc1 prevents release and bypasses the requirement for Eco1, we suggested that release is mediated by disengagement of the Smc3/Scc1 interface. We show that mutations capable of bypassing Eco1 in Smc1, Smc3, Scc1, Wapl, Pds5, and Scc3 subunits reduce dissociation of N-terminal cleavage fragments of Scc1 (NScc1) from Smc3. This process involves interaction between Smc ATPase heads and is inhibited by Smc3 acetylation.

U2 - 10.1016/j.molcel.2016.01.026

DO - 10.1016/j.molcel.2016.01.026

M3 - Article

SN - 1097-2765

VL - 61

SP - 563

EP - 574

JO - Molecular Cell

JF - Molecular Cell

IS - 4

ER -

Releasing Activity Disengages Cohesin’s Smc3/Scc1 Interface in a Process Blocked by Acetylation

Abstract

Bibliographical note

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