In eukaryotes, chromatin binding to the inner nuclear membrane (INM) and nuclear pore complexes (NPCs) contributes to spatial organization of the genome and epigenetic programs important for gene expression. In mitosis, chromatin–nuclear envelope (NE) interactions are lost and then formed again as sister chromosomes segregate to postmitotic nuclei. Investigating these processes in S. cerevisiae, we identified temporally and spatially controlled phosphorylation-dependent SUMOylation events that positively regulate postmetaphase chromatin association with the NE. Our work establishes a phosphorylation-mediated targeting mechanism of the SUMO ligase Siz2 to the INM during mitosis, where Siz2 binds to and SUMOylates the VAP protein Scs2. The recruitment of Siz2 through Scs2 is further responsible for a wave of SUMOylation along the INM that supports the assembly and anchorage of subtelomeric chromatin at the INM and localization of an active gene (INO1) to NPCs during the later stages of mitosis and into G1-phase.
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6 December 2021
Article|
November 17 2021
Phosphorylation-dependent mitotic SUMOylation drives nuclear envelope–chromatin interactions
Christopher Ptak,
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
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Natasha O. Saik,
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
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Ashwini Premashankar
,
Ashwini Premashankar
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
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Diego L. Lapetina
,
Diego L. Lapetina
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
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John D. Aitchison
,
John D. Aitchison
2
Seattle Children’s Research Institute, Seattle, WA
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Ben Montpetit
,
Ben Montpetit
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
3
Department of Viticulture and Enology, University of California Davis, Davis, CA
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Richard W. Wozniak
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
Correspondence to Richard W. Wozniak: rick.wozniak@ualberta.ca
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Ashwini Premashankar
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
Diego L. Lapetina
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
John D. Aitchison
2
Seattle Children’s Research Institute, Seattle, WA
Ben Montpetit
1
Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada
3
Department of Viticulture and Enology, University of California Davis, Davis, CA
Correspondence to Richard W. Wozniak: rick.wozniak@ualberta.ca
*
C. Ptak and N.O. Saik contributed equally to this paper.
Received:
March 05 2021
Revision Received:
July 30 2021
Accepted:
September 22 2021
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
Canadian Institutes of Health Research
- Award Id(s): MOP 106502,36519
Funder(s):
National Institutes of Health
- Award Id(s): NCDIR: 2P41GM109824-06,R01: 2R01GM112108-05,R01GM124120
© 2021 Ptak et al.
2021
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2021) 220 (12): e202103036.
Article history
Received:
March 05 2021
Revision Received:
July 30 2021
Accepted:
September 22 2021
Connected Content
Commentary
A SUMOylation wave to anchor the genome
Citation
Christopher Ptak, Natasha O. Saik, Ashwini Premashankar, Diego L. Lapetina, John D. Aitchison, Ben Montpetit, Richard W. Wozniak; Phosphorylation-dependent mitotic SUMOylation drives nuclear envelope–chromatin interactions. J Cell Biol 6 December 2021; 220 (12): e202103036. doi: https://doi.org/10.1083/jcb.202103036
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