As eukaryotic cells progress through cell division, the nuclear envelope (NE) membrane must expand to accommodate the formation of progeny nuclei. In Saccharomyces cerevisiae, closed mitosis allows visualization of NE biogenesis during mitosis. During this period, the SUMO E3 ligase Siz2 binds the inner nuclear membrane (INM) and initiates a wave of INM protein SUMOylation. Here, we show these events increase INM levels of phosphatidic acid (PA), an intermediate of phospholipid biogenesis, and are necessary for normal mitotic NE membrane expansion. The increase in INM PA is driven by the Siz2-mediated inhibition of the PA phosphatase Pah1. During mitosis, this results from the binding of Siz2 to the INM and dissociation of Spo7 and Nem1, a complex required for the activation of Pah1. As cells enter interphase, the process is then reversed by the deSUMOylase Ulp1. This work further establishes a central role for temporally controlled INM SUMOylation in coordinating processes, including membrane expansion, that regulate NE biogenesis during mitosis.
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7 August 2023
Article|
July 03 2023
SUMOylation at the inner nuclear membrane facilitates nuclear envelope biogenesis during mitosis
Natasha O. Saik
,
Natasha O. Saik
(Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
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Christopher Ptak
,
Christopher Ptak
(Conceptualization, Investigation, Visualization, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
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Saif Rehman
,
Saif Rehman
(Investigation, Visualization, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
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John D. Aitchison
,
John D. Aitchison
(Conceptualization, Funding acquisition, Methodology, Visualization, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
2
Seattle Children’s Research Institute
, Seattle, WA, USA
3Department of Pediatrics and Department of Biochemistry,
University of Washington
, Seattle, WA, USA
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Ben Montpetit
,
Ben Montpetit
(Conceptualization, Funding acquisition, Methodology, Supervision, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
4Department of Viticulture and Enology,
University of California Davis
, Davis, CA, USA
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Richard W. Wozniak
(Conceptualization, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Supervision, Visualization, Writing - original draft, Writing - review & editing)
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
Correspondence to Richard W. Wozniak: rick.wozniak@ualberta.ca
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Natasha O. Saik
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
Christopher Ptak
Conceptualization, Investigation, Visualization, Writing - review & editing
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
Saif Rehman
Investigation, Visualization, Writing - review & editing
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
John D. Aitchison
Conceptualization, Funding acquisition, Methodology, Visualization, Writing - review & editing
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
2
Seattle Children’s Research Institute
, Seattle, WA, USA
3Department of Pediatrics and Department of Biochemistry,
University of Washington
, Seattle, WA, USA
Ben Montpetit
Conceptualization, Funding acquisition, Methodology, Supervision, Writing - review & editing
1Department of Cell Biology,
University of Alberta
, Edmonton, Alberta, Canada
4Department of Viticulture and Enology,
University of California Davis
, Davis, CA, USA
Correspondence to Richard W. Wozniak: rick.wozniak@ualberta.ca
Disclosures: The authors declare no competing interests exist.
Received:
August 24 2022
Revision Received:
March 24 2023
Accepted:
May 15 2023
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funding
Funder(s):
Canadian Institutes of Health Research
- Award Id(s): MOP 106502,PJT 180467
Funder(s):
National Institutes of Health
- Award Id(s): 2P41GM109824-06,2R01GM112108-05,R01GM124120
© 2023 Saik et al.
2023
Saik et al.
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 (2023) 222 (8): e202208137.
Article history
Received:
August 24 2022
Revision Received:
March 24 2023
Accepted:
May 15 2023
Connected Content
Citation
Natasha O. Saik, Christopher Ptak, Saif Rehman, John D. Aitchison, Ben Montpetit, Richard W. Wozniak; SUMOylation at the inner nuclear membrane facilitates nuclear envelope biogenesis during mitosis. J Cell Biol 7 August 2023; 222 (8): e202208137. doi: https://doi.org/10.1083/jcb.202208137
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