SUMOylation at the inner nuclear membrane facilitates nuclear envelope biogenesis during mitosis.
Journal
The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356
Informations de publication
Date de publication:
07 08 2023
07 08 2023
Historique:
received:
24
08
2022
revised:
24
03
2023
accepted:
15
05
2023
pmc-release:
03
01
2024
medline:
5
7
2023
pubmed:
3
7
2023
entrez:
3
7
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 37398994
pii: 214212
doi: 10.1083/jcb.202208137
pmc: PMC10318406
pii:
doi:
Substances chimiques
Nem1 protein, S cerevisiae
0
Nuclear Proteins
0
Saccharomyces cerevisiae Proteins
0
Siz2 protein, S cerevisiae
0
ULP1 protein, S cerevisiae
EC 3.4.22.68
SPO7 protein, S cerevisiae
0
PAH1 protein, S cerevisiae
EC 3.1.3.4
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : P41 GM109824
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM112108
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM124120
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 Saik et al.
Références
Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1047-52
pubmed: 11792863
Nat Genet. 2001 Jan;27(1):121-4
pubmed: 11138012
Nature. 2003 Oct 16;425(6959):737-41
pubmed: 14562106
J Biol Chem. 2008 Jul 18;283(29):20433-42
pubmed: 18458075
PLoS One. 2014 Aug 12;9(8):e104194
pubmed: 25117580
Cell. 2011 Aug 5;146(3):408-20
pubmed: 21816276
Dev Cell. 2012 Dec 11;23(6):1129-40
pubmed: 23237950
J Cell Biol. 2016 Nov 21;215(4):575-590
pubmed: 27831485
EMBO J. 2005 Jun 1;24(11):1931-41
pubmed: 15889145
Nature. 2003 Oct 16;425(6959):686-91
pubmed: 14562095
J Cell Biol. 2009 May 4;185(3):459-73
pubmed: 19414608
Annu Rev Genet. 2013;47:167-86
pubmed: 24016193
J Biol Chem. 1989 May 25;264(15):8641-5
pubmed: 2542283
Dev Cell. 2019 Sep 23;50(6):755-766.e6
pubmed: 31422915
J Cell Sci. 2016 Dec 15;129(24):4480-4495
pubmed: 27831493
Mol Biol Cell. 2006 Apr;17(4):1768-78
pubmed: 16467382
Curr Biol. 2012 Jun 19;22(12):1128-33
pubmed: 22658600
Yeast. 1998 Jul;14(10):953-61
pubmed: 9717241
PLoS Biol. 2004 Nov;2(11):e342
pubmed: 15455074
Proc Natl Acad Sci U S A. 2010 Oct 12;107(41):17539-44
pubmed: 20876142
Nature. 2007 Nov 29;450(7170):695-701
pubmed: 18046406
J Biol Chem. 2012 Mar 30;287(14):11290-301
pubmed: 22334681
Exp Cell Res. 2016 Mar 1;342(1):83-94
pubmed: 26921507
J Cell Sci. 2023 Feb 1;136(3):
pubmed: 36695178
J Cell Biol. 2021 Dec 6;220(12):
pubmed: 34714326
Cold Spring Harb Perspect Biol. 2010 Mar;2(3):a000539
pubmed: 20300205
EMBO J. 2003 May 1;22(9):2025-35
pubmed: 12727870
Cell. 2013 Feb 28;152(5):969-83
pubmed: 23452847
J Cell Biol. 2010 Dec 13;191(6):1079-88
pubmed: 21135138
EMBO J. 2021 Nov 15;40(22):e107958
pubmed: 34617598
J Biol Chem. 2013 Dec 13;288(50):35781-92
pubmed: 24196957
J Biol Chem. 2008 Oct 24;283(43):29166-74
pubmed: 18694939
Mol Biol Cell. 2011 May;22(9):1430-9
pubmed: 21372176
Curr Opin Cell Biol. 2014 Jun;28:46-53
pubmed: 24657998
PLoS One. 2009 Sep 15;4(9):e7031
pubmed: 19753306
Cell. 2001 Sep 21;106(6):735-44
pubmed: 11572779
J Cell Biol. 2021 Dec 6;220(12):
pubmed: 34787675
EMBO J. 1998 Nov 16;17(22):6449-64
pubmed: 9822591
Anal Biochem. 2017 Jun 1;526:69-70
pubmed: 28359787
Methods Enzymol. 2002;350:87-96
pubmed: 12073338
Mol Cell. 2019 Dec 5;76(5):811-825.e14
pubmed: 31628041
Annu Rev Biochem. 2011;80:859-83
pubmed: 21275641
J Biol Chem. 2007 Jan 5;282(1):277-86
pubmed: 17105729
J Cell Biol. 2021 Mar 1;220(3):
pubmed: 33464310
J Biol Chem. 2014 Dec 12;289(50):34699-708
pubmed: 25359770
Biochim Biophys Acta Mol Cell Biol Lipids. 2020 Jan;1865(1):158434
pubmed: 30910690
J Biol Chem. 2006 Apr 7;281(14):9210-8
pubmed: 16467296
Cell. 2020 Oct 1;183(1):28-45
pubmed: 32976797
Cell Cycle. 2014;13(5):859-68
pubmed: 24418822
J Cell Biol. 2017 Oct 2;216(10):3145-3159
pubmed: 28883038
J Cell Sci. 2021 Sep 1;134(17):
pubmed: 34387316
Dev Cell. 2018 May 21;45(4):481-495.e8
pubmed: 29754800
J Electron Microsc (Tokyo). 2011;60(5):321-35
pubmed: 21908548
Cell Cycle. 2019 Jul;18(14):1646-1659
pubmed: 31203714
Genetics. 1989 May;122(1):19-27
pubmed: 2659436
Yeast. 1998 Jan 30;14(2):115-32
pubmed: 9483801
J Biol Chem. 2006 Nov 10;281(45):34537-48
pubmed: 16968695
J Biol Chem. 2011 Jan 14;286(2):1486-98
pubmed: 21081492
Science. 2004 Jun 11;304(5677):1644-7
pubmed: 15192221
Cell. 2018 Jul 26;174(3):700-715.e18
pubmed: 29937227