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Cited by 17Nuclear Structure and FunctionMicrotubule and mitosis dynamicsGenomics and Chromatin Dynamics

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Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure

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Barger, Sarah R., Penfield, Lauren, Bahmanyar, Shirin·2023·Journal of Cell Science
DOI 10.1242/jcs.261385PMC PMC10668030

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Abstract

Barrier-to-autointegration factor (BAF) protein is a DNA-binding protein that crosslinks chromatin to allow mitotic nuclear envelope (NE) assembly. The LAP2-emerin-MAN1 (LEM)-domain protein LEMD2 and ESCRT-II/III hybrid protein CHMP7 close NE holes surrounding spindle microtubules (MTs). BAF binds LEM-domain family proteins to repair NE ruptures in interphase, but whether BAF–LEM binding participates in NE hole closure around spindle MTs is not known. Here, we took advantage of the stereotypical event of NE formation in fertilized Caenorhabditis elegans oocytes to show that BAF–LEM binding and LEM-2–CHMP-7 have distinct roles in NE closure around spindle MTs. LEM-2 and EMR-1 (homologs of LEMD2 and emerin) function redundantly with BAF-1 (the C. elegans BAF protein) in NE closure. Compromising BAF–LEM binding revealed an additional role for EMR-1 in the maintenance of the NE permeability barrier. In the absence of BAF–LEM binding, LEM-2–CHMP-7 was required for NE assembly and embryo survival. The winged helix domain of LEM-2 recruits CHMP-7 to the NE in C. elegans and a LEM-2-independent nucleoplasmic pool of CHMP-7 also contributes to NE stability. Thus, NE hole closure surrounding spindle MTs requires redundant mechanisms that safeguard against failure in NE assembly to support embryogenesis.

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Metadata

Authors
Barger, S. R., Penfield, L., & Bahmanyar, S.
Affiliations
  • Yale University (US)
  • University of California, Santa Barbara (US)
Corresponding author
Bahmanyar, Shirin
ORCID
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2023-11-01
Volume
136
Issue
21
ISSN
  • 0021-9533 (ISSN-L)
  • 1477-9137
DOI
10.1242/jcs.261385
PMC
PMC10668030
OpenAlex
W4387357147
Cited by
17
References
1
Citations by year
2026: 3 · 2025: 1 · 2024: 12 · 2023: 1
FWCI
1.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Cell Science (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
  • American Cancer Society (PF-21-187-01-CCB)
  • National Science Foundation (1846010)
  • National Institutes of Health (R01 GM131004)
  • Yale University
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
nuclear envelope assembly, emerin, spindle microtubules, fertilisation (biology), embryonic development, winged-helix domain

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