Cargando…

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

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 L...

Descripción completa

Detalles Bibliográficos
Autores principales: Barger, Sarah R., Penfield, Lauren, Bahmanyar, Shirin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668030/
https://www.ncbi.nlm.nih.gov/pubmed/37795681
http://dx.doi.org/10.1242/jcs.261385
_version_ 1785149073891786752
author Barger, Sarah R.
Penfield, Lauren
Bahmanyar, Shirin
author_facet Barger, Sarah R.
Penfield, Lauren
Bahmanyar, Shirin
author_sort Barger, Sarah R.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-10668030
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-106680302023-11-13 Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure Barger, Sarah R. Penfield, Lauren Bahmanyar, Shirin J Cell Sci Research Article 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. The Company of Biologists Ltd 2023-11-13 /pmc/articles/PMC10668030/ /pubmed/37795681 http://dx.doi.org/10.1242/jcs.261385 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Barger, Sarah R.
Penfield, Lauren
Bahmanyar, Shirin
Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title_full Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title_fullStr Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title_full_unstemmed Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title_short Nuclear envelope assembly relies on CHMP-7 in the absence of BAF–LEM-mediated hole closure
title_sort nuclear envelope assembly relies on chmp-7 in the absence of baf–lem-mediated hole closure
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10668030/
https://www.ncbi.nlm.nih.gov/pubmed/37795681
http://dx.doi.org/10.1242/jcs.261385
work_keys_str_mv AT bargersarahr nuclearenvelopeassemblyreliesonchmp7intheabsenceofbaflemmediatedholeclosure
AT penfieldlauren nuclearenvelopeassemblyreliesonchmp7intheabsenceofbaflemmediatedholeclosure
AT bahmanyarshirin nuclearenvelopeassemblyreliesonchmp7intheabsenceofbaflemmediatedholeclosure