A tubule-sheet continuum model for the mechanism of nuclear envelope assembly.

endoplasmic reticulum micronuclei mitosis mitotic actin myosin V nuclear envelope nuclear pore complexes

Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
22 05 2023
Historique:
received: 01 11 2022
revised: 25 01 2023
accepted: 01 04 2023
pmc-release: 22 05 2024
medline: 25 5 2023
pubmed: 26 4 2023
entrez: 25 4 2023
Statut: ppublish

Résumé

Nuclear envelope (NE) assembly defects cause chromosome fragmentation, cancer, and aging. However, major questions about the mechanism of NE assembly and its relationship to nuclear pathology are unresolved. In particular, how cells efficiently assemble the NE starting from vastly different, cell type-specific endoplasmic reticulum (ER) morphologies is unclear. Here, we identify a NE assembly mechanism, "membrane infiltration," that defines one end of a continuum with another NE assembly mechanism, "lateral sheet expansion," in human cells. Membrane infiltration involves the recruitment of ER tubules or small sheets to the chromatin surface by mitotic actin filaments. Lateral sheet expansion involves actin-independent envelopment of peripheral chromatin by large ER sheets that then extend over chromatin within the spindle. We propose a "tubule-sheet continuum" model that explains the efficient NE assembly from any starting ER morphology, the cell type-specific patterns of nuclear pore complex (NPC) assembly, and the obligatory NPC assembly defect of micronuclei.

Identifiants

pubmed: 37098350
pii: S1534-5807(23)00156-9
doi: 10.1016/j.devcel.2023.04.003
pmc: PMC10205699
mid: NIHMS1892899
pii:
doi:

Substances chimiques

Chromatin 0
Actins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

847-865.e10

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM130298
Pays : United States
Organisme : NIGMS NIH HHS
ID : R37 GM061345
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests D.P. is a member of the Developmental Cell advisory board. D.P. is a member of the Volastra Therapeutics scientific advisory board. D.P.’s spouse is an employee of Novartis Institutes for Biomedical Research.

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Auteurs

Gengjing Zhao (G)

Howard Hughes Medical Institute, Chevy Chase, MD, USA; Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Cell Biology, Harvard Medical School, Boston, MA, USA.

Shiwei Liu (S)

Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.

Sanjana Arun (S)

Howard Hughes Medical Institute, Chevy Chase, MD, USA; Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Cell Biology, Harvard Medical School, Boston, MA, USA.

Fioranna Renda (F)

Wadsworth Center, New York State Department of Health, Albany, NY, USA.

Alexey Khodjakov (A)

Wadsworth Center, New York State Department of Health, Albany, NY, USA.

David Pellman (D)

Howard Hughes Medical Institute, Chevy Chase, MD, USA; Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Cell Biology, Harvard Medical School, Boston, MA, USA. Electronic address: david_pellman@dfci.harvard.edu.

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Classifications MeSH