Multiscale biophysical analysis of nucleolus disassembly during mitosis.

critical phenomena membraneless organelles nucleolus disassembly

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
06 Feb 2024
Historique:
medline: 29 1 2024
pubmed: 29 1 2024
entrez: 29 1 2024
Statut: ppublish

Résumé

During cell division, precise and regulated distribution of cellular material between daughter cells is a critical step and is governed by complex biochemical and biophysical mechanisms. To achieve this, membraneless organelles and condensates often require complete disassembly during mitosis. The biophysical principles governing the disassembly of condensates remain poorly understood. Here, we used a physical biology approach to study how physical and material properties of the nucleolus, a prominent nuclear membraneless organelle in eukaryotic cells, change during mitosis and across different scales. We found that nucleolus disassembly proceeds continuously through two distinct phases with a slow and reversible preparatory phase followed by a rapid irreversible phase that was concurrent with the nuclear envelope breakdown. We measured microscopic properties of nucleolar material including effective diffusion rates and binding affinities as well as key macroscopic properties of surface tension and bending rigidity. By incorporating these measurements into the framework of critical phenomena, we found evidence that near mitosis surface tension displays a power-law behavior as a function of biochemically modulated interaction strength. This two-step disassembly mechanism maintains structural and functional stability of nucleolus while enabling its rapid and efficient disassembly in response to cell cycle cues.

Identifiants

pubmed: 38285946
doi: 10.1073/pnas.2312250121
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2312250121

Subventions

Organisme : HHS | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM140272
Organisme : HHS | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM149076
Organisme : Simons Foundation (SF)
ID : 597491

Déclaration de conflit d'intérêts

Competing interests statement:The authors declare no competing interest.

Auteurs

An T Pham (AT)

Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208.

Madhav Mani (M)

Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208.
NSF-Simons Center for Quantitative Biology, Northwestern University, Evanston, IL 60208.

Xiaozhong Wang (X)

Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208.
NSF-Simons Center for Quantitative Biology, Northwestern University, Evanston, IL 60208.

Reza Vafabakhsh (R)

Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208.

Classifications MeSH