title: An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes.
abstract: Animal cells disassemble and reassemble their nuclear envelopes (NEs) upon each division. Nuclear envelope breakdown (NEBD) serves as a major regulatory mechanism by which mixing of cytoplasmic and nuclear compartments drives the complete reorganization of cellular architecture, committing the cell for division. Breakdown is initiated by phosphorylation-driven partial disassembly of the nuclear pore complexes (NPCs), increasing their permeability but leaving the overall NE structure intact. Subsequently, the NE is rapidly broken into membrane fragments, defining the transition from prophase to prometaphase and resulting in complete mixing of cyto- and nucleoplasm. However, the mechanism underlying this rapid NE fragmentation remains largely unknown. Here, we show that NE fragmentation during NEBD in starfish oocytes is driven by an Arp2/3 complex-nucleated F-actin "shell" that transiently polymerizes on the inner surface of the NE. Blocking the formation of this F-actin shell prevents membrane fragmentation and delays entry of large cytoplasmic molecules into the nucleus. We observe spike-like protrusions extending from the F-actin shell that appear to "pierce" the NE during the fragmentation process. Finally, we show that NE fragmentation is essential for successful reproduction, because blocking this process in meiosis leads to formation of aneuploid eggs.
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: Masashi
authors.initials: M
authors.lastname: Mori
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: Kálmán
authors.initials: K
authors.lastname: Somogyi
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: Hiroshi
authors.initials: H
authors.lastname: Kondo
authors.affiliation: Laboratory for Computational Biology and Biophysics, Department of Biological Engineering, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Graduate Program in Biophysics, Harvard University, 1350 Massachusetts Avenue, Cambridge, MA 02138, USA.
authors.forename: Nilah
authors.initials: N
authors.lastname: Monnier
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: Henning J
authors.initials: HJ
authors.lastname: Falk
authors.affiliation: Electron Microscopy Core Facility, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: Pedro
authors.initials: P
authors.lastname: Machado
authors.affiliation: Laboratory for Computational Biology and Biophysics, Department of Biological Engineering, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Broad Institute of MIT and Harvard, 301 Binney Street, Cambridge, MA 02142, USA.
authors.forename: Mark
authors.initials: M
authors.lastname: Bathe
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany.
authors.forename: François
authors.initials: F
authors.lastname: Nédélec
authors.affiliation: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, Heidelberg 69117, Germany. Electronic address: lenart@embl.de.
authors.forename: Péter
authors.initials: P
authors.lastname: Lénárt
mesh_terms: D051376:Actin-Related Protein 2-3 Complex / Q000235:genetics* / Q000378:metabolism; D000185:Actinin / Q000235:genetics* / Q000378:metabolism; D000199:Actins / Q000235:genetics* / Q000378:metabolism; D000818:Animals; D008540:Meiosis; D008969:Molecular Sequence Data; D009685:Nuclear Envelope / Q000378:metabolism*; D009865:Oocytes / Q000378:metabolism; D058105:Polymerization; D017422:Sequence Analysis, DNA; D013215:Starfish
chemical_list: D051376:Actin-Related Protein 2-3 Complex; D000199:Actins; D000185:Actinin