An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes

Masashi Mori, K. Somogyi, Hiroshi Kondo, Nilah Monnier, Henning J. Falk, Pedro MacHado, Mark Bathe, François Nédélec, Péter Lénárt

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Animal cells disassemble and reassemble their nuclear envelopes (NEs) upon each division [1, 2]. 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 [2, 3]. Breakdown is initiated by phosphorylation-driven partial disassembly of the nuclear pore complexes (NPCs), increasing their permeability but leaving the overall NE structure intact [4-7]. 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 [6, 8]. 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.

Original languageEnglish
Pages (from-to)1421-1428
Number of pages8
JournalCurrent Biology
Volume24
Issue number12
DOIs
Publication statusPublished - Jun 16 2014

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Starfish
Asteroidea
Nuclear Envelope
nuclear membrane
Oocytes
actin
Actins
oocytes
Membranes
Actin-Related Protein 2-3 Complex
Phosphorylation
Animals
Cells
Molecules
Prometaphase
nucleoporins
Nuclear Pore
Prophase
aneuploidy
prophase

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes. / Mori, Masashi; Somogyi, K.; Kondo, Hiroshi; Monnier, Nilah; Falk, Henning J.; MacHado, Pedro; Bathe, Mark; Nédélec, François; Lénárt, Péter.

In: Current Biology, Vol. 24, No. 12, 16.06.2014, p. 1421-1428.

Research output: Contribution to journalArticle

Mori, M, Somogyi, K, Kondo, H, Monnier, N, Falk, HJ, MacHado, P, Bathe, M, Nédélec, F & Lénárt, P 2014, 'An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes', Current Biology, vol. 24, no. 12, pp. 1421-1428. https://doi.org/10.1016/j.cub.2014.05.019
Mori, Masashi ; Somogyi, K. ; Kondo, Hiroshi ; Monnier, Nilah ; Falk, Henning J. ; MacHado, Pedro ; Bathe, Mark ; Nédélec, François ; Lénárt, Péter. / An Arp2/3 nucleated F-actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes. In: Current Biology. 2014 ; Vol. 24, No. 12. pp. 1421-1428.
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