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Published online 24 March 2003. doi:10.1083/jcb.200211076
 The Rockefeller University Press, 0021-9525 $8.00
The Journal of Cell Biology
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© The Rockefeller University Press, 0021-9525
The Journal of Cell Biology

Article

Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes



Péter Lénárt1, Gwénaël Rabut1, Nathalie Daigle1, Arthur R. Hand2, Mark Terasaki2,3 and Jan Ellenberg1

1 Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory (EMBL), D-69117 Heidelberg, Germany
2 University of Connecticut Health Center, Farmington, CT 06030
3 Marine Biological Laboratory, Woods Hole, MA 02543

Address correspondence to Jan Ellenberg, Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, D-69117 Heidelberg, Germany. Tel.: (49) 6221-387-328. Fax: (49) 6221-387-518. E-mail: jan.ellenberg{at}embl-heidelberg.de

Breakdown of the nuclear envelope (NE) was analyzed in live starfish oocytes using a size series of fluorescently labeled dextrans, membrane dyes, and GFP-tagged proteins of the nuclear pore complex (NPC) and the nuclear lamina. Permeabilization of the nucleus occurred in two sequential phases. In phase I the NE became increasingly permeable for molecules up to ~40 nm in diameter, concurrent with a loss of peripheral nuclear pore components over a time course of 10 min. The NE remained intact on the ultrastructural level during this time. In phase II the NE was completely permeabilized within 35 s. This rapid permeabilization spread as a wave from one epicenter on the animal half across the nuclear surface and allowed free diffusion of particles up to ~100 nm in diameter into the nucleus. While the lamina and nuclear membranes appeared intact at the light microscopic level, a fenestration of the NE was clearly visible by electron microscopy in phase II. We conclude that NE breakdown in starfish oocytes is triggered by slow sequential disassembly of the NPCs followed by a rapidly spreading fenestration of the NE caused by the removal of nuclear pores from nuclear membranes still attached to the lamina.

Key Words: meiosis; oocyte maturation; nuclear envelope; nuclear envelope breakdown; starfish oocyte

The online version of this paper contains supplemental material.

* Abbreviations used in this paper: INM, inner nuclear membrane; MBP, maltose binding protein; MPF, maturation promoting factor; MW, molecular weight; NE, nuclear envelope; NEBD, nuclear envelope breakdown; NPC, nuclear pore complex.


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