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

Lénárt P, Rabut G, Daigle N, Hand AR, Terasaki M, Ellenberg J - J. Cell Biol. (2003)

Bottom Line: 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 approximately 100 nm in diameter into the nucleus.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.

View Article: PubMed Central - PubMed

Affiliation: Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany.

ABSTRACT
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 approximately 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 approximately 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.

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Model for phase I and II of NEBD. (Top) cross section of the NE through the center of an NPC. (Bottom) top view from the cytoplasmic side of the NE. Lamina, dark gray; nuclear membranes, transparent gray; NPC, middle gray; permeability barrier of NPC, light gray. The channel diameter indicated by dashed lines corresponds to the apparent diffusion channel calculated from dextran fluxes. (A) immature oocytes, (B) phase I oocytes, (C) phase II oocytes. Bar, 50 nm.
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fig8: Model for phase I and II of NEBD. (Top) cross section of the NE through the center of an NPC. (Bottom) top view from the cytoplasmic side of the NE. Lamina, dark gray; nuclear membranes, transparent gray; NPC, middle gray; permeability barrier of NPC, light gray. The channel diameter indicated by dashed lines corresponds to the apparent diffusion channel calculated from dextran fluxes. (A) immature oocytes, (B) phase I oocytes, (C) phase II oocytes. Bar, 50 nm.

Mentions: Phase I of NEBD lasted for ∼10 min and was characterized by the gradual entry of macromolecules between 20 and 40 nm diameter into the nucleus. Our observations are best explained by a model in which the sequential loss of peripheral nucleoporins from NPCs continuously increases their permeability until only an “empty” core channel embedded in the otherwise intact NE is left behind (Fig. 8, A and B).


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

Lénárt P, Rabut G, Daigle N, Hand AR, Terasaki M, Ellenberg J - J. Cell Biol. (2003)

Model for phase I and II of NEBD. (Top) cross section of the NE through the center of an NPC. (Bottom) top view from the cytoplasmic side of the NE. Lamina, dark gray; nuclear membranes, transparent gray; NPC, middle gray; permeability barrier of NPC, light gray. The channel diameter indicated by dashed lines corresponds to the apparent diffusion channel calculated from dextran fluxes. (A) immature oocytes, (B) phase I oocytes, (C) phase II oocytes. Bar, 50 nm.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172766&req=5

fig8: Model for phase I and II of NEBD. (Top) cross section of the NE through the center of an NPC. (Bottom) top view from the cytoplasmic side of the NE. Lamina, dark gray; nuclear membranes, transparent gray; NPC, middle gray; permeability barrier of NPC, light gray. The channel diameter indicated by dashed lines corresponds to the apparent diffusion channel calculated from dextran fluxes. (A) immature oocytes, (B) phase I oocytes, (C) phase II oocytes. Bar, 50 nm.
Mentions: Phase I of NEBD lasted for ∼10 min and was characterized by the gradual entry of macromolecules between 20 and 40 nm diameter into the nucleus. Our observations are best explained by a model in which the sequential loss of peripheral nucleoporins from NPCs continuously increases their permeability until only an “empty” core channel embedded in the otherwise intact NE is left behind (Fig. 8, A and B).

Bottom Line: 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 approximately 100 nm in diameter into the nucleus.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.

View Article: PubMed Central - PubMed

Affiliation: Gene Expression and Cell Biology/Biophysics Programmes, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany.

ABSTRACT
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 approximately 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 approximately 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.

Show MeSH
Related in: MedlinePlus