Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina

Porntula Panorchan, Benjamin W. Schafer, Denis Wirtz, Yiider Tseng

Research output: Contribution to journalArticle

Abstract

In prophase cells, lamin B1 is the major component of the nuclear lamina, a filamentous network underlying the nucleoplasmic side of the nuclear membrane, whereas lamin A/C is dissociated from the scaffold. In vivo fluorescence microscopy studies have shown that, during the G2/M transition, the first gap in the nuclear envelope (NE) appears before lamin B1 disassembly and is caused by early spindle microtubules impinging on the NE. This result suggests that the mechanical tearing of the NE by microtubules plays a central role to the progression of mitosis. To investigate whether this microtubule-induced NE deformation is sufficient for NE breakdown, we assess the mechanical resilience of a reconstituted lamin B1 network. Quantitative rheological methods demonstrate that human lamin B1 filaments form stiff networks that can resist much greater deformations than those caused by microtubules impinging on the NE. Moreover, lamin B1 networks possess an elastic stiffness, which increases under tension, and an exceptional resilience against shear deformations. These results demonstrate that both mechanical tearing of the lamina and biochemical modification of lamin B1 filaments are required for NE breakdown.

Original languageEnglish (US)
Pages (from-to)43462-43467
Number of pages6
JournalJournal of Biological Chemistry
Volume279
Issue number42
DOIs
StatePublished - Oct 15 2004

Fingerprint

Nuclear Lamina
Nuclear Envelope
Microtubules
Lamin Type A
Fluorescence microscopy
Scaffolds
Prophase
Shear deformation
lamin B1
Fluorescence Microscopy
Stiffness
Mitosis
Membranes

ASJC Scopus subject areas

  • Biochemistry

Cite this

Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina. / Panorchan, Porntula; Schafer, Benjamin W.; Wirtz, Denis; Tseng, Yiider.

In: Journal of Biological Chemistry, Vol. 279, No. 42, 15.10.2004, p. 43462-43467.

Research output: Contribution to journalArticle

Panorchan, Porntula ; Schafer, Benjamin W. ; Wirtz, Denis ; Tseng, Yiider. / Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina. In: Journal of Biological Chemistry. 2004 ; Vol. 279, No. 42. pp. 43462-43467.
@article{43d290d4017643a08d55abed549be87b,
title = "Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina",
abstract = "In prophase cells, lamin B1 is the major component of the nuclear lamina, a filamentous network underlying the nucleoplasmic side of the nuclear membrane, whereas lamin A/C is dissociated from the scaffold. In vivo fluorescence microscopy studies have shown that, during the G2/M transition, the first gap in the nuclear envelope (NE) appears before lamin B1 disassembly and is caused by early spindle microtubules impinging on the NE. This result suggests that the mechanical tearing of the NE by microtubules plays a central role to the progression of mitosis. To investigate whether this microtubule-induced NE deformation is sufficient for NE breakdown, we assess the mechanical resilience of a reconstituted lamin B1 network. Quantitative rheological methods demonstrate that human lamin B1 filaments form stiff networks that can resist much greater deformations than those caused by microtubules impinging on the NE. Moreover, lamin B1 networks possess an elastic stiffness, which increases under tension, and an exceptional resilience against shear deformations. These results demonstrate that both mechanical tearing of the lamina and biochemical modification of lamin B1 filaments are required for NE breakdown.",
author = "Porntula Panorchan and Schafer, {Benjamin W.} and Denis Wirtz and Yiider Tseng",
year = "2004",
month = "10",
day = "15",
doi = "10.1074/jbc.M402474200",
language = "English (US)",
volume = "279",
pages = "43462--43467",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "42",

}

TY - JOUR

T1 - Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina

AU - Panorchan, Porntula

AU - Schafer, Benjamin W.

AU - Wirtz, Denis

AU - Tseng, Yiider

PY - 2004/10/15

Y1 - 2004/10/15

N2 - In prophase cells, lamin B1 is the major component of the nuclear lamina, a filamentous network underlying the nucleoplasmic side of the nuclear membrane, whereas lamin A/C is dissociated from the scaffold. In vivo fluorescence microscopy studies have shown that, during the G2/M transition, the first gap in the nuclear envelope (NE) appears before lamin B1 disassembly and is caused by early spindle microtubules impinging on the NE. This result suggests that the mechanical tearing of the NE by microtubules plays a central role to the progression of mitosis. To investigate whether this microtubule-induced NE deformation is sufficient for NE breakdown, we assess the mechanical resilience of a reconstituted lamin B1 network. Quantitative rheological methods demonstrate that human lamin B1 filaments form stiff networks that can resist much greater deformations than those caused by microtubules impinging on the NE. Moreover, lamin B1 networks possess an elastic stiffness, which increases under tension, and an exceptional resilience against shear deformations. These results demonstrate that both mechanical tearing of the lamina and biochemical modification of lamin B1 filaments are required for NE breakdown.

AB - In prophase cells, lamin B1 is the major component of the nuclear lamina, a filamentous network underlying the nucleoplasmic side of the nuclear membrane, whereas lamin A/C is dissociated from the scaffold. In vivo fluorescence microscopy studies have shown that, during the G2/M transition, the first gap in the nuclear envelope (NE) appears before lamin B1 disassembly and is caused by early spindle microtubules impinging on the NE. This result suggests that the mechanical tearing of the NE by microtubules plays a central role to the progression of mitosis. To investigate whether this microtubule-induced NE deformation is sufficient for NE breakdown, we assess the mechanical resilience of a reconstituted lamin B1 network. Quantitative rheological methods demonstrate that human lamin B1 filaments form stiff networks that can resist much greater deformations than those caused by microtubules impinging on the NE. Moreover, lamin B1 networks possess an elastic stiffness, which increases under tension, and an exceptional resilience against shear deformations. These results demonstrate that both mechanical tearing of the lamina and biochemical modification of lamin B1 filaments are required for NE breakdown.

UR - http://www.scopus.com/inward/record.url?scp=6344282993&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=6344282993&partnerID=8YFLogxK

U2 - 10.1074/jbc.M402474200

DO - 10.1074/jbc.M402474200

M3 - Article

C2 - 15292200

AN - SCOPUS:6344282993

VL - 279

SP - 43462

EP - 43467

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 42

ER -