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J. Biol. Chem., Vol. 279, Issue 42, 43462-43467, October 15, 2004

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Nuclear Envelope Breakdown Requires Overcoming the Mechanical Integrity of the Nuclear Lamina^*

Porntula Panorchan, Benjamin W. Schafer, Denis Wirtz¶||, and Yiider Tseng**

From the Departments of Chemical and Biomolecular Engineering, Civil Engineering, and ^¶Materials Science and Engineering, The Johns Hopkins University, Baltimore, Maryland 21218

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.

Received for publication, May 4, 2004 , and in revised form, July 7, 2004.

^* This work was funded by National Science Foundation Grants NIRT CTS0210718 (to D. W.) and DMII-0228246 (to B. W. S.) and NASA Grant NAG9–1563 (to D. W. and Y. T.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains additional information and Supplemental Figs. 1–3.

^|| To whom correspondence may be addressed: Dept. of Chemical and Biomolecular Engineering, The Johns Hopkins University, 3400 N. Charles St., Baltimore, MD 21218. Tel.: 410-516-7006; Fax: 410-516-5510; E-mail: wirtz{at}jhu.edu. ** To whom correspondence may be addressed: Dept. of Chemical and Biomolecular Engineering, The Johns Hopkins University, 3400 N. Charles St., Baltimore, MD 21218. Tel.: 410-516-5287; Fax: 410-516-5510; E-mail: yiider{at}jhu.edu.

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