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J. Biol. Chem., Vol. 279, Issue 7, 5118-5126, February 13, 2004

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The Mitotic Chromosome Is an Assembly of Rigid Elastic Axes Organized by Structural Maintenance of Chromosomes (SMC) Proteins and Surrounded by a Soft Chromatin Envelope^*

Sébastien Almagro, Daniel Riveline¶, Tatsuya Hirano||, Bahram Houchmandzadeh¶, and Stefan Dimitrov**

From the Laboratoire de Biologie Moléculaire et Cellulaire de la Différenciation, INSERM U309, Institut Albert Bonniot, Domaine de la Merci, 38706 La Tronche Cedex, France, the ^¶Laboratoire de Spectrométrie Physique, UMR 5588, Université Joseph Fourier, 38402 Saint-Martin d'Hères, France, and the ^||Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724

The structure of mitotic chromosomes is still poorly understood. Here we describe the use of a novel approach based on elasticity measurements of a single chromosome for studying the organization of these objects. The data reveal that mitotic chromosomes exhibit a non-homogenous structure consisting of rigid elastic axes surrounded by a soft chromatin envelope. The chemical continuity of DNA, but not RNA, was required for the maintenance of these axes. The axes show a modular structure, and the structural maintenance of chromosomes (SMC) proteins participate in their organization. Topoisomerase II was not involved in either the organization of the axes or the maintenance of the mitotic chromosomes. A model for the assembly and the structure of the mitotic chromosome is proposed. According this model, the chromosome axes are dynamic structures that assemble at the onset and disassemble the end of mitosis, respectively. The SMC proteins, in addition to maintaining axis elasticity, are essential for the determination of the rod-like chromosome shape. The extreme compaction of mitotic chromosomes is determined mainly by the high amount of bivalent ions bound to DNA at mitosis.

Received for publication, July 7, 2003 , and in revised form, November 24, 2003.

^* This work was supported by CNRS and INSERM. 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.

Supported by La Ligue contre le Cancer and the Association pour la Recherche sur le Cancer (ARC).

^** To whom correspondence should be addressed. Tel.: 33-4-76-54-94-73; Fax: 33-4-76-54-95-95; E-mail: stefan.dimitrov{at}ujf-grenoble.fr.

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