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Published online 7 September 2004. doi:10.1083/jcb.200406049
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 6, 775-785
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Article

Visualization of early chromosome condensation

: a hierarchical folding, axial glue model of chromosome structure



Natashe Kireeva1, Margot Lakonishok1, Igor Kireev1, Tatsuya Hirano2, and Andrew S. Belmont1

1 Department of Cell and Structural Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801
2 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724

Address correspondence to Andrew S. Belmont, Dept. of Cell and Structural Biology, University of Illinois at Urbana-Champaign, B107 CLSL, 601 S. Goodwin Ave., Urbana, IL 61801. Tel.: (217) 244-2311. Fax: (217) 244-1648. email: asbel{at}uiuc.edu

Current models of mitotic chromosome structure are based largely on the examination of maximally condensed metaphase chromosomes. Here, we test these models by correlating the distribution of two scaffold components with the appearance of prophase chromosome folding intermediates. We confirm an axial distribution of topoisomerase II{alpha} and the condensin subunit, structural maintenance of chromosomes 2 (SMC2), in unextracted metaphase chromosomes, with SMC2 localizing to a 150–200-nm-diameter central core. In contrast to predictions of radial loop/scaffold models, this axial distribution does not appear until late prophase, after formation of uniformly condensed middle prophase chromosomes. Instead, SMC2 associates throughout early and middle prophase chromatids, frequently forming foci over the chromosome exterior. Early prophase condensation occurs through folding of large-scale chromatin fibers into condensed masses. These resolve into linear, 200–300-nm-diameter middle prophase chromatids that double in diameter by late prophase. We propose a unified model of chromosome structure in which hierarchical levels of chromatin folding are stabilized late in mitosis by an axial "glue."

Key Words: chromosome structure; condensins; topoisomerase II; mitosis; SMC

N. Kireeva and I. Kereev's present address is Department of Electron Microscopy, A.N. Belozersky Institute for Physical Chemical Biology, Moscow State University, Moscow 119899, Russia.

Abbreviations used in this paper: SMC2, structural maintenance of chromosomes 2; TEM, transmission electron microscopy.


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