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Published 10 December 2001. doi:10.1083/jcb.200105026
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© The Rockefeller University Press, 0021-9525/2001/12/899 $5.00
The Journal of Cell Biology, Volume 155, Number 6, December 10, 2001 899-910

Article

Cation–chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes



Reiner Strick1, Pamela L. Strissel1, Konstantin Gavrilov2 and Riccardo Levi-Setti2

1 Division of Biological Sciences, Department of Medicine
2 Division of Physical Sciences, Enrico Fermi Institute and Department of Physics, University of Chicago, Chicago, IL 60637

Address correspondence to Reiner Strick, Dept. of Medicine, University of Chicago, 5841 S. Maryland Ave., MC2115, Chicago, IL 60637-1470. Tel.: (773) 834-1539. Fax: (773) 702-3002. E-mail: rstrick{at}medicine.bsd.uchicago.edu

Mammalian interphase and mitotic cells were analyzed for their cation composition using a three-dimensional high resolution scanning ion microprobe. This instrument maps the distribution of bound and unbound cations by secondary ion mass spectrometry (SIMS). SIMS analysis of cryofractured interphase and mitotic cells revealed a cell cycle dynamics of Ca2+, Mg2+, Na+, and K+. Direct analytical images showed that all four, but no other cations, were detected on mitotic chromosomes. SIMS measurements of the total cation content for diploid chromosomes imply that one Ca2+ binds to every 12.5–20 nucleotides and one Mg2+ to every 20–30 nucleotides. Only Ca2+ was enriched at the chromosomal DNA axis and colocalized with topoisomerase II{alpha} (Topo II) and scaffold protein II (ScII). Cells depleted of Ca2+ and Mg2+ showed partially decondensed chromosomes and a loss of Topo II and ScII, but not hCAP-C and histones. The Ca2+-induced inhibition of Topo II catalytic activity and direct binding of Ca2+ to Topo II by a fluorescent filter-binding assay supports a regulatory role of Ca2+ during mitosis in promoting solely the structural function of Topo II. Our study directly implicates Ca2+, Mg2+, Na+, and K+ in higher order chromosome structure through electrostatic neutralization and a functional interaction with nonhistone proteins.

Key Words: cations; chromosome structure; condensation; ion microscopy; topoisomerase II


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