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Published 3 July 2006. doi:10.1083/jcb.200603083
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 174, Number 1, 27-38
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Article

Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence



Lindsay S. Shopland1,2, Christopher R. Lynch1,2, Kevin A. Peterson1,3, Kathleen Thornton3, Nick Kepper4, Johann von Hase2,4, Stefan Stein4, Sarah Vincent3, Kelly R. Molloy1,5, Gregor Kreth4, Christoph Cremer1,2,4, Carol J. Bult1, and Timothy P. O'Brien1,2

1 The Jackson Laboratory, Bar Harbor, ME 04609
2 Institute for Molecular Biophysics and 3 Program in Functional Genomics, University of Maine, Orono, ME 04469
4 Kirchhoff Institute for Physics, University of Heidelberg, D-69120 Germany
5 Department of Physics, Brown University, Providence, RI 02912

Correspondence to Lindsay S. Shopland: lindsay.shopland{at}jax.org; or Timothy P. O'Brien: tpo5{at}cornell.edu

Specific mammalian genes functionally and dynamically associate together within the nucleus. Yet, how an array of many genes along the chromosome sequence can be spatially organized and folded together is unknown. We investigated the 3D structure of a well-annotated, highly conserved 4.3-Mb region on mouse chromosome 14 that contains four clusters of genes separated by gene "deserts." In nuclei, this region forms multiple, nonrandom "higher order" structures. These structures are based on the gene distribution pattern in primary sequence and are marked by preferential associations among multiple gene clusters. Associating gene clusters represent expressed chromatin, but their aggregation is not simply dependent on ongoing transcription. In chromosomes with aggregated gene clusters, gene deserts preferentially align with the nuclear periphery, providing evidence for chromosomal region architecture by specific associations with functional nuclear domains. Together, these data suggest dynamic, probabilistic 3D folding states for a contiguous megabase-scale chromosomal region, supporting the diverse activities of multiple genes and their conserved primary sequence organization.

K.A. Peterson and T.P. O'Brien's present address is the Dept. of Biomedical Sciences, Cornell University, Ithaca, NY 14853.

Abbreviations used in this paper: BAC, bacterial artificial chromosome; DRB, 5,6-dichlorobenzimidazole riboside; ES, embryonic stem; Mmu, Mus musculus; KS, Kolmogorov-Smirnov; pol II, RNA polymerase II.


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