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© The Rockefeller University Press, 0021-9525/2003/9/981 $5.00
The Journal of Cell Biology, Volume 162, Number 6, 981-990

Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains

Lindsay S. Shopland, Carol V. Johnson, Meg Byron, John McNeil and Jeanne B. Lawrence

Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01655

Address correspondence to Jeanne Lawrence, Dept. of Cell Biology, University of Massachusetts Medical Center, 55 Lake Avenue North, Worcester, MA 01655. Tel.: (508) 856-6015. Fax: (508) 856-5178. email: jeanne.lawrence{at}umassmed.edu

Typically, eukaryotic nuclei contain 10–30 prominent domains (referred to here as SC-35 domains) that are concentrated in mRNA metabolic factors. Here, we show that multiple specific genes cluster around a common SC-35 domain, which contains multiple mRNAs. Nonsyntenic genes are capable of associating with a common domain, but domain "choice" appears random, even for two coordinately expressed genes. Active genes widely separated on different chromosome arms associate with the same domain frequently, assorting randomly into the 3–4 subregions of the chromosome periphery that contact a domain. Most importantly, visualization of six individual chromosome bands showed that large genomic segments (5 Mb) have striking differences in organization relative to domains. Certain bands showed extensive contact, often aligning with or encircling an SC-35 domain, whereas others did not. All three gene-rich reverse bands showed this more than the gene-poor Giemsa dark bands, and morphometric analyses demonstrated statistically significant differences. Similarly, late-replicating DNA generally avoids SC-35 domains. These findings suggest a functional rationale for gene clustering in chromosomal bands, which relates to nuclear clustering of genes with SC-35 domains. Rather than random reservoirs of splicing factors, or factors accumulated on an individual highly active gene, we propose a model of SC-35 domains as functional centers for a multitude of clustered genes, forming local euchromatic "neighborhoods."

Key Words: cell nucleus; chromosome banding; genome; splicing factor SC-35; chromosome structure

L.S. Shopland's present address is The Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609.

Abbreviations used in this paper: ACTB, ß-actin; COL1A1, collagen type 1, 1; COL1A2, collagen type 1, 2; G-band, Giemsa dark band; R-band, reverse band.

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