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Published 13 September 2004. doi:10.1083/jcb.200404107
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 6, 815-825
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Article

Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei



Daniele Zink1, Margarida D. Amaral2,3, Andreas Englmann1, Susanne Lang1, Luka A. Clarke2, Carsten Rudolph4, Felix Alt1, Kathrin Luther1, Carla Braz2, Nicolas Sadoni1, Joseph Rosenecker4, and Dirk Schindelhauer5,6

1 Ludwig Maximilians University Munich, Department of Biology II, 80336 Munich, Germany
2 Department of Chemistry and Biochemistry, Faculty of Sciences, University of Lisboa, 1749-016 Lisboa, Portugal
3 Center of Human Genetics, National Institute of Health, 1649-016 Lisboa, Portugal
4 Ludwig Maximilians University Munich, Division of Molecular Pulmonology, Department of Pediatrics, 80337 Munich, Germany
5 Technical University of Munich, Institute of Human Genetics, 81675 Munich, Germany
6 Life Science Center Weihenstephan, 85354 Freising, Germany

Address correspondence to D. Zink, Ludwig Maximilians University Munich, Department of Biology II, Grosshaderner Str. 2, 82152 Planegg-Martinstried, Germany. Tel.: (49) 89-2180-74133. Fax: (49) 89-2180-75618. email: Dani.Zink{at}lrz.uni-muenchen.de

We investigated in different human cell types nuclear positioning and transcriptional regulation of the functionally unrelated genes GASZ, CFTR, and CORTBP2, mapping to adjacent loci on human chromosome 7q31. When inactive, GASZ, CFTR, and CORTBP2 preferentially associated with the nuclear periphery and with perinuclear heterochromatin, whereas in their actively transcribed states the gene loci preferentially associated with euchromatin in the nuclear interior. Adjacent genes associated simultaneously with these distinct chromatin fractions localizing at different nuclear regions, in accordance with their individual transcriptional regulation. Although the nuclear localization of CFTR changed after altering its transcription levels, the transcriptional status of CFTR was not changed by driving this gene into a different nuclear environment. This implied that the transcriptional activity affected the nuclear positioning, and not vice versa. Together, the results show that small chromosomal subregions can display highly flexible nuclear organizations that are regulated at the level of individual genes in a transcription-dependent manner.

Key Words: CFTR; nuclear architecture; gene positioning; chromatin organization; chromosome territory

S. Lang's present address is Max Planck Institute for Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany.

K. Luther's present address is Max von Pettenkofer Institute, 80336 Munich, Germany.

Abbreviations used in this paper: 3D, three-dimensional; CFTR, cystic fibrosis transmembrane conductance regulator; CORTBP2, cortactin-binding protein 2; DRB, 5,6-dichlorobenzimidazole riboside; GASZ, germ cell–specific expression, presence of ANK, SAM, and basic leucine zipper domains; H4Ac8, H4 acetylated at lysine 8; LAP2ß, lamina-associated polypeptide 2ß; TSA, trichostatin A.


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