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The Journal of Neuroscience, October 1, 2000, 20(19):7317-7324

The Architectural Transcription Factor High Mobility Group I(Y) Participates in Photoreceptor-Specific Gene Expression

Kai-Yin Chau¹, Nikhil Munshi², Andrea Keane-Myers¹, Kam-Wa Cheung-Chau¹, Albert Kwong-Fuk Tai¹, Guidalberto Manfioletti³, C. Kathleen Dorey¹, Dimitris Thanos², Donald J. Zack⁴, and Santa Jeremy Ono¹

¹ The Schepens Eye Research Institute, Harvard Medical School, Boston, Massachusetts 02114, ² Department of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, ³ Dipartimento di Biochimica, Biofisica e Chimica delle Macromolecole, Universita di Trieste, I-34127 Trieste, Italy, and ⁴ Departments of Ophthalmology, Molecular Biology and Genetics, and Neuroscience, Johns Hopkins School of Medicine, Baltimore, Maryland 21287

The nonhistone chromosomal proteins high mobility group I(Y) [HMG I(Y)] have been shown to function as architectural transcription factors facilitating enhanceosome formation on a variety of mammalian promoters. Specifically, they have been shown to act as a "molecular glue" mediating protein-protein and protein-DNA contacts within the enhanceosome complex. HMG I(Y) proteins are expressed at high levels in embryonic and transformed cells and have been implicated in transcriptional regulation in these cells. Terminally differentiated cells, however, have been reported to express only minimal, if any, HMG I(Y). In contrast to these observations, we show here that adult mouse retinal photoreceptors, which are terminally differentiated cells, express high levels of these proteins. Using retinoblastoma cells as an approximate model, we further demonstrate in transiently transfected cells that inhibition of HMG I(Y) expression and mutation of HMG I(Y) binding sites significantly reduce rhodopsin promoter activity. DNase I footprint analysis indicates that HMG I protein interacts with a discrete site within the rhodopsin proximal promoter. This site overlaps with the binding site for Crx, a paired-like homeodomain transcription factor that is essential for photoreceptor functioning and that when mutated causes several forms of human photoreceptor degeneration. Both biochemical and functional experiments demonstrate that HMG I(Y) physically associate with Crx and that their interaction with DNA is required for high-level transcription of the rhodopsin gene. These data provide the first demonstration that HMG I(Y) can be important for gene activation in terminally differentiated cells.

Key words: HMG I(Y); Crx; rhodopsin; retinoblastoma; retina; photoreceptors

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20197317-08$05.00/0

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