Phosphorylation of histone H3T6 by PKCβI controls demethylation at histone H3K4

Histone demethylation mechanisms The N-terminal tails of histones are subject to a variety of post-translational modifications; addition or removal of these marks by specific enzymes facilitates gene activation or silencing. Here, a mechanism is defined that modulates the activity of the dual specif...

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Published in:Nature (London) Vol. 464; no. 7289; pp. 792 - 796
Main Authors: Metzger, Eric, Imhof, Axel, Patel, Dharmeshkumar, Kahl, Philip, Hoffmeyer, Katrin, Friedrichs, Nicolaus, Müller, Judith M., Greschik, Holger, Kirfel, Jutta, Ji, Sujuan, Kunowska, Natalia, Beisenherz-Huss, Christian, Günther, Thomas, Buettner, Reinhard, Schüle, Roland
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01.04.2010
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ISSN:0028-0836, 1476-4687
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Summary:Histone demethylation mechanisms The N-terminal tails of histones are subject to a variety of post-translational modifications; addition or removal of these marks by specific enzymes facilitates gene activation or silencing. Here, a mechanism is defined that modulates the activity of the dual specificity histone demethylase LSD1 during androgen-dependent transcription. Androgen-dependent signalling through protein kinase C beta I leads to phosphorylation of a histone residue that prevents demethylation of an adjacent residue by LSD1. This mechanism may potentially be important in prostate cancer. The amino-terminal tails of histone proteins are subject to a variety of post-translational modifications; addition or removal of these 'marks' facilitates gene activation or silencing. Here, a mechanism is defined that modulates the activity of the dual-specificity histone demethylase LSD1 during androgen-dependent transcription. Androgen-dependent signalling through protein kinase C beta I leads to phosphorylation of a histone amino acid, which prevents demethylation of an adjacent amino acid by LSD1. Demethylation at distinct lysine residues in histone H3 by lysine-specific demethylase 1 (LSD1) causes either gene repression or activation 1 , 2 . As a component of co-repressor complexes, LSD1 contributes to target gene repression by removing mono- and dimethyl marks from lysine 4 of histone H3 (H3K4) 1 , 3 . In contrast, during androgen receptor (AR)-activated gene expression, LSD1 removes mono- and dimethyl marks from lysine 9 of histone H3 (H3K9) 2 . Yet, the mechanisms that control this dual specificity of demethylation are unknown. Here we show that phosphorylation of histone H3 at threonine 6 (H3T6) by protein kinase C beta I (PKCβ I , also known as PRKCβ) is the key event that prevents LSD1 from demethylating H3K4 during AR-dependent gene activation. In vitro , histone H3 peptides methylated at lysine 4 and phosphorylated at threonine 6 are no longer LSD1 substrates. In vivo , PKCβ I co-localizes with AR and LSD1 on target gene promoters and phosphorylates H3T6 after androgen-induced gene expression. RNA interference (RNAi)-mediated knockdown of PKCβ I abrogates H3T6 phosphorylation, enhances demethylation at H3K4, and inhibits AR-dependent transcription. Activation of PKCβ I requires androgen-dependent recruitment of the gatekeeper kinase protein kinase C (PKC)-related kinase 1 (PRK1) 4 . Notably, increased levels of PKCβ I and phosphorylated H3T6 (H3T6ph) positively correlate with high Gleason scores of prostate carcinomas, and inhibition of PKCβ I blocks AR-induced tumour cell proliferation in vitro and cancer progression of tumour xenografts in vivo . Together, our data establish that androgen-dependent kinase signalling leads to the writing of the new chromatin mark H3T6ph, which in consequence prevents removal of active methyl marks from H3K4 during AR-stimulated gene expression.
ISSN:0028-0836
1476-4687
DOI:10.1038/nature08839