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Molecular and Cellular Biology, January 2007, p. 709-720, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01627-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Ctk Complex-Mediated Regulation of Histone Methylation by COMPASS{triangledown}

Adam Wood,1,{dagger} Abhijit Shukla,2,{dagger} Jessica Schneider,1 Jung Shin Lee,1 Julie D. Stanton,3 Tiffany Dzuiba,1 Selene K. Swanson,4 Laurence Florens,4 Michael P. Washburn,4 John Wyrick,3 Sukesh R. Bhaumik,2 and Ali Shilatifard1,5*

Department of Biochemistry, Saint Louis University School of Medicine, 1402 South Grand Blvd., St. Louis, Missouri 63104,1 Department of Biochemistry and Molecular Biology, Southern Illinois University School of Medicine, 1245 Lincoln Drive, Carbondale, Illinois 62901,2 School of Molecular Biosciences, Washington State University, Pullman, Washington 99164,3 Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, Missouri 64110,4 Saint Louis University Cancer Center, Saint Louis University School of Medicine, St. Louis, Missouri 631045

Received 31 August 2006/ Returned for modification 5 October 2006/ Accepted 24 October 2006

A comparative global proteomic screen identified factors required for COMPASS (complex of proteins associated with Set1)-mediated mono-, di-, and trimethylation of the fourth lysine of histone H3 (H3K4), which included components of a cyclin-dependent protein kinase (Ctk complex) that phosphorylates the C-terminal domain of the largest subunit of RNA polymerase II (Pol II). Our results indicate that histone H3K4 methylation levels are regulated by the Ctk1, Ctk2, and Ctk3 components of the Ctk complex. We show that loss of Ctk1 kinase activity results in reduced histone H3K4 monomethylation levels, followed by a global increase in histone H3K4 trimethylation levels on chromatin. Ctk1 loss does not appear to have a substantial effect on histone H2B monoubiquitination levels or COMPASS and Paf1 complex phosphorylation. Our chromatin immunoprecipitation studies demonstrate that histone H3 eviction during active transcription is decelerated in a CTK1 deletion strain in response to reduced levels of Pol II recruitment. Our in vitro studies show that the onset of monomethylation on an unmethylated histone H3 by COMPASS is virtually immediate, while the onset of trimethylation occurs upon extended time of association between the histone tail and COMPASS. Our study suggests a role for the Ctk complex in the regulation of the pattern of H3K4 mono-, di-, and trimethylation via COMPASS.

* Corresponding author. Mailing address: Saint Louis University School of Medicine, Department of Biochemistry, 1402 South Grand Blvd., St. Louis, MO 63104. Phone: (314) 977-9228. Fax: (314) 977-5737. E-mail: shilatia{at}slu.edu.

{triangledown} Published ahead of print on 6 November 2006.

{dagger} A.W. and A.S. contributed equally to this report.

Molecular and Cellular Biology, January 2007, p. 709-720, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01627-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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