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A Class II Histone Deacetylase Acts on Newly Synthesized Histones in Tetrahymena

Joshua J. Smith, Sharon E. Torigoe, Julia Maxson, Lisa C. Fish, and Emily A. Wiley^*

Joint Science Department, Claremont McKenna, Scripps, and Pitzer Colleges, Claremont, California 91711

Received 7 November 2007/ Accepted 19 December 2007

Newly synthesized histones are acetylated prior to their deposition into nucleosomes. Following nucleosome formation and positioning, they are rapidly deacetylated, an event that coincides with further maturation of the chromatin fiber. The histone deacetylases (HDACs) used for histone deposition and de novo chromatin formation are poorly understood. In the ciliate Tetrahymena thermophila, transcription-related deacetylation in the macronucleus is physically separated from deposition-related deacetylation in the micronucleus. This feature was utilized to identify an HDAC named Thd2, a class II HDAC that acts on newly synthesized histones to remove deposition-related acetyl moieties. The THD2 transcript is alternatively spliced, and the major form contains a putative inositol polyphosphate kinase (IPK) domain similar to Ipk2, an enzyme that promotes chromatin remodeling by SWI/SNF remodeling complexes. Cells lacking Thd2, which retain deposition-related acetyl moieties on new histones, exhibit chromatin and cytological phenotypes indicative of a role for Thd2 in chromatin maturation, including the proteolytic processing of histone H3.

Published ahead of print on 4 January 2008.

Present address: Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093.

Present address: Department of Cell and Developmental Biology, Oregon Health and Science University, Portland, OR 97219.

Present address: Fred Hutchinson Cancer Research Center, Seattle, WA 98109.