Abstract
Histone deacetylases such as human HDAC1 and yeast RPD3 are trichostatin A (TSA)-sensitive enzymes that are members of large, multiprotein complexes. These contain specialized subunits that help target the catalytic protein to histones at the appropriate DNA regulatory element, where the enzyme represses transcription. To date, no deacetylase catalytic subunits have been shown to have intrinsic activity, suggesting that noncatalytic subunits of the deacetylase complex are required for their enzymatic function. In this paper we describe a novel yeast histone deacetylase HOS3 that is relatively insensitive to the histone deacetylase inhibitor TSA, forms a homodimer when expressed ectopically both in yeast and Escherichia coli, and has intrinsic activity when produced in the bacterium. Most HOS3 protein can be found associated with a larger complex in partially purified yeast nuclear extracts, arguing that the HOS3 homodimer may be dissociated from a very large nuclear structure during purification. We also demonstrate, using a combination of mass spectrometry, tandem mass spectrometry, and proteolytic digestion, that recombinant HOS3 has a distinct specificity in vitro for histone H4 sites K5 and K8, H3 sites K14 and K23, H2A site K7, and H2B site K11. We propose that while factors that interact with HOS3 may sequester the catalytic subunit at specific cellular sites, they are not required for HOS3 histone deacetylase activity.
MeSH Terms
Amino Acid Sequence
Base Sequence
Cloning, Molecular
DNA Primers
Dimerization
Fungal Proteins/chemistry,genetics,metabolism
Histone Deacetylases/genetics,metabolism
Humans
Hydroxamic Acids/pharmacology
Molecular Sequence Data
Recombinant Proteins/chemistry,genetics,metabolism
Saccharomyces cerevisiae/metabolism
Chemicals
DNA Primers
Fungal Proteins
Hydroxamic Acids
Recombinant Proteins
trichostatin A
Histone Deacetylases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Carmen A A
Department of Biological Chemistry, UCLA School of Medicine, University of California, Los Angeles, CA 90095, USA.
Griffin P R
Calaycay J R
Rundlett S E
Suka Y
Grunstein M
References (30)
30 references, click to expand
-
The highly conserved amino-terminal region of the protein encoded by the v-myb oncogene functions as a DNA-binding domain.
EMBO J. 1987 Sep;6(9):2719-25
PMID: 2824190
-
The regulation of gene activity by histones and the histone deacetylase RPD3.
Cold Spring Harb Symp Quant Biol. 1998;63:391-9
PMID: 10384304
-
A bipartite DNA-binding domain in yeast Reb1p.
Mol Cell Biol. 1993 Feb;13(2):1173-82
PMID: 8423784
-
Disturbance of normal cell cycle progression enhances the establishment of transcriptional silencing in Saccharomyces cerevisiae.
Mol Cell Biol. 1995 Jul;15(7):3608-17
PMID: 7791768
-
A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.
Science. 1996 Apr 19;272(5260):408-11
PMID: 8602529
-
HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex.
J Biol Chem. 1996 Jun 28;271(26):15837-44
PMID: 8663039
-
Spreading of transcriptional repressor SIR3 from telomeric heterochromatin.
Nature. 1996 Sep 5;383(6595):92-6
PMID: 8779721
-
Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase.
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13143-7
PMID: 8917558
-
HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription.
Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14503-8
PMID: 8962081
-
A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression.
Nature. 1997 May 1;387(6628):43-8
PMID: 9139820
-
Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression.
Nature. 1997 May 1;387(6628):49-55
PMID: 9139821
-
Histone deacetylase activity is required for full transcriptional repression by mSin3A.
Cell. 1997 May 2;89(3):341-7
PMID: 9150133
-
Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression.
Cell. 1997 May 2;89(3):349-56
PMID: 9150134
-
Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex.
Cell. 1997 May 2;89(3):357-64
PMID: 9150135
-
Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters.
Cell. 1997 May 2;89(3):365-71
PMID: 9150136
-
Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase.
Cell. 1997 May 2;89(3):373-80
PMID: 9150137
-
Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex.
Genes Dev. 1997 Jul 1;11(13):1640-50
PMID: 9224714
-
A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators.
Mol Cell Biol. 1997 Aug;17(8):4852-8
PMID: 9234741
-
Crystal structure of the nucleosome core particle at 2.8 A resolution.
Nature. 1997 Sep 18;389(6648):251-60
PMID: 9305837
-
Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase.
Curr Biol. 1998 Jan 15;8(2):96-108
PMID: 9427644
-
Distinct requirements for chromatin assembly in transcriptional repression by thyroid hormone receptor and histone deacetylase.
EMBO J. 1998 Jan 15;17(2):520-34
PMID: 9430643
-
Retinoblastoma protein recruits histone deacetylase to repress transcription.
Nature. 1998 Feb 5;391(6667):597-601
PMID: 9468139
-
Retinoblastoma protein represses transcription by recruiting a histone deacetylase.
Nature. 1998 Feb 5;391(6667):601-5
PMID: 9468140
-
Rb interacts with histone deacetylase to repress transcription.
Cell. 1998 Feb 20;92(4):463-73
PMID: 9491888
-
ESA1 is a histone acetyltransferase that is essential for growth in yeast.
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3561-5
PMID: 9520405
-
A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase.
Curr Biol. 1998 Jul 2;8(14):843-6
PMID: 9663395
-
A histone deacetylase corepressor complex regulates the Notch signal transduction pathway.
Genes Dev. 1998 Aug 1;12(15):2269-77
PMID: 9694793
-
The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities.
Cell. 1998 Oct 16;95(2):279-89
PMID: 9790534
-
Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex.
Nature. 1998 Oct 29;395(6705):917-21
PMID: 9804427
-
Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A.
J Biol Chem. 1990 Oct 5;265(28):17174-9
PMID: 2211619