Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1).
Journal: 2002/February - Molecular and Cellular Biology
ISSN: 0270-7306
PUBMED: 11784859
Abstract:
Sin3 is an evolutionarily conserved corepressor that exists in different complexes with the histone deacetylases HDAC1 and HDAC2. Sin3-HDAC complexes are believed to deacetylate nucleosomes in the vicinity of Sin3-regulated promoters, resulting in a repressed chromatin structure. We have previously found that a human Sin3-HDAC complex includes HDAC1 and HDAC2, the histone-binding proteins RbAp46 and RbAp48, and two novel polypeptides SAP30 and SAP18. SAP30 is a specific component of Sin3 complexes since it is absent in other HDAC1/2-containing complexes such as NuRD. SAP30 mediates interactions with different polypeptides providing specificity to Sin3 complexes. We have identified p33ING1b, a negative growth regulator involved in the p53 pathway, as a SAP30-associated protein. Two distinct Sin3-p33ING1b-containing complexes were isolated, one of which associates with the subunits of the Brg1-based Swi/Snf chromatin remodeling complex. The N terminus of p33ING1b, which is divergent among a family of ING1 polypeptides, associates with the Sin3 complex through direct interaction with SAP30. The N-terminal domain of p33 is present in several uncharacterized human proteins. We show that overexpression of p33ING1b suppresses cell growth in a manner dependent on the intact Sin3-HDAC-interacting domain.
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Mol Cell Biol 22(3): 835-848

Role of the Sin3-Histone Deacetylase Complex in Growth Regulation by the Candidate Tumor Suppressor p33<sup>ING1</sup>

Howard Hughes Medical Institute, Division of Nucleic Acids Enzymology, Department of Biochemistry, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, Piscataway, New Jersey 08854, Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 100212
Corresponding author. Mailing address: Howard Hughes Medical Institute, Division of Nucleic Acids Enzymology, Department of Biochemistry, University of Medicine and Dentistry of New Jersey, Robert Wood Johnson Medical School, Piscataway, NJ 08854. Phone: (732) 235-4195. Fax: (732) 235-5294. E-mail: ude.jndmu@fdebnier.
Present Address: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.
Received 2001 Jul 3; Revised 2001 Aug 3; Accepted 2001 Oct 31.

Abstract

Sin3 is an evolutionarily conserved corepressor that exists in different complexes with the histone deacetylases HDAC1 and HDAC2. Sin3-HDAC complexes are believed to deacetylate nucleosomes in the vicinity of Sin3-regulated promoters, resulting in a repressed chromatin structure. We have previously found that a human Sin3-HDAC complex includes HDAC1 and HDAC2, the histone-binding proteins RbAp46 and RbAp48, and two novel polypeptides SAP30 and SAP18. SAP30 is a specific component of Sin3 complexes since it is absent in other HDAC1/2-containing complexes such as NuRD. SAP30 mediates interactions with different polypeptides providing specificity to Sin3 complexes. We have identified p33ING1b, a negative growth regulator involved in the p53 pathway, as a SAP30-associated protein. Two distinct Sin3-p33ING1b-containing complexes were isolated, one of which associates with the subunits of the Brg1-based Swi/Snf chromatin remodeling complex. The N terminus of p33ING1b, which is divergent among a family of ING1 polypeptides, associates with the Sin3 complex through direct interaction with SAP30. The N-terminal domain of p33 is present in several uncharacterized human proteins. We show that overexpression of p33ING1b suppresses cell growth in a manner dependent on the intact Sin3-HDAC-interacting domain.

Abstract

In eukaryotic cells, the DNA is packaged with histones in the form of chromatin (24). The primary unit of chromatin is the nucleosome, composed of 146 bp of DNA wrapped around an octamer of histone proteins (32). The packaging of DNA into chromatin allows for efficient storage of genetic information, although this compaction impedes the access of proteins to DNA. In the nucleus there are machineries that alter chromatin structure and aid proteins in gaining access to their DNA sites (reviewed in references 23 and 51). Types of activities that alter chromatin structure include ATP-dependent nucleosome remodeling and covalent modification of core histones, particularly acetylation-deacetylation of lysine residues and methylation of lysine and arginine residues. These covalent modifications occur primarily within the N-terminal histone tails (46, 61).

Several ATP-dependent nucleosome-remodeling factors have been characterized. These fall into two broad classes: the Swi-Snf and ISWI-related families. Two human complexes related to the yeast Swi-Snf complex. Brg1 and Brm, have been characterized (53, 54). These complexes contain a set of common as well as unique subunits, referred to as Brg1-associated factors (BAFs). Several ISWI-containing complexes have also been isolated from different species (reviewed in reference 50). These chromatin-remodeling complexes possess a DNA-stimulated ATPase activity that resides in the highly conserved Snf2-related subunit.

Different regions of the genome exhibit specific patterns of histone acetylation, which are established by the action of histone acetyltransferases and histone deacetylases (HDACs). Several histone acetyltransferases have been identified. Some of these histone acetylases exist in large complexes and participate in transcriptional activation. HDACs have also been identified. In mammals, there appear to be at least nine different HDACs: HDAC1, HDAC2, and HDAC3 are related to the yeast HDAC Rpd3, whereas HDAC4, HDAC5, HDAC6, HDAC7, HDAC8, and HDAC9 are related to the yeast HDA1 (reviewed in references 6 and 25). Recently, the yeast and mouse Sir2 proteins, which function in the establishment of silencing, were found to possess NAD-dependent HDAC activity in vitro (21, 29, 45). Some of these HDACs exist in large protein complexes and are directed to specific regions of the genome by interacting, directly or indirectly, with sequence-specific DNA-binding proteins. Yeast Sin3, and the Sin3-associated HDAC Rpd3, have been implicated in promoter-specific repression as well as in silencing (39, 47). Recruitment of the Sin3-Rpd3 complex to the promoter by the DNA-binding repressor Ume6 results in local deacetylation of two nucleosomes in the vicinity of the Ume6-binding site (39). Surprisingly, deletion of Saccharomyces cerevisiae SIN3, RPD3, and HDA1 leads to an increase rather than a loss of silencing (38, 47).

The human Sin3 protein was identified as a corepressor that interacts with the E-box-binding repressor complex Mad-Max (4, 41). Furthermore, interaction with Sin3 was found to be essential for Mad to suppress Myc-induced transformation (15). Subsequent studies revealed that Sin3 also interacts with N-CoR and SMRT (1, 16, 36), corepressors that bind to unliganded nuclear hormone receptors (5, 20).

Two major human HDAC1/2-containing complexes have been characterized biochemically in HeLa cells—Sin3 and NuRD (9, 5860, 62). Human Sin3 and NuRD complexes share a set of four polypeptides, a presumed catalytic core complex composed of HDAC1, HDAC2, and the histone-binding proteins RbAp46, and RbAp48 (60). In addition to these four polypeptides, a Sin3 complex contains mSIN3A, SAP30, and SAP18 (58). However, several other polypeptides are associated with Sin3-containing complexes, including the CpG-methylated binding protein MeCP2 (37), the Rb-binding protein RBP1 (28), and the corepressors NCoR and SMRT (1, 16, 36). The SAP30 subunit was found to interact with NCoR, SMRT, RBP1, and other polypeptides, suggesting that SAP30 may tether the core HDAC1/2 complex to different polypeptides (26, 62).

The NuRD complex provides an unexpected link between two chromatin-modifying activities. In addition to the HDAC core complex, it contains an ISWI-related polypeptide, CHD4 (Mi2β). CHD4 contains a SNF2-like helicase domain, which enables the NuRD complex to alter the structure of nucleosomes in an ATP-dependent manner. NuRD contains a nucleosome-stimulated ATPase activity. NuRD is able to deacetylate oligonucleosomal histones in vitro in a manner that is stimulated by ATP (49, 52, 55, 59). In light of this finding, it was proposed that access of the HDACs to histone tails in oligonucleosomes requires alteration and/or mobilization of nucleosome structure (49, 59).

In the present studies, we have analyzed polypeptides that associate with the Sin3 complex. We found that the p53-binding protein p33ING1b interacts with the Sin3 complex.

The p53-binding protein ING1 was identified in a genetic selection for genes whose inactivation can cause neoplastic transformation (12). Overexpression of p33ING1 inhibits cell growth in a manner dependent on the wild-type p53, and p33ING1 interacts with p53 in vivo (11). Recently, it was found that the human ING1 gene encodes three alternatively spliced transcripts that give rise to proteins of 47 kDa (ING1a), 33 kDa (ING1b), and 24 kDa (ING1c) (12). All ING1 isoforms share a conserved C terminus containing a plant homeodomain (PHD) Zn finger motif. Curiously, the mouse ING1 gene appears to produce only two alternatively spliced forms, p37 (similar to human ING1b) and p24/31 (similar to the human ING1c) (56). A recent study has identified ING1b as the breast and testis cancer-specific antigen (22).

In this work, we further characterized the human Sin3-HDAC containing ING1. Two different ING1-containing Sin3 complexes were observed in HeLa cells. One of these complexes additionally contains the subunits of the Brg1-based human Swi-Snf chromatin-remodeling complex. We found that the ING1b-Sin3-HDAC-containing complexes possess HDAC and oligonucleosome deacetylase activity and that interaction with the Sin3 complex is important for the growth suppression activity of p33ING1b.

Acknowledgments

We thank R. Kingston and S. Sif for providing us with the data presented in Fig. Fig.4d4d and for providing mammalian expression vectors encoding wild-type and mutant Brg1 proteins, D. Allis for providing antibodies specific to acetylated histones, K. Riabowol and A. Gudkov for providing p33 cDNA, and L. Lacomis for helping with mass spectrometric analysis.

This work was supported by grants from Howard Hughes Medical Institute and NIH (grant GM-48518) to D. Reinberg and NCI Cancer Center (grant P30 CA08748) to P. Tempst.

Acknowledgments

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