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The HP1 Protein Family: Getting a Grip on Chromatin Washington University in St. Louis Washington University Open Scholarship Biology Faculty Publications & Presentations Biology 4-2000 The HP1 protein family: getting a grip on chromatin J Eissenberg Sarah C.R. Elgin Washington University in St. Louis, [email protected] Follow this and additional works at: https://openscholarship.wustl.edu/bio_facpubs Part of the Biology Commons Recommended Citation Eissenberg, J and Elgin, Sarah C.R., "The HP1 protein family: getting a grip on chromatin" (2000). Biology Faculty Publications & Presentations. 208. https://openscholarship.wustl.edu/bio_facpubs/208 This Article is brought to you for free and open access by the Biology at Washington University Open Scholarship. It has been accepted for inclusion in Biology Faculty Publications & Presentations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. GDA202.QXD 03/22/2000 02:16 Page 204 204 The HP1 protein family: getting a grip on chromatin Joel C Eissenberg* and Sarah CR Elgin† HP1 was first described in Drosophila as a heterochromatin- in this review is to summarize the structural and function- associated protein with dosage-dependent effects on al properties of HP1 family members and to highlight heterochromatin-induced gene silencing. Recently, reported interactions with HP1 family proteins that may membership of the HP1 protein family has expanded have functional significance. tremendously. A number of intriguing interactions between HP1 and other proteins have been described, implicating HP1 Identification of HP1 and its gene in gene regulation, DNA replication, and nuclear architecture. HP1 was originally identified by immunolocalization analysis of a fraction of tightly bound nonhistone chromosomal pro- Addresses teins prepared from Drosophila melanogaster embryo nuclei *Edward A Doisy Department of Biochemistry and Molecular Biology, [7]. A monoclonal antibody was used to demonstrate a pre- Saint Louis University School of Medicine, 1402 South Grand dominantly heterochromatic distribution of the protein [8] Boulevard, St Louis, Missouri 63104, USA; e-mail: [email protected] and to isolate the corresponding cDNA clone from a recom- †Department of Biology, One Brookings Drive, Box 1229, Washington University, St Louis, Missouri 63130, USA; binant expression library [7]. Molecular genetic studies e-mail: [email protected] [9–11] determined that the gene encoding the HP1 protein was identical to a locus previously identified as a dominant Current Opinion in Genetics & Development 2000, 10:204–210 suppressor of position effect variegation (PEV), Su(var)2-5 0959-437X/00/$ — see front matter © 2000 Elsevier Science Ltd. [12,13]. PEV, a mosaic silencing, results when a euchromatic All rights reserved. gene is placed next to or within heterochromatin. Su(var)2-5 Abbreviations satisfies the genetic criteria of dosage dependency for a GST glutathione S transferase structural protein of heterochromatin [14]: it is a haplo-insuf- HP1 heterochromatin protein 1 ficient suppressor and triplo-abnormal enhancer of PEV. All INCENP inner centromere protein known Su(var)2-5 mutations are recessive lethal, demon- KRAB Krüppel-associated box LBR lamin B receptor strating that HP1 is essential in Drosophila. ORC origin recognition complex Pc Polycomb HP1 structure and the chromo domain PEV position effect variegation The cloning of the homeotic gene silencer Polycomb (Pc) TIF transcription intermediary factor led to the identification of a sequence motif of ~44 amino acid residues shared by HP1 and PC, termed the ‘chromo Introduction domain’ (for chromosome organization modifier [15]). This The compartmentalization of chromatin in the nuclei of motif has now been found in a large number of chromoso- higher eukaryotes has been recognized for over 100 years. mal proteins from diverse sources [16,17]. Among these are At the cytological level, this is seen in the individualization proteins from yeast, nematode, insects, chicken, frog and of chromosomes at the onset of mitosis and in the differ- mammals (Table 1) that display the defining characteristics ential condensation of heterochromatin and euchromatin of the HP1 family: all are relatively small proteins in interphase nuclei [1]. At the biochemical level, the (15–35 kDa) with an amino-terminal chromo domain and a DNA of eukaryotes is packaged in nucleosomes, of which structurally related carboxy-terminal motif, the ‘chromo the spacing, acetylation state, and association with nonhis- shadow’ domain (Figure 1). tone proteins differs regionally. The three-dimensional structure of a chromo domain (from Within euchromatic domains, gene activation is accom- mouse M31) has been determined by nuclear magnetic plished by transactivators working in concert with resonance (NMR) [18]. It consists of a three-stranded chromatin-remodeling complexes [2]; however, hete- rochromatin formation can result in the functional Figure 1 inactivation of regions of chromatin that would otherwise be transcriptionally active. In Drosophila — the organism in which heterochromatin is best-characterized — genes that become mislocalized to heterochromatin by rearrangement or transposition are silenced (reviewed in [3,4]). This silencing occurs at the transcriptional level and is correlated with a more heterochromatin-like cytological appearance Schematic representation of the generic HP1 protein. A single amino- in polytene chromosomes [5] and increased resistance to terminal chromo domain motif (CHD) and a single carboxy-terminal nuclease attack [6]. Among the nonhistone proteins pri- chromo shadow domain motif (CSD) are separated by a variable length linker (hinge) region. The lengths of the amino- and carboxy- marily associated with heterochromatin, the best terminal tails are also variable. characterized is heterochromatin protein 1 (HP1). Our goal GDA202.QXD 03/22/2000 02:16 Page 205 The HP1 protein family Eissenberg and Elgin 205 Table 1 Members of the HP1 family. Name Organism Size (amino Reported cytology Silencing activity Refs acid residues) demonstrated Swi6p S. pombe 328 Centromeres, telomeres, silent mating type cassettes + [56] Hhp1p T. thermophila 184 Absent in micronuclei; enriched in condensed chromatin of macronuclei – [43] pchet1 P. citri 173 Male specific nuclear protein; not heterochromatin-specific ND [40] pchet2 P. citri 194 ND ND [40] HP1 D. melanogaster 206 Pericentric heterochromatin, telomeres, several non-pericentric sites + [7] DvHP1 D. virilis 213 ND ND [57] emb|CAB07241 C. elegans 175 ND ND (a) gi|3702834 C. elegans 184 ND ND (a) Xhp1α X. laevis 141 ND ND [37•] Xhp1γ X. laevis 171 ND ND [37•] CHCB1 G. gallus 185 ND ND [58] CHCB2 G. gallus 174 ND ND [58] mHP1α M. musculus 191 ND + [28] M31; MoMOD1 M. musculus 185 Pericentric heterochromatin – [59] M32; MoMOD2 M. musculus 173 Euchromatic; excluded from heterochromatin – [59] HP1hsα H. sapiens 191 Pericentric heterochromatin + [60] HP1hsβ H. sapiens 185 Pericentric heterochromatin – [59] HP1hsγ H. sapiens 173 Euchromatic; excluded from heterochromatin + [32] (a) GenBank database. ND, not determined. β sheet packed against an α helix, a motif also described SU(VAR)3-7 for two DNA-binding proteins from thermophilic archea. Su(var)3-7 was also identified as a dominant suppressor of On the basis of its overall negative surface charge distribu- heterochromatic PEV. The SU(VAR)3-7 protein includes tion, however, the chromo domain appears to be better seven zinc-finger motifs, suggesting a possible DNA bind- suited for protein–protein interactions than for protein– ing activity. Immunofluorescent localization of SU(VAR)3-7 nucleic acid interactions. Because of its high sequence on larval salivary gland polytene chromosomes reveals that homology to M31, the Drosophila chromo domain structure it has a distribution nearly identical to that of HP1, and is likely to resemble the M31 chromo domain (Figure 2). antibodies to SU(VAR)3-7 co-immunoprecipitate HP1 from embryo extracts [25]. Chromo domain mutations in HP1 and PC abolish the genet- ic activity of these proteins [19,20]. Additionally, SU(VAR)3-9 β-galactosidase fusion proteins with the PC chromo domain, Su(var)3-9, another dominant suppressor of PEV, encodes a or either the HP1 chromo or chromo shadow domains, target protein containing a chromo domain [26]. The protein appears β-galactosidase to euchromatic PC binding sites or hetero- to be enriched in heterochromatin [27]. A human SU(VAR)3-9 chromatic HP1 binding sites, respectively [19–21]. As homolog, SUV39H1, can be co-immunoprecipitated from expected, a chimeric HP1–PC fusion protein (in which the human or mouse nuclear extracts using an antibody to HP1 chromo domain is replaced with the PC chromo domain) M31, suggesting that these proteins form a complex [27]. targets β-galactosidase to both HP1 and PC binding sites. Interestingly, the chimeric protein also mislocalizes endoge- TIF1α and TIF1β nous HP1 to euchromatic PC sites and endogenous PC to The transcription intermediary factors (TIF) 1α and TIF1β heterochromatin [19,22]. This latter behavior implicates the interact with nuclear hormone receptors and the Krüppel- PC chromo domain and HP1 chromo shadow domain in associated box (KRAB) domains of several proteins; they mediating protein–protein interactions in the nucleus. may function as co-activators in ligand-dependent activation of transcription and co-repressors with KRAB-containing re- Targets of HP1 binding in the nucleus pressor proteins. Yeast two-hybrid
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