Esperanto for histones: CENP-A, not CenH3, is the centromeric histone H3 variant

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Abstract

The first centromeric protein identified in any species was CENP-A, a divergent member of the histone H3 family that was recognised by autoantibodies from patients with scleroderma-spectrum disease. It has recently been suggested to rename this protein CenH3. Here, we argue that the original name should be maintained both because it is the basis of a long established nomenclature for centromere proteins and because it avoids confusion due to the presence of canonical histone H3 at centromeres.

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Most cited references 14

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The human CENP-A centromeric nucleosome-associated complex.

Daniel Foltz, Lars E T Jansen, Ben Black … (2006)

The basic element for chromosome inheritance, the centromere, is epigenetically determined in mammals. The prime candidate for specifying centromere identity is the array of nucleosomes assembled with CENP-A, the centromere-specific histone H3 variant. Here, we show that CENP-A nucleosomes directly recruit a proximal CENP-A nucleosome associated complex (NAC) comprised of three new human centromere proteins (CENP-M, CENP-N and CENP-T), along with CENP-U(50), CENP-C and CENP-H. Assembly of the CENP-A NAC at centromeres is dependent on CENP-M, CENP-N and CENP-T. Facilitates chromatin transcription (FACT) and nucleophosmin-1 (previously implicated in transcriptional chromatin remodelling and as a multifunctional nuclear chaperone, respectively) are absent from histone H3-containing nucleosomes, but are stably recruited to CENP-A nucleosomes independent of CENP-A NAC. Seven new CENP-A-nucleosome distal (CAD) centromere components (CENP-K, CENP-L, CENP-O, CENP-P, CENP-Q, CENP-R and CENP-S) are identified as assembling on the CENP-A NAC. The CENP-A NAC is essential, as disruption of the complex causes errors of chromosome alignment and segregation that preclude cell survival despite continued centromere-derived mitotic checkpoint signalling.

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Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin.

Beth A Sullivan, Gary H. Karpen (2004)

Post-translational histone modifications regulate epigenetic switching between different chromatin states. Distinct histone modifications, such as acetylation, methylation and phosphorylation, define different functional chromatin domains, and often do so in a combinatorial fashion. The centromere is a unique chromosomal locus that mediates multiple segregation functions, including kinetochore formation, spindle-mediated movements, sister cohesion and a mitotic checkpoint. Centromeric (CEN) chromatin is embedded in heterochromatin and contains blocks of histone H3 nucleosomes interspersed with blocks of CENP-A nucleosomes, the histone H3 variant that provides a structural and functional foundation for the kinetochore. Here, we demonstrate that the spectrum of histone modifications present in human and Drosophila melanogaster CEN chromatin is distinct from that of both euchromatin and flanking heterochromatin. We speculate that this distinct modification pattern contributes to the unique domain organization and three-dimensional structure of centromeric regions, and/or to the epigenetic information that determines centromere identity.

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CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore.

Tetsuya Hori, Miho Amano, Aussie Suzuki … (2008)

Kinetochore specification and assembly requires the targeted deposition of specialized nucleosomes containing the histone H3 variant CENP-A at centromeres. However, CENP-A is not sufficient to drive full-kinetochore assembly, and it is not clear how centromeric chromatin is established. Here, we identify CENP-W as a component of the DNA-proximal constitutive centromere-associated network (CCAN) of proteins. We demonstrate that CENP-W forms a DNA-binding complex together with the CCAN component CENP-T. This complex directly associates with nucleosomal DNA and with canonical histone H3, but not with CENP-A, in centromeric regions. CENP-T/CENP-W functions upstream of other CCAN components with the exception of CENP-C, an additional putative DNA-binding protein. Our analysis indicates that CENP-T/CENP-W and CENP-C provide distinct pathways to connect the centromere with outer kinetochore assembly. In total, our results suggest that the CENP-T/CENP-W complex is directly involved in establishment of centromere chromatin structure coordinately with CENP-A.

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Author and article information

Contributors

: bill.earnshaw@ed.ac.uk

: dcleveland@ucsd.edu

Journal

Journal ID (nlm-ta): Chromosome Res

Journal ID (iso-abbrev): Chromosome Res

Title: Chromosome Research

Publisher: Springer Netherlands (Dordrecht )

ISSN (Print): 0967-3849

ISSN (Electronic): 1573-6849

Publication date (Electronic): 12 April 2013

Publication date PMC-release: 12 April 2013

Publication date (Print): April 2013

Volume: 21

Issue: 2

Pages: 101-106

Affiliations

[ ]Wellcome Trust Centre for Cell Biology, University of Edinburgh, Mayfield Road, Edinburgh, EH9 3JR Scotland UK

[ ]Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104-6059 USA

[ ]Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-3280 USA

[ ]Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030 USA

[ ]School of Biology, Medical School Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH UK

[ ]Whitehead Institute and Department of Biology, MIT, Nine Cambridge Center, Cambridge, MA 02142 USA

[ ]Chromosome Research, Murdoch Childrens Research Institute, Department of Paediatrics, Royal Children’s Hospital, Parkville, Victoria Australia

[ ]Department of Biology and the Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, 27599-3280 USA

[ ]Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, CO 80523 USA

[ ]Ludwig Institute for Cancer Research, University of California at San Diego, La Jolla, CA USA

[ ]Molecular Biology, FLI, Beutenbergstr. 11, 07745 Jena, Germany

[ ]ZMBH, DKFZ-ZMBH Alliance, University of Heidelberg, INF 282, 69120 Heidelberg, Germany

[ ]Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA 01003 USA

[ ]Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, VA 22908 USA

[ ]Department of Molecular Genetics, National Institute of Genetics, Mishima, Shizuoka 411-8540 Japan

[ ]IBMC—Instituto de Biologia Molecular e Celular, Universidade do Porto, Porto, Portugal

[ ]Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Dr. Bohr Gasse 3, 1030 Vienna, Austria

[ ]Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH UK

[ ]Cell Cycle and Cancer Biology, Oklahoma Medical Research Foundation, 825 NE 13th St, MS 48, Oklahoma City, OK 73104 USA

[ ]Jack and Eileen Connors Structural Biology Laboratory, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School and Howard Hughes Medical Institute, Boston, MA USA

[ ]Max Planck Institute of Immunobiology and Epigenetics, Stübeweg 51, 79108 Freiburg, Germany

[ ]Cancer Institute of the Japanese Foundation for Cancer Research (JFCR), Ariake 3-8-31, Koto-ku, 135-8550 Tokyo Japan

[ ]Instituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugal

[ ]Lawrence Berkeley National Lab, Life Sciences Division and UC Berkeley, Department of Molecular and Cell Biology, One Cyclotron Road, MS977, Berkeley, CA 94720 USA

[ ]Departments of Medical Oncology and Cancer Genomics Netherlands, University Medical Center Utrecht, 3584 CG Utrecht, The Netherlands

[ ]Department of Biology, University of Pennsylvania, Philadelphia, PA USA

[ ]Department of Medical Oncology, University Medical Center Utrecht, 3584 CG Utrecht, The Netherlands

[ ]Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO), Melchor Fernández Almagro 3, 28029 Madrid, Spain

[ ]Institute for Research in Immunology and Cancer (IRIC), Department of Pathology and Cell Biology, Université de Montréal, P.O. Box 6128, Station Centre-Ville, Montréal, QC H3C 3J7 Canada

[ ]Tumor Development Program, Sanford-Burnham Medical Research Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037 USA

[ ]Department of Human Genome Research, Kazusa DNA Research Institute, 2-6-7 Kazusa-Kamatari, Kisarazu, Chiba 292-0818 Japan

[ ]Centre for Mechanochemical Cell Biology, Division of Biomedical Cell Biology, Warwick Medical School, University of Warwick, Coventry, UK

[ ]Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269 USA

[ ]Physiology and Metabolism Department, Medical Faculty, University of Geneva, Geneva, Switzerland

[ ]Department of Mechanistic Cell Biology, Max Planck Institute of Molecular Physiology, Otto-Hahn-Straße 11, 44227 Dortmund, Germany

[ ]Institute for Genome Sciences and Policy, Department of Molecular Genetics and Microbiology, Duke University, 101 Science Drive, Durham, NC 27708 USA

[ ]Department of Biochemistry, Stanford University, Stanford, CA USA

[ ]Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA 22908 USA

[ ]Centre for Chromosome Biology, School of Natural Sciences, National University of Ireland, Galway, Galway, Ireland

[ ]IBMC—Instituto de Biologia Molecular e Celular and ICBAS—Instituto de Ciencias Biomédica Abel Salazar, Universidade do Porto, Porto, Portugal

[ ]Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dundee, DD1 5EH UK

[ ]Medical Sciences Program, Indiana University, 915 East 3rd St., Bloomington, IN 47405 USA

[ ]Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY USA

[ ]Research Institute of Molecular Pathology (IMP), Dr. Bohr Gasse 7, 1030 Vienna, Austria

[ ]Institute for Genome Sciences and Policy, Duke University, 101 Science Drive, Durham, NC 27708 USA

[ ]Department of Physiology and Biophysics, University of Washington School of Medicine, Seattle, WA 98195 USA

[ ]G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Tancha 1919-1, Onnason, 904-0495 Okinawa Japan

[ ]Fox Chase Cancer Center, Philadelphia, PA 19111 USA

[ ]Bioscience and Biotechnology Center, Nagoya University, Nagoya, Aichi Japan

Author notes

Responsible Editor: Conly Rieder.

Article

Publisher ID: 9347

DOI: 10.1007/s10577-013-9347-y

PMC ID: 3627038

PubMed ID: 23580138

SO-VID: 320d2cf3-fcbf-419e-91d9-947d41d538db

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

History

Date received : 15 March 2013

Date revision received : 17 March 2013

Date accepted : 17 March 2013

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: cenh3,cenp-a,centromere,histone,kinetochore

Data availability:

ScienceOpen disciplines: Genetics

Keywords: cenh3, cenp-a, centromere, histone, kinetochore

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Esperanto for histones: CENP-A, not CenH3, is the centromeric histone H3 variant

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G3: Genes|Genomes|Genetics

Most cited references 14

The human CENP-A centromeric nucleosome-associated complex.

Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin.

CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore.

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Cited by 15