Genome-wide analysis reveals a cell cycle–dependent mechanism controlling centromere propagation

Erhardt, Sylvia; Mellone, Barbara G.; Betts, Craig M.; Zhang, Weiguo; Karpen, Gary H.; Straight, Aaron F.

doi:10.1083/jcb.200806038

Genome-wide analysis reveals a cell cycle–dependent mechanism controlling centromere propagation

Journal Article · Mon Dec 01 00:00:00 EST 2008 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.200806038· OSTI ID:1625150

Erhardt, Sylvia ^[1]; Mellone, Barbara G. ^[2]; Betts, Craig M. ^[3]; Zhang, Weiguo ^[4]; Karpen, Gary H. ^[4]; Straight, Aaron F. ^[3]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Genome Dynamics; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Heidelberg Univ. (Germany). Zentrum für Molekulare Biologie; DOE/OSTI
Department of Genome Dynamics, Lawrence Berkeley National Laboratory; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720
Stanford Stanford Univ., CA (United States). Medical School. Dept. of Biochemistry
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Genome Dynamics; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology

Centromeres are the structural and functional foundation for kinetochore formation, spindle attachment, and chromosome segregation. In this study, we isolated factors required for centromere propagation using genome-wide RNA interference screening for defects in centromere protein A (CENP-A; centromere identifier [CID]) localization in Drosophila melanogaster. We identified the proteins CAL1 and CENP-C as essential factors for CID assembly at the centromere. CID, CAL1, and CENP-C coimmunoprecipitate and are mutually dependent for centromere localization and function. We also identified the mitotic cyclin A (CYCA) and the anaphase-promoting complex (APC) inhibitor RCA1/Emi1 as regulators of centromere propagation. We show that CYCA is centromere localized and that CYCA and RCA1/Emi1 couple centromere assembly to the cell cycle through regulation of the fizzy-related/CDH1 subunit of the APC. Our findings identify essential components of the epigenetic machinery that ensures proper specification and propagation of the centromere and suggest a mechanism for coordinating centromere inheritance with cell division.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625150

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 5 Vol. 183; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Concurrent Duplication of Drosophila Cid and Cenp-C Genes Resulted in Accelerated Evolution and Male Germline-Biased Expression of the New Copies Teixeira, José R.; Dias, Guilherme B.; Svartman, Marta Journal of Molecular Evolution, Vol. 86, Issue 6 https://doi.org/10.1007/s00239-018-9851-y	journal	June 2018
Centromeres of filamentous fungi Smith, Kristina M.; Galazka, Jonathan M.; Phatale, Pallavi A. Chromosome Research, Vol. 20, Issue 5 https://doi.org/10.1007/s10577-012-9290-3	journal	July 2012
Temporal control of epigenetic centromere specification Valente, Luis P.; Silva, Mariana C. C.; Jansen, Lars E. T. Chromosome Research, Vol. 20, Issue 5 https://doi.org/10.1007/s10577-012-9291-2	journal	June 2012
Evolutionary insights into the role of the essential centromere protein CAL1 in Drosophila Phansalkar, Ragini; Lapierre, Pascal; Mellone, Barbara G. Chromosome Research, Vol. 20, Issue 5 https://doi.org/10.1007/s10577-012-9299-7	journal	July 2012
The CENP-A nucleosome: a dynamic structure and role at the centromere Quénet, Delphine; Dalal, Yamini Chromosome Research, Vol. 20, Issue 5 https://doi.org/10.1007/s10577-012-9301-4	journal	July 2012
Hypermorphic expression of centromeric retroelement-encoded small RNAs impairs CENP-A loading Carone, Dawn M.; Zhang, Chu; Hall, Laura E. Chromosome Research, Vol. 21, Issue 1 https://doi.org/10.1007/s10577-013-9337-0	journal	February 2013
The molecular basis for centromere identity and function McKinley, Kara L.; Cheeseman, Iain M. Nature Reviews Molecular Cell Biology, Vol. 17, Issue 1 https://doi.org/10.1038/nrm.2015.5	journal	November 2015
Centromeres: unique chromatin structures that drive chromosome segregation Verdaasdonk, Jolien S.; Bloom, Kerry Nature Reviews Molecular Cell Biology, Vol. 12, Issue 5 https://doi.org/10.1038/nrm3107	journal	April 2011
Genetic screening identifies a SUMO protease dynamically maintaining centromeric chromatin Mitra, Sreyoshi; Bodor, Dani L.; David, Ana F. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-14276-x	journal	January 2020
Nuclear F-actin and myosins drive relocalization of heterochromatic breaks Caridi, Christopher P.; D’Agostino, Carla; Ryu, Taehyun Nature, Vol. 559, Issue 7712 https://doi.org/10.1038/s41586-018-0242-8	journal	June 2018
The long non-coding RNA LINC00152 is essential for cell cycle progression through mitosis in HeLa cells Nötzold, Linda; Frank, Lukas; Gandhi, Minakshi Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-02357-0	journal	May 2017
The MIS12 complex is a protein interaction hub for outer kinetochore assembly Petrovic, Arsen; Pasqualato, Sebastiano; Dube, Prakash Journal of Cell Biology, Vol. 190, Issue 5 https://doi.org/10.1083/jcb.201002070	journal	September 2010
Xenopus HJURP and condensin II are required for CENP-A assembly Bernad, Rafael; Sánchez, Patricia; Rivera, Teresa Journal of Cell Biology, Vol. 192, Issue 5 https://doi.org/10.1083/jcb.2010051361925c	journal	March 2011
Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division Rošić, Silvana; Köhler, Florian; Erhardt, Sylvia The Journal of Cell Biology, Vol. 207, Issue 3 https://doi.org/10.1083/jcb.201404097	journal	November 2014
Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division Rošić, Silvana; Köhler, Florian; Erhardt, Sylvia Journal of Cell Biology, Vol. 207, Issue 5 https://doi.org/10.1083/jcb.20140409711122014c	journal	December 2014
A cell-free CENP-A assembly system defines the chromatin requirements for centromere maintenance Westhorpe, Frederick G.; Fuller, Colin J.; Straight, Aaron F. Journal of Cell Biology, Vol. 209, Issue 6 https://doi.org/10.1083/jcb.201503132	journal	June 2015
Centromere transcription allows CENP-A to transit from chromatin association to stable incorporation Bobkov, Georg O. M.; Gilbert, Nick; Heun, Patrick Journal of Cell Biology, Vol. 217, Issue 6 https://doi.org/10.1083/jcb.201611087	journal	April 2018
Hierarchical Inactivation of a Synthetic Human Kinetochore by a Chromatin Modifier Cardinale, Stefano; Bergmann, Jan H.; Kelly, David Molecular Biology of the Cell, Vol. 20, Issue 19 https://doi.org/10.1091/mbc.e09-06-0489	journal	October 2009
In vitro BioID: mapping the CENP-A microenvironment with high temporal and spatial resolution Remnant, Lucy; Booth, Daniel G.; Vargiu, Giulia Molecular Biology of the Cell, Vol. 30, Issue 11 https://doi.org/10.1091/mbc.e18-12-0799	journal	May 2019
Phosphorylation of Drosophila CENP-A on serine 20 regulates protein turn-over and centromere-specific loading Huang, Anming; Kremser, Leopold; Schuler, Fabian Nucleic Acids Research, Vol. 47, Issue 20 https://doi.org/10.1093/nar/gkz809	journal	September 2019
Localization of Drosophila CENP-A to non-centromeric sites depends on the NuRD complex Demirdizen, Engin; Spiller-Becker, Matthias; Förtsch, Arion Nucleic Acids Research https://doi.org/10.1093/nar/gkz962	journal	November 2019
Centromeric CENP-A loading requires accurate mitotic timing, which is linked to checkpoint proteins Pauleau, Anne Laure; Bergner, Andrea; Kajtez, Janko BioRxiv https://doi.org/10.1101/394981	posted_content	January 2019
Islands of retroelements are the major components of Drosophila centromeres Chang, Ching-Ho; Chavan, Ankita; Palladino, Jason PLOS Biology https://doi.org/10.1101/537357	journal	February 2019
Epigenetic inheritance of centromere identity in a heterologous system Roure, Virginie; Medina-Pritchard, Bethan; Anselm, Eduard BioRxiv https://doi.org/10.1101/560391	posted_content	January 2019
Genetic screening identifies a SUMO protease dynamically maintaining centromeric chromatin and the associated centromere complex Mitra, Sreyoshi; Bodor, Dani L.; David, Ana F. https://doi.org/10.1101/620088	posted_content	April 2019
Structural Basis for CAL1-Mediated Centromere Maintenance Medina-Pritchard, Bethan; Lazou, Vasiliki; Zou, Juan National Institutes of Health https://doi.org/10.1101/723213	posted_content	January 2019
Hap2-Ino80 facilitated transcription promotes de novo establishment of CENP-A chromatin Singh, Puneet P.; Shukla, Manu; White, Sharon A. Genes & Development https://doi.org/10.1101/778639	posted_content	January 2019
CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere Falk, S. J.; Guo, L. Y.; Sekulic, N. Science, Vol. 348, Issue 6235 https://doi.org/10.1126/science.1259308	journal	May 2015
Centromeres: unique chromatin structures that drive chromosome segregation S., Verdaasdonk, Jolien; Kerry, Bloom, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/5z3s-n165	text	January 2011
A Molecular View of Kinetochore Assembly and Function Musacchio, Andrea; Desai, Arshad Biology, Vol. 6, Issue 4 https://doi.org/10.3390/biology6010005	journal	January 2017

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