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

Title: 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
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.

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

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

Grant/Contract Number:: AC02-05CH11231; R01 GM066272; R01 GM074728

OSTI ID:: 1625150

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

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Swr1 mediated H2A.ZPht1 incorporation designates centromere DNA for de novo CENP-ACnp1 assembly Kulasegaran-Shylini, Raghavendran; Subramanian, Lakzmi; Kerr, Alastair R. W. National Institutes of Health https://doi.org/10.1101/215962	journal	November 2017
The C-Terminal Domain of CENP-C Displays Multiple and Critical Functions for Mammalian Centromere Formation Trazzi, Stefania; Perini, Giovanni; Bernardoni, Roberto PLoS ONE, Vol. 4, Issue 6 https://doi.org/10.1371/journal.pone.0005832	journal	June 2009
Cdk Activity Couples Epigenetic Centromere Inheritance to Cell Cycle Progression Silva, Mariana C. C.; Bodor, Dani L.; Stellfox, Madison E. Developmental Cell, Vol. 22, Issue 1 https://doi.org/10.1016/j.devcel.2011.10.014	journal	January 2012
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
Super-coil me: Sizing up centromeric nucleosomes Hill, Emma; Williams, Ruth Journal of Cell Biology, Vol. 186, Issue 4 https://doi.org/10.1083/jcb.200908012	journal	August 2009
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
Winged migration Mellone, Barbara G. Molecular Biology of the Cell, Vol. 27, Issue 21 https://doi.org/10.1091/mbc.e16-07-0492	journal	November 2016
Epigenetics as an Evolutionary Tool for Centromere Flexibility Leo, Laura; Marchetti, Marcella; Giunta, Simona Genes, Vol. 11, Issue 7 https://doi.org/10.3390/genes11070809	journal	July 2020
ATP synthase F1 subunits recruited to centromeres by CENP-A are required for male meiosis Collins, Caitríona M.; Malacrida, Beatrice; Burke, Colin Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05093-9	journal	July 2018
Xenopus HJURP and condensin II are required for CENP-A assembly Bernad, Rafael; Sánchez, Patricia; Rivera, Teresa Journal of Cell Biology, Vol. 192, Issue 4 https://doi.org/10.1083/jcb.201005136	journal	February 2011
Centromere and Pericentromere Transcription: Roles and Regulation … in Sickness and in Health Smurova, Ksenia; De Wulf, Peter Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00674	journal	December 2018
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
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
Nucleolar activity and CENP-C regulate CENP-A and CAL1 availability for centromere assembly in meiosis Kwenda, Lucretia; Collins, Caitriona M.; Dattoli, Anna A. Development, Vol. 143, Issue 8 https://doi.org/10.1242/dev.130625	journal	April 2016
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
The E3-ligases SCFPpa and APC/CCdh1 co-operate to regulate CENP-ACID expression across the cell cycle Moreno-Moreno, Olga; Torras-Llort, Mònica; Azorin, Fernando Nucleic Acids Research, Vol. 47, Issue 7 https://doi.org/10.1093/nar/gkz060	journal	February 2019
The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly Hori, Tetsuya; Shang, Wei-Hao; Takeuchi, Kozo The Journal of Cell Biology, Vol. 200, Issue 1 https://doi.org/10.1083/jcb.201210106	journal	December 2012
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
Translation of incenp During Oocyte Maturation Is Required for Embryonic Development in Xenopus laevis1 Leblond, Geoffrey G.; Sarazin, Heather; Li, Ruizhen Biology of Reproduction, Vol. 86, Issue 5 https://doi.org/10.1095/biolreprod.111.097972	journal	May 2012
New clues to understand how CENP-A maintains centromere identity Sánchez, Patricia; Losada, Ana Cell Division, Vol. 6, Issue 1 https://doi.org/10.1186/1747-1028-6-11	journal	January 2011
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

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