Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment

Toyoaki Natsume, Carolin A. Müller, Yuki Katou, Renata Retkute, Marek Gierlinski, Hiroyuki Araki, J. Julian Blow, Katsuhiko Shirahige, Conrad A. Nieduszynski, Tomoyuki U. Tanaka (Lead / Corresponding author)

    Research output: Contribution to journalArticle

    72 Citations (Scopus)

    Abstract

    Centromeres play several important roles in ensuring proper chromosome segregation. Not only do they promote kinetochore assembly for microtubule attachment, but they also support robust sister chromatid cohesion at pericentromeres and facilitate replication of centromeric DNA early in S phase. However, it is still elusive how centromeres orchestrate all these functions at the same site. Here, we show that the budding yeast Dbf4-dependent kinase (DDK) accumulates at kinetochores in telophase, facilitated by the Ctf19 kinetochore complex. This promptly recruits Sld3-Sld7 replication initiator proteins to pericentromeric replication origins so that they initiate replication early in S phase. Furthermore, DDK at kinetochores independently recruits the Scc2-Scc4 cohesin loader to centromeres in G1 phase. This enhances cohesin loading and facilitates robust pericentromeric cohesion in S phase. Thus, we have found the central mechanism by which kinetochores orchestrate early S phase DNA replication and robust sister chromatid cohesion at microtubule attachment sites.

    Original languageEnglish
    Pages (from-to)661-674
    Number of pages14
    JournalMolecular Cell
    Volume50
    Issue number5
    DOIs
    Publication statusPublished - 6 Jun 2013

    Keywords

    • YEAST GENOME
    • SISTER CHROMATIDS
    • S-PHASE
    • CELL IMAGING REVEALS
    • HETEROCHROMATIN
    • ASSOCIATION
    • EUKARYOTIC CELLS
    • SACCHAROMYCES-CEREVISIAE
    • CHROMOSOME-REPLICATION
    • XENOPUS EGG EXTRACTS

    Cite this

    Natsume, Toyoaki ; Müller, Carolin A. ; Katou, Yuki ; Retkute, Renata ; Gierlinski, Marek ; Araki, Hiroyuki ; Blow, J. Julian ; Shirahige, Katsuhiko ; Nieduszynski, Conrad A. ; Tanaka, Tomoyuki U. / Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. In: Molecular Cell. 2013 ; Vol. 50, No. 5. pp. 661-674.
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    abstract = "Centromeres play several important roles in ensuring proper chromosome segregation. Not only do they promote kinetochore assembly for microtubule attachment, but they also support robust sister chromatid cohesion at pericentromeres and facilitate replication of centromeric DNA early in S phase. However, it is still elusive how centromeres orchestrate all these functions at the same site. Here, we show that the budding yeast Dbf4-dependent kinase (DDK) accumulates at kinetochores in telophase, facilitated by the Ctf19 kinetochore complex. This promptly recruits Sld3-Sld7 replication initiator proteins to pericentromeric replication origins so that they initiate replication early in S phase. Furthermore, DDK at kinetochores independently recruits the Scc2-Scc4 cohesin loader to centromeres in G1 phase. This enhances cohesin loading and facilitates robust pericentromeric cohesion in S phase. Thus, we have found the central mechanism by which kinetochores orchestrate early S phase DNA replication and robust sister chromatid cohesion at microtubule attachment sites.",
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    Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. / Natsume, Toyoaki; Müller, Carolin A.; Katou, Yuki; Retkute, Renata; Gierlinski, Marek; Araki, Hiroyuki; Blow, J. Julian; Shirahige, Katsuhiko; Nieduszynski, Conrad A.; Tanaka, Tomoyuki U. (Lead / Corresponding author).

    In: Molecular Cell, Vol. 50, No. 5, 06.06.2013, p. 661-674.

    Research output: Contribution to journalArticle

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    T1 - Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment

    AU - Natsume, Toyoaki

    AU - Müller, Carolin A.

    AU - Katou, Yuki

    AU - Retkute, Renata

    AU - Gierlinski, Marek

    AU - Araki, Hiroyuki

    AU - Blow, J. Julian

    AU - Shirahige, Katsuhiko

    AU - Nieduszynski, Conrad A.

    AU - Tanaka, Tomoyuki U.

    PY - 2013/6/6

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    N2 - Centromeres play several important roles in ensuring proper chromosome segregation. Not only do they promote kinetochore assembly for microtubule attachment, but they also support robust sister chromatid cohesion at pericentromeres and facilitate replication of centromeric DNA early in S phase. However, it is still elusive how centromeres orchestrate all these functions at the same site. Here, we show that the budding yeast Dbf4-dependent kinase (DDK) accumulates at kinetochores in telophase, facilitated by the Ctf19 kinetochore complex. This promptly recruits Sld3-Sld7 replication initiator proteins to pericentromeric replication origins so that they initiate replication early in S phase. Furthermore, DDK at kinetochores independently recruits the Scc2-Scc4 cohesin loader to centromeres in G1 phase. This enhances cohesin loading and facilitates robust pericentromeric cohesion in S phase. Thus, we have found the central mechanism by which kinetochores orchestrate early S phase DNA replication and robust sister chromatid cohesion at microtubule attachment sites.

    AB - Centromeres play several important roles in ensuring proper chromosome segregation. Not only do they promote kinetochore assembly for microtubule attachment, but they also support robust sister chromatid cohesion at pericentromeres and facilitate replication of centromeric DNA early in S phase. However, it is still elusive how centromeres orchestrate all these functions at the same site. Here, we show that the budding yeast Dbf4-dependent kinase (DDK) accumulates at kinetochores in telophase, facilitated by the Ctf19 kinetochore complex. This promptly recruits Sld3-Sld7 replication initiator proteins to pericentromeric replication origins so that they initiate replication early in S phase. Furthermore, DDK at kinetochores independently recruits the Scc2-Scc4 cohesin loader to centromeres in G1 phase. This enhances cohesin loading and facilitates robust pericentromeric cohesion in S phase. Thus, we have found the central mechanism by which kinetochores orchestrate early S phase DNA replication and robust sister chromatid cohesion at microtubule attachment sites.

    KW - YEAST GENOME

    KW - SISTER CHROMATIDS

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    KW - CELL IMAGING REVEALS

    KW - HETEROCHROMATIN

    KW - ASSOCIATION

    KW - EUKARYOTIC CELLS

    KW - SACCHAROMYCES-CEREVISIAE

    KW - CHROMOSOME-REPLICATION

    KW - XENOPUS EGG EXTRACTS

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    JO - Molecular Cell

    JF - Molecular Cell

    SN - 1097-2765

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