Dynamic SUMO modification regulates mitotic chromosome assembly and cell cycle progression in Caenorhabditis elegans

Federico Pelisch, Remi Sonneville, Ehsan Pourkarimi, Ana Agostinho, J. Julian Blow, Anton Gartner, Ronald T. Hay (Lead / Corresponding author)

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    22 Citations (Scopus)

    Abstract

    The small ubiquitin-like modifier (SUMO), initially characterized as a suppressor of a mutation in the gene encoding the centromeric protein MIF2, is involved in many aspects of cell cycle regulation. The dynamics of conjugation and deconjugation and the role of SUMO during the cell cycle remain unexplored. Here we used Caenorhabditis elegans to establish the contribution of SUMO to a timely and accurate cell division. Chromatin-associated SUMO conjugates increase during metaphase but decrease rapidly during anaphase. Accumulation of SUMO conjugates on the metaphase plate and proper chromosome alignment depend on the SUMO E2 conjugating enzyme UBC-9 and SUMO E3 ligase PIAS(GEI-17). Deconjugation is achieved by the SUMO protease ULP-4 and is crucial for correct progression through the cell cycle. Moreover, ULP-4 is necessary for Aurora B(AIR-2) extraction from chromatin and relocation to the spindle mid-zone. Our results show that dynamic SUMO conjugation plays a role in cell cycle progression.

    Original languageEnglish
    Article number5485
    Number of pages12
    JournalNature Communications
    Volume5
    DOIs
    Publication statusPublished - 5 Dec 2014

    Fingerprint

    chromosomes
    Caenorhabditis elegans
    Chromosomes
    Ubiquitin
    progressions
    Cell Cycle
    assembly
    Cells
    chromatin
    cycles
    conjugation
    cell division
    suppressors
    relocation
    protease
    spindles
    mutations
    genes
    Metaphase
    enzymes

    Cite this

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    title = "Dynamic SUMO modification regulates mitotic chromosome assembly and cell cycle progression in Caenorhabditis elegans",
    abstract = "The small ubiquitin-like modifier (SUMO), initially characterized as a suppressor of a mutation in the gene encoding the centromeric protein MIF2, is involved in many aspects of cell cycle regulation. The dynamics of conjugation and deconjugation and the role of SUMO during the cell cycle remain unexplored. Here we used Caenorhabditis elegans to establish the contribution of SUMO to a timely and accurate cell division. Chromatin-associated SUMO conjugates increase during metaphase but decrease rapidly during anaphase. Accumulation of SUMO conjugates on the metaphase plate and proper chromosome alignment depend on the SUMO E2 conjugating enzyme UBC-9 and SUMO E3 ligase PIAS(GEI-17). Deconjugation is achieved by the SUMO protease ULP-4 and is crucial for correct progression through the cell cycle. Moreover, ULP-4 is necessary for Aurora B(AIR-2) extraction from chromatin and relocation to the spindle mid-zone. Our results show that dynamic SUMO conjugation plays a role in cell cycle progression.",
    author = "Federico Pelisch and Remi Sonneville and Ehsan Pourkarimi and Ana Agostinho and Blow, {J. Julian} and Anton Gartner and Hay, {Ronald T.}",
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    AU - Pelisch, Federico

    AU - Sonneville, Remi

    AU - Pourkarimi, Ehsan

    AU - Agostinho, Ana

    AU - Blow, J. Julian

    AU - Gartner, Anton

    AU - Hay, Ronald T.

    PY - 2014/12/5

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    AB - The small ubiquitin-like modifier (SUMO), initially characterized as a suppressor of a mutation in the gene encoding the centromeric protein MIF2, is involved in many aspects of cell cycle regulation. The dynamics of conjugation and deconjugation and the role of SUMO during the cell cycle remain unexplored. Here we used Caenorhabditis elegans to establish the contribution of SUMO to a timely and accurate cell division. Chromatin-associated SUMO conjugates increase during metaphase but decrease rapidly during anaphase. Accumulation of SUMO conjugates on the metaphase plate and proper chromosome alignment depend on the SUMO E2 conjugating enzyme UBC-9 and SUMO E3 ligase PIAS(GEI-17). Deconjugation is achieved by the SUMO protease ULP-4 and is crucial for correct progression through the cell cycle. Moreover, ULP-4 is necessary for Aurora B(AIR-2) extraction from chromatin and relocation to the spindle mid-zone. Our results show that dynamic SUMO conjugation plays a role in cell cycle progression.

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