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Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores

Author

Listed:
  • Ksenia Smurova

    (University of Trento)

  • Michela Damizia

    (University of Trento)

  • Carmela Irene

    (University of Trento)

  • Stefania Stancari

    (University of Trento)

  • Giovanna Berto

    (University of Trento)

  • Giulia Perticari

    (University of Trento)

  • Maria Giuseppina Iacovella

    (European Institute of Oncology)

  • Ilaria D’Ambrosio

    (University of Trento)

  • Maria Giubettini

    (University of Trento)

  • Réginald Philippe

    (University of Trento)

  • Chiara Baggio

    (University of Trento)

  • Elisabetta Callegaro

    (University of Trento)

  • Andrea Casagranda

    (University of Trento)

  • Alessandro Corsini

    (University of Trento)

  • Vincenzo Gentile Polese

    (University of Trento)

  • Anna Ricci

    (University of Trento)

  • Erik Dassi

    (University of Trento)

  • Peter Wulf

    (University of Trento)

Abstract

Kinetochores assemble on centromeres via histone H3 variant CENP-A and low levels of centromere transcripts (cenRNAs). The latter are ensured by the downregulation of RNA polymerase II (RNAPII) activity, and cenRNA turnover by the nuclear exosome. Using S. cerevisiae, we now add protein kinase Rio1 to this scheme. Yeast cenRNAs are produced either as short (median lengths of 231 nt) or long (4458 nt) transcripts, in a 1:1 ratio. Rio1 limits their production by reducing RNAPII accessibility and promotes cenRNA degradation by the 5’−3’exoribonuclease Rat1. Rio1 similarly curtails the concentrations of noncoding pericenRNAs. These exist as short transcripts (225 nt) at levels that are minimally two orders of magnitude higher than the cenRNAs. In yeast depleted of Rio1, cen- and pericenRNAs accumulate, CEN nucleosomes and kinetochores misform, causing chromosome instability. The latter phenotypes are also observed with human cells lacking orthologue RioK1, suggesting that CEN regulation by Rio1/RioK1 is evolutionary conserved.

Suggested Citation

  • Ksenia Smurova & Michela Damizia & Carmela Irene & Stefania Stancari & Giovanna Berto & Giulia Perticari & Maria Giuseppina Iacovella & Ilaria D’Ambrosio & Maria Giubettini & Réginald Philippe & Chiar, 2023. "Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38920-9
    DOI: 10.1038/s41467-023-38920-9
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    References listed on IDEAS

    as
    1. V. Barra & D. Fachinetti, 2018. "The dark side of centromeres: types, causes and consequences of structural abnormalities implicating centromeric DNA," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    2. Maria G. Iacovella & Cristina Golfieri & Lucia F. Massari & Sara Busnelli & Cinzia Pagliuca & Marianna Dal Maschio & Valentina Infantino & Rosella Visintin & Karl Mechtler & Sébastien Ferreira-Cerca &, 2015. "Rio1 promotes rDNA stability and downregulates RNA polymerase I to ensure rDNA segregation," Nature Communications, Nature, vol. 6(1), pages 1-16, May.
    3. Ruifang Guan & Tengfei Lian & Bing-Rui Zhou & Emily He & Carl Wu & Martin Singleton & Yawen Bai, 2021. "Structural and dynamic mechanisms of CBF3-guided centromeric nucleosome formation," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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