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

Ksenia Smurova, Michela Damizia, Carmela Irene, Stefania Stancari, Giovanna Berto, Giulia Perticari, Maria Giuseppina Iacovella, Ilaria D’Ambrosio, Maria Giubettini, Réginald Philippe, Chiara Baggio, Elisabetta Callegaro, Andrea Casagranda, Alessandro Corsini, Vincenzo Gentile Polese, Anna Ricci, Erik Dassi and Peter Wulf ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-38920-9

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