Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores
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 kin...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-06-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-38920-9 |
| _version_ | 1797811409676926976 |
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| author | 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 Peter De Wulf |
| author_facet | 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 Peter De Wulf |
| author_sort | Ksenia Smurova |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-13T07:22:14Z |
| format | Article |
| id | doaj.art-65fd3056dd134eea9504a13623d57fe2 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-13T07:22:14Z |
| publishDate | 2023-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-65fd3056dd134eea9504a13623d57fe22023-06-04T11:33:24ZengNature PortfolioNature Communications2041-17232023-06-0114111910.1038/s41467-023-38920-9Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochoresKsenia Smurova0Michela Damizia1Carmela Irene2Stefania Stancari3Giovanna Berto4Giulia Perticari5Maria Giuseppina Iacovella6Ilaria D’Ambrosio7Maria Giubettini8Réginald Philippe9Chiara Baggio10Elisabetta Callegaro11Andrea Casagranda12Alessandro Corsini13Vincenzo Gentile Polese14Anna Ricci15Erik Dassi16Peter De Wulf17Department of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Experimental Oncology, European Institute of OncologyDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoDepartment of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoAbstract 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.https://doi.org/10.1038/s41467-023-38920-9 |
| spellingShingle | 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 Peter De Wulf Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores Nature Communications |
| title | Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores |
| title_full | Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores |
| title_fullStr | Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores |
| title_full_unstemmed | Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores |
| title_short | Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores |
| title_sort | rio1 downregulates centromeric rna levels to promote the timely assembly of structurally fit kinetochores |
| url | https://doi.org/10.1038/s41467-023-38920-9 |
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