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Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human

Ribosome biogenesis is a major metabolic effort for growing cells. In Saccharomyces cerevisiae, Hmo1, an abundant high-mobility group box protein (HMGB) binds to the coding region of the RNA polymerase I transcribed ribosomal RNAs genes and the promoters of ∼70% of ribosomal protein genes. In this s...

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Autores principales: Albert, Benjamin, Colleran, Christine, Léger-Silvestre, Isabelle, Berger, Axel B., Dez, Christophe, Normand, Christophe, Perez-Fernandez, Jorge, McStay, Brian, Gadal, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905846/
https://www.ncbi.nlm.nih.gov/pubmed/24021628
http://dx.doi.org/10.1093/nar/gkt770
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author Albert, Benjamin
Colleran, Christine
Léger-Silvestre, Isabelle
Berger, Axel B.
Dez, Christophe
Normand, Christophe
Perez-Fernandez, Jorge
McStay, Brian
Gadal, Olivier
author_facet Albert, Benjamin
Colleran, Christine
Léger-Silvestre, Isabelle
Berger, Axel B.
Dez, Christophe
Normand, Christophe
Perez-Fernandez, Jorge
McStay, Brian
Gadal, Olivier
author_sort Albert, Benjamin
collection PubMed
description Ribosome biogenesis is a major metabolic effort for growing cells. In Saccharomyces cerevisiae, Hmo1, an abundant high-mobility group box protein (HMGB) binds to the coding region of the RNA polymerase I transcribed ribosomal RNAs genes and the promoters of ∼70% of ribosomal protein genes. In this study, we have demonstrated the functional conservation of eukaryotic HMGB proteins involved in ribosomal DNA (rDNA) transcription. We have shown that when expressed in budding yeast, human UBF1 and a newly identified Sp-Hmo1 (Schizosaccharomyces pombe) localize to the nucleolus and suppress growth defect of the RNA polymerase I mutant rpa49-Δ. Owing to the multiple functions of both proteins, Hmo1 and UBF1 are not fully interchangeable. By deletion and domains swapping in Hmo1, we identified essential domains that stimulate rDNA transcription but are not fully required for stimulation of ribosomal protein genes expression. Hmo1 is organized in four functional domains: a dimerization module, a canonical HMGB motif followed by a conserved domain and a C-terminal nucleolar localization signal. We propose that Hmo1 has acquired species-specific functions and shares with UBF1 and Sp-Hmo1 an ancestral function to stimulate rDNA transcription.
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spelling pubmed-39058462014-01-29 Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human Albert, Benjamin Colleran, Christine Léger-Silvestre, Isabelle Berger, Axel B. Dez, Christophe Normand, Christophe Perez-Fernandez, Jorge McStay, Brian Gadal, Olivier Nucleic Acids Res Gene Regulation, Chromatin and Epigenetics Ribosome biogenesis is a major metabolic effort for growing cells. In Saccharomyces cerevisiae, Hmo1, an abundant high-mobility group box protein (HMGB) binds to the coding region of the RNA polymerase I transcribed ribosomal RNAs genes and the promoters of ∼70% of ribosomal protein genes. In this study, we have demonstrated the functional conservation of eukaryotic HMGB proteins involved in ribosomal DNA (rDNA) transcription. We have shown that when expressed in budding yeast, human UBF1 and a newly identified Sp-Hmo1 (Schizosaccharomyces pombe) localize to the nucleolus and suppress growth defect of the RNA polymerase I mutant rpa49-Δ. Owing to the multiple functions of both proteins, Hmo1 and UBF1 are not fully interchangeable. By deletion and domains swapping in Hmo1, we identified essential domains that stimulate rDNA transcription but are not fully required for stimulation of ribosomal protein genes expression. Hmo1 is organized in four functional domains: a dimerization module, a canonical HMGB motif followed by a conserved domain and a C-terminal nucleolar localization signal. We propose that Hmo1 has acquired species-specific functions and shares with UBF1 and Sp-Hmo1 an ancestral function to stimulate rDNA transcription. Oxford University Press 2013-12 2013-09-09 /pmc/articles/PMC3905846/ /pubmed/24021628 http://dx.doi.org/10.1093/nar/gkt770 Text en © The Author(s) 2013. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Gene Regulation, Chromatin and Epigenetics
Albert, Benjamin
Colleran, Christine
Léger-Silvestre, Isabelle
Berger, Axel B.
Dez, Christophe
Normand, Christophe
Perez-Fernandez, Jorge
McStay, Brian
Gadal, Olivier
Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title_full Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title_fullStr Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title_full_unstemmed Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title_short Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human
title_sort structure-function analysis of hmo1 unveils an ancestral organization of hmg-box factors involved in ribosomal dna transcription from yeast to human
topic Gene Regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905846/
https://www.ncbi.nlm.nih.gov/pubmed/24021628
http://dx.doi.org/10.1093/nar/gkt770
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