The box C/D snoRNP assembly factor Bcd1 interacts with the histone chaperone Rtt106 and controls its transcription dependent activity

Benoît Bragantini, Christophe Charron, Maxime Bourguet, Arnaud Paul, Decebal Tiotiu, Benjamin Rothé, Hélène Marty, Guillaume Terral, Steve Hessmann, Laurence Decourty, Marie-Eve Chagot, Jean-Marc Strub, Séverine Massenet, Edouard Bertrand, Marc Quinternet, Cosmin Saveanu, Sarah Cianférani, Stéphane Labialle (), Xavier Manival () and Bruno Charpentier ()
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Benoît Bragantini: Université de Lorraine, CNRS, IMoPA
Christophe Charron: Université de Lorraine, CNRS, IMoPA
Maxime Bourguet: Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS IPHC UMR 7178
Arnaud Paul: Université de Lorraine, CNRS, IMoPA
Decebal Tiotiu: Université de Lorraine, CNRS, IMoPA
Benjamin Rothé: Université de Lorraine, CNRS, IMoPA
Hélène Marty: Université de Lorraine, CNRS, IMoPA
Guillaume Terral: Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS IPHC UMR 7178
Steve Hessmann: Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS IPHC UMR 7178
Laurence Decourty: Génétique des Interactions Macromoléculaires, Département de Génomes et Génétique, Institut Pasteur (UMR3525-CNRS)
Marie-Eve Chagot: Université de Lorraine, CNRS, IMoPA
Jean-Marc Strub: Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS IPHC UMR 7178
Séverine Massenet: Université de Lorraine, CNRS, IMoPA
Edouard Bertrand: IGH, CNRS, Université de Montpellier
Marc Quinternet: Université de Lorraine, CNRS, INSERM, IBSLor
Cosmin Saveanu: Génétique des Interactions Macromoléculaires, Département de Génomes et Génétique, Institut Pasteur (UMR3525-CNRS)
Sarah Cianférani: Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS IPHC UMR 7178
Stéphane Labialle: Université de Lorraine, CNRS, IMoPA
Xavier Manival: Université de Lorraine, CNRS, IMoPA
Bruno Charpentier: Université de Lorraine, CNRS, IMoPA

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract Biogenesis of eukaryotic box C/D small nucleolar ribonucleoproteins initiates co-transcriptionally and requires the action of the assembly machinery including the Hsp90/R2TP complex, the Rsa1p:Hit1p heterodimer and the Bcd1 protein. We present genetic interactions between the Rsa1p-encoding gene and genes involved in chromatin organization including RTT106 that codes for the H3-H4 histone chaperone Rtt106p controlling H3K56ac deposition. We show that Bcd1p binds Rtt106p and controls its transcription-dependent recruitment by reducing its association with RNA polymerase II, modulating H3K56ac levels at gene body. We reveal the 3D structures of the free and Rtt106p-bound forms of Bcd1p using nuclear magnetic resonance and X-ray crystallography. The interaction is also studied by a combination of biophysical and proteomic techniques. Bcd1p interacts with a region that is distinct from the interaction interface between the histone chaperone and histone H3. Our results are evidence for a protein interaction interface for Rtt106p that controls its transcription-associated activity.

Date: 2021
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DOI: 10.1038/s41467-021-22077-4

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