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

Benoît Bragantini (1, 2) , Christophe Charron (1) , Maxime Bourguet (3) , Arnaud Paul (1) , Decebal Tiotiu (1) , Benjamin Rothé (1, 4) , Hélène Marty (1) , Guillaume Terral (3) , Steve Hessmann (3) , Laurence Decourty (5) , Marie-Eve Chagot (1) , Jean-Marc Strub (3) , Séverine Massenet (1) , Edouard Bertrand (6) , Marc Quinternet (7) , Cosmin Saveanu (5) , Sarah Cianférani (3) , Stéphane Labialle (1) , Xavier Manival (1) , Bruno Charpentier (1)

1 IMoPA - Ingénierie Moléculaire et Physiopathologie Articulaire
2 Mayo Clinic [Rochester]
3 LSMBO - Laboratoire de Spectrométrie de Masse BioOrganique [Strasbourg]
4 EPFL - Ecole Polytechnique Fédérale de Lausanne
5 Génétique des Interactions macromoléculaires / Genetics of Macromolecular Interactions
6 IGH - Institut de génétique humaine
7 IBSLor - Ingénierie, Biologie et Santé en Lorraine

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.

Domaines: Biologie moléculaire; Biologie structurale [q-bio.BM]; Génomique, Transcriptomique et Protéomique [q-bio.GN]

Benoît Bragantini, Christophe Charron, Maxime Bourguet, Arnaud Paul, Decebal Tiotiu, et al.. The box C/D snoRNP assembly factor Bcd1 interacts with the histone chaperone Rtt106 and controls its transcription dependent activity. Nature Communications, 2021, 12 (1), pp.1859. ⟨10.1038/s41467-021-22077-4⟩. ⟨hal-03181046⟩