The H3K27 Demethylase JMJD3 Is Required for Maintenance of the Embryonic Respiratory Neuronal Network, Neonatal Breathing, and Survival
Thomas Burgold,
Nicolas Voituron,
Marieta Caganova,
Prem Prakash Tripathi,
Clement Menuet,
Betsabeh Khoramian Tusi,
Fabio Spreafico,
Michelle Bévengut,
Christian Gestreau,
Serena Buontempo,
Antonio Simeone,
Laurens Kruidenier,
Gioacchino Natoli,
Stefano Casola,
Gérard Hilaire,
Giuseppe Testa
Affiliations
Thomas Burgold
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Nicolas Voituron
Mp3-respiration, Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Unité Mixte de Recherche 6132 CNRS-Université Aix-Marseille II et III, Faculté Saint Jérôme, 13397 Marseille Cedex 20, France
Marieta Caganova
FIRC Institute of Molecular Oncology Foundation (IFOM), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Prem Prakash Tripathi
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Clement Menuet
Mp3-respiration, Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Unité Mixte de Recherche 6132 CNRS-Université Aix-Marseille II et III, Faculté Saint Jérôme, 13397 Marseille Cedex 20, France
Betsabeh Khoramian Tusi
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Fabio Spreafico
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Michelle Bévengut
Mp3-respiration, Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Unité Mixte de Recherche 6132 CNRS-Université Aix-Marseille II et III, Faculté Saint Jérôme, 13397 Marseille Cedex 20, France
Christian Gestreau
Mp3-respiration, Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Unité Mixte de Recherche 6132 CNRS-Université Aix-Marseille II et III, Faculté Saint Jérôme, 13397 Marseille Cedex 20, France
Serena Buontempo
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Antonio Simeone
CEINGE Biotecnologie Avanzate, Via Comunale Margherita 482, 80145 and Institute of Genetics and Biophysics “A. Buzzati-Traverso,” National Research Council, Via Pietro Castellino 111, 80131 Naples, Italy
Laurens Kruidenier
Epinova DPU, Immuno-Inflammation Therapy Area, GlaxoSmithKline R&D, Medicines Research Centre, Gunnels Wood Road, Stevenage SG1 2NY, UK
Gioacchino Natoli
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Stefano Casola
FIRC Institute of Molecular Oncology Foundation (IFOM), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
Gérard Hilaire
Mp3-respiration, Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Unité Mixte de Recherche 6132 CNRS-Université Aix-Marseille II et III, Faculté Saint Jérôme, 13397 Marseille Cedex 20, France
Giuseppe Testa
European Institute of Oncology (IEO), IFOM-IEO Campus, Via Adamello 16, 20139 Milan, Italy
JMJD3 (KDM6B) antagonizes Polycomb silencing by demethylating lysine 27 on histone H3. The interplay of methyltransferases and demethylases at this residue is thought to underlie critical cell fate transitions, and the dynamics of H3K27me3 during neurogenesis posited for JMJD3 a critical role in the acquisition of neural fate. Despite evidence of its involvement in early neural commitment, however, its role in the emergence and maturation of the mammalian CNS remains unknown. Here, we inactivated Jmjd3 in the mouse and found that its loss causes perinatal lethality with the complete and selective disruption of the pre-Bötzinger complex (PBC), the pacemaker of the respiratory rhythm generator. Through genetic and electrophysiological approaches, we show that the enzymatic activity of JMJD3 is selectively required for the maintenance of the PBC and controls critical regulators of PBC activity, uncovering an unanticipated role of this enzyme in the late structuring and function of neuronal networks.