Development of a genetically encoded sensor for probing endogenous nociceptin opioid peptide release

Article Article scientifique Article Development of a genetically encoded sensor for probing endogenous nociceptin opioid peptide release eng 2024-06-25 2024-06-25 author Zhou Xuehan 0009-0004-2737-0156 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland.,Neuroscience Center Zurich, University and ETH Zürich, Zürich, Switzerland. author Stine Carrie 0000-0001-8171-3464 Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA.,Molecular and Cellular Biology, University of Washington School of Medicine, Seattle, WA, USA. author Prada Patricia Oliveira Max Planck Institute for Metabolism Research, Cologne, Germany.,Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.,School of Applied Sciences, State University of Campinas (UNICAMP), Limeira, Sao Paulo, Brazil. author Fusca Debora Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.,Institute of Zoology, Department of Biology, University of Cologne, Cologne, Germany. author Assoumou Kevin Department of Cell Physiology and Metabolism, University of Geneva, Geneva, Switzerland. 870598 Département de physiologie cellulaire et métabolisme (PHYME) author Dernic Jan Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland. author Bhat Musadiq A 0000-0002-0894-9996 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland. author Achanta Ananya S 0009-0008-3573-2873 Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. author Johnson Joseph C 0009-0000-9211-1346 Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. author Pasqualini Amanda Loren Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. author Jadhav Sanjana Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. author Bauder Corinna A Max Planck Institute for Metabolism Research, Cologne, Germany.,Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany. author Steuernagel Lukas 0000-0003-0043-1436 Max Planck Institute for Metabolism Research, Cologne, Germany.,Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany. author Ravotto Luca 0000-0002-0431-9866 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland. author Benke Dietmar 0000-0003-1846-4711 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland.,Neuroscience Center Zurich, University and ETH Zürich, Zürich, Switzerland. author Weber Bruno 0000-0002-9089-0689 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland.,Neuroscience Center Zurich, University and ETH Zürich, Zürich, Switzerland. author Suko Azra Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. author Palmiter Richard D 0000-0001-6587-0582 Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA.,Howard Hughes Medical Institute and Departments of Biochemistry and Genome Sciences, University of Washington, Seattle, WA, 98195, USA. author Stoeber Miriam Carolin Department of Cell Physiology and Metabolism, University of Geneva, Geneva, Switzerland. 930635 Département de physiologie cellulaire et métabolisme (PHYME) author Kloppenburg Peter 0000-0002-4554-404X Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.,Institute of Zoology, Department of Biology, University of Cologne, Cologne, Germany. author Brüning Jens C 0000-0002-6619-0092 Max Planck Institute for Metabolism Research, Cologne, Germany.,Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.,Policlinic for Endocrinology, Diabetes and Preventive Medicine (PEDP), University Hospital Cologne, Cologne, Germany. author Bruchas Michael R 0000-0003-4713-7816 Center for the Neurobiology of Addiction, Pain, and Emotion, University of Washington, Seattle, WA, USA. mbruchas@uw.edu.,Departments of Anesthesiology and Pharmacology and Bioengineering, University of Washington, Seattle, WA, USA. mbruchas@uw.edu.,Molecular and Cellular Biology, University of Washington School of Medicine, Seattle, WA, USA. mbruchas@uw.edu. author Patriarchi Tommaso 0000-0001-9351-3734 Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland. patriarchi@pharma.uzh.ch.,Neuroscience Center Zurich, University and ETH Zürich, Zürich, Switzerland. patriarchi@pharma.uzh.ch. 5353 10.1038/s41467-024-49712-0 38918403 2041-1723 PMC11199706 https://www.nature.com/articles/s41467-024-49712-0 Nociceptin/orphanin-FQ (N/OFQ) is a recently appreciated critical opioid peptide with key regulatory functions in several central behavioral processes including motivation, stress, feeding, and sleep. The functional relevance of N/OFQ action in the mammalian brain remains unclear due to a lack of high-resolution approaches to detect this neuropeptide with appropriate spatial and temporal resolution. Here we develop and characterize NOPLight, a genetically encoded sensor that sensitively reports changes in endogenous N/OFQ release. We characterized the affinity, pharmacological profile, spectral properties, kinetics, ligand selectivity, and potential interaction with intracellular signal transducers of NOPLight in vitro. Its functionality was established in acute brain slices by exogeneous N/OFQ application and chemogenetic induction of endogenous N/OFQ release from PNOC neurons. In vivo studies with fibre photometry enabled direct recording of NOPLight binding to exogenous N/OFQ receptor ligands, as well as detection of endogenous N/OFQ release within the paranigral ventral tegmental area (pnVTA) during natural behaviors and chemogenetic activation of PNOC neurons. In summary, we show here that NOPLight can be used to detect N/OFQ opioid peptide signal dynamics in tissue and freely behaving animals. Animals Opioid Peptides / metabolism Nociceptin Receptors, Opioid / metabolism Receptors, Opioid / genetics Neurons / metabolism Humans Mice Male Ventral Tegmental Area / metabolism Nociceptin Receptor HEK293 Cells Brain / metabolism Mice, Inbred C57BL Ligands Biosensing Techniques / methods Dewey 612 Swiss National Science Foundation Mechanisms Underlying Subcellular Location Bias of Opioid Receptor Signaling 181282 CH Careers 134 Département de physiologie cellulaire et métabolisme 21C false 1283 Contrôle subcellulaire des récepteurs de signalisation 1005 Nature communications 15 1 ccd17e37-a13a-45a6-a70c-69d11fcb84e9 Article (Published version) Public Article_scientifique_from_unpaywall.pdf 12709491 application/pdf CC BY-4.0 e13dd1c16e7842b82b2b46c570a05460af27e02c0ac54c329811a3d651d6b771 openAccess Faculté de médecine / Section de médecine fondamentale / Département de physiologie cellulaire et métabolisme

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