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Research ArticleArticle

S29434, a Quinone Reductase 2 Inhibitor: Main Biochemical and Cellular Characterization

Jean A. Boutin, Frederic Bouillaud, Elzbieta Janda, István Gacsalyi, Gérald Guillaumet, Etienne C. Hirsch, Daniel A. Kane, Françoise Nepveu, Karine Reybier, Philippe Dupuis, Marc Bertrand, Monivan Chhour, Thierry Le Diguarher, Mathias Antoine, Karen Brebner, Hervé Da Costa, Pierre Ducrot, Adeline Giganti, Vishalgiri Goswami, Hala Guedouari, Patrick P. Michel, Aakash Patel, Jérôme Paysant, Johann Stojko, Marie-Claude Viaud-Massuard and Gilles Ferry
Molecular Pharmacology March 2019, 95 (3) 269-285; DOI: https://doi.org/10.1124/mol.118.114231
Jean A. Boutin
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Frederic Bouillaud
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Elzbieta Janda
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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István Gacsalyi
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Gérald Guillaumet
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Etienne C. Hirsch
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Daniel A. Kane
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Françoise Nepveu
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Karine Reybier
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Philippe Dupuis
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Marc Bertrand
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Monivan Chhour
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Thierry Le Diguarher
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Mathias Antoine
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Karen Brebner
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Hala Guedouari
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Patrick P. Michel
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Aakash Patel
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Jérôme Paysant
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Johann Stojko
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Marie-Claude Viaud-Massuard
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Gilles Ferry
Pôle d’Expertise Biotechnologie, Chimie & Biologie, Institut de Recherches SERVIER, Croissy-sur-Seine, France (J.A.B., M.A., Pi.D., A.G., J.S., G.F.); Institut Cochin, INSERM U1016, CNRS-UMR8104, Université Paris Descartes, Paris, France (F.B., H.G.); Department of Health Sciences, Magna Graecia University, Catanzaro, Italy (E.J.); Egis Pharmaceuticals PLC, Budapest, Hungary (I.G.); Institut de Chimie Organique et Analytique (ICOA), Université d'Orléans, UMR CNRS 7311, Orléans Cedex 2, France (G.G., H.D.C.); Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France (E.C.H., P.P.M.); Departments of Human Kinetics (D.A.K.) and Psychology (K.B.), St. Francis Xavier University, Antigonish, Nova Scotia, Canada; UMR 152 Pharma-Dev, Université de Toulouse, IRD, UPS, Toulouse, France (F.N., K.R., M.C.); EUROFINS-CEREP SA, Celle L'Evescault, France (Ph.D.); Technologie Servier, Orléans, France (M.B., T.L.D.); CNRS-UMR 7292, GICC Innovation Moléculaire et Thérapeutique, Université de Tours, Tours, France (H.D.C., M.-C.V.-M.); Oxygen Healthcare Pvt Ltd, Ahmedabad, Gujarat, India (V.G., A.P.); and Pôle d’Innovation Thérapeutique de Cardiologie, Institut de Recherches SERVIER, Suresnes, France (J.P.)
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Abstract

Quinone reductase 2 (QR2, E.C. 1.10.5.1) is an enzyme with a feature that has attracted attention for several decades: in standard conditions, instead of recognizing NAD(P)H as an electron donor, it recognizes putative metabolites of NADH, such as N-methyl- and N-ribosyl-dihydronicotinamide. QR2 has been particularly associated with reactive oxygen species and memory, strongly suggesting a link among QR2 (as a possible key element in pro-oxidation), autophagy, and neurodegeneration. In molecular and cellular pharmacology, understanding physiopathological associations can be difficult because of a lack of specific and powerful tools. Here, we present a thorough description of the potent, nanomolar inhibitor [2-(2-methoxy-5H-1,4b,9-triaza(indeno[2,1-a]inden-10-yl)ethyl]-2-furamide (S29434 or NMDPEF; IC50 = 5–16 nM) of QR2 at different organizational levels. We provide full detailed syntheses, describe its cocrystallization with and behavior at QR2 on a millisecond timeline, show that it penetrates cell membranes and inhibits QR2-mediated reactive oxygen species (ROS) production within the 100 nM range, and describe its actions in several in vivo models and lack of actions in various ROS-producing systems. The inhibitor is fairly stable in vivo, penetrates cells, specifically inhibits QR2, and shows activities that suggest a key role for this enzyme in different pathologic conditions, including neurodegenerative diseases.

Footnotes

    • Received September 3, 2018.
    • Accepted December 17, 2018.
  • ↵1 Current affiliation: Institut de Recherches Internationales Servier, Suresnes, France.

  • ↵2 Current affiliation: ATRC Aurigon Ltd., Budapest, Hungary.

  • E.C.H. and P.P.M. acknowledge the support of the funding programs “Investissements d’avenir” ANR-10-IAIHU-06 and “Investissements d’avenir” ANR-11-INBS-0011-NeurATRIS: Translational Research Infrastructure for Biotherapies in Neurosciences. This work benefited from equipment and services from the CELIS core facility (Institut du Cerveau et de la Moelle Epinière, Paris). Dr. D.A.K. acknowledges support from the Canada Foundation for Innovation and the Natural Sciences and Engineering Research Council of Canada. Dr. E.J. received financial support from Herbal and Antioxidant Derivatives srl, Biano (RC), Italy, and from FFARB 2017 (Basic Research Activities Fund).

  • https://doi.org/10.1124/mol.118.114231.

  • ↵Embedded ImageThis article has supplemental material available at molpharm.aspetjournals.org.

  • Copyright © 2019 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 95 (3)
Molecular Pharmacology
Vol. 95, Issue 3
1 Mar 2019
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S29434, a Quinone Reductase 2 Inhibitor: Main Biochemical and Cellular Characterization
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Quinone Reductase 2 Inhibitor: S29434

Jean A. Boutin, Frederic Bouillaud, Elzbieta Janda, István Gacsalyi, Gérald Guillaumet, Etienne C. Hirsch, Daniel A. Kane, Françoise Nepveu, Karine Reybier, Philippe Dupuis, Marc Bertrand, Monivan Chhour, Thierry Le Diguarher, Mathias Antoine, Karen Brebner, Hervé Da Costa, Pierre Ducrot, Adeline Giganti, Vishalgiri Goswami, Hala Guedouari, Patrick P. Michel, Aakash Patel, Jérôme Paysant, Johann Stojko, Marie-Claude Viaud-Massuard and Gilles Ferry
Molecular Pharmacology March 1, 2019, 95 (3) 269-285; DOI: https://doi.org/10.1124/mol.118.114231

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Research ArticleArticle

Quinone Reductase 2 Inhibitor: S29434

Jean A. Boutin, Frederic Bouillaud, Elzbieta Janda, István Gacsalyi, Gérald Guillaumet, Etienne C. Hirsch, Daniel A. Kane, Françoise Nepveu, Karine Reybier, Philippe Dupuis, Marc Bertrand, Monivan Chhour, Thierry Le Diguarher, Mathias Antoine, Karen Brebner, Hervé Da Costa, Pierre Ducrot, Adeline Giganti, Vishalgiri Goswami, Hala Guedouari, Patrick P. Michel, Aakash Patel, Jérôme Paysant, Johann Stojko, Marie-Claude Viaud-Massuard and Gilles Ferry
Molecular Pharmacology March 1, 2019, 95 (3) 269-285; DOI: https://doi.org/10.1124/mol.118.114231
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