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Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain

Neuropathic pain is a major incurable clinical problem resulting from peripheral nerve trauma or disease. A central mechanism is the reduced expression of the potassium chloride cotransporter 2 (KCC2) in dorsal horn neurons induced by brain-derived neurotrophic factor (BDNF), causing neuronal disinh...

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Autores principales: Richner, Mette, Pallesen, Lone T., Ulrichsen, Maj, Poulsen, Ebbe T., Holm, Thomas H., Login, Hande, Castonguay, Annie, Lorenzo, Louis-Etienne, Gonçalves, Nádia P., Andersen, Olav M., Lykke-Hartmann, Karin, Enghild, Jan J., Rønn, Lars C. B., Malik, Ibrahim J., De Koninck, Yves, Bjerrum, Ole J., Vægter, Christian B., Nykjær, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6584543/
https://www.ncbi.nlm.nih.gov/pubmed/31223654
http://dx.doi.org/10.1126/sciadv.aav9946
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author Richner, Mette
Pallesen, Lone T.
Ulrichsen, Maj
Poulsen, Ebbe T.
Holm, Thomas H.
Login, Hande
Castonguay, Annie
Lorenzo, Louis-Etienne
Gonçalves, Nádia P.
Andersen, Olav M.
Lykke-Hartmann, Karin
Enghild, Jan J.
Rønn, Lars C. B.
Malik, Ibrahim J.
De Koninck, Yves
Bjerrum, Ole J.
Vægter, Christian B.
Nykjær, Anders
author_facet Richner, Mette
Pallesen, Lone T.
Ulrichsen, Maj
Poulsen, Ebbe T.
Holm, Thomas H.
Login, Hande
Castonguay, Annie
Lorenzo, Louis-Etienne
Gonçalves, Nádia P.
Andersen, Olav M.
Lykke-Hartmann, Karin
Enghild, Jan J.
Rønn, Lars C. B.
Malik, Ibrahim J.
De Koninck, Yves
Bjerrum, Ole J.
Vægter, Christian B.
Nykjær, Anders
author_sort Richner, Mette
collection PubMed
description Neuropathic pain is a major incurable clinical problem resulting from peripheral nerve trauma or disease. A central mechanism is the reduced expression of the potassium chloride cotransporter 2 (KCC2) in dorsal horn neurons induced by brain-derived neurotrophic factor (BDNF), causing neuronal disinhibition within spinal nociceptive pathways. Here, we demonstrate how neurotensin receptor 2 (NTSR2) signaling impairs BDNF-induced spinal KCC2 down-regulation, showing how these two pathways converge to control the abnormal sensory response following peripheral nerve injury. We establish how sortilin regulates this convergence by scavenging neurotensin from binding to NTSR2, thus modulating its inhibitory effect on BDNF-mediated mechanical allodynia. Using sortilin-deficient mice or receptor inhibition by antibodies or a small-molecule antagonist, we lastly demonstrate that we are able to fully block BDNF-induced pain and alleviate injury-induced neuropathic pain, validating sortilin as a clinically relevant target.
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spelling pubmed-65845432019-06-20 Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain Richner, Mette Pallesen, Lone T. Ulrichsen, Maj Poulsen, Ebbe T. Holm, Thomas H. Login, Hande Castonguay, Annie Lorenzo, Louis-Etienne Gonçalves, Nádia P. Andersen, Olav M. Lykke-Hartmann, Karin Enghild, Jan J. Rønn, Lars C. B. Malik, Ibrahim J. De Koninck, Yves Bjerrum, Ole J. Vægter, Christian B. Nykjær, Anders Sci Adv Research Articles Neuropathic pain is a major incurable clinical problem resulting from peripheral nerve trauma or disease. A central mechanism is the reduced expression of the potassium chloride cotransporter 2 (KCC2) in dorsal horn neurons induced by brain-derived neurotrophic factor (BDNF), causing neuronal disinhibition within spinal nociceptive pathways. Here, we demonstrate how neurotensin receptor 2 (NTSR2) signaling impairs BDNF-induced spinal KCC2 down-regulation, showing how these two pathways converge to control the abnormal sensory response following peripheral nerve injury. We establish how sortilin regulates this convergence by scavenging neurotensin from binding to NTSR2, thus modulating its inhibitory effect on BDNF-mediated mechanical allodynia. Using sortilin-deficient mice or receptor inhibition by antibodies or a small-molecule antagonist, we lastly demonstrate that we are able to fully block BDNF-induced pain and alleviate injury-induced neuropathic pain, validating sortilin as a clinically relevant target. American Association for the Advancement of Science 2019-06-19 /pmc/articles/PMC6584543/ /pubmed/31223654 http://dx.doi.org/10.1126/sciadv.aav9946 Text en Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). http://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Research Articles
Richner, Mette
Pallesen, Lone T.
Ulrichsen, Maj
Poulsen, Ebbe T.
Holm, Thomas H.
Login, Hande
Castonguay, Annie
Lorenzo, Louis-Etienne
Gonçalves, Nádia P.
Andersen, Olav M.
Lykke-Hartmann, Karin
Enghild, Jan J.
Rønn, Lars C. B.
Malik, Ibrahim J.
De Koninck, Yves
Bjerrum, Ole J.
Vægter, Christian B.
Nykjær, Anders
Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title_full Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title_fullStr Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title_full_unstemmed Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title_short Sortilin gates neurotensin and BDNF signaling to control peripheral neuropathic pain
title_sort sortilin gates neurotensin and bdnf signaling to control peripheral neuropathic pain
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6584543/
https://www.ncbi.nlm.nih.gov/pubmed/31223654
http://dx.doi.org/10.1126/sciadv.aav9946
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