Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1783428530770542592 |
---|---|
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. |
format | Online Article Text |
id | pubmed-6584543 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | American Association for the Advancement of Science |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT richnermette sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT pallesenlonet sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT ulrichsenmaj sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT poulsenebbet sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT holmthomash sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT loginhande sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT castonguayannie sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT lorenzolouisetienne sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT goncalvesnadiap sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT andersenolavm sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT lykkehartmannkarin sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT enghildjanj sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT rønnlarscb sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT malikibrahimj sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT dekoninckyves sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT bjerrumolej sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT vægterchristianb sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain AT nykjæranders sortilingatesneurotensinandbdnfsignalingtocontrolperipheralneuropathicpain |