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Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain

Pain often persists in patients with an inflammatory disease, even when inflammation has subsided. The molecular mechanisms leading to this failure in pain resolution and the transition to chronic pain are poorly understood. Mitochondrial dysfunction in sensory neurons links to chronic pain, but its...

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Autores principales: Willemen, Hanneke L.D.M., Santos Ribeiro, Patrícia Silva, Broeks, Melissa, Meijer, Nils, Versteeg, Sabine, Tiggeler, Annefien, de Boer, Teun P., Małecki, Jędrzej M., Falnes, Pål Ø., Jans, Judith, Eijkelkamp, Niels
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694662/
https://www.ncbi.nlm.nih.gov/pubmed/37944527
http://dx.doi.org/10.1016/j.xcrm.2023.101265
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author Willemen, Hanneke L.D.M.
Santos Ribeiro, Patrícia Silva
Broeks, Melissa
Meijer, Nils
Versteeg, Sabine
Tiggeler, Annefien
de Boer, Teun P.
Małecki, Jędrzej M.
Falnes, Pål Ø.
Jans, Judith
Eijkelkamp, Niels
author_facet Willemen, Hanneke L.D.M.
Santos Ribeiro, Patrícia Silva
Broeks, Melissa
Meijer, Nils
Versteeg, Sabine
Tiggeler, Annefien
de Boer, Teun P.
Małecki, Jędrzej M.
Falnes, Pål Ø.
Jans, Judith
Eijkelkamp, Niels
author_sort Willemen, Hanneke L.D.M.
collection PubMed
description Pain often persists in patients with an inflammatory disease, even when inflammation has subsided. The molecular mechanisms leading to this failure in pain resolution and the transition to chronic pain are poorly understood. Mitochondrial dysfunction in sensory neurons links to chronic pain, but its role in resolution of inflammatory pain is unclear. Transient inflammation causes neuronal plasticity, called hyperalgesic priming, which impairs resolution of pain induced by a subsequent inflammatory stimulus. We identify that hyperalgesic priming in mice increases the expression of a mitochondrial protein (ATPSc-KMT) and causes mitochondrial and metabolic disturbances in sensory neurons. Inhibition of mitochondrial respiration, knockdown of ATPSCKMT expression, or supplementation of the affected metabolite is sufficient to restore resolution of inflammatory pain and prevents chronic pain development. Thus, inflammation-induced mitochondrial-dependent disturbances in sensory neurons predispose to a failure in resolution of inflammatory pain and development of chronic pain.
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spelling pubmed-106946622023-12-05 Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain Willemen, Hanneke L.D.M. Santos Ribeiro, Patrícia Silva Broeks, Melissa Meijer, Nils Versteeg, Sabine Tiggeler, Annefien de Boer, Teun P. Małecki, Jędrzej M. Falnes, Pål Ø. Jans, Judith Eijkelkamp, Niels Cell Rep Med Article Pain often persists in patients with an inflammatory disease, even when inflammation has subsided. The molecular mechanisms leading to this failure in pain resolution and the transition to chronic pain are poorly understood. Mitochondrial dysfunction in sensory neurons links to chronic pain, but its role in resolution of inflammatory pain is unclear. Transient inflammation causes neuronal plasticity, called hyperalgesic priming, which impairs resolution of pain induced by a subsequent inflammatory stimulus. We identify that hyperalgesic priming in mice increases the expression of a mitochondrial protein (ATPSc-KMT) and causes mitochondrial and metabolic disturbances in sensory neurons. Inhibition of mitochondrial respiration, knockdown of ATPSCKMT expression, or supplementation of the affected metabolite is sufficient to restore resolution of inflammatory pain and prevents chronic pain development. Thus, inflammation-induced mitochondrial-dependent disturbances in sensory neurons predispose to a failure in resolution of inflammatory pain and development of chronic pain. Elsevier 2023-11-08 /pmc/articles/PMC10694662/ /pubmed/37944527 http://dx.doi.org/10.1016/j.xcrm.2023.101265 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Willemen, Hanneke L.D.M.
Santos Ribeiro, Patrícia Silva
Broeks, Melissa
Meijer, Nils
Versteeg, Sabine
Tiggeler, Annefien
de Boer, Teun P.
Małecki, Jędrzej M.
Falnes, Pål Ø.
Jans, Judith
Eijkelkamp, Niels
Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title_full Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title_fullStr Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title_full_unstemmed Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title_short Inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
title_sort inflammation-induced mitochondrial and metabolic disturbances in sensory neurons control the switch from acute to chronic pain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694662/
https://www.ncbi.nlm.nih.gov/pubmed/37944527
http://dx.doi.org/10.1016/j.xcrm.2023.101265
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