Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models

Abstract Objective Charcot–Marie Tooth (CMT) is a hereditary neuropathy characterized by muscle weakness and fatigue with no approved therapies. Preclinical studies implicate neuromuscular junction (NMJ) transmission deficits in muscle dysfunction in CMT. This study aimed to evaluate NMJ function in...

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Main Authors: Thomas Skjærlund Grønnebæk, Helga Haahr‐Lillevang, Martin Skov, Kristina Kelly, Nathan R. Kerr, Jose A. Viteri, Andrea Jaworek, Amy Bartlett, Jane Bold, John Hutchison, Jorge Quiroz, Hatice Tankisi, Thomas Holm Pedersen, Henning Andersen, William David Arnold
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Annals of Clinical and Translational Neurology
Online Access:https://doi.org/10.1002/acn3.52252
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author Thomas Skjærlund Grønnebæk
Helga Haahr‐Lillevang
Martin Skov
Kristina Kelly
Nathan R. Kerr
Jose A. Viteri
Andrea Jaworek
Amy Bartlett
Jane Bold
John Hutchison
Jorge Quiroz
Hatice Tankisi
Thomas Holm Pedersen
Henning Andersen
William David Arnold
author_facet Thomas Skjærlund Grønnebæk
Helga Haahr‐Lillevang
Martin Skov
Kristina Kelly
Nathan R. Kerr
Jose A. Viteri
Andrea Jaworek
Amy Bartlett
Jane Bold
John Hutchison
Jorge Quiroz
Hatice Tankisi
Thomas Holm Pedersen
Henning Andersen
William David Arnold
author_sort Thomas Skjærlund Grønnebæk
collection DOAJ
description Abstract Objective Charcot–Marie Tooth (CMT) is a hereditary neuropathy characterized by muscle weakness and fatigue with no approved therapies. Preclinical studies implicate neuromuscular junction (NMJ) transmission deficits in muscle dysfunction in CMT. This study aimed to evaluate NMJ function in patients with CMT types 1 and 2, and to determine whether enhancing NMJ transmission can improve muscle function in preclinical CMT models. Methods First, an observational study involving single fiber electromyography (SFEMG) and clinical testing in patients with CMT 1 and 2 and healthy controls (HC) was conducted. Next, preclinical studies examined muscle function, specifically nerve‐stimulated muscle force after partially inhibiting ClC‐1 chloride channels with the novel small molecule NMD670. Results Twenty‐one CMT patients (46.4 ± 14.4 years) and 10 HC (43.3 ± 12.7 years) were enrolled. SFEMG jitter (NMJ variability) was higher [median (range)] in the CMT patients [56 μs (35; 197 μs)] vs. HC [29 μs (19; 36 μs)], (p < 0.05). Blocking (NMJ failure) was higher in the CMT patients (13.4% (0.0; 90.9%)) vs. HC (0.0% (0.0; 4.5%)), (p < 0.05). In CMT, jitter and blocking correlated inversely with muscle strength, mobility, balance, and endurance. In CMT 1A and 2D mice, NMD670 increased both peak force and contractile endurance in vivo. Interpretation Our study suggests that NMJ dysfunction contributes to muscle dysfunction in patients with CMT 1 and 2. Furthermore, our preclinical data provide proof‐of‐mechanism for recovery of muscle function with ClC‐1 inhibition in CMT mouse models. Collectively, these findings suggest that targeting NMJ dysfunction with ClC‐1 inhibitors could enhance muscle function in CMT patients, warranting further clinical trials.
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spelling doaj-art-29f7575ec0fd41cca95b1ea4a34acfc52025-08-20T02:28:00ZengWileyAnnals of Clinical and Translational Neurology2328-95032025-02-0112232033110.1002/acn3.52252Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal modelsThomas Skjærlund Grønnebæk0Helga Haahr‐Lillevang1Martin Skov2Kristina Kelly3Nathan R. Kerr4Jose A. Viteri5Andrea Jaworek6Amy Bartlett7Jane Bold8John Hutchison9Jorge Quiroz10Hatice Tankisi11Thomas Holm Pedersen12Henning Andersen13William David Arnold14NMD Pharma A/S Aarhus DenmarkDepartment of Neurology Aarhus University Hospital Aarhus DenmarkNMD Pharma A/S Aarhus DenmarkNextGen Precision Health University of Missouri Columbia Missouri USANextGen Precision Health University of Missouri Columbia Missouri USANextGen Precision Health University of Missouri Columbia Missouri USADepartment of Neurology The Ohio State University Columbus OH USADepartment of Neurology The Ohio State University Columbus OH USANMD Pharma A/S Aarhus DenmarkNMD Pharma A/S Aarhus DenmarkNMD Pharma A/S Aarhus DenmarkDepartment of Neurology Aarhus University Hospital Aarhus DenmarkNMD Pharma A/S Aarhus DenmarkDepartment of Neurology Aarhus University Hospital Aarhus DenmarkNextGen Precision Health University of Missouri Columbia Missouri USAAbstract Objective Charcot–Marie Tooth (CMT) is a hereditary neuropathy characterized by muscle weakness and fatigue with no approved therapies. Preclinical studies implicate neuromuscular junction (NMJ) transmission deficits in muscle dysfunction in CMT. This study aimed to evaluate NMJ function in patients with CMT types 1 and 2, and to determine whether enhancing NMJ transmission can improve muscle function in preclinical CMT models. Methods First, an observational study involving single fiber electromyography (SFEMG) and clinical testing in patients with CMT 1 and 2 and healthy controls (HC) was conducted. Next, preclinical studies examined muscle function, specifically nerve‐stimulated muscle force after partially inhibiting ClC‐1 chloride channels with the novel small molecule NMD670. Results Twenty‐one CMT patients (46.4 ± 14.4 years) and 10 HC (43.3 ± 12.7 years) were enrolled. SFEMG jitter (NMJ variability) was higher [median (range)] in the CMT patients [56 μs (35; 197 μs)] vs. HC [29 μs (19; 36 μs)], (p < 0.05). Blocking (NMJ failure) was higher in the CMT patients (13.4% (0.0; 90.9%)) vs. HC (0.0% (0.0; 4.5%)), (p < 0.05). In CMT, jitter and blocking correlated inversely with muscle strength, mobility, balance, and endurance. In CMT 1A and 2D mice, NMD670 increased both peak force and contractile endurance in vivo. Interpretation Our study suggests that NMJ dysfunction contributes to muscle dysfunction in patients with CMT 1 and 2. Furthermore, our preclinical data provide proof‐of‐mechanism for recovery of muscle function with ClC‐1 inhibition in CMT mouse models. Collectively, these findings suggest that targeting NMJ dysfunction with ClC‐1 inhibitors could enhance muscle function in CMT patients, warranting further clinical trials.https://doi.org/10.1002/acn3.52252
spellingShingle Thomas Skjærlund Grønnebæk
Helga Haahr‐Lillevang
Martin Skov
Kristina Kelly
Nathan R. Kerr
Jose A. Viteri
Andrea Jaworek
Amy Bartlett
Jane Bold
John Hutchison
Jorge Quiroz
Hatice Tankisi
Thomas Holm Pedersen
Henning Andersen
William David Arnold
Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
Annals of Clinical and Translational Neurology
title Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
title_full Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
title_fullStr Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
title_full_unstemmed Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
title_short Neuromuscular transmission deficits in patients with CMT and ClC‐1 inhibition in CMT animal models
title_sort neuromuscular transmission deficits in patients with cmt and clc 1 inhibition in cmt animal models
url https://doi.org/10.1002/acn3.52252
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