Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment

The potassium sodium-activated channel subtype T member 1 (<i>KCNT1</i>) gene encodes the Slack channel K<sub>Na</sub>1.1, which is expressed in neurons throughout the brain. Gain-of-function variants in <i>KCNT1</i> are associated with a spectrum of epilepsy synd...

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Main Authors: Fangxu Sun, Huafeng Wang, Jing Wu, Imran H. Quraishi, Yalan Zhang, Maysam Pedram, Benbo Gao, Elizabeth A. Jonas, Viet Nguyen, Sijia Wu, Omar S. Mabrouk, Paymaan Jafar-nejad, Leonard K. Kaczmarek
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Language:English
Published: MDPI AG 2024-11-01
Series:Biomolecules
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Online Access:https://www.mdpi.com/2218-273X/14/11/1397
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author Fangxu Sun
Huafeng Wang
Jing Wu
Imran H. Quraishi
Yalan Zhang
Maysam Pedram
Benbo Gao
Elizabeth A. Jonas
Viet Nguyen
Sijia Wu
Omar S. Mabrouk
Paymaan Jafar-nejad
Leonard K. Kaczmarek
author_facet Fangxu Sun
Huafeng Wang
Jing Wu
Imran H. Quraishi
Yalan Zhang
Maysam Pedram
Benbo Gao
Elizabeth A. Jonas
Viet Nguyen
Sijia Wu
Omar S. Mabrouk
Paymaan Jafar-nejad
Leonard K. Kaczmarek
author_sort Fangxu Sun
collection DOAJ
description The potassium sodium-activated channel subtype T member 1 (<i>KCNT1</i>) gene encodes the Slack channel K<sub>Na</sub>1.1, which is expressed in neurons throughout the brain. Gain-of-function variants in <i>KCNT1</i> are associated with a spectrum of epilepsy syndromes, and mice carrying those variants exhibit a robust phenotype similar to that observed in patients. <i>Kcnt1</i> knockout (KO) mice, however, have a normal lifespan without any epileptic phenotype. To understand the molecular differences between these two models, we conducted a comprehensive proteomic analysis of the cerebral cortices of <i>Kcnt1</i> KO and <i>Kcnt1</i><sup>R455H/+</sup> mice, an animal model bearing a cytoplasmic C-terminal mutation homologous to a human R474H variant that results in EIMFS. The greatest change observed in <i>Kcnt1</i> KO mice compared to the wild-type mice was the increased expression of multiple proteins of the inner mitochondrial membrane. Electron microscopy studies of cortical mitochondria from <i>Kcnt1</i> KO mice further confirmed a significant increase in the density of mitochondrial cristae compared to that in wild-type mice. <i>Kcnt1</i> reduction by a murine-specific <i>Kcnt1</i> antisense oligonucleotide (ASO) in <i>Kcnt1</i><sup>R455H/+</sup> mice partially corrected the proteomic dysregulations in the disease model. The results support the hypothesis that ASO-mediated <i>KCNT1</i> reduction could be therapeutically useful in the treatment of <i>KCNT1</i> epilepsies.
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spelling doaj-art-8a904d7c53544b2a91ebca9afa5698d42025-08-20T01:53:52ZengMDPI AGBiomolecules2218-273X2024-11-011411139710.3390/biom14111397Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide TreatmentFangxu Sun0Huafeng Wang1Jing Wu2Imran H. Quraishi3Yalan Zhang4Maysam Pedram5Benbo Gao6Elizabeth A. Jonas7Viet Nguyen8Sijia Wu9Omar S. Mabrouk10Paymaan Jafar-nejad11Leonard K. Kaczmarek12Biogen Inc., Cambridge, MA 02142, USADepartment of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USADepartment of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USADepartment of Neurology, Yale University School of Medicine, New Haven, CT 06520, USADepartment of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USADepartment of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USABiogen Inc., Cambridge, MA 02142, USADepartment of Internal Medicine, Yale School of Medicine, New Haven, CT 06520, USABiogen Inc., Cambridge, MA 02142, USABiogen Inc., Cambridge, MA 02142, USABiogen Inc., Cambridge, MA 02142, USAIonis Pharmaceuticals Inc., Carlsbad, CA 92010, USADepartment of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USAThe potassium sodium-activated channel subtype T member 1 (<i>KCNT1</i>) gene encodes the Slack channel K<sub>Na</sub>1.1, which is expressed in neurons throughout the brain. Gain-of-function variants in <i>KCNT1</i> are associated with a spectrum of epilepsy syndromes, and mice carrying those variants exhibit a robust phenotype similar to that observed in patients. <i>Kcnt1</i> knockout (KO) mice, however, have a normal lifespan without any epileptic phenotype. To understand the molecular differences between these two models, we conducted a comprehensive proteomic analysis of the cerebral cortices of <i>Kcnt1</i> KO and <i>Kcnt1</i><sup>R455H/+</sup> mice, an animal model bearing a cytoplasmic C-terminal mutation homologous to a human R474H variant that results in EIMFS. The greatest change observed in <i>Kcnt1</i> KO mice compared to the wild-type mice was the increased expression of multiple proteins of the inner mitochondrial membrane. Electron microscopy studies of cortical mitochondria from <i>Kcnt1</i> KO mice further confirmed a significant increase in the density of mitochondrial cristae compared to that in wild-type mice. <i>Kcnt1</i> reduction by a murine-specific <i>Kcnt1</i> antisense oligonucleotide (ASO) in <i>Kcnt1</i><sup>R455H/+</sup> mice partially corrected the proteomic dysregulations in the disease model. The results support the hypothesis that ASO-mediated <i>KCNT1</i> reduction could be therapeutically useful in the treatment of <i>KCNT1</i> epilepsies.https://www.mdpi.com/2218-273X/14/11/1397slackKCNT1K<sub>Na</sub>1.1epilepsyintellectual disabilityEIMFS
spellingShingle Fangxu Sun
Huafeng Wang
Jing Wu
Imran H. Quraishi
Yalan Zhang
Maysam Pedram
Benbo Gao
Elizabeth A. Jonas
Viet Nguyen
Sijia Wu
Omar S. Mabrouk
Paymaan Jafar-nejad
Leonard K. Kaczmarek
Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
Biomolecules
slack
KCNT1
K<sub>Na</sub>1.1
epilepsy
intellectual disability
EIMFS
title Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
title_full Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
title_fullStr Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
title_full_unstemmed Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
title_short Molecular Profiling of Mouse Models of Loss or Gain of Function of the KCNT1 (Slack) Potassium Channel and Antisense Oligonucleotide Treatment
title_sort molecular profiling of mouse models of loss or gain of function of the kcnt1 slack potassium channel and antisense oligonucleotide treatment
topic slack
KCNT1
K<sub>Na</sub>1.1
epilepsy
intellectual disability
EIMFS
url https://www.mdpi.com/2218-273X/14/11/1397
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