Literature DB >> 31978607

Neuron-specific Kv1.1 deficiency is sufficient to cause epilepsy, premature death, and cardiorespiratory dysregulation.

Krystle Trosclair1, Hemangini A Dhaibar2, Nicole M Gautier3, Vikas Mishra4, Edward Glasscock5.   

Abstract

Sudden unexpected death in epilepsy (SUDEP) is the leading cause of epilepsy-related mortality, but the precise cellular substrates involved remain elusive. Epilepsy-associated ion channel genes with co-expression in brain and heart have been proposed as SUDEP candidate genes since they provide a singular unifying link between seizures and lethal cardiac arrhythmias. Here, we generated a conditional knockout (cKO) mouse with neuron-specific deletion of Kcna1, a SUDEP-associated gene with brain-heart co-expression, to test whether seizure-evoked cardiac arrhythmias and SUDEP require the absence of Kv1.1 in both brain and heart or whether ablation in neurons is sufficient. To obtain cKO mice, we developed a floxed Kcna1 mouse which we crossed to mice with the Synapsin1-Cre transgene, which selectively deletes Kcna1 in most neurons. Molecular analyses confirmed neuron-specific Kcna1 deletion in cKO mice and corresponding loss of Kv1.1 except in cerebellum where Synapsin1-Cre is not highly expressed. Survival studies and electroencephalography, electrocardiography, and plethysmography recordings showed that cKO mice exhibit premature death, epilepsy, and cardiorespiratory dysregulation but to a lesser degree than global knockouts. Heart rate variability (HRV) was increased in cKO mice with peaks during daytime suggesting disturbed diurnal HRV patterns as a SUDEP biomarker. Residual Kv1.1 expression in cKO cerebellum suggests it may play an unexpected role in regulating ictal cardiorespiratory dysfunction and SUDEP risk. This work demonstrates the principle that channelopathies with brain-heart expression patterns can increase death risk by brain-driven mechanisms alone without a functionally compromised heart, reinforcing seizure control as a primary clinical strategy for SUDEP prevention.
Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Apnea; Epilepsy; Heart rate variability; Kcna1; Kv1.1; Sudden unexpected death in epilepsy (SUDEP)

Mesh:

Substances:

Year:  2020        PMID: 31978607      PMCID: PMC7050436          DOI: 10.1016/j.nbd.2020.104759

Source DB:  PubMed          Journal:  Neurobiol Dis        ISSN: 0969-9961            Impact factor:   5.996


  57 in total

1.  Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: role of potassium channels under the myelin sheath in young nerves.

Authors:  L Zhou; C L Zhang; A Messing; S Y Chiu
Journal:  J Neurosci       Date:  1998-09-15       Impact factor: 6.167

2.  Expression of Kv1.1, a Shaker-like potassium channel, is temporally regulated in embryonic neurons and glia.

Authors:  J L Hallows; B L Tempel
Journal:  J Neurosci       Date:  1998-08-01       Impact factor: 6.167

3.  Incidence and mechanisms of cardiorespiratory arrests in epilepsy monitoring units (MORTEMUS): a retrospective study.

Authors:  Philippe Ryvlin; Lina Nashef; Samden D Lhatoo; Lisa M Bateman; Jonathan Bird; Andrew Bleasel; Paul Boon; Arielle Crespel; Barbara A Dworetzky; Hans Høgenhaven; Holger Lerche; Louis Maillard; Michael P Malter; Cecile Marchal; Jagarlapudi M K Murthy; Michael Nitsche; Ekaterina Pataraia; Terje Rabben; Sylvain Rheims; Bernard Sadzot; Andreas Schulze-Bonhage; Masud Seyal; Elson L So; Mark Spitz; Anna Szucs; Meng Tan; James X Tao; Torbjörn Tomson
Journal:  Lancet Neurol       Date:  2013-09-04       Impact factor: 44.182

Review 4.  Mechanisms of sudden unexpected death in epilepsy: the pathway to prevention.

Authors:  Cory A Massey; Levi P Sowers; Brian J Dlouhy; George B Richerson
Journal:  Nat Rev Neurol       Date:  2014-04-22       Impact factor: 42.937

5.  A novel mutation in the human voltage-gated potassium channel gene (Kv1.1) associates with episodic ataxia type 1 and sometimes with partial epilepsy.

Authors:  S M Zuberi; L H Eunson; A Spauschus; R De Silva; J Tolmie; N W Wood; R C McWilliam; J B Stephenson; J P Stephenson; D M Kullmann; M G Hanna
Journal:  Brain       Date:  1999-05       Impact factor: 13.501

6.  Long-term mortality in childhood-onset epilepsy.

Authors:  Matti Sillanpää; Shlomo Shinnar
Journal:  N Engl J Med       Date:  2010-12-23       Impact factor: 91.245

7.  Alterations of biological features of the cerebellum in sudden perinatal and infant death.

Authors:  Anna Maria Lavezzi; Giulia Ottaviani; Maria Mauri; Luigi Matturri
Journal:  Curr Mol Med       Date:  2006-06       Impact factor: 2.222

8.  Pharmacogenetics of KCNQ channel activation in 2 potassium channelopathy mouse models of epilepsy.

Authors:  Stephanie L Vanhoof-Villalba; Nicole M Gautier; Vikas Mishra; Edward Glasscock
Journal:  Epilepsia       Date:  2017-12-19       Impact factor: 5.864

9.  Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice.

Authors:  Petra May; Astrid Rohlmann; Hans H Bock; Kai Zurhove; Jamey D Marth; Eike D Schomburg; Jeffrey L Noebels; Uwe Beffert; J David Sweatt; Edwin J Weeber; Joachim Herz
Journal:  Mol Cell Biol       Date:  2004-10       Impact factor: 4.272

10.  The analysis of circadian rhythm of heart rate variability in patients with drug-resistant epilepsy.

Authors:  Zhao Yang; Hongyun Liu; Fangang Meng; Yuguang Guan; Mingming Zhao; Wei Qu; Hongwei Hao; Guoming Luan; Jianguo Zhang; Luming Li
Journal:  Epilepsy Res       Date:  2018-08-06       Impact factor: 3.045

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  9 in total

1.  Kv1.1 preserves the neural stem cell pool and facilitates neuron maturation during adult hippocampal neurogenesis.

Authors:  Yuan-Hung Lin King; Chao Chen; John V Lin King; Jeffrey Simms; Edward Glasscock; Shi-Bing Yang; Yuh-Nung Jan; Lily Y Jan
Journal:  Proc Natl Acad Sci U S A       Date:  2022-05-25       Impact factor: 12.779

Review 2.  Clinical Spectrum of KCNA1 Mutations: New Insights into Episodic Ataxia and Epilepsy Comorbidity.

Authors:  Kelsey Paulhus; Lauren Ammerman; Edward Glasscock
Journal:  Int J Mol Sci       Date:  2020-04-17       Impact factor: 5.923

3.  Kv1.1 potassium channel subunit deficiency alters ventricular arrhythmia susceptibility, contractility, and repolarization.

Authors:  Krystle Trosclair; Man Si; Megan Watts; Nicole M Gautier; Niels Voigt; James Traylor; Miklós Bitay; Istvan Baczko; Dobromir Dobrev; Kathryn A Hamilton; Md Shenuarin Bhuiyan; Paari Dominic; Edward Glasscock
Journal:  Physiol Rep       Date:  2021-01

4.  X-linked serotonin 2C receptor is associated with a non-canonical pathway for sudden unexpected death in epilepsy.

Authors:  Cory A Massey; Samantha J Thompson; Ryan W Ostrom; Janice Drabek; Olafur A Sveinsson; Torbjörn Tomson; Elisabeth A Haas; Othon J Mena; Alica M Goldman; Jeffrey L Noebels
Journal:  Brain Commun       Date:  2021-07-09

Review 5.  Cre-recombinase systems for induction of neuron-specific knockout models: a guide for biomedical researchers.

Authors:  Tetiana Shcholok; Eftekhar Eftekharpour
Journal:  Neural Regen Res       Date:  2023-02       Impact factor: 6.058

6.  Directed Connectivity Analysis of the Neuro-Cardio- and Respiratory Systems Reveals Novel Biomarkers of Susceptibility to SUDEP.

Authors:  T Noah Hutson; Farnaz Rezaei; Nicole M Gautier; Jagadeeswaran Indumathy; Edward Glasscock; Leonidas Iasemidis
Journal:  IEEE Open J Eng Med Biol       Date:  2020-11-06

Review 7.  Kv1.1 Channelopathies: Pathophysiological Mechanisms and Therapeutic Approaches.

Authors:  Maria Cristina D'Adamo; Antonella Liantonio; Jean-Francois Rolland; Mauro Pessia; Paola Imbrici
Journal:  Int J Mol Sci       Date:  2020-04-22       Impact factor: 5.923

Review 8.  The brain-heart interaction in epilepsy: implications for diagnosis, therapy, and SUDEP prevention.

Authors:  Giorgio Costagliola; Alessandro Orsini; Monica Coll; Ramon Brugada; Pasquale Parisi; Pasquale Striano
Journal:  Ann Clin Transl Neurol       Date:  2021-05-28       Impact factor: 4.511

9.  Severe deficiency of the voltage-gated sodium channel NaV1.2 elevates neuronal excitability in adult mice.

Authors:  Jingliang Zhang; Xiaoling Chen; Muriel Eaton; Jiaxiang Wu; Zhixiong Ma; Shirong Lai; Anthony Park; Talha S Ahmad; Zhefu Que; Ji Hea Lee; Tiange Xiao; Yuansong Li; Yujia Wang; Maria I Olivero-Acosta; James A Schaber; Krishna Jayant; Chongli Yuan; Zhuo Huang; Nadia A Lanman; William C Skarnes; Yang Yang
Journal:  Cell Rep       Date:  2021-08-03       Impact factor: 9.423

  9 in total

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