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Stretch-activated ion channel TMEM63B associates with developmental and epileptic encephalopathies and progressive neurodegeneration

The American Journal of Human Genetics, ISSN: 0002-9297, Vol: 110, Issue: 8, Page: 1356-1376
2023
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Article Description

By converting physical forces into electrical signals or triggering intracellular cascades, stretch-activated ion channels allow the cell to respond to osmotic and mechanical stress. Knowledge of the pathophysiological mechanisms underlying associations of stretch-activated ion channels with human disease is limited. Here, we describe 17 unrelated individuals with severe early-onset developmental and epileptic encephalopathy (DEE), intellectual disability, and severe motor and cortical visual impairment associated with progressive neurodegenerative brain changes carrying ten distinct heterozygous variants of TMEM63B, encoding for a highly conserved stretch-activated ion channel. The variants occurred de novo in 16/17 individuals for whom parental DNA was available and either missense, including the recurrent p.Val44Met in 7/17 individuals, or in-frame, all affecting conserved residues located in transmembrane regions of the protein. In 12 individuals, hematological abnormalities co-occurred, such as macrocytosis and hemolysis, requiring blood transfusions in some. We modeled six variants (p.Val44Met, p.Arg433His, p.Thr481Asn, p.Gly580Ser, p.Arg660Thr, and p.Phe697Leu), each affecting a distinct transmembrane domain of the channel, in transfected Neuro2a cells and demonstrated inward leak cation currents across the mutated channel even in isotonic conditions, while the response to hypo-osmotic challenge was impaired, as were the Ca 2+ transients generated under hypo-osmotic stimulation. Ectopic expression of the p.Val44Met and p.Gly580Cys variants in Drosophila resulted in early death. TMEM63B -associated DEE represents a recognizable clinicopathological entity in which altered cation conductivity results in a severe neurological phenotype with progressive brain damage and early-onset epilepsy associated with hematological abnormalities in most individuals.

Bibliographic Details

Annalisa Vetro; Cristiana Pelorosso; Simona Balestrini; Valerio Conti; Davide Mei; Renzo Guerrini; Alessio Masi; Guido Mannaioni; Sophie Hambleton; Anita Devlin; Emanuela Argilli; Elliott Sherr; Simone Giubbolini; Riccardo Parra; Gian Michele Ratto; Rebekah Barrick; Gaber Bergant; Karin Writzl; Emilia K. Bijlsma; Mariëtte J.V. Hoffer; Theresa Brunet; Celina von Stülpnagel; Pilar Cacheiro; Damian Smedley; Keren Machol; Masamune Sakamoto; Naomichi Matsumoto; Manoj P. Menezes; Thomas Courtin; Ruth Richardson; Emma Vittery; Tony Roscioli; Marcello Scala; Annalaura Torella; Jun Tohyama; Reiko Koichihara; Keisuke Hamada; Kazuhiro Ogata; Takashi Suzuki; Atsushi Sugie; Jasper J. van der Smagt; Koen van Gassen; Stephanie Valence; Stephen Malone; Mitsuhiro Kato; Francesca Pochiero; Francesco Mari; Venkateswaran Ramesh; Valeria Capra; Margherita Mancardi; Boris Keren; Cyiril Mignot; Matteo Lulli; Kendall Parks; Helen Griffin; Melanie Brugger; Vincenzo Nigro; Yuko Hirata; Borut Peterlin; Ryuto Maki; Yohei Nitta; John C. Ambrose; Prabhu Arumugam; Roel Bevers; Marta Bleda; Freya Boardman-Pretty; Christopher R. Boustred; Helen Brittain; Matthew A. Brown; Mark J. Caulfield; Georgia C. Chan; Adam Giess; John N. Griffin; Angela Hamblin; Shirley Henderson; Tim J.P. Hubbard; Rob Jackson; Louise J. Jones; Dalia Kasperaviciute; Melis Kayikci; Athanasios Kousathanas; Lea Lahnstein; Anna Lakey; Sarah E.A. Leigh; Ivonne U.S. Leong; Javier F. Lopez; Fiona Maleady-Crowe; Meriel McEntagart; Federico Minneci; Jonathan Mitchell; Loukas Moutsianas; Michael Mueller; Nirupa Murugaesu; Anna C. Need; Peter O'Donovan; Chris A. Odhams; Christine Patch; Daniel Perez-Gil; Marina B. Pereira; John Pullinger; Tahrima Rahim; Augusto Rendon; Tim Rogers; Kevin Savage; Kushmita Sawant; Richard H. Scott; Afshan Siddiq; Alexander Sieghart; Samuel C. Smith; Alona Sosinsky; Alexander Stuckey; Mélanie Tanguy; Ana Lisa Taylor Tavares; Ellen R.A. Thomas; Simon R. Thompson; Arianna Tucci; Matthew J. Welland; Eleanor Williams; Katarzyna Witkowska; Suzanne M. Wood; Magdalena Zarowiecki

Elsevier BV

Biochemistry, Genetics and Molecular Biology; Medicine

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