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HCN2-associated neurodevelopmental disorders: data from patients and xenopus cell models

Objective We aimed to characterize the phenotypic spectrum and functional consequences associated with variants in HCN2, encoding for the hyperpolarization-activated cyclic nucleotide (HCN) gated channel 2. Methods GeneMatcher facilitated the recruitment of 21 individuals with HCN2 variants from 15...

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Hauptverfasser: Houdayer, Clara (VerfasserIn) , Phillips, A. Marie (VerfasserIn) , Chabbert, Marie (VerfasserIn) , Bourreau, Jennifer (VerfasserIn) , Maroofian, Reza (VerfasserIn) , Houlden, Henry (VerfasserIn) , Richards, Kay (VerfasserIn) , Saadi, Nebal Waill (VerfasserIn) , Dad'ová, Eliška (VerfasserIn) , Van Bogaert, Patrick (VerfasserIn) , Rupin, Mailys (VerfasserIn) , Keren, Boris (VerfasserIn) , Charles, Perrine (VerfasserIn) , Smol, Thomas (VerfasserIn) , Riquet, Audrey (VerfasserIn) , Pais, Lynn (VerfasserIn) , O'Donnell-Luria, Anne (VerfasserIn) , VanNoy, Grace E. (VerfasserIn) , Bayat, Allan (VerfasserIn) , Møller, Rikke S (VerfasserIn) , Olofsson, Kern (VerfasserIn) , Jamra, Rami Abou (VerfasserIn) , Syrbe, Steffen (VerfasserIn) , Dasouki, Majed (VerfasserIn) , Seaver, Laurie H. (VerfasserIn) , Sullivan, Jennifer A. (VerfasserIn) , Shashi, Vandana (VerfasserIn) , Alkuraya, Fowzan S. (VerfasserIn) , Poss, Alexis F. (VerfasserIn) , Spence, J. Edward (VerfasserIn) , Schnur, Rhonda E. (VerfasserIn) , Forster, Ian C. (VerfasserIn) , Mckenzie, Chaseley E. (VerfasserIn) , Simons, Cas (VerfasserIn) , Wang, Min (VerfasserIn) , Snell, Penny (VerfasserIn) , Kothur, Kavitha (VerfasserIn) , Buckley, Michael (VerfasserIn) , Roscioli, Tony (VerfasserIn) , Elserafy, Noha (VerfasserIn) , Dauriat, Benjamin (VerfasserIn) , Procaccio, Vincent (VerfasserIn) , Henrion, Daniel (VerfasserIn) , Lenaers, Guy (VerfasserIn) , Colin, Estelle (VerfasserIn) , Verbeek, Nienke E. (VerfasserIn) , Van Gassen, Koen L. (VerfasserIn) , Legendre, Claire (VerfasserIn) , Bonneau, Dominique (VerfasserIn) , Reid, Christopher A. (VerfasserIn) , Howell, Katherine B. (VerfasserIn) , Ziegler, Alban (VerfasserIn) , Legros, Christian (VerfasserIn)
Dokumenttyp: Article (Journal)
Sprache:Englisch
Veröffentlicht: Sep 2025
In: Annals of neurology
Year: 2025, Jahrgang: 98, Heft: 3, Pages: 573-589
ISSN:1531-8249
DOI:10.1002/ana.27277
Online-Zugang:Verlag, kostenfrei, Volltext: https://doi.org/10.1002/ana.27277
Verlag, kostenfrei, Volltext: https://onlinelibrary.wiley.com/doi/abs/10.1002/ana.27277
Volltext
Verfasserangaben:Clara Houdayer, MSc, MD, A. Marie Phillips, PhD, Marie Chabbert, PhD, Jennifer Bourreau, BS, Reza Maroofian, PhD, Henry Houlden, MD, Kay Richards, PhD, Nebal Waill Saadi, MD, Eliska Dad’ová, MS, Patrick Van Bogaert, MD, PhD, Mailys Rupin, MD, Boris Keren, MD, Perrine Charles, MD, PhD, Thomas Smol, MD, PhD, Audrey Riquet, MD, Lynn Pais, MS, Anne O’Donnell-Luria, MD, PhD, Grace E. VanNoy, MS, Allan Bayat, MD, PhD, Rikke S Møller, PhD, Kern Olofsson, MD, Rami Abou Jamra, MD, Steffen Syrbe, MD, PhD, Majed Dasouki, MD, Laurie H. Seaver, MD, Jennifer A. Sullivan, MS, Vandana Shashi, MBBS, MD, Fowzan S. Alkuraya, MD, Alexis F. Poss, MS, J. Edward Spence, MD, Rhonda E. Schnur, MD, Ian C. Forster, PhD, Chaseley E. Mckenzie, MS, Cas Simons, PhD, Min Wang, PhD, Penny Snell, MGenCouns, Kavitha Kothur, MD, PhD, Michael Buckley, MD, Tony Roscioli, MD, PhD, Noha Elserafy, MD, Benjamin Dauriat, MD, Vincent Procaccio, MD, PhD, Daniel Henrion, PharmD, PhD, Guy Lenaers, PhD, Estelle Colin, MD, PhD, Nienke E. Verbeek, MD, PhD, Koen L. Van Gassen, MD, PhD, Claire Legendre, PhD, Dominique Bonneau, MD, PhD, Christopher A. Reid, PhD, Katherine B. Howell, MBBS, PhD , Alban Ziegler, MD, PhD, and Christian Legros, PhD

MARC

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520 |a Objective We aimed to characterize the phenotypic spectrum and functional consequences associated with variants in HCN2, encoding for the hyperpolarization-activated cyclic nucleotide (HCN) gated channel 2. Methods GeneMatcher facilitated the recruitment of 21 individuals with HCN2 variants from 15 unrelated families, carrying HCN2 variants. In vitro functional studies were performed by electrophysiology with Xenopus laevis oocytes and membrane trafficking was investigated in HEK cells by confocal imaging. Structural 3D-analysis of the HCN2 variants was performed. Results The phenotypic spectrum included developmental delay/intellectual disability (DD/ID, 17/21), epilepsy (10/21), language disorders (16/21), movement disorders (12/21), and axial hypotonia (10/21). Thirteen pathogenic variants (12 new and 1 already described) were identified: 11 missense (8 monoallelic and 3 biallelic), 1 recurrent inframe deletion (monoallelic), and 1 frameshift (biallelic). Functional analysis of p.(Arg324His) variant showed a strong increase of HCN2 conductance, whereas p.(Ala363Val) and p.(Met374Leu) exhibited dominant negative effects. The p.(Leu377His), p.(Pro493Leu), and p.(Gly587Asp) variants rendered HCN2 electrophysiologically silent and impaired membrane trafficking. Structural 3D-analysis revealed that, except for p.(Arg324His), all variants altered HCN2 stability. Interpretation Our findings broadened the HCN2 disease clinical spectrum to include DD/ID with or without epilepsy. Functional analysis in cellular models reveal that pathogenic HCN2 variants can cause either loss-of-function or gain-of-function, providing critical information for the development of targeted therapies for HCN2-related disorders. ANN NEUROL 2025;98:573-589 
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