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@ARTICLE{Guzman:1043576,
author = {Guzman, Raul and Diaz Castillo, Alberto Rafael and
Aretzweiler von Schwartzenberg, Christoph and guanxiao, qi
and Steinmetz, Lilly and Bungert, Stefanie and Müller,
Frank and Feldmeyer, Dirk and Guzman, Raul},
title = {{E}ndosomal 2{C}l-/{H}+ exchangersregulate neuronal
excitability {B}ytuning {K}v7/{KCNQ} channel density},
journal = {Brain},
volume = {148},
issn = {0006-8950},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {FZJ-2025-02933},
pages = {4299–4314},
year = {2025},
note = {This work was funded by the German Research Foundation
(DFG) (GU 2042/2-1 to R.E.G.) and the European Union’s
Horizon 2020 Framework Programme for Research and Innovation
under the Human Brain Project Framework Partnership
Agreement (HBP FPA) (No. 650003 to D.F.).},
abstract = {CLCN3 and CLCN4 encode the endosomal 2Cl−/H+ exchangers
ClC-3 and ClC-4, which are highly expressed within the CNS,
including the hippocampal formation. Pathogenic variants
recently found in these genes have given rise to the rare
CLCN3- and CLCN4-related neurodevelopmental conditions,
characterized by a range of neurological and
neuropsychiatric complications, such as global developmental
delay, intellectual disability as a core feature, seizures,
behavioural issues and brain abnormalities. The mechanisms
by which ClC-3 and ClC-4 regulate neuronal function and
viability, in addition to the molecular pathways affected in
CLCN3- and CLCN4-related neurodevelopmental conditions,
remain unknown. In neurodegenerative diseases, neuronal
dendrites undergo pathological changes often associated with
aberrant electrical activity.To investigate how ClC-3 or
ClC-4 deficit alters neuronal excitability and morphology,
we combined patch-clamp recordings in acute hippocampal
slice preparations with simultaneous intracellular biocytin
filling. We analysed the functional and structural
properties of Clcn3−/− and Clcn4−/− neurons. Two
firing patterns are found in the cornu ammonis 2 (CA2)
region of the hippocampus: regular and burst firing. At
postnatal Day 13, $62\%$ of the assessed CA2 wild-type
neurons showed a rhythmic bursting behaviour; this was
reduced to $19\%$ in Clcn4−/− and completely absent in
the Clcn3−/− condition. Changes in the firing patterns
were accompanied by a depolarizing shift in the action
potential threshold and an increase in the
after-hyperpolarizing phase of the action potentials.
Blockade of Kv7/KCNQ and, to a lesser extent, Kv1, but not
BK, SK or Kv2 channels, recapitulates the wild-type firing
pattern phenotype in the Clcn3−/− condition. Moreover,
we detected abnormalities in the complexity of the dendritic
arborization. Branching and lengths of apical and basal
domains were significantly reduced in the Clcn3−/−
neurons and moderately altered in the Clcn4−/− neurons.
At postnatal Day 3, we found $25\%$ of bursting neurons in
Clcn3−/− with no significant morphological abnormalities
in the dendritic arborization in comparison to the
wild-type, suggesting that functional defects precede
structural changes in Cl−/H+ exchanger-deficient neurons.
Likewise, dentate granule cells exhibited defective action
potential properties and reduced burst-firing activity,
which was substantially but not fully rescued by Kv7/KCNQ
blockage.We conclude that Cl−/H+ exchangers regulate the
electrical excitability and firing patterns of neurons
primarily by fine- tuning Kv7/KCNQ channel density, and that
functional defects might contribute to alterations in
dendritic morphology. Our findings provide new insights into
the underlying molecular mechanisms of Cl−/H+ exchangers
in neurons and pave the way for potential therapeutic
interventions for CLCN3- and CLCN4-related patients
associated with disruption of Cl−/H+ exchange function.},
cin = {IBI-1 / INM-10},
ddc = {610},
cid = {I:(DE-Juel1)IBI-1-20200312 / I:(DE-Juel1)INM-10-20170113},
pnm = {5244 - Information Processing in Neuronal Networks
(POF4-524) / 5241 - Molecular Information Processing in
Cellular Systems (POF4-524) / DFG project
G:(GEPRIS)430631456 - Funktionelle Rolle der
intrazellulären Chlorid/Proton Austauscher ClC-3, ClC-4 und
ClC-5 in der Neurosekretion (430631456)},
pid = {G:(DE-HGF)POF4-5244 / G:(DE-HGF)POF4-5241 /
G:(GEPRIS)430631456},
typ = {PUB:(DE-HGF)16},
doi = {10.1093/brain/awaf243},
url = {https://juser.fz-juelich.de/record/1043576},
}