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A Depolarizing Leak in Sodium Bicarbonate Cotransporter NBCe1 Causes Brain Edema

Bisseling, Quinty ; Parker, Mark D. ; Kerst, Sven ; Pasternack, Richard A. ; Tondreau, Jacob ; Breur, Marjolein ; van Rooijen-van Leeuwen, Gemma M. ; Tonduti, Davide ; Salsano, Ettore and Darling, Alejandra , et al. (2026) In Annals of Clinical and Translational Neurology
Abstract

Objectives: SLC4A4 encodes electrogenic sodium bicarbonate cotransporter NBCe1, prominently expressed in kidney and brain. Recessive loss-of-function variants in SLC4A4 cause proximal renal tubular acidosis, no brain edema. In the brain, NBCe1 is expressed by astrocytes, where it regulates pH and mediates astrocyte volume changes. Here we describe a novel dominant variant in SLC4A4 in patients with brain edema and investigate how it affects NBCe1 function. Methods: Genetic studies identified a novel gene variant in three unrelated pediatric patients with the same MRI pattern of cerebral subcortical white matter signal abnormality and swelling, and medulla lesions. Immunohistochemical and electrophysiological experiments were performed... (More)

Objectives: SLC4A4 encodes electrogenic sodium bicarbonate cotransporter NBCe1, prominently expressed in kidney and brain. Recessive loss-of-function variants in SLC4A4 cause proximal renal tubular acidosis, no brain edema. In the brain, NBCe1 is expressed by astrocytes, where it regulates pH and mediates astrocyte volume changes. Here we describe a novel dominant variant in SLC4A4 in patients with brain edema and investigate how it affects NBCe1 function. Methods: Genetic studies identified a novel gene variant in three unrelated pediatric patients with the same MRI pattern of cerebral subcortical white matter signal abnormality and swelling, and medulla lesions. Immunohistochemical and electrophysiological experiments were performed to determine the localization of the transporter in the brain and the functional consequence of the patient variant. Results: The same heterozygous variant in SLC4A4 was found in all three patients and one parent. The children displayed infantile-onset progressive macrocephaly, motor and cognitive impairment, autism, epilepsy, and recurrent episodes of increased intracranial pressure. Bicarbonate treatment of two patients led to clinical and MRI improvement. Immunohistochemistry revealed that brain NBCe1 is mainly present in astrocytes, more in cortex than white matter. Functional experiments revealed impaired transporter activity of mutant NBCe1 due to reduced membrane expression and a prominent depolarizing ion leak. Interpretation: The most likely pathomechanism of this novel SLC4A4-related disease is that a depolarizing leak in NBCe1 disrupts astrocyte pH regulation, promoting swelling and impairing volume control. These findings uncover a previously unrecognized mechanism of genetic brain edema and establish NBCe1 as a critical modulator of astrocyte homeostasis.

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organization
publishing date
type
Contribution to journal
publication status
in press
subject
keywords
astrocyte, brain edema, leukodystrophy, NBCe1, renal tubular acidosis, SLC4A4
in
Annals of Clinical and Translational Neurology
publisher
John Wiley & Sons Inc.
external identifiers
  • scopus:105033263374
  • pmid:41841191
ISSN
2328-9503
DOI
10.1002/acn3.70363
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2026 The Author(s). Annals of Clinical and Translational Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
id
0ba3f856-2e70-418a-b414-1e66b5095748
date added to LUP
2026-05-19 15:01:33
date last changed
2026-06-02 16:03:50
@article{0ba3f856-2e70-418a-b414-1e66b5095748,
  abstract     = {{<p>Objectives: SLC4A4 encodes electrogenic sodium bicarbonate cotransporter NBCe1, prominently expressed in kidney and brain. Recessive loss-of-function variants in SLC4A4 cause proximal renal tubular acidosis, no brain edema. In the brain, NBCe1 is expressed by astrocytes, where it regulates pH and mediates astrocyte volume changes. Here we describe a novel dominant variant in SLC4A4 in patients with brain edema and investigate how it affects NBCe1 function. Methods: Genetic studies identified a novel gene variant in three unrelated pediatric patients with the same MRI pattern of cerebral subcortical white matter signal abnormality and swelling, and medulla lesions. Immunohistochemical and electrophysiological experiments were performed to determine the localization of the transporter in the brain and the functional consequence of the patient variant. Results: The same heterozygous variant in SLC4A4 was found in all three patients and one parent. The children displayed infantile-onset progressive macrocephaly, motor and cognitive impairment, autism, epilepsy, and recurrent episodes of increased intracranial pressure. Bicarbonate treatment of two patients led to clinical and MRI improvement. Immunohistochemistry revealed that brain NBCe1 is mainly present in astrocytes, more in cortex than white matter. Functional experiments revealed impaired transporter activity of mutant NBCe1 due to reduced membrane expression and a prominent depolarizing ion leak. Interpretation: The most likely pathomechanism of this novel SLC4A4-related disease is that a depolarizing leak in NBCe1 disrupts astrocyte pH regulation, promoting swelling and impairing volume control. These findings uncover a previously unrecognized mechanism of genetic brain edema and establish NBCe1 as a critical modulator of astrocyte homeostasis.</p>}},
  author       = {{Bisseling, Quinty and Parker, Mark D. and Kerst, Sven and Pasternack, Richard A. and Tondreau, Jacob and Breur, Marjolein and van Rooijen-van Leeuwen, Gemma M. and Tonduti, Davide and Salsano, Ettore and Darling, Alejandra and van Wijk, Joanna A.E. and Törnroth-Horsefield, Susanna and Bugiani, Marianna and Pouwels, Petra J.W. and Waisfisz, Quinten and van der Knaap, Marjo S. and Min, Rogier}},
  issn         = {{2328-9503}},
  keywords     = {{astrocyte; brain edema; leukodystrophy; NBCe1; renal tubular acidosis; SLC4A4}},
  language     = {{eng}},
  publisher    = {{John Wiley & Sons Inc.}},
  series       = {{Annals of Clinical and Translational Neurology}},
  title        = {{A Depolarizing Leak in Sodium Bicarbonate Cotransporter NBCe1 Causes Brain Edema}},
  url          = {{http://dx.doi.org/10.1002/acn3.70363}},
  doi          = {{10.1002/acn3.70363}},
  year         = {{2026}},
}