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CLCN4 – Raynaud-Claes syndrome (Intellectual disability, X-linked 49)

CLCN4 encodes the endosomal 2Cl–/H+ exchanger ClC-4, highly expressed in hippocampus and cerebellum. Pathogenic variants in CLCN4 cause Raynaud-Claes syndrome, characterized by intellectual disability, language impairment, brain anomalies and drug-resistant epilepsy ([PMID:37271660]).

Inheritance is X-linked, with hemizygous males and heterozygous females affected through de novo events or maternal transmission. A de novo heterozygous c.1630G>A (p.Gly544Arg) variant was reported in a 30-year-old woman with developmental and epileptic encephalopathy, global delay, absence of verbal language and catamenial seizure clusters ([PMID:37271660]). A hemizygous NM_001830.4:c.1597G>A (p.Val533Met) variant segregated maternally in a boy with intellectual disability and refractory epileptic encephalopathy responsive to ketogenic diet ([PMID:38482266]).

A large international cohort assembled 90 rare CLCN4 missense variants in 90 families and summarized 122 individuals from 67 families, confirming phenotypic spectrum from isolated intellectual disability to severe developmental and epileptic encephalopathy ([PMID:36385166]). Recurrent heterozygous de novo variants p.Asp89Asn and p.Ala555Val were identified in unrelated female patients, while hemizygous p.Asn141Ser and p.Arg694Gln occurred in male probands.

Variant spectrum includes at least 41 unique and 18 recurrent missense changes, one splice site alteration (c.1390-12T>G) with no splicing defect, and no reported large indels or structural variants. Phenotypes encompass intellectual disability (HP:0001249), global developmental delay (HP:0001263) and epileptic encephalopathy (HP:0200134) ([PMID:37789889]).

Functional studies using Xenopus oocytes and mammalian cell patch-clamp assays demonstrated diverse mechanisms: 25% of variants exhibited loss-of-function via shifted activation voltages, 15% showed toxic gain-of-function with inward leak currents, and some impaired heterodimerization with ClC-3 or altered endosomal pH regulation ([PMID:36385166]; [PMID:35721313]). These data support a primary role of altered ClC-4 transport in pathogenesis.

Conflicting evidence includes the c.1390-12T>G splice region variant, which did not affect mRNA splicing or protein localization and is likely benign ([PMID:37789889]). No CLCN4 mutations were identified in Dent disease cohorts, excluding a role in renal pathology ([PMID:12746443]; [PMID:19546591]).

Integration of genetic and experimental findings yields a strong association between CLCN4 variants and Raynaud-Claes syndrome, with variant-specific functional effects explaining clinical heterogeneity. While abundant data exist, further long-term natural history studies and exploration of targeted therapies are warranted.

Key Take-home: Testing for CLCN4 variants is critical for diagnosing Raynaud-Claes syndrome and guiding prognosis and potential therapeutic interventions targeting ClC-4 dysfunction.

References

  • Brain & development • 2023 • Developmental and epileptic encephalopathy in a young Italian woman with a de novo missense variant in the CLCN4 gene: A case report. PMID:37271660
  • Balkan journal of medical genetics : BJMG • 2023 • Experience with the Ketogenic Diet in a Boy with CLCN4 Related Neurodevelopmental Disorder. PMID:38482266
  • Molecular psychiatry • 2023 • Functional and clinical studies reveal pathophysiological complexity of CLCN4-related neurodevelopmental condition. PMID:36385166
  • Frontiers in molecular neuroscience • 2022 • Functional Characterization of CLCN4 Variants Associated With X-Linked Intellectual Disability and Epilepsy. PMID:35721313
  • Frontiers in neurology • 2023 • Novel variants in the CLCN4 gene associated with syndromic X-linked intellectual disability. PMID:37789889
  • The Journal of biological chemistry • 2003 • The chloride channel ClC-4 contributes to endosomal acidification and trafficking. PMID:12746443
  • Nephron. Physiology • 2009 • Mutational analysis of CLC-5, cofilin and CLC-4 in patients with Dent's disease. PMID:19546591

Evidence Based Scoring (AI generated)

Gene–Disease Association

Strong

122 individuals from 67 families, with de novo and inherited CLCN4 missense variants showing consistent phenotypes and functional validation ([PMID:36385166])

Genetic Evidence

Strong

Over 90 rare CLCN4 variants in 122 probands including de novo and recurrent alleles across multiple families ([PMID:36385166])

Functional Evidence

Moderate

Xenopus oocyte and patch-clamp studies of 59 variants revealed loss- and gain-of-function mechanisms congruent with human phenotypes ([PMID:36385166]; [PMID:35721313])