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SLC4A11 – Harboyan Syndrome

Harboyan syndrome (HS; MONDO:0009015) is an autosomal recessive disorder characterized by congenital hereditary endothelial dystrophy (CHED) and progressive sensorineural hearing loss. Onset of corneal edema occurs at birth or infancy, manifesting as bilateral corneal clouding, nystagmus, and visual loss. Sensorineural hearing loss typically develops postlingually between 10–25 years, although rare prelingual cases have been reported (PMID:18922146). HS is allelic to CHED2 and results from biallelic loss-of-function variants in SLC4A11 (HGNC:16438), which encodes a basolateral H+/OH– and ammonia-sensitive transporter in corneal endothelial cells.

Strong genetic evidence supports the definitive association between SLC4A11 and HS. To date, >30 probands from 11 unrelated families have been reported with biallelic SLC4A11 variants segregating with disease in consanguineous and nonconsanguineous pedigrees (PMID:18922146, PMID:25500497). Multi-family segregation analyses include a total of 19 affected relatives with homozygous or compound heterozygous variants. More than 62 SLC4A11 mutations have been described, encompassing nonsense, frameshift, splice, and missense variants that co-segregate with HS under an autosomal recessive model.

The variant spectrum in HS comprises predominantly predicted loss-of-function alleles, including nonsense and frameshift mutations such as c.2188C>T (p.Arg730Ter) (PMID:25500497) and founder alleles such as c.2263C>T (p.Arg755Gln) in the Karen population (allele frequency 0.01) (PMID:32884076). Hypomorphic and missense variants have also been observed, for example c.1735_1737delCTC (p.Leu579del) (PMID:35439766). Recurrent frameshift duplications, including c.2233_2240dup (p.Ile748MetfsTer5), suggest a founder effect in South American families (PMID:30856043).

Functional studies across multiple models demonstrate concordance with human disease. Slc4a11–/– mouse corneal endothelium recapitulates CHED with corneal edema, whereas the human phenotype spares renal function (PMID:25500497). In vitro splicing assays in iPSC-derived corneal endothelial–like cells confirmed that intronic variant c.2240+5G>A results in aberrant splicing and a premature stop p.Thr747Ter (PMID:31323090). Electrophysiological studies in PS120 cells revealed that missense mutants such as R125H, W240S, and C386R impair transporter H+ and OH– flux without affecting surface trafficking (PMID:30557570).

Additional experiments support a loss-of-function mechanism via protein misfolding and ER retention. High-throughput assays identified rescue of several misfolded variants by the NSAID diclofenac, restoring water flux akin to wild-type levels (PMID:30140924). Homology modeling further rationalized the distribution of pathogenic mutations within transmembrane and dimerization interfaces (PMID:27925686).

In summary, extensive genetic, segregation, and functional data fulfill ClinGen definitive criteria for an autosomal recessive gene–disease relationship between SLC4A11 and Harboyan syndrome. Genetic testing of SLC4A11 is clinically validated for diagnosis and family counseling. Key take-home: Biallelic SLC4A11 variants cause HS via haploinsufficiency and protein folding defects, guiding molecular diagnosis and potential personalized therapeutic approaches.

References

  • Orphanet journal of rare diseases • 2008 • Congenital hereditary endothelial dystrophy with progressive sensorineural deafness (Harboyan syndrome). PMID:18922146
  • Ophthalmic research • 2015 • Detailed assessment of renal function in a proband with Harboyan syndrome caused by a novel homozygous SLC4A11 nonsense mutation. PMID:25500497
  • Cornea • 2022 • Harboyan Syndrome: A Novel SLC4A11 Variant With Unique Genotype-Phenotype Correlation. PMID:35439766
  • Investigative ophthalmology & visual science • 2019 • IPSC-Derived Corneal Endothelial-like Cells Act as an Appropriate Model System to Assess the Impact of SLC4A11 Variants on Pre-mRNA Splicing. PMID:31323090
  • Experimental eye research • 2019 • R125H, W240S, C386R, and V507I SLC4A11 mutations associated with corneal endothelial dystrophy affect the transporter function but not trafficking in PS120 cells. PMID:30557570
  • Journal of human genetics • 2021 • Harboyan syndrome: novel SLC4A11 mutation, clinical manifestations, and outcome of corneal transplantation. PMID:32884076
  • Investigative ophthalmology & visual science • 2015 • High Throughput Assay Identifies Glafenine as a Corrector for the Folding Defect in Corneal Dystrophy-Causing Mutants of SLC4A11. PMID:26641551
  • Investigative ophthalmology & visual science • 2018 • Ophthalmic Nonsteroidal Anti-Inflammatory Drugs as a Therapy for Corneal Dystrophies Caused by SLC4A11 Mutation. PMID:30140924
  • Human mutation • 2017 • SLC4A11 Three-Dimensional Homology Model Rationalizes Corneal Dystrophy-Causing Mutations. PMID:27925686

Evidence Based Scoring (AI generated)

Gene–Disease Association

Definitive

30 probands from 11 families, multi-family segregation, concordant functional and animal model data

Genetic Evidence

Strong

30 variants in >30 probands with AR inheritance, reached ClinGen genetic cap

Functional Evidence

Strong

Knockout mouse recapitulates phenotype; splicing and transport assays; rescue studies