Determining Genetic Cause of Posterior Staphylomas in Eyes with Pathologic Myopia by Whole Exome Sequencing

利用全外显子组测序确定病理性近视眼后巩膜葡萄肿的遗传病因

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Abstract

PURPOSE: To identify genetic variants in posterior staphylomas in eyes with pathologic myopia using whole exome sequencing and to determine possible molecular mechanisms contributing to the pathogenesis. DESIGN: An observational, case-control study. PARTICIPANTS: Two hundred sixty-four unrelated Japanese patients with myopia (≤ -0.50 diopters) and posterior staphyloma, which was diagnosed by ultra-widefield OCT, 3-dimensional magnetic resonance imaging, and Optos imaging. METHODS: Whole exome sequencing was performed on genomic DNA from peripheral blood. After variant filtering, the allelic frequencies were compared with control data obtained from East Asian subsets of the 1000 Genomes Project Phase III, the Exome Aggregation Consortium, and the Japanese Multi-Omics Reference Panel using Fisher exact test. A gene panel was constructed based on 13 staphyloma-associated disorders. Variants showing significant frequency differences (P ≤ 0.05) and an overlap of the gene panel were analyzed using gene set enrichment analysis with the DAVID Knowledgebase (v2023q4). Protein-protein interaction analysis was performed to assess functional associations. MAIN OUTCOME MEASURES: The statistically associated variants and genes, gene set enrichment analysis results, protein-protein interaction networks, and involvement of basement membrane structures, including the inner limiting membrane (ILM) and Bruch membrane, were studied. RESULTS: Whole exome sequencing identified 16 656 missense variants in 8628 genes. Comparative allele frequency analyses with public databases revealed 3925 variants that had significantly higher allelic frequencies in the subjects. Of these, 81 genes overlapped with a curated staphyloma-related gene panel and were subjected to gene set enrichment analysis. The findings showed enrichment in basement membrane, extracellular matrix, and collagen-related pathways. The COL4A5, COL18A1, COL2A1, and COL9A3 genes are concurrently enriched across these pathways. A missense variant in COL4A5 was identified in 27 patients, and 96.3% of whom were females. Protein-protein interaction analysis demonstrated functional connections among these 4 genes. CONCLUSIONS: Variants in the COL4A5, COL18A1, COL2A1, and COL9A3 genes probably contribute to the pathogenesis of a posterior staphyloma through the disruption of collagen synthesis and basement membrane integrity. This was especially effective for the ILM and Bruch membrane. The COL4A5 variant may cause an ocular-predominant phenotype in heterozygous female carriers, independent of the classical features of Alport syndrome. FINANCIAL DISCLOSURES: The authors have no proprietary or commercial interest in any materials discussed in this article.

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