Exploring the genetics of primary open-angle glaucoma with next generation sequencing

Author: Tiger Zhou

Zhou, Tiger, 2021 Exploring the genetics of primary open-angle glaucoma with next generation sequencing, Flinders University, College of Medicine and Public Health

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Abstract

Primary open-angle glaucoma (POAG) is a common complex eye condition that leads to blindness if left untreated. Important risk factors for developing POAG are positive family history and high intraocular pressure (IOP). Patients with high IOP are said to have high tension glaucoma, while those with normal IOP have normal tension glaucoma. The precise pathophysiology of POAG remains elusive despite advances in understanding of its genetic risk factors. Around five percent of POAG cases have been linked to known monogenic Mendelian inherited genes found predominantly by familial linkage studies. Common risks alleles for POAG have been identified via genome wide association studies. These single nucleotide polymorphisms individually increase the risk of developing POAG by around 50 percent each at best. The unidentified genetic causes of POAG likely include rare disease-causing variants that are not detected by genome wide association studies or familial linkage studies.

The advent of next generation high-throughput massively parallel sequencing, such as whole exome and RNA sequencing, has made comprehensive investigation of rare disease-causing variants possible. Using whole exome sequencing, this thesis found the genetic contributions of all known monogenic glaucoma disease-causing genes in a cohort with extreme phenotypic POAG of severe disease and younger onset to be 22.9 percent. This thesis also identified one gene associated with genome wide association loci (CARD10) that demonstrated enrichment of rare disease-causing variants. However, the presence of rare disease-causing variants in genes with genome wide association was not the norm, as no enrichment of rare-disease causing variants was found in the remaining one hundred genes examined.

Using rare variant SKAT analysis on the whole exome data, we identified neuroglobin as a POAG candidate gene. Neuroglobin is a highly conserved protein with neuroprotective properties shown to act in cerebral and retinal ischaemia. Three predicted pathogenic variants were identified in the exome sequenced advanced glaucoma cohort of 187 participants with none in our control cohort of 1096 participants. However, further functional experimentation of the three variants is required to confirm pathogenicity.

Using network and pathway analysis of the exome data from the high tension and normal tension POAG participants, this thesis identified potentially differing biological mechanisms involved in each disease subtype. Participants with high tension glaucoma showed significant enrichment of rare predicted pathogenic variants in genes associated with unfolded protein response, the biological pathway responsible for removal of misfolded insoluble gene products, while participants with normal tension glaucoma had enrichment of variants in genes associated with transmembrane transport homeostasis, a deficiency of which leads to susceptibility to apoptosis.

The ocular gene expression data acquired in this thesis through RNA sequencing was found to have a greater dynamic range and sensitivity than previously published microarray ocular expression data. Archetypical high tension glaucoma genes were found to be selectively expressed within the trabecular meshwork, peripheral iris and ciliary body, which are tissues associated with IOP regulation. Network and pathway analysis of gene expression of IOP related tissues identified focal adhesion and extracellular matrix interactions to be the pathways selectively enriched in these tissues.

Keywords: ophthalmology, glaucoma, primary open-angle, next generation sequencing, exome sequencing, RNA sequencing, gene expression, network analysis, myocilin, neuroglobin, CARD10, unfolded protein response, transmembrane protein, extracellular matrix

Subject: Ophthalmology thesis

Thesis type: Doctor of Philosophy
Completed: 2021
School: College of Medicine and Public Health
Supervisor: Jamie Craig