Exploring the Novel Susceptibility Gene Variants for Primary Open-Angle Glaucoma in East Asian Cohorts: The GLAU-GENDISK Study.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
14 01 2020
Historique:
received: 16 07 2019
accepted: 19 12 2019
entrez: 16 1 2020
pubmed: 16 1 2020
medline: 18 11 2020
Statut: epublish

Résumé

Primary open-angle glaucoma (POAG) can develop even within normal ranges of intraocular pressure, and this type of glaucoma (so-called 'normal-tension glaucoma [NTG]') is highly prevalent in East Asia including Korea and Japan. We conducted exome chip analysis to identify low-frequency and rare variants associated with POAG from the primary cohort (309 POAG patients and 5,400 control, all Koreans). For replication, Korean (310 POAG patients and 5,612 controls) and Japanese (565 POAG patients and 1,104 controls) cohorts were further investigated by targeted genotyping. SNP rs116121322 in LRRC27 showed nominally significant association with POAG in the discovery cohort (OR = 29.85, P = 2E-06). This SNP was validated in the Korean replication cohort but only in the NTG subgroups (OR = 9.86, P = 0.007). Japanese replication cohort did not show significant association with POAG (P .00.44). However, the meta-analysis in the entire cohort revealed significant association of rs116121322 with POAG (OR

Identifiants

pubmed: 31937794
doi: 10.1038/s41598-019-57066-7
pii: 10.1038/s41598-019-57066-7
pmc: PMC6959350
doi:

Substances chimiques

Biomarkers 0
Nuclear Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

221

Références

Tham, Y. C. et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology 121, 2081–2090, https://doi.org/10.1016/j.ophtha.2014.05.013 (2014).
doi: 10.1016/j.ophtha.2014.05.013 pubmed: 24974815
Kwon, Y. H., Fingert, J. H., Kuehn, M. H. & Alward, W. L. Primary open-angle glaucoma. N. Engl. J. Med. 360, 1113–1124, https://doi.org/10.1056/NEJMra0804630 (2009).
doi: 10.1056/NEJMra0804630 pubmed: 19279343 pmcid: 3700399
The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Collaborative Normal-Tension Glaucoma Study Group. American journal of ophthalmology 126, 498–505 (1998).
Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Collaborative Normal-Tension Glaucoma Study Group. American journal of ophthalmology 126, 487–497 (1998).
Anderson, D. R., Drance, S. M. & Schulzer, M., Collaborative Normal-Tension Glaucoma Study, G. Natural history of normal-tension glaucoma. Ophthalmology 108, 247–253 (2001).
doi: 10.1016/S0161-6420(00)00518-2
Drance, S., Anderson, D. R. & Schulzer, M., Collaborative Normal-Tension Glaucoma Study, G. Risk factors for progression of visual field abnormalities in normal-tension glaucoma. Am. J. Ophthalmol. 131, 699–708 (2001).
doi: 10.1016/S0002-9394(01)00964-3
Iwase, A. et al. The prevalence of primary open-angle glaucoma in Japanese: the Tajimi Study. Ophthalmology 111, 1641–1648, https://doi.org/10.1016/j.ophtha.2004.03.029 (2004).
doi: 10.1016/j.ophtha.2004.03.029 pubmed: 15350316
Liang, Y. B. et al. Prevalence of primary open angle glaucoma in a rural adult Chinese population: the Handan eye study. Invest. Ophthalmol. Vis. Sci. 52, 8250–8257, https://doi.org/10.1167/iovs.11-7472 (2011).
doi: 10.1167/iovs.11-7472 pubmed: 21896871
Kim, C. S., Seong, G. J., Lee, N. H. & Song, K. C., Namil Study Group, K. G. S. Prevalence of primary open-angle glaucoma in central South Korea the Namil study. Ophthalmology 118, 1024–1030, https://doi.org/10.1016/j.ophtha.2010.10.016 (2011).
doi: 10.1016/j.ophtha.2010.10.016 pubmed: 21269703
Mackey, D. A. & Hewitt, A. W. Genome-wide association study success in ophthalmology. Curr. Opin. Ophthalmol. 25, 386–393, https://doi.org/10.1097/ICU.0000000000000090 (2014).
doi: 10.1097/ICU.0000000000000090 pubmed: 25014751
Abu-Amero, K., Kondkar, A. A. & Chalam, K. V. An Updated Review on the Genetics of Primary Open Angle Glaucoma. Int. J. Mol. Sci. 16, 28886–28911, https://doi.org/10.3390/ijms161226135 (2015).
doi: 10.3390/ijms161226135 pubmed: 26690118 pmcid: 4691082
Thorleifsson, G. et al. Common variants near CAV1 and CAV2 are associated with primary open-angle glaucoma. Nat. Genet. 42, 906–909, https://doi.org/10.1038/ng.661 (2010).
doi: 10.1038/ng.661 pubmed: 20835238 pmcid: 3222888
Burdon, K. P. et al. Genome-wide association study identifies susceptibility loci for open angle glaucoma at TMCO1 and CDKN2B-AS1. Nat. Genet. 43, 574–578, https://doi.org/10.1038/ng.824 (2011).
doi: 10.1038/ng.824 pubmed: 21532571
Osman, W., Low, S. K., Takahashi, A., Kubo, M. & Nakamura, Y. A genome-wide association study in the Japanese population confirms 9p21 and 14q23 as susceptibility loci for primary open angle glaucoma. Hum. Mol. Genet. 21, 2836–2842, https://doi.org/10.1093/hmg/dds103 (2012).
doi: 10.1093/hmg/dds103 pubmed: 22419738
Nakano, M. et al. Common variants in CDKN2B-AS1 associated with optic-nerve vulnerability of glaucoma identified by genome-wide association studies in Japanese. PLoS One 7, e33389, https://doi.org/10.1371/journal.pone.0033389 (2012).
doi: 10.1371/journal.pone.0033389 pubmed: 22428042 pmcid: 3299784
Li, Z. et al. A common variant near TGFBR3 is associated with primary open angle glaucoma. Hum. Mol. Genet. 24, 3880–3892, https://doi.org/10.1093/hmg/ddv128 (2015).
doi: 10.1093/hmg/ddv128 pubmed: 25861811 pmcid: 4459396
van Koolwijk, L. M. et al. Common genetic determinants of intraocular pressure and primary open-angle glaucoma. PLoS Genet. 8, e1002611, https://doi.org/10.1371/journal.pgen.1002611 (2012).
doi: 10.1371/journal.pgen.1002611 pubmed: 22570627 pmcid: 3342933
Ramdas, W. D. et al. Common genetic variants associated with open-angle glaucoma. Hum. Mol. Genet. 20, 2464–2471, https://doi.org/10.1093/hmg/ddr120 (2011).
doi: 10.1093/hmg/ddr120 pubmed: 21427129
Iglesias, A. I. et al. Exome sequencing and functional analyses suggest that SIX6 is a gene involved in an altered proliferation-differentiation balance early in life and optic nerve degeneration at old age. Hum. Mol. Genet. 23, 1320–1332, https://doi.org/10.1093/hmg/ddt522 (2014).
doi: 10.1093/hmg/ddt522 pubmed: 24150847
Vishal, M. et al. Genetic association and stress mediated down-regulation in trabecular meshwork implicates MPP7 as a novel candidate gene in primary open angle glaucoma. BMC Med. Genomics 9, 15, https://doi.org/10.1186/s12920-016-0177-6 (2016).
doi: 10.1186/s12920-016-0177-6 pubmed: 27001270 pmcid: 4802647
Mabuchi, F. et al. Association between genetic variants associated with vertical cup-to-disc ratio and phenotypic features of primary open-angle glaucoma. Ophthalmology 119, 1819–1825, https://doi.org/10.1016/j.ophtha.2012.02.044 (2012).
doi: 10.1016/j.ophtha.2012.02.044 pubmed: 22584021
Wiggs, J. L. et al. Common variants at 9p21 and 8q22 are associated with increased susceptibility to optic nerve degeneration in glaucoma. PLoS Genet. 8, e1002654, https://doi.org/10.1371/journal.pgen.1002654 (2012).
doi: 10.1371/journal.pgen.1002654 pubmed: 22570617 pmcid: 3343074
Chen, Y. et al. Genetic Variants Associated With Different Risks for High Tension Glaucoma and Normal Tension Glaucoma in a Chinese Population. Invest. Ophthalmol. Vis. Sci. 56, 2595–2600, https://doi.org/10.1167/iovs.14-16269 (2015).
doi: 10.1167/iovs.14-16269 pubmed: 25711633
Takamoto, M. et al. Common variants on chromosome 9p21 are associated with normal tension glaucoma. PLoS One 7, e40107, https://doi.org/10.1371/journal.pone.0040107 (2012).
doi: 10.1371/journal.pone.0040107 pubmed: 22792221 pmcid: 3390321
Shiga, Y. et al. Genetic analysis of Japanese primary open-angle glaucoma patients and clinical characterization of risk alleles near CDKN2B-AS1, SIX6 and GAS7. PLoS One 12, e0186678, https://doi.org/10.1371/journal.pone.0186678 (2017).
doi: 10.1371/journal.pone.0186678 pubmed: 29261660 pmcid: 5737967
Youngblood, H., Hauser, M. A. & Liu, Y. Update on the genetics of primary open-angle glaucoma. Exp. eye Res. 188, 107795, https://doi.org/10.1016/j.exer.2019.107795 (2019).
doi: 10.1016/j.exer.2019.107795 pubmed: 31525344
Sayers, E. W. et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 37, D5–15, https://doi.org/10.1093/nar/gkn741 (2009).
doi: 10.1093/nar/gkn741 pubmed: 18940862
Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 37, D26–31, https://doi.org/10.1093/nar/gkn723 (2009).
doi: 10.1093/nar/gkn723 pubmed: 18940867
Munaut, C. et al. Presence of oestrogen receptor type beta in human retina. Br. J. Ophthalmol. 85, 877–882 (2001).
doi: 10.1136/bjo.85.7.877
Akar, M. E., Taskin, O., Yucel, I. & Akar, Y. The effect of the menstrual cycle on optic nerve head analysis in healthy women. Acta ophthalmologica Scandinavica 82, 741–745, https://doi.org/10.1111/j.1600-0420.2004.00351.x (2004).
doi: 10.1111/j.1600-0420.2004.00351.x pubmed: 15606474
Agapova, O. A., Kaufman, P. L. & Hernandez, M. R. Androgen receptor and NFkB expression in human normal and glaucomatous optic nerve head astrocytes in vitro and in experimental glaucoma. Exp. eye Res. 82, 1053–1059, https://doi.org/10.1016/j.exer.2005.10.021 (2006).
doi: 10.1016/j.exer.2005.10.021 pubmed: 16310187
Rudnicka, A. R., Mt-Isa, S., Owen, C. G., Cook, D. G. & Ashby, D. Variations in primary open-angle glaucoma prevalence by age, gender, and race: a Bayesian meta-analysis. Invest. Ophthalmol. Vis. Sci. 47, 4254–4261, https://doi.org/10.1167/iovs.06-0299 (2006).
doi: 10.1167/iovs.06-0299 pubmed: 17003413
Kapetanakis, V. V. et al. Global variations and time trends in the prevalence of primary open angle glaucoma (POAG): a systematic review and meta-analysis. Br. J. Ophthalmol. 100, 86–93, https://doi.org/10.1136/bjophthalmol-2015-307223 (2016).
doi: 10.1136/bjophthalmol-2015-307223 pubmed: 26286821
Eckert, R. L. et al. Regulation of involucrin gene expression. J. Investig. dermatology 123, 13–22, https://doi.org/10.1111/j.0022-202X.2004.22723.x (2004).
doi: 10.1111/j.0022-202X.2004.22723.x
Kalinin, A. E., Kajava, A. V. & Steinert, P. M. Epithelial barrier function: assembly and structural features of the cornified cell envelope. Bioessays 24, 789–800, https://doi.org/10.1002/bies.10144 (2002).
doi: 10.1002/bies.10144 pubmed: 12210515
Moers, K. et al. Substrate elasticity as biomechanical modulator of tissue homeostatic parameters in corneal keratinocytes. Exp. Cell Res. 319, 1889–1901, https://doi.org/10.1016/j.yexcr.2013.05.002 (2013).
doi: 10.1016/j.yexcr.2013.05.002 pubmed: 23664838
Malecki, J., Ho, A. Y., Moen, A., Dahl, H. A. & Falnes, P. O. Human METTL20 is a mitochondrial lysine methyltransferase that targets the beta subunit of electron transfer flavoprotein (ETFbeta) and modulates its activity. J. Biol. Chem. 290, 423–434, https://doi.org/10.1074/jbc.M114.614115 (2015).
doi: 10.1074/jbc.M114.614115 pubmed: 25416781
Van Bergen, N. J. et al. Measurement of Systemic Mitochondrial Function in Advanced Primary Open-Angle Glaucoma and Leber Hereditary Optic Neuropathy. PLoS One 10, e0140919, https://doi.org/10.1371/journal.pone.0140919 (2015).
doi: 10.1371/journal.pone.0140919 pubmed: 26496696 pmcid: 4619697
Osborne, N. N., Nunez-Alvarez, C., Joglar, B. & Del Olmo-Aguado, S. Glaucoma: Focus on mitochondria in relation to pathogenesis and neuroprotection. Eur. J. pharmacology. https://doi.org/10.1016/j.ejphar.2016.04.032 (2016).
doi: 10.1016/j.ejphar.2016.04.032
Jeoung, J. W. et al. Mitochondrial DNA variant discovery in normal-tension glaucoma patients by next-generation sequencing. Invest. Ophthalmol. Vis. Sci. 55, 986–992, https://doi.org/10.1167/iovs.13-12968 (2014).
doi: 10.1167/iovs.13-12968 pubmed: 24448266
Heller, G. et al. DNA methylation transcriptionally regulates the putative tumor cell growth suppressor ZNF677 in non-small cell lung cancers. Oncotarget 6, 394–408, https://doi.org/10.18632/oncotarget.2697 (2015).
doi: 10.18632/oncotarget.2697 pubmed: 25504438
Guo, Y. et al. Association of TP53 polymorphisms with primary open-angle glaucoma: a meta-analysis. Invest. Ophthalmol. Vis. Sci. 53, 3756–3763, https://doi.org/10.1167/iovs.12-9818 (2012).
doi: 10.1167/iovs.12-9818 pubmed: 22562509
Vishal, M. et al. Evaluation of genetic association of the INK4 locus with primary open angle glaucoma in East Indian population. Sci. Rep. 4, 5115, https://doi.org/10.1038/srep05115 (2014).
doi: 10.1038/srep05115 pubmed: 24875940 pmcid: 4038833
Gao, S. & Jakobs, T. C. Mice Homozygous for a Deletion in the Glaucoma Susceptibility Locus INK4 Show Increased Vulnerability of Retinal Ganglion Cells to Elevated Intraocular Pressure. Am. J. Pathol. 186, 985–1005, https://doi.org/10.1016/j.ajpath.2015.11.026 (2016).
doi: 10.1016/j.ajpath.2015.11.026 pubmed: 26883755 pmcid: 5848263
Wilson, P. D. Polycystic kidney disease. N. Engl. J. Med. 350, 151–164, https://doi.org/10.1056/NEJMra022161 (2004).
doi: 10.1056/NEJMra022161 pubmed: 14711914
Nauli, S. M. et al. Loss of polycystin-1 in human cyst-lining epithelia leads to ciliary dysfunction. J. Am. Soc. Nephrology: JASN 17, 1015–1025, https://doi.org/10.1681/ASN.2005080830 (2006).
doi: 10.1681/ASN.2005080830
Wilson, P. D. Mouse models of polycystic kidney disease. Curr. Top. Dev. Biol. 84, 311–350, https://doi.org/10.1016/S0070-2153(08)00606-6 (2008).
doi: 10.1016/S0070-2153(08)00606-6 pubmed: 19186247
Xu, C. et al. Human ADPKD primary cyst epithelial cells with a novel, single codon deletion in the PKD1 gene exhibit defective ciliary polycystin localization and loss of flow-induced Ca
doi: 10.1152/ajprenal.00285.2006
Nachury, M. V. et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201–1213, https://doi.org/10.1016/j.cell.2007.03.053 (2007).
doi: 10.1016/j.cell.2007.03.053 pubmed: 17574030
Zhang, X., Jefferson, A. B., Auethavekiat, V. & Majerus, P. W. The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase. Proc. Natl Acad. Sci. USA 92, 4853–4856 (1995).
doi: 10.1073/pnas.92.11.4853
Luo, N. et al. Compensatory Role of Inositol 5-Phosphatase INPP5B to OCRL in Primary Cilia Formation in Oculocerebrorenal Syndrome of Lowe. PLoS One 8, e66727, https://doi.org/10.1371/journal.pone.0066727 (2013).
doi: 10.1371/journal.pone.0066727 pubmed: 23805271 pmcid: 3689662
Luo, N. et al. Primary cilia signaling mediates intraocular pressure sensation. Proc. Natl Acad. Sci. USA 111, 12871–12876, https://doi.org/10.1073/pnas.1323292111 (2014).
doi: 10.1073/pnas.1323292111 pubmed: 25143588
Kim, Y., Han, B. G. & Ko, G. E. S. g. Cohort Profile: The Korean Genome and Epidemiology Study (KoGES) Consortium. International journal of epidemiology, https://doi.org/10.1093/ije/dyv316 (2016).
doi: 10.1093/ije/dyv316
Lee, S., Wu, M. C. & Lin, X. Optimal tests for rare variant effects in sequencing association studies. Biostatistics 13, 762–775, https://doi.org/10.1093/biostatistics/kxs014 (2012).
doi: 10.1093/biostatistics/kxs014 pubmed: 22699862 pmcid: 3440237
Wu, M. C. et al. Rare-variant association testing for sequencing data with the sequence kernel association test. Am. J. Hum. Genet. 89, 82–93, https://doi.org/10.1016/j.ajhg.2011.05.029 (2011).
doi: 10.1016/j.ajhg.2011.05.029 pubmed: 21737059 pmcid: 3135811
Livak, K. J. Allelic discrimination using fluorogenic probes and the 5′ nuclease assay. Genet. Anal. 14, 143–149 (1999).
doi: 10.1016/S1050-3862(98)00019-9

Auteurs

Yong Woo Kim (YW)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.
Department of Ophthalmology, Seoul National University Hospital, Seoul, Korea.

Yu Jeong Kim (YJ)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.

Hyun Sub Cheong (HS)

Department of Genetic Epidemiology, SNP Genetics, Inc., Seoul, Korea.

Yukihiro Shiga (Y)

Department of Ophthalmic Imaging and Information Analytics, Tohoku University Graduate School of Medicine, Miyagi, Japan.
Department of Ophthalmology, Tohoku University Graduate School of Medicine, Miyagi, Japan.

Kazuki Hashimoto (K)

Department of Ophthalmology, Tohoku University Graduate School of Medicine, Miyagi, Japan.

Yong Ju Song (YJ)

Department of Ophthalmology, Chosun University College of Medicine, Gwangju, Korea.

Seok Hwan Kim (SH)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.
Department of Ophthalmology, Seoul National University Boramae Hospital, Seoul, Korea.

Hyuk Jin Choi (HJ)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.
Healthcare System Gangnam Center, Seoul National University Hospital, Seoul, Korea.

Koji M Nishiguchi (KM)

Department of Advanced Ophthalmic Medicine, Tohoku University Graduate School of Medicine, Miyagi, Japan.

Yosuke Kawai (Y)

Department of Integrative Genomics, Tohoku Medical Megabank Organization, Tohoku University, Miyagi, Japan.
Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.

Masao Nagasaki (M)

Department of Integrative Genomics, Tohoku Medical Megabank Organization, Tohoku University, Miyagi, Japan.
Graduate School of Information Sciences, Tohoku University, Miyagi, Japan.

Toru Nakazawa (T)

Department of Ophthalmic Imaging and Information Analytics, Tohoku University Graduate School of Medicine, Miyagi, Japan.
Department of Ophthalmology, Tohoku University Graduate School of Medicine, Miyagi, Japan.
Department of Advanced Ophthalmic Medicine, Tohoku University Graduate School of Medicine, Miyagi, Japan.
Department of Retinal Disease Control, Tohoku University Graduate School of Medicine, Miyagi, Japan.

Ki Ho Park (KH)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.
Department of Ophthalmology, Seoul National University Hospital, Seoul, Korea.

Dong Myung Kim (DM)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea.

Jin Wook Jeoung (JW)

Department of Ophthalmology, Seoul National University College of Medicine, Seoul, Korea. neuroprotect@gmail.com.
Department of Ophthalmology, Seoul National University Hospital, Seoul, Korea. neuroprotect@gmail.com.

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