Meta-Analysis

. 2018 May 14;9(1):1864.

doi: 10.1038/s41467-018-03646-6.

Cross-ancestry genome-wide association analysis of corneal thickness strengthens link between complex and Mendelian eye diseases

Adriana I Iglesias^{1

2

3}, Aniket Mishra⁴, Veronique Vitart⁵, Yelena Bykhovskaya^{6

7}, René Höhn^{8

9}, Henriët Springelkamp¹, Gabriel Cuellar-Partida¹⁰, Puya Gharahkhani¹⁰, Jessica N Cooke Bailey^{11

12}, Colin E Willoughby^{13

14}, Xiaohui Li^{15

16}, Seyhan Yazar^{5

17}, Abhishek Nag¹⁸, Anthony P Khawaja^{19

20}, Ozren Polašek²¹, David Siscovick^{22

23}, Paul Mitchell²⁴, Yih Chung Tham²⁵, Jonathan L Haines^{11

12}, Lisa S Kearns²⁶, Caroline Hayward⁵, Yuan Shi²⁵, Elisabeth M van Leeuwen¹, Kent D Taylor^{15

16}; Blue Mountains Eye Study—GWAS group; Pieter Bonnemaijer¹, Jerome I Rotter^{15

16}, Nicholas G Martin²⁷, Tanja Zeller^{28

29}, Richard A Mills³⁰, Emmanuelle Souzeau³⁰, Sandra E Staffieri²⁶, Jost B Jonas³¹, Irene Schmidtmann³², Thibaud Boutin⁵, Jae H Kang³³, Sionne E M Lucas³⁴, Tien Yin Wong^{25

35

36}, Manfred E Beutel³⁷, James F Wilson^{5

38}; NEIGHBORHOOD Consortium; Wellcome Trust Case Control Consortium 2 (WTCCC2); André G Uitterlinden^{2

39

40}, Eranga N Vithana²⁵, Paul J Foster²⁰, Pirro G Hysi¹⁸, Alex W Hewitt^{26

41}, Chiea Chuen Khor⁴², Louis R Pasquale^{33

43}, Grant W Montgomery^{27

44}, Caroline C W Klaver^{1

2

45}, Tin Aung^{25

35

36}, Norbert Pfeiffer⁸, David A Mackey¹⁷, Christopher J Hammond¹⁸, Ching-Yu Cheng^{25

35

36}, Jamie E Craig³⁰, Yaron S Rabinowitz^{6

7}, Janey L Wiggs⁴³, Kathryn P Burdon³⁴, Cornelia M van Duijn², Stuart MacGregor⁴⁶

Collaborators, Affiliations

Collaborators

Jie Jin Wang, Elena Rochtchina, John Attia, Rodney Scott, Elizabeth G Holliday, Tien Yin Wong, Paul N Baird, Jing Xie, Michael Inouye, Ananth Viswanathan, Xueling Sim, R Rand Allingham, Murray H Brilliant, Donald L Budenz, William G Christen, John Fingert, David S Friedman, Douglas Gaasterland, Terry Gaasterland, Michael A Hauser, Peter Kraft, Richard K Lee, Paul R Lichter, Yutao Liu, Stephanie J Loomis, Sayoko E Moroi, Margaret A Pericak-Vance, Anthony Realini, Julia E Richards, Joel S Schuman, William K Scott, Kuldev Singh, Arthur J Sit, Douglas Vollrath, Robert N Weinreb, Gadi Wollstein, Donald J Zack, Kang Zhang, Peter Donnelly, Ines Barroso, Jenefer M Blackwell, Elvira Bramon, Matthew A Brown, Juan P Casas, Aiden Corvin, Panos Deloukas, Audrey Duncanson, Janusz Jankowski, Hugh S Markus, Christopher G Mathew, Colin N A Palmer, Robert Plomin, Anna Rautanen, Stephen J Sawcer, Richard C Trembath, Nicholas W Wood, Chris C A Spencer, Gavin Band, Céline Bellenguez, Colin Freeman, Garrett Hellenthal, Eleni Giannoulatou, Matti Pirinen, Richard Pearson, Amy Strange, Zhan Su, Damjan Vukcevic, Cordelia Langford, Sarah E Hunt, Sarah Edkins, Rhian Gwilliam, Hannah Blackburn, Suzannah J Bumpstead, Serge Dronov, Matthew Gillman, Emma Gray, Naomi Hammond, Alagurevathi Jayakumar, Owen T McCann, Jennifer Liddle, Simon C Potter, Radhi Ravindrarajah, Michelle Ricketts, Matthew Waller, Paul Weston, Sara Widaa, Pamela Whittaker

Affiliations

¹ Department of Ophthalmology, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
² Department of Epidemiology, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
³ Department of Clinical Genetics, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
⁴ University of Bordeaux, Bordeaux Population Health Research Center, INSERM UMR 1219, F-33000, Bordeaux, France.
⁵ Institute of Genetics and Molecular Medicine, Medical Research Council Human Genetics Unit, University of Edinburgh, EH42XU, Edinburgh, UK.
⁶ Regenerative Medicine Institute and Department of Surgery, Cedars-Sinai Medical Center, CA 90048, Los Angeles, CA, USA.
⁷ Cornea Genetic Eye Institute, CA 90048, Los Angeles, CA, USA.
⁸ Department of Ophthalmology, University Medical Center Mainz, 55131, Mainz, Germany.
⁹ Department of Ophthalmology, Inselspital, University Hospital Bern, University of Bern, Bern, CH-3010, Switzerland.
¹⁰ Statistical Genetics, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia.
¹¹ Department of Population and Quantitative Health Sciences, Case Western Reserve University, OH 44106, Cleveland, OH, USA.
¹² Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, 44106, USA.
¹³ Biomedical Sciences Research Institute, Ulster University, BT52 1SA, Belfast, Northern Ireland, UK.
¹⁴ Royal Victoria Hospital, Belfast Health and Social Care Trust, BT12 6BA, Belfast, Northern Ireland, UK.
¹⁵ Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA 90509, CA, USA.
¹⁶ Division of Genomic Outcomes, Departments of Pediatrics and Medicine, Harbor-UCLA Medical Center, Torrance, CA 90502, CA, USA.
¹⁷ Centre for Ophthalmology and Visual Science, University of Western Australia, Lions Eye Institute, WA 6009, Perth, WA, Australia.
¹⁸ Department of Twin Research and Genetic Epidemiology, King's College London, WC2R 2LS, London, UK.
¹⁹ Department of Public Health and Primary Care, Institute of Public Health, University of Cambridge School of Clinical Medicine, CB2 0SR, Cambridge, UK.
²⁰ NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology, EC1V 9EL, London, UK.
²¹ Faculty of Medicine, University of Split, HR-21000, Split, Croatia.
²² Departments of Medicine and Epidemiology and Cardiovascular Health Research Unit, University of Washington, WA 98101, Washington, USA.
²³ The New York Academy of Medicine, NY 10029, New York, NY, USA.
²⁴ Centre for Vision Research, Department of Ophthalmology and Westmead Institute for Medical Research, University of Sydney, NSW 2145, Sydney, NSW, Australia.
²⁵ Singapore Eye Research Institute, Singapore National Eye Centre, 168751, Singapore, Singapore.
²⁶ Centre for Eye Research Australia, University of Melbourne, Royal Victorian Eye and Ear Hospital, VIC 3002, East Melbourne, Australia.
²⁷ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia.
²⁸ Department of General and Interventional Cardiology, University Heart Center Hamburg, 20251, Hamburg, Germany.
²⁹ German Center for Cardiovascular Research (DZHK), Partner Site Hamburg/Kiel/Lübeck, 20246, Hamburg, Germany.
³⁰ Department of Ophthalmology, Flinders University, SA 5042, Adelaide, Australia.
³¹ Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University of Heidelberg, 68167, Mannheim, Germany.
³² Institute for Medical Biostatistics, Epidemiology and Informatics, University Medical Center Mainz, 55131, Mainz, Germany.
³³ Channing Division of Network Medicine, Brigham and Women's Hospital, Boston, MA 02115, MA, USA.
³⁴ Menzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7005, TAS, Australia.
³⁵ Ophthalmology & Visual Sciences Academic Clinical Program (Eye ACP), Duke-NUS Medical School, 169857, Singapore, Singapore.
³⁶ Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117549, Singapore.
³⁷ Department of Psychosomatic Medicine and Psychotherapy, University Medical Center Mainz, Mainz, 55131, Germany.
³⁸ Centre for Global Health Research, Usher Institute for Population Health Sciences and Informatics, University of Edinburgh, EH16 4UX, Edinburgh, UK.
³⁹ Department of Internal Medicine, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
⁴⁰ Netherlands Consortium for Healthy Ageing, Netherlands Genomics Initiative, 2593 HW, The Hague, The Netherlands.
⁴¹ School of Medicine, Menzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7005, TAS, Australia.
⁴² Genome Institute of Singapore, 60 Biopolis Street, Singapore, 138672, Singapore.
⁴³ Department of Ophthalmology, Harvard Medical School and Massachusetts Eye and Ear Infirmary, Boston, MA 02114, MA, USA.
⁴⁴ Institute for Molecular Bioscience, University of Queensland, QLD 4067, Brisbane, Australia.
⁴⁵ Department of Ophthalmology, Radboud University Medical Center, 6525 GA, Nijmegen, The Netherlands.
⁴⁶ Statistical Genetics, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia. Stuart.MacGregor@qimrberghofer.edu.au.

PMID: 29760442
PMCID: PMC5951816
DOI: 10.1038/s41467-018-03646-6

Meta-Analysis

Cross-ancestry genome-wide association analysis of corneal thickness strengthens link between complex and Mendelian eye diseases

Adriana I Iglesias et al. Nat Commun. 2018.

. 2018 May 14;9(1):1864.

doi: 10.1038/s41467-018-03646-6.

Authors

Collaborators

Jie Jin Wang, Elena Rochtchina, John Attia, Rodney Scott, Elizabeth G Holliday, Tien Yin Wong, Paul N Baird, Jing Xie, Michael Inouye, Ananth Viswanathan, Xueling Sim, R Rand Allingham, Murray H Brilliant, Donald L Budenz, William G Christen, John Fingert, David S Friedman, Douglas Gaasterland, Terry Gaasterland, Michael A Hauser, Peter Kraft, Richard K Lee, Paul R Lichter, Yutao Liu, Stephanie J Loomis, Sayoko E Moroi, Margaret A Pericak-Vance, Anthony Realini, Julia E Richards, Joel S Schuman, William K Scott, Kuldev Singh, Arthur J Sit, Douglas Vollrath, Robert N Weinreb, Gadi Wollstein, Donald J Zack, Kang Zhang, Peter Donnelly, Ines Barroso, Jenefer M Blackwell, Elvira Bramon, Matthew A Brown, Juan P Casas, Aiden Corvin, Panos Deloukas, Audrey Duncanson, Janusz Jankowski, Hugh S Markus, Christopher G Mathew, Colin N A Palmer, Robert Plomin, Anna Rautanen, Stephen J Sawcer, Richard C Trembath, Nicholas W Wood, Chris C A Spencer, Gavin Band, Céline Bellenguez, Colin Freeman, Garrett Hellenthal, Eleni Giannoulatou, Matti Pirinen, Richard Pearson, Amy Strange, Zhan Su, Damjan Vukcevic, Cordelia Langford, Sarah E Hunt, Sarah Edkins, Rhian Gwilliam, Hannah Blackburn, Suzannah J Bumpstead, Serge Dronov, Matthew Gillman, Emma Gray, Naomi Hammond, Alagurevathi Jayakumar, Owen T McCann, Jennifer Liddle, Simon C Potter, Radhi Ravindrarajah, Michelle Ricketts, Matthew Waller, Paul Weston, Sara Widaa, Pamela Whittaker

Affiliations

¹ Department of Ophthalmology, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
² Department of Epidemiology, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
³ Department of Clinical Genetics, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
⁴ University of Bordeaux, Bordeaux Population Health Research Center, INSERM UMR 1219, F-33000, Bordeaux, France.
⁵ Institute of Genetics and Molecular Medicine, Medical Research Council Human Genetics Unit, University of Edinburgh, EH42XU, Edinburgh, UK.
⁶ Regenerative Medicine Institute and Department of Surgery, Cedars-Sinai Medical Center, CA 90048, Los Angeles, CA, USA.
⁷ Cornea Genetic Eye Institute, CA 90048, Los Angeles, CA, USA.
⁸ Department of Ophthalmology, University Medical Center Mainz, 55131, Mainz, Germany.
⁹ Department of Ophthalmology, Inselspital, University Hospital Bern, University of Bern, Bern, CH-3010, Switzerland.
¹⁰ Statistical Genetics, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia.
¹¹ Department of Population and Quantitative Health Sciences, Case Western Reserve University, OH 44106, Cleveland, OH, USA.
¹² Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, 44106, USA.
¹³ Biomedical Sciences Research Institute, Ulster University, BT52 1SA, Belfast, Northern Ireland, UK.
¹⁴ Royal Victoria Hospital, Belfast Health and Social Care Trust, BT12 6BA, Belfast, Northern Ireland, UK.
¹⁵ Institute for Translational Genomics and Population Sciences and Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA 90509, CA, USA.
¹⁶ Division of Genomic Outcomes, Departments of Pediatrics and Medicine, Harbor-UCLA Medical Center, Torrance, CA 90502, CA, USA.
¹⁷ Centre for Ophthalmology and Visual Science, University of Western Australia, Lions Eye Institute, WA 6009, Perth, WA, Australia.
¹⁸ Department of Twin Research and Genetic Epidemiology, King's College London, WC2R 2LS, London, UK.
¹⁹ Department of Public Health and Primary Care, Institute of Public Health, University of Cambridge School of Clinical Medicine, CB2 0SR, Cambridge, UK.
²⁰ NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology, EC1V 9EL, London, UK.
²¹ Faculty of Medicine, University of Split, HR-21000, Split, Croatia.
²² Departments of Medicine and Epidemiology and Cardiovascular Health Research Unit, University of Washington, WA 98101, Washington, USA.
²³ The New York Academy of Medicine, NY 10029, New York, NY, USA.
²⁴ Centre for Vision Research, Department of Ophthalmology and Westmead Institute for Medical Research, University of Sydney, NSW 2145, Sydney, NSW, Australia.
²⁵ Singapore Eye Research Institute, Singapore National Eye Centre, 168751, Singapore, Singapore.
²⁶ Centre for Eye Research Australia, University of Melbourne, Royal Victorian Eye and Ear Hospital, VIC 3002, East Melbourne, Australia.
²⁷ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia.
²⁸ Department of General and Interventional Cardiology, University Heart Center Hamburg, 20251, Hamburg, Germany.
²⁹ German Center for Cardiovascular Research (DZHK), Partner Site Hamburg/Kiel/Lübeck, 20246, Hamburg, Germany.
³⁰ Department of Ophthalmology, Flinders University, SA 5042, Adelaide, Australia.
³¹ Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University of Heidelberg, 68167, Mannheim, Germany.
³² Institute for Medical Biostatistics, Epidemiology and Informatics, University Medical Center Mainz, 55131, Mainz, Germany.
³³ Channing Division of Network Medicine, Brigham and Women's Hospital, Boston, MA 02115, MA, USA.
³⁴ Menzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7005, TAS, Australia.
³⁵ Ophthalmology & Visual Sciences Academic Clinical Program (Eye ACP), Duke-NUS Medical School, 169857, Singapore, Singapore.
³⁶ Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117549, Singapore.
³⁷ Department of Psychosomatic Medicine and Psychotherapy, University Medical Center Mainz, Mainz, 55131, Germany.
³⁸ Centre for Global Health Research, Usher Institute for Population Health Sciences and Informatics, University of Edinburgh, EH16 4UX, Edinburgh, UK.
³⁹ Department of Internal Medicine, Erasmus Medical Center, 3000 CA, Rotterdam, The Netherlands.
⁴⁰ Netherlands Consortium for Healthy Ageing, Netherlands Genomics Initiative, 2593 HW, The Hague, The Netherlands.
⁴¹ School of Medicine, Menzies Institute for Medical Research, University of Tasmania, Hobart, TAS 7005, TAS, Australia.
⁴² Genome Institute of Singapore, 60 Biopolis Street, Singapore, 138672, Singapore.
⁴³ Department of Ophthalmology, Harvard Medical School and Massachusetts Eye and Ear Infirmary, Boston, MA 02114, MA, USA.
⁴⁴ Institute for Molecular Bioscience, University of Queensland, QLD 4067, Brisbane, Australia.
⁴⁵ Department of Ophthalmology, Radboud University Medical Center, 6525 GA, Nijmegen, The Netherlands.
⁴⁶ Statistical Genetics, QIMR Berghofer Medical Research Institute, QLD 4029, Brisbane, Australia. Stuart.MacGregor@qimrberghofer.edu.au.

PMID: 29760442
PMCID: PMC5951816
DOI: 10.1038/s41467-018-03646-6

Erratum in

Author Correction: Cross-ancestry genome-wide association analysis of corneal thickness strengthens link between complex and Mendelian eye diseases.
Iglesias AI, Mishra A, Vitart V, Bykhovskaya Y, Höhn R, Springelkamp H, Cuellar-Partida G, Gharahkhani P, Bailey JNC, Willoughby CE, Li X, Yazar S, Nag A, Khawaja AP, Polašek O, Siscovick D, Mitchell P, Tham YC, Haines JL, Kearns LS, Hayward C, Shi Y, van Leeuwen EM, Taylor KD; Blue Mountains Eye Study - GWAS group; Bonnemaijer P, Rotter JI, Martin NG, Zeller T, Mills RA, Souzeau E, Staffieri SE, Jonas JB, Schmidtmann I, Boutin T, Kang JH, Lucas SEM, Wong TY, Beutel ME, Wilson JF; Wellcome Trust Case Control Consortium 2 (WTCCC2); NEIGHBORHOOD consortium; Uitterlinden AG, Vithana EN, Foster PJ, Hysi PG, Hewitt AW, Khor CC, Pasquale LR, Montgomery GW, Klaver CCW, Aung T, Pfeiffer N, Mackey DA, Hammond CJ, Cheng CY, Craig JE, Rabinowitz YS, Wiggs JL, Burdon KP, van Duijn CM, MacGregor S. Iglesias AI, et al. Nat Commun. 2019 Jan 8;10(1):155. doi: 10.1038/s41467-018-07819-1. Nat Commun. 2019. PMID: 30622277 Free PMC article.

Abstract

Central corneal thickness (CCT) is a highly heritable trait associated with complex eye diseases such as keratoconus and glaucoma. We perform a genome-wide association meta-analysis of CCT and identify 19 novel regions. In addition to adding support for known connective tissue-related pathways, pathway analyses uncover previously unreported gene sets. Remarkably, >20% of the CCT-loci are near or within Mendelian disorder genes. These included FBN1, ADAMTS2 and TGFB2 which associate with connective tissue disorders (Marfan, Ehlers-Danlos and Loeys-Dietz syndromes), and the LUM-DCN-KERA gene complex involved in myopia, corneal dystrophies and cornea plana. Using index CCT-increasing variants, we find a significant inverse correlation in effect sizes between CCT and keratoconus (r = -0.62, P = 5.30 × 10^-5) but not between CCT and primary open-angle glaucoma (r = -0.17, P = 0.2). Our findings provide evidence for shared genetic influences between CCT and keratoconus, and implicate candidate genes acting in collagen and extracellular matrix regulation.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

**Fig. 1**
Manhattan plot of CCT in the cross-ancestry meta-analysis. Manhattan plot of the GWAS meta-analysis for CCT in the cross-ancestry analysis (n = 25,910). The plot shows −log10-transformed P-values for all SNPs. The red horizontal line represents the genome-wide significance threshold of P < 5.0 × 10⁻⁸; the blue horizontal line indicates a P-value of 1 × 10⁻⁵. Loci are annotated to the nearest gene as in Tables 1 and 2. New loci are in bold

**Fig. 2**
Correlation of effect sizes between CCT and keratoconus and CCT and primary-open angle glaucoma. Each dot represents a CCT-associated variant. In green, variants that surpassed the Bonferroni-corrected significance threshold (P < 5.56 × 10⁻⁴) in the keratoconus analysis (a). In blue, variants that were associated with a nominal level of significance (P < 0.05) in the keratoconus or primary-open angle glaucoma analysis. In gray, variants that did not show association with keratoconus or primary-open angle glaucoma (P > 0.05). a shows correlation of effect sizes between CCT and keratoconus, b shows correlation of effect sizes between CCT and primary-open angle glaucoma

See this image and copyright information in PMC

References

1. Dimasi DP, Burdon KP, Craig JE. The genetics of central corneal thickness. Br. J. Ophthalmol. 2010;94:971–976. doi: 10.1136/bjo.2009.162735. - DOI - PubMed
1. Landers JA, et al. Heritability of central corneal thickness in nuclear families. Invest. Ophthalmol. Vis. Sci. 2009;50:4087–4090. doi: 10.1167/iovs.08-3271. - DOI - PubMed
1. Toh T, et al. Central corneal thickness is highly heritable: the twin eye studies. Invest. Ophthalmol. Vis. Sci. 2005;46:3718–3722. doi: 10.1167/iovs.04-1497. - DOI - PubMed
1. Zheng Y, et al. Heritability of central corneal thickness in Chinese: the Guangzhou Twin Eye Study. Invest. Ophthalmol. Vis. Sci. 2008;49:4303–4307. doi: 10.1167/iovs.08-1934. - DOI - PubMed
1. Villani E, et al. The cornea in classic type Ehlers-Danlos syndrome: macro- and microstructural changes. Invest. Ophthalmol. Vis. Sci. 2013;54:8062–8068. doi: 10.1167/iovs.13-12837. - DOI - PubMed

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Cross-ancestry genome-wide association analysis of corneal thickness strengthens link between complex and Mendelian eye diseases

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Cross-ancestry genome-wide association analysis of corneal thickness strengthens link between complex and Mendelian eye diseases

Authors

Collaborators

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Erratum in

Abstract

Conflict of interest statement

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