Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error

Qiao Fan^{1

2}, Virginie J M Verhoeven^{3

4}, Robert Wojciechowski^{5

6}, Veluchamy A Barathi^{1

2

7}, Pirro G Hysi⁸, Jeremy A Guggenheim⁹, René Höhn^{10

11}, Veronique Vitart¹², Anthony P Khawaja¹³, Kenji Yamashiro¹⁴, S Mohsen Hosseini¹⁵, Terho Lehtimäki¹⁶, Yi Lu¹⁷, Toomas Haller¹⁸, Jing Xie¹⁹, Cécile Delcourt^{20

21}, Mario Pirastu²², Juho Wedenoja^{23

24}, Puya Gharahkhani¹⁷, Cristina Venturini^{8

25}, Masahiro Miyake¹⁴, Alex W Hewitt^{19

26}, Xiaobo Guo²⁷, Johanna Mazur²⁸, Jenifer E Huffman¹², Katie M Williams^{8

29}, Ozren Polasek³⁰, Harry Campbell³¹, Igor Rudan³¹, Zoran Vatavuk³², James F Wilson³¹, Peter K Joshi³¹, George McMahon^{33

34}, Beate St Pourcain^{33

34

35}, David M Evans^{33

34

36}, Claire L Simpson^{5

37}, Tae-Hwi Schwantes-An⁵, Robert P Igo³⁸, Alireza Mirshahi^{10

39}, Audrey Cougnard-Gregoire^{20

21}, Céline Bellenguez^{40

41

42}, Maria Blettner²⁸, Olli Raitakari^{43

44}, Mika Kähönen⁴⁵, Ilkka Seppala¹⁶, Tanja Zeller⁴⁶, Thomas Meitinger^{47

48}; Consortium for Refractive Error and Myopia; Janina S Ried⁴⁹, Christian Gieger⁴⁹, Laura Portas²², Elisabeth M van Leeuwen⁴, Najaf Amin⁴, André G Uitterlinden^{4

50

51}, Fernando Rivadeneira^{4

50

51}, Albert Hofman^{4

51}, Johannes R Vingerling³, Ya Xing Wang⁵², Xu Wang⁵³, Eileen Tai-Hui Boh⁵³, M Kamran Ikram^{1

2}, Charumathi Sabanayagam^{1

2}, Preeti Gupta¹, Vincent Tan¹, Lei Zhou¹, Candice E H Ho¹, Wan'e Lim⁷, Roger W Beuerman^{1

2

7}, Rosalynn Siantar^{1

54}, E-Shyong Tai^{2

53

55}, Eranga Vithana^{1

2

7}, Evelin Mihailov¹⁸, Chiea-Chuen Khor^{1

53

56}, Caroline Hayward¹², Robert N Luben¹³, Paul J Foster^{57

58}, Barbara E K Klein⁵⁹, Ronald Klein⁵⁹, Hoi-Suen Wong¹⁵, Paul Mitchell⁶⁰, Andres Metspalu¹⁸, Tin Aung^{1

7}, Terri L Young⁶¹, Mingguang He⁶², Olavi Pärssinen^{63

64}, Cornelia M van Duijn⁴, Jie Jin Wang⁶⁰, Cathy Williams³⁴, Jost B Jonas^{52

65}, Yik-Ying Teo^{53

56

66}, David A Mackey^{26

67}, Konrad Oexle⁴⁸, Nagahisa Yoshimura¹⁴, Andrew D Paterson¹⁵, Norbert Pfeiffer¹⁰, Tien-Yin Wong^{1

2

7

53}, Paul N Baird¹⁹, Dwight Stambolian⁶⁸, Joan E Bailey Wilson⁵, Ching-Yu Cheng^{1

2

7}, Christopher J Hammond^{8

29}, Caroline C W Klaver^{3

4}, Seang-Mei Saw^{1

2

7

53}, Jugnoo S Rahi, Jean-François Korobelnik, John P Kemp, Nicholas J Timpson, George Davey Smith, Jamie E Craig, Kathryn P Burdon, Rhys D Fogarty, Sudha K Iyengar, Emily Chew, Sarayut Janmahasatian, Nicholas G Martin, Stuart MacGregor¹⁷, Liang Xu⁵², Maria Schache¹⁹, Vinay Nangia, Songhomitra Panda-Jonas, Alan F Wright¹², Jeremy R Fondran, Jonathan H Lass, Sheng Feng, Jing Hua Zhao, Kay-Tee Khaw¹³, Nick J Wareham, Taina Rantanen, Jaakko Kaprio, Chi Pui Pang, Li Jia Chen, Pancy O Tam, Vishal Jhanji, Alvin L Young, Angela Döring, Leslie J Raffel, Mary-Frances Cotch, Xiaohui Li, Shea Ping Yip, Maurice K H Yap, Ginevra Biino, Simona Vaccargiu²², Maurizio Fossarello²², Brian Fleck, Seyhan Yazar^{19

67}, Jan Willem L Tideman^{3

4}, Milly Tedja^{3

4}, Margaret M Deangelis, Margaux Morrison, Lindsay Farrer, Xiangtian Zhou, Wei Chen, Nobuhisa Mizuki, Akira Meguro, Kari Matti Mäkelä

Affiliations

¹ Singapore Eye Research Institute, Singapore National Eye Centre, Singapore 169856, Singapore.
² Duke-NUS Medical School, Singapore 169857, Singapore.
³ Department of Ophthalmology, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁴ Department of Epidemiology, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁵ Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Baltimore, Maryland 21224, USA.
⁶ Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland 20205, USA.
⁷ Department of Ophthalmology, National University Health Systems, National University of Singapore Singapore 119228, Singapore.
⁸ Department of Twin Research and Genetic Epidemiology, King's College London School of Medicine, London SE1 7EH, UK.
⁹ School of Optometry and Vision Sciences, Cardiff University, Cardiff CF24 4HQ, UK.
¹⁰ Department of Ophthalmology, University Medical Center Mainz, 55131 Mainz, Germany.
¹¹ Department of Ophthalmology, Inselspital, University Hospital Bern, CH-3010 Bern, Switzerland.
¹² Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh EH4 2XU, Scotland.
¹³ Department of Public Health and Primary Care, Institute of Public Health, University of Cambridge School of Clinical Medicine, Cambridge CB2 0SR, UK.
¹⁴ Department of Ophthalmology and Visual Sciences, Kyoto University Graduate School of Medicine, Kyoto 6068507, Japan.
¹⁵ Program in Genetics and Genome Biology, The Hospital for Sick Children and Institute for Medical Sciences, University of Toronto, Toronto Ontario, Canada M5G 1X8.
¹⁶ Department of Clinical Chemistry, Fimlab Laboratories and School of Medicine, University of Tampere, Tampere 33520, Finland.
¹⁷ Statistical Genetics Laboratory, QIMR Berghofer Medical Research Institute, Herston, Brisbane, Queensland 4029, Australia.
¹⁸ Estonian Genome Center, University of Tartu, Tartu 51010, Estonia.
¹⁹ Centre for Eye Research Australia (CERA), Royal Victorian Eye and Ear Hospital, University of Melbourne, Melbourne, Victoria 3002, Australia.
²⁰ Université de Bordeaux, ISPED (Institut de Santé Publique d'Épidémiologie et de Développement), Bordeaux 33000, France.
²¹ INSERM, U1219-Bordeaux Population Health Research Center, Bordeaux 33000, France.
²² Institute of Population Genetics, National Research Council, Sassari 07100, Italy.
²³ Department of Public Health, University of Helsinki, Helsinki 00014, Finland.
²⁴ Department of Ophthalmology, University of Helsinki and Helsinki University Hospital, Helsinki 00014, Finland.
²⁵ UCL Institute of Ophthalmology, London SE1 7EH, UK.
²⁶ Menzies Research Institute Tasmania, University of Tasmania, Hobart, Tasmania 7000, Australia.
²⁷ Department of Statistical Science, School of Mathematics and Computational Science, Sun Yat-Sen University, Guangzhou 510275, China.
²⁸ Institute of Medical Biostatistics, Epidemiology and Informatics, University Medical Center Mainz, 55131 Mainz, Germany.
²⁹ Department of Ophthalmology, King's College London, London SE1 7EH, UK.
³⁰ Faculty of Medicine, University of Split, Split 21000, Croatia.
³¹ Usher Institute for Population Health Sciences and Informatics, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, Scotland.
³² Department of Ophthalmology, Sisters of Mercy University Hospital, Zagreb 10000, Croatia.
³³ MRC Integrative Epidemiology Unit (IEU), University of Bristol, Bristol BS8 2BN, UK.
³⁴ School of Social and Community Medicine, University of Bristol, Bristol BS8 2BN, UK.
³⁵ Max Planck Institute for Psycholinguistics, Wundtlaan 1, 6525 XD Nijmegen, The Netherlands.
³⁶ University of Queensland Diamantina Institute, Translational Research Institute, Brisbane, Queensland 4102, Australia.
³⁷ Department of Genetics, Genomics and Informatics, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA.
³⁸ Department of Epidemiology and Biostatistics, Case Western Reserve University, Cleveland, Ohio 44106, USA.
³⁹ Dardenne Eye Hospital, Bonn-Bad Godesberg, 53177 Bonn, Germany.
⁴⁰ Inserm, U1167, Lille 59000, France.
⁴¹ Univ. Lille, U1167, Lille 59000, France.
⁴² Université Lille 2, Lille 59000, France.
⁴³ Research Centre of Applied and Preventive Medicine, University of Turku, Turku 20520, Finland.
⁴⁴ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku 20520, Finland.
⁴⁵ Department of Clinical Physiology, Tampere University Hospital and School of Medicine, University of Tampere, Tampere 33520, Finland.
⁴⁶ Clinic for General and Interventional Cardiology, University Heart Center Hamburg, 20246 Hamburg, Germany.
⁴⁷ Institute of Human Genetics, Helmholtz Zentrum München, 85764 Neuherberg, Germany.
⁴⁸ Institute of Human Genetics, Klinikum rechts der Isar, Technische Universität München, 81675 Munich, Germany.
⁴⁹ Institute of Genetic Epidemiology, Helmholtz Zentrum München-German Research Center for Environmental Health, 85764 Neuherberg, Germany.
⁵⁰ Department of Internal Medicine, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁵¹ Netherlands Consortium for Healthy Ageing, Netherlands Genomics Initiative, 2518 AD Hague, The Netherlands.
⁵² Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing 100044, China.
⁵³ Saw Swee Hock School of Public Health, National University of Singapore and National University Health Systems, Singapore 117549, Singapore.
⁵⁴ National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore 308433, Singapore.
⁵⁵ Department of Medicine, National University of Singapore, Singapore 119228, Singapore.
⁵⁶ Division of Human Genetics, Genome Institute of Singapore, Singapore 138672, Singapore.
⁵⁷ Division of Genetics and Epidemiology, UCL Institute of Ophthalmology, London EC1V 9EL, UK.
⁵⁸ NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology, London EC1V 2PD, UK.
⁵⁹ Department of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53726, USA.
⁶⁰ Department of Ophthalmology, Centre for Vision Research, Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales 2145, Australia.
⁶¹ Department of Ophthalmology and Visual Sciences, School of Medicine and Public Health, University of Wisconsin, Madison, Wisconsin 53705, USA.
⁶² State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou 510060, China.
⁶³ Department of Ophthalmology, Central Hospital of Central Finland, Jyväskylä 40620, Finland.
⁶⁴ Gerontology Research Center and Department of Health Sciences, University of Jyväskylä, Jyväskylä 40014, Finland.
⁶⁵ Medical Faculty Mannheim, Department of Ophthalmology, Ruprecht-Karls-University Heidelberg, 69115 Mannheim, Germany.
⁶⁶ Department of Statistics and Applied Probability, National University of Singapore, Singapore 117546, Singapore.
⁶⁷ Centre for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia, Perth, Western Australia 6009, Australia.
⁶⁸ Department of Ophthalmology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

PMID: 27020472
PMCID: PMC4820539
DOI: 10.1038/ncomms11008

Meta-Analysis

Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error

Qiao Fan et al. Nat Commun. 2016.

. 2016 Mar 29:7:11008.

doi: 10.1038/ncomms11008.

Authors

Affiliations

¹ Singapore Eye Research Institute, Singapore National Eye Centre, Singapore 169856, Singapore.
² Duke-NUS Medical School, Singapore 169857, Singapore.
³ Department of Ophthalmology, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁴ Department of Epidemiology, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁵ Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Baltimore, Maryland 21224, USA.
⁶ Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland 20205, USA.
⁷ Department of Ophthalmology, National University Health Systems, National University of Singapore Singapore 119228, Singapore.
⁸ Department of Twin Research and Genetic Epidemiology, King's College London School of Medicine, London SE1 7EH, UK.
⁹ School of Optometry and Vision Sciences, Cardiff University, Cardiff CF24 4HQ, UK.
¹⁰ Department of Ophthalmology, University Medical Center Mainz, 55131 Mainz, Germany.
¹¹ Department of Ophthalmology, Inselspital, University Hospital Bern, CH-3010 Bern, Switzerland.
¹² Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh EH4 2XU, Scotland.
¹³ Department of Public Health and Primary Care, Institute of Public Health, University of Cambridge School of Clinical Medicine, Cambridge CB2 0SR, UK.
¹⁴ Department of Ophthalmology and Visual Sciences, Kyoto University Graduate School of Medicine, Kyoto 6068507, Japan.
¹⁵ Program in Genetics and Genome Biology, The Hospital for Sick Children and Institute for Medical Sciences, University of Toronto, Toronto Ontario, Canada M5G 1X8.
¹⁶ Department of Clinical Chemistry, Fimlab Laboratories and School of Medicine, University of Tampere, Tampere 33520, Finland.
¹⁷ Statistical Genetics Laboratory, QIMR Berghofer Medical Research Institute, Herston, Brisbane, Queensland 4029, Australia.
¹⁸ Estonian Genome Center, University of Tartu, Tartu 51010, Estonia.
¹⁹ Centre for Eye Research Australia (CERA), Royal Victorian Eye and Ear Hospital, University of Melbourne, Melbourne, Victoria 3002, Australia.
²⁰ Université de Bordeaux, ISPED (Institut de Santé Publique d'Épidémiologie et de Développement), Bordeaux 33000, France.
²¹ INSERM, U1219-Bordeaux Population Health Research Center, Bordeaux 33000, France.
²² Institute of Population Genetics, National Research Council, Sassari 07100, Italy.
²³ Department of Public Health, University of Helsinki, Helsinki 00014, Finland.
²⁴ Department of Ophthalmology, University of Helsinki and Helsinki University Hospital, Helsinki 00014, Finland.
²⁵ UCL Institute of Ophthalmology, London SE1 7EH, UK.
²⁶ Menzies Research Institute Tasmania, University of Tasmania, Hobart, Tasmania 7000, Australia.
²⁷ Department of Statistical Science, School of Mathematics and Computational Science, Sun Yat-Sen University, Guangzhou 510275, China.
²⁸ Institute of Medical Biostatistics, Epidemiology and Informatics, University Medical Center Mainz, 55131 Mainz, Germany.
²⁹ Department of Ophthalmology, King's College London, London SE1 7EH, UK.
³⁰ Faculty of Medicine, University of Split, Split 21000, Croatia.
³¹ Usher Institute for Population Health Sciences and Informatics, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, Scotland.
³² Department of Ophthalmology, Sisters of Mercy University Hospital, Zagreb 10000, Croatia.
³³ MRC Integrative Epidemiology Unit (IEU), University of Bristol, Bristol BS8 2BN, UK.
³⁴ School of Social and Community Medicine, University of Bristol, Bristol BS8 2BN, UK.
³⁵ Max Planck Institute for Psycholinguistics, Wundtlaan 1, 6525 XD Nijmegen, The Netherlands.
³⁶ University of Queensland Diamantina Institute, Translational Research Institute, Brisbane, Queensland 4102, Australia.
³⁷ Department of Genetics, Genomics and Informatics, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA.
³⁸ Department of Epidemiology and Biostatistics, Case Western Reserve University, Cleveland, Ohio 44106, USA.
³⁹ Dardenne Eye Hospital, Bonn-Bad Godesberg, 53177 Bonn, Germany.
⁴⁰ Inserm, U1167, Lille 59000, France.
⁴¹ Univ. Lille, U1167, Lille 59000, France.
⁴² Université Lille 2, Lille 59000, France.
⁴³ Research Centre of Applied and Preventive Medicine, University of Turku, Turku 20520, Finland.
⁴⁴ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku 20520, Finland.
⁴⁵ Department of Clinical Physiology, Tampere University Hospital and School of Medicine, University of Tampere, Tampere 33520, Finland.
⁴⁶ Clinic for General and Interventional Cardiology, University Heart Center Hamburg, 20246 Hamburg, Germany.
⁴⁷ Institute of Human Genetics, Helmholtz Zentrum München, 85764 Neuherberg, Germany.
⁴⁸ Institute of Human Genetics, Klinikum rechts der Isar, Technische Universität München, 81675 Munich, Germany.
⁴⁹ Institute of Genetic Epidemiology, Helmholtz Zentrum München-German Research Center for Environmental Health, 85764 Neuherberg, Germany.
⁵⁰ Department of Internal Medicine, Erasmus Medical Center, 3000 CA Rotterdam, The Netherlands.
⁵¹ Netherlands Consortium for Healthy Ageing, Netherlands Genomics Initiative, 2518 AD Hague, The Netherlands.
⁵² Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing 100044, China.
⁵³ Saw Swee Hock School of Public Health, National University of Singapore and National University Health Systems, Singapore 117549, Singapore.
⁵⁴ National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore 308433, Singapore.
⁵⁵ Department of Medicine, National University of Singapore, Singapore 119228, Singapore.
⁵⁶ Division of Human Genetics, Genome Institute of Singapore, Singapore 138672, Singapore.
⁵⁷ Division of Genetics and Epidemiology, UCL Institute of Ophthalmology, London EC1V 9EL, UK.
⁵⁸ NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology, London EC1V 2PD, UK.
⁵⁹ Department of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53726, USA.
⁶⁰ Department of Ophthalmology, Centre for Vision Research, Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales 2145, Australia.
⁶¹ Department of Ophthalmology and Visual Sciences, School of Medicine and Public Health, University of Wisconsin, Madison, Wisconsin 53705, USA.
⁶² State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, Guangzhou 510060, China.
⁶³ Department of Ophthalmology, Central Hospital of Central Finland, Jyväskylä 40620, Finland.
⁶⁴ Gerontology Research Center and Department of Health Sciences, University of Jyväskylä, Jyväskylä 40014, Finland.
⁶⁵ Medical Faculty Mannheim, Department of Ophthalmology, Ruprecht-Karls-University Heidelberg, 69115 Mannheim, Germany.
⁶⁶ Department of Statistics and Applied Probability, National University of Singapore, Singapore 117546, Singapore.
⁶⁷ Centre for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia, Perth, Western Australia 6009, Australia.
⁶⁸ Department of Ophthalmology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

PMID: 27020472
PMCID: PMC4820539
DOI: 10.1038/ncomms11008

Abstract

Myopia is the most common human eye disorder and it results from complex genetic and environmental causes. The rapidly increasing prevalence of myopia poses a major public health challenge. Here, the CREAM consortium performs a joint meta-analysis to test single-nucleotide polymorphism (SNP) main effects and SNP × education interaction effects on refractive error in 40,036 adults from 25 studies of European ancestry and 10,315 adults from 9 studies of Asian ancestry. In European ancestry individuals, we identify six novel loci (FAM150B-ACP1, LINC00340, FBN1, DIS3L-MAP2K1, ARID2-SNAT1 and SLC14A2) associated with refractive error. In Asian populations, three genome-wide significant loci AREG, GABRR1 and PDE10A also exhibit strong interactions with education (P<8.5 × 10(-5)), whereas the interactions are less evident in Europeans. The discovery of these loci represents an important advance in understanding how gene and environment interactions contribute to the heterogeneity of myopia.

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Figures

**Figure 1. Forest plot of education main effects on spherical equivalent across studies.**
The β-coefficient represents the differences of dioptres in refractive error comparing individuals in higher education group versus lower education group in Europeans (n=40,036), Asians (n=10,315) and all studies (n=50,351). The studies are sorted by effect size of education on spherical equivalent within Europeans and Asians studies, respectively.

**Figure 2. Manhattan plots of −log₁₀(P) for the JMA on SNP main effects and SNP × education effects on spherical equivalent in (a) European ancestry populations and (b) Asian populations.**
The horizontal red line indicates the genome-wide significance level of P_JMA<5 × 10⁻⁸. The horizontal blue line indicates the suggestive significance level of P_JMA<1 × 10⁻⁵. Novel loci reaching genome-wide significance are labelled in red and known loci are in grey.

See this image and copyright information in PMC

References

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Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error

Affiliations

Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error

Authors

Affiliations

Abstract

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Miscellaneous