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

Qiao Fan; Virginie Verhoeven; Robert Wojciechowski; Veluchamy Barathi; Pirro Hysi; Jeremy Guggenheim; Rene Hohn; Veronique Vitart; Anthony Khawaja; Kenji Yamashiro; S Hosseini; Terho Lehtimaki; Yi Lu; Toomas Haller; Jing Xie; Cécile Delcourt; Mario Pirastu; Juho Wedenoja; Puya Gharahkhani; Cristina Venturini; Masahiro Miyake; Alex Hewitt; Xiaobo Guo; Johanna Mazur; Jenifer Huffman; Katie Williams; Ozren Polasek; Harry Campbell; Igor Rudan; Zoran Vatavuk; James Wilson; Peter Joshi; George McMahon; Beate St. Pourcain; David Evans; Claire Simpson; Tai-Hwi Schantes-An; Robert Igo; Alireza Mirshahi; Audrey Cougnard-Gregoire; Céline Bellenguez; Maria Blettner; Olli Raitakari; Mika Kahonen; Ilkka Seppala; Tanja Zeller; Thomas Meitinger; Janina Ried; Christian Gieger; Laura Portas; Elisabeth Van Leeuwen; Najaf Amin; André Uitterlinden; Fernando Rivadeneira; Albert Hofman; Johannes Vingerling; Ya Xing Wang; Wang Xu; Eileen Boh; M Kamran Ikram; Charumathi Sabanayagam; Preeti Gupti; Vincent Tan; Zhou Lei; Candice Ho; Wan'e Lim; Roger Beuerman; Rosalynn Siantar; E-Shyong Tai; Eranga Vithana; Evelin Mihailov; Chiea-Chuen Khor; Caroline Hayward; Robert Luben; Paul Foster; Barbara Klein; Ronald Klein; Hoi Wong; Paul Mitchell; Andres Metspalu; Tin Aung; Terri Young; Mingguang He; Olavi Parssinen; Cornelia van Duijn; Jie Wang; Cathy Williams; Jost Jonas; Yik-Ying Teo; David Mackey; Konrad Oexle; Nagahisa Yoshimura; Andrew Paterson; Norbert Pfeiffer; Tien-Yin Wong; Paul Baird; Dwight Stambolian; Joan Bailey-Wilson; Ching-Yu Cheng; Christopher Hammond; Caroline Klaver; Seang-Mei Saw; Jugnoo Rahi; Jean-Francois Korobelnik; John Kemp; Nicholas Timpson; George Smith; Jamie Craig; Kathryn Burdon; Rhys Fogarty; Sudha Iyengar; Emily Chew; Sarayut Janmahasatian; Nicholas Martin; Stuart Macgregor; Liang Xu; Maria Schache; Vinay Nangia; Songhomitra Panda-Jones; Alan Wright; Jeremy Fondran; Jonathan Lass; Sheng Feng; Jing Zhao; Kay-Tee Khaw; Nicholas Wareham; Taina Rantanen; Jaako Kaprio; Chi Pui Pang; Li Chen; Pancy Tam; Vishal Jhanji; Alvin Youn; Angela Doring; Leslie Raffel; Mary Cotch; Xiaohui Liu; Shea Yip; Maurice Yap; Ginevra Biino; Simona Vaccargiu; Maurizio Fossarello; Brian Fleck; Seyhan Yazar; Jan Tideman; Milly Tedja; Margaret Deangelis; Margaux Morrison; Lindsay Ferrer; Xiangtian Zhou; Wei Chen; Nobuhisa Mizuki; Akira Meguro; Kari Makela

doi:10.1038/ncomms11008

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

Qiao Fan, Virginie Verhoeven, Robert Wojciechowski, Veluchamy Barathi, Pirro Hysi, Jeremy Guggenheim, Rene Hohn, Veronique Vitart, Anthony Khawaja, Kenji Yamashiro, S Hosseini, Terho Lehtimaki, Yi Lu, Toomas Haller, Jing Xie, Cécile Delcourt, Mario Pirastu, Juho Wedenoja, Puya Gharahkhani, Cristina VenturiniMasahiro Miyake, Alex Hewitt, Xiaobo Guo, Johanna Mazur, Jenifer Huffman, Katie Williams, Ozren Polasek, Harry Campbell, Igor Rudan, Zoran Vatavuk, James Wilson, Peter Joshi, George McMahon, Beate St. Pourcain, David Evans, Claire Simpson, Tai-Hwi Schantes-An, Robert Igo, Alireza Mirshahi, Audrey Cougnard-Gregoire, Céline Bellenguez, Maria Blettner, Olli Raitakari, Mika Kahonen, Ilkka Seppala, Tanja Zeller, Thomas Meitinger, Janina Ried, Christian Gieger, Laura Portas, Elisabeth Van Leeuwen, Najaf Amin, André Uitterlinden, Fernando Rivadeneira, Albert Hofman, Johannes Vingerling, Ya Xing Wang, Wang Xu, Eileen Boh, M Kamran Ikram, Charumathi Sabanayagam, Preeti Gupti, Vincent Tan, Zhou Lei, Candice Ho, Wan'e Lim, Roger Beuerman, Rosalynn Siantar, E-Shyong Tai, Eranga Vithana, Evelin Mihailov, Chiea-Chuen Khor, Caroline Hayward, Robert Luben, Paul Foster, Barbara Klein, Ronald Klein, Hoi Wong, Paul Mitchell, Andres Metspalu, Tin Aung, Terri Young, Mingguang He, Olavi Parssinen, Cornelia van Duijn, Jie Wang, Cathy Williams, Jost Jonas, Yik-Ying Teo, David Mackey, Konrad Oexle, Nagahisa Yoshimura, Andrew Paterson, Norbert Pfeiffer, Tien-Yin Wong, Paul Baird, Dwight Stambolian, Joan Bailey-Wilson, Ching-Yu Cheng, Christopher Hammond, Caroline Klaver, Seang-Mei Saw, Jugnoo Rahi, Jean-Francois Korobelnik, John Kemp, Nicholas Timpson, George Smith, Jamie Craig, Kathryn Burdon, Rhys Fogarty, Sudha Iyengar, Emily Chew, Sarayut Janmahasatian, Nicholas Martin, Stuart Macgregor, Liang Xu, Maria Schache, Vinay Nangia, Songhomitra Panda-Jones, Alan Wright, Jeremy Fondran, Jonathan Lass, Sheng Feng, Jing Zhao, Kay-Tee Khaw, Nicholas Wareham, Taina Rantanen, Jaako Kaprio, Chi Pui Pang, Li Chen, Pancy Tam, Vishal Jhanji, Alvin Youn, Angela Doring, Leslie Raffel, Mary Cotch, Xiaohui Liu, Shea Yip, Maurice Yap, Ginevra Biino, Simona Vaccargiu, Maurizio Fossarello, Brian Fleck, Seyhan Yazar, Jan Tideman, Milly Tedja, Margaret Deangelis, Margaux Morrison, Lindsay Ferrer, Xiangtian Zhou, Wei Chen, Nobuhisa Mizuki, Akira Meguro, Kari Makela

College of Medicine and Public Health

Research output: Contribution to journal › Article › peer-review

104 Citations (Scopus)

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.

Original language	English
Article number	11008
Number of pages	12
Journal	Nature Communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms11008
Publication status	Published - 29 Mar 2016

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10.1038/ncomms11008

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Fan, Q., Verhoeven, V., Wojciechowski, R., Barathi, V., Hysi, P., Guggenheim, J., Hohn, R., Vitart, V., Khawaja, A., Yamashiro, K., Hosseini, S., Lehtimaki, T., Lu, Y., Haller, T., Xie, J., Delcourt, C., Pirastu, M., Wedenoja, J., Gharahkhani, P., ... Makela, K. (2016). Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error. Nature Communications, 7, Article 11008. https://doi.org/10.1038/ncomms11008

@article{2d8400ceee4a4b5c9bba99402f298a1e,

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

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.",

author = "Qiao Fan and Virginie Verhoeven and Robert Wojciechowski and Veluchamy Barathi and Pirro Hysi and Jeremy Guggenheim and Rene Hohn and Veronique Vitart and Anthony Khawaja and Kenji Yamashiro and S Hosseini and Terho Lehtimaki and Yi Lu and Toomas Haller and Jing Xie and C{\'e}cile Delcourt and Mario Pirastu and Juho Wedenoja and Puya Gharahkhani and Cristina Venturini and Masahiro Miyake and Alex Hewitt and Xiaobo Guo and Johanna Mazur and Jenifer Huffman and Katie Williams and Ozren Polasek and Harry Campbell and Igor Rudan and Zoran Vatavuk and James Wilson and Peter Joshi and George McMahon and {St. Pourcain}, Beate and David Evans and Claire Simpson and Tai-Hwi Schantes-An and Robert Igo and Alireza Mirshahi and Audrey Cougnard-Gregoire and C{\'e}line Bellenguez and Maria Blettner and Olli Raitakari and Mika Kahonen and Ilkka Seppala and Tanja Zeller and Thomas Meitinger and Janina Ried and Christian Gieger and Laura Portas and {Van Leeuwen}, Elisabeth and Najaf Amin and Andr{\'e} Uitterlinden and Fernando Rivadeneira and Albert Hofman and Johannes Vingerling and Wang, {Ya Xing} and Wang Xu and Eileen Boh and Ikram, {M Kamran} and Charumathi Sabanayagam and Preeti Gupti and Vincent Tan and Zhou Lei and Candice Ho and Wan'e Lim and Roger Beuerman and Rosalynn Siantar and E-Shyong Tai and Eranga Vithana and Evelin Mihailov and Chiea-Chuen Khor and Caroline Hayward and Robert Luben and Paul Foster and Barbara Klein and Ronald Klein and Hoi Wong and Paul Mitchell and Andres Metspalu and Tin Aung and Terri Young and Mingguang He and Olavi Parssinen and {van Duijn}, Cornelia and Jie Wang and Cathy Williams and Jost Jonas and Yik-Ying Teo and David Mackey and Konrad Oexle and Nagahisa Yoshimura and Andrew Paterson and Norbert Pfeiffer and Tien-Yin Wong and Paul Baird and Dwight Stambolian and Joan Bailey-Wilson and Ching-Yu Cheng and Christopher Hammond and Caroline Klaver and Seang-Mei Saw and Jugnoo Rahi and Jean-Francois Korobelnik and John Kemp and Nicholas Timpson and George Smith and Jamie Craig and Kathryn Burdon and Rhys Fogarty and Sudha Iyengar and Emily Chew and Sarayut Janmahasatian and Nicholas Martin and Stuart Macgregor and Liang Xu and Maria Schache and Vinay Nangia and Songhomitra Panda-Jones and Alan Wright and Jeremy Fondran and Jonathan Lass and Sheng Feng and Jing Zhao and Kay-Tee Khaw and Nicholas Wareham and Taina Rantanen and Jaako Kaprio and Pang, {Chi Pui} and Li Chen and Pancy Tam and Vishal Jhanji and Alvin Youn and Angela Doring and Leslie Raffel and Mary Cotch and Xiaohui Liu and Shea Yip and Maurice Yap and Ginevra Biino and Simona Vaccargiu and Maurizio Fossarello and Brian Fleck and Seyhan Yazar and Jan Tideman and Milly Tedja and Margaret Deangelis and Margaux Morrison and Lindsay Ferrer and Xiangtian Zhou and Wei Chen and Nobuhisa Mizuki and Akira Meguro and Kari Makela",

year = "2016",

month = mar,

day = "29",

doi = "10.1038/ncomms11008",

language = "English",

volume = "7",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature",

}

Fan, Q, Verhoeven, V, Wojciechowski, R, Barathi, V, Hysi, P, Guggenheim, J, Hohn, R, Vitart, V, Khawaja, A, Yamashiro, K, Hosseini, S, Lehtimaki, T, Lu, Y, Haller, T, Xie, J, Delcourt, C, Pirastu, M, Wedenoja, J, Gharahkhani, P, Venturini, C, Miyake, M, Hewitt, A, Guo, X, Mazur, J, Huffman, J, Williams, K, Polasek, O, Campbell, H, Rudan, I, Vatavuk, Z, Wilson, J, Joshi, P, McMahon, G, St. Pourcain, B, Evans, D, Simpson, C, Schantes-An, T-H, Igo, R, Mirshahi, A, Cougnard-Gregoire, A, Bellenguez, C, Blettner, M, Raitakari, O, Kahonen, M, Seppala, I, Zeller, T, Meitinger, T, Ried, J, Gieger, C, Portas, L, Van Leeuwen, E, Amin, N, Uitterlinden, A, Rivadeneira, F, Hofman, A, Vingerling, J, Wang, YX, Xu, W, Boh, E, Ikram, MK, Sabanayagam, C, Gupti, P, Tan, V, Lei, Z, Ho, C, Lim, W, Beuerman, R, Siantar, R, Tai, E-S, Vithana, E, Mihailov, E, Khor, C-C, Hayward, C, Luben, R, Foster, P, Klein, B, Klein, R, Wong, H, Mitchell, P, Metspalu, A, Aung, T, Young, T, He, M, Parssinen, O, van Duijn, C, Wang, J, Williams, C, Jonas, J, Teo, Y-Y, Mackey, D, Oexle, K, Yoshimura, N, Paterson, A, Pfeiffer, N, Wong, T-Y, Baird, P, Stambolian, D, Bailey-Wilson, J, Cheng, C-Y, Hammond, C, Klaver, C, Saw, S-M, Rahi, J, Korobelnik, J-F, Kemp, J, Timpson, N, Smith, G, Craig, J, Burdon, K, Fogarty, R, Iyengar, S, Chew, E, Janmahasatian, S, Martin, N, Macgregor, S, Xu, L, Schache, M, Nangia, V, Panda-Jones, S, Wright, A, Fondran, J, Lass, J, Feng, S, Zhao, J, Khaw, K-T, Wareham, N, Rantanen, T, Kaprio, J, Pang, CP, Chen, L, Tam, P, Jhanji, V, Youn, A, Doring, A, Raffel, L, Cotch, M, Liu, X, Yip, S, Yap, M, Biino, G, Vaccargiu, S, Fossarello, M, Fleck, B, Yazar, S, Tideman, J, Tedja, M, Deangelis, M, Morrison, M, Ferrer, L, Zhou, X, Chen, W, Mizuki, N, Meguro, A & Makela, K 2016, 'Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error', Nature Communications, vol. 7, 11008. https://doi.org/10.1038/ncomms11008

TY - JOUR

T1 - Meta-analysis of gene-environment-wide association scans accounting for education level identifies additional loci for refractive error

AU - Fan, Qiao

AU - Verhoeven, Virginie

AU - Wojciechowski, Robert

AU - Barathi, Veluchamy

AU - Hysi, Pirro

AU - Guggenheim, Jeremy

AU - Hohn, Rene

AU - Vitart, Veronique

AU - Khawaja, Anthony

AU - Yamashiro, Kenji

AU - Hosseini, S

AU - Lehtimaki, Terho

AU - Lu, Yi

AU - Haller, Toomas

AU - Xie, Jing

AU - Delcourt, Cécile

AU - Pirastu, Mario

AU - Wedenoja, Juho

AU - Gharahkhani, Puya

AU - Venturini, Cristina

AU - Miyake, Masahiro

AU - Hewitt, Alex

AU - Guo, Xiaobo

AU - Mazur, Johanna

AU - Huffman, Jenifer

AU - Williams, Katie

AU - Polasek, Ozren

AU - Campbell, Harry

AU - Rudan, Igor

AU - Vatavuk, Zoran

AU - Wilson, James

AU - Joshi, Peter

AU - McMahon, George

AU - St. Pourcain, Beate

AU - Evans, David

AU - Simpson, Claire

AU - Schantes-An, Tai-Hwi

AU - Igo, Robert

AU - Mirshahi, Alireza

AU - Cougnard-Gregoire, Audrey

AU - Bellenguez, Céline

AU - Blettner, Maria

AU - Raitakari, Olli

AU - Kahonen, Mika

AU - Seppala, Ilkka

AU - Zeller, Tanja

AU - Meitinger, Thomas

AU - Ried, Janina

AU - Gieger, Christian

AU - Portas, Laura

AU - Van Leeuwen, Elisabeth

AU - Amin, Najaf

AU - Uitterlinden, André

AU - Rivadeneira, Fernando

AU - Hofman, Albert

AU - Vingerling, Johannes

AU - Wang, Ya Xing

AU - Xu, Wang

AU - Boh, Eileen

AU - Ikram, M Kamran

AU - Sabanayagam, Charumathi

AU - Gupti, Preeti

AU - Tan, Vincent

AU - Lei, Zhou

AU - Ho, Candice

AU - Lim, Wan'e

AU - Beuerman, Roger

AU - Siantar, Rosalynn

AU - Tai, E-Shyong

AU - Vithana, Eranga

AU - Mihailov, Evelin

AU - Khor, Chiea-Chuen

AU - Hayward, Caroline

AU - Luben, Robert

AU - Foster, Paul

AU - Klein, Barbara

AU - Klein, Ronald

AU - Wong, Hoi

AU - Mitchell, Paul

AU - Metspalu, Andres

AU - Aung, Tin

AU - Young, Terri

AU - He, Mingguang

AU - Parssinen, Olavi

AU - van Duijn, Cornelia

AU - Wang, Jie

AU - Williams, Cathy

AU - Jonas, Jost

AU - Teo, Yik-Ying

AU - Mackey, David

AU - Oexle, Konrad

AU - Yoshimura, Nagahisa

AU - Paterson, Andrew

AU - Pfeiffer, Norbert

AU - Wong, Tien-Yin

AU - Baird, Paul

AU - Stambolian, Dwight

AU - Bailey-Wilson, Joan

AU - Cheng, Ching-Yu

AU - Hammond, Christopher

AU - Klaver, Caroline

AU - Saw, Seang-Mei

AU - Rahi, Jugnoo

AU - Korobelnik, Jean-Francois

AU - Kemp, John

AU - Timpson, Nicholas

AU - Smith, George

AU - Craig, Jamie

AU - Burdon, Kathryn

AU - Fogarty, Rhys

AU - Iyengar, Sudha

AU - Chew, Emily

AU - Janmahasatian, Sarayut

AU - Martin, Nicholas

AU - Macgregor, Stuart

AU - Xu, Liang

AU - Schache, Maria

AU - Nangia, Vinay

AU - Panda-Jones, Songhomitra

AU - Wright, Alan

AU - Fondran, Jeremy

AU - Lass, Jonathan

AU - Feng, Sheng

AU - Zhao, Jing

AU - Khaw, Kay-Tee

AU - Wareham, Nicholas

AU - Rantanen, Taina

AU - Kaprio, Jaako

AU - Pang, Chi Pui

AU - Chen, Li

AU - Tam, Pancy

AU - Jhanji, Vishal

AU - Youn, Alvin

AU - Doring, Angela

AU - Raffel, Leslie

AU - Cotch, Mary

AU - Liu, Xiaohui

AU - Yip, Shea

AU - Yap, Maurice

AU - Biino, Ginevra

AU - Vaccargiu, Simona

AU - Fossarello, Maurizio

AU - Fleck, Brian

AU - Yazar, Seyhan

AU - Tideman, Jan

AU - Tedja, Milly

AU - Deangelis, Margaret

AU - Morrison, Margaux

AU - Ferrer, Lindsay

AU - Zhou, Xiangtian

AU - Chen, Wei

AU - Mizuki, Nobuhisa

AU - Meguro, Akira

AU - Makela, Kari

PY - 2016/3/29

Y1 - 2016/3/29

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84962655499&partnerID=8YFLogxK

U2 - 10.1038/ncomms11008

DO - 10.1038/ncomms11008

M3 - Article

SN - 2041-1723

VL - 7

JO - Nature Communications

JF - Nature Communications

M1 - 11008

ER -

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

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