Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study

Background Idiopathic pulmonary fibrosis (IPF) is a chronic progressive lung disease with high mortality, uncertain cause, and few treatment options. Studies have identified a significant genetic risk associated with the development of IPF; however, mechanisms by which genetic risk factors promote...

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Main Authors: Allen, Richard J., Porte, Joanne, Braybrooke, Rebecca, Flores, Carlos, Fingerlin, Tasha E., Oldham, Justin M., Guillen-Guio, Beatriz, Ma, Shwu-Fan, Okamoto, Tsukasa, John, Alison E., Obeidat, Ma'en, Yang, Ivana V., Henry, Amanda, Hubbard, Richard B., Navaratnam, Vidya, Saini, Gauri, Thompson, Norma, Booth, Helen L., Hart, Simon P., Hill, Mike R., Hirani, Nik, Maher, Toby M., McAnulty, Robin J., Millar, Ann B., Molyneaux, Philip L., Parfrey, Helen, Rassl, Doris M., Whyte, Moira K.B., Fahy, William A., Marshall, Richard P., Oballa, Eunice, Bossé, Yohan, Nickle, David C., Sin, Don D., Timens, Wim, Shrine, Nick, Sayers, Ian, Hall, Ian P., Noth, Imre, Schwartz, David A., Tobin, Martin D., Wain, Louise V., Jenkins, R. Gisli
Format: Article
Published: Elsevier 2017
Online Access:https://eprints.nottingham.ac.uk/50335/
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author Allen, Richard J.
Porte, Joanne
Braybrooke, Rebecca
Flores, Carlos
Fingerlin, Tasha E.
Oldham, Justin M.
Guillen-Guio, Beatriz
Ma, Shwu-Fan
Okamoto, Tsukasa
John, Alison E.
Obeidat, Ma'en
Yang, Ivana V.
Henry, Amanda
Hubbard, Richard B.
Navaratnam, Vidya
Saini, Gauri
Thompson, Norma
Booth, Helen L.
Hart, Simon P.
Hill, Mike R.
Hirani, Nik
Maher, Toby M.
McAnulty, Robin J.
Millar, Ann B.
Molyneaux, Philip L.
Parfrey, Helen
Rassl, Doris M.
Whyte, Moira K.B.
Fahy, William A.
Marshall, Richard P.
Oballa, Eunice
Bossé, Yohan
Nickle, David C.
Sin, Don D.
Timens, Wim
Shrine, Nick
Sayers, Ian
Hall, Ian P.
Noth, Imre
Schwartz, David A.
Tobin, Martin D.
Wain, Louise V.
Jenkins, R. Gisli
author_facet Allen, Richard J.
Porte, Joanne
Braybrooke, Rebecca
Flores, Carlos
Fingerlin, Tasha E.
Oldham, Justin M.
Guillen-Guio, Beatriz
Ma, Shwu-Fan
Okamoto, Tsukasa
John, Alison E.
Obeidat, Ma'en
Yang, Ivana V.
Henry, Amanda
Hubbard, Richard B.
Navaratnam, Vidya
Saini, Gauri
Thompson, Norma
Booth, Helen L.
Hart, Simon P.
Hill, Mike R.
Hirani, Nik
Maher, Toby M.
McAnulty, Robin J.
Millar, Ann B.
Molyneaux, Philip L.
Parfrey, Helen
Rassl, Doris M.
Whyte, Moira K.B.
Fahy, William A.
Marshall, Richard P.
Oballa, Eunice
Bossé, Yohan
Nickle, David C.
Sin, Don D.
Timens, Wim
Shrine, Nick
Sayers, Ian
Hall, Ian P.
Noth, Imre
Schwartz, David A.
Tobin, Martin D.
Wain, Louise V.
Jenkins, R. Gisli
author_sort Allen, Richard J.
building Nottingham Research Data Repository
collection Online Access
description Background Idiopathic pulmonary fibrosis (IPF) is a chronic progressive lung disease with high mortality, uncertain cause, and few treatment options. Studies have identified a significant genetic risk associated with the development of IPF; however, mechanisms by which genetic risk factors promote IPF remain unclear. We aimed to identify genetic variants associated with IPF susceptibility and provide mechanistic insight using gene and protein expression analyses. Methods We used a two-stage approach: a genome-wide association study in patients with IPF of European ancestry recruited from nine different centres in the UK and controls selected from UK Biobank (stage 1) matched for age, sex, and smoking status; and a follow-up of associated genetic variants in independent datasets of patients with IPF and controls from two independent US samples from the Chicago consortium and the Colorado consortium (stage 2). We investigated the effect of novel signals on gene expression in large transcriptomic and genomic data resources, and examined expression using lung tissue samples from patients with IPF and controls. Findings 602 patients with IPF and 3366 controls were selected for stage 1. For stage 2, 2158 patients with IPF and 5195 controls were selected. We identified a novel genome-wide significant signal of association with IPF susceptibility near A-kinase anchoring protein 13 (AKAP13; rs62025270, odds ratio [OR] 1·27 [95% CI 1·18–1·37], p=1·32 × 10−9) and confirmed previously reported signals, including in mucin 5B (MUC5B; rs35705950, OR 2·89 [2·56–3·26], p=1·12 × 10−66) and desmoplakin (DSP; rs2076295, OR 1·44 [1·35–1·54], p=7·81 × 10−28). For rs62025270, the allele A associated with increased susceptibility to IPF was also associated with increased expression of AKAP13 mRNA in lung tissue from patients who had lung resection procedures (n=1111). We showed that AKAP13 is expressed in the alveolar epithelium and lymphoid follicles from patients with IPF, and AKAP13 mRNA expression was 1·42-times higher in lung tissue from patients with IPF (n=46) than that in lung tissue from controls (n=51). Interpretation AKAP13 is a Rho guanine nucleotide exchange factor regulating activation of RhoA, which is known to be involved in profibrotic signalling pathways. The identification of AKAP13 as a susceptibility gene for IPF increases the prospect of successfully targeting RhoA pathway inhibitors in patients with IPF.
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spelling nottingham-503352020-05-04T19:54:27Z https://eprints.nottingham.ac.uk/50335/ Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study Allen, Richard J. Porte, Joanne Braybrooke, Rebecca Flores, Carlos Fingerlin, Tasha E. Oldham, Justin M. Guillen-Guio, Beatriz Ma, Shwu-Fan Okamoto, Tsukasa John, Alison E. Obeidat, Ma'en Yang, Ivana V. Henry, Amanda Hubbard, Richard B. Navaratnam, Vidya Saini, Gauri Thompson, Norma Booth, Helen L. Hart, Simon P. Hill, Mike R. Hirani, Nik Maher, Toby M. McAnulty, Robin J. Millar, Ann B. Molyneaux, Philip L. Parfrey, Helen Rassl, Doris M. Whyte, Moira K.B. Fahy, William A. Marshall, Richard P. Oballa, Eunice Bossé, Yohan Nickle, David C. Sin, Don D. Timens, Wim Shrine, Nick Sayers, Ian Hall, Ian P. Noth, Imre Schwartz, David A. Tobin, Martin D. Wain, Louise V. Jenkins, R. Gisli Background Idiopathic pulmonary fibrosis (IPF) is a chronic progressive lung disease with high mortality, uncertain cause, and few treatment options. Studies have identified a significant genetic risk associated with the development of IPF; however, mechanisms by which genetic risk factors promote IPF remain unclear. We aimed to identify genetic variants associated with IPF susceptibility and provide mechanistic insight using gene and protein expression analyses. Methods We used a two-stage approach: a genome-wide association study in patients with IPF of European ancestry recruited from nine different centres in the UK and controls selected from UK Biobank (stage 1) matched for age, sex, and smoking status; and a follow-up of associated genetic variants in independent datasets of patients with IPF and controls from two independent US samples from the Chicago consortium and the Colorado consortium (stage 2). We investigated the effect of novel signals on gene expression in large transcriptomic and genomic data resources, and examined expression using lung tissue samples from patients with IPF and controls. Findings 602 patients with IPF and 3366 controls were selected for stage 1. For stage 2, 2158 patients with IPF and 5195 controls were selected. We identified a novel genome-wide significant signal of association with IPF susceptibility near A-kinase anchoring protein 13 (AKAP13; rs62025270, odds ratio [OR] 1·27 [95% CI 1·18–1·37], p=1·32 × 10−9) and confirmed previously reported signals, including in mucin 5B (MUC5B; rs35705950, OR 2·89 [2·56–3·26], p=1·12 × 10−66) and desmoplakin (DSP; rs2076295, OR 1·44 [1·35–1·54], p=7·81 × 10−28). For rs62025270, the allele A associated with increased susceptibility to IPF was also associated with increased expression of AKAP13 mRNA in lung tissue from patients who had lung resection procedures (n=1111). We showed that AKAP13 is expressed in the alveolar epithelium and lymphoid follicles from patients with IPF, and AKAP13 mRNA expression was 1·42-times higher in lung tissue from patients with IPF (n=46) than that in lung tissue from controls (n=51). Interpretation AKAP13 is a Rho guanine nucleotide exchange factor regulating activation of RhoA, which is known to be involved in profibrotic signalling pathways. The identification of AKAP13 as a susceptibility gene for IPF increases the prospect of successfully targeting RhoA pathway inhibitors in patients with IPF. Elsevier 2017-11 Article PeerReviewed Allen, Richard J., Porte, Joanne, Braybrooke, Rebecca, Flores, Carlos, Fingerlin, Tasha E., Oldham, Justin M., Guillen-Guio, Beatriz, Ma, Shwu-Fan, Okamoto, Tsukasa, John, Alison E., Obeidat, Ma'en, Yang, Ivana V., Henry, Amanda, Hubbard, Richard B., Navaratnam, Vidya, Saini, Gauri, Thompson, Norma, Booth, Helen L., Hart, Simon P., Hill, Mike R., Hirani, Nik, Maher, Toby M., McAnulty, Robin J., Millar, Ann B., Molyneaux, Philip L., Parfrey, Helen, Rassl, Doris M., Whyte, Moira K.B., Fahy, William A., Marshall, Richard P., Oballa, Eunice, Bossé, Yohan, Nickle, David C., Sin, Don D., Timens, Wim, Shrine, Nick, Sayers, Ian, Hall, Ian P., Noth, Imre, Schwartz, David A., Tobin, Martin D., Wain, Louise V. and Jenkins, R. Gisli (2017) Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study. Lancet Respiratory Medicine, 5 (11). pp. 869-880. ISSN 2213-2619 https://www.sciencedirect.com/science/article/pii/S2213260017303879 doi:10.1016/S2213-2600(17)30387-9 doi:10.1016/S2213-2600(17)30387-9
spellingShingle Allen, Richard J.
Porte, Joanne
Braybrooke, Rebecca
Flores, Carlos
Fingerlin, Tasha E.
Oldham, Justin M.
Guillen-Guio, Beatriz
Ma, Shwu-Fan
Okamoto, Tsukasa
John, Alison E.
Obeidat, Ma'en
Yang, Ivana V.
Henry, Amanda
Hubbard, Richard B.
Navaratnam, Vidya
Saini, Gauri
Thompson, Norma
Booth, Helen L.
Hart, Simon P.
Hill, Mike R.
Hirani, Nik
Maher, Toby M.
McAnulty, Robin J.
Millar, Ann B.
Molyneaux, Philip L.
Parfrey, Helen
Rassl, Doris M.
Whyte, Moira K.B.
Fahy, William A.
Marshall, Richard P.
Oballa, Eunice
Bossé, Yohan
Nickle, David C.
Sin, Don D.
Timens, Wim
Shrine, Nick
Sayers, Ian
Hall, Ian P.
Noth, Imre
Schwartz, David A.
Tobin, Martin D.
Wain, Louise V.
Jenkins, R. Gisli
Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title_full Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title_fullStr Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title_full_unstemmed Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title_short Genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of European ancestry: a genome-wide association study
title_sort genetic variants associated with susceptibility to idiopathic pulmonary fibrosis in people of european ancestry: a genome-wide association study
url https://eprints.nottingham.ac.uk/50335/
https://eprints.nottingham.ac.uk/50335/
https://eprints.nottingham.ac.uk/50335/