Whole-genome sequencing identifies EN1 as a determinant of bone density and fracture

Hou-Feng Zheng, Vincenzo Forgetta, Yi-Hsiang Hsu, Karol Estrada, Alberto Rosello-Diez, Paul J Leo, Chitra L Dahia, Kyung Hyun Park-Min, Jonathan H Tobias, Charles Kooperberg, Aaron Kleinman, Unnur Styrkarsdottir, Ching-Ti Liu, Charlotta Uggla, Daniel S Evans, Carrie M Nielson, Klaudia Walter, Ulrika Pettersson-Kymmer, Shane McCarthy, Joel ErikssonTony Kwan, Mila Jhamai, Katerina Trajanoska, Yasin Memari, Josine Min, Jie Huang, Petr Danecek, Beth Wilmot, Rui Li, Wen-Chi Chou, Lauren E Mokry, Alireza Moayyeri, Melina Claussnitzer, Chia-Ho Cheng, Warren Cheung, Carolina Medina-Gómez, Bing Ge, Shu-Huang Chen, Kwangbom Choi, Ling Oei, James Fraser, Robert Kraaij, Matthew A Hibbs, Celia L Gregson, Denis Paquette, Albert Hofman, Carl Wibom, Gregory J Tranah, Mhairi Marshall, Jens-Erik B Jensen, AOGC Consortium

456 Citationer (Scopus)

Abstract

The extent to which low-frequency (minor allele frequency (MAF) between 1-5%) and rare (MAF ≤ 1%) variants contribute to complex traits and disease in the general population is mainly unknown. Bone mineral density (BMD) is highly heritable, a major predictor of osteoporotic fractures, and has been previously associated with common genetic variants, as well as rare, population-specific, coding variants. Here we identify novel non-coding genetic variants with large effects on BMD (ntotal = 53,236) and fracture (ntotal = 508,253) in individuals of European ancestry from the general population. Associations for BMD were derived from whole-genome sequencing (n = 2,882 from UK10K (ref. 10); a population-based genome sequencing consortium), whole-exome sequencing (n = 3,549), deep imputation of genotyped samples using a combined UK10K/1000 Genomes reference panel (n = 26,534), and de novo replication genotyping (n = 20,271). We identified a low-frequency non-coding variant near a novel locus, EN1, with an effect size fourfold larger than the mean of previously reported common variants for lumbar spine BMD (rs11692564(T), MAF = 1.6%, replication effect size = +0.20 s.d., Pmeta = 2 × 10(-14)), which was also associated with a decreased risk of fracture (odds ratio = 0.85; P = 2 × 10(-11); ncases = 98,742 and ncontrols = 409,511). Using an En1(cre/flox) mouse model, we observed that conditional loss of En1 results in low bone mass, probably as a consequence of high bone turnover. We also identified a novel low-frequency non-coding variant with large effects on BMD near WNT16 (rs148771817(T), MAF = 1.2%, replication effect size = +0.41 s.d., Pmeta = 1 × 10(-11)). In general, there was an excess of association signals arising from deleterious coding and conserved non-coding variants. These findings provide evidence that low-frequency non-coding variants have large effects on BMD and fracture, thereby providing rationale for whole-genome sequencing and improved imputation reference panels to study the genetic architecture of complex traits and disease in the general population.

OriginalsprogEngelsk
TidsskriftNature
Vol/bind526
Udgave nummer7571
Sider (fra-til)112-117
Antal sider6
ISSN0028-0836
DOI
StatusUdgivet - 14 sep. 2015

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