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

H. Zheng, V. Forgetta, Y.H. Hsu, K. Estrada, A. Rosello-Diez, C.P.G.M. de Groot

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443 Citations (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 variants1, 2, 3, 4, 5, 6, 7, 8, as well as rare, population-specific, coding variants9. 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 BMD8 (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 En1cre/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.
Original languageEnglish
Pages (from-to)112-117
JournalNature
Volume526
DOIs
Publication statusPublished - 2015

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