PUBLICATION

A rare mutation in SMAD9 associated with high bone mass identifies the SMAD-dependent BMP signalling pathway as a potential anabolic target for osteoporosis

Authors
Gregson, C.L., Bergen, D., Leo, P., Sessions, R.B., Wheeler, L., Hartley, A., Youlten, S., Croucher, P.I., McInerney-Leo, A.M., Fraser, W., Tang, J.C.Y., Anderson, L., Marshall, M., Sergot, L., Paternoster, L., Davey-Smith, G., AOGC Consortium, Brown, M.A., Hammond, C., Kemp, J.P., Tobias, J.H., Duncan, E.L.
ID
ZDB-PUB-190917-3
Date
2019
Source
Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research   35(1): 92-105 (Journal)
Registered Authors
Bergen, Dylan, Hammond, Chrissy
Keywords
DXA, High Bone Mass, SMAD9, exon sequencing, monogenic, osteoanabolic, zebrafish
MeSH Terms
  • Animals
  • Bone and Bones
  • Humans
  • Mice
  • Mutation
  • Osteoporosis*/diagnostic imaging
  • Osteoporosis*/drug therapy
  • Osteoporosis*/genetics
  • Signal Transduction
  • Smad8 Protein
  • Zebrafish*
PubMed
31525280 Full text @ J. Bone Miner. Res.
Abstract
Novel anabolic drug targets are needed to treat osteoporosis. Having established a large national cohort with unexplained high bone mass (HBM), we aimed to identify a novel monogenic cause of HBM and provide insight into a regulatory pathway potentially amenable to therapeutic intervention. We investigated a pedigree with unexplained HBM in whom previous sequencing had excluded known causes of monogenic HBM. Whole exome sequencing identified a rare (minor allele frequency 0.0023), highly evolutionarily conserved, missense mutation in SMAD9 (c.65T>C, p.Leu22Pro) segregating with HBM in this autosomal dominant family. The same mutation was identified in another two unrelated individuals both with HBM. In-silico protein modelling predicts the mutation severely disrupts the MH1 DNA-binding domain of SMAD9. Affected individuals have bone mineral density [BMD] Z-Scores +3 to +5, mandible enlargement, a broad frame, torus palatinus/ mandibularis, pes planus, increased shoe size and a tendency to sink when swimming. Peripheral quantitative computer tomography (pQCT) measurement demonstrates increased trabecular volumetric BMD and increased cortical thickness conferring greater predicted bone strength; bone turnover markers are low/normal. Notably, fractures and nerve compression are not seen. Both genome-wide, and gene-based association testing involving estimated-BMD measured at the heel in 362,924 white British subjects from the UK Biobank Study showed strong associations with SMAD9 (PGWAS = 6 x 10-16 ; PGENE = 8 × 10-17 ). Furthermore, we found Smad9 to be highly expressed in both murine cortical bone derived osteocytes and skeletal elements of zebrafish larvae. Our findings support SMAD9 as a novel HBM gene, and a potential novel osteoanabolic target for osteoporosis therapeutics. SMAD9 is thought to inhibit bone morphogenetic protein (BMP) dependent target gene transcription to reduce osteoblast activity. Thus, we hypothesise SMAD9 c.65T>C is a loss-of-function mutation reducing BMP inhibition. Lowering SMAD9 as a potential novel anabolic mechanism for osteoporosis therapeutics warrants further investigation.
Genes / Markers
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping