Clinical case: A 27-year-old woman with known familial exudative vitreoretinopathy (FEVR) presented to the metabolic bone clinic for further evaluation of recurrent fragility fractures occurring since childhood including a wrist fracture at age 7, a hip fracture at age 10 and numerous vertebral fractures in pre-adolescence. Bone mineral density (BMD) performed at the spine (L1-4) at age 9 was 0.47 g/cm2 (Z-score -2.6). Her most recent BMD at age 26 showed a nadir BMD at the left neck of femur of 0.68g/m2 (Z-score -2.5). Her height is below the 1st centile. Her 45-year-old mother, also affected by FEVR, shares striking similarities including distinct facies, dental hypoplasia, thin hair, mild intellectual impairment, and height below the 1st centile. She had fractures of the humerus, scapula and clavicle after a fall from standing height at age 36. Her most recent BMD at age 44 shows density at the spine of 0.56 g/cm2 (T-score -5.2, Z-score -4.3) and right neck of femur 0.51g/cm2 (T-score -4.0, Z-score -3.0).
The combination of osteoporosis and exudative vitreoretinopathy strongly suggested osteoporosis pseudoglioma syndrome (OPPG), however both mother and daughter were negative for LRP5 mutation. Targeted exome sequencing revealed a missense variant in CTNNB1 (c.1723G>A; pGly575Arg), resulting in a single amino acid change in a highly conserved glycine residue in exon 11 of the ß-catenin protein; it was absent from controls (frequency of 0 in gnomAD database) and predicted to be deleterious by a number of in silico tools, and classified as likely pathogenic. Segregation testing in the mother revealed the same variant. Mutations in CTNNB1 are a known cause of autosomal dominant FEVR. However, although the ophthalmological phenotype is well described, no skeletal phenotype within this patient population has previously been reported.
Mutations in LRP5 are the established cause of OPPG, a hitherto autosomal recessive condition characterised by abnormal development of peripheral retinal vasculature leading to sight-threatening complications of ischaemia, neovascularization, retinal traction, detachment, exudation and dysplasia and corneal opacity (1). Classically, OPPG causes low bone mass and frequent fractures but LRP5 mutations may also cause FEVR without skeletal abnormalities, including autosomal-dominant forms (2,3). Similarly, CTNNB1 mutations can cause a range of ophthalmological conditions including FEVR, optic nerve atrophy, refractive errors and strabismus (1,4) including in an 11-year-old patient with the same p.Gly575Arg mutation seen in the family we are reporting (5). Other reported conditions associated with variants of CTNNB1 include behavioural abnormalities including autism, developmental delay and intellectual disability with a wide variability in severity observed (6). In one family affected by FEVR with a CTNNB1 mutation the unaffected mother was found to be a carrier for the mutant allele. As such, it appears that penetrance and expressivity is highly variable (4).
Both LRP5 and ß-catenin are widely expressed and form part of the canonical Wnt signalling pathway which is critical for normal skeletal development. Wnt signalling potentiates mesenchymal stem cells towards osteochondral differentiation and subsequently, to an osteoblast lineage cell fate (9). In a mouse model, Hill et al. demonstrated that ß-catenin stabilisation and knockout resulted in osteopetrotic and osteopaenic phenotypes respectively (9). In mature bone, Wnt binds to cell-surface Frizzled (Fzd) receptor and the LRP5/6 coreceptor on osteoblasts, resulting in canonical amplification of ß-catenin and a pro-anabolic milieu by promoting osteoblast and osteocyte survival and inhibiting osteoclast differentiation (10).
The association of CTNNB1 gene changes and bone disease in humans has not been clearly described. In a meta-analysis of genome-wide association studies, a single-nucleotide polymorphism (SNP) on chromosome 3, upstream of the CTNNB1 gene was identified as one of twenty statistically significant SNPs for low BMD at the femoral neck (7). Pertussa et al. demonstrated a similar association of low spine BMD with this SNP in a cohort of Spanish women (8).
Despite compelling evidence for an effect of CTNNB1 haploinsufficiency on bone, to our knowledge, this is the first report to highlight the bone phenotype in patients with FEVR due to a CTNNB1 mutation, and the first report of an autosomal dominant cause of an OPPG-like syndrome.
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