Original Article
High Bone Density Due to a Mutation in LDL-Receptor–Related Protein 5
N Engl J Med 2002; 346:1513-1521May 16, 2002
- Abstract
Background
Osteoporosis is a major public health problem of largely unknown cause. Loss-of-function mutations in the gene for low-density lipoprotein receptor–related protein 5 (LRP5), which acts in the Wnt signaling pathway, have been shown to cause osteoporosis–pseudoglioma.
Methods
We performed genetic and biochemical analyses of a kindred with an autosomal dominant syndrome characterized by high bone density, a wide and deep mandible, and torus palatinus.
Results
Genetic analysis revealed linkage of the syndrome to chromosome 11q12–13 (odds of linkage, >1 million to 1), an interval that contains LRP5. Affected members of the kindred had a mutation in this gene, with valine substituted for glycine at codon 171 (LRP5V171 ). This mutation segregated with the trait in the family and was absent in control subjects. The normal glycine lies in a so-called propeller motif that is highly conserved from fruit flies to humans. Markers of bone resorption were normal in the affected subjects, whereas markers of bone formation such as osteocalcin were markedly elevated. Levels of fibronectin, a known target of signaling by Wnt, a developmental protein, were also elevated. In vitro studies showed that the normal inhibition of Wnt signaling by another protein, Dickkopf-1 (Dkk-1), was defective in the presence of LRP5V171 and that this resulted in increased signaling due to unopposed Wnt activity.
Conclusions
The LRP5V171 mutation causes high bone density, with a thickened mandible and torus palatinus, by impairing the action of a normal antagonist of the Wnt pathway and thus increasing Wnt signaling. These findings demonstrate the role of altered LRP5 function in high bone mass and point to Dkk as a potential target for the prevention or treatment of osteoporosis.
Media in This Article
Figure 3
Mutation in LRP5.Figure 2
Pedigree of the Kindred Showing the Linkage of Bone Density to 11q12–13.Article Activity
- Article
Osteoporosis is a major public health problem, and its prevalence is increasing.1-3 In the United States, nearly 1 million fractures occur annually in people over the age of 65 years, the majority of which are due to osteoporosis.1,4 Osteoporotic fractures are associated with substantial morbidity, and the estimated rate of death in the first year after a hip fracture is 25 to 30 percent.5,6
Bone mass, a major determinant of the risk of osteoporotic fracture, increases during childhood and adolescence, reaching a peak at about the age of 20 years.7 Twin and family studies indicate that genetic factors account for approximately 75 percent of the variation in peak bone mass,7 although the genes that contribute to this variation are largely unknown.
In this setting, the investigation of rare mendelian disorders may identify pathways that affect the trait. One disorder characterized by increased bone density with largely normal bone is an autosomal dominant disease with variable clinical features, including entrapment neuropathies, increased levels of alkaline phosphatase, a square jaw, and torus palatinus.8-15 In 1997, Johnson et al. reported the linkage of a gene causing nonsyndromic high bone mass in a single family to a 30-cM region of 11q12–13 with a lod score of 5.74.16 Because few kindreds have been studied, the question of whether these varied clinical manifestations arise from mutations in the same gene or in different genes has not been answered.
Osteoporosis–pseudoglioma, an autosomal recessive disease characterized by low bone mass, with childhood fractures and abnormal eye development, has also been mapped to 11q12–13.17 The disorder has recently been shown to be due to an inherited loss of function of the gene for low-density lipoprotein receptor–related protein 5 (LRP5).18 This protein is involved in the Wnt signaling pathway, acting as a coreceptor for Wnt, a developmental protein, and as a target for the inhibitory effects of Dickkopf (Dkk), another developmental protein, on Wnt signaling.19-21 These findings suggest a link between Wnt signaling through LRP5 and bone density, and they raise the question of whether gain-of-function mutations in the LRP5 gene cause high bone mass. We performed genetic and biochemical analyses in a kindred with an autosomal dominant syndrome characterized by high bone density, a wide and deep mandible, and torus palatinus.
Methods
Subjects
Twenty members of a kindred of white ancestry from Connecticut participated in the study. The protocol was approved by the Human Investigation Committee at Yale University School of Medicine. All the subjects (or their guardians, in the case of minors) provided written informed consent. Assent was also obtained from minors. The subjects provided a medical history and a blood sample for DNA preparation. Bone density was measured in 16 of the 20 kindred members. The four members in whom bone density was not measured included two children (10 and 13 years old), one person who died before the study, and one person who declined to participate. We performed detailed serum and urinary biochemical measurements in four kindred members with very high bone density; these values were compared with the values in nine healthy control subjects.
Bone-Density Measurements
We measured bone mineral density in the lumbar spine, femoral neck, and total body, using dual-energy x-ray absorptiometry with a densitometer (QDR 4500W, Hologic, or DPXL, Lunar). The results are expressed as z scores (the number of standard deviations from the mean value for persons in the general population matched for age, sex, and race).
Biochemical Evaluation
Serum levels of parathyroid hormone and tartrate-resistant acid phosphatase and plasma levels of vitamin D metabolites were measured as previously reported.22,23 Serum calcium was measured with the use of flame atomic absorptiometry. Serum creatinine and phosphate levels and levels of the brain isoform of creatine kinase were measured with the use of an AutoAnalyzer (model 747-200, Hitachi) in the clinical-chemistry laboratory of Yale–New Haven Hospital in New Haven, Connecticut. Serum osteocalcin, bone-specific alkaline phosphatase, urinary N-telopeptide of type 1 collagen, the receptor for activation of nuclear factor-κB ligand, osteoprotegerin, transforming growth factor β1 (TGF-β1), and fibronectin were measured with the use of commercial kits. Mean (±SD) values in affected subjects and controls were compared with the use of unpaired two-tailed t-tests.
Genetic Studies
Polymorphic markers on 11q were genotyped with the use of a polymerase-chain-reaction (PCR) assay and specific fluorescent primers and genomic DNA from members of the kindred as the template. The products were fractionated by electrophoresis on an ABI 3700 DNA analyzer (Applied Biosystems), and genotypes were determined with the use of Genotyper software. We analyzed linkage with the use of the Linkage program, specifying high bone density as an autosomal dominant trait with a disease-allele frequency of 0.00001, complete penetrance, and a phenocopy prevalence of 0.00001. Unstudied obligate carriers were classified as “phenotype unknown.” Altering the specified model had minor effects on the lod score.
LRP5 mutations in members of the kindred were sought by PCR amplification of short segments spanning the coding region and intron–exon boundaries of LRP5; the products were analyzed by electrophoresis under nondenaturing conditions. Identified variants were subjected to DNA sequencing. The controls were 210 unrelated white persons not known to have abnormalities in bone density.
In Vitro Biochemical Studies
We used a well-characterized signaling system in the mouse fibroblast NIH3T3 cell line to examine the effect of mutant LRP5 on Wnt signaling.19 In each experiment, plasmids encoding LEF-1 (a transcription factor activated by Wnt signaling) constitutively expressed from a cytomegalovirus promoter, luciferase under control of an LEF-1–responsive promoter, and green fluorescent protein were introduced by transfection into cells seeded in 24-well plates. In addition, plasmids encoding wild-type (normal) LRP5 or LRP5V171, Wnt-1, and Dkk type 1 (Dkk-1) were transfected in indicated combinations. The total amount of DNA transfected in each experiment was kept constant (0.5 μg per well) by the addition of varying amounts of a plasmid encoding β-galactosidase (LacZ). One day after transfection, the cells were lysed, and the levels of luciferase activity and green fluorescent protein were measured; luciferase activity was normalized according to the green fluorescent protein level in order to account for variation in the efficiency of transfection. Each experiment was conducted in triplicate. Values are reported as means ±SD.
Results
Identification of the Kindred
The kindred was identified when two persons found on clinical screening to have extremely high bone density (Subjects 3 and 6) were incidentally noted to be related to one another. In addition to high bone density, both had a strikingly wide and deep mandible (Figure 1AFigure 1
Clinical and Radiographic Features of Affected Members of the Kindred. and Figure 1B) and torus palatinus (Figure 1C). Radiographic studies showed normal skeletal morphology except for dramatically thickened mandibular ramii (Figure 1D), marked cortical thickening in long bones (Figure 1E), and dense vertebrae (Figure 1F). There was no radiographic evidence of osteopetrosis, and the shape of the vertebral bodies was normal. There were no cranial-nerve palsies. Both persons were asymptomatic but noted difficulty staying afloat while swimming. They reported that other family members had the same facial features, prompting an investigation of the kindred.Bone Density
A total of seven members of the kindred had strikingly elevated age- and sex-adjusted bone mineral density in the lumbar spine, femoral neck, and total body, whereas nine had normal bone density at all sites (Table 1Table 1
Clinical Phenotypes in the Kindred.). Phenotypic classification of bone density as either very high (indicating affected subjects) or normal (indicating unaffected subjects) was unambiguous. In affected subjects, age- and sex-adjusted bone density of the lumbar spine was at least 5 SD above the population mean, and the mean z scores for bone density in the lumbar spine, femoral neck, and total body were 6.83, 4.42, and 4.78, respectively. In contrast, none of the unaffected subjects had a z score at any site that was greater than 2.71, and the mean z scores for bone density in the lumbar spine, femoral neck, and total body were 0.40, –0.61, and –0.08, respectively. All affected subjects had torus palatinus and the striking square jaw; none of the unaffected subjects had either of these features. None of the affected subjects had a history of bone fracture.The pattern of elevated bone density with torus palatinus and a square jaw was characteristic of autosomal dominant transmission with high penetrance (Figure 2Figure 2
Pedigree of the Kindred Showing the Linkage of Bone Density to 11q12–13.). The trait was present in successive generations, affected or obligate-carrier parents had approximately equal numbers of affected and unaffected offspring overall, and there was male-to-male transmission. There were four deceased obligate gene carriers, one of whom (Subject 16) was examined before death and found to have torus palatinus and the characteristic mandible. Three living family members (Subjects 17, 18, and 19) did not undergo bone-density measurements, but they did not have torus palatinus or the characteristic facies.Biochemical Findings
The mean serum calcium and phosphate levels were normal in the affected subjects; the urinary calcium level was at the high end of the normal range (Table 2Table 2
Indexes of Mineral Metabolism and Markers of Bone Turnover in Four Affected Subjects and Nine Controls.). Serum levels of parathyroid hormone and vitamin D metabolites were also normal. In addition, the mean serum level of tartrate-resistant acid phosphatase was normal (1.2±2 U per liter), and serum levels of the brain isoform of creatine kinase were undetectable; these two biochemical markers may be elevated in patients with osteopetrosis.24,25 The mean level of urinary N-telopeptide of type 1 collagen, a marker of bone resorption, was normal in the affected subjects (Table 2). Circulating levels of the receptor for activation of nuclear factor-κB ligand and osteoprotegerin, cytokines that regulate rates of bone resorption,26 were also normal. As noted above, the level of tartrate-resistant acid phosphatase, a marker of osteoclast activity, was normal. In contrast, the mean level of serum osteocalcin, a marker of bone formation, was markedly elevated — more than three times the value in the controls. The values for bone-specific alkaline phosphatase were not elevated in the affected subjects (mean value, 25±6 U per liter; normal range, 15 to 41). The levels of TGF-β1 were markedly elevated. These findings suggested that increased bone formation with unaltered bone resorption was the mechanism of high bone density in affected members of this family.
Point Mutation in LRP5
Because of prior reports of linkage of both high-bone-density and low-bone-density phenotypes to 11q12–13,16,17,27,28 we performed genotyping for 37 polymorphic genetic markers across a 40-cM segment of this interval (Figure 2). Analysis of the relation between inheritance of this chromosome segment and high bone density provided strong evidence of linkage, with a multipoint lod score of 5.30. When the three subjects in whom bone density was not measured but who did not have torus palatinus or a square jaw were included in the analysis as unaffected subjects, the lod score was 6.21 (odds of linkage to 11q12–13, >1 million to 1). Meiotic recombination events in affected subjects localized the disease gene to the 16-cM interval flanked by loci D11S4191 and D11S4207. This linked interval contains LRP5, the gene for osteoporosis–pseudoglioma.18
The protein encoded by LRP5 spans the plasma membrane once and contains a large extracellular segment with four domains that are each predicted to form a structure resembling a propeller with six blades (Figure 3AFigure 3
Mutation in LRP5.). The amino acid sequence YWTD or a variant of this sequence is found as a conserved element (a YWTD repeat) in each propeller blade.29,30 We examined the coding sequence of LRP5 for DNA-sequence variants and identified one variant in all the affected subjects (Figure 3B). This variant introduced a single base substitution that resulted in a missense mutation, with valine substituted for glycine at residue 171 (LRP5V171) (Figure 3C). The residue lies in the fourth blade of the first propeller, two amino acids beyond the aspartate residue of the YWTD sequence (Figure 3A and Figure 3D).
The heterozygous LRP5V171 mutation precisely cosegregated with high bone density in the kindred (Figure 3B); LRP5V171 is not a simple polymorphism, since it was absent in 420 control chromosomes from unrelated, unaffected subjects. The normal glycine residue shows extraordinary evolutionary conservation (Figure 3D). Glycine is found at the same position in the fourth blade of the first three propellers of LRP5 and LRP6 in humans and mice, as well as in the single propeller of the low-density lipoprotein (LDL) receptor in humans, mice, rats, pigs, hamsters, and rabbits. Moreover, glycine is also found at this position in the first propeller of the Drosophila melanogaster LDL-receptor–related protein homologue, arrow. In addition, glycine is present at this position in a wide range of other YWTD propellers, including those in other LDL-receptor–related proteins, as well as those in the epidermal growth factor precursor, the very-low-density lipoprotein receptor, and the vitellogenin receptor in fruit flies and mosquitos (protein sequences are available at http://www.ncbi.nlm.nih.gov/entrez). The evolutionary conservation of this glycine residue is strong evidence of the functional importance of its mutation in our kindred.
Molecular Studies
If this mutation indeed causes gain of LRP5 function and increased Wnt signaling, downstream target genes in the Wnt signaling pathway should show increased expression in vivo. A direct transcriptional target of Wnt signaling is the extracellular matrix protein fibronectin.31 Fibronectin levels were markedly elevated in the affected members of our kindred, with a mean level that was more than 3 SD above the mean level in controls (Table 2).
Possible mechanisms of increased Wnt signaling include constitutive signaling in the absence of a ligand, increased signaling in response to a ligand, or loss of action of a normal inhibitor of signaling. To identify the mechanism, we performed in vitro studies using the mouse fibroblast NIH3T3 cell line, in which the expression of normal LRP5 potentiates Wnt signaling.19 We found that the expression of LRP5V171 did not activate signaling in the absence of Wnt-1, a finding that ruled out constitutive signaling as the mechanism (Figure 4AFigure 4
Level of Wnt Signaling with Normal and Mutant LRP5.). Activation of the signaling pathway in response to Wnt-1 was the same with normal and mutant LRP5; this finding ruled out increased activation by a ligand as the mechanism (Figure 4A). Finally, we tested the action of the endogenous antagonist of Wnt signaling, Dkk-1. Although Dkk-1 inhibited Wnt signaling in conjunction with wild-type LRP5, Dkk-1 inhibition of Wnt signaling was virtually abolished in cells expressing LRP5V171 (Figure 4B). These findings indicated that LRP5V171 results in increased Wnt signaling because of loss of Dkk antagonism.Discussion
Recent work has established that loss of function of LRP5 leads to reduced bone mass.18 Our study shows that a gain-of-function mutation in LRP5 causes an autosomal dominant disorder characterized by high bone density, torus palatinus, and a wide, deep mandible.
Our in vitro and in vivo studies show that the LRP5V171 mutation increases Wnt signaling. The mutation impairs antagonism of Wnt signaling by Dkk-1 in vitro, and the levels of fibronectin, a downstream target of Wnt signaling, are increased in vivo in patients with this mutation. These findings indicate that unopposed Wnt signaling due to loss of action of a normal antagonist is the molecular mechanism that accounts for the effect of the mutation.
Nonsyndromic high bone mass has been linked to 11q12–13 in another kindred.16 While we were preparing this report, Little et al. identified an LRP5 mutation in the other kindred.32 Remarkably, this mutation is identical to the LRP5V171 mutation in our kindred. To our knowledge, these families do not share a common ancestor, suggesting that the mutations have arisen independently; however, the possibility of a very remote common ancestor cannot be excluded. It is striking that the same mutation is associated with nonsyndromic high bone mass in one family and syndromic high bone mass in the other. These findings suggest that alleles of other genes or environmental factors influence phenotypic manifestations of the mutation and that other phenotypes in kindreds with autosomal dominant high bone mass may also arise from the same mutation. If this is correct, all these disorders could be diagnosed with the use of a simple genetic test. The findings also suggest that the target for gain-of-function mutations in LRP5 is very small, possibly indicating a site critical for Dkk binding or action.
Our findings provide evidence that the Wnt signaling pathway alters bone mass through a primary effect on bone formation. Biochemical markers of bone resorption were unaltered in affected members of our kindred, whereas levels of specific markers of osteoblast activity were strikingly elevated. These findings indicate an uncoupling of bone turnover in favor of increased bone formation. The observation that LRP5 is expressed at high levels in osteoblasts is consistent with its having a role in this axis.33 The elevated fibronectin levels are also consistent with an effect on bone formation, since fibronectin is an early scaffolding protein in osteoid formation and enhances the survival and differentiation of osteoblasts.34-37 Finally, the observed elevation in TGF-β1 levels is noteworthy. TGF-β1 has stimulatory effects on osteoblasts, and targeted disruption in mice results in reduced bone mass.38-40
Given the established role of rare LRP5 mutations in abnormal bone density, it is of particular interest that variation in bone density in the general population may be linked to the chromosome segment containing LRP5.28 This finding raises the possibility that common variants that alter the expression or function of LRP5 will be found to have a role in the risk of osteoporosis in the general population. Further studies will be required to investigate this possibility. Finally, the observation that the impaired action of Dkk at LRP5 increases bone density suggests that pharmacologic antagonism of Dkk action, either at the prereceptor level or through the inhibition of binding or action at LRP5, may have a role in the prevention or treatment of osteoporosis.
Supported by grants from the National Institutes of Health (AG15345, to Dr. Insogna, and CA85420, to Dr. Wu), the Danbury Hospital Medical Education Center, the Yale Core Center for Musculoskeletal Disorders (AR46032, to Dr. Insogna), the Yale Bone Center, and the Yale General Clinical Research Center (National Center for Research Resources grant RR00125). Dr. Lifton is an Investigator of the Howard Hughes Medical Institute.
We are indebted to the members of the kindred who participated in the study for making this work possible, and to Carol Nelson-Williams, Ana Quinones, Diane Wall, and the staff of the Yale General Clinical Research Center, for technical assistance and helpful discussions.
Source Information
From the Departments of Genetics (L.M.B., A.F., R.P.L.) and Medicine (J.B., L.M., M.A.M., K.I., R.P.L.), Yale University School of Medicine, New Haven; and the Department of Genetics and Developmental Biology (J.M., D.W.), University of Connecticut Health Center, Farmington — both in Connecticut.
Address reprint requests to Dr. Lifton at the Yale University School of Medicine, Boyer Center for Molecular Medicine, 295 Congress Ave., New Haven, CT 06510, or at richard.lifton@yale.edu.
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