Congenital bone fractures in spinal muscular atrophy: functional role for SMN protein in bone remodeling - PubMed (original) (raw)
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Congenital bone fractures in spinal muscular atrophy: functional role for SMN protein in bone remodeling
Srinivasan Shanmugarajan et al. J Child Neurol. 2007 Aug.
Abstract
Spinal muscular atrophy is the second most common fatal childhood disorder. Core clinical features include muscle weakness caused by degenerating lower motor neurons and a high incidence of bone fractures and hypercalcemia. Fractures further compromise quality of life by progression of joint contractures or additional loss of motor function. Recent observations suggest that bone disease in spinal muscular atrophy may not be attributed entirely to lower motor neuron degeneration. The presence of the spinal muscular atrophy disease-determining survival motor neuron gene (SMN), SMN expression, and differential splicing in bone-resorbing osteoclasts was recently discovered. Its ubiquitous expression and the differential expression of splice variants suggest that SMN has specific roles in bone cell function. SMN protein also interacts with osteoclast stimulatory factor. Mouse models of human spinal muscular atrophy disease suggest a potential role of SMN protein in skeletal development. Dual energy x-ray absorptiometry analysis demonstrated a substantial decrease in total bone area and poorly developed caudal vertebra in the mouse model. These mice also had pelvic bone fractures. Studies delineating SMN signaling mechanisms and gene transcription in a cell-specific manner will provide important molecular insights into the pathogenesis of bone disease in children with spinal muscular atrophy. Moreover, understanding bone remodeling in spinal muscular atrophy may lead to novel therapeutic approaches to enhance skeletal health and quality of life. This article reviews the skeletal complications associated with spinal muscular atrophy and describes a functional role for SMN protein in osteoclast development and bone resorption activity.
Figures
Figure 1
The arrow indicates a bone fracture in a newborn with spinal muscular atrophy. The radiograph is courtesy of the University of Miami and the University of Maryland Brain and Tissue Bank for Developmental Disorders.
Figure 2
Skeletal phenotype in Smn−/−SMN2 mice. (A) Radiologic assessment of 4-week-old Smn−/−SMN2 (Jackson Laboratories, Bar Harbor, ME) mice shows short tails compared with wild-type mice. A high-resolution (3x) radiogram indicates pelvic bone fractures and poorly developed caudal vertebra in spinal muscular atrophy mice. (B) Dual energy x-ray absorptiometry analyses of total animal bone area and total spine for bone area, bone mineral content, and bone mineral density in spinal muscular atrophy mice. (C) Dual energy x-ray absorptiometry analysis of caudal vertebra region for bone area, bone mineral content, and bone mineral density (n = 3, P < .05).
Figure 2
Skeletal phenotype in Smn−/−SMN2 mice. (A) Radiologic assessment of 4-week-old Smn−/−SMN2 (Jackson Laboratories, Bar Harbor, ME) mice shows short tails compared with wild-type mice. A high-resolution (3x) radiogram indicates pelvic bone fractures and poorly developed caudal vertebra in spinal muscular atrophy mice. (B) Dual energy x-ray absorptiometry analyses of total animal bone area and total spine for bone area, bone mineral content, and bone mineral density in spinal muscular atrophy mice. (C) Dual energy x-ray absorptiometry analysis of caudal vertebra region for bone area, bone mineral content, and bone mineral density (n = 3, P < .05).
Figure 3
Osteoclast stimulatory factor and SMN protein interactions in osteoclasts. Osteoclast stimulatory factor contains a proline-rich sequence at the amino terminus, followed by an SH3 domain and ankyrin repeats. Osteoclast stimulatory factor interacts with c-Src through a proline-rich sequence. Osteoclast stimulatory factor SH3 domain binds to SMN at the exon 6 encoding region. Osteoclast stimulatory factor and SMN signaling release soluble factors that stimulate osteoclast formation and survival.
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References
- Hausmanowa-Petrusewicz I, Vrbová G. Spinal muscular atrophy: a delayed development hypothesis. Neuroreport. 2005;16(7):657–661. - PubMed
- Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80(1):155–165. - PubMed
- Le TT, Pham LT, Butchbach ME, et al. SMNΔ7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum Mol Genet. 2005;14(6):845–857. - PubMed
- Lorson CL, Strasswimmer J, Yao JM, et al. SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat Genet. 1998;19(1):63–66. - PubMed
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