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The Role of Osteoblast Cells in the Pathogenesis of Unicameral Bone Cysts

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The Role of Osteoblast Cells in the Pathogenesis of Unicameral Bone Cysts J Child Orthop (2012) 6:339–346 DOI 10.1007/s11832-012-0419-x BASIC SCIENCE The role of osteoblast cells in the pathogenesis of unicameral bone cysts Alexander Aarvold • James O. Smith • Edward R. Tayton • Caroline J. Edwards • Darren J. Fowler • Edward D. Gent • Richard O. C. Oreffo Received: 3 May 2012 / Accepted: 14 June 2012 / Published online: 7 July 2012 Ó EPOS 2012 Abstract which was highly significant (p \ 0.001). Osteoclasts were Purpose The pathogenesis of unicameral bone cysts demonstrated in abundance in the cyst lining. The cyst fluid (UBCs) remains largely unknown. Osteoclasts have been cytokine profile revealed levels of the pro-osteoclast implicated, but the role of osteoblastic cells has, to date, cytokines IL-6, MIP-1a and MCP-1 that were 199,319 not been explored. This study investigated the pathophys- and 359 greater than those in reference serum. iology of UBCs by examining the interactions between the Conclusions Cyst fluid promoted osteoblastic growth and cyst fluid and human bone marrow stromal cells (hBMSCs) differentiation. Despite appearing paradoxical that the cyst and the effect of the fluid on osteogenesis. fluid promoted osteogenesis, osteoblastic cells are required Methods Fluid was aspirated from two UBCs and ana- for osteoclastogenesis through RANKL signalling. Three lysed for protein, electrolyte and cytokine levels. Graded key cytokines in this pathway (IL-6, MIP-1a, MCP-1) were concentrations of the fluid were used as culture media for highly elevated in cyst fluid. These findings may hold the hBMSCs to determine the effects of the fluid on hBMSC key to the pathogenesis of UBCs, with implications for proliferation and osteogenic differentiation. The fibrocel- treatment methods. lular lining was analysed histologically and by electron microscopy. Keywords Unicameral bone cyst Á Osteoblast cell Á Results Alkaline phosphatase (ALP) staining of hBMSCs Osteoclast Á Cytokine Á RANK ligand that were cultured in cyst fluid demonstrated increased cell proliferation and osteogenic differentiation compared to basal media controls. Biochemical analysis of these Introduction hBMSCs compared to basal controls confirmed a marked increase in DNA content (as a marker of proliferation) and Unicameral bone cysts (UBCs) are benign bone defects that ALP activity (as a marker of osteogenic differentiation) are defined as minimally expansile lucent lesions consisting of a cavity filled with fluid and lined with a fibrocellular membrane [1]. The pathogenesis of UBCs remains largely & A. Aarvold ( ) Á J. O. Smith Á E. R. Tayton Á R. O. C. Oreffo unknown, but theories presented in the literature include Bone and Joint Research Group, Centre for Human Development, Stem Cells and Regeneration, Institute pressure effects due to blocked fluid drainage [2], local of Developmental Sciences, University of Southampton School venous obstruction [3, 4], increased lysosomal enzyme of Medicine, Tremona Road, Southampton SO16 6YD, UK activity [5], prostaglandins [6], nitric oxide [3], oxygen free e-mail: [email protected] radicals [7], disorders of synovial origin [8] and genetic A. Aarvold Á C. J. Edwards Á E. D. Gent causes [9]. As these hypotheses concerning the pathogen- Department of Paediatric Orthopaedics, University Hospital esis of UBCs have evolved, multiple diverse treatment Southampton, Tremona Road, Southampton SO16 6YD, UK strategies have emerged. However, theories have often been based on the analysis of single reports or small case series, D. J. Fowler Department of Paediatric Pathology, University Hospital so a unified hypothesis (and hence targeted treatment) Southampton, Tremona Road, Southampton SO16 6YD, UK remains elusive. Therapeutic aspiration, curettage [10], 123 340 J Child Orthop (2012) 6:339–346 autologous bone marrow injection [11, 12], steroid injec- Materials and methods tions [6, 13, 14], demineralised bone matrix [15], grafting of synthetic materials [16, 17] and intramedullary fixation [18, Cyst fluid from UBCs of two patients was analysed for this 19] are routinely employed to treat UBCs, though all have a study. The use of human tissue was prospectively approved high failure and/or recurrence rate. by the local regional ethics committee (LREC194/99/1) Much of the literature defining the pathogenesis of and informed parental consent was obtained. UBCs has suggested a role for osteoclasts. Shindell et al. [6] have reported increased levels of PGE2 within UBC Case 1 fluid. PGE2 is a protein kinase A (PKA)-mediated signal- ling molecule involved in the stimulation and proliferation A nine-year-old healthy male had a one-year history of of osteoclasts. A reduction in levels following intralesional progressive pain in his right thigh, and radiographic inves- steroid injection has been associated with cyst resolution tigation revealed a lesion of the proximal femur character- [6]. Similarly, osteoclasts require lysosomal enzymes for istic of a UBC (Fig. 1a, b). Due to the risk of impending bone resorption, and increased levels of these, together fracture, the patient was listed for surgical stabilisation. with collagen degradation products, have been demon- Under general anaesthetic and fluoroscopic guidance, 20 ml strated in UBCs, indicating ongoing osteoclast-mediated of straw-coloured fluid was aspirated percutaneously from bone destruction [5]. Increased osteoclast activity within the cyst in the proximal femur (Fig. 1c), prior to stabilisation UBCs has also been established by detecting elevated acid with a flexible intramedullary nail (Fig. 1d). phosphatase levels [20] and increased osteoclast-related bone resorptive factors within the cyst fluid and lining [3]. Case 2 Furthermore, the presence of osteoclasts has also been confirmed in the fibrocellular lining of UBCs by histology A six-year-old boy suffered a pathological fracture through [3] and electron microscopy [21]. a previously asymptomatic unicameral bone cyst of his Complex signalling pathways exist between osteoclasts right proximal humerus. The fractured cortices progressed and cells of the osteoblast lineage [human bone marrow to bony union, but the cyst remained, and required surgical stromal cells (hBMSCs), osteoblasts, osteocytes and bone stabilisation (Fig. 1e, f). Intraoperatively, 4 ml of straw- lining cells] [22], abnormalities of which contribute to a coloured fluid was aspirated percutaneously (Fig. 1g), and wide range of bone pathologies, including osteoporosis, a window of bone and UBC membrane was excised from osteopetrosis, Paget’s disease, rheumatoid arthritis and the medial wall. The proximal humerus was stabilised with periodontal disease [23, 24]. Differentiation, fusion and a flexible intramedullary nail (Fig. 1h). activation of osteoclasts from macrophage-monocyte pre- cursors are stimulated by factors derived from cells of the Cyst fluid separation osteoblast lineage, notably RANK ligand (RANKL), so-called because it binds to a receptor on osteoclast pre- The aspirated samples were centrifuged at 1,100 rpm for cursors, receptor activator of NFjB (RANK) [25]. Cells 4 min at 21 °C to separate the supernatant, which was expressing the osteoblast markers Stro-1 and RUNX-2 removed, providing a pure fluid fraction which was used have been identified in the UBC fibrocellular lining, and for further analysis. these have been shown to induce osteoclastogenesis in vitro [21]. Beyond this single manuscript, the role of cells Harvesting of human cells of the osteoblast lineage of the osteoblast lineage in the pathogenesis of UBCs has not been explored. Furthermore, whilst many of the Bone marrow is a reliable source of human bone marrow abnormalities that have been identified in UBCs have been stromal cells (hBMSCs), which have the potential for self- discovered by analysing the cyst fluid [3, 5–7, 20], the renewal and osteogenic differentiation [25]. Human bone effect that the fluid itself contributes to UBC pathology marrow was obtained for this study from haematologically has, to date, not been investigated. normal adults undergoing routine total hip replacement surgery with the approval of the local ethics committee (LREC194/99/1). Adult hBMSCs were harvested by Aims repeatedly washing the marrow in 0.9 % saline, centrifu- gation, passage through a 70 lm filter and culture expan- The purpose of this study was to explore the underlying sion in basal media at 37 °C in 4 % humidified CO2.At pathophysiology of unicameral bone cysts (UBCs) by 30 % confluence, the adult hBMSCs were released using investigating the relationship between cells of the osteo- trypsin in EDTA (ethylene diamine tetraacetic acid), cen- blast lineage and the cyst fluid. trifuged, re-suspended in basal media and a cell count was 123 J Child Orthop (2012) 6:339–346 341 Fig. 1 Radiographs of UBCs from cases 1 and 2: preoperative AP aspiration and cystogram, followed by stabilisation with flexible and lateral radiographs of case 1 (a, b proximal femur) and case 2 (e, nailing, of case 1 (c, d) and case 2 (g, h) f proximal humerus). Intraoperative fluoroscopy of percutaneous performed using a haemocytometer. The hBMSC solution Zeiss Axiovision software v.3.0 via an AxioCam HR dig- was titrated to a concentration of 5 9 103 hBMSCs per ital camera on an Axiovert 200 inverted microscope (Carl 100 ll of basal media prior to seeding onto culture plates Zeiss Ltd, Welwyn Garden City, UK). (n = 18). Biochemical analysis hBMSC culture in cyst fluid Culture wells were assessed by biochemical analysis for Graded concentrations of cyst fluid were prepared by DNA content (as a measure of total cell
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