Osteoclastic differentiation of mouse and human monocytes in a plasma clot/biphasic calcium phosphate microparticles composite

European Cells and Materials

Volumn 20, Issue , 2010, Pages 379-392

  Mouline, Caroline C ^a   Quincey, Danielle ^a   Laugier, Jean Pierre ^b   Carle, Georges F ^a   Bouler, Jean Michel ^c   Rochet, Nathalie ^a   Scimeca, Jean Claude ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b Universite Co te d'Azur Parc Valrose   (France)

^c UNIVERSITÉ DE NANTES   (France)

Author keywords

Biphasic calcium phosphate microparticles; Monocyte; Osteoclastic differentiation; Sdf1 CXCL12; Three dimensional cell culture; VegfC

Indexed keywords

BETA-TRICALCIUM PHOSPHATE; CALCIUM PHOSPHATE; HYDROXYAPATITE; TISSUE SCAFFOLD;

ANIMAL; ARTICLE; BLOOD; BLOOD CLOTTING; BONE DEVELOPMENT; BONE REMODELING; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; GENE EXPRESSION PROFILING; HUMAN; MONOCYTE; MOUSE; OSTEOCLAST; PARTICLE SIZE;

ANIMALS; BLOOD; BLOOD COAGULATION; BONE REMODELING; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELL LINE; DURAPATITE; GENE EXPRESSION PROFILING; HUMANS; MICE; MICE, INBRED C57BL; MONOCYTES; OSTEOCLASTS; OSTEOGENESIS; PARTICLE SIZE; TISSUE SCAFFOLDS;

EID: 79953040759     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v020a31     Document Type: Article

References (70)

1. Alam I., Asahina I, Ohmamiuda K, Enomoto S (2001) Comparative study of biphasic calcium phosphate ceramics impregnated with rhBMP-2 as bone substitutes. J Biomed Mater Res 54: 129-138.
2. Arrington E. D, Smith WJ, Chambers HG, Bucknell AL, Davino N. A (1996) Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res (329): 300-309.
3. Aulakh T. S, Jayasekera N, Kuiper JH, Richardson JB (2009) Long-term clinical outcomes following the use of synthetic hydroxyapatite and bone graft in impaction in revision hip arthroplasty. Biomaterials 30: 1732-1738.
4. Balaguer T., Boukhechba F, Clavé A, Bouvet-Gerbettaz S, Trojani C, Michiels JF, Laugier JP, Bouler JM, Carle GF, Scimeca JC, Rochet N (2010) Biphasic calcium phosphate micro-particles for bone formation: benefits of combination with blood clot. Tissue Eng Part A 16: 3495-3505.
5. Beranger G. E, Momier D, Guigonis JM, Samson M, Carle G. F, Scimeca JC (2007) Differential binding of poly(ADP-Ribose) polymerase-1 and JunD/Fra2 accounts for RANKL-induced Tcirg1 gene expression during osteoclastogenesis. J Bone Miner Res 22: 975-983.
6. Birgersdotter A., Sandberg R, Ernberg I (2005) Gene expression perturbation in vitro-a growing case for threedimensional (3D) culture systems. Semin Cancer Biol 15: 405-412.
7. Brouard N., Driessen R, Short B, Simmons PJ (2010) G-CSF increases mesenchymal precursor cell numbers in the bone marrow via an indirect mechanism involving osteoclast-mediated bone resorption. Stem Cell Res 5: 65-75.
8. Cackowski F. C, Roodman GD (2007) Perspective on the osteoclast: an angiogenic cell? AnnNY Acad Sci 1117: 12-25.
9. Cao Y., Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, Alitalo K (1998) Vascular endothelial growth factor C induces angiogenesis in vitro. Proc Natl Acad Sci U S A 95: 14389-14394.
10. Cavagna R., Daculsi G, Bouler JM (1999) Macroporous calcium phosphate ceramic: a prospective study of 106 cases in lumbar spinal fusion. J Long Term Eff Med Implants, 9: 403-412.
11. Chung E. S, Chauhan SK, Jin Y, Nakao S, Hafezi-Moghadam A., van Rooijen N, Zhang Q, Chen L, Dana R (2009) Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands. Am J Pathol 175: 1984-1992.
12. Claase M. B, de Bruijn JD, Grijpma DW, Feijen J (2007) Ectopic bone formation in cell-seeded poly(ethylene oxide)/poly(butylene terephthalate) copolymer scaffolds of varying porosity. J Mater Sci Mater Med 18: 1299-1307.
13. Clarke S. A, Hoskins NL, Jordan GR, Marsh DR (2007) Healing of an ulnar defect using a proprietary TCP bone graft substitute, JAX, in association with autologous osteogenic cells and growth factors. Bone 40: 939-947.
14. Cordaro L., Bosshardt DD, Palattella P, Rao W, Serino G, Chiapasco M (2008) Maxillary sinus grafting with Bio-Oss or Straumann Bone Ceramic: histomorphometric results from a randomized controlled multicenter clinical trial. Clin Oral Implants Res 19: 796-803.
15. Cordonnier T., Layrolle P, Gaillard J, Langonne A, Sensebe L., Rosset P, Sohier J (2010) 3D environment on human mesenchymal stem cells differentiation for bone tissue engineering. J Mater Sci Mater Med 21: 981-987.
16. De Long WG, Jr., Einhorn TA, Koval K, McKee M, Smith W., Sanders R, Watson T (2007) Bone grafts and bone graft substitutes in orthopaedic trauma surgery. A critical analysis. J Bone Joint Surg Am 89: 649-658.
17. Delaisse J. M, Engsig MT, Everts V, del Carmen Ovejero M, Ferreras M, Lund L, Vu TH, Werb Z, Winding B, Lochter A., Karsdal MA, Troen T, Kirkegaard T, Lenhard T, Heegaard AM, Neff L, Baron R, Foged NT (2000) Proteinases in bone resorption: obvious and less obvious roles. Clin Chim Acta 291: 223-234.
18. Deschaseaux F., Sensebe L, Heymann D (2009) Mechanisms of bone repair and regeneration. Trends Mol Med 15: 417-429.
19. Dupraz A., Delecrin J, Moreau A, Pilet P, Passuti N (1998) Long-term bone response to particulate injectable ceramic. J Biomed Mater Res 42: 368-375.
20. Engsig M. T, Chen QJ, Vu TH, Pedersen AC, Therkidsen B, Lund LR, Henriksen K, Lenhard T, Foged NT, Werb Z, Delaisse J. M (2000) Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol 151: 879-889.
21. Fellah B. H, Josselin N, Chappard D, Weiss P, Layrolle P (2007) Inflammatory reaction in rats muscle after implantation of biphasic calcium phosphate micro particles. J Mater Sci Mater Med 18: 287-294.
22. Fellah B. H, Weiss P, Gauthier O, Rouillon T, Pilet P, Daculsi G., Layrolle P (2006) Bone repair using a new injectable self-crosslinkable bone substitute. J Orthop Res 24: 628-635.
23. Frenken J. W, Bouwman WF, Bravenboer N, Zijderveld SA, Schulten EA, ten Bruggenkate CM (2010) The use of Straumann Bone Ceramic in a maxillary sinus floor elevation procedure: a clinical, radiological, histological and histomorphometric evaluation with a 6-month healing period. Clin Oral Implants Res 21: 201-208.
24. Friedmann A., Dard M, Kleber BM, Bernimoulin JP, Bosshardt D. D (2009) Ridge augmentation and maxillary sinus grafting with a biphasic calcium phosphate: histologic and histomorphometric observations. Clin Oral Implants Res 20: 708-714.
25. Froum S. J, Wallace SS, Cho SC, Elian N, Tarnow DP (2008) Histomorphometric comparison of a biphasic bone ceramic to anorganic bovine bone for sinus augmentation: 6-to 8-month postsurgical assessment of vital bone formation. A pilot study. Int J Periodontics Restorative Dent 28: 273-281.
26. Gauthier O., Boix D, Grimandi G, Aguado E, Bouler JM, Weiss P, Daculsi G (1999a) A new injectable calcium phosphate biomaterial for immediate bone filling of extraction sockets: a preliminary study in dogs. J Periodontol 70: 375-383.
27. Gauthier O., Bouler JM, Weiss P, Bosco J, Daculsi G, Aguado E. (1999b) Kinetic study of bone ingrowth and ceramic resorption associated with the implantation of different injectable calcium-phosphate bone substitutes. J Biomed Mater Res 47: 28-35.
28. Gauthier O., Muller R, von Stechow D, Lamy B, Weiss P, Bouler JM, Aguado E, Daculsi G (2005) In vivo bone regeneration with injectable calcium phosphate biomaterial: a three-dimensional micro-computed tomographic, biomechanical and SEM study. Biomaterials 26: 5444-5453.
29. Geiger F., Bertram H, Berger I, Lorenz H, Wall O, Eckhardt C., Simank HG, Richter W (2005) Vascular endothelial growth factor gene-activated matrix (VEGF165-GAM) enhances osteogenesis and angiogenesis in large segmental bone defects. J Bone Miner Res 20: 2028-2035.
30. Georges S., Ruiz Velasco C, Trichet V, Fortun Y, Heymann D., Padrines M (2009) Proteases and bone remodelling. Cytokine Growth Factor Rev 20: 29-41.
31. Grassi F., Piacentini A, Cristino S, Toneguzzi S, Cavallo C, Facchini A, Lisignoli G (2003) Human osteoclasts express different CXC chemokines depending on cell culture substrate: molecular and immunocytochemical evidence of high levels of CXCL10 and CXCL12. Histochem Cell Biol 120: 391-400.
32. Henriksen K., Neutzsky-Wulff AV, Bonewald LF, Karsdal M. A (2009) Local communication on and within bone controls bone remodeling. Bone 44: 1026-1033.
33. Huang Y. C, Kaigler D, Rice KG, Krebsbach PH, Mooney D. J (2005) Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res 20: 848-857.
34. Ishibashi O., Niwa S, Kadoyama K, Inui T (2006) MMP-9 antisense oligodeoxynucleotide exerts an inhibitory effect on osteoclastic bone resorption by suppressing cell migration. Life Sci 79: 1657-1660.
35. Ito H., Koefoed M, Tiyapatanaputi P, Gromov K, Goater JJ, Carmouche J, Zhang X, Rubery PT, Rabinowitz J, Samulski R. J, Nakamura T, Soballe K, O'Keefe RJ, Boyce BF, Schwarz EM (2005) Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nature Medicine 11: 291-297.
36. Joukov V., Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15: 290-298.
37. Kaigler D., Wang Z, Horger K, Mooney DJ, Krebsbach PH (2006) VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res 21: 735-744.
38. Karp J. M, Leng Teo GS (2009) Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4: 206-216.
39. Karsdal M. A, Martin TJ, Bollerslev J, Christiansen C, Henriksen K. (2007) Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 22: 487-494.
40. Karsdal M. A, Neutzsky-Wulff AV, Dziegiel MH, Christiansen C., Henriksen K (2008) Osteoclasts secrete non-bone derived signals that induce bone formation. Biochem Biophys Res Commun 366: 483-488.
41. Kitaori T., Ito H, Schwarz EM, Tsutsumi R, Yoshitomi H, Oishi S, Nakano M, Fujii N, Nagasawa T, Nakamura T (2009) Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 60: 813-823.
42. Lelongt B., Bengatta S, Delauche M, Lund LR, Werb Z, Ronco PM (2001) Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity. Journal Exp Med 193: 793-802.
43. Lerouxel E., Weiss P, Giumelli B, Moreau A, Pilet P, Guicheux J., Corre P, Bouler JM, Daculsi G, Malard O (2006) Injectable calcium phosphate scaffold and bone marrow graft for bone reconstruction in irradiated areas: an experimental study in rats. Biomaterials 27: 4566-4572.
44. Lindgren C., Hallman M, Sennerby L, Sammons R (2010) Back-scattered electron imaging and elemental analysis of retrieved bone tissue following sinus augmentation with deproteinized bovine bone or biphasic calcium phosphate. Clin Oral Implants Res, in press.
45. Lindgren C., Sennerby L, Mordenfeld A, Hallman M (2009) Clinical histology of microimplants placed in two different biomaterials. Int J Oral Maxillofac Implants 24: 1093-1100.
46. Linton J. L, Sohn BW, Yook JI, Le Geros RZ (2002) Effects of calcium phosphate ceramic bone graft materials on permanent teeth eruption in beagles. Cleft Palate Craniofac J 39: 197-207. Littlewood-Evans A, Kokubo T, Ishibashi O, Inaoka
47. Littlewood-Evans A, Kokubo T, Ishibashi O, Inaoka T, Wlodarski B, Gallagher JA, Bilbe G (1997) Localization of cathepsin K in human osteoclasts by in situ hybridization and immunohistochemistry. Bone 20: 81-86.
48. Lu J., Blary MC, Vavasseur S, Descamps M, Anselme K, Hardouin P (2004) Relationship between bioceramics sintering and micro-particles-induced cellular damages. J Mater Sci Mater Med 15: 361-365.
49. Malard O., Bouler JM, Guicheux J, Heymann D, Pilet P, Coquard C, Daculsi G (1999) Influence of biphasic calcium phosphate granulometry on bone ingrowth, ceramic resorption, and inflammatory reactions: preliminary in vitro and in vivo study. J Biomed Mater Res, 46:103-111.
50. Ortega N., Wang K, Ferrara N, Werb Z, Vu TH (2010) Complementary interplay between matrix metalloproteinase-9, vascular endothelial growth factor and osteoclast function drives endochondral bone formation. Dis Model Mech 3: 224-235.
51. Otrock Z. K, Makarem JA, Shamseddine AI (2007) Vascular endothelial growth factor family of ligands and receptors: review. Blood Cells Mol Dis 38: 258-268.
52. Park S. H, Gil ES, Kim HJ, Lee K, Kaplan DL (2010) Relationships between degradability of silk scaffolds and osteogenesis. Biomaterials 31: 6162-6172.
53. Peng H., Usas A, Olshanski A, Ho AM, Gearhart B, Cooper G. M, Huard J (2005) VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res 20:2017-2027.
54. Peng H., Wright V, Usas A, Gearhart B, Shen HC, Cummins J., Huard J (2002) Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 110: 751-759.
55. Piattelli A., Scarano A, Mangano C (1996) Clinical and histologic aspects of biphasic calcium phosphate ceramic (BCP) used in connection with implant placement. Biomaterials 17: 1767-1770.
56. Ransford A. O, Morley T, Edgar MA, Webb P, Passuti N, Chopin D, Morin C, Michel F, Garin C, Pries D (1998) Synthetic porous ceramic compared with autograft in scoliosis surgery. A prospective, randomized study of 341 patients. J Bone Joint Surg Br 80: 13-18.
57. Saldana L., Sanchez-Salcedo S, Izquierdo-Barba I, Bensiamar F., Munuera L, Vallet-Regi M, Vilaboa N (2009) Calcium phosphate-based particles influence osteogenic maturation of human mesenchymal stem cells. Acta Biomater 5: 1294-1305.
58. Sculean A., Windisch P, Szendroi-Kiss D, Horvath A, Rosta P., Becker J, Gera I, Schwarz F (2008) Clinical and histologic evaluation of an enamel matrix derivative combined with a biphasic calcium phosphate for the treatment of human intrabony periodontal defects. J Periodontol 79: 1991-1999.
59. Seeman E., Delmas PD (2006) Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med 354: 2250-2261.
60. Segovia-Silvestre T, Neutzsky-Wulff AV, Sorensen MG, Christiansen C., Bollerslev J, Karsdal MA, Henriksen K (2009) Advances in osteoclast biology resulting from the study of osteopetrotic mutations. Hum Genet 124: 561-577.
61. Sen M. K, Miclau T (2007) Autologous iliac crest bone graft: should it still be the gold standard for treating nonunions? Injury 38 Suppl 1: S75-80.
62. Shibuya M., Claesson-Welsh L (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 312: 549-560.
63. Silva S. N, Pereira MM, Goes AM, Leite MF (2003) Effect of biphasic calcium phosphate on human macrophage functions in vitro. J Biomed Mater Res A 65: 475-481.
64. Tombran-Tink J, Barnstable CJ (2004) Osteoblasts and osteoclasts express PEDF, VEGF-A isoforms, and VEGF receptors: possible mediators of angiogenesis and matrix remodeling in the bone. Biochem Biophys Res Commun 316: 573-579.
65. Weiss P., Layrolle P, Clergeau LP, Enckel B, Pilet P, Amouriq Y., Daculsi G, Giumelli B (2007) The safety and efficacy of an injectable bone substitute in dental sockets demonstrated in a human clinical trial. Biomaterials 28: 3295-3305.
66. Wernike E., Montjovent MO, Liu Y, Wismeijer D, Hunziker E. B, Siebenrock KA, Hofstetter W, Klenke FM (2010) VEGF incorporated into calcium phosphate ceramics promotes vascularisation and bone formation in vitro. Eur Cell Mater 19: 30-40.
67. Yamada S., Heymann D, Bouler JM, Daculsi G (1997) Osteoclastic resorption of biphasic calcium phosphate ceramic in vitro. J Biomed Mater Res 37: 346-352.
68. Yang Q., McHugh KP, Patntirapong S, Gu X, Wunderlich L., Hauschka PV (2008) VEGF enhancement of osteoclast survival and bone resorption involves VEGF receptor-2 signaling and beta3-integrin. Matrix Biol 27: 589-599.
69. Younger E. M, Chapman MW (1989) Morbidity at bone graft donor sites. J Orthop Trauma, 3:192-195.
70. Zhang Q., Guo R, Lu Y, Zhao L, Zhou Q, Schwarz EM, Huang J., Chen D, Jin ZG, Boyce BF, Xing L (2008) VEGFC, a lymphatic growth factor, is a RANKL target gene in osteoclasts that enhances osteoclastic bone resorption through an autocrine mechanism. The J Biol Chem 283: 13491-13499.