Enhanced osteoporotic bone regeneration by strontium-substituted calcium silicate bioactive ceramics

Biomaterials

Volumn 34, Issue 38, 2013, Pages 10028-10042

  Lin, Kaili ^a   Xia, Lunguo ^b   Li, Haiyan ^c   Jiang, Xinquan ^b   Pan, Haobo ^d   Xu, Yuanjin ^b   Lu, William W ^d   Zhang, Zhiyuan ^b   Chang, Jiang ^a  

^a SHANGHAI INSTITUTE OF CERAMICS   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Angiogenesis; Bioceramics; ERK p38 signaling pathways; Osteoclastogenesis; Osteogenesis; Strontium substituted calcium silicate

Indexed keywords

BIOCERAMICS; CALCIUM SILICATE; CELL CULTURE; CELL ENGINEERING; DEFECTS; ENDOTHELIAL CELLS; GENE EXPRESSION; PHOSPHATASES; SILICATES; SILICON; STEM CELLS; STRONTIUM COMPOUNDS;

ANGIOGENESIS; BONE MARROW MESENCHYMAL STEM CELLS; EXTRACELLULAR SIGNAL RELATED KINASE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; OSTEOCLASTOGENESIS; OSTEOGENESIS; SIGNALING PATHWAYS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

BONE;

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALKALINE PHOSPHATASE; BIOCERAMICS; CALCIUM SILICATE; MITOGEN ACTIVATED PROTEIN KINASE 14; OSTEOCLAST DIFFERENTIATION FACTOR; SILICATE; SILICON; STRONTIUM; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE REGENERATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; POROSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

RATTUS;

ANGIOGENESIS; BIOCERAMICS; ERK/P38 SIGNALING PATHWAYS; OSTEOCLASTOGENESIS; OSTEOGENESIS; STRONTIUM-SUBSTITUTED CALCIUM SILICATE;

ANIMALS; BLOTTING, WESTERN; BONE REGENERATION; CALCIUM COMPOUNDS; CELL LINE; CERAMICS; ENDOTHELIAL GROWTH FACTORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FLAVONOIDS; HUMANS; IMIDAZOLES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RATS; RATS, INBRED F344; REAL-TIME POLYMERASE CHAIN REACTION; SILICATES; STRONTIUM;

EID: 84885384287     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.09.056     Document Type: Article

References (54)

1. Liu H.Y., Wu A.T.H., Tsai C.Y., Chou K.R., Zeng R., Wang M.F., et al. The balance between adipogenesis and osteogenesis in bone regeneration by platelet-rich plasma for age-related osteoporosis. Biomaterials 2011, 32:6773-6780.
2. Rachner T.D., Khosla S., Hofbauer L.C. Osteoporosis: now and the future. Lancet 2011, 377:1276-1287.
3. Verron E., Gauthier O., Janvier P., Pilet P., Lesoeur J., Bujoli B., et al. Invivo bone augmentation in an osteoporotic environment using bisphosphonate-loaded calcium deficient apatite. Biomaterials 2010, 31:7776-7784.
4. Cao L., Liu G., Gan Y., Fan Q., Yang F., Zhang X., et al. The use of autologous enriched bone marrow MSCs to enhance osteoporotic bone defect repair in long-term estrogen deficient goats. Biomaterials 2012, 33:5076-5084.
5. Reichert J.C., Saifzadeh S., Wullschleger M.E., Epari D.R., Schütz M.A., Duda G.N., et al. The challenge of establishing preclinical models for segmental bone defect research. Biomaterials 2009, 30:2149-2163.
6. Jiang X.Q., Sun X.J., Lai H.C., Zhao J., Wang S.Y., Zhang Z.Y. Maxillary sinus floor elevation using a tissue-engineered bone complex with beta-TCP and BMP-2 gene-modified bMSCs in rabbits. Clin Oral Implant. Res 2009, 20:1333-1340.
7. Wang Z., Das J.G., De S., Ge Z., Ouyang H., Chong J.S., et al. Efficacy of bone marrow-derived stem cells in strengthening osteoporotic bone in a rabbit model. Tissue Eng 2006, 12:1753-1761.
8. Cho S.W., Sun H.J., Yang J.Y., Jung J.Y., Choi H.J., An J.H., et al. Human adipose tissue-derived stromal cell therapy prevents bone loss in ovariectomized nude mouse. Tissue Eng 2012, 18A:1067-1078.
9. Guan M., Yao W., Liu R., Lam K.S., Nolta J., Jia J., et al. Directing mesenchymal stem cells to bone to augment bone formation and increase bone mass. Nat Med 2012, 8:456-462.
10. Zhao L.Z., Wang H.R., Huo K.F., Zhang X.M., Wang W., Zhang Y.M., et al. The osteogenic activity of strontium loaded titania nanotube arrays on titanium substrates. Biomaterials 2013, 34:19-29.
11. Peng S., Liu X.S., Wang T., Li Z., Zhou G., Luk K.D.K., et al. Invivo anabolic effect of strontium on trabecular bone was associated with increased osteoblastogenesis of bone marrow stromal cells. JOrthop Res 2010, 28:1208-1214.
12. Neve A., Cantatore F.P., Corrado A., Gaudio A., Ruggieri S., Ribatti D. Invitro and invivo angiogenic activity of osteoarthritic and osteoporotic osteoblasts is modulated by VEGF and vitamin D3 treatment. Regul Pept 2013, 184:81-84.
13. Xu S.F., Lin K.L., Hu Y.Y., Wang Z., Chang J., Wang L., et al. Reconstruction of calvarial defect of rabbits using porous calcium silicate bioactive ceramics. Biomaterials 2008, 29:2588-2596.
14. 3/PDLGA composite scaffold via activation of AMPK/ERK1/2 and PI3K/Akt pathways. Biomaterials 2013, 34:64-77.
15. 2 composite porous bioceramic scaffolds. Acta Biomater 2012, 8:350-360.
16. Saidak Z., Hay E., Marty C., Barbara A., Marie P.J. Strontium ranelate rebalances bone marrow adipogenesis and osteoblastogenesis in senescent osteopenic mice through NFATc/Maf and Wnt signaling. Aging Cell 2012, 11:467-474.
17. Meunier P.J., Roux C., Seeman E., Ortolani S., Badurski J.E., Spector T.D., et al. The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. NEngl J Med 2004, 350:459-468.
18. Yang F., Yang D., Tu J., Zheng Q., Cai L., Wang L. Strontium enhances osteogenic differentiation of mesenchymal stem cells and invivo bone formation by activating wnt/catenin signaling. Stem Cells 2011, 29:981-991.
19. Peng S., Liu X.S., Huang S., Li Z., Pan H., Zhen W., et al. The cross-talk between osteoclasts and osteoblasts in response to strontium treatment: involvement of osteoprotegerin. Bone 2011, 49:1290-1298.
20. Chung C.J., Long H.Y. Systematic strontium substitution in hydroxyapatite coatings on titanium via micro-arc treatment and their osteoblast/osteoclast responses. Acta Biomater 2011, 7:4081-4087.
21. Shen Y.H., Liu W.C., Lin K.L., Pan H.B., Darvell B.W., Peng S.L., et al. pH effects on solid/liquid interface - the critical factor to stimulate osteoporotic bone regeneration. Langmuir 2011, 27:2701-2708.
22. Peng S.L., Zhou G.Q., Luk K.D.K., Cheung K.M.C., Li Z.Y., Lam W.M., et al. Strontium promotes osteogenic differentiation of mesenchymal stem cells through the Ras/MAPK signaling pathway. Cell Phys Biochem 2009, 23:165-174.
23. Marie P.J., Felsenberg D., Brandi M.L. How strontium ranelate, via opposite effects on bone resorption and formation, prevents osteoporosis. Osteoporos Int 2011, 22:1659-1667.
24. Li Y., Li Q., Zhu S., Luo E., Li J., Feng G., et al. The effect of strontium-substituted hydroxyapatite coating on implant fixation in ovariectomized rats. Biomaterials 2010, 31:9006-9014.
25. Saidak Z., Marie P.J. Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther 2012, 136:216-226.
26. Thormann U., Ray S., Sommer U., ElKhassawna T., Rehling T., Hundgeburth M., et al. Bone formation induced by strontium modified calcium phosphate cement in critical-size metaphyseal fracture defects in ovariectomized rats. Biomaterials 2013, 34:8589-8598.
27. Li Z.Y., Lu W.W., Lam W.M., Yang C., Xu B., Ni G.X., et al. Chemical composition, crystal size and lattice structural changes after incorporation of strontium into biomimetic apatite. Biomaterials 2007, 28:1452-1460.
28. Wong C.T., Chen Q.Z., Lu W.W., Leong J.C.Y., Chan W.K., Cheung K.M.C., et al. Ultrastructural study of mineralization of a strontium-containing hydroxyapatite (Sr-HA) cement invivo. JBiomed Mater Res 2004, 70A:428-435.
29. Yuan H., Fernandes H., Habibovic P., De Boer J., Barradas A.M.C., De Ruiter A., et al. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci USA 2010, 107:13614-13619.
30. Lin K.L., Liu P.Y., Zhang W.B., Wei L., Zou Z.Y., Qian Y., et al. Mesoporous strontium substituted hydroxyapatite microspheres: surfactant-free hydrothermal synthesis, enhanced biological response and sustained drug release. Chem Eng J 2013, 222:49-59.
31. Christoffersen J., Christoffersen M.R., Kolthoff N., Barenholdt O. Effects of strontium ions on growth and dissolution of hydroxyapatite and on bone mineral detection. Bone 1997, 20:47-54.
32. Pan H.B., Li Z.Y., Lam W.M., Wong J.C., Darvell B.W., Luk K.D.K., et al. Solubility of strontium-substituted apatite by solid titration. Acta Biomater 2009, 5:1678-1685.
33. Food and Drug Administration Guidelines for preclinical and clinical evaluation of agents used in the prevention or treatment of postmenopausal osteoporosis 1994, FDA, Rockville, USA.
34. Turner A.S. Animal models of osteoporosis - necessity and limitations. Eur Cell Mater 2001, 1:66-81.
35. Engin N.O., Tas A.C. Manufacture of macroporous calcium hydroxyapatite bioceramics. JEur Ceram Soc 1999, 19:2569-2572.
36. Shen Q., Zeng D., Zhou Y., Xia L., Zhao Y., Qiao G., et al. Curculigoside promotes osteogenic differentiation of bone marrow stromal cells from ovariectomized rats. JPharm Pharmacol 2013, 65:1005-1013.
37. Xia L., Zhang Z., Chen L., Zhang W., Zeng D., Zhang X., et al. Proliferation and osteogenic differentiation of human periodontal ligament cells on akermanite and β-TCP bioceramics. Eur Cell Mater 2011, 15(22):68-82.
38. Bordenave L., Baquey C., Bareille R., Lefebvre F., Lauroua C., et al. Endothelial cell, compatibility testing of three different pellethanes. JBiomed Mater Res 1993, 27:1367-1381.
39. Jaffe E.A. Culture of human endothelial cells. Transplant Proc 1980, 12:49-53.
40. Li H., Chang J. Stimulation of proangiogenesis by calcium silicate bioactive ceramic. Acta Biomater 2013, 9:5379-5389.
41. Zhao J., Shen G., Liu C., Wang S., Zhang W., Zhang X., et al. Enhanced healing of rat calvarial defects with sulfated chitosan-coated calcium-deficient hydroxyapatite/bone morphogenetic protein 2 scaffolds. Tissue Eng 2012, 18A:185-197.
42. Zou D., Zhang Z., He J., Zhang K., Ye D., Han W., et al. Blood vessel formation in the tissue-engineered bone with the constitutively active form of HIF-1a mediated BMSCs. Biomaterials 2012, 33:2097-2108.
43. Schumacher M., Lode A., Helth A., Gelinsky M. Anovel strontium(II)-modified calcium phosphate bone cement stimulates human-bone-marrow-derived mesenchymal stem cell proliferation and osteogenic differentiation invitro. Acta Biomater 2013, 10.1016/j.actbio.2013.07.027.
44. Gu Z., Zhang X., Li L., Wang Q., Yu X., Feng T. Acceleration of segmental bone regeneration in a rabbit model by strontium-doped calcium polyphosphate scaffold through stimulating VEGF and bFGF secretion from osteoblasts. Mater Sci Eng 2013, 33C:274-281.
45. Boanini E., Torricelli P., Fini M., Bigi A. Osteopenic bone cell response tostrontium-substituted hydroxyapatite. JMater Sci Mater Med 2011, 22:2079-2088.
46. Wiens M., Wang X., Schröder H.C., Kolb U., Schloßmacher U., Ushijima H., et al. The role of biosilica in the osteoprotegerin/RANKL ratio in human osteoblast-like cells. Biomaterials 2010, 31:7716-7725.
47. Pearson G., Robinson F., Gibson T.B., Xu B.E., Karandikar M., Berman K., et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001, 22:153-183.
48. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
49. Li H., Daculsi R., Grellier M., Bareille R., Bourget C., Remy M., et al. The role of vascular actors in two dimensional dialogue of human bone marrow stromal cell and endothelial cell for inducing tubular-like network. PLoS One 2011, 6:e16767.
50. Terman B.I., Dougher-Vermazen M. Biological properties of VEGF/VPF receptors. Cancer Metastasis Rev 1996, 15:159-163.
51. Breier G., Clauss M., Risau W. Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggests a paracrine regulation of murine vascular development. Dev Dyn 1995, 204:228-239.
52. Lamalice L., Le Boeuf F., Huot J. Endothelial cell migration during angiogenesis. Circ Res 2007, 100:782-794.
53. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
54. Fong E.L., Chan C.K., Goodman S.B. Stem cell homing in musculoskeletal injury. Biomaterials 2011, 32:395-409.