Competing Roles of Substrate Composition, Microstructure, and Sustained Strontium Release in Directing Osteogenic Differentiation of hMSCs

ACS Applied Materials and Interfaces

Volumn 9, Issue 23, 2017, Pages 19389-19408

  Boda, Sunil Kumar ^a   Thrivikraman, Greeshma ^a   Panigrahy, Bharati ^a   Sarma, D D ^a   Basu, Bikramjit ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

human mesenchymal stem cells; hydroxyapatite; nanobiomaterial; osteogenesis; Rietveld refinement; strontium hexaferrite

Indexed keywords

BIOCOMPATIBILITY; BONE; CELL CULTURE; CELLS; CYTOLOGY; FERRITE; GENE EXPRESSION; HYDROXYAPATITE; NANOMAGNETICS; NANOPARTICLES; PHOSPHATASES; RIETVELD REFINEMENT; SINTERING; SPARK PLASMA SINTERING; STEM CELLS; SYNTHESIS (CHEMICAL);

HUMAN MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); MORPHOLOGICAL ANALYSIS; NANOBIOMATERIAL; OSTEOGENESIS; OSTEOGENIC DIFFERENTIATION; STEM CELL DIFFERENTIATION; STRONTIUM HEXAFERRITE;

STRONTIUM;

EID: 85020808757     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b08694     Document Type: Review

References (70)

1. Bolland, M. J.; Grey, A. A Comparison of Adverse Event and Fracture Efficacy Data for Strontium Ranelate in Regulatory Documents and the Publication Record BMJ. Open. 2014, 4 (10) e005787 10.1136/bmjopen-2014-005787
2. Abou Neel, E. A.; Chrzanowski, W.; Pickup, D. M.; O'Dell, L. A.; Mordan, N. J.; Newport, R. J.; Smith, M. E.; Knowles, J. C. Structure and Properties of Strontium-doped Phosphate-based Glasses J. R. Soc., Interface 2009, 6 (34) 435-446 10.1098/rsif.2008.0348
3. Gentleman, E.; Fredholm, Y. C.; Jell, G.; Lotfibakhshaiesh, N.; O'Donnell, M. D.; Hill, R. G.; Stevens, M. M. The Effects of Strontium-substituted Bioactive Glasses on Osteoblasts and Osteoclasts in Vitro Biomaterials 2010, 31 (14) 3949-3956 10.1016/j.biomaterials.2010.01.121
4. Fonseca, J. E.; Brandi, M. L. Mechanism of Action of Strontium Ranelate: What are the Facts? Clin. Cases Miner. Bone Metab. 2010, 7 (1) 17-18
5. Bose, S.; Fielding, G.; Tarafder, S.; Bandyopadhyay, A. Understanding of Dopant-induced Osteogenesis and Angiogenesis in Calcium Phosphate Ceramics Trends Biotechnol. 2013, 31 (10) 594-605 10.1016/j.tibtech.2013.06.005
6. Autefage, H.; Gentleman, E.; Littmann, E.; Hedegaard, M. A. B.; Von Erlach, T.; O'Donnell, M.; Burden, F. R.; Winkler, D. A.; Stevens, M. M. Sparse Feature Selection Methods Identify Unexpected Global Cellular Response to Strontium-containing Materials Proc. Natl. Acad. Sci. U. S. A. 2015, 112 (14) 4280-4285 10.1073/pnas.1419799112
7. Liu, X.; Rahaman, M. N.; Hilmas, G. E.; Bal, B. S. Mechanical Properties of Bioactive Glass (13-93) Scaffolds Fabricated by Robotic Deposition for Structural Bone Repair Acta Biomater. 2013, 9 (6) 7025-7034 10.1016/j.actbio.2013.02.026
8. Thompson, I. D.; Hench, L. L. Mechanical Properties of Bioactive Glasses, Glass-Ceramics and Composites Proc. Inst. Mech. Eng., Part H 1998, 212 (2) 127-136 10.1243/0954411981533908
9. Sabareeswaran, A.; Basu, B.; Shenoy, S. J.; Jaffer, Z.; Saha, N.; Stamboulis, A. Early Osseointegration of a Strontium Containing Glass Ceramic in a Rabbit Model Biomaterials 2013, 34 (37) 9278-9286 10.1016/j.biomaterials.2013.08.070
10. Basu, B.; Sabareeswaran, A.; Shenoy, S. J. Biocompatibility Property of 100% Strontium-substituted SiO2-Al2O3-P2O5-CaO-CaF2 Glass Ceramics Over 26 Weeks Implantation in Rabbit Model: Histology and Micro-Computed Tomography Analysis J. Biomed. Mater. Res., Part B 2015, 103 (6) 1168-1179 10.1002/jbm.b.33270
11. Terra, J.; Dourado, E. R.; Eon, J.-G.; Ellis, D. E.; Gonzalez, G.; Rossi, A. M. The Structure of Strontium-doped Hydroxyapatite: An Experimental and Theoretical Study Phys. Chem. Chem. Phys. 2009, 11 (3) 568-577 10.1039/B802841A
12. Curran, D. J.; Fleming, T. J.; Towler, M. R.; Hampshire, S. Mechanical Parameters of Strontium Doped Hydroxyapatite Sintered Using Microwave and Conventional Methods J. Mech Behav Biomed Mater. 2011, 4 (8) 2063-2073 10.1016/j.jmbbm.2011.07.005
13. Boda, S. K.; V, A. A.; Basu, B.; Sahoo, B. Structural and Magnetic Phase Transformations of Hydroxyapatite-Magnetite Composites under Inert and Ambient Sintering Atmospheres J. Phys. Chem. C 2015, 119 (12) 6539-6555 10.1021/jp5114027
14. Boda, S. K.; Thrivikraman, G.; Basu, B. Magnetic Field Assisted Stem Cell Differentiation-Role of Substrate Magnetization in Osteogenesis J. Mater. Chem. B 2015, 3 (16) 3150-3168 10.1039/C5TB00118H
15. Meininger, S.; Mandal, S.; Kumar, A.; Groll, J.; Basu, B.; Gbureck, U. Strength Reliability and In Vitro Degradation of Three-Dimensional Powder Printed Strontium-Substituted Magnesium Phosphate Scaffolds Acta Biomater. 2016, 31, 401-411 10.1016/j.actbio.2015.11.050
16. Davoodi, A.; Hashemi, B.; Yousefi, M. H. Synthesis of Coprecipitated Strontium Hexaferrite Nanoparticles in the Presence of Polyvinyl Alcohol J. Magn. Magn. Mater. 2011, 323 (23) 3054-3057 10.1016/j.jmmm.2011.06.051
17. Chen, D.-H.; Chen, Y.-Y. Synthesis of Strontium Ferrite Nanoparticles by Coprecipitation in the Presence of Polyacrylic Acid Mater. Res. Bull. 2002, 37 (4) 801-810 10.1016/S0025-5408(01)00590-6
18. Li, T.; Li, Y.; Wu, R.; Zhou, H.; Fang, X.; Su, S.; Xia, A.; Jin, C.; Liu, X. A Solution for the Preparation of Hexagonal M-type SrFe12O19 Ferrite using Egg-white: Structural and Magnetic Properties J. Magn. Magn. Mater. 2015, 393, 325-330 10.1016/j.jmmm.2015.05.088
19. Mirkazemi, S. M.; Alamolhoda, S.; Ghiami, Z. Microstructure and Magnetic Properties of SrFe 12 O 19 Nano-sized Powders Prepared by Sol-Gel Auto-combustion Method with CTAB Surfactant J. Supercond. Novel Magn. 2015, 28 (5) 1543-1549 10.1007/s10948-014-2872-x
20. Boda, S. K.; Bajpai, I.; Basu, B. Inhibitory Effect of Direct Electric Field and HA-ZnO Composites on S. aureus Biofilm Formation J. Biomed. Mater. Res., Part B 2016, 104 (6) 1064-1075 10.1002/jbm.b.33455
21. Larson, A. C.; Von Dreele, R. B. General Structure and Analysis System (GSAS); Los Alamos National Laboratory Report LAUR 86-748; Los Alamos National Laboratory: Los Alamos, NM, 2000.
22. Humphries, J. D.; Wang, P.; Streuli, C.; Geiger, B.; Humphries, M. J.; Ballestrem, C. Vinculin Controls Focal Adhesion Formation by Direct Interactions with Talin and Actin J. Cell Biol. 2007, 179 (5) 1043-1057 10.1083/jcb.200703036
23. Thrivikraman, G.; Mallik, P. K.; Basu, B. Substrate Conductivity Dependent Modulation of Cell Proliferation and Differentiation in Vitro Biomaterials 2013, 34 (29) 7073-7085 10.1016/j.biomaterials.2013.05.076
24. Stingaciu, M.; Topole, M.; McGuiness, P.; Christensen, M. Magnetic Properties of Ball-milled SrFe12O19 Particles Consolidated by Spark-Plasma Sintering Sci. Rep. 2015, 5, 14112 10.1038/srep14112
25. Thrivikraman, G.; Madras, G.; Basu, B. In vitro/In vivo Assessment and Mechanisms of Toxicity of Bioceramic Materials and its Wear Particulates RSC Adv. 2014, 4 (25) 12763-12781 10.1039/c3ra44483j
26. Berbenni, V.; Marini, A. Solid State Synthesis of Strontium Oxoferrates from the Mechanically Activated System SrCO3-Fe2O3 Mater. Res. Bull. 2002, 37 (2) 221-234 10.1016/S0025-5408(01)00767-X
27. Rakshit, S. K.; Parida, S. C.; Dash, S.; Singh, Z.; Sen, B. K.; Venugopal, V. Thermodynamic studies on SrFe12O19(s), SrFe2O4(s), Sr2Fe2O5(s) and Sr3Fe2O6(s) J. Solid State Chem. 2007, 180 (2) 523-532 10.1016/j.jssc.2006.11.012
28. Alavi, M. A.; Morsali, A. Syntheses and Characterization of Sr(OH)2 and SrCO3 Nanostructures by Ultrasonic Method Ultrason. Sonochem. 2010, 17 (1) 132-138 10.1016/j.ultsonch.2009.05.004
29. Zhang, X.; Niu, Y.; Meng, X.; Li, Y.; Zhao, J. Structural Evolution and Characteristics of the Phase Transformations between α-Fe2O3, Fe3O4 and γ-Fe2O3 Nanoparticles under Reducing and Oxidizing Atmospheres CrystEngComm 2013, 15 (40) 8166-8172 10.1039/c3ce41269e
30. Saura-Muzquiz, M.; Granados-Miralles, C.; Stingaciu, M.; Bojesen, E. D.; Li, Q.; Song, J.; Dong, M.; Eikeland, E.; Christensen, M. Improved Performance of SrFe12O19 Bulk Magnets Through Bottom-up Nanostructuring Nanoscale 2016, 8 (5) 2857-2866 10.1039/C5NR07854G
31. Gu, Y. W.; Loh, N. H.; Khor, K. A.; Tor, S. B.; Cheang, P. Spark Plasma Sintering of Hydroxyapatite Powders Biomaterials 2002, 23 (1) 37-43 10.1016/S0142-9612(01)00076-X
32. Mayer, I.; Diab, H.; Felner, I. Ferric Iron in Synthetic Carbonate Apatites: A Mossbauer Effect Study J. Inorg. Biochem. 1992, 45 (2) 129-133 10.1016/0162-0134(92)80007-I
33. Han, R.; Li, W.; Pan, W.; Zhu, M.; Zhou, D.; Li, F. S. 1D Magnetic Materials of Fe(3)O(4) and Fe with High Performance of Microwave Absorption Fabricated by Electrospinning Method Sci. Rep. 2014, 4, 7493 10.1038/srep07493
34. Jing, P.; Du, J.; Wang, J.; Wei, J.; Pan, L.; Li, J.; Liu, Q. Width-Controlled M-type Hexagonal Strontium Ferrite (SrFe12O19) Nanoribbons with High Saturation Magnetization and Superior Coercivity Synthesized by Electrospinning Sci. Rep. 2015, 5, 15089 10.1038/srep15089
35. Thrivikraman, G.; Lee, P. S.; Hess, R.; Haenchen, V.; Basu, B.; Scharnweber, D. Interplay of Substrate Conductivity, Cellular Microenvironment, and Pulsatile Electrical Stimulation toward Osteogenesis of Human Mesenchymal Stem Cells in Vitro ACS Appl. Mater. Interfaces 2015, 7 (41) 23015-23028 10.1021/acsami.5b06390
36. Horzum, U.; Ozdil, B.; Pesen-Okvur, D. Step-by-step Quantitative Analysis of Focal Adhesions MethodsX 2014, 1, 56-59 10.1016/j.mex.2014.06.004
37. Kim, D. H.; Wirtz, D. Focal Adhesion Size Uniquely Predicts Cell Migration FASEB J. 2013, 27 (4) 1351-1361 10.1096/fj.12-220160
38. Yim, E. K. F.; Darling, E. M.; Kulangara, K.; Guilak, F.; Leong, K. W. Nanotopography-induced Changes in Focal Adhesions, Cytoskeletal Organization, and Mechanical Properties of Human Mesenchymal Stem Cells Biomaterials 2010, 31 (6) 1299-1306 10.1016/j.biomaterials.2009.10.037
39. Prager-Khoutorsky, M.; Lichtenstein, A.; Krishnan, R.; Rajendran, K.; Mayo, A.; Kam, Z.; Geiger, B.; Bershadsky, A. D. Fibroblast Polarization is a Matrix-Rigidity-Dependent Process Controlled by Focal Adhesion Mechanosensing Nat. Cell Biol. 2011, 13 (12) 1457-1465 10.1038/ncb2370
40. Chen, Y.-J.; Shie, M.-Y.; Hung, C., Jr.; Wu, B.-C.; Liu, S.-L.; Huang, T.-H.; Kao, C.-T. Activation of Focal Adhesion Kinase Induces Extracellular Signal-Regulated Kinase-Mediated Osteogenesis in Tensile Force-Subjected Periodontal Ligament Fibroblasts but not in Osteoblasts J. Bone Miner. Metab. 2014, 32 (6) 671-682 10.1007/s00774-013-0549-3
41. Hu, J.; Liao, H.; Ma, Z.; Chen, H.; Huang, Z.; Zhang, Y.; Yu, M.; Chen, Y.; Xu, J. Focal Adhesion Kinase Signaling Mediated the Enhancement of Osteogenesis of Human Mesenchymal Stem Cells Induced by Extracorporeal Shockwave Sci. Rep. 2016, 6, 20875 10.1038/srep20875
42. Mendez, M. G.; Kojima, S.-I.; Goldman, R. D. Vimentin Induces Changes in Cell Shape, Motility, and Adhesion During the Epithelial to Mesenchymal Transition FASEB J. 2010, 24 (6) 1838-1851 10.1096/fj.09-151639
43. Lian, N.; Wang, W.; Li, L.; Elefteriou, F.; Yang, X. Vimentin Inhibits ATF4-mediated Osteocalcin Transcription and Osteoblast Differentiation J. Biol. Chem. 2009, 284 (44) 30518-30525 10.1074/jbc.M109.052373
44. Yang, J.; McNamara, L. E.; Gadegaard, N.; Alakpa, E. V.; Burgess, K. V.; Meek, R. M. D.; Dalby, M. J. Nanotopographical Induction of Osteogenesis through Adhesion, Bone Morphogenic Protein Cosignaling, and Regulation of MicroRNAs ACS Nano 2014, 8 (10) 9941-9953 10.1021/nn504767g
45. Barbara, A.; Delannoy, P.; Denis, B. G.; Marie, P. J. Normal Matrix Mineralization Induced by Strontium Ranelate in MC3T3-E1 Osteogenic Cells Metab., Clin. Exp. 2004, 53 (4) 532-537 10.1016/j.metabol.2003.10.022
46. Zhang, J.; Shi, H. S.; Liu, J. Q.; Yu, T.; Shen, Z. H.; Ye, J. D. Good Hydration and Cell-Biological Performances of Superparamagnetic Calcium Phosphate Cement with Concentration-Dependent Osteogenesis and Angiogenesis Induced by Ferric Iron J. Mater. Chem. B 2015, 3 (45) 8782-8795 10.1039/C5TB01440A
47. Tran, N.; Webster, T. J. Magnetic Nanoparticles: Biomedical Applications and Challenges J. Mater. Chem. 2010, 20 (40) 8760-8767 10.1039/c0jm00994f
48. Cannas, C.; Musinu, A.; Ardu, A.; Orru, F.; Peddis, D.; Casu, M.; Sanna, R.; Angius, F.; Diaz, G.; Piccaluga, G. CoFe2O4 and CoFe2O4/SiO2 Core/Shell Nanoparticles: Magnetic and Spectroscopic Study Chem. Mater. 2010, 22 (11) 3353-3361 10.1021/cm903837g
49. Zhang, W.; Shen, Y.; Pan, H.; Lin, K.; Liu, X.; Darvell, B. W.; Lu, W. W.; Chang, J.; Deng, L.; Wang, D.; Huang, W. Effects of Strontium in Modified Biomaterials Acta Biomater. 2011, 7 (2) 800-808 10.1016/j.actbio.2010.08.031
50. Toxqui, L.; Vaquero, M. Chronic Iron Deficiency as an Emerging Risk Factor for Osteoporosis: A Hypothesis Nutrients 2015, 7 (4) 2324 10.3390/nu7042324
51. Pan, H. B.; Li, Z. Y.; Lam, W. M.; Wong, J. C.; Darvell, B. W.; Luk, K. D. K.; Lu, W. W. Solubility of Strontium-Substituted Apatite by Solid Titration Acta Biomater. 2009, 5 (5) 1678-1685 10.1016/j.actbio.2008.11.032
52. Nardone, V.; Zonefrati, R.; Mavilia, C.; Romagnoli, C.; Ciuffi, S.; Fabbri, S.; Palmini, G.; Galli, G.; Tanini, A.; Brandi, M. L. In Vitro Effects of Strontium on Proliferation and Osteoinduction of Human Preadipocytes Stem Cells Int. 2015, 2015, 871863 10.1155/2015/871863
53. Pouria, A.; Bandegani, H.; Pourbaghi-Masouleh, M.; Hesaraki, S.; Alizadeh, M. Physicochemical Properties and Cellular Responses of Strontium-Doped Gypsum Biomaterials Bioinorg. Chem. Appl. 2012, 2012, 976495 10.1155/2012/976495
54. Hao, Y.; Yan, H.; Wang, X.; Zhu, B.; Ning, C.; Ge, S. Evaluation of Osteoinduction and Proliferation on Nano-Sr-HAP: A Novel Orthopedic Biomaterial for Bone Tissue Regeneration J. Nanosci. Nanotechnol. 2012, 12 (1) 207-212 10.1166/jnn.2012.5125
55. Fromigue, O.; Hay, E.; Barbara, A.; Marie, P. J. Essential Role of Nuclear Factor of Activated T Cells (NFAT)-mediated Wnt Signaling in Osteoblast Differentiation Induced by Strontium Ranelate J. Biol. Chem. 2010, 285 (33) 25251-25258 10.1074/jbc.M110.110502
56. Li, Y.; Li, J.; Zhu, S.; Luo, E.; Feng, G.; Chen, Q.; Hu, J. Effects of Strontium on Proliferation and Differentiation of Rat Bone Marrow Mesenchymal Stem Cells Biochem. Biophys. Res. Commun. 2012, 418 (4) 725-730 10.1016/j.bbrc.2012.01.088
57. Subbiah, R.; Suhaeri, M.; Hwang, M. P.; Kim, W.; Park, K. Investigation of the Changes of Biophysical/Mechanical Characteristics of Differentiating Preosteoblasts in Vitro Biomater Res. 2015, 19, 24 10.1186/s40824-015-0046-y
58. Veljović, D.; Čolic, M.; Kojić, V.; Bogdanović, G.; Kojić, Z.; Banjac, A.; Palcevskis, E.; Petrović, R.; Janaćković, D. The Effect of Grain Size on the Biocompatibility, Cell-Materials Interface, and Mechanical Properties of Microwave-Sintered Bioceramics J. Biomed. Mater. Res., Part A 2012, 100A (11) 3059-3070 10.1002/jbm.a.34225
59. Lapczyna, H.; Galea, L.; Wust, S.; Bohner, M.; Jerban, S.; Sweedy, A.; Doebelin, N.; van Garderen, N.; Hofmann, S.; Baroud, G.; Muller, R.; von Rechenberg, B. Effect of Grain Size and Microporosity on the In Vivo Behaviour of β-tricalcium Phosphate Scaffolds Eur. Cell Mater. 2014, 28, 299-319
60. Saidak, Z.; Marie, P. J. Strontium Signaling: Molecular Mechanisms and Therapeutic Implications in Osteoporosis Pharmacol. Ther. 2012, 136 (2) 216-226 10.1016/j.pharmthera.2012.07.009
61. Jaiswal, R. K.; Jaiswal, N.; Bruder, S. P.; Mbalaviele, G.; Marshak, D. R.; Pittenger, M. F. Adult Human Mesenchymal Stem Cell Differentiation to the Osteogenic or Adipogenic Lineage is Regulated by Mitogen-Activated Protein Kinase J. Biol. Chem. 2000, 275 (13) 9645-9652 10.1074/jbc.275.13.9645
62. Xiao, G.; Jiang, D.; Thomas, P.; Benson, M. D.; Guan, K.; Karsenty, G.; Franceschi, R. T. MAPK Pathways Activate and Phosphorylate the Osteoblast-Specific Transcription Factor, Cbfa1 J. Biol. Chem. 2000, 275 (6) 4453-4459 10.1074/jbc.275.6.4453
63. Peng, S.; Zhou, G.; Luk, K. D.; Cheung, K. M.; Li, Z.; Lam, W. M.; Zhou, Z.; Lu, W. W. Strontium Promotes Osteogenic Differentiation of Mesenchymal Stem Cells Through the Ras/MAPK Signaling Pathway Cell. Physiol. Biochem. 2009, 23 (1-3) 165-174 10.1159/000204105
64. Takeuchi, Y.; Suzawa, M.; Kikuchi, T.; Nishida, E.; Fujita, T.; Matsumoto, T. Differentiation and Transforming Growth Factor-β Receptor Down-regulation by Collagen-α2β1 Integrin Interaction Is Mediated by Focal Adhesion Kinase and Its Downstream Signals in Murine Osteoblastic Cells J. Biol. Chem. 1997, 272 (46) 29309-29316 10.1074/jbc.272.46.29309
65. Yang, H. W.; Lin, M. H.; Xu, Y. Z.; Shang, G. W.; Wang, R. R.; Chen, K. Osteogenesis of Bone Marrow Mesenchymal Stem Cells on Strontium-Substituted Nano-Hydroxyapatite Coated Roughened Titanium Surfaces Int. J. Clin. Exp. Med. 2015, 8 (1) 257-264
66. Beck, G. R.; Zerler, B.; Moran, E. Phosphate is a Specific Signal for Induction of Osteopontin Gene Expression Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (15) 8352-8357 10.1073/pnas.140021997
67. Yoshiko, Y.; Candeliere, G. A.; Maeda, N.; Aubin, J. E. Osteoblast Autonomous Pi Regulation via Pit1 Plays a Role in Bone Mineralization Mol. Cell. Biol. 2007, 27 (12) 4465-4474 10.1128/MCB.00104-07
68. Schack, L. M.; Noack, S.; Winkler, R.; Wissmann, G.; Behrens, P.; Wellmann, M.; Jagodzinski, M.; Krettek, C.; Hoffmann, A. The Phosphate Source Influences Gene Expression and Quality of Mineralization during Osteogenic Differentiation of Human Mesenchymal Stem Cells PLoS One 2013, 8 (6) e65943 10.1371/journal.pone.0065943
69. Oh, S.; Brammer, K. S.; Li, Y. S.; Teng, D.; Engler, A. J.; Chien, S.; Jin, S. Stem Cell Fate Dictated Solely by Altered Nanotube Dimension Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (7) 2130-2135 10.1073/pnas.0813200106
70. Boda, S. K.; Basu, B. Engineered Biomaterial and Biophysical Stimulation as Combinatorial Strategies to Address Prosthetic Infection by Pathogenic Bacteria. J. Biomed. Mater. Res., Part B 2016, DOI: 10.1002/jbm.b.33740.