Promotion of pro-osteogenic responses by a bioactive ceramic coating†
Aniket
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorAmy Young
Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorIan Marriott
Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorCorresponding Author
Ahmed El-Ghannam
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223Search for more papers by this authorAniket
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorAmy Young
Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorIan Marriott
Department of Biology, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Search for more papers by this authorCorresponding Author
Ahmed El-Ghannam
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223
Department of Mechanical Engineering and Engineering Science, University of North Carolina at Charlotte, Charlotte, North Carolina 28223Search for more papers by this authorHow to cite this article: Aniket, Young A, Marriott I, El-Ghannam A. 2012. Promotion of pro-osteogenic responses by a bioactive ceramic coating. J Biomed Mater Res Part A 2012:100A:3314–3325.
Abstract
The objective of this study was to analyze the responses of bone-forming osteoblasts to Ti-6Al-4V implant material coated with silica-calcium phosphate nanocomposite (SCPC50). Osteoblast differentiation at the interface with SCPC50-coated Ti-6Al-4V was correlated to the adsorption of high amount of serum proteins, high surface affinity to fibronectin, Ca uptake from and P and Si release into the medium. SCPC50-coated Ti-6Al-4V adsorbed significantly more serum protein (p < 0.05) than control uncoated substrates. Moreover, Western blot analysis showed that the SCPC50 coating had a high affinity for serum fibronectin. Protein conformation analyses by FTIR showed that the ratio of the area under the peak for amide I/amide II bands was significantly higher (p < 0.05) on the surface of SCPC50-coated substrates than that on the surface of the control uncoated substrates. Moreover, ICP − OES analyses indicated that SCPC50-coated substrates withdrew Ca ions from, and released P and Si ions into, the tissue culture medium, respectively. In conjunction with the favorable protein adsorption and modifications in medium composition, MC3T3-E1 osteoblast-like cells attached to SCPC50-coated substrates expressed 10-fold higher level of mRNA encoding osteocalcin and had significantly higher production of osteopontin and osteocalcin proteins than cells attached to the uncoated Ti-6A1-4V substrates. In addition, osteoblast-like cells attached to the SCPC50-coated substrates produced significantly lower levels of the inflammatory and osteoclastogenic cytokines, IL-6, IL-12p40, and RANKL than those attached to uncoated Ti-6Al-4V substrates. These results suggest that SCPC50 coating could enhance bone integration with orthopedic and maxillofacial implants while minimizing the induction of inflammatory bone cell responses. © 2012 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 100A:3314–3325, 2012.
REFERENCES
- 1 LeGeros RZ. Properties of osteoconductive biomaterials: Calcium phosphates. Clin Orthop Relat Res 2002; 395: 81.
- 2 Tanzer M, Kantor S, Rosenthall L, Bobyn JD. Femoral remodeling after porous-coated total hip arthroplasty with and without hydroxyapatite-tricalcium phosphate coating: A prospective randomized trial. J Arthroplasty 2001; 16: 552–558.
- 3 Geesink R, de Groot K, Klein C. Bonding of bone to apatite-coated implants. J Bone Joint Surg Br 1988; 70: 17.
- 4 Reikerås O, Gunderson RB. Excellent results of HA coating on a grit-blasted stem: 245 patients followed for 8–12 years. Acta Orthop 2003; 74: 140–145.
- 5 Wong M, Eulenberger J, Schenk R, Hunziker E. Effect of surface topology on the osseointegration of implant materials in trabecular bone. J Biomed Mater Res 1995; 29: 1567–1575.
- 6
Gross KA,
Berndt CC.
Thermal processing of hydroxyapatite for coating production.
J Biomed Mater Res
1998;
39:
580–587.
10.1002/(SICI)1097-4636(19980315)39:4<580::AID-JBM12>3.0.CO;2-B CAS PubMed Web of Science® Google Scholar
- 7 Sun L, Berndt CC, Gross KA, Kucuk A. Material fundamentals and clinical performance of plasma-sprayed hydroxyapatite coatings: A review. J Biomed Mater Res 2001; 58: 570–592.
- 8 Yang YC, Chang E. Influence of residual stress on bonding strength and fracture of plasma-sprayed hydroxyapatite coatings on Ti-6Al-4V substrate. Biomaterials 2001; 22: 1827–1836.
- 9
Gross KA,
Berndt CC,
HH.
Amorphous phase formation in plasma-sprayed hydroxyapatite coatings.
J Biomed Mater Res
1998;
39:
407–414.
10.1002/(SICI)1097-4636(19980305)39:3<407::AID-JBM9>3.0.CO;2-N CAS PubMed Web of Science® Google Scholar
- 10
Yang C,
Wang B,
Lee T,
Chang E,
Chang G.
Intramedullary implant of plasma-sprayed hydroxyapatite coating: An interface study.
J Biomed Mater Res
1997;
36:
39–48.
10.1002/(SICI)1097-4636(199707)36:1<39::AID-JBM5>3.0.CO;2-M CAS PubMed Web of Science® Google Scholar
- 11 Aniket, El-Ghannam A. Electrophoretic deposition of bioactive silica-calcium phosphate nanocomposite on Ti-6Al-4V orthopedic implant. J Biomed Mater Res Part B: Appl Biomater 2011; 99B: 369–379.
- 12 Wang C, Ma J, Cheng W, Zhang R. Thick hydroxyapatite coatings by electrophoretic deposition. Mater Lett 2002; 57: 99–105.
- 13 Javidi M, Javadpour S, Bahrololoom M, Ma J. Electrophoretic deposition of natural hydroxyapatite on medical grade 316L stainless steel. Mater Sci Eng: C 2008; 28: 1509–1515.
- 14 Roach P, Farrar D, Perry CC. Surface tailoring for controlled protein adsorption: Effect of topography at the nanometer scale and chemistry. J Am Chem Soc 2006; 128: 3939–3945.
- 15 Yang Y, Cavin R, Ong JL. Protein adsorption on titanium surfaces and their effect on osteoblast attachment. J Biomed Mater Res Part A 2003; 67: 344–349.
- 16 Keselowsky BG, Collard DM, Garcia AJ. Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials 2004; 25: 5947–5954.
- 17 Keselowsky BG, Collard DM, García AJ. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. J Biomed Mater Res Part A 2003; 66: 247–259.
- 18
El-Ghannam A,
Hamazawy E,
Yehia A.
Effect of thermal treatment on bioactive glass microstructure, corrosion behavior, ζ potential, and protein adsorption.
J Biomed Mater Res
2001;
55:
387–395.
10.1002/1097-4636(20010605)55:3<387::AID-JBM1027>3.0.CO;2-V CAS PubMed Web of Science® Google Scholar
- 19 Buchanan LA, El-Ghannam A. Effect of bioactive glass crystallization on the conformation and bioactivity of adsorbed proteins. J Biomed Mater Res Part A 2010; 93: 537–546.
- 20 Patil S, Sandberg A, Heckert E, Self W, Seal S. Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 2007; 28: 4600–4607.
- 21 Boyd A, Burke G, Duffy H, Holmberg M, O'Kane C, Meenan B, Kingshott P. Sputter deposited bioceramic coatings: Surface characterisation and initial protein adsorption studies using surface-MALDI-MS. J Mater Sci: Mater Med 2011: 1–14.
- 22 El-Ghannam A, Ducheyne P, Shapiro I. Effect of serum proteins on osteoblast adhesion to surface-modified bioactive glass and hydroxyapatite. J Orthop Res 1999; 17: 340–345.
- 23 Kilpadi KL, Chang PL, Bellis SL. Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. J Biomed Mater Res 2001; 57: 258–267.
- 24
García AJ,
Ducheyne P,
Boettiger D.
Effect of surface reaction stage on fibronectin-mediated adhesion of osteoblast-like cells to bioactive glass.
J Biomed Mater Res
1998;
40:
48–56.
10.1002/(SICI)1097-4636(199804)40:1<48::AID-JBM6>3.0.CO;2-R CAS PubMed Web of Science® Google Scholar
- 25 Botelho C, Brooks RA, Kawai T, Ogata S, Ohtsuki C, Best SM, Lopes M, Santos J, Rushton N, Bonfield W. In vitro analysis of protein adhesion to phase pure hydroxyapatite and silicon substituted hydroxyapatite. Key Eng Mater 2005; 284: 461–464.
- 26 Cowles E, DeRome M, Pastizzo G, Brailey L, Gronowicz G. Mineralization and the expression of matrix proteins during in vivo bone development. Calcif Tissue Int 1998; 62: 74–82.
- 27 Stein GS, Lian JB, Owen TA. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 1990; 4: 3111.
- 28 Lian J, McKee M, Todd A, Gerstenfeld LC. Induction of bone-related proteins, osteocalcin and osteopontin, and their matrix ultrastructural localization with development of chondrocyte hypertrophy in vitro. J Cell Biochem 1993; 52: 206–219.
- 29 Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature 2003; 423: 337–342.
- 30 Haynes DR, Crotti T, Zreiqat H. Regulation of osteoclast activity in peri-implant tissues. Biomaterials 2004; 25: 4877–4885.
- 31 Amcheslavsky A, Bar-Shavit Z. Interleukin (IL)-12 mediates the anti-osteoclastogenic activity of CpG-oligodeoxynucleotides. J Cell Physiol 2006; 207: 244–250.
- 32 Gupta G, Kirakodu S, El-Ghannam A. Dissolution kinetics of a Si-rich nanocomposite and its effect on osteoblast gene expression. J Biomed Mater Res Part A 2007; 80: 486–496.
- 33 El-Ghannam AR. Advanced bioceramic composite for bone tissue engineering: Design principles and structure–bioactivity relationship. J Biomed Mater Res Part A 2004; 69: 490–501.
- 34 Alexander EH, Bento JL, Hughes JrFM, Marriott I, Hudson MC, Bost KL. Staphylococcus aureus and Salmonella enterica serovar Dublin induce tumor necrosis factor-related apoptosis-inducing ligand expression by normal mouse and human osteoblasts. Infect Immun 2001; 69: 1581.
- 35 Tropel P, Noël D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res 2004; 295: 395–406.
- 36 Chackalaparampil I, Peri A, Nemir M, Mckee MD, Lin PH, Mukherjee BB, Mukherjee AB. Cells in vivo and in vitro from osteopetrotic mice homozygous for c-src disruption show suppression of synthesis of osteopontin, a multifunctional extracellular matrix protein. Oncogene 1996; 12: 1457.
- 37 Windahl SH, Vidal O, Andersson G, Gustafsson J, Ohlsson C. Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ERbeta (-/-) mice. J Clin Invest 1999; 104: 895–901.
- 38 McCall SH, Sahraei M, Young AB, Worley CS, Duncan JA, Ting JPY, Marriott I. Osteoblasts express NLRP3, a nucleotide-binding domain and leucine-rich repeat region containing receptor implicated in bacterially induced cell death. J Bone Miner Res 2008; 23: 30–40.
- 39 Chaiyasut C, Tsuda T. Isoelectric points estimation of proteins by electroosmotic flow: pH relationship using physically adsorbed proteins on silica gel. Chromatography 2001; 22: 91–96.
- 40 Ji Z, Jin X, George S, Xia T, Meng H, Wang X, Suarez E, Zhang H, Hoek EMV, Godwin H. Dispersion and stability optimization of TiO2 nanoparticles in cell culture media. Environ Sci Technol 2010; 44: 7309–7314.
- 41 Murdock RC, Braydich-Stolle L, Schrand AM, Schlager JJ, Hussain SM. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol Sci 2008; 101: 239–253.
- 42 Ask M, Lausmaa J, Kasemo B. Preparation and surface spectroscopic characterization of oxide films on Ti6Al4V. Appl Surf Sci 1989; 35: 283–301.
- 43 Steinberg D, Klinger A, Kohavi D, Sela MN. Adsorption of human salivary proteins to titanium powder. I. Adsorption of human salivary albumin. Biomaterials 1995; 16: 1339–1343.
- 44 Amphlett GW, Hrinda ME. The binding of calcium to human fibronectin. Biochem Biophys Res Commun 1983; 111: 1045–1053.
- 45 Scott BJ, Bradwell A. Identification of the serum binding proteins for iron, zinc, cadmium, nickel, and calcium. Clin Chem 1983; 29: 629.
- 46
Klinger A,
Steinberg D,
Kohavi D,
Sela M.
Mechanism of adsorption of human albumin to titanium in vitro.
J Biomed Mater Res
1997;
36:
387–392.
10.1002/(SICI)1097-4636(19970905)36:3<387::AID-JBM13>3.0.CO;2-B CAS PubMed Web of Science® Google Scholar
- 47 Liu X, EI-Ghannam A. Effect of processing parameters on the microstructure and mechanical behavior of silica-calcium phosphate nanocomposite. J Mater Sci: Mater Med 2010; 21: 2087–2094.
- 48 Kawano M, Hwang J. Influence of guanidine, imidazole, and some heterocyclic compounds on dissolution rates of amorphous silica. Clays Clay Miner 2011; 58: 757.
- 49 Fournier AC, McGrath KM. Porous protein–silica composite formation: Manipulation of silicate porosity and protein conformation. Soft Matter 2011; 7: 4918–4927.
- 50 Chittur KK. FTIR/ATR for protein adsorption to biomaterial surfaces. Biomaterials 1998; 19: 357–369.
- 51 Roach P, Farrar D, Perry CC. Interpretation of protein adsorption: Surface-induced conformational changes. J Am Chem Soc 2005; 127: 8168–8173.
- 52 Dvorak MM, Riccardi D. Ca2+ as an extracellular signal in bone. Cell Calcium 2004; 35: 249–255.
- 53 Maeno S, Niki Y, Matsumoto H, Morioka H, Yatabe T, Funayama A, Toyama Y, Taguchi T, Tanaka J. The effect of calcium ion concentration on osteoblast viability, proliferation and differentiation in monolayer and 3D culture. Biomaterials 2005; 26: 4847–4855.
- 54 Anselme K. Osteoblast adhesion on biomaterials. Biomaterials 2000; 21: 667–681.
- 55 Beck GR, Jr. Inorganic phosphate as a signaling molecule in osteoblast differentiation. J Cell Biochem 2003; 90: 234–243.
- 56 Boskey AL, Guidon P, Doty SB, Stiner D, Leboy P, Binderman I. The mechanism of β-glycerophosphate action in mineralizing chick limb-bud mesenchymal cell cultures. J Bone Miner Res 1996; 11: 1694–1702.
- 57 Chung CH, Golub EE, Forbes E, Tokuoka T, Shapiro IM. Mechanism of action of β-glycerophosphate on bone cell mineralization. Calcif Tissue Int 1992; 51: 305–311.
- 58 Gupta G, Kirakodu S, El-Ghannam A. Effects of exogenous phosphorus and silicon on osteoblast differentiation at the interface with bioactive ceramics. J Biomed Mater Res Part A 2010.
- 59 Gomes PS, Botelho C, Lopes MA, Santos JD, Fernandes MH. Evaluation of human osteoblastic cell response to plasma-sprayed silicon-substituted hydroxyapatite coatings over titanium substrates. J Biomed Mater Res Part B: Appl Biomater 2010; 94: 337–346.
- 60 Arumugam MQ, Ireland D, Brooks RA, Rushton N, Bonfield W. The effect orthosilicic acid on collagen type I, alkaline phosphatase and osteocalcin mRNA expression in human bone-derived osteoblasts in vitro. Key Eng Mater 2006; 309: 121–124.
- 61 Reffitt D, Ogston N, Jugdaohsingh R, Cheung H, Evans B, Thompson R, Powell J, Hampson G. Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 2003; 32: 127–135.
- 62 Carlisle EM. Silicon as an essential trace element in animal nutrition. Ciba Found Symp 1986; 121: 123–139.
- 63 El-Ghannam A, Ning C. Effect of bioactive ceramic dissolution on the mechanism of bone mineralization and guided tissue growth in vitro. J Biomed Mater Res Part A 2006; 76: 386–397.
- 64 Lian JB, Stein GS. Concepts of osteoblast growth and differentiation: Basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med 1992; 3: 269–305.
- 65 Gori F, Hofbauer LC, Dunstan CR, Spelsberg TC, Khosla S, Riggs BL. The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated. Endocrinology 2000; 141: 4768.