Calcium phosphates including β-tricalcium phosphate (β-TCP) and hydroxyapatite (HAp) have been widely used for bone regeneration application because of their high osteoconductive activities. In addition, various kinds of inorganic ions enhance differentiation, proliferation, and mineralization of osteoblasts. However, information about the effects of silver-doped β-TCP [β-TCP (Ag)] and HAp [HAp (Ag)] particles on osteogenic differentiation is not available yet.
OBJECTIVE:
We focused on the impact of β-TCP (Ag) and HAp (Ag) particles on the osteogenic differentiation of MC3T3-E1 osteoblast precursor cells.
METHODS:
MC3T3-E1 osteoblast precursor cells were pre-treated by β-TCP (Ag) or HAp (Ag). And then the medium was changed to differentiation medium. Subsequently, osteoblast differentiation-related markers were determined.
RESULTS:
We found that treatment with β-TCP (Ag) or HAp (Ag) particles increased alkaline phosphatase activity in MC3T3-E1 cells. Expression of osteoblast differentiation-related genes also increased after treatment with β-TCP (Ag) or HAp (Ag) particles, a response thought to be regulated by zinc finger-containing transcription factor osterix. The ratio of the receptor activator of nuclear factor kappa-B ligand (RANKL) to osteoprotegerin (OPG) was decreased by β-TCP (Ag) and HAp (Ag) particles.
CONCLUSION:
Silver doping of β-TCP and HAp particles is effective for bone regeneration.
LevingstoneT.J.HerbajS. and DunneN.J., Calcium phosphate nanoparticles for therapeutic applications in bone regeneration, Nanomaterials9(11) (2019), 1570. doi:10.3390/nano9111570.
2.
JonesJ.R. and HenchL.L., Regeneration of trabecular bone using porous ceramics, Curr Opin Solid State Mater Sci7 (2003), 301–307.
3.
JeongJ.KimJ.H.SimJ.H.HwangN.S. and HeoC.Y., Bioactive calcium phosphate materials and applications in bone regeneration, Biomater Res23 (2019), 4.
4.
LuJ.YuH. and ChenC., Biological properties of calcium phosphate biomaterials for bone repair: a review, RSC Adv8 (2018), 2015–2033.
5.
HoppeA.GüldalN.S. and BoccacciniA.R., A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics, Biomaterials32(11) (2011), 2757–2774. doi:10.1016/j.biomaterials.2011.01.004.
6.
GlenskeK.DonkiewiczP.KöwitschA.Milosevic-OljacaN.RiderP.RofallS., Application of metals for bone regeneration, Int J Mol Sci19(3) (2018), 826. doi:10.3390/ijms19030826.
7.
YangF.YangD.TuJ.ZhengQ.CaiL. and WangL., Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling, Stem Cells29(6) (2011), 981–991. doi:10.1002/stem.646.
8.
AriokaM.Takahashi-YanagaF.SasakiM.YoshiharaT.MorimotoS.HirataM., Acceleration of bone regeneration by local application of lithium: Wnt signal-mediated osteoblastogenesis and Wnt signal-independent suppression of osteoclastogenesis, Biochem Pharmacol90(4) (2014), 397–405. doi:10.1016/j.bcp.2014.06.011.
9.
YamaguchiM. and WeitzmannM.N., Zinc stimulates osteoblastogenesis and suppresses osteoclastogenesis by antagonizing NF-𝜅B activation, Mol Cell Biochem355(1–2) (2011), 179–186.
10.
MahmoodM.LiZ.CascianoD.KhodakovskavaM.V.ChenT.KarmakarA., Nanostructural materials increase mineralization in bone cells and affect gene expression through miRNA regulation, J Cell Mol Med15(11) (2011), 2297–2306. doi:10.1111/j.1582-4934.2010.01234.x.
11.
QingT.MahmoodM.ZhengY.BirisA.S.ShiL. and CascianoD.A., A genomic characterization of the influence of silver nanoparticles on bone differentiation in MC3T3-E1 cells, J Appl Toxicol38(2) (2018), 172–179. doi:10.1002/jat.3528.
12.
O’NeillE.AwaleG.DaneshmandiL.UmerahO. and LoK.W., The roles of ions on bone regeneration, Drug Discov Today23(4) (2018), 879–890. doi:10.1016/j.drudis.2018.01.049.
13.
RauJ.V.FoscaM.GrazianiV.EgorovA.A.ZobkovY.V.FedotovA.Y., Silver-doped calcium phosphate bone cements with antibacterial properties, J Funct Biomater7(2) (2016), 10. doi:10.3390/jfb7020010.
14.
EwaldA.HöselD.PatelS.GroverL.M.BarraletJ.E. and GbureckU., Silver-doped calcium phosphate cements with antimicrobial activity, Acta Biomater7(11) (2011), 4064–4070. doi:10.1016/j.actbio.2011.06.049.
15.
JacquartS.SiadousR.Henocq-PigasseC.BareilleR.RoquesC.ReyC., Composition and properties of silver-containing calcium carbonate-calcium phosphate bone cement, J Mater Sci Mater Med24(12) (2013), 2665–2675. doi:10.1007/s10856-013-5014-2.
16.
KohaneD.S., Microparticles and nanoparticles for drug delivery, Biotechnol Bioeng96(2) (2007), 203–209. doi:10.1002/bit.21301.
17.
KhannaP.OngC.BayB.H. and BaegG.H., Nanotoxicity: An interplay of oxidative stress, inflammation and cell death, Nanomaterials5(3) (2005), 1163–1180. doi:10.3390/nano5031163.
18.
HorieM. and TabeiY., Role of oxidative stress in nanoparticles toxicity, Free Radic Res55(4) (2021), 331–342. doi:10.1080/10715762.2020.1859108.
19.
LaquerriereP.Grandjean-LaquerriereA.JallotE.BalossierG.FrayssinetP. and GuenounouM., Importance of hydroxyapatite particles characteristics on cytokines production by human monocytes in vitro, Biomaterials24(16) (2003), 2739–2747. doi:10.1016/s0142-9612(03)00089-9.
20.
Grandjean-LaquerriereA.LaquerriereP.GuenounouM.Laurent-MaquinD. and PhillipsT.M., Importance of the surface area ratio on cytokines production by human monocytes in vitro induced by various hydroxyapatite particles, Biomaterials26(15) (2005), 2361–2369. doi:10.1016/j.biomaterials.2004.07.036.
21.
LangeT.SchillingA.F.PetersF.HaagF.MorlockM.M.RuegerJ.M., Proinflammatory and osteoclastogenic effects of beta-tricalciumphosphate and hydroxyapatite particles on human mononuclear cells in vitro, Biomaterials30(29) (2009), 5312–5318. doi:10.1016/j.biomaterials.2009.06.023.
22.
LangeT.SchillingA.F.PetersF.MujasJ.WickleinD. and AmlingM., Size dependent induction of proinflammatory cytokines and cytotoxicity of particulate beta-tricalciumphosphate in vitro, Biomaterials32(17) (2011), 4067–4075. doi:10.1016/j.biomaterials.2011.02.039.
23.
VelardF.BrauxJ.AmedeeJ. and LaquerriereP., Inflammatory cell response to calcium phosphate biomaterial particles: an overview, Acta Biomater9(2) (2013), 4956–4963. doi:10.1016/j.actbio.2012.09.035.
24.
ChenZ.KleinT.MurrayR.Z.CrawfordR.ChangJ.WuC., Osteoimmunomodulation for the development of advanced bone biomaterials, Materials Today19 (2016), 304–321.
25.
TabeiY.SuginoS.EguchiK.TajikaM.AbeH.NakajimaY., Effect of calcium carbonate particle shape on phagocytosis and pro-inflammatory response in differentiated THP-1 macrophages, Biochem Biophys Res Commun490(2) (2017), 499–505. doi:10.1016/j.bbrc.2017.06.069.
26.
QingF.WangZ.HongY.LiuM.GuoB.LuoH., Selective effects of hydroxyapatite nanoparticles on osteosarcoma cells and osteoblast, J Mater Sci Mater Med23(9) (2012), 2245–2251. doi:10.1007/s10856-012-4703-6.
27.
WangL.ZhouG.LiuH.NiuX.HanJ.ZhengL., Nano-hydroxyapatite particles induce apoptosis on MC3T3-E1 cells and tissue cells in SD rats, Nanoscale4(9) (2012), 2894–2899. doi:10.1039/c2nr00044j.
28.
SunX.Y.ChenJ.Y.RaoC.Y. and OuyangJ.M., Size-dependent cytotoxicity of hydroxyapatite crystals on renal epithelial cells, Int J Nanomedicine15 (2020), 5043–5060. doi:10.2147/IJN.S232926.
29.
YazidM.D.AriffinS.H.Z.SenafiS.RazakM.A. and WahabR.M.A., Determination of the differentiation capacities of murines’ primary mononucleated cells and MC3T3-E1 cells, Cancer Cell Int10 (2010), 42. doi:10.1186/1475-2867-10-42.
30.
HaS.W.JangH.L.NamK.T. and BeckG.R., Nano-hydroxyapatite modulates osteoblast lineage commitment by stimulation of DNA methylation and regulation of gene expression, Biomaterials65 (2015), 32–42. doi:10.1016/j.biomaterials.2015.06.039.
31.
KimS.E.ChoiS.HongJ.Y.ShimK.S.KimT.H.ParkK., Accelerated osteogenic differentiation of MC3T3-E1 cells by lactoferrin-conjugated nanodiamonds through enhanced anti-oxidant and anti-inflammatory effects, Nanomaterials10(1) (2019), 50. doi:10.3390/nano10010050.
32.
ZhouH.Y.TakitaH.FujiwaraR.MizunoM. and KubokiY., Stimulation by bone sialoprotein of calcification in osteoblast-like MC3T3-E1 cells, Calcif Tissue Int56(5) (1995), 403–407. doi:10.1007/BF00301610.
33.
D’AlonzoR.C.KowalskiA.J.DenhardtD.T.NickolsG.A. and PartridgeN.C., Regulation of collagenase-3 and osteocalcin gene expression by collagen and osteopontin in differentiating MC3T3-E1 cells, J Biol Chem277(27) (2002), 24788–24798. doi:10.1074/jbc.M202604200.
34.
YangW.TaoC.CuiZ.LuoD.LeeI.S.YaoJ., Poly(acrylic acid)-regulated synthesis of rod-like calcium carbonate nanoparticles for inducing the osteogenic differentiation of MC3T3-E1 cells, Int J Mol Sci17(5) (2016), 639. doi:10.3390/ijms17050639.
35.
KomoriT.YagiH.NomuraS.YamaguchiA.SasakiK.DeguchiK., Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblast, Cell89(5) (1997), 755–764. doi:10.1016/s0092-8674(00)80258-5.
36.
NishioY.DongY.ParisM.O’KeefeR.J.SchwarzE.M. and DrissiH., Runx2-mediated regulation of the zinc finger osterix/Sp7 gene, Gene372 (2006), 62–70. doi:10.1016/j.gene.2005.12.022.
37.
NakashimaK.ZhouX.KunkelG.ZhangZ.DengJ.M.BehringerP.R., The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation, Cell108(1) (2002), 17–29. doi:10.1016/s0092-8674(01)00622-5.
38.
LeeM.H.KwonT.G.ParkH.S.WozneyJ.M. and RyooH.M., BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2, Biochem Biophys Res Commun309(3) (2003), 689–694. doi:10.1016/j.bbrc.2003.08.058.
39.
MatsubaraT.KidaK.YamaguchiA.HataK.IchidaF.MeguroH., BMP2 regulates osterix through Msx2 and Runx2 during osteoblast differentiation, J Biol Chem283(43) (2008), 29119–29125. doi:10.1074/jbc.M801774200.
40.
TantikanlayapornD.WichitP.SuksenK.SuksamrarnA. and PiyachaturawatP., Andrographolide modulates OPG/RANKL axis to promote osteoblastic differentiation in MC3T3-E1 cells and protects bone loss during estrogen deficiency in rats, Biomed Pharmacother131 (2020), 110763. doi:10.1016/j.biopha.2020.110763.
41.
KawashimaN.SuzukiN.YangG.OhiC.OkuharaS.Nakano-KawanishiH., Kinetics of RANKL, RANK and OPG expressions in experimentally induced rat periapical lesions, Oral Surg Oral Med Oral Pathol Oral Radiol Endod103(5) (2007), 707–711. doi:10.1016/j.tripleo.2006.11.036.
42.
BoyceB.F. and XingL., Functions of RANKL/RANK/OPG in bone modeling and remodeling, Arch Biochem Biophys473(2) (2008), 139–146. doi:10.1016/j.abb.2008.03.018.
43.
BoyceB.F. and XingL., The RANKL/RANK/OPG pathway, Curr Osteoporos Rep5(3) (2007), 98–104. doi:10.1007/s11914-007-0024-y.
