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Microarc oxidation surface of titanium implants promote osteogenic differentiation by activating ERK1/2-miR-1827-Osterix

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Abstract

There has been a constant requirement from the clinic to develop biomedical titanium (Ti) implants with high osteogenic ability. In this study, we clarified a novel mechanism of how MAO (microarc oxidation) coating of Ti implants facilitates osteogenic differentiation of human bone marrow mesenchymal stem cells (hB-MSCs) by activating ERK1/2-miR-1827-Osterix signaling pathway in vitro. MAO surface of titanium implant was more favorable to promote osteogenic differentiation than SLA and AOS coating. Besides, titanium implants regulated hB-MSCs osteogenesis through the p38 MAPK pathway and ERK1/2 might be the most efficient target. Furthermore, MAO coating induced osteogenic differentiation though ERK1/2-miR-1827 pathway. Finally, we verified miR-1827 regulated osteogenic differentiation partially through Osterix. Our study reveals novel insights that MAO surface of titanium implant is a prior choice for biomedical trial and for its use in periprosthetic osteolysis (PIO) treatment in an evidence-based rationale.

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Data availability statement

The authors declare all of the data are available.

References

  • Baranowski A, Klein A, Ritz U, Ackermann A, Anthonissen J, Kaufmann KB, Brendel C, Götz H, Rommens PM, Hofmann A (2016) Surface functionalization of orthopedic titanium implants with bone sialoprotein. PLoS One 11(4):e0153978

    PubMed  PubMed Central  Google Scholar 

  • Beutner R et al (2010) Biological nano-functionalization of titanium-based biomaterial surfaces: a flexible toolbox. J R Soc Interface 7(Suppl 1):S93–S105

    CAS  PubMed  Google Scholar 

  • Boyan BD, Cheng A, Olivares-Navarrete R, Schwartz Z (2016) Implant surface design regulates mesenchymal stem cell differentiation and maturation. Adv Dent Res 28(1):10–17

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen D, Guo Y, Mao X, Zhang X (2012) Inhibition of p38 mitogen-activated protein kinase down-regulates the inflammatory osteolysis response to titanium particles in a murine osteolysis model. Inflammation 35(6):1798–1806

    CAS  PubMed  Google Scholar 

  • Chen D, Li Y, Guo F, Lu Z, Hei C, Li P, Jin Q (2015) Protective effect of p38 MAPK inhibitor on wear debris-induced inflammatory osteolysis through downregulating RANK/RANKL in a mouse model. Genet Mol Res 14(1):40–52

    CAS  PubMed  Google Scholar 

  • Chen M, Chen PM, Dong QR, Huang Q, She C, Xu W (2014) p38 signaling in titanium particle-induced MMP-2 secretion and activation in differentiating MC3T3-E1 cells. J Biomed Mater Res A 102(8):2824–2832

    PubMed  Google Scholar 

  • Chen W et al (2018) Multilayered coating of titanium implants promotes coupled osteogenesis and angiogenesis in vitro and in vivo. Acta Biomater 74:489–504

    CAS  PubMed  Google Scholar 

  • Cho SA, Park KT (2003) The removal torque of titanium screw inserted in rabbit tibia treated by dual acid etching. Biomaterials 24(20):3611–3617

    CAS  PubMed  Google Scholar 

  • Coelho PG et al (2009) Basic research methods and current trends of dental implant surfaces. J Biomed Mater Res B Appl Biomater 88(2):579–596

    PubMed  Google Scholar 

  • Cohen, D.M. and C.S. Chen, Mechanical control of stem cell differentiation, in StemBook. 2008: Cambridge (MA)

  • Hata K, Ikebe K, Wada M, Nokubi T (2007) Osteoblast response to titanium regulates transcriptional activity of Runx2 through MAPK pathway. J Biomed Mater Res A 81(2):446–452

    PubMed  Google Scholar 

  • He M, Zhang Z, Zheng D, Ding N, Liu Y (2014) Effect of sandblasting on surface roughness of zirconia-based ceramics and shear bond strength of veneering porcelain. Dent Mater J 33(6):778–785

    CAS  PubMed  Google Scholar 

  • Ho CS, Noor SM, Nagoor NH (2018) MiR-378 and MiR-1827 regulate tumor invasion, migration and angiogenesis in human lung adenocarcinoma by targeting RBX1 and CRKL. Respectively J Cancer 9(2):331–345

  • Hotchkiss KM, Reddy GB, Hyzy SL, Schwartz Z, Boyan BD, Olivares-Navarrete R (2016) Titanium surface characteristics, including topography and wettability, alter macrophage activation. Acta Biomater 31:425–434

    CAS  PubMed  Google Scholar 

  • Ishizawa H, Ogino M (1995) Formation and characterization of anodic titanium oxide films containing Ca and P. J Biomed Mater Res 29(1):65–72

    CAS  PubMed  Google Scholar 

  • Jing D et al (2016) Pulsed electromagnetic fields promote osteogenesis and osseointegration of porous titanium implants in bone defect repair through a Wnt/beta-catenin signaling-associated mechanism. Sci Rep 6:32045

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kern S, Eichler H, Stoeve J, Klüter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24(5):1294–1301

    CAS  PubMed  Google Scholar 

  • Kim HW, Koh YH, Li LH, Lee S, Kim HE (2004) Hydroxyapatite coating on titanium substrate with titania buffer layer processed by sol-gel method. Biomaterials 25(13):2533–2538

    CAS  PubMed  Google Scholar 

  • Li X et al (2018) Accelerated and enhanced osteointegration of MAO-treated implants: histological and histomorphometric evaluation in a rabbit model. Int J Oral Sci 10(2):11

    PubMed  PubMed Central  Google Scholar 

  • Lotz EM, Berger MB, Schwartz Z, Boyan BD (2018) Regulation of osteoclasts by osteoblast lineage cells depends on titanium implant surface properties. Acta Biomater 68:296–307

    CAS  PubMed  Google Scholar 

  • Mahla RS (2016) Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol 2016:6940283

    PubMed  PubMed Central  Google Scholar 

  • Makihira S et al (2007) Titanium surface roughness accelerates RANKL-dependent differentiation in the osteoclast precursor cell line, RAW264.7. Dent Mater J 26(5):739–745

    CAS  PubMed  Google Scholar 

  • Orsini E et al (2012) Early healing events around titanium implant devices with different surface microtopography: a pilot study in an in vivo rabbit model. Sci World J 2012:349842

    Google Scholar 

  • Peng L, Jia Z, Yin X, Zhang X, Liu Y, Chen P, Ma K, Zhou C (2008) Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue. Stem Cells Dev 17(4):761–773

    CAS  PubMed  Google Scholar 

  • Raines AL, Olivares-Navarrete R, Wieland M, Cochran DL, Schwartz Z, Boyan BD (2010) Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials 31(18):4909–4917

    CAS  PubMed  PubMed Central  Google Scholar 

  • Samanipour F, Bayati MR, Golestani-Fard F, Zargar HR, Troczynski T, Mirhabibi AR (2011) An innovative technique to simply fabricate ZrO(2)-HA-TiO(2) nanostructured layers. Colloids Surf B: Biointerfaces 86(1):14–20

    CAS  PubMed  Google Scholar 

  • Shen MJ, Wang GG, Wang YZ, Xie J, Ding X (2018) Nell-1 enhances osteogenic differentiation of pre-osteoblasts on titanium surfaces via the MAPK-ERK signaling pathway. Cell Physiol Biochem 50(4):1522–1534

    CAS  PubMed  Google Scholar 

  • Silva HF, Abuna RPF, Lopes HB, Francischini MS, de Oliveira PT, Rosa AL, Beloti MM (2017) Participation of extracellular signal-regulated kinases 1/2 in osteoblast and adipocyte differentiation of mesenchymal stem cells grown on titanium surfaces. Eur J Oral Sci 125(5):355–360

    CAS  PubMed  Google Scholar 

  • Spriano S, Yamaguchi S, Baino F, Ferraris S (2018) A critical review of multifunctional titanium surfaces: new frontiers for improving osseointegration and host response, avoiding bacteria contamination. Acta Biomater 79:1–22

    CAS  PubMed  Google Scholar 

  • Stanko P et al (2014) Comparison of human mesenchymal stem cells derived from dental pulp, bone marrow, adipose tissue, and umbilical cord tissue by gene expression. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 158(3):373–377

    PubMed  Google Scholar 

  • Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79(1):143–180

    CAS  PubMed  Google Scholar 

  • Wu K, Song W, Zhao L, Liu M, Yan J, Andersen MØ, Kjems J, Gao S, Zhang Y (2013) MicroRNA functionalized microporous titanium oxide surface by lyophilization with enhanced osteogenic activity. ACS Appl Mater Interfaces 5(7):2733–2744

    CAS  PubMed  Google Scholar 

  • Yue G, Song W, Xu S, Sun Y, Wang Z (2019) Role of ILK/p38 pathway in mediating the enhanced osteogenic differentiation of bone marrow mesenchymal stem cells on amorphous carbon coating. Biomater Sci 7(3):975–984

    CAS  PubMed  Google Scholar 

  • Yun HS, Zhou H, Honma I (2004) Synthesis of self-standing mesoporous nanocrystalline titania-phosphorus oxide composite films. Chem Commun (Camb) 24:2836–2837

    Google Scholar 

  • Zeng RC, Cui LY, Jiang K, Liu R, Zhao BD, Zheng YF (2016) In vitro corrosion and cytocompatibility of a microarc oxidation coating and poly(L-lactic acid) composite coating on Mg-1Li-1Ca alloy for orthopedic implants. ACS Appl Mater Interfaces 8(15):10014–10028

    CAS  PubMed  Google Scholar 

  • Zhang C, Zhang Y, Feng Z, Zhang F, Liu Z, Sun X, Ruan M, Liu M, Jin S (2018) Therapeutic effect of dental pulp stem cell transplantation on a rat model of radioactivity-induced esophageal injury. Cell Death Dis 9(7):738

    PubMed  PubMed Central  Google Scholar 

  • Zhang W, Cao H, Zhang X, Li G, Chang Q, Zhao J, Qiao Y, Ding X, Yang G, Liu X, Jiang X (2016) A strontium-incorporated nanoporous titanium implant surface for rapid osseointegration. Nanoscale 8(9):5291–5301

    CAS  PubMed  Google Scholar 

  • Zhu S et al (2017) miR-1827 inhibits osteogenic differentiation by targeting IGF1 in MSMSCs. Sci Rep 7:46136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zomorodian A, Garcia MP, Moura e Silva T, Fernandes JC, Fernandes MH, Montemor MF (2013) Corrosion resistance of a composite polymeric coating applied on biodegradable AZ31 magnesium alloy. Acta Biomater 9(10):8660–8670

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank The First Affiliated Hospital, Fujian Medical University, for the capital and equipment support.

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Correspondence to Bin Shi.

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The authors declare that they have no competing interests.

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Editor: Tetsuji Okamoto

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Liu, L., Zeng, D., Chen, Y. et al. Microarc oxidation surface of titanium implants promote osteogenic differentiation by activating ERK1/2-miR-1827-Osterix. In Vitro Cell.Dev.Biol.-Animal 56, 296–306 (2020). https://doi.org/10.1007/s11626-020-00444-7

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  • DOI: https://doi.org/10.1007/s11626-020-00444-7

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