775
Views
10
CrossRef citations to date
0
Altmetric
Review

Nanostructured Titanium Implant Surface Facilitating Osseointegration from Protein Adsorption to Osteogenesis: The Example of TiO2 NTAs

, , , &
Pages 1865-1879 | Published online: 29 Apr 2022

References

  • Brånemark PI, Hansson BO, Adell R, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1–132.
  • Zhou Z, Shi Q, Wang J, et al. The unfavorable role of titanium particles released from dental implants. Nanotheranostics. 2021;5(3):321–332. doi:10.7150/ntno.56401
  • Quinn J, McFadden R, Chan CW, Carson L. Titanium for orthopedic applications: an overview of surface modification to improve biocompatibility and prevent bacterial biofilm formation. iScience. 2020;23(11):101745. doi:10.1016/j.isci.2020.101745
  • Nair LS, Laurencin CT. Biodegradable polymers as biomaterials. Prog Polym Sci. 2007;32(8–9):762–798. doi:10.1016/j.progpolymsci.2007.05.017
  • Eliaz N. Corrosion of metallic biomaterials: a review. Materials. 2019;12(3):407. doi:10.3390/ma12030407
  • Jager M, Jennissen HP, Dittrich F, Fischer A, Kohling HL. Antimicrobial and osseointegration properties of nanostructured titanium orthopaedic implants. Materials. 2017;10(11):1302. doi:10.3390/ma10111302
  • Kusakawa Y, Yoshida E, Hayakawa T. Protein adsorption to titanium and zirconia using a quartz crystal microbalance method. Biomed Res Int. 2017;2017:1521593. doi:10.1155/2017/1521593
  • Arabnejad S, Johnston B, Tanzer M, Pasini D. Fully porous 3D printed titanium femoral stem to reduce stress-shielding following total hip arthroplasty. J Orthop Res. 2017;35(8):1774–1783. doi:10.1002/jor.23445
  • Nair M, Elizabeth E. Applications of titania nanotubes in bone biology. J Nanosci Nanotechnol. 2015;15(2):939–955. doi:10.1166/jnn.2015.9771
  • Ahn TK, Lee DH, Kim TS, et al. Modification of titanium implant and titanium dioxide for bone tissue engineering. Adv Exp Med Biol. 2018;1077:355–368.
  • Awad NK, Edwards SL, Morsi YS. A review of TiO(2) NTs on Ti metal: electrochemical synthesis, functionalization and potential use as bone implants. Mater Sci Eng C Mater Biol Appl. 2017;76:1401–1412. doi:10.1016/j.msec.2017.02.150
  • Jafari S, Mahyad B, Hashemzadeh H, Janfaza S, Gholikhani T, Tayebi L. Biomedical applications of TiO(2) nanostructures: recent advances. Int J Nanomedicine. 2020;15:3447–3470. doi:10.2147/IJN.S249441
  • Chopra D, Gulati K, Ivanovski S. Understanding and optimizing the antibacterial functions of anodized nano-engineered titanium implants. Acta Biomater. 2021;127:80–101. doi:10.1016/j.actbio.2021.03.027
  • Barberi J, Spriano S. Titanium and protein adsorption: an overview of mechanisms and effects of surface features. Materials. 2021;14(7):1590. doi:10.3390/ma14071590
  • Li Y, Xiao Y, Liu C. The horizon of materiobiology: a perspective on material-guided cell behaviors and tissue engineering. Chem Rev. 2017;117(5):4376–4421. doi:10.1021/acs.chemrev.6b00654
  • Zhu Y, Liang H, Liu X, et al. Regulation of macrophage polarization through surface topography design to facilitate implant-to-bone osteointegration. Sci Adv. 2021;7(14):eabf6654. doi:10.1126/sciadv.abf6654
  • Yang D, Lü X, Hong Y, Xi T, Zhang D. The molecular mechanism of mediation of adsorbed serum proteins to endothelial cells adhesion and growth on biomaterials. Biomaterials. 2013;34(23):5747–5758. doi:10.1016/j.biomaterials.2013.04.028
  • Nobles KP, Janorkar AV, Williamson RS. Surface modifications to enhance osseointegration-resulting material properties and biological responses. J Biomed Mater Res B Appl Biomater. 2021;109(11):1909–1923. doi:10.1002/jbm.b.34835
  • Bauer S, Schmuki P, von der Mark K, Park J. Engineering biocompatible implant surfaces: part I: materials and surfaces. Prog Mater Sci. 2013;58(3):261–326.
  • Xu AT, Xie YW, Xu JG, Li J, Wang H, He FM. Effects of strontium-incorporated micro/nano rough titanium surfaces on osseointegration via modulating polarization of macrophages. Colloids Surf B Biointerfaces. 2021;207:111992. doi:10.1016/j.colsurfb.2021.111992
  • Ngandu Mpoyi E, Cantini M, Reynolds PM, Gadegaard N, Dalby MJ, Salmerón-Sánchez M. Protein adsorption as a key mediator in the nanotopographical control of cell behavior. ACS Nano. 2016;10(7):6638–6647. doi:10.1021/acsnano.6b01649
  • Kane R, Ma PX. Mimicking the nanostructure of bone matrix to regenerate bone. Mater Today. 2013;16(11):418–423. doi:10.1016/j.mattod.2013.11.001
  • Gittens RA, Olivares-Navarrete R, Schwartz Z, Boyan BD. Implant osseointegration and the role of microroughness and nanostructures: lessons for spine implants. Acta Biomater. 2014;10(8):3363–3371. doi:10.1016/j.actbio.2014.03.037
  • Davies JE. Mechanisms of endosseous integration. Int J Prosthodont. 1998;11(5):391–401.
  • Ma QL, Zhao LZ, Liu RR, et al. Improved implant osseointegration of a nanostructured titanium surface via mediation of macrophage polarization. Biomaterials. 2014;35(37):9853–9867. doi:10.1016/j.biomaterials.2014.08.025
  • Zhang L, Liao X, Fok A, Ning C, Ng P, Wang Y. Effect of crystalline phase changes in titania (TiO(2)) nanotube coatings on platelet adhesion and activation. Mater Sci Eng C Mater Biol Appl. 2018;82:91–101. doi:10.1016/j.msec.2017.08.024
  • Wang W, Zhao L, Ma Q, Wang Q, Chu PK, Zhang Y. The role of the Wnt/β-catenin pathway in the effect of implant topography on MG63 differentiation. Biomaterials. 2012;33(32):7993–8002. doi:10.1016/j.biomaterials.2012.07.064
  • Li Y, Wang S, Dong Y, et al. Effect of size and crystalline phase of TiO(2) nanotubes on cell behaviors: a high throughput study using gradient TiO(2) nanotubes. Bioact Mater. 2020;5(4):1062–1070. doi:10.1016/j.bioactmat.2020.07.005
  • von Wilmowsky C, Bauer S, Roedl S, Neukam FW, Schmuki P, Schlegel KA. The diameter of anodic TiO2 nanotubes affects bone formation and correlates with the bone morphogenetic protein-2 expression in vivo. Clin Oral Implants Res. 2012;23(3):359–366. doi:10.1111/j.1600-0501.2010.02139.x
  • Ma QL, Fang L, Jiang N, et al. Bone mesenchymal stem cell secretion of sRANKL/OPG/M-CSF in response to macrophage-mediated inflammatory response influences osteogenesis on nanostructured Ti surfaces. Biomaterials. 2018;154:234–247. doi:10.1016/j.biomaterials.2017.11.003
  • Gui N, Xu W, Myers DE, Shukla R, Tang HP, Qian M. The effect of ordered and partially ordered surface topography on bone cell responses: a review. Biomater Sci. 2018;6(2):250–264. doi:10.1039/C7BM01016H
  • Sjöström T, Dalby MJ, Hart A, Tare R, Oreffo RO, Su B. Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. Acta Biomater. 2009;5(5):1433–1441. doi:10.1016/j.actbio.2009.01.007
  • Sjostrom T, Lalev G, Mansell JP, Su B. Initial attachment and spreading of MG63 cells on nanopatterned titanium surfaces via through-mask anodization. Appl Surf Sci. 2011;257(10):4552–4558. doi:10.1016/j.apsusc.2010.11.064
  • Pan HA, Hung YC, Chiou JC, Tai SM, Chen HH, Huang GS. Nanosurface design of dental implants for improved cell growth and function. Nanotechnology. 2012;23(33):335703. doi:10.1088/0957-4484/23/33/335703
  • Silverwood RK, Fairhurst PG, Sjöström T, et al. Analysis of osteoclastogenesis/osteoblastogenesis on nanotopographical titania surfaces. Adv Healthc Mater. 2016;5(8):947–955. doi:10.1002/adhm.201500664
  • Sahlin H, Contreras R, Gaskill DF, Bjursten LM, Frangos JA. Anti-inflammatory properties of micropatterned titanium coatings. J Biomed Mater Res A. 2006;77(1):43–49. doi:10.1002/jbm.a.30642
  • Zhou J, Li B, Han Y, Zhao L. The osteogenic capacity of biomimetic hierarchical micropore/nanorod-patterned Sr-HA coatings with different interrod spacings. Nanomedicine. 2016;12(5):1161–1173. doi:10.1016/j.nano.2016.01.011
  • Zhang G, Yang Y, Shi J, et al. Near-infrared light II - assisted rapid biofilm elimination platform for bone implants at mild temperature. Biomaterials. 2021;269:120634. doi:10.1016/j.biomaterials.2020.120634
  • Yang H, Yu M, Wang R, et al. Hydrothermally grown TiO(2)-nanorods on surface mechanical attrition treated Ti: improved corrosion fatigue and osteogenesis. Acta Biomater. 2020;116:400–414. doi:10.1016/j.actbio.2020.09.005
  • Su EP, Justin DF, Pratt CR, et al. Effects of titanium nanotubes on the osseointegration, cell differentiation, mineralisation and antibacterial properties of orthopaedic implant surfaces. Bone Joint J. 2018;100-b(1 Supple A):9–16. doi:10.1302/0301-620X.100B1.BJJ-2017-0551.R1
  • Lu R, Wang C, Wang X, et al. Effects of hydrogenated TiO(2) nanotube arrays on protein adsorption and compatibility with osteoblast-like cells. Int J Nanomedicine. 2018;13:2037–2049. doi:10.2147/IJN.S155532
  • Bai L, Zhao Y, Chen P, et al. Targeting early healing phase with titania nanotube arrays on tunable diameters to accelerate bone regeneration and osseointegration. Small. 2021;17(4):e2006287. doi:10.1002/smll.202006287
  • Lee K, Mazare A, Schmuki P. One-dimensional titanium dioxide nanomaterials: nanotubes. Chem Rev. 2014;114(19):9385–9454. doi:10.1021/cr500061m
  • Necula MG, Mazare A, Ion RN, et al. Lateral spacing of TiO(2) nanotubes modulates osteoblast behavior. Materials. 2019;12(18):2956. doi:10.3390/ma12182956
  • Park J, Bauer S, Schlegel KA, Neukam FW, von der Mark K, Schmuki P. TiO2 nanotube surfaces: 15 nm–an optimal length scale of surface topography for cell adhesion and differentiation. Small. 2009;5(6):666–671. doi:10.1002/smll.200801476
  • Ahmed F, Pervez SA, Aljaafari A, et al. Fabrication of TiO(2)-nanotube-array-based supercapacitors. Micromachines. 2019;10(11):742. doi:10.3390/mi10110742
  • Spriano S, Yamaguchi S, Baino F, Ferraris S. A critical review of multifunctional titanium surfaces: new frontiers for improving osseointegration and host response, avoiding bacteria contamination. Acta Biomater. 2018;79:1–22. doi:10.1016/j.actbio.2018.08.013
  • Wang Q, Zhou P, Liu S, et al. Multi-scale surface treatments of titanium implants for rapid osseointegration: a review. Nanomaterials. 2020;10(6):1244.
  • Gong Z, Hu Y, Gao F, et al. Effects of diameters and crystals of titanium dioxide nanotube arrays on blood compatibility and endothelial cell behaviors. Colloids Surf B Biointerfaces. 2019;184:110521. doi:10.1016/j.colsurfb.2019.110521
  • Park J, Bauer S, von der Mark K, Schmuki P. Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett. 2007;7(6):1686–1691. doi:10.1021/nl070678d
  • Brammer KS, Oh S, Cobb CJ, Bjursten LM, Heyde Hvd JS, Jin S. Improved bone-forming functionality on diameter-controlled TiO2 nanotube surface. Acta Biomater. 2009;5(8):3215–3223. doi:10.1016/j.actbio.2009.05.008
  • Qi H, Shi M, Ni Y, et al. Size-confined effects of nanostructures on fibronectin-induced macrophage inflammation on titanium implants. Adv Healthc Mater. 2021;10:e2100994. doi:10.1002/adhm.202100994
  • Tong Z, Liu Y, Xia R, et al. F-actin regulates osteoblastic differentiation of mesenchymal stem cells on TiO2 nanotubes through MKL1 and YAP/TAZ. Nanoscale Res Lett. 2020;15(1):183. doi:10.1186/s11671-020-03415-9
  • Smeets R, Stadlinger B, Schwarz F, et al. Impact of dental implant surface modifications on osseointegration. Biomed Res Int. 2016;2016:6285620. doi:10.1155/2016/6285620
  • Skoog SA, Kumar G, Narayan RJ, Goering PL. Biological responses to immobilized microscale and nanoscale surface topographies. Pharmacol Ther. 2018;182:33–55. doi:10.1016/j.pharmthera.2017.07.009
  • Roach P, Eglin D, Rohde K, Perry CC. Modern biomaterials: a review - bulk properties and implications of surface modifications. J Mater Sci Mater Med. 2007;18(7):1263–1277. doi:10.1007/s10856-006-0064-3
  • Liu X, Lim JY, Donahue HJ, Dhurjati R, Mastro AM, Vogler EA. Influence of substratum surface chemistry/energy and topography on the human fetal osteoblastic cell line hFOB 1.19: phenotypic and genotypic responses observed in vitro. Biomaterials. 2007;28(31):4535–4550. doi:10.1016/j.biomaterials.2007.06.016
  • Lin DJ, Fuh LJ, Chen WC. Nano-morphology, crystallinity and surface potential of anatase on micro-arc oxidized titanium affect its protein adsorption, cell proliferation and cell differentiation. Mater Sci Eng C Mater Biol Appl. 2020;107:110204. doi:10.1016/j.msec.2019.110204
  • Hidalgo-Bastida LA, Cartmell SH. Mesenchymal stem cells, osteoblasts and extracellular matrix proteins: enhancing cell adhesion and differentiation for bone tissue engineering. Tissue Eng Part B Rev. 2010;16(4):405–412. doi:10.1089/ten.teb.2009.0714
  • Saran U, Gemini Piperni S, Chatterjee S. Role of angiogenesis in bone repair. Arch Biochem Biophys. 2014;561:109–117. doi:10.1016/j.abb.2014.07.006
  • McWhorter FY, Davis CT, Liu WF. Physical and mechanical regulation of macrophage phenotype and function. Cell Mol Life Sci. 2015;72(7):1303–1316. doi:10.1007/s00018-014-1796-8
  • Cai B, Lin D, Li Y, et al. N2-polarized neutrophils guide bone mesenchymal stem cell recruitment and initiate bone regeneration: a missing piece of the bone regeneration puzzle. Adv Sci. 2021;8(19):e2100584. doi:10.1002/advs.202100584
  • Murray PJ, Allen JE, Biswas SK, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14–20. doi:10.1016/j.immuni.2014.06.008
  • Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958–969. doi:10.1038/nri2448
  • Lee J, Byun H, Madhurakkat Perikamana SK, Lee S, Shin H. Current advances in immunomodulatory biomaterials for bone regeneration. Adv Healthc Mater. 2019;8(4):e1801106. doi:10.1002/adhm.201801106
  • Mahon OR, Browe DC, Gonzalez-Fernandez T, et al. Nano-particle mediated M2 macrophage polarization enhances bone formation and MSC osteogenesis in an IL-10 dependent manner. Biomaterials. 2020;239:119833. doi:10.1016/j.biomaterials.2020.119833
  • Dondossola E, Holzapfel BM, Alexander S, Filippini S, Hutmacher DW, Friedl P. Examination of the foreign body response to biomaterials by nonlinear intravital microscopy. Nat Biomed Eng. 2016;1:0007. doi:10.1038/s41551-016-0007
  • Hotchkiss KM, Clark NM, Olivares-Navarrete R. Macrophage response to hydrophilic biomaterials regulates MSC recruitment and T-helper cell populations. Biomaterials. 2018;182:202–215. doi:10.1016/j.biomaterials.2018.08.029
  • Nuhn H, Blanco CE, Desai TA. Nanoengineered stent surface to reduce in-stent restenosis in vivo. ACS Appl Mater Interfaces. 2017;9(23):19677–19686. doi:10.1021/acsami.7b04626
  • 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(2):258–267. doi:10.1002/1097-4636(200111)57:2<258::AID-JBM1166>3.0.CO;2-R
  • Szaba FM, Smiley ST. Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood. 2002;99(3):1053–1059. doi:10.1182/blood.V99.3.1053
  • Maciel J, Oliveira MI, Gonçalves RM, Barbosa MA. The effect of adsorbed fibronectin and osteopontin on macrophage adhesion and morphology on hydrophilic and hydrophobic model surfaces. Acta Biomater. 2012;8(10):3669–3677. doi:10.1016/j.actbio.2012.06.010
  • Gongadze E, Kabaso D, Bauer S, Park J, Schmuki P, Iglič A. Adhesion of osteoblasts to a vertically aligned TiO2 nanotube surface. Mini Rev Med Chem. 2013;13(2):194–200.
  • Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng. 2005;11(1–2):1–18. doi:10.1089/ten.2005.11.1
  • Zhang K, Xing J, Chen J, et al. A spatially varying charge model for regulating site-selective protein adsorption and cell behaviors. Biomater Sci. 2019;7(3):876–888. doi:10.1039/C8BM01158C
  • Rupp F, Gittens RA, Scheideler L, et al. A review on the wettability of dental implant surfaces I: theoretical and experimental aspects. Acta Biomater. 2014;10(7):2894–2906. doi:10.1016/j.actbio.2014.02.040
  • Khudhair D, Bhatti A, Li Y, et al. Anodization parameters influencing the morphology and electrical properties of TiO2 nanotubes for living cell interfacing and investigations. Mater Sci Eng C Mater Biol Appl. 2016;59:1125–1142. doi:10.1016/j.msec.2015.10.042
  • Shin DH, Shokuhfar T, Choi CK, Lee SH, Friedrich C. Wettability changes of TiO2 nanotube surfaces. Nanotechnology. 2011;22(31):315704. doi:10.1088/0957-4484/22/31/315704
  • Aiyelabegan HT, Sadroddiny E. Fundamentals of protein and cell interactions in biomaterials. Biomed Pharmacother. 2017;88:956–970. doi:10.1016/j.biopha.2017.01.136
  • Visalakshan RM, MacGregor MN, Sasidharan S, et al. Biomaterial surface hydrophobicity-mediated serum protein adsorption and immune responses. ACS Appl Mater Interfaces. 2019;11(31):27615–27623. doi:10.1021/acsami.9b09900
  • Abitorabi MA, Pachynski RK, Ferrando RE, Tidswell M, Erle DJ. Presentation of integrins on leukocyte microvilli: a role for the extracellular domain in determining membrane localization. J Cell Biol. 1997;139(2):563–571. doi:10.1083/jcb.139.2.563
  • Wu S, Zhang D, Bai J, et al. Adsorption of serum proteins on titania nanotubes and its role on regulating adhesion and migration of mesenchymal stem cells. J Biomed Mater Res A. 2020;108(11):2305–2318. doi:10.1002/jbm.a.36987
  • Smith SA, Travers RJ, Morrissey JH. How it all starts: initiation of the clotting cascade. Crit Rev Biochem Mol Biol. 2015;50(4):326–336. doi:10.3109/10409238.2015.1050550
  • Huang Q, Yang Y, Zheng D, et al. Effect of construction of TiO(2) nanotubes on platelet behaviors: structure-property relationships. Acta Biomater. 2017;51:505–512. doi:10.1016/j.actbio.2017.01.044
  • Anitua E, Sánchez M, Nurden AT, Nurden P, Orive G, Andía I. New insights into and novel applications for platelet-rich fibrin therapies. Trends Biotechnol. 2006;24(5):227–234. doi:10.1016/j.tibtech.2006.02.010
  • Herter JM, Rossaint J, Zarbock A. Platelets in inflammation and immunity. J Thromb Haemost. 2014;12(11):1764–1775. doi:10.1111/jth.12730
  • Burkhardt MA, Gerber I, Moshfegh C, et al. Clot-entrapped blood cells in synergy with human mesenchymal stem cells create a pro-angiogenic healing response. Biomater Sci. 2017;5(10):2009–2023. doi:10.1039/C7BM00276A
  • Alfarsi MA, Hamlet SM, Ivanovski S. The effect of platelet proteins released in response to titanium implant surfaces on macrophage pro-inflammatory cytokine gene expression. Clin Implant Dent Relat Res. 2015;17(6):1036–1047. doi:10.1111/cid.12231
  • Chen Z, Klein T, Murray RZ, et al. Osteoimmunomodulation for the development of advanced bone biomaterials. Mater Today. 2016;19(6):304–321. doi:10.1016/j.mattod.2015.11.004
  • Yao Q, Liu J, Zhang Z, et al. Peroxisome proliferator-activated receptor γ (PPARγ) induces the gene expression of integrin α(V)β(5) to promote macrophage M2 polarization. J Biol Chem. 2018;293(43):16572–16582. doi:10.1074/jbc.RA118.003161
  • Xu Y, Cui K, Li J, et al. Melatonin attenuates choroidal neovascularization by regulating macrophage/microglia polarization via inhibition of RhoA/ROCK signaling pathway. J Pineal Res. 2020;69(1):e12660. doi:10.1111/jpi.12660
  • Yu WP, Ding JL, Liu XL, et al. Titanium dioxide nanotubes promote M2 polarization by inhibiting macrophage glycolysis and ultimately accelerate endothelialization. Immun Inflamm Dis. 2021;9:746–757. doi:10.1002/iid3.429
  • Zhu L, Zhao Q, Yang T, Ding W, Zhao Y. Cellular metabolism and macrophage functional polarization. Int Rev Immunol. 2015;34(1):82–100. doi:10.3109/08830185.2014.969421
  • Deng RH, Zou MZ, Zheng D, et al. Nanoparticles from cuttlefish ink inhibit tumor growth by synergizing immunotherapy and photothermal therapy. ACS Nano. 2019;13(8):8618–8629. doi:10.1021/acsnano.9b02993
  • Zhou H, Coveney AP, Wu M, et al. Activation of both TLR and NOD signaling confers host innate immunity-mediated protection against microbial infection. Front Immunol. 2018;9:3082. doi:10.3389/fimmu.2018.03082
  • Wu TM, Nan FH, Chen KC, Wu YS. Sarcodia suieae acetyl-xylogalactan regulate RAW 264.7 macrophage NF-kappa B activation and IL-1 beta cytokine production in macrophage polarization. Sci Rep. 2019;9(1):19627. doi:10.1038/s41598-019-56246-9
  • Chen D, Xie J, Fiskesund R, et al. Chloroquine modulates antitumor immune response by resetting tumor-associated macrophages toward M1 phenotype. Nat Commun. 2018;9(1):873. doi:10.1038/s41467-018-03225-9
  • Singhatanadgit W, Toso M, Pratheepsawangwong B, Pimpin A, Srituravanich W. Titanium dioxide nanotubes of defined diameter enhance mesenchymal stem cell proliferation via JNK- and ERK-dependent up-regulation of fibroblast growth factor-2 by T lymphocytes. J Biomater Appl. 2019;33(7):997–1010. doi:10.1177/0885328218816565
  • Adusei KM, Ngo TB, Sadtler K. T lymphocytes as critical mediators in tissue regeneration, fibrosis, and the foreign body response. Acta Biomater. 2021;133:17–33. doi:10.1016/j.actbio.2021.04.023
  • Paavolainen O, Peuhu E. Integrin-mediated adhesion and mechanosensing in the mammary gland. Semin Cell Dev Biol. 2021;114:113–125. doi:10.1016/j.semcdb.2020.10.010
  • Boettiger D. Mechanical control of integrin-mediated adhesion and signaling. Curr Opin Cell Biol. 2012;24(5):592–599. doi:10.1016/j.ceb.2012.07.002
  • Sun Z, Costell M, Fässler R. Integrin activation by talin, kindlin and mechanical forces. Nat Cell Biol. 2019;21(1):25–31. doi:10.1038/s41556-018-0234-9
  • Khrunyk YY, Belikov SV, Tsurkan MV, et al. Surface-dependent osteoblasts response to TiO(2) nanotubes of different crystallinity. Nanomaterials. 2020;10(2):320. doi:10.3390/nano10020320
  • Xu Z, Lai Y, Wu D, et al. Increased mesenchymal stem cell response and decreased staphylococcus aureus adhesion on titania nanotubes without pharmaceuticals. Biomed Res Int. 2015;2015:172898. doi:10.1155/2015/172898
  • Mu P, Li Y, Zhang Y, et al. High-throughput screening of rat mesenchymal stem cell behavior on gradient TiO(2) nanotubes. ACS Biomater Sci Eng. 2018;4(8):2804–2814. doi:10.1021/acsbiomaterials.8b00488
  • Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005;6(1):56–68. doi:10.1038/nrm1549
  • Chen S, Guo Y, Liu R, et al. Tuning surface properties of bone biomaterials to manipulate osteoblastic cell adhesion and the signaling pathways for the enhancement of early osseointegration. Colloids Surf B Biointerfaces. 2018;164:58–69. doi:10.1016/j.colsurfb.2018.01.022
  • Fischer RS, Lam PY, Huttenlocher A, Waterman CM. Filopodia and focal adhesions: an integrated system driving branching morphogenesis in neuronal pathfinding and angiogenesis. Dev Biol. 2019;451(1):86–95. doi:10.1016/j.ydbio.2018.08.015
  • Dai J, Rabie AB. VEGF: an essential mediator of both angiogenesis and endochondral ossification. J Dent Res. 2007;86(10):937–950. doi:10.1177/154405910708601006
  • Raines AL, Olivares-Navarrete R, Wieland M, Cochran DL, Schwartz Z, Boyan BD. Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials. 2010;31(18):4909–4917. doi:10.1016/j.biomaterials.2010.02.071
  • Lee PP, Cerchiari A, Desai TA. Nitinol-based nanotubular coatings for the modulation of human vascular cell function. Nano Lett. 2014;14(9):5021–5028. doi:10.1021/nl501523v
  • Peng L, Eltgroth ML, LaTempa TJ, Grimes CA, Desai TA. The effect of TiO2 nanotubes on endothelial function and smooth muscle proliferation. Biomaterials. 2009;30(7):1268–1272. doi:10.1016/j.biomaterials.2008.11.012
  • Brammer KS, Oh S, Gallagher JO, Jin S. Enhanced cellular mobility guided by TiO2 nanotube surfaces. Nano Lett. 2008;8(3):786–793. doi:10.1021/nl072572o
  • Beltrán-Partida E, Valdéz-Salas B, Moreno-Ulloa A, et al. Improved in vitro angiogenic behavior on anodized titanium dioxide nanotubes. J Nanobiotechnology. 2017;15(1):10. doi:10.1186/s12951-017-0247-8
  • Shi B, Andrukhov O, Berner S, Schedle A, Rausch-Fan X. The angiogenic behaviors of human umbilical vein endothelial cells (HUVEC) in co-culture with osteoblast-like cells (MG-63) on different titanium surfaces. Dent Mater. 2014;30(8):839–847. doi:10.1016/j.dental.2014.05.005
  • Peng Z, Ni J, Zheng K, et al. Dual effects and mechanism of TiO2 nanotube arrays in reducing bacterial colonization and enhancing C3H10T1/2 cell adhesion. Int J Nanomedicine. 2013;8:3093–3105. doi:10.2147/IJN.S48084
  • Oh S, Daraio C, Chen LH, Pisanic TR, Fiñones RR, Jin S. Significantly accelerated osteoblast cell growth on aligned TiO2 nanotubes. J Biomed Mater Res A. 2006;78(1):97–103. doi:10.1002/jbm.a.30722
  • Oh S, Brammer KS, Li YS, et al. Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci U S A. 2009;106(7):2130–2135. doi:10.1073/pnas.0813200106
  • Eyckmans J, Luyten FP. Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng. 2006;12(8):2203–2213. doi:10.1089/ten.2006.12.2203
  • Zhang Y, Polman M, Mohammad AF, et al. Species-independent stimulation of osteogenic differentiation induced by osteoclasts. Biochem Biophys Res Commun. 2022;606:149–155. doi:10.1016/j.bbrc.2022.03.115
  • Caetano-Lopes J, Canhão H, Fonseca JE. Osteoimmunology–the hidden immune regulation of bone. Autoimmun Rev. 2009;8(3):250–255. doi:10.1016/j.autrev.2008.07.038