Research progress on the effect of surface charge of biomaterials on bone formation_Journal of Biomedical Engineering

Authors：

WANG Shaotai ^1,3 , SONG Dongsheng ^1,3 ,  QIAO Chunyan ^2,3

1. Department of Orthodontics, Hospital of Stomatology, Jilin University, Changchun 130021, P.R.China;
2. Department of Pathology, Hospital of Stomatology, Jilin University, Changchun 130021, P.R.China;
3. Jilin Provincial Key Laboratory of Tooth Development and Bone Remodeling, Changchun 130021, P.R.China;

Corresponding author：

Keywords：

biomaterials; bone defects; surface charge; surface wettability; surface composition; immune regulation

DOI：

10.7507/1001-5515.202104022

Video：

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Abstract Full text Figures/Tables Video References Cited by

With the continuous progress of materials science and biology, the significance of biomaterials with dual characteristics of materials science and biology is keeping on increasing. Nowadays, more and more biomaterials are being used in tissue engineering, pharmaceutical engineering and regenerative medicine. In repairing bone defects caused by trauma, tumor invasion, congenital malformation and other factors, a variety of biomaterials have emerged with different characteristics, such as surface charge, surface wettability, surface composition, immune regulation and so on, leading to significant differences in repair effects. This paper mainly discusses the influence of surface charge of biomaterials on bone formation and the methods of introducing surface charge, aiming to promote bone formation by changing the charge distribution on the surface of the biomaterials to serve the clinical treatment better.

Citation： WANG Shaotai, SONG Dongsheng, QIAO Chunyan. Research progress on the effect of surface charge of biomaterials on bone formation. Journal of Biomedical Engineering, 2021, 38(6): 1229-1234. doi: 10.7507/1001-5515.202104022 Copy

1.	Andi M A, Sengo K, Satoshi O. Effect of heat treatments on wettability of nacre. Mater Sci Forum, 2020, 4808: 86-90.
2.	Zhang R, Liu X, Xiong Z, et al. The immunomodulatory effects of Zn-incorporated micro/nanostructured coating in inducing osteogenesis. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 1123-1130.
3.	Sharma R I, Snedeker J G. Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes. PLoS One, 2012, 7(2): e31504.
4.	Yang C, Delrio F W, Ma H, et al. Spatially patterned matrix elasticity directs stem cell fate. Proc Natl Acad Sci U S A, 2016, 113(31): E4439-E4445.
5.	Yang C, Tibbitt M W, Basta L, et al. Mechanical memory and dosing influence stem cell fate. Nat Mater, 2014, 13(6): 645-652.
6.	Lin D J, Fuh L J, Chen W C. 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.
7.	Liene P, Edijs F, Karlis A G, et al. Functionalizing surface electrical potential of hydroxyapatite coatings. Adv Sci Technol, 2017, 4475(204): 12-17.
8.	Agour M, Abdal-Hay A, Hassan M K, et al. Alkali-treated titanium coated with a polyurethane, magnesium and hydroxyapatite composite for bone tissue engineering. Nanomaterials, 2021, 11(5): 1129.
9.	Isoshima K, Ueno T, Arai Y, et al. The change of surface charge by lithium ion coating enhances protein adsorption on titanium. J Mech Behav Biomed Mater, 2019, 100: 103393.
10.	Ribeiro C, Panadero J A, Sencadas V, et al. Fibronectin adsorption and cell response on electroactive poly(vinylidene fluoride) films. Biomed Mater, 2012, 7(3): 035004.
11.	Long X, Wang X, Yao L, et al. Graphene/Si-promoted osteogenic differentiation of BMSCs through light illumination. ACS Appl Mater Interfaces, 2019, 11(47): 43857-43864.
12.	Petecchia L, Sbrana F, Utzeri R, et al. Electro-magnetic field promotes osteogenic differentiation of BM-hMSCs through a selective action on Ca(2+)-related mechanisms. Sci Rep, 2015, 5: 13856.
13.	Nakamura M, Nagai A, Yamashita K. Surface electric fields of apatite electret promote osteoblastic responses. Key Eng Mater, 2013, 2050: 357-360.
14.	Zhou Z, Li W, He T, et al. Polarization of an electroactive functional film on titanium for inducing osteogenic differentiation. Sci Rep, 2016, 6: 35512.
15.	Carville N C, Collins L, Manzo M, et al. Biocompatibility of ferroelectric lithium niobate and the influence of polarization charge on osteoblast proliferation and function. J Biomed Mater Res A, 2015, 103(8): 2540-2548.
16.	Ding X, Xu S, Li S, et al. Biological effects of titanium surface charge with a focus on protein adsorption. ACS Omega, 2020, 5(40): 25617-25624.
17.	Lawton J M, Habib M, MA B, et al. The effect of cationically-modified phosphorylcholine polymers on human osteoblasts in vitro and their effect on bone formation in vivo. J Mater Sci Mater Med, 2017, 28(9): 144.
18.	Casagrande S, Tiribuzi R, Cassetti E, et al. Biodegradable composite porous poly(dl-lactide-co-glycolide) scaffold supports mesenchymal stem cell differentiation and calcium phosphate deposition. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 219-229.
19.	Wang Z, Dong L, Han L, et al. Self-assembled biodegradable nanoparticles and polysaccharides as biomimetic ECM nanostructures for the synergistic effect of RGD and BMP-2 on bone formation. Sci Rep, 2016, 6: 25090.
20.	Aguilar A, Zein N, Harmouch E, et al. Application of chitosan in bone and dental engineering. Molecules, 2019, 24(16): 3009.
21.	Lin J H, Chang H Y, Kao W L, et al. Effect of surface potential on extracellular matrix protein adsorption. Langmuir, 2014, 30(34): 10328-10335.
22.	Koch F, Wolff A, Mathes S, et al. Amino acid composition of nanofibrillar self-assembling peptide hydrogels affects responses of periodontal tissue cells in vitro. Int J Nanomedicine, 2018, 13: 6717-6733.
23.	Marchesano V, Gennari O, Mecozzi L, et al. Effects of Lithium niobate polarization on cell adhesion and morphology. ACS Appl Mater Interfaces, 2015, 7(32): 18113-18119.
24.	Griffanti G, James-Bhasin M, Donelli I, et al. Functionalization of silk fibroin through anionic fibroin derived polypeptides. Biomed Mater, 2018, 14(1): 015006.
25.	Griffanti G, Jiang W, Nazhat S N. Bioinspired mineralization of a functionalized injectable dense collagen hydrogel through silk sericin incorporation. Biomater Sci, 2019, 7(3): 1064-1077.
26.	Kim H D, Lee E A, An Y H, et al. Chondroitin sulfate-based biomineralizing surface hydrogels for bone tissue engineering. ACS Appl Mater Interfaces, 2017, 9(26): 21639-21650.
27.	Tan F, Liu J, Liu M, et al. Charge density is more important than charge polarity in enhancing osteoblast-like cell attachment on poly(ethylene glycol)-diacrylate hydrogel. Mater Sci Eng C Mater Biol Appl, 2017, 76: 330-339.
28.	Dadsetan M, Pumberger M, Casper M E, et al. The effects of fixed electrical charge on chondrocyte behavior. Acta Biomater, 2011, 7(5): 2080-2090.
29.	Olthof M G L, Kempen D H R, Liu X, et al. Effect of biomaterial electrical charge on bone morphogenetic protein-2-induced in vivo bone formation. Tissue Eng Part A, 2019, 25(13/14): 1037-1052.
30.	De Luca I, Di Salle A, Alessio N, et al. Positively charged polymers modulate the fate of human mesenchymal stromal cells via ephrinB2/EphB4 signaling. Stem Cell Res, 2016, 17(2): 248-255.
31.	Tiwari J N, Seo Y K, Yoon T, et al. Accelerated bone regeneration by two-photon photoactivated carbon nitride nanosheets. ACS Nano, 2017, 11(1): 742-751.
32.	Yu P, Ning C, Zhang Y, et al. Bone-inspired spatially specific piezoelectricity induces bone regeneration. Theranostics, 2017, 7(13): 3387-3397.
33.	Tang B, Zhang B, Zhuang J, et al. Surface potential-governed cellular osteogenic differentiation on ferroelectric polyvinylidene fluoride trifluoroethylene films. Acta Biomater, 2018, 74: 291-301.
34.	Xu C, Wang S, Liu L, et al. Manipulating mesenchymal stem cells differentiation under sinusoidal electromagnetic fields using intracellular superparamagnetic nanoparticles. J Biomed Nanotechnol, 2019, 15(2): 301-310.
35.	Jiang Pengfei, Zhang Yixian, Zhu Chaonan, et al. Fe₃O₄/BSA particles induce osteogenic differentiation of mesenchymal stem cells under static magnetic field. Acta Biomater, 2016, 46: 141-150.
36.	Love M R, Palee S, Chattipakorn S C, et al. Effects of electrical stimulation on cell proliferation and apoptosis. J Cell Physiol, 2018, 233(3): 1860-1876.
37.	O'Hearn S F, Ackerman B J, Mower M M. Paced monophasic and biphasic waveforms alter transmembrane potentials and metabolism of human fibroblasts. Biochem Biophys Rep, 2016, 8: 249-253.
38.	Wang Jing, Tian Lingling, Chen Nuan, et al. The cellular response of nerve cells on poly-L-lysine coated PLGA-MWCNTs aligned nanofibers under electrical stimulation. Mater Sci Eng C, 2018, 91: 715-726.
39.	Zhu B, Li Y, Huang F, et al. Promotion of the osteogenic activity of an antibacterial polyaniline coating by electrical stimulation. Biomater Sci, 2019, 7(11): 4730-4737.
40.	Jing W, Huang Y, Wei P, et al. Roles of electrical stimulation in promoting osteogenic differentiation of BMSCs on conductive fibers. J Biomed Mater Res A, 2019, 107(7): 1443-1454.
41.	Li J, Liu X, Crook J M, et al. Electrical stimulation-induced osteogenesis of human adipose derived stem cells using a conductive graphene-cellulose scaffold. Mater Sci Eng C Mater Biol Appl, 2020, 107: 110312.
42.	Zhao Y Q, Meng L, Zhang K, et al. Ultra-small nanodots coated with oligopeptides providing highly negative charges to enhance osteogenic differentiation of hBMSCs better than osteogenic induction medium. Chin Chem Lett, 2021, 32(1): 266-270.
43.	Calabrese R, Raia N, Huang W, et al. Silk-ionomer and silk-tropoelastin hydrogels as charged three-dimensional culture platforms for the regulation of hMSC response. J Tissue Eng Regen Med, 2017, 11(9): 2549-2564.
44.	Saghiri M A, Asatourian A, Garcia-Godoy F, et al. The role of angiogenesis in implant dentistry part I: review of titanium alloys, surface characteristics and treatments. Med Oral Patol Oral Cir Bucal, 2016, 21(4): e514-e525.
45.	Hao L, Fu X, Li T, et al. Surface chemistry from wettability and charge for the control of mesenchymal stem cell fate through self-assembled monolayers. Colloids Surf B Biointerfaces, 2016, 148: 549-556.
46.	Sasayama S, Hara T, Tanaka T, et al. Osteogenesis of multipotent progenitor cells using the epigallocatechin gallate-modified gelatin sponge scaffold in the rat congenital cleft-jaw model. Int J Mol Sci, 2018, 19(12): 3803.
47.	Cámara-Torres M, Sinha R, Scopece P, et al. Tuning cell behavior on 3D scaffolds fabricated by atmospheric plasma-assisted additive manufacturing. ACS Appl Mater Interfaces, 2021, 13(3): 3631-3644.
48.	Ritz U, Eberhardt M, Klein A, et al. Photocrosslinked Dextran-Based hydrogels as carrier system for the cells and cytokines induce bone regeneration in critical size defects in mice. Gels, 2018, 4(3): 63.
49.	Fearon P V, Lind T, McCaskie A W, et al. Improving osteogenesis on biomaterial surfaces-using novel biomolecules. Orthopaedic Proceedings, 2018, 87-B(SIII): 222.
50.	Luo K, Gao X, Gao Y, et al. Multiple integrin ligands provide a highly adhesive and osteoinductive surface that improves selective cell retention technology. Acta Biomater, 2019, 85: 106-116.
51.	Zhao W, He B, Zhou A, et al. D-RADA16-RGD-reinforced nano-hydroxyapatite/polyamide 66 ternary biomaterial for bone formation. Tissue Eng Regen Med, 2019, 16(2): 177-189.
52.	Ma Y, Li Y, Hao J, et al. Evaluation of the degradation, biocompatibility and osteogenesis behavior of lithium-doped calcium polyphosphate for bone tissue engineering. Biomed Mater Eng, 2019, 30(1): 23-36.
53.	Romero-Gavilán F, Araújo-Gomes N, García-Arnáez I, et al. The effect of strontium incorporation into sol-gel biomaterials on their protein adsorption and cell interactions. Colloids Surf B Biointerfaces, 2019, 174: 9-16.
54.	Saeedeh Z J, Nafiseh B, Fatemeh B. The effects of Strontium incorporation on a novel gelatin/bioactive glass bone graft: In vitro and in vivo characterization. Ceram Int, 2018, 44(12): 14217-14227.
55.	He F, Lu T, Fang X, et al. Modification of honeycomb bioceramic scaffolds for bone regeneration under the condition of excessive bone resorption. J Biomed Mater Res A, 2019, 107(6): 1314-1323.
56.	Gu Y, Zhang J, Zhang X, et al. Three-dimensional printed Mg-doped β-TCP bone tissue engineering scaffolds: effects of magnesium ion concentration on osteogenesis and angiogenesis in vitro. Tissue Eng Regen Med, 2019, 16(4): 415-429.
57.	Wang Chenbing, Liu Jinlong, Liu Yanbo, et al. Study on osteogenesis of zinc-loaded carbon nanotubes/chitosan composite biomaterials in rat skull defects. J Mater Sci Mater Med, 2020, 31(2): 15.
58.	Zhou S, Pan Y, Zhang J, et al. Dendritic polyglycerol-conjugated gold nanostars with different densities of functional groups to regulate osteogenesis in human mesenchymal stem cells. Nanoscale, 2020, 12(47): 24006-24019.
59.	Shi H, Ye X, Zhang J, et al. A thermostability perspective on enhancing physicochemical and cytological characteristics of octacalcium phosphate by doping iron and strontium. Bioact Mater, 2021, 6(5): 1267-1282.
60.	Shi M, Wang C, Wang Y, et al. Deproteinized bovine bone matrix induces osteoblast differentiation via macrophage polarization. J Biomed Mater Res A, 2018, 106(5): 1236-1246.
61.	Bartnikowski M, Moon H J, Ivanovski S. Release of Lithium from 3D printed polycaprolactone scaffolds regulates macrophage and osteoclast response. Biomed Mater, 2018, 13(6): 065003.
62.	Zhao F, Lei B, Li X, et al. Promoting in vivo early angiogenesis with sub-micrometer strontium-contained bioactive microspheres through modulating macrophage phenotypes. Biomaterials, 2018, 178: 36-47.
63.	Zhang X, Chen Q, Mao X. Magnesium enhances osteogenesis of BMSCs by tuning osteoimmunomodulation. Biomed Res Int, 2019, 2019: 7908205.
64.	Liu W, Li J, Cheng M, et al. Zinc-modified sulfonated polyetheretherketone surface with immunomodulatory function for guiding cell fate and bone regeneration. Adv Sci (Weinh), 2018, 5(10): 1800749.
65.	Lu X, Li K, Xie Y, et al. Improved osteogenesis of boron incorporated calcium silicate coatings via immunomodulatory effects. J Biomed Mater Res A, 2019, 107(1): 12-24.
66.	Hoare J I, Rajnicek A M, McCaig C D, et al. Electric fields are novel determinants of human macrophage functions. J Leukoc Biol, 2016, 99(6): 1141-1151.
67.	Dai X, Heng B C, Bai Y, et al. Restoration of electrical microenvironment enhances bone regeneration under diabetic conditions by modulating macrophage polarization. Bioact Mater, 2021, 6(7): 2029-2038.
68.	Zhang W, Liu J, Shi H, et al. Communication between nitric oxide synthase and positively-charged surface and bone formation promotion. Colloids Surf B Biointerfaces, 2016, 148: 354-362.

1. Andi M A, Sengo K, Satoshi O. Effect of heat treatments on wettability of nacre. Mater Sci Forum, 2020, 4808: 86-90.
2. Zhang R, Liu X, Xiong Z, et al. The immunomodulatory effects of Zn-incorporated micro/nanostructured coating in inducing osteogenesis. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 1123-1130.
3. Sharma R I, Snedeker J G. Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes. PLoS One, 2012, 7(2): e31504.
4. Yang C, Delrio F W, Ma H, et al. Spatially patterned matrix elasticity directs stem cell fate. Proc Natl Acad Sci U S A, 2016, 113(31): E4439-E4445.
5. Yang C, Tibbitt M W, Basta L, et al. Mechanical memory and dosing influence stem cell fate. Nat Mater, 2014, 13(6): 645-652.
6. Lin D J, Fuh L J, Chen W C. 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.
7. Liene P, Edijs F, Karlis A G, et al. Functionalizing surface electrical potential of hydroxyapatite coatings. Adv Sci Technol, 2017, 4475(204): 12-17.
8. Agour M, Abdal-Hay A, Hassan M K, et al. Alkali-treated titanium coated with a polyurethane, magnesium and hydroxyapatite composite for bone tissue engineering. Nanomaterials, 2021, 11(5): 1129.
9. Isoshima K, Ueno T, Arai Y, et al. The change of surface charge by lithium ion coating enhances protein adsorption on titanium. J Mech Behav Biomed Mater, 2019, 100: 103393.
10. Ribeiro C, Panadero J A, Sencadas V, et al. Fibronectin adsorption and cell response on electroactive poly(vinylidene fluoride) films. Biomed Mater, 2012, 7(3): 035004.
11. Long X, Wang X, Yao L, et al. Graphene/Si-promoted osteogenic differentiation of BMSCs through light illumination. ACS Appl Mater Interfaces, 2019, 11(47): 43857-43864.
12. Petecchia L, Sbrana F, Utzeri R, et al. Electro-magnetic field promotes osteogenic differentiation of BM-hMSCs through a selective action on Ca(2+)-related mechanisms. Sci Rep, 2015, 5: 13856.
13. Nakamura M, Nagai A, Yamashita K. Surface electric fields of apatite electret promote osteoblastic responses. Key Eng Mater, 2013, 2050: 357-360.
14. Zhou Z, Li W, He T, et al. Polarization of an electroactive functional film on titanium for inducing osteogenic differentiation. Sci Rep, 2016, 6: 35512.
15. Carville N C, Collins L, Manzo M, et al. Biocompatibility of ferroelectric lithium niobate and the influence of polarization charge on osteoblast proliferation and function. J Biomed Mater Res A, 2015, 103(8): 2540-2548.
16. Ding X, Xu S, Li S, et al. Biological effects of titanium surface charge with a focus on protein adsorption. ACS Omega, 2020, 5(40): 25617-25624.
17. Lawton J M, Habib M, MA B, et al. The effect of cationically-modified phosphorylcholine polymers on human osteoblasts in vitro and their effect on bone formation in vivo. J Mater Sci Mater Med, 2017, 28(9): 144.
18. Casagrande S, Tiribuzi R, Cassetti E, et al. Biodegradable composite porous poly(dl-lactide-co-glycolide) scaffold supports mesenchymal stem cell differentiation and calcium phosphate deposition. Artif Cells Nanomed Biotechnol, 2018, 46(sup1): 219-229.
19. Wang Z, Dong L, Han L, et al. Self-assembled biodegradable nanoparticles and polysaccharides as biomimetic ECM nanostructures for the synergistic effect of RGD and BMP-2 on bone formation. Sci Rep, 2016, 6: 25090.
20. Aguilar A, Zein N, Harmouch E, et al. Application of chitosan in bone and dental engineering. Molecules, 2019, 24(16): 3009.
21. Lin J H, Chang H Y, Kao W L, et al. Effect of surface potential on extracellular matrix protein adsorption. Langmuir, 2014, 30(34): 10328-10335.
22. Koch F, Wolff A, Mathes S, et al. Amino acid composition of nanofibrillar self-assembling peptide hydrogels affects responses of periodontal tissue cells in vitro. Int J Nanomedicine, 2018, 13: 6717-6733.
23. Marchesano V, Gennari O, Mecozzi L, et al. Effects of Lithium niobate polarization on cell adhesion and morphology. ACS Appl Mater Interfaces, 2015, 7(32): 18113-18119.
24. Griffanti G, James-Bhasin M, Donelli I, et al. Functionalization of silk fibroin through anionic fibroin derived polypeptides. Biomed Mater, 2018, 14(1): 015006.
25. Griffanti G, Jiang W, Nazhat S N. Bioinspired mineralization of a functionalized injectable dense collagen hydrogel through silk sericin incorporation. Biomater Sci, 2019, 7(3): 1064-1077.
26. Kim H D, Lee E A, An Y H, et al. Chondroitin sulfate-based biomineralizing surface hydrogels for bone tissue engineering. ACS Appl Mater Interfaces, 2017, 9(26): 21639-21650.
27. Tan F, Liu J, Liu M, et al. Charge density is more important than charge polarity in enhancing osteoblast-like cell attachment on poly(ethylene glycol)-diacrylate hydrogel. Mater Sci Eng C Mater Biol Appl, 2017, 76: 330-339.
28. Dadsetan M, Pumberger M, Casper M E, et al. The effects of fixed electrical charge on chondrocyte behavior. Acta Biomater, 2011, 7(5): 2080-2090.
29. Olthof M G L, Kempen D H R, Liu X, et al. Effect of biomaterial electrical charge on bone morphogenetic protein-2-induced in vivo bone formation. Tissue Eng Part A, 2019, 25(13/14): 1037-1052.
30. De Luca I, Di Salle A, Alessio N, et al. Positively charged polymers modulate the fate of human mesenchymal stromal cells via ephrinB2/EphB4 signaling. Stem Cell Res, 2016, 17(2): 248-255.
31. Tiwari J N, Seo Y K, Yoon T, et al. Accelerated bone regeneration by two-photon photoactivated carbon nitride nanosheets. ACS Nano, 2017, 11(1): 742-751.
32. Yu P, Ning C, Zhang Y, et al. Bone-inspired spatially specific piezoelectricity induces bone regeneration. Theranostics, 2017, 7(13): 3387-3397.
33. Tang B, Zhang B, Zhuang J, et al. Surface potential-governed cellular osteogenic differentiation on ferroelectric polyvinylidene fluoride trifluoroethylene films. Acta Biomater, 2018, 74: 291-301.
34. Xu C, Wang S, Liu L, et al. Manipulating mesenchymal stem cells differentiation under sinusoidal electromagnetic fields using intracellular superparamagnetic nanoparticles. J Biomed Nanotechnol, 2019, 15(2): 301-310.
35. Jiang Pengfei, Zhang Yixian, Zhu Chaonan, et al. Fe₃O₄/BSA particles induce osteogenic differentiation of mesenchymal stem cells under static magnetic field. Acta Biomater, 2016, 46: 141-150.
36. Love M R, Palee S, Chattipakorn S C, et al. Effects of electrical stimulation on cell proliferation and apoptosis. J Cell Physiol, 2018, 233(3): 1860-1876.
37. O'Hearn S F, Ackerman B J, Mower M M. Paced monophasic and biphasic waveforms alter transmembrane potentials and metabolism of human fibroblasts. Biochem Biophys Rep, 2016, 8: 249-253.
38. Wang Jing, Tian Lingling, Chen Nuan, et al. The cellular response of nerve cells on poly-L-lysine coated PLGA-MWCNTs aligned nanofibers under electrical stimulation. Mater Sci Eng C, 2018, 91: 715-726.
39. Zhu B, Li Y, Huang F, et al. Promotion of the osteogenic activity of an antibacterial polyaniline coating by electrical stimulation. Biomater Sci, 2019, 7(11): 4730-4737.
40. Jing W, Huang Y, Wei P, et al. Roles of electrical stimulation in promoting osteogenic differentiation of BMSCs on conductive fibers. J Biomed Mater Res A, 2019, 107(7): 1443-1454.
41. Li J, Liu X, Crook J M, et al. Electrical stimulation-induced osteogenesis of human adipose derived stem cells using a conductive graphene-cellulose scaffold. Mater Sci Eng C Mater Biol Appl, 2020, 107: 110312.
42. Zhao Y Q, Meng L, Zhang K, et al. Ultra-small nanodots coated with oligopeptides providing highly negative charges to enhance osteogenic differentiation of hBMSCs better than osteogenic induction medium. Chin Chem Lett, 2021, 32(1): 266-270.
43. Calabrese R, Raia N, Huang W, et al. Silk-ionomer and silk-tropoelastin hydrogels as charged three-dimensional culture platforms for the regulation of hMSC response. J Tissue Eng Regen Med, 2017, 11(9): 2549-2564.
44. Saghiri M A, Asatourian A, Garcia-Godoy F, et al. The role of angiogenesis in implant dentistry part I: review of titanium alloys, surface characteristics and treatments. Med Oral Patol Oral Cir Bucal, 2016, 21(4): e514-e525.
45. Hao L, Fu X, Li T, et al. Surface chemistry from wettability and charge for the control of mesenchymal stem cell fate through self-assembled monolayers. Colloids Surf B Biointerfaces, 2016, 148: 549-556.
46. Sasayama S, Hara T, Tanaka T, et al. Osteogenesis of multipotent progenitor cells using the epigallocatechin gallate-modified gelatin sponge scaffold in the rat congenital cleft-jaw model. Int J Mol Sci, 2018, 19(12): 3803.
47. Cámara-Torres M, Sinha R, Scopece P, et al. Tuning cell behavior on 3D scaffolds fabricated by atmospheric plasma-assisted additive manufacturing. ACS Appl Mater Interfaces, 2021, 13(3): 3631-3644.
48. Ritz U, Eberhardt M, Klein A, et al. Photocrosslinked Dextran-Based hydrogels as carrier system for the cells and cytokines induce bone regeneration in critical size defects in mice. Gels, 2018, 4(3): 63.
49. Fearon P V, Lind T, McCaskie A W, et al. Improving osteogenesis on biomaterial surfaces-using novel biomolecules. Orthopaedic Proceedings, 2018, 87-B(SIII): 222.
50. Luo K, Gao X, Gao Y, et al. Multiple integrin ligands provide a highly adhesive and osteoinductive surface that improves selective cell retention technology. Acta Biomater, 2019, 85: 106-116.
51. Zhao W, He B, Zhou A, et al. D-RADA16-RGD-reinforced nano-hydroxyapatite/polyamide 66 ternary biomaterial for bone formation. Tissue Eng Regen Med, 2019, 16(2): 177-189.
52. Ma Y, Li Y, Hao J, et al. Evaluation of the degradation, biocompatibility and osteogenesis behavior of lithium-doped calcium polyphosphate for bone tissue engineering. Biomed Mater Eng, 2019, 30(1): 23-36.
53. Romero-Gavilán F, Araújo-Gomes N, García-Arnáez I, et al. The effect of strontium incorporation into sol-gel biomaterials on their protein adsorption and cell interactions. Colloids Surf B Biointerfaces, 2019, 174: 9-16.
54. Saeedeh Z J, Nafiseh B, Fatemeh B. The effects of Strontium incorporation on a novel gelatin/bioactive glass bone graft: In vitro and in vivo characterization. Ceram Int, 2018, 44(12): 14217-14227.
55. He F, Lu T, Fang X, et al. Modification of honeycomb bioceramic scaffolds for bone regeneration under the condition of excessive bone resorption. J Biomed Mater Res A, 2019, 107(6): 1314-1323.
56. Gu Y, Zhang J, Zhang X, et al. Three-dimensional printed Mg-doped β-TCP bone tissue engineering scaffolds: effects of magnesium ion concentration on osteogenesis and angiogenesis in vitro. Tissue Eng Regen Med, 2019, 16(4): 415-429.
57. Wang Chenbing, Liu Jinlong, Liu Yanbo, et al. Study on osteogenesis of zinc-loaded carbon nanotubes/chitosan composite biomaterials in rat skull defects. J Mater Sci Mater Med, 2020, 31(2): 15.
58. Zhou S, Pan Y, Zhang J, et al. Dendritic polyglycerol-conjugated gold nanostars with different densities of functional groups to regulate osteogenesis in human mesenchymal stem cells. Nanoscale, 2020, 12(47): 24006-24019.
59. Shi H, Ye X, Zhang J, et al. A thermostability perspective on enhancing physicochemical and cytological characteristics of octacalcium phosphate by doping iron and strontium. Bioact Mater, 2021, 6(5): 1267-1282.
60. Shi M, Wang C, Wang Y, et al. Deproteinized bovine bone matrix induces osteoblast differentiation via macrophage polarization. J Biomed Mater Res A, 2018, 106(5): 1236-1246.
61. Bartnikowski M, Moon H J, Ivanovski S. Release of Lithium from 3D printed polycaprolactone scaffolds regulates macrophage and osteoclast response. Biomed Mater, 2018, 13(6): 065003.
62. Zhao F, Lei B, Li X, et al. Promoting in vivo early angiogenesis with sub-micrometer strontium-contained bioactive microspheres through modulating macrophage phenotypes. Biomaterials, 2018, 178: 36-47.
63. Zhang X, Chen Q, Mao X. Magnesium enhances osteogenesis of BMSCs by tuning osteoimmunomodulation. Biomed Res Int, 2019, 2019: 7908205.
64. Liu W, Li J, Cheng M, et al. Zinc-modified sulfonated polyetheretherketone surface with immunomodulatory function for guiding cell fate and bone regeneration. Adv Sci (Weinh), 2018, 5(10): 1800749.
65. Lu X, Li K, Xie Y, et al. Improved osteogenesis of boron incorporated calcium silicate coatings via immunomodulatory effects. J Biomed Mater Res A, 2019, 107(1): 12-24.
66. Hoare J I, Rajnicek A M, McCaig C D, et al. Electric fields are novel determinants of human macrophage functions. J Leukoc Biol, 2016, 99(6): 1141-1151.
67. Dai X, Heng B C, Bai Y, et al. Restoration of electrical microenvironment enhances bone regeneration under diabetic conditions by modulating macrophage polarization. Bioact Mater, 2021, 6(7): 2029-2038.
68. Zhang W, Liu J, Shi H, et al. Communication between nitric oxide synthase and positively-charged surface and bone formation promotion. Colloids Surf B Biointerfaces, 2016, 148: 354-362.

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