REVIEW ARTICLE
Osteoinductive and antimicrobial mechanisms of graphene-based materials for enhancing bone tissue engineering
Mengsong Wu,
Ling Zou,
Linli Jiang,
Zhihe Zhao,
Jun Liu,
Mengsong Wu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorLing Zou
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorLinli Jiang
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorZhihe Zhao
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorCorresponding Author
Jun Liu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Correspondence
Jun Liu, Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China.
Email: [email protected]
Search for more papers by this authorMengsong Wu,
Ling Zou,
Linli Jiang,
Zhihe Zhao,
Jun Liu,
Mengsong Wu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorLing Zou
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorLinli Jiang
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorZhihe Zhao
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Search for more papers by this authorCorresponding Author
Jun Liu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Correspondence
Jun Liu, Department of Orthodontics, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China.
Email: [email protected]
Search for more papers by this authorAbstract
Graphene-based materials (GMs) have great application prospects in bone tissue engineering due to their osteoinductive ability and antimicrobial activity. GMs induce osteogenic differentiation through several mechanisms and pathways in bone tissue engineering. First of all, the surface and high hardness of the porous folds of graphene or graphene oxide (GO) can generate mechanical stimulation to initiate a cascade of reactions that promote osteogenic differentiation without any chemical inducers. In addition, change of the extracellular matrix (ECM), regulation of macrophage polarization, the oncostatin M (OSM) signaling pathway, the MAPK signaling pathway, the BMP signaling pathway, the Wnt/β-catenin signaling pathway, and other pathways are involved in GMs' regulation of osteogenesis. In bone tissue engineering, GMs prevent the formation of microbial biofilms mainly through preventing microbial adhesion and killing them. The former is mainly achieved by reducing surface free energy (SFE) and increasing hydrophobicity. The latter mainly includes oxidative stress and photothermal/photodynamic effects. Graphene and its derivatives (GDs) are mainly combined with bioactive ceramic materials, metal materials and macromolecular polymers to play an antimicrobial effect in bone tissue engineering. Concentration, number of layers, and type of GDs often affect the antimicrobial activity of GMs. In this paper, we reviewed relevant osteoinductive and antimicrobial mechanisms of GMs and their applications in bone tissue engineering.
CONFLICTS OF INTEREST
The authors declare no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
REFERENCES
- Adeel, M., Bilal, M., Rasheed, T., Sharma, A., & Iqbal, H. (2018). Graphene and graphene oxide: Functionalization and nano-bio-catalytic system for enzyme immobilization and biotechnological perspective. International Journal of Biological Macromolecules, 120(Pt B), 1430–1440. https://doi.org/10.1016/j.ijbiomac.2018.09.144
- Agarwalla, S. V., Ellepola, K., Costa, M., Fechine, G., Morin, J., Castro, N. A., Seneviratne, C. J., & Rosa, V. (2019). Hydrophobicity of graphene as a driving force for inhibiting biofilm formation of pathogenic bacteria and fungi. Dental Materials, 35(3), 403–413. https://doi.org/10.1016/j.dental.2018.09.016
- Agarwalla, S. V., Ellepola, K., Silikas, N., Castro, N. A., Seneviratne, C. J., & Rosa, V. (2021). Persistent inhibition of Candida albicans biofilm and hyphae growth on titanium by graphene nanocoating. Dental Materials, 37(2), 370–377. https://doi.org/10.1016/j.dental.2020.11.028
- Akhavan, O., Ghaderi, E., & Shahsavar, M. (2013). Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon, 59, 200–211. https://doi.org/10.1016/j.carbon.2013.03.010
- Alford, A. I., Kozloff, K. M., & Hankenson, K. D. (2015). Extracellular matrix networks in bone remodeling. The International Journal of Biochemistry & Cell Biology, 65, 20–31. https://doi.org/10.1016/j.biocel.2015.05.008
- Bays, J. L., & DeMali, K. A. (2017). Vinculin in cell-cell and cell-matrix adhesions. Cellular and Molecular Life Sciences, 74(16), 2999–3009. https://doi.org/10.1007/s00018-017-2511-3
- Bordoni, V., Reina, G., Orecchioni, M., Furesi, G., Thiele, S., Gardin, C., Zavan, B., Cuniberti, G., Bianco, A., Rauner, M., & Delogu, L. G. (2019). Stimulation of bone formation by monocyte-activator functionalized graphene oxide in vivo. Nanoscale, 11(41), 19408–19421. https://doi.org/10.1039/c9nr03975a
- Brambilla, E., Ionescu, A., Mazzoni, A., Cadenaro, M., Gagliani, M., Ferraroni, M., Tay, F., Pashley, D., & Breschi, L. (2014). Hydrophilicity of dentin bonding systems influences in vitro Streptococcus mutans biofilm formation. Dental Materials, 30(8), 926–935. https://doi.org/10.1016/j.dental.2014.05.009
- Byron, A., & Frame, M. C. (2016). Adhesion protein networks reveal functions proximal and distal to cell-matrix contacts. Current Opinion in Cell Biology, 39, 93–100. https://doi.org/10.1016/j.ceb.2016.02.013
- Chen, G., Deng, C., & Li, Y. P. (2012). TGF-beta and BMP signaling in osteoblast differentiation and bone formation. International Journal of Biological Sciences, 8(2), 272–288. https://doi.org/10.7150/ijbs.2929
- Chen, G., Lv, Y., Guo, P., Lin, C., Zhang, X., Yang, L., & Xu, Z. (2013). Matrix mechanics and fluid shear stress control stem cells fate in three dimensional microenvironment. Current Stem Cell Research and Therapy, 8(4), 313–323. https://doi.org/10.2174/1574888x11308040007
- Chen, J., Zhang, X., Cai, H., Chen, Z., Wang, T., Jia, L., Wang, J., Wan, Q., & Pei, X. (2016). Osteogenic activity and antibacterial effect of zinc oxide/carboxylated graphene oxide nanocomposites: Preparation and in vitro evaluation. Colloids and Surfaces B: Biointerfaces, 147, 397–407. https://doi.org/10.1016/j.colsurfb.2016.08.023
- Chen, X., Wang, M., Chen, F., Wang, J., Li, X., Liang, J., Fan, Y., Xiao, Y., & Zhang, X. (2020). Correlations between macrophage polarization and osteoinduction of porous calcium phosphate ceramics. Acta Biomaterialia, 103, 318–332. https://doi.org/10.1016/j.actbio.2019.12.019
- Compton, O. C., Cranford, S. W., Putz, K. W., An, Z., Brinson, L. C., Buehler, M. J., & Nguyen, S. T. (2012). Tuning the mechanical properties of graphene oxide paper and its associated polymer nanocomposites by controlling cooperative intersheet hydrogen bonding. ACS Nano, 6(3), 2008–2019. https://doi.org/10.1021/nn202928w
- Curry, A. S., Pensa, N. W., Barlow, A. M., & Bellis, S. L. (2016). Taking cues from the extracellular matrix to design bone-mimetic regenerative scaffolds. Matrix Biology, 52–54, 397–412. https://doi.org/10.1016/j.matbio.2016.02.011
- Dellieu, L., Lawarée, E., Reckinger, N., Didembourg, C., Letesson, J. J., Sarrazin, M., Deparis, O., Matroule, J. Y., & Colomer, J. F. (2015). Do CVD grown graphene films have antibacterial activity on metallic substrates? Carbon, 84, 310–316. https://doi.org/10.1016/j.carbon.2014.12.025
- Diez-Pascual, A. M., & Diez-Vicente, A. L. (2016). Poly(propylene fumarate)/polyethylene glycol-modified graphene oxide nanocomposites for tissue engineering. ACS Applied Materials & Interfaces, 8(28), 17902–17914. https://doi.org/10.1021/acsami.6b05635
- Diez-Pascual, A. M., & Diez-Vicente, A. L. (2017). Multifunctional poly(glycolic acid-co-propylene fumarate) electrospun fibers reinforced with graphene oxide and hydroxyapatite nanorods. Journal of Materials Chemistry B, 5(22), 4084–4096. https://doi.org/10.1039/c7tb00497d
- Dong, W., Hou, L., Li, T., Gong, Z., Huang, H., Wang, G., Chen, X., & Li, X. (2015). A dual role of graphene oxide sheet deposition on titanate nanowire scaffolds for osteo-implantation: Mechanical hardener and surface activity regulator. Scientific Reports, 5, 18266. https://doi.org/10.1038/srep18266
- Du, Z., Wang, C., Zhang, R., Wang, X., & Li, X. (2020). Applications of graphene and its derivatives in bone repair: Advantages for promoting bone formation and providing real-time detection, challenges and future prospects. International Journal of Nanomedicine, 15, 7523–7551. https://doi.org/10.2147/IJN.S271917
- Dubey, N., Ellepola, K., Decroix, F., Morin, J., Castro, N. A., Seneviratne, C. J., & Rosa, V. (2018). Graphene onto medical grade titanium: An atom-thick multimodal coating that promotes osteoblast maturation and inhibits biofilm formation from distinct species. Nanotoxicology, 12(4), 274–289. https://doi.org/10.1080/17435390.2018.1434911
- Dubey, N., Morin, J. L. P., Luong-Van, E. K., Agarwalla, S. V., Silikas, N., Castro Neto, A. H., & Rosa, V. (2020). Osteogenic potential of graphene coated titanium is independent of transfer technique. Materialia, 9, 100604. https://doi.org/10.1016/j.mtla.2020.100604
- Elkhenany, H., Amelse, L., Lafont, A., Bourdo, S., Caldwell, M., Neilsen, N., Dervishi, E., Derek, O., Biris, A. S., Anderson, D., & Dhar, M. (2015). Graphene supports in vitro proliferation and osteogenic differentiation of goat adult mesenchymal stem cells: Potential for bone tissue engineering. Journal of Applied Toxicology, 35(4), 367–374. https://doi.org/10.1002/jat.3024
- El-Rashidy, A. A., Roether, J. A., Harhaus, L., Kneser, U., & Boccaccini, A. R. (2017). Regenerating bone with bioactive glass scaffolds: A review of in vivo studies in bone defect models. Acta Biomaterialia, 62, 1–28. https://doi.org/10.1016/j.actbio.2017.08.030
- Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126(4), 677–689. https://doi.org/10.1016/j.cell.2006.06.044
- Fasolino, A., Los, J. H., & Katsnelson, M. I. (2007). Intrinsic ripples in graphene. Nature Materials, 6(11), 858–861. https://doi.org/10.1038/nmat2011
- Feng, J., & Guo, Z. (2019). Wettability of graphene: From influencing factors and reversible conversions to potential applications. Nanoscale Horizons, 4(2), 339–364. https://doi.org/10.1039/c8nh00348c
- Feng, X., Shen, S., Cao, P., Zhu, L., Zhang, Y., Zheng, K., Feng, G., & Zhang, D. (2016). The role of oncostatin M regulates osteoblastic differentiation of dental pulp stem cells through STAT3 pathway. Cytotechnology, 68(6), 2699–2709. https://doi.org/10.1007/s10616-016-9995-9
- Francolini, I., & Donelli, G. (2010). Prevention and control of biofilm-based medical-device-related infections. FEMS Immunology and Medical Microbiology, 59(3), 227–238. https://doi.org/10.1111/j.1574-695X.2010.00665.x
- Fu, C., Bai, H., Zhu, J., Niu, Z., Wang, Y., Li, J., Yang, X., & Bai, Y. (2017). Enhanced cell proliferation and osteogenic differentiation in electrospun PLGA/hydroxyapatite nanofibre scaffolds incorporated with graphene oxide. PLoS One, 12(11), e188352. https://doi.org/10.1371/journal.pone.0188352
- Fu, C., Yang, X., Tan, S., & Song, L. (2017). Enhancing cell proliferation and osteogenic differentiation of MC3T3-E1 pre-osteoblasts by BMP-2 delivery in graphene oxide-incorporated PLGA/HA biodegradable microcarriers. Scientific Reports, 7(1), 12549. https://doi.org/10.1038/s41598-017-12935-x
- Gallardo-Lopez, A., Munoz-Ferreiro, C., Lopez-Pernia, C., Jimenez-Pique, E., Gutierrez-Mora, F., Morales-Rodriguez, A., & Poyato, R. (2020). Critical influence of the processing route on the mechanical properties of zirconia composites with graphene nanoplatelets. Materials (Basel), 14(1), 108. https://doi.org/10.3390/ma14010108
- Gao, Y., Wang, Y., Wang, Y., & Cui, W. (2016). Fabrication of gelatin-based electrospun composite fibers for anti-bacterial properties and protein adsorption. Marine Drugs, 14(10), 192. https://doi.org/10.3390/md14100192
- Garcia, A. J., & Reyes, C. D. (2005). Bio-adhesive surfaces to promote osteoblast differentiation and bone formation. Journal of Dental Research, 84(5), 407–413. https://doi.org/10.1177/154405910508400502
- Gilbert, L., He, X., Farmer, P., Rubin, J., Drissi, H., van Wijnen, A. J., Lian, J. B., Stein, G. S., & Nanes, M. S. (2002). Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. Journal of Biological Chemistry, 277(4), 2695–2701. https://doi.org/10.1074/jbc.M106339200
- Gong, L., Zhao, Y., Zhang, Y., & Ruan, Z. (2016). The macrophage polarization regulates MSC osteoblast differentiation in vitro. Annals of Clinical and Laboratory Science, 46(1), 65–71.
- Gu, M., Lv, L., Du, F., Niu, T., Chen, T., Xia, D., Wang, S., Zhao, X., Liu, J., Liu, Y., Xiong, C., & Zhou, Y. (2018). Effects of thermal treatment on the adhesion strength and osteoinductive activity of single-layer graphene sheets on titanium substrates. Scientific Reports, 8(1), 8141. https://doi.org/10.1038/s41598-018-26551-w
- Guan, J., Zhang, J., Guo, S., Zhu, H., Zhu, Z., Li, H., Wang, Y., Zhang, C., & Chang, J. (2015). Human urine-derived stem cells can be induced into osteogenic lineage by silicate bioceramics via activation of the Wnt/beta-catenin signaling pathway. Biomaterials, 55, 1–11. https://doi.org/10.1016/j.biomaterials.2015.03.029
- Halim, A., Liu, L., Ariyanti, A. D., Ju, Y., Luo, Q., & Song, G. (2019). Low-dose suspended graphene oxide nanosheets induce antioxidant response and osteogenic differentiation of bone marrow-derived mesenchymal stem cells via JNK-dependent FoxO1 activation. Journal of Materials Chemistry B, 7(39), 5998–6009. https://doi.org/10.1039/c9tb01413f
- He, J., Zhu, X., Qi, Z., Wang, L., Aldalbahi, A., Shi, J., Song, S., Fan, C., Lv, M., & Tang, Z. (2017). The inhibition effect of graphene oxide nanosheets on the development of Streptococcus mutans biofilms. Particle & Particle Systems Characterization, 34(5), 1700001. https://doi.org/10.1002/ppsc.201700001
- He, M., Zhu, C., Xu, H., Sun, D., Chen, C., Feng, G., Liu, L., Li, Y., & Zhang, L. (2020). Conducting polyetheretherketone nanocomposites with an electrophoretically deposited bioactive coating for bone tissue regeneration and multimodal therapeutic applications. ACS Applied Materials & Interfaces, 12(51), 56924–56934. https://doi.org/10.1021/acsami.0c20145
- Hirata, E., Miyako, E., Hanagata, N., Ushijima, N., Sakaguchi, N., Russier, J., Yudasaka, M., Iijima, S., Bianco, A., & Yokoyama, A. (2016). Carbon nanohorns allow acceleration of osteoblast differentiation via macrophage activation. Nanoscale, 8(30), 14514–14522. https://doi.org/10.1039/c6nr02756c
- Huang, H., Zhao, N., Xu, X., Xu, Y., Li, S., Zhang, J., & Yang, P. (2011). Dose-specific effects of tumor necrosis factor alpha on osteogenic differentiation of mesenchymal stem cells. Cell Proliferation, 44(5), 420–427. https://doi.org/10.1111/j.1365-2184.2011.00769.x
- Huang, I. H., Hsiao, C. T., Wu, J. C., Shen, R. F., Liu, C. Y., Wang, Y. K., Chen, Y. C., Huang, C. M., Del, A. J., Chang, Z. F., Tang, M. J., Khoo, K. H., & Kuo, J. C. (2014). GEF-H1 controls focal adhesion signaling that regulates mesenchymal stem cell lineage commitment. Journal of Cell Science, 127(Pt 19), 4186–4200. https://doi.org/10.1242/jcs.150227
- Huang, L., Xu, S., Wang, Z., Xue, K., Su, J., Song, Y., Chen, S., Zhu, C., Tang, B. Z., & Ye, R. (2020). Self-reporting and photothermally enhanced rapid bacterial killing on a laser-induced graphene mask. ACS Nano, 14(9), 12045–12053. https://doi.org/10.1021/acsnano.0c05330
- Jia, Z., Shi, Y., Xiong, P., Zhou, W., Cheng, Y., Zheng, Y., Xi, T., & Wei, S. (2016). From solution to biointerface: Graphene self-assemblies of varying lateral sizes and surface properties for biofilm control and osteodifferentiation. ACS Applied Materials & Interfaces, 8(27), 17151–17165. https://doi.org/10.1021/acsami.6b05198
- Jin, L., Yuan, F., Chen, C., Wu, J., Gong, R., Yuan, G., Zeng, H., Pei, J., & Chen, T. (2019). Degradation products of polydopamine restrained inflammatory response of LPS-Stimulated macrophages through mediation TLR-4-MYD88 dependent signaling pathways by antioxidant. Inflammation, 42(2), 658–671. https://doi.org/10.1007/s10753-018-0923-3
- Kang, E. S., Song, I., Kim, D. S., Lee, U., Kim, J. K., Son, H., Min, J., & Kim, T. H. (2018). Size-dependent effects of graphene oxide on the osteogenesis of human adipose-derived mesenchymal stem cells. Colloids and Surfaces B: Biointerfaces, 169, 20–29. https://doi.org/10.1016/j.colsurfb.2018.04.053
- Katagiri, T., & Watabe, T. (2016). Bone morphogenetic proteins. Cold Spring Harbor Perspectives in Biology, 8(6), a021899. https://doi.org/10.1101/cshperspect.a021899
- Kim, H. D., Kim, J., Koh, R. H., Shim, J., Lee, J. C., Kim, T. I., & Hwang, N. S. (2017). Enhanced osteogenic commitment of human mesenchymal stem cells on polyethylene glycol-based cryogel with graphene oxide substrate. ACS Biomaterials Science & Engineering, 3(10), 2470–2479. https://doi.org/10.1021/acsbiomaterials.7b00299
- Kim, J., Kim, H. D., Park, J., Lee, E. S., Kim, E., Lee, S. S., Yang, J. K., Lee, Y. S., & Hwang, N. S. (2018). Enhanced osteogenic commitment of murine mesenchymal stem cells on graphene oxide substrate. Biomaterials Research, 22, 1. https://doi.org/10.1186/s40824-017-0112-8
- Kim, J. W., Shin, Y. C., Lee, J. J., Bae, E. B., Jeon, Y. C., Jeong, C. M., Yun, M. J., Lee, S. H., Han, D. W., & Huh, J. B. (2017). The effect of reduced graphene oxide-coated biphasic calcium phosphate bone graft material on osteogenesis. International Journal of Molecular Sciences, 18(8), 1725. https://doi.org/10.3390/ijms18081725
- Kulangara, K., Yang, Y., Yang, J., & Leong, K. W. (2012). Nanotopography as modulator of human mesenchymal stem cell function. Biomaterials, 33(20), 4998–5003. https://doi.org/10.1016/j.biomaterials.2012.03.053
- Kumar, S., Raj, S., Kolanthai, E., Sood, A. K., Sampath, S., & Chatterjee, K. (2015). Chemical functionalization of graphene to augment stem cell osteogenesis and inhibit biofilm formation on polymer composites for orthopedic applications. ACS Applied Materials & Interfaces, 7(5), 3237–3252. https://doi.org/10.1021/am5079732
- Kundu, A. K., Khatiwala, C. B., & Putnam, A. J. (2009). Extracellular matrix remodeling, integrin expression, and downstream signaling pathways influence the osteogenic differentiation of mesenchymal stem cells on poly(lactide-co-glycolide) substrates. Tissue Engineering Part A, 15(2), 273–283. https://doi.org/10.1089/ten.tea.2008.0055
- La, W. G., Park, S., Yoon, H. H., Jeong, G. J., Lee, T. J., Bhang, S. H., Han, J. Y., Char, K., & Kim, B. S. (2013). Delivery of a therapeutic protein for bone regeneration from a substrate coated with graphene oxide. Small, 9(23), 4051–4060. https://doi.org/10.1002/smll.201300571
- Lee, J., Byun, H., Madhurakkat, P. S., Lee, S., & Shin, H. (2019). Current advances in immunomodulatory biomaterials for bone regeneration. Advanced Healthcare Materials, 8(4), e1801106. https://doi.org/10.1002/adhm.201801106
- Lee, J. H., Choi, H. K., Yang, L., Chueng, S. D., Choi, J. W., & Lee, K. B. (2018). Nondestructive real-time monitoring of enhanced stem cell differentiation using a graphene-Au hybrid nanoelectrode array. Advanced Materials, 30(39), e1802762. https://doi.org/10.1002/adma.201802762
- Lee, W. C., Lim, C. H., Shi, H., Tang, L. A., Wang, Y., Lim, C. T., & Loh, K. P. (2011). Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano, 5(9), 7334–7341. https://doi.org/10.1021/nn202190c
- Li, C., Li, G., Liu, M., Zhou, T., & Zhou, H. (2016). Paracrine effect of inflammatory cytokine-activated bone marrow mesenchymal stem cells and its role in osteoblast function. Journal of Bioscience and Bioengineering, 121(2), 213–219. https://doi.org/10.1016/j.jbiosc.2015.05.017
- Li, J., Liu, X., Crook, J. M., & Wallace, G. G. (2020). Electrical stimulation-induced osteogenesis of human adipose derived stem cells using a conductive graphene-cellulose scaffold. Materials Science and Engineering: C, 107, 110312. https://doi.org/10.1016/j.msec.2019.110312
- Li, J., Wang, G., Zhu, H., Zhang, M., Zheng, X., Di, Z., Liu, X., & Wang, X. (2014). Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Scientific Reports, 4, 4359. https://doi.org/10.1038/srep04359
- Li, Q., Lai, Q., He, C., Fang, Y., Yan, Q., Zhang, Y., Wang, X., Gu, C., Wang, Y., Ye, L., Han, L., Lin, X., Chen, J., Cai, J., Li, A., & Liu, S. (2019). RUNX1 promotes tumour metastasis by activating the Wnt/beta-catenin signalling pathway and EMT in colorectal cancer. Journal of Experimental & Clinical Cancer Research, 38(1), 334. https://doi.org/10.1186/s13046-019-1330-9
- Li, Q., & Wang, Z. (2020). Involvement of FAK/P38 signaling pathways in mediating the enhanced osteogenesis induced by nano-graphene oxide modification on titanium implant surface. International Journal of Nanomedicine, 15, 4659–4676. https://doi.org/10.2147/IJN.S245608
- Li, Y., Xu, X., Liu, X., Li, B., Han, Y., Zheng, Y., Chen, D. F., Yeung, K., Cui, Z., Li, Z., Liang, Y., Zhu, S., Wang, X., & Wu, S. (2020). Photoelectrons mediating angiogenesis and immunotherapy through heterojunction film for noninvasive disinfection. Advancement of Science, 7(17), 2000023. https://doi.org/10.1002/advs.202000023
- Liao, C., Li, Y., & Tjong, S. C. (2018). Graphene nanomaterials: Synthesis, biocompatibility, and cytotoxicity. International Journal of Molecular Sciences, 19(11), 3564. https://doi.org/10.3390/ijms19113564
- Liao, C., Li, Y., & Tjong, S. C. (2019). Antibacterial activities of aliphatic polyester nanocomposites with silver nanoparticles and/or graphene oxide sheets. Nanomaterials (Basel), 9(8), 1102. https://doi.org/10.3390/nano9081102
- Lim, K., Hexiu, J., Kim, J., Seonwoo, H., Cho, W. J., Choung, P. H., & Chung, J. H. (2013). Effects of electromagnetic fields on osteogenesis of human alveolar bone-derived mesenchymal stem cells. BioMed Research International, 2013, 296019. https://doi.org/10.1155/2013/296019
- Lim, K. T., Seonwoo, H., Choi, K. S., Jin, H., Jang, K. J., Kim, J., Kim, J. W., Kim, S. Y., Choung, P. H., & Chung, J. H. (2016). Pulsed-electromagnetic-field-assisted reduced graphene oxide substrates for multidifferentiation of human mesenchymal stem cells. Advanced Healthcare Materials, 5(16), 2069–2079. https://doi.org/10.1002/adhm.201600429
- Lin, Y. H., Chuang, T. Y., Chiang, W. H., Chen, I. P., Wang, K., Shie, M. Y., & Chen, Y. W. (2019). The synergistic effects of graphene-contained 3D-printed calcium silicate/poly-epsilon-caprolactone scaffolds promote FGFR-induced osteogenic/angiogenic differentiation of mesenchymal stem cells. Materials Science and Engineering C, 104, 109887. https://doi.org/10.1016/j.msec.2019.109887
- Liu, S., Zeng, T. H., Hofmann, M., Burcombe, E., Wei, J., Jiang, R., Kong, J., & Chen, Y. (2011). Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: Membrane and oxidative stress. ACS Nano, 5(9), 6971–6980. https://doi.org/10.1021/nn202451x
- Lowery, J. W., & Rosen, V. (2018). The BMP pathway and its inhibitors in the skeleton. Physiological Reviews, 98(4), 2431–2452. https://doi.org/10.1152/physrev.00028.2017
- Lu, J., He, Y., Cheng, C., Wang, Y., Qiu, L., Li, D., & Zou, D. (2013). Self-supporting graphene hydrogel film as an experimental platform to evaluate the potential of graphene for bone regeneration. Advanced Functional Materials, 23(28), 3494–3502. https://doi.org/10.1002/adfm.201203637
- Lu, N., Wang, L., Lv, M., Tang, Z., & Fan, C. (2019). Graphene-based nanomaterials in biosystems. Nano Research, 12(2), 247–264. https://doi.org/10.1007/s12274-018-2209-3
- Lu, Z., Wang, G., Dunstan, C. R., & Zreiqat, H. (2012). Short-term exposure to tumor necrosis factor-alpha enables human osteoblasts to direct adipose tissue-derived mesenchymal stem cells into osteogenic differentiation. Stem Cells and Development, 21(13), 2420–2429. https://doi.org/10.1089/scd.2011.0589
- Maldonado-Magnere, S., Yazdani-Pedram, M., Aguilar-Bolados, H., & Quijada, R. (2020). Thermally reduced graphene oxide/thermoplastic polyurethane nanocomposites: Mechanical and barrier properties. Polymers (Basel), 13(1), 85. https://doi.org/10.3390/polym13010085
- Marrella, A., Tedeschi, G., Giannoni, P., Lagazzo, A., Sbrana, F., Barberis, F., Quarto, R., Puglisi, F., & Scaglione, S. (2018). Green-reduced graphene oxide induces in vitro an enhanced biomimetic mineralization of polycaprolactone electrospun meshes. Materials Science and Engineering C, 93, 1044–1053. https://doi.org/10.1016/j.msec.2018.08.052
- McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., & Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Developmental Cell, 6(4), 483–495. https://doi.org/10.1016/s1534-5807(04)00075-9
- Mirza, E. H., Khan, A. A., Al-Khureif, A. A., Saadaldin, S. A., Mohamed, B. A., Fareedi, F., Khan, M. M., Alfayez, M., Al-Fotawi, R., Vallittu, P. K., & Mahmood, A. (2019). Characterization of osteogenic cells grown over modified graphene-oxide-biostable polymers. Biomedical Materials, 14(6), 65004. https://doi.org/10.1088/1748-605X/ab3ab2
- Mitchison, T., & Kirschner, M. (1988). Cytoskeletal dynamics and nerve growth. Neuron, 1(9), 761–772. https://doi.org/10.1016/0896-6273(88)90124-9
- Mohammadrezaei, D., Golzar, H., Rezai, R. M., Omidi, M., Rashedi, H., Yazdian, F., Khojasteh, A., & Tayebi, L. (2018). In vitro effect of graphene structures as an osteoinductive factor in bone tissue engineering: A systematic review. Journal of Biomedical Materials Research Part A, 106(8), 2284–2343. https://doi.org/10.1002/jbm.a.36422
- Mountziaris, P. M., Tzouanas, S. N., & Mikos, A. G. (2010). Dose effect of tumor necrosis factor-alpha on in vitro osteogenic differentiation of mesenchymal stem cells on biodegradable polymeric microfiber scaffolds. Biomaterials, 31(7), 1666–1675. https://doi.org/10.1016/j.biomaterials.2009.11.058
- Mukai, T., Otsuka, F., Otani, H., Yamashita, M., Takasugi, K., Inagaki, K., Yamamura, M., & Makino, H. (2007). TNF-alpha inhibits BMP-induced osteoblast differentiation through activating SAPK/JNK signaling. Biochemical and Biophysical Research Communications, 356(4), 1004–1010. https://doi.org/10.1016/j.bbrc.2007.03.099
- Munoz, J., Akhavan, N. S., Mullins, A. P., & Arjmandi, B. H. (2020). Macrophage polarization and osteoporosis: A review. Nutrients, 12(10), 2999. https://doi.org/10.3390/nu12102999
- Muralidhar, S., Filia, A., Nsengimana, J., Pozniak, J., O'Shea, S. J., Diaz, J. M., Harland, M., Randerson-Moor, J. A., Reichrath, J., Laye, J. P., van der Weyden, L., Adams, D. J., Bishop, D. T., & Newton-Bishop, J. (2019). Vitamin D-VDR signaling inhibits Wnt/beta-Catenin-mediated melanoma progression and promotes antitumor immunity. Cancer Research, 79(23), 5986–5998. https://doi.org/10.1158/0008-5472.CAN-18-3927
- Natarajan, J., Madras, G., & Chatterjee, K. (2017). Development of graphene oxide-/galactitol polyester-based biodegradable composites for biomedical applications. ACS Omega, 2(9), 5545–5556. https://doi.org/10.1021/acsomega.7b01139
- Nayak, T. R., Andersen, H., Makam, V. S., Khaw, C., Bae, S., Xu, X., Ee, P. L., Ahn, J. H., Hong, B. H., Pastorin, G., & Ozyilmaz, B. (2011). Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano, 5(6), 4670–4678. https://doi.org/10.1021/nn200500h
- Newby, S. D., Masi, T., Griffin, C. D., King, W. J., Chipman, A., Stephenson, S., Anderson, D. E., Biris, A. S., Bourdo, S. E., & Dhar, M. (2020). Functionalized graphene nanoparticles induce human mesenchymal stem cells to express distinct extracellular matrix proteins mediating osteogenesis. International Journal of Nanomedicine, 15, 2501–2513. https://doi.org/10.2147/IJN.S245801
- Nicosia, A., Vento, F., Pellegrino, A. L., Ranc, V., Piperno, A., Mazzaglia, A., & Mineo, P. (2020). Polymer-based graphene derivatives and microwave-assisted silver nanoparticles decoration as a potential antibacterial agent. Nanomaterials (Basel), 10(11), 2269. https://doi.org/10.3390/nano10112269
- Nishida, E., Miyaji, H., Kato, A., Takita, H., Iwanaga, T., Momose, T., Ogawa, K., Murakami, S., Sugaya, T., & Kawanami, M. (2016). Graphene oxide scaffold accelerates cellular proliferative response and alveolar bone healing of tooth extraction socket. International Journal of Nanomedicine, 11, 2265–2277. https://doi.org/10.2147/IJN.S104778
- Norahan, M. H., Amroon, M., Ghahremanzadeh, R., Rabiee, N., & Baheiraei, N. (2019). Reduced graphene oxide: Osteogenic potential for bone tissue engineering. IET Nanobiotechnology, 13(7), 720–725. https://doi.org/10.1049/iet-nbt.2019.0125
- Ongaro, A., Pellati, A., Bagheri, L., Fortini, C., Setti, S., & De Mattei, M. (2014). Pulsed electromagnetic fields stimulate osteogenic differentiation in human bone marrow and adipose tissue derived mesenchymal stem cells. Bioelectromagnetics, 35(6), 426–436. https://doi.org/10.1002/bem.21862
- Osta, B., Benedetti, G., & Miossec, P. (2014). Classical and paradoxical effects of TNF-alpha on bone homeostasis. Frontiers in Immunology, 5, 48. https://doi.org/10.3389/fimmu.2014.00048
- Ou, L., Lan, Y., Feng, Z., Feng, L., Yang, J., Liu, Y., Bian, L., Tan, J., Lai, R., & Guo, R. (2019). Functionalization of SF/HAP scaffold with GO-PEI-miRNA inhibitor complexes to enhance bone regeneration through activating transcription factor 4. Theranostics, 9(15), 4525–4541. https://doi.org/10.7150/thno.34676
- Ouyang, L., Deng, Y., Yang, L., Shi, X., Dong, T., Tai, Y., Yang, W., & Chen, Z. G. (2018). Graphene-oxide-decorated microporous polyetheretherketone with superior antibacterial capability and in vitro osteogenesis for orthopedic implant. Macromolecular Bioscience, 18(6), e1800036. https://doi.org/10.1002/mabi.201800036
- Palmieri, V., Barba, M., Di Pietro, L., Conti, C., De Spirito, M., Lattanzi, W., & Papi, M. (2018). Graphene oxide induced osteogenesis quantification by in-situ 2D-FLuorescence spectroscopy. International Journal of Molecular Sciences, 19(11), 3336. https://doi.org/10.3390/ijms19113336
- Park, S., Lee, K. S., Bozoklu, G., Cai, W., Nguyen, S. T., & Ruoff, R. S. (2008). Graphene oxide papers modified by divalent ions-enhancing mechanical properties via chemical cross-linking. ACS Nano, 2(3), 572–578. https://doi.org/10.1021/nn700349a
- Parra, C., Dorta, F., Jimenez, E., Henriquez, R., Ramirez, C., Rojas, R., & Villalobos, P. (2015). A nanomolecular approach to decrease adhesion of biofouling-producing bacteria to graphene-coated material. Journal of Nanobiotechnology, 13, 82. https://doi.org/10.1186/s12951-015-0137-x
- Patel, S. C., Alam, O., & Sitharaman, B. (2018). Osteogenic differentiation of human adipose derived stem cells on chemically crosslinked carbon nanomaterial coatings. Journal of Biomedical Materials Research Part A, 106(5), 1189–1199. https://doi.org/10.1002/jbm.a.36317
- Peng, R., Yao, X., & Ding, J. (2011). Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. Biomaterials, 32(32), 8048–8057. https://doi.org/10.1016/j.biomaterials.2011.07.035
- Peng, S., Feng, P., Wu, P., Huang, W., Yang, Y., Guo, W., Gao, C., & Shuai, C. (2017). Graphene oxide as an interface phase between polyetheretherketone and hydroxyapatite for tissue engineering scaffolds. Scientific Reports, 7, 46604. https://doi.org/10.1038/srep46604
- Prakash, J., Prema, D., Venkataprasanna, K. S., Balagangadharan, K., Selvamurugan, N., & Venkatasubbu, G. D. (2020). Nanocomposite chitosan film containing graphene oxide/hydroxyapatite/gold for bone tissue engineering. International Journal of Biological Macromolecules, 154, 62–71. https://doi.org/10.1016/j.ijbiomac.2020.03.095
- Qi, C., Deng, Y., Xu, L., Yang, C., Zhu, Y., Wang, G., Wang, Z., & Wang, L. (2020). A sericin/graphene oxide composite scaffold as a biomimetic extracellular matrix for structural and functional repair of calvarial bone. Theranostics, 10(2), 741–756. https://doi.org/10.7150/thno.39502
- Qiu, J., Geng, H., Wang, D., Qian, S., Zhu, H., Qiao, Y., Qian, W., & Liu, X. (2017). Layer-Number dependent antibacterial and osteogenic behaviors of graphene oxide electrophoretic deposited on titanium. ACS Applied Materials & Interfaces, 9(14), 12253–12263. https://doi.org/10.1021/acsami.7b00314
- Qiu, J., Li, D., Mou, X., Li, J., Guo, W., Wang, S., Yu, X., Ma, B., Zhang, S., Tang, W., Sang, Y., Gil, P. R., & Liu, H. (2016). Effects of graphene quantum dots on the Self-Renewal and differentiation of mesenchymal stem cells. Advanced Healthcare Materials, 5(6), 702–710. https://doi.org/10.1002/adhm.201500770
- Rafiee, J., Mi, X., Gullapalli, H., Thomas, A. V., Yavari, F., Shi, Y., Ajayan, P. M., & Koratkar, N. A. (2012). Wetting transparency of graphene. Nature Materials, 11(3), 217–222. https://doi.org/10.1038/nmat3228
- Ricci, R., Leite, N., Da-Silva, N. S., Pacheco-Soares, C., Canevari, R. A., Marciano, F. R., Webster, T. J., & Lobo, A. O. (2017). Graphene oxide nanoribbons as nanomaterial for bone regeneration: Effects on cytotoxicity, gene expression and bactericidal effect. Materials Science and Engineering C, 78, 341–348. https://doi.org/10.1016/j.msec.2017.03.278
- Rosa, V., Della, B. A., Cavalcanti, B. N., & Nor, J. E. (2012). Tissue engineering: From research to dental clinics. Dental Materials, 28(4), 341–348. https://doi.org/10.1016/j.dental.2011.11.025
- Rosa, V., Xie, H., Dubey, N., Madanagopal, T. T., Rajan, S. S., Morin, J. L., Islam, I., & Castro, N. A. (2016). Graphene oxide-based substrate: Physical and surface characterization, cytocompatibility and differentiation potential of dental pulp stem cells. Dental Materials, 32(8), 1019–1025. https://doi.org/10.1016/j.dental.2016.05.008
- Rosa, V., Zhang, Z., Grande, R. H., & Nor, J. E. (2013). Dental pulp tissue engineering in full-length human root canals. Journal of Dental Research, 92(11), 970–975. https://doi.org/10.1177/0022034513505772
- Roseti, L., Parisi, V., Petretta, M., Cavallo, C., Desando, G., Bartolotti, I., & Grigolo, B. (2017). Scaffolds for bone tissue engineering: State of the art and new perspectives. Materials Science and Engineering C, 78, 1246–1262. https://doi.org/10.1016/j.msec.2017.05.017
- Sahu, A., Choi, W. I., & Tae, G. (2012). A stimuli-sensitive injectable graphene oxide composite hydrogel. Chemical Communications, 48(47), 5820–5822. https://doi.org/10.1039/c2cc31862h
- Saidova, A. A., & Vorobjev, I. A. (2020). Lineage commitment, signaling pathways, and the cytoskeleton systems in mesenchymal stem cells. Tissue Engineering Part B Reviews, 26(1), 13–25. https://doi.org/10.1089/ten.TEB.2019.0250
- Schwab, E. H., Halbig, M., Glenske, K., Wagner, A. S., Wenisch, S., & Cavalcanti-Adam, E. A. (2013). Distinct effects of RGD-glycoproteins on Integrin-mediated adhesion and osteogenic differentiation of human mesenchymal stem cells. International Journal of Medical Sciences, 10(13), 1846–1859. https://doi.org/10.7150/ijms.6908
- Schwarz, U. S., Erdmann, T., & Bischofs, I. B. (2006). Focal adhesions as mechanosensors: The two-spring model. Biosystems, 83(2–3), 225–232. https://doi.org/10.1016/j.biosystems.2005.05.019
- Seifi, T., & Kamali, A. R. (2020). Anti-pathogenic activity of graphene nanomaterials: A review. Colloids and Surfaces B: Biointerfaces, 199, 111509. https://doi.org/10.1016/j.colsurfb.2020.111509
- Shafiee, A., & Atala, A. (2017). Tissue engineering: Toward a new era of medicine. Annual Review of Medicine, 68, 29–40. https://doi.org/10.1146/annurev-med-102715-092331
- Shi, L., Chen, J., Teng, L., Wang, L., Zhu, G., Liu, S., Luo, Z., Shi, X., Wang, Y., & Ren, L. (2016). The antibacterial applications of graphene and its derivatives. Small, 12(31), 4165–4184. https://doi.org/10.1002/smll.201601841
- Shie, M. Y., Chiang, W. H., Chen, I. P., Liu, W. Y., & Chen, Y. W. (2017). Synergistic acceleration in the osteogenic and angiogenic differentiation of human mesenchymal stem cells by calcium silicate-graphene composites. Materials Science and Engineering C, 73, 726–735. https://doi.org/10.1016/j.msec.2016.12.071
- Shih, Y. R., Tseng, K. F., Lai, H. Y., Lin, C. H., & Lee, O. K. (2011). Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells. Journal of Bone and Mineral Research, 26(4), 730–738. https://doi.org/10.1002/jbmr.278
- Siednienko, J., Halle, A., Nagpal, K., Golenbock, D. T., & Miggin, S. M. (2010). TLR3-mediated IFN-beta gene induction is negatively regulated by the TLR adaptor MyD88 adaptor-like. European Journal of Immunology, 40(11), 3150–3160. https://doi.org/10.1002/eji.201040547
- Simchi, A., Tamjid, E., Pishbin, F., & Boccaccini, A. R. (2011). Recent progress in inorganic and composite coatings with bactericidal capability for orthopaedic applications. Nanomedicine, 7(1), 22–39. https://doi.org/10.1016/j.nano.2010.10.005
- Song, H. Y., Jeon, E. S., Kim, J. I., Jung, J. S., & Kim, J. H. (2007). Oncostatin M promotes osteogenesis and suppresses adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells. Journal of Cellular Biochemistry, 101(5), 1238–1251. https://doi.org/10.1002/jcb.21245
- Stolyarova, E., Rim, K. T., Ryu, S., Maultzsch, J., Kim, P., Brus, L. E., Heinz, T. F., Hybertsen, M. S., & Flynn, G. W. (2007). High-resolution scanning tunneling microscopy imaging of mesoscopic graphene sheets on an insulating surface. Proceedings of the National Academy of Sciences of the United States of America, 104(22), 9209–9212. https://doi.org/10.1073/pnas.0703337104
- Su, J., Du, Z., Xiao, L., Wei, F., Yang, Y., Li, M., Qiu, Y., Liu, J., Chen, J., & Xiao, Y. (2020). Graphene oxide coated titanium surfaces with osteoimmunomodulatory role to enhance osteogenesis. Materials Science and Engineering C, 113, 110983. https://doi.org/10.1016/j.msec.2020.110983
- Sun, M., Chi, G., Li, P., Lv, S., Xu, J., Xu, Z., Xia, Y., Tan, Y., Xu, J., Li, L., & Li, Y. (2018). Effects of matrix stiffness on the morphology, adhesion, proliferation and osteogenic differentiation of mesenchymal stem cells. International Journal of Medical Sciences, 15(3), 257–268. https://doi.org/10.7150/ijms.21620
- Syama, S., & Mohanan, P. V. (2016). Safety and biocompatibility of graphene: A new generation nanomaterial for biomedical application. International Journal of Biological Macromolecules, 86, 546–555. https://doi.org/10.1016/j.ijbiomac.2016.01.116
- Tan, K. H., Sattari, S., Beyranvand, S., Faghani, A., Ludwig, K., Schwibbert, K., Bottcher, C., Haag, R., & Adeli, M. (2019). Thermoresponsive amphiphilic functionalization of thermally reduced graphene oxide to study Graphene/Bacteria hydrophobic interactions. Langmuir, 35(13), 4736–4746. https://doi.org/10.1021/acs.langmuir.8b03660
- Tarchala, M., Harvey, E. J., & Barralet, J. (2016). Biomaterial-Stabilized soft tissue healing for healing of Critical-Sized bone defects: The masquelet technique. Advanced Healthcare Materials, 5(6), 630–640. https://doi.org/10.1002/adhm.201500793
- Vasilev, K., Cook, J., & Griesser, H. J. (2009). Antibacterial surfaces for biomedical devices. Expert Review of Medical Devices, 6(5), 553–567. https://doi.org/10.1586/erd.09.36
- Wang, C., Lin, K., Chang, J., & Sun, J. (2013). Osteogenesis and angiogenesis induced by porous beta-CaSiO(3)/PDLGA composite scaffold via activation of AMPK/ERK1/2 and PI3K/Akt pathways. Biomaterials, 34(1), 64–77. https://doi.org/10.1016/j.biomaterials.2012.09.021
- Wang, J., Mu, X., & Sun, M. (2019). The thermal, electrical and thermoelectricproperties of graphene nanomaterials. Nanomaterials (Basel), 9(2), 218. https://doi.org/10.3390/nano9020218
- Wang, J., Wang, Y., Liu, D., Yang, Q., Huang, C., Yang, C., & Zhang, Q. (2018). Preparation and cytological study of collagen/nano-hydroxyapatite/graphene oxide composites. Acta of Bioengineering and Biomechanics, 20(4), 65–74.
- Wang, Q., Xu, L., Willumeit-Romer, R., & Luthringer-Feyerabend, B. (2020). Macrophage-derived oncostatin M/bone morphogenetic protein 6 in response to Mg-based materials influences pro-osteogenic activity of human umbilical cord perivascular cells. Acta Biomaterialia. https://doi.org/10.1016/j.actbio.2020.12.016
10.1016/j.actbio.2020.12.016 Google Scholar
- Wang, R., Shi, M., Xu, F., Qiu, Y., Zhang, P., Shen, K., Zhao, Q., Yu, J., & Zhang, Y. (2020). Graphdiyne-modified TiO2 nanofibers with osteoinductive and enhanced photocatalytic antibacterial activities to prevent implant infection. Nature Communications, 11(1), 4465. https://doi.org/10.1038/s41467-020-18267-1
- Wang, S., Duan, C., Yang, W., Gao, X., Shi, J., Kang, J., Deng, Y., Shi, X. L., & Chen, Z. G. (2020). Two-dimensional nanocoating-enabled orthopedic implants for bimodal therapeutic applications. Nanoscale, 12(22), 11936–11946. https://doi.org/10.1039/d0nr02327b
- Wang, S., Zhang, Y., Abidi, N., & Cabrales, L. (2009). Wettability and surface free energy of graphene films. Langmuir, 25(18), 11078–11081. https://doi.org/10.1021/la901402f
- Wang, Y. K., Yu, X., Cohen, D. M., Wozniak, M. A., Yang, M. T., Gao, L., Eyckmans, J., & Chen, C. S. (2012). Bone morphogenetic protein-2-induced signaling and osteogenesis is regulated by cell shape, RhoA/ROCK, and cytoskeletal tension. Stem Cells and Development, 21(7), 1176–1186. https://doi.org/10.1089/scd.2011.0293
- Wei, C., Liu, Z., Jiang, F., Zeng, B., Huang, M., & Yu, D. (2017). Cellular behaviours of bone marrow-derived mesenchymal stem cells towards pristine graphene oxide nanosheets. Cell Proliferation, 50(5), e12367. https://doi.org/10.1111/cpr.12367
- Weng, W., Li, X., Nie, W., Liu, H., Liu, S., Huang, J., Zhou, Q., He, J., Su, J., Dong, Z., & Wang, D. (2020). One-step preparation of an AgNP-nHA@RGO three-dimensional porous scaffold and its application in infected bone defect treatment. International Journal of Nanomedicine, 15, 5027–5042. https://doi.org/10.2147/IJN.S241859
- Wu, C., Wang, G., & Dai, J. (2013). Controlled functionalization of graphene oxide through surface modification with acetone. Journal of Materials Science, 48, 3436–3442. https://doi.org/10.1007/s10853-012-7131-6
- Wu, J., Zheng, A., Liu, Y., Jiao, D., Zeng, D., Wang, X., Cao, L., & Jiang, X. (2019). Enhanced bone regeneration of the silk fibroin electrospun scaffolds through the modification of the graphene oxide functionalized by BMP-2 peptide. International Journal of Nanomedicine, 14, 733–751. https://doi.org/10.2147/IJN.S187664
- Wu, S., Lei, L., Zhang, H., Liu, J., Weir, M. D., Schneider, A., Zhao, L., Liu, J., & Xu, H. (2020). Nanographene oxide-calcium phosphate to inhibit Staphylococcus aureus infection and support stem cells for bone tissue engineering. Journal of Tissue Engineering and Regenerative Medicine, 14(12), 1779–1791. https://doi.org/10.1002/term.3139
- Wu, X., Zheng, S., Ye, Y., Wu, Y., Lin, K., & Su, J. (2018). Enhanced osteogenic differentiation and bone regeneration of poly(lactic-co-glycolic acid) by graphene via activation of PI3K/Akt/GSK-3beta/beta-catenin signal circuit. Biomaterials Science, 6(5), 1147–1158. https://doi.org/10.1039/C8BM00127H
- Xie, C., Lu, X., Han, L., Xu, J., Wang, Z., Jiang, L., Wang, K., Zhang, H., Ren, F., & Tang, Y. (2016). Biomimetic mineralized hierarchical graphene Oxide/Chitosan scaffolds with adsorbability for immobilization of nanoparticles for biomedical applications. ACS Applied Materials & Interfaces, 8(3), 1707–1717. https://doi.org/10.1021/acsami.5b09232
- Xie, H., Cao, T., Franco-Obregon, A., & Rosa, V. (2019). Graphene-Induced osteogenic differentiation is mediated by the Integrin/FAK axis. International Journal of Molecular Sciences, 20(3), 574. https://doi.org/10.3390/ijms20030574
- Xie, H., Cao, T., Gomes, J. V., Castro Neto, A. H., & Rosa, V. (2015). Two and three-dimensional graphene substrates to magnify osteogenic differentiation of periodontal ligament stem cells. Carbon, 93, 266–275. https://doi.org/10.1016/j.carbon.2015.05.071
- Xie, H., Chua, M., Islam, I., Bentini, R., Cao, T., Viana-Gomes, J. C., Castro, N. A., & Rosa, V. (2017). CVD-grown monolayer graphene induces osteogenic but not odontoblastic differentiation of dental pulp stem cells. Dental Materials, 33(1), e13–e21. https://doi.org/10.1016/j.dental.2016.09.030
- Xiong, K., Wu, T., Fan, Q., Chen, L., & Yan, M. (2017). Novel reduced graphene Oxide/Zinc Silicate/Calcium silicate electroconductive biocomposite for stimulating osteoporotic bone regeneration. ACS Applied Materials & Interfaces, 9(51), 44356–44368. https://doi.org/10.1021/acsami.7b16206
- Xu, W. G. (2017). Comparison of intramedullary nail versus conventional ilizarov method for lower limb lengthening: A systematic review and meta-analysis. Orthopaedic Surgery, 9(2), 159–166. https://doi.org/10.1111/os.12330
- Xue, D., Chen, E., Zhong, H., Zhang, W., Wang, S., Joomun, M. U., Yao, T., Tan, Y., Lin, S., Zheng, Q., & Pan, Z. (2018). Immunomodulatory properties of graphene oxide for osteogenesis and angiogenesis. International Journal of Nanomedicine, 13, 5799–5810. https://doi.org/10.2147/IJN.S170305
- Yan, X., Yang, W., Shao, Z., Yang, S., & Liu, X. (2016). Graphene/single-walled carbon nanotube hybrids promoting osteogenic differentiation of mesenchymal stem cells by activating p38 signaling pathway. International Journal of Nanomedicine, 11, 5473–5484. https://doi.org/10.2147/IJN.S115468
- Yang, L., Zhou, J., Yu, K., Yang, S., Sun, T., Ji, Y., Xiong, Z., & Guo, X. (2021). Surface modified small intestinal submucosa membrane manipulates sequential immunomodulation coupled with enhanced angio- and osteogenesis towards ameliorative guided bone regeneration. Materials Science and Engineering C, 119, 111641. https://doi.org/10.1016/j.msec.2020.111641
- Yang, X., Zhao, Q., Chen, Y., Fu, Y., Lu, S., Yu, X., Yu, D., & Zhao, W. (2019). Effects of graphene oxide and graphene oxide quantum dots on the osteogenic differentiation of stem cells from human exfoliated deciduous teeth. Artificial Cells, Nanomedicine, and Biotechnology, 47(1), 822–832. https://doi.org/10.1080/21691401.2019.1576706
- Yao, Q., Jing, J., Zeng, Q., Lu, T. L., Liu, Y., Zheng, X., & Chen, Q. (2017). Bilayered BMP2 eluting coatings on graphene foam by electrophoretic deposition: Electroresponsive BMP2 release and enhancement of osteogenic differentiation. ACS Applied Materials & Interfaces, 9(46), 39962–39970. https://doi.org/10.1021/acsami.7b10180
- Yao, Q., Liu, H., Lin, X., Ma, L., Zheng, X., Liu, Y., Huang, P., Yu, S., Zhang, W., Lin, M., Dai, L., & Liu, Y. (2019). 3D interpenetrated graphene foam/58S bioactive glass scaffolds for electrical-stimulation-assisted differentiation of rabbit mesenchymal stem cells to enhance bone regeneration. Journal of Biomedical Nanotechnology, 15(3), 602–611. https://doi.org/10.1166/jbn.2019.2703
- Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V., & Janmey, P. A. (2005). Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motility and the Cytoskeleton, 60(1), 24–34. https://doi.org/10.1002/cm.20041
- Zhang, G., Zhang, X., Yang, Y., Chi, R., Shi, J., Hang, R., Huang, X., Yao, X., Chu, P. K., & Zhang, X. (2020). Dual light-induced in situ antibacterial activities of biocompatibleTiO2/MoS2/PDA/RGD nanorod arrays on titanium. Biomaterials Science, 8(1), 391–404. https://doi.org/10.1039/c9bm01507h
- Zhang, S., Yang, Q., Zhao, W., Qiao, B., Cui, H., Fan, J., Li, H., Tu, X., & Jiang, D. (2016). In vitro and in vivo biocompatibility and osteogenesis of graphene-reinforced nanohydroxyapatite polyamide66 ternary biocomposite as orthopedic implant material. International Journal of Nanomedicine, 11, 3179–3189. https://doi.org/10.2147/IJN.S105794
- Zhang, W., Chang, Q., Xu, L., Li, G., Yang, G., Ding, X., Wang, X., Cui, D., & Jiang, X. (2016). Graphene oxide-copper Nanocomposite-coated porous CaP scaffold for vascularized bone regeneration via activation of hif-1alpha. Advanced Healthcare Materials, 5(11), 1299–1309. https://doi.org/10.1002/adhm.201500824
- Zhang, X., Wan, S., Pu, J., Wang, L., & Liu, X. (2011). Highly hydrophobic and adhesive performance of graphene films. Journal of Materials Chemistry, 21(33), 12251–12258. https://doi.org/10.1039/C1JM12087E
- Zhang, Y., Bose, T., Unger, R. E., Jansen, J. A., Kirkpatrick, C. J., & van den Beucken, J. (2017). Macrophage type modulates osteogenic differentiation of adipose tissue MSCs. Cell and Tissue Research, 369(2), 273–286. https://doi.org/10.1007/s00441-017-2598-8
- Zhang, Y., Wang, C., Fu, L., Ye, S., Wang, M., & Zhou, Y. (2019). Fabrication and application of novel porous scaffold in situ-loaded graphene oxide and osteogenic peptide by cryogenic 3D printing for repairing critical-sized bone defect. Molecules, 24(9), 1669. https://doi.org/10.3390/molecules24091669
- Zhao, L., Huang, J., Zhang, H., Wang, Y., Matesic, L. E., Takahata, M., Awad, H., Chen, D., & Xing, L. (2011). Tumor necrosis factor inhibits mesenchymal stem cell differentiation into osteoblasts via the ubiquitin E3 ligase Wwp1. Stem Cells, 29(10), 1601–1610. https://doi.org/10.1002/stem.703
- Zhao, M., Dai, Y., Li, X., Li, Y., Zhang, Y., Wu, H., Wen, Z., & Dai, C. (2018). Evaluation of long-term biocompatibility and osteogenic differentiation of graphene nanosheet doped calcium phosphate-chitosan AZ91D composites. Materials Science and Engineering C, 90, 365–378. https://doi.org/10.1016/j.msec.2018.04.082
- Zhao, X., Xie, L., Wang, Z., Wang, J., Xu, H., Han, X., Bai, D., & Deng, P. (2020). ZBP1 (DAI/DLM-1) promotes osteogenic differentiation while inhibiting adipogenic differentiation in mesenchymal stem cells through a positive feedback loop of Wnt/beta-catenin signaling. Bone Research, 8, 12. https://doi.org/10.1038/s41413-020-0085-4
- Zheng, Z., Chen, Y., Hong, H., Shen, Y., Wang, Y., Sun, J., & Wang, X. (2021). The "Yin and Yang" of immunomodulatory magnesium-enriched graphene oxide nanoscrolls decorated biomimetic scaffolds in promoting bone regeneration. Advanced Healthcare Materials, 10(2), e2000631. https://doi.org/10.1002/adhm.202000631
- Zhou, K., Yu, P., Shi, X., Ling, T., Zeng, W., Chen, A., Yang, W., & Zhou, Z. (2019). Hierarchically porous hydroxyapatite hybrid scaffold incorporated with reduced graphene oxide for rapid bone ingrowth and repair. ACS Nano, 13(8), 9595–9606. https://doi.org/10.1021/acsnano.9b04723
- Zhou, P., Xia, D., Ni, Z., Ou, T., Wang, Y., Zhang, H., Mao, L., Lin, K., Xu, S., & Liu, J. (2021). Calcium silicate bioactive ceramics induce osteogenesis through oncostatin M. Bioactive Materials, 6(3), 810–822. https://doi.org/10.1016/j.bioactmat.2020.09.018
- Zhou, T., Li, G., Lin, S., Tian, T., Ma, Q., Zhang, Q., Shi, S., Xue, C., Ma, W., Cai, X., & Lin, Y. (2017). Electrospun poly(3-hydroxybutyrate-co-4-hydroxybutyrate)/graphene oxide scaffold: Enhanced properties and promoted in vivo bone repair in rats. ACS Applied Materials & Interfaces, 9(49), 42589–42600. https://doi.org/10.1021/acsami.7b14267
- Zhou, Z., Xu, Z., Wang, F., Lu, Y., Yin, P., Jiang, C., Liu, Y., Li, H., Yu, X., & Sun, Y. (2016). New strategy to rescue the inhibition of osteogenesis of human bone marrow-derived mesenchymal stem cells under oxidative stress: Combination of vitamin C and graphene foams. Oncotarget, 7(44), 71998–72010. https://doi.org/10.18632/oncotarget.12456
- Zou, M., Sun, J., & Xiang, Z. (2020). Early effect of graphene oxide-carboxymethyl chitosan hydrogel loaded with interleukin 4 and bone morphogenetic protein 2 on bone immunity and repair. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi, 34(8), 1044–1051. https://doi.org/10.7507/1002-1892.201911068
- Zou, X., Zhang, L., Wang, Z., & Luo, Y. (2016). Mechanisms of the antimicrobial activities of graphene materials. Journal of the American Chemical Society, 138(7), 2064–2077. https://doi.org/10.1021/jacs.5b11411
- Zou, Y., Qazvini, N. T., Zane, K., Sadati, M., Wei, Q., Liao, J., Fan, J., Song, D., Liu, J., Ma, C., Qu, X., Chen, L., Yu, X., Zhang, Z., Zhao, C., Zeng, Z., Zhang, R., Yan, S., Wu, T., … Deng, Z. L. (2017). Gelatin-derived graphene-silicate hybrid materials are biocompatible and synergistically promote BMP9-Induced osteogenic differentiation of mesenchymal stem cells. ACS Applied Materials & Interfaces, 9(19), 15922–15932. https://doi.org/10.1021/acsami.7b00272
