journal article·2024-02-12Open access

Enhanced Osteogenic Activity and Antibacterial Properties of Graphene Oxide-Poly(Lactic Acid) Films for the Repair of Cranial Defects in Rats

Kai Liu, Wen Lai, Jianyong Wu, Yongjian Lu

Coatings· Volume 14· Issue 2

Abstract

The failure of bone defect repair caused by bacterial infection is a significant clinical challenge. However, the currently utilized bone graft materials lack antibacterial properties, necessitating the development of bone repair materials with both osteoinductive and antibacterial capabilities. Graphene oxide (GO) has garnered considerable attention due to its distinctive physical, chemical, and biological characteristics. In this study, we prepared a graphene oxide-poly(lactic acid) (GO-PLA) film with exceptional biological properties. In vitro investigations demonstrated that the GO-PLA film substantially enhanced the adhesion and proliferation capacity of rat bone marrow mesenchymal stem cells (rBMSCs). Furthermore, we observed augmented alkaline phosphatase activity as well as increased expression levels of osteogenic genes in rBMSCs cultured on the GO-PLA film. Additionally, we evaluated the antibacterial activity of our samples using gram-positive Streptococcus mutans (Sm) and gram-negative Actinobacillus actinomycetemcomitans (Aa). Our findings revealed that GO doping significantly inhibited bacterial growth. Moreover, implantation experiments conducted on rat skull defects demonstrated excellent guided bone regeneration performance exhibited by the GO-PLA film. Overall, our results indicate that the GO-PLA film possesses outstanding osteogenic and antibacterial properties, making it a promising biomaterial for bone tissue regeneration.
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Research context

OpenAlex topics: Graphene and Nanomaterials Applications · Bone Tissue Engineering Materials · Nanoparticles: synthesis and applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Stomatology, Xinhua Hospital Affiliated to Shanghai Jiaotong University School of Medicine, Kongjiang Road 1665, Shanghai 200092, China

Shanghai Jing-An Dental Clinic, Pingxingguan Road 15, Shanghai 200070, China

Funding

Xinhua Hospital Affiliated to Shanghai Jiaotong University School of Medicine Rolling fund for scientific research and Development

References (72)

Show source-provided references
1. Additively Manufactured Macroporous Titanium with Silver-Releasing Micro-/Nanoporous Surface for Multipurpose Infection Control and Bone Repair—A Proof of Concept10.1021/acsami.6b10473 ↗
2. Dual-Functional 3D-Printed Composite Scaffold for Inhibiting Bacterial Infection and Promoting Bone Regeneration in Infected Bone Defect Models10.1016/j.actbio.2018.08.015 ↗
3. The Roles of Signaling Pathways in Bone Repair and Regeneration10.1002/jcp.26042 ↗
4. Graphene-Based Material-Mediated Immunomodulation in Tissue Engineering and Regeneration: Mechanism and Significance10.1021/acsnano.3c03857 ↗
5. Bone Tissue Engineering Scaffolds: Function of Multi-Material Hierarchically Structured Scaffolds10.1002/adhm.202202766 ↗
6. Multifunctional Copper-Containing Carboxymethyl Chitosan/Alginate Scaffolds for Eradicating Clinical Bacterial Infection and Promoting Bone Formation10.1021/acsami.7b13750 ↗
7. The Antibacterial Effect, Biocompatibility, and Osteogenesis of Vancomycin-Nanodiamond Composite Scaffold for Infected Bone Defects10.2147/IJN.S397316 ↗
8. Yao, H., Wang, J., Deng, Y., Li, Z., and Wei, J. (2023). Osteogenic and Antibacterial PLLA Membrane for Bone Tissue Engineering. Int. J. Biol. Macromol., 247.10.1016/j.ijbiomac.2023.125671 ↗
9. Graphene Oxide as a Chemically Tunable Platform for Optical Applications10.1038/nchem.907 ↗
10. Enhanced Differentiation of Human Neural Stem Cells into Neurons on Graphene10.1002/adma.201101503 ↗
11. Engineering of Gadolinium-Decorated Graphene Oxide Nanosheets for Multimodal Bioimaging and Drug Delivery10.1021/acsomega.9b00883 ↗
12. Fast and Sensitive Graphene oxide-DNAzyme-based Biosensor for Vibrio Alginolyticus Detection10.1111/jfd.13594 ↗
13. Functionalized Graphene Oxide as a Vehicle for Targeted Drug Delivery and Bioimaging Applications10.1039/D0TB01149E ↗
14. Holt, B.D., Wright, Z.M., Arnold, A.M., and Sydlik, S.A. (2017). Graphene Oxide as a Scaffold for Bone Regeneration. WIREs Nanomed. Nanobiotechnol., 9.10.1002/wnan.1437 ↗
15. Enhanced Osteogenic Differentiation of Stem Cells on Phase-Engineered Graphene Oxide10.1021/acsami.8b02225 ↗
16. Enhanced Osteogenic Differentiation of BMSCs and M2-Phenotype Polarization of Macrophages on a Titanium Surface Modified with Graphene Oxide for Potential Implant Applications10.1039/C9RA10563H ↗
17. Graphene Oxide-Modified Concentric Microgrooved Titanium Surfaces for the Dual Effects of Osteogenesis and Antiosteoclastogenesis10.1021/acsami.2c14271 ↗
18. Biomineralized Poly(L-Lactic-Co-Glycolic Acid)/Graphene Oxide/Tussah Silk Fibroin Nanofiber Scaffolds with Multiple Orthogonal Layers Enhance Osteoblastic Differentiation of Mesenchymal Stem Cells10.1021/acsbiomaterials.6b00533 ↗
19. Biocompatible Graphene Oxide–Collagen Composite Aerogel for Enhanced Stiffness and in Situ Bone Regeneration10.1016/j.msec.2019.110137 ↗
20. Electron Transfer Directed Antibacterial Properties of Graphene Oxide on Metals10.1002/adma.201702149 ↗
21. Killing Dental Pathogens Using Antibacterial Graphene Oxide10.1021/acsami.5b01069 ↗
22. Wrinkled Surface-Mediated Antibacterial Activity of Graphene Oxide Nanosheets10.1021/acsami.6b15085 ↗
23. Antibacterial Activity of Graphite, Graphite Oxide, Graphene Oxide, and Reduced Graphene Oxide: Membrane and Oxidative Stress10.1021/nn202451x ↗
24. Graphene Oxide Exhibits Differential Mechanistic Action towards Gram-Positive and Gram-Negative Bacteria10.1016/j.colsurfb.2019.05.023 ↗
25. Influences of Graphene Oxide on Biofilm Formation of Gram-Negative and Gram-Positive Bacteria10.1007/s11356-017-0616-8 ↗
26. Layer-Number Dependent Antibacterial and Osteogenic Behaviors of Graphene Oxide Electrophoretic Deposited on Titanium10.1021/acsami.7b00314 ↗
27. Cytotoxicity Effects of Graphene and Single-Wall Carbon Nanotubes in Neural Phaeochromocytoma-Derived PC12 Cells10.1021/nn1007176 ↗
28. Li, G., Zhao, M., Xu, F., Yang, B., Li, X., Meng, X., Teng, L., Sun, F., and Li, Y. (2020). Synthesis and Biological Application of Polylactic Acid. Molecules, 25.10.3390/molecules25215023 ↗
29. Haroosh, H.J., Dong, Y., Jasim, S., and Ramakrishna, S. (2021). Improvement of Drug Release and Compatibility between Hydrophilic Drugs and Hydrophobic Nanofibrous Composites. Materials, 14.10.3390/ma14185344 ↗
30. A Review of Current Advancements for Wound Healing: Biomaterial Applications and Medical Devices10.1002/jbm.b.35086 ↗
31. Effect of Polylactic Acid Membrane on Guided Bone Regeneration in Anterior Maxillary Implantation10.12659/MSM.938566 ↗
32. 3D Printed Membranes of Polylactic Acid and Graphene Oxide for Guided Bone Regeneration10.1039/D3NA00112A ↗
33. Zhou, X., Zhou, G., Junka, R., Chang, N., Anwar, A., Wang, H., and Yu, X. (2021). Fabrication of Polylactic Acid (PLA)-Based Porous Scaffold through the Combination of Traditional Bio-Fabrication and 3D Printing Technology for Bone Regeneration. Colloids Surf. B Biointerfaces, 197.10.1016/j.colsurfb.2020.111420 ↗
34. Inside-Outside Ag Nanoparticles-Loaded Polylactic Acid Electrospun Fiber for Long-Term Antibacterial and Bone Regeneration10.1016/j.ijbiomac.2020.11.088 ↗
35. Strontium-Incorporated Mineralized PLLA Nanofibrous Membranes for Promoting Bone Defect Repair10.1016/j.colsurfb.2019.04.011 ↗
36. The Treatment Efficacy of Bone Tissue Engineering Strategy for Repairing Segmental Bone Defects Under Osteoporotic Conditions10.1089/ten.tea.2015.0071 ↗
37. Double-Edged Effects and Mechanisms of Zn2+ Microenvironments on Osteogenic Activity of BMSCs: Osteogenic Differentiation or Apoptosis10.1039/D0RA01465F ↗
38. Evaluation of Bone Regeneration Using the Rat Critical Size Calvarial Defect10.1038/nprot.2012.113 ↗
39. Preparation of Polylactic Acid/TiO2/GO Nano-Fibrous Films and Their Preservation Effect on Green Peppers10.1016/j.ijbiomac.2021.02.125 ↗
40. Antibacterial Biomaterials in Bone Tissue Engineering10.1039/D0TB02983A ↗
41. Treatment Options for Infected Bone Defects in the Lower Extremities: Free Vascularized Fibular Graft or Ilizarov Bone Transport?10.1186/s13018-020-01907-z ↗
42. Biomaterial-Centered Infection: Microbial Adhesion Versus Tissue Integration10.1126/science.3629258 ↗
43. Antibiotic Prescribing Practices in Periodontal Surgeries with and without Bone Grafting10.1002/JPER.19-0195 ↗
44. Antibiotic-Loaded Nanoparticles Targeted to the Site of Infection Enhance Antibacterial Efficacy10.1038/s41551-017-0187-5 ↗
45. Silver Nanoparticles as Potential Antibacterial Agents10.3390/molecules20058856 ↗
46. The Antimicrobial Activity of Nanoparticles: Present Situation and Prospects for the Future10.2147/IJN.S121956 ↗
47. Translating Musculoskeletal Bioengineering into Tissue Regeneration Therapies10.1126/scitranslmed.abn9074 ↗
48. Synthesis and Functionalization of Graphene Materials for Biomedical Applications: Recent Advances, Challenges, and Perspectives10.1002/advs.202205292 ↗
49. Bhatt, S., Punetha, V.D., Pathak, R., and Punetha, M. (2023). Graphene in Nanomedicine: A Review on Nano-Bio Factors and Antibacterial Activity. Colloids Surf. B Biointerfaces, 226.10.1016/j.colsurfb.2023.113323 ↗
50. Self-Targeting Nanotherapy Based on Functionalized Graphene Oxide for Synergistic Thermochemotherapy10.1016/j.jcis.2021.06.072 ↗
51. Multifunctional Graphene Oxide Nanoparticles for Drug Delivery in Cancer10.1016/j.jconrel.2022.08.011 ↗
52. Graphene-Based Nanomaterials for Bioimaging10.1016/j.addr.2016.05.013 ↗
53. Cytotoxic Evaluation of Nanostructured Zinc Oxide (ZnO) Thin Films and Leachates10.1016/j.tiv.2014.05.004 ↗
54. Involvement of FAK/P38 Signaling Pathways in Mediating the Enhanced Osteogenesis Induced by Nano-Graphene Oxide Modification on Titanium Implant Surface10.2147/IJN.S245608 ↗
55. Biocompatibility of Graphene Oxide10.1007/s11671-010-9751-6 ↗
56. MC3T3-E1 Pre-Osteoblast Response and Differentiation after Graphene Oxide Nanosheet Uptake10.1016/j.colsurfb.2017.06.019 ↗
57. Unraveling Stress-Induced Toxicity Properties of Graphene Oxide and the Underlying Mechanism10.1002/adma.201202678 ↗
58. Wang, Q., Li, M., Cui, T., Wu, R., Guo, F., Fu, M., Zhu, Y., Yang, C., Chen, B., and Sun, G. (2023). A Novel Zwitterionic Hydrogel Incorporated with Graphene Oxide for Bone Tissue Engineering: Synthesis, Characterization, and Promotion of Osteogenic Differentiation of Bone Mesenchymal Stem Cells. Int. J. Mol. Sci., 24.10.3390/ijms24032691 ↗
59. Fibrin Glue/Fibronectin/Heparin-Based Delivery System of BMP2 Induces Osteogenesis in MC3T3-E1 Cells and Bone Formation in Rat Calvarial Critical-Sized Defects10.1021/acsami.0c01371 ↗
60. Osteocalcin and Osteopontin Influence Bone Morphology and Mechanical Properties10.1111/nyas.13470 ↗
61. Characterization of Adhesion and Differentiation Markers of Osteogenic Marrow Stromal Cells10.1002/jcp.20109 ↗
62. Graphene Family Nanomaterials for Stem Cell Neurogenic Differentiation and Peripheral Nerve Regeneration10.1021/acsabm.2c00663 ↗
63. Bayaraa, O., Dashnyam, K., Singh, R.K., Mandakhbayar, N., Lee, J.H., Park, J.-T., Lee, J.-H., and Kim, H.-W. (2023). Nanoceria-GO-Intercalated Multicellular Spheroids Revascularize and Salvage Critical Ischemic Limbs through Anti-Apoptotic and pro-Angiogenic Functions. Biomaterials, 292.10.1016/j.biomaterials.2022.121914 ↗
64. Enhanced Osteogenic Differentiation and Bone Regeneration of Poly(Lactic-Co-Glycolic Acid) by Graphene via Activation of PI3K/Akt/GSK-3β/β-Catenin Signal Circuit10.1039/C8BM00127H ↗
65. Enhanced Proliferation and Osteogenic Differentiation of Mesenchymal Stem Cells on Graphene Oxide-Incorporated Electrospun Poly(Lactic-Co-Glycolic Acid) Nanofibrous Mats10.1021/acsami.5b00862 ↗
66. Antibacterial activity, bio-compatibility and osteogenic differentiation of graphene oxide coating on 3D-network poly-ether-ether-ketone for orthopaedic implants10.1007/s10856-021-06614-7 ↗
67. Graphene oxide-coated porous titanium for pulp sealing: An antibacterial and dentino-inductive restorative material10.1039/D0TB00697A ↗
68. Mechanisms of the Antimicrobial Activities of Graphene Materials10.1021/jacs.5b11411 ↗
69. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets10.1038/nnano.2013.125 ↗
70. Control of the Graphene–Protein Interface Is Required to Preserve Adsorbed Protein Function10.1021/ac303268z ↗
71. Mohammed, H., Kumar, A., Bekyarova, E., Al-Hadeethi, Y., Zhang, X., Chen, M., Ansari, M.S., Cochis, A., and Rimondini, L. (2020). Antimicrobial Mechanisms and Effectiveness of Graphene and Graphene-Functionalized Biomaterials. A Scope Review. Front. Bioeng. Biotechnol., 8.10.3389/fbioe.2020.00465 ↗
72. Pathmanapan, S., Periyathambi, P., and Anandasadagopan, S.K. (2020). Fibrin hydrogel incorporated with graphene oxide functionalized nanocomposite scaffolds for bone repair—In vitro and in vivo study. Nanomed. Nanotechnol. Biol. Med., 29.10.1016/j.nano.2020.102251 ↗