Recent advances in application of graphene oxide for bone tissue engineering_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

CHEN Li , DUAN Xin ,  XIANG Zhou

Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

XIANG Zhou, Email: xiangzhou15@hotmail.com

Keywords：

Graphene oxide; bone tissue engineering; scaffold material

DOI：

10.7507/1002-1892.201712063

Video：

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Objective To review the recent advances in the application of graphene oxide (GO) for bone tissue engineering. Methods The latest literature at home and abroad on the GO used in the bone regeneration and repair was reviewed, including general properties of GO, degradation performance, biocompatibility, and application in bone tissue engineering. Results GO has an abundance of oxygen-containing functionalities, high surface area, and good biocompatibility. In addition, it can promote stem cell adhesion, proliferation, and differentiation. Moreover, GO has many advantages in the construction of new composite scaffolds and improvement of the performance of traditional scaffolds. Conclusion GO has been a hot topic in the field of bone tissue engineering due to its excellent physical and chemical properties. And many problems still need to be solved.

Citation： CHEN Li, DUAN Xin, XIANG Zhou. Recent advances in application of graphene oxide for bone tissue engineering. Chinese Journal of Reparative and Reconstructive Surgery, 2018, 32(5): 625-629. doi: 10.7507/1002-1892.201712063 Copy

1.	Shakir M, Jolly R, Khan AA, et al. Resol based chitosan/nano-hydroxyapatite nanoensemble for effective bone tissue engineering. Carbohydr Polym, 2018, 179: 317-327.
2.	Mishra R, Bishop T, Valerio IL, et al. The potential impact of bone tissue engineering in the clinic. Regen Med, 2016, 11(6): 571-587.
3.	Holzapfel BM, Rudert M, Hutmacher DW. Scaffold-based bone tissue engineering. Orthopade, 2017, 46(8): 701-710.
4.	Roseti L, Parisi V, Petretta M, et al. Scaffolds for bone tissue engineering: state of the art and new perspectives. Mater Sci Eng C Mater Biol Appl, 2017, 78: 1246-1262.
5.	Foo ME, Gopinath SCB. Feasibility of graphene in biomedical applications. Biomed Pharmacother, 2017, 94: 354-361.
6.	Lee J, Kim J, Kim S, et al. Biosensors based on graphene oxide and its biomedical application. Adv Drug Deliv Rev, 2016, 105(Pt B): 275-287.
7.	McCallion C, Burthem J, Rees-Unwin K, et al. Graphene in therapeutics delivery: Problems, solutions and future opportunities. Eur J Pharm Biopharm, 2016, 104: 235-250.
8.	Zhao H, Ding R, Zhao X, et al. Graphene-based nanomaterials for drug and/or gene delivery, bioimaging, and tissue engineering. Drug Discov Today, 2017, 22(9): 1302-1317.
9.	Yu P, Bao RY, Shi XJ, et al. Self-assembled high-strength hydroxyapatite/graphene oxide/chitosan composite hydrogel for bone tissue engineering. Carbohydr Polym, 2017, 155: 507-515.
10.	Usman MS, Hussein MZ, Fakurazi S, et al. Gadolinium-based layered double hydroxide and graphene oxide nano-carriers for magnetic resonance imaging and drug delivery. Chem Cent J, 2017, 11(1): 47.
11.	Forsyth R, Devadoss A, Guy OJ. Graphene field effect transistors for biomedical applications: current status and future prospects. Diagnostics (Basel), 2017,7(3): 45.
12.	Pandey RP, Shukla G, Manohar M, et al. Graphene oxide based nanohybrid proton exchange membranes for fuel cell applications: An overview. Adv Colloid Interface Sci, 2017, 240: 15-30.
13.	Georgakilas V, Tiwari JN, Kemp KC, et al. Noncovalent functionalization of graphene and graphene oxide for energy materials, biosensing, catalytic, and biomedical applications. Chem Rev, 2016, 116(9): 5464-5519.
14.	Garcia-Tuñön E, Feilden E, Zheng H, et al. Graphene oxide: an all-in-one processing additive for 3D printing. ACS Appl Mater Interfaces, 2017, 9(38): 32977-32989.
15.	Kumar S, Wani MY, Arranja CT, et al. Synthesis, physicochemical and optical properties of bis-thiosemicarbazone functionalized graphene oxide. Spectrochim Acta A Mol Biomol Spectrosc, 2018, 188: 183-188.
16.	Ur Rahman Z, Pompa L, Haider W. Electrochemical characterization and in-vitro bio-assessment of AZ31B and AZ91E alloys as biodegradable implant materials. J Mater Sci Mater Med, 2015, 26(8): 217.
17.	Prakasam M, Locs J, Salma-Ancane K, et al. Biodegradable materials and metallic implants——A review. J Funct Biomater, 2017, 8(4): 44.
18.	Szeto GL, Lavik EB. Materials design at the interface of nanoparticles and innate immunity. J Mater Chem B, 2016, 4(9): 1610-1618.
19.	Allen BL, Kotchey GP, Chen Y, et al. Mechanistic investigations of horseradish peroxidase-catalyzed degradation of single-walled carbon nanotubes. J Am Chem Soc, 2009, 131(47): 17194-17205.
20.	Kurapati R, Russier J, Squillaci MA, et al. Dispersibility-dependent biodegradation of graphene oxide by myeloperoxidase. Small, 2015,11(32): 3985-3994.
21.	Fahmi T, Branch D, Nima ZA, et al. Mechanism of graphene-induced cytotoxicity: role of endonucleases. J Appl Toxicol, 2017, 37(11): 1325-1332.
22.	Zhou R, Gao H. Cytotoxicity of graphene: recent advances and future perspective. Wiley Interdiscip Rev Nanomed Nanobiotechnol, 2014, 6(5): 452-474.
23.	Wang K, Ruan J, Song H, et al. Biocompatibility of graphene oxide. Nanoscale Res Lett, 2011, 6(1): 8.
24.	Liao KH, Lin YS, Macosko CW, et al. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces, 2011, 3(7): 2607-2615.
25.	Yang K, Wan J, Zhang S, et al. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano, 2011, 5(1): 516-522.
26.	Lee WC, Lim CH, Shi H, et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano, 2011, 5(9): 7334-7341.
27.	Kim J, Kim HD, Park J, et al. Enhanced osteogenic commitment of murine mesenchymal stem cells on graphene oxide substrate. Biomater Res, 2018, 22: 1.
28.	Nayak TR, Andersen H, Makam VS, et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano, 2011, 5(6): 4670-4678.
29.	La WG, Park S, Yoon HH, et al. Delivery of a therapeutic protein for bone regeneration from a substrate coated with graphene oxide. Small, 2013, 9(23): 4051-4060.
30.	Duan S, Yang X, Mei F, et al. Enhanced osteogenic differentiation of mesenchymal stem cells on poly (L-lactide) nanofibrous scaffolds containing carbon nanomaterials. J Biomed Mater Res A, 2015,103(4): 1424-1435.
31.	Wei C, Liu Z, Jiang F, et al. Cellular behaviours of bone marrow-derived mesenchymal stem cells towards pristine graphene oxide nanosheets. Cell Prolif, 2017, 50(5): e12367.
32.	Zhao C, Lu X, Zanden C, et al. The promising application of graphene oxide as coating materials in orthopedic implants: preparation, characterization and cell behavior. Biomed Mater, 2015, 10(1): 15019.
33.	Zhao CH, Pandit S, Fu YF, et al. Graphene oxide based coatings on nitinol for biomedical implant applications: effectively promote mammalian cell growth but kill bacteria. RSC Advances, 2016, 6(44): 38124-38134.
34.	Liu H, Cheng J, Chen F, et al. Gelatin functionalized graphene oxide for mineralization of hydroxyapatite: biomimetic and in vitro evaluation. Nanoscale, 2014, 6(10): 5315-5322.
35.	Jung HS, Lee T, Kwon IK, et al. Surface modification of multipass caliber-rolled Ti alloy with dexamethasone-loaded graphene for dental applications. ACS Appl Mater Interfaces, 2015, 7(18): 9598-9607.
36.	La WG, Jin M, Park S, et al. Delivery of bone morphogenetic protein-2 and substance P using graphene oxide for bone regeneration. Int J Nanomedicine, 2014, 9 Suppl 1: S107-S116.
37.	Kumar S, Chatterjee K. Strontium eluting graphene hybrid nanoparticles augment osteogenesis in a 3D tissue scaffold. Nanoscale, 2015, 7(5): 2023-2033.
38.	Wang SD, Ma Q, Wang K, et al. Strong and biocompatible three-dimensional porous silk fibroin/graphene oxide scaffold prepared by phase separation. Int J Biol Macromol, 2018, 111: 237-246.
39.	Depan D, Girase B, Shah JS, et al. Structure-process-property relationship of the polar graphene oxide-mediated cellular response and stimulated growth of osteoblasts on hybrid chitosan network structure nanocomposite scaffolds. Acta Biomater, 2011, 7(9): 3432-3445.
40.	Luo Y, Shen H, Fang Y, et al. Enhanced proliferation and osteogenic differentiation of mesenchymal stem cells on graphene oxide-incorporated electrospun poly(lactic-co-glycolic acid) nanofibrous mats. ACS Appl Mater Interfaces, 2015, 7(11): 6331-6339.
41.	Shuai CJ, Feng P, Gao CD, et al. Graphene oxide reinforced poly(vinyl alcohol): nanocomposite scaffolds for tissue engineering applications. RSC Aavances, 2015,5(32): 25416-25423.
42.	Zhang C, Wang L, Zhai T, et al. The surface grafting of graphene oxide with poly(ethylene glycol) as a reinforcement for poly(lactic acid) nanocomposite scaffolds for potential tissue engineering applications. J Mech Behav Biomed Mater, 2016, 53: 403-413.
43.	Saravanan S, Chawla A, Vairamani M, et al. Scaffolds containing chitosan, gelatin and graphene oxide for bone tissue regeneration in vitro and in vivo. Int J Biol Macromol, 2017, 104(Pt B): 1975-1985.
44.	Lai PX, Chen CW, Wei SC, et al. Ultrastrong trapping of VEGF by graphene oxide: Anti-angiogenesis application. Biomaterials, 2016, 109: 12-22.
45.	Zhang W, Chang Q, Xu L, et al. Graphene oxide-copper nanocomposite-coated porous CaP scaffold for vascularized bone regeneration via activation of Hif-1α. Adv Healthc Mater, 2016, 5(11): 1299-1309.
46.	Hermenean A, Codreanu A, Herman H, et al. Chitosan-graphene oxide 3D scaffolds as promising tools for bone regeneration in critical-size mouse calvarial defects. Sci Rep, 2017, 7(1): 16641.

1. Shakir M, Jolly R, Khan AA, et al. Resol based chitosan/nano-hydroxyapatite nanoensemble for effective bone tissue engineering. Carbohydr Polym, 2018, 179: 317-327.
2. Mishra R, Bishop T, Valerio IL, et al. The potential impact of bone tissue engineering in the clinic. Regen Med, 2016, 11(6): 571-587.
3. Holzapfel BM, Rudert M, Hutmacher DW. Scaffold-based bone tissue engineering. Orthopade, 2017, 46(8): 701-710.
4. Roseti L, Parisi V, Petretta M, et al. Scaffolds for bone tissue engineering: state of the art and new perspectives. Mater Sci Eng C Mater Biol Appl, 2017, 78: 1246-1262.
5. Foo ME, Gopinath SCB. Feasibility of graphene in biomedical applications. Biomed Pharmacother, 2017, 94: 354-361.
6. Lee J, Kim J, Kim S, et al. Biosensors based on graphene oxide and its biomedical application. Adv Drug Deliv Rev, 2016, 105(Pt B): 275-287.
7. McCallion C, Burthem J, Rees-Unwin K, et al. Graphene in therapeutics delivery: Problems, solutions and future opportunities. Eur J Pharm Biopharm, 2016, 104: 235-250.
8. Zhao H, Ding R, Zhao X, et al. Graphene-based nanomaterials for drug and/or gene delivery, bioimaging, and tissue engineering. Drug Discov Today, 2017, 22(9): 1302-1317.
9. Yu P, Bao RY, Shi XJ, et al. Self-assembled high-strength hydroxyapatite/graphene oxide/chitosan composite hydrogel for bone tissue engineering. Carbohydr Polym, 2017, 155: 507-515.
10. Usman MS, Hussein MZ, Fakurazi S, et al. Gadolinium-based layered double hydroxide and graphene oxide nano-carriers for magnetic resonance imaging and drug delivery. Chem Cent J, 2017, 11(1): 47.
11. Forsyth R, Devadoss A, Guy OJ. Graphene field effect transistors for biomedical applications: current status and future prospects. Diagnostics (Basel), 2017,7(3): 45.
12. Pandey RP, Shukla G, Manohar M, et al. Graphene oxide based nanohybrid proton exchange membranes for fuel cell applications: An overview. Adv Colloid Interface Sci, 2017, 240: 15-30.
13. Georgakilas V, Tiwari JN, Kemp KC, et al. Noncovalent functionalization of graphene and graphene oxide for energy materials, biosensing, catalytic, and biomedical applications. Chem Rev, 2016, 116(9): 5464-5519.
14. Garcia-Tuñön E, Feilden E, Zheng H, et al. Graphene oxide: an all-in-one processing additive for 3D printing. ACS Appl Mater Interfaces, 2017, 9(38): 32977-32989.
15. Kumar S, Wani MY, Arranja CT, et al. Synthesis, physicochemical and optical properties of bis-thiosemicarbazone functionalized graphene oxide. Spectrochim Acta A Mol Biomol Spectrosc, 2018, 188: 183-188.
16. Ur Rahman Z, Pompa L, Haider W. Electrochemical characterization and in-vitro bio-assessment of AZ31B and AZ91E alloys as biodegradable implant materials. J Mater Sci Mater Med, 2015, 26(8): 217.
17. Prakasam M, Locs J, Salma-Ancane K, et al. Biodegradable materials and metallic implants——A review. J Funct Biomater, 2017, 8(4): 44.
18. Szeto GL, Lavik EB. Materials design at the interface of nanoparticles and innate immunity. J Mater Chem B, 2016, 4(9): 1610-1618.
19. Allen BL, Kotchey GP, Chen Y, et al. Mechanistic investigations of horseradish peroxidase-catalyzed degradation of single-walled carbon nanotubes. J Am Chem Soc, 2009, 131(47): 17194-17205.
20. Kurapati R, Russier J, Squillaci MA, et al. Dispersibility-dependent biodegradation of graphene oxide by myeloperoxidase. Small, 2015,11(32): 3985-3994.
21. Fahmi T, Branch D, Nima ZA, et al. Mechanism of graphene-induced cytotoxicity: role of endonucleases. J Appl Toxicol, 2017, 37(11): 1325-1332.
22. Zhou R, Gao H. Cytotoxicity of graphene: recent advances and future perspective. Wiley Interdiscip Rev Nanomed Nanobiotechnol, 2014, 6(5): 452-474.
23. Wang K, Ruan J, Song H, et al. Biocompatibility of graphene oxide. Nanoscale Res Lett, 2011, 6(1): 8.
24. Liao KH, Lin YS, Macosko CW, et al. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces, 2011, 3(7): 2607-2615.
25. Yang K, Wan J, Zhang S, et al. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano, 2011, 5(1): 516-522.
26. Lee WC, Lim CH, Shi H, et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano, 2011, 5(9): 7334-7341.
27. Kim J, Kim HD, Park J, et al. Enhanced osteogenic commitment of murine mesenchymal stem cells on graphene oxide substrate. Biomater Res, 2018, 22: 1.
28. Nayak TR, Andersen H, Makam VS, et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano, 2011, 5(6): 4670-4678.
29. La WG, Park S, Yoon HH, et al. Delivery of a therapeutic protein for bone regeneration from a substrate coated with graphene oxide. Small, 2013, 9(23): 4051-4060.
30. Duan S, Yang X, Mei F, et al. Enhanced osteogenic differentiation of mesenchymal stem cells on poly (L-lactide) nanofibrous scaffolds containing carbon nanomaterials. J Biomed Mater Res A, 2015,103(4): 1424-1435.
31. Wei C, Liu Z, Jiang F, et al. Cellular behaviours of bone marrow-derived mesenchymal stem cells towards pristine graphene oxide nanosheets. Cell Prolif, 2017, 50(5): e12367.
32. Zhao C, Lu X, Zanden C, et al. The promising application of graphene oxide as coating materials in orthopedic implants: preparation, characterization and cell behavior. Biomed Mater, 2015, 10(1): 15019.
33. Zhao CH, Pandit S, Fu YF, et al. Graphene oxide based coatings on nitinol for biomedical implant applications: effectively promote mammalian cell growth but kill bacteria. RSC Advances, 2016, 6(44): 38124-38134.
34. Liu H, Cheng J, Chen F, et al. Gelatin functionalized graphene oxide for mineralization of hydroxyapatite: biomimetic and in vitro evaluation. Nanoscale, 2014, 6(10): 5315-5322.
35. Jung HS, Lee T, Kwon IK, et al. Surface modification of multipass caliber-rolled Ti alloy with dexamethasone-loaded graphene for dental applications. ACS Appl Mater Interfaces, 2015, 7(18): 9598-9607.
36. La WG, Jin M, Park S, et al. Delivery of bone morphogenetic protein-2 and substance P using graphene oxide for bone regeneration. Int J Nanomedicine, 2014, 9 Suppl 1: S107-S116.
37. Kumar S, Chatterjee K. Strontium eluting graphene hybrid nanoparticles augment osteogenesis in a 3D tissue scaffold. Nanoscale, 2015, 7(5): 2023-2033.
38. Wang SD, Ma Q, Wang K, et al. Strong and biocompatible three-dimensional porous silk fibroin/graphene oxide scaffold prepared by phase separation. Int J Biol Macromol, 2018, 111: 237-246.
39. Depan D, Girase B, Shah JS, et al. Structure-process-property relationship of the polar graphene oxide-mediated cellular response and stimulated growth of osteoblasts on hybrid chitosan network structure nanocomposite scaffolds. Acta Biomater, 2011, 7(9): 3432-3445.
40. Luo Y, Shen H, Fang Y, et al. Enhanced proliferation and osteogenic differentiation of mesenchymal stem cells on graphene oxide-incorporated electrospun poly(lactic-co-glycolic acid) nanofibrous mats. ACS Appl Mater Interfaces, 2015, 7(11): 6331-6339.
41. Shuai CJ, Feng P, Gao CD, et al. Graphene oxide reinforced poly(vinyl alcohol): nanocomposite scaffolds for tissue engineering applications. RSC Aavances, 2015,5(32): 25416-25423.
42. Zhang C, Wang L, Zhai T, et al. The surface grafting of graphene oxide with poly(ethylene glycol) as a reinforcement for poly(lactic acid) nanocomposite scaffolds for potential tissue engineering applications. J Mech Behav Biomed Mater, 2016, 53: 403-413.
43. Saravanan S, Chawla A, Vairamani M, et al. Scaffolds containing chitosan, gelatin and graphene oxide for bone tissue regeneration in vitro and in vivo. Int J Biol Macromol, 2017, 104(Pt B): 1975-1985.
44. Lai PX, Chen CW, Wei SC, et al. Ultrastrong trapping of VEGF by graphene oxide: Anti-angiogenesis application. Biomaterials, 2016, 109: 12-22.
45. Zhang W, Chang Q, Xu L, et al. Graphene oxide-copper nanocomposite-coated porous CaP scaffold for vascularized bone regeneration via activation of Hif-1α. Adv Healthc Mater, 2016, 5(11): 1299-1309.
46. Hermenean A, Codreanu A, Herman H, et al. Chitosan-graphene oxide 3D scaffolds as promising tools for bone regeneration in critical-size mouse calvarial defects. Sci Rep, 2017, 7(1): 16641.

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