Biomimetic mineralization and cytocompatibility of nanorod hydroxyapatite/graphene oxide composites

Abstract

Nanorod hydroxyapatite (NRHA)/graphene oxide (GO) composites with weight ratios of 0.4, 1.5, and 5 have been fabricated by a facile ultrasonic-assisted method at room temperature and atmospheric pressure. The chemical structure properties and morphology of the composites were characterized by field emission source scanning electron microscope, X-ray diffraction, transmission electron microscopy, and high-resolution transmission electron microscopy. The results indicate that the NRHA/GO composites have an irregular surface with different degree wrinkles and are stable, and NRHA are well combined with GO. In addition, the biomimetic mineralization mechanism of hydroxyapatite on the NRHA/GO composites in simulated body fluid (SBF) is presented. The presence of a bone-like apatite layer on the composite surface indicate that the NRHA/GO composites facilitate the nucleation and growth of hydroxyapatite crystals in SBF for biomimetic mineralization. Moreover, the NRHA-1.5/GO composite and pure GO were cultured with MC3T3-E1 cells to investigate the proliferation and adhesion of cells. In vitro cytocompatibility evaluation demonstrated that the NRHA/GO composite can act as a good template for the growth and adhesion of cells. Therefore, the NRHA/GO composite could be applied as a GO-based, free-template, non-toxic, and bioactive composite to substitute for a damaged or defect bone.

Graphical abstract

Keywords

hydroxyapatite / graphene oxide / biomimetic mineralization / cytocompatibility

References

[1] Shi Y Y, Li M, Liu Q, Jia Z J, Xu X C, Cheng Y, Zheng Y F. Electrophoretic deposition of graphene oxide reinforced chitosan-hydroxyapatite nanocomposite coatings on Ti substrate. Journal of Materials Science. Materials in Medicine, 2016, 27(3): 48

[2] Li M, Liu Q, Jia Z J, Xu X C, Shi Y Y, Cheng Y, Zheng Y F, Xi T F, Wei S C. Electrophoretic deposition and electrochemical behavior of novel graphene oxide-hyaluronic acid-hydroxyapatite nanocomposite coatings. Applied Surface Science, 2013, 284: 804–810

[3] Li P, Sun S Y, Dong A, Hao Y P, Shi S Q, Sun Z J, Gao G, Chen Y X. Developing of a novel antibacterial agent by functionalization of graphene oxide with guanidine polymer with enhanced antibacterial activity. Applied Surface Science, 2015, 355: 446–452

[4] Wang K W, Zhu Y J, Chen F, Cheng G F, Huang Y H. Microwave-assisted synthesis of hydroxyapatite hollow microspheres in aqueous solution. Materials Letters, 2011, 65(15-16): 2361–2363

[5] Kumar S, Chatterjee K. Comprehensive review on the use of graphene-based substrates for regenerative medicine and biomedical devices. ACS Applied Materials & Interfaces, 2016, 8(40): 26431–26457

[6] Liu L P, Yang X N, Ye L, Xue D D, Liu M, Jia S R, Hou Y, Chu L Q, Zhong C. Preparation and characterization of a photocatalytic antibacterial material: Graphene oxide/TiO₂/bacterial cellulose nanocomposite. Carbohydrate Polymers, 2017, 174: 1078–1086

[7] Li Q, Yong C Y, Cao W W, Wang X, Wang L N, Zhou J, Xing X D. Fabrication of charge reversible graphene oxide-based nanocomposite with multiple antibacterial modes and magnetic recyclability. Journal of Colloid and Interface Science, 2017, 511: 285–295

[8] Xie X Y, Hu K W, Fang D D, Shang L H, Tran S D, Cerruti M. Graphene and hydroxyapatite self-assemble into homogeneous, free standing nanocomposite hydrogels for bone tissue engineering. Nanoscale, 2015, 7(17): 7992–8002

[9] Moosavi R, Ramanathan S, Lee Y Y, Siew L K C, Afkhami A, Archunan G, Padmanabhan P, Gulyás B, Kakran M, Selvan S T. Synthesis of antibacterial and magneticnanocomposites by decorating graphene oxide surface with metal nanoparticles. RSC Advances, 2015, 5(93): 76442–76450

[10] Wei G, Zhang J T, Xie L, Jandt K D. Biomimetic growth of hydroxyapatite on super water-soluble carbon nanotube-protein hybrid nanofibers. Carbon, 2011, 49(7): 2216–2226

[11] Wei G, Reichert J, Bossert J, Jandt K D. Novel biopolymeric template for the nucleation and growth of hydroxyapatite crystals based on self-assembled fibrinogen fibrils. Biomacromolecules, 2008, 9(11): 3258–3267

[12] Wang J H, Wang H X, Wang Y Z, Li J F, Su Z Q, Wei G. Alternate layer-by-layer assembly of graphene oxide nanosheets and fibrinogen nanofibers on a silicon substrate for a biomimetic three-dimensional hydroxyapatite scaffold. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2014, 2(42): 7360–7368

[13] Kaur B, Srivastava R, Satpati B, Kondepudi K K, Bishnoi M. Biomineralization of hydroxyapatite in silver ion-exchanged nanocrystalline ZSM-5 zeolite using simulated body fluid. Colloids and Surfaces. B, Biointerfaces, 2015, 135: 201–208

[14] Yu W, Wang X X, Zhao J L, Tang Q G, Wang M L, Ning X W. Preparation and mechanical properties of reinforced hydroxyapatite bone cement with nano-ZrO₂. Ceramics International, 2015, 41(9): 10600–11060

[15] Shen J, Jin B, Qi Y C, Jiang Q Y, Gao X F. Carboxylated chitosan/silver-hydroxyapatite hybrid microspheres with improved antibacterial activity and cytocompatibility. Materials Science and Engineering C, 2017, 78: 589–597

[16] Jadalannagari S, Deshmukh K, Ramanan S R, Kowshik M. Antimicrobial activity of hemocompatible silver doped hydroxyapatite nanoparticles synthesized by modified sol-gel technique. Applied Nanoscience, 2013, 4(2): 133–141

[17] Lin K L, Wu C T, Chang J. Advances in synthesis of calcium phosphate crystals with controlled size and shape. Acta Biomaterialia, 2014, 10(10): 4071–4102

[18] Raucci M G, Giugliano D, Longo A, Zeppetelli S, Carotenuto G, Ambrosio L. Comparative facile methods for preparing graphene oxide-hydroxyapatite for bone tissue engineering. Journal of Tissue Engineering and Regenerative Medicine, 2016, 11(8): 2204–2216

[19] Santos C, Almeida M M, Costa M E. Morphological evolution of hydroxyapatite particles in the presence of different citrate: Calcium ratios. Crystal Growth & Design, 2015, 15(9): 4417–4426

[20] Zhao X Y, Zhu Y J, Chen F, Lu B Q, Wu J. Nanosheet-assembled hierarchical nanostructures of hydroxyapatite: Surfactant-free microwave-hydrothermal rapid synthesis, protein/DNA adsorption and pH-controlled release. CrystEngComm, 2013, 15(1): 206–212

[21] Fan Z J, Wang J Q, Wang Z F, Ran H Q, Li Y, Niu L Y, Gong P W, Liu B, Yang S R. One-pot synthesis of graphene/hydroxyapatite nanorod composite for tissue engineering. Carbon, 2014, 66: 407–416

[22] Fielding G A, Roy M, Bandyopadhyay A, Bose S. Antibacterial and biological characteristics of silver containing and strontium doped plasma sprayed hydroxyapatite coatings. Acta Biomaterialia, 2012, 8(8): 3144–3152

[23] Gao F, Xu C Y, Hu H T, Wang Q, Gao Y Y, Chen H, Guo Q N, Chen D N, Eder D. Biomimetic synthesis and characterization of hydroxyapatite/graphene oxide hybrid coating on Mg alloy with enhanced corrosion resistance. Materials Letters, 2015, 138: 25–28

[24] Liu H Y, Xi P X, Xie G Q, Shi Y J, Hou F P, Huang L, Chen F J, Zeng Z Z, Shao C W, Wang J. Simultaneous reduction and surface functionalization of graphene oxide for hydroxyapatite mineralization. Journal of Physical Chemistry C, 2012, 116(5): 3334–3341

[25] Baradaran S, Moghaddam E, Basirun W J, Mehrali M, Sookhakian M, Hamdi M, Moghaddam N M R, Alias Y. Mechanical properties and biomedical applications of a nanotube hydroxyapatite-reduced graphene oxide composite. Carbon, 2014, 69: 32–45

[26] Bharath G, Madhu R, Chen S M, Veeramani V, Balamurugan A, Mangalaraj D, Viswanathan C, Ponpandian N. Enzymatic electrochemical glucose biosensors by mesoporous 1D hydroxyapatite-on-2D reduced graphene oxide. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2015, 3(7): 1360–1370

[27] Li M, Liu Q, Jia Z J, Xu X C, Cheng Y, Zheng Y F, Xi T F, Wei S C. Graphene oxide/hydroxyapatite composite coatings fabricated by electrophoretic nanotechnology for biological applications. Carbon, 2014, 67: 185–197

[28] Ma H B, Su W X, Tai Z X, Sun D F, Yan X B, Liu B, Xue Q J. Preparation and cytocompatibility of polylactic acid/hydroxyapatite/graphene oxide nanocomposite fibrous membrane. Chinese Science Bulletin, 2012, 57(23): 3051–3058

[29] Zhu J T, Wong H M, Kwok Y K W, Tjong S C. Spark plasma sintered hydroxyapatite/graphite nanosheet and hydroxyapatite/multiwalled carbon nanotube composites: Mechanical and in vitro cellular properties. Advanced Engineering Materials, 2011, 13(4): 336–341

[30] Rajesh R, Ravichandran D Y. Development of new graphene oxide incorporated tricomponent scaffolds with polysaccharides and hydroxyapatite and study of their osteoconductivity on MG-63 cell line for bone tissue engineering. RSC Advances, 2015, 5(51): 41135–41143

[31] Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials, 2006, 27(15): 2907–2915

[32] Zhang M F, Li Y Z, Su Z Q, Wei G. Recent advances in the synthesis and applications of graphene-polymer nanocomposites. Polymer Chemistry, 2015, 6(34): 6107–6124

[33] Chen F, Zhu Y J, Wang K W, Zhao K L. Surfactant-free solvothermal synthesis of hydroxyapatite nanowire/nanotube ordered arrays with biomimetic structures. CrystEngComm, 2011, 13(6): 1858–1863

[34] Xiong G Y, Luo H L, Zuo G F, Ren K J, Wan Y Z. Novel porous graphene oxide and hydroxyapatite nanosheets-reinforced sodium alginate hybrid nanocomposites formedical applications. Materials Characterization, 2015, 107: 419–425

[35] Shen J, Jin B, Jiang Q Y, Hu Y M, Wang X Y. Morphology-controlled synthesis of fluorapatite nano/microstructures via surfactant-assisted hydrothermal process. Materials & Design, 2016, 97: 204–212

[36] Roach P, Eglin D, Rohde K, Perry C C. Modern biomaterials: A review-bulk properties and implications of surface modifications. Journal of Materials Science. Materials in Medicine, 2007, 18(7): 1263–1277

[37] Mehrali M, Moghaddam E, Seyed S S F, Baradaran S, Mehrali M, Latibari S T, Cornelis M H S, Kadri N A, Zandi K, Abu O N A. Mechanical and in vitro biological performance of graphene nanoplatelets reinforced calcium silicate composite. PLoS One, 2014, 9(9): e106802

[38] Yu X Q, Wang Z P, Su Z Q, Wei G. Design, fabrication, and biomedical applications of bioinspired peptide-inorganic nanomaterial hybrids. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2017, 5(6): 1130–1142

[39] Li C X, Born A K, Schweizer T, Zenobi-Wong M, Cerruti M, Mezzenga R. Amyloid-hydroxyapatite bone biomimetic composites. Advanced Materials, 2014, 26(20): 3207–3212

[40] Liu Y, Huang J, Li H. Synthesis of hydroxyapatite-reduced graphite oxide nanocomposites for biomedical applications: Oriented nucleation and epitaxial growth of hydroxyapatite. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2013, 1(13): 1826

[41] Zhang Q, Liu Y, Zhang Y, Li H X, Tan Y N, Luo L L, Duan J H, Li K Y, Banks C E. Facile and controllable synthesis of hydroxyapatite/graphene hybrid materials with enhanced sensing performance towards ammonia. Analyst (London), 2013, 00: 1–8

[42] Ren J, Zhang X G, Chen Y. Graphene accelerates osteoblast attachment and biomineralization. Carbon Letters, 2017, 22: 42–44

[43] Zhao X N, Zhang P P, Chen Y T, Su Z Q, Wei G. Recent advances in the fabrication and structure-specific applications of graphene- based inorganic hybrid membranes. Nanoscale, 2015, 7(12): 5080–5093

[44] Wen T, Wu X L, Liu M C, Xing Z H, Wang X K, Xu A W. Efficient capture of strontium from aqueous solutions using graphene oxide-hydroxyapatite nanocomposites. Dalton Transactions (Cambridge, England), 2014, 43(20): 7464–7472

[45] Li D P, Liu T J, Yu X Q, Wu D, Su Z Q. Fabrication of graphene-biomacromolecule hybrid materials for tissue engineering application. Polymer Chemistry, 2017, 8(30): 4309–4321

[46] Zhang L, Liu W W, Yue C G, Zhang T H, Li P, Xing Z W, Chen Y. A tough graphene nanosheet/hydroxyapatite composite with improved in vitro biocompatibility. Carbon, 2013, 61: 105–115

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 21201142 and 11502158) and Southwest University of Science and Technology researching project (Grant No. 14tdsc03).

RIGHTS & PERMISSIONS

2018 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature