Graphene Oxide-Templated Synthesis of Hydroxyapatite

Feb 19, 2018 - (16) This is in line with the high-resolution TEM (HR-TEM) images revealing that HA nanowhiskers were intimately coherent with GO nanos...
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Cite This: ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Graphene Oxide-Templated Synthesis of Hydroxyapatite Nanowhiskers To Improve the Mechanical and Osteoblastic Performance of Poly(lactic acid) for Bone Tissue Regeneration Chen Chen,*,† Xiaodong Sun,‡,§ Wu Pan,† Yi Hou,† Rui Liu,‡ Xin Jiang,† and Li Zhang*,† †

Analytical and Testing Center, Sichuan University, Chengdu 610065, China West China School of Preclinical and Forensic Medicine, Sichuan University, Chengdu 610041, China § State Key Laboratory of Medicinal Chemical Biology, Nankai University, Tianjin 300071, China ‡

S Supporting Information *

ABSTRACT: Central to the design and development of biomedical-adaptive graphene oxide (GO) is functional modification of GO amenable to technologically reliable and economically viable processing. Here we describe a highefficiency and low-temperature approach to in situ synthesis of hydroxyapatite (HA) nanowhiskers at GO surfaces (HA@ GO), strategically involving microwave-assisted mineralization in stimulated body fluid at room temperature. Being preferentially nucleated and accommodated at GO surfaces, the highly crystalline HA nanowhiskers with an average diameter of 20 nm and a length of 150 nm were characterized by coherent bonding with the host nanosheets. The strong GO−HA interactions, combined with the high density of oxygen functional groups, endowed the HA@GO with good exfoliation and dispersion in a poly(lactic acid) (PLA) matrix even at the highest filler content of 30 wt % (HG30). Inheriting the excellent biocompatibility of HA and the remarkable strength of GO, the PLA/HA@GO nanocomposites exhibited an unusual combination of prominent cytocompatibility with osteoblast cells and high mechanical strength and toughness. In particular, compared to that of the normal PLA/HA counterpart, HG30 exhibited a >85% increase in cell viability, accompanied by 2- and 7.9-fold increases in tensile strength and toughness (105 MPa and 2.9 MJ/m3), respectively. This work paves a facile yet effective way to GO functionalization with biologically beneficial HA nanowhiskers, which may prompt the realistic development of GO-based biomaterials, especially in the realm of polymer/GO nanocomposites. KEYWORDS: Biomimetic mineralization, Hydroxyapatite nanowhiskers, Graphene oxide, Poly(lactic acid) nanocomposites, Osteoblastic proliferation

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INTRODUCTION

increasingly on affordable and efficient synthesis of surfacemodified GO sheets. Emerging as an innovative and low-cost surface modification approach, mineralization of one-dimensional hydroxyapatite (HA) nanocrystals at the surfaces of 2D GO nanosheets has been developed to engender highly bioactive composites,14,15 during which GO may serve as an active platform to facilitate the nucleation of HA crystals.16,17 Given the combination of the high strength of GO and excellent biocompatibility of HA,18 the hybrid GO/HA nanostructures exhibit remarkable improvements in mechanical strength and cytocompatibility.19 Despite the contributions revealing the great application promise of GO/HA composites, it is pertinent to point out that the currently accessible manufacturing methods are generally related to large energy footprints and specific technical demands. For instance, functionalization of GO by oxidative

Graphene oxide (GO) nanosheets, an alluring two-dimensional (2D) nanomaterial with high mechanical strength and potential biocompatibility, have rapidly garnered interest in the biomedical and pharmaceutical fields,1,2 opening up new possibilities for delivery vehicles for drugs and biomacromolecules,3,4 cellular imaging agents,5,6 and implantable tissues.7 The presence of oxygen-rich functional groups,8 combined with a large surface area and a high surface energy,9 favorably allows functional modification of GO with biologically beneficial particles or polymers, contributing to significant enhancements of biological character.10,11 This methodology has been convincingly elaborated by recent advances in GO-based biomedical materials. As an example, the thrombotoxicity of GO was removed by amine functionalization,12 while modification of GO with dopamine-grafted heparin led to the enhanced viability of human umbilical vein endothelial cells.13 Within this context, the quest to realize the enormous biomedical potential of versatile GO nanostructures focuses © XXXX American Chemical Society

Received: November 12, 2017 Revised: January 25, 2018

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DOI: 10.1021/acssuschemeng.7b04192 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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and homogeneous distribution of HA nanowhiskers at GO nanosheets mimicking the microstructures of the inorganic phase in human bones for isotropic reinforcements,30 and (4) incorporation of highly uniform HA@GO nanostructures into the PLA matrix for use in high-performance biomedical materials with improved mechanical properties and bioactivity.

polymerization of dopamine was essential to induce mineralization in stimulated body fluid (SBF) for up to 2 weeks,14 while an electrochemical workstation was used to deposit HA nanocrystals onto superhydrophilic reduced GO films.20 Development of GO/HA composites may be further thwarted by challenges in controlling the size and morphology of HA nanoparticles. Hollow HA nanotubes with a diameter of >500 nm were created at GO surfaces using a hydrothermal reaction at 200 °C for 24 h,21 whereas the hydrothermal mineralization at 200 °C for 24 h led to HA nanorods with a diameter of 20-fold increase was observed for HG10 and HG20 (44.9 and 48.0%, respectively) compared to that of the normal PLA/HA composites (105 and ∼3900 MPa for HG30 (increases of 245 and 31%, respectively, compared to that of HA30), respectively. It is of interest to find that the ductility and toughness of HA@GO-filled composites were substantially increased, as indicated by the 2- and 7.9-fold increase in elongation at break and toughness of HG30 (8.4% and 5.88 MJ/m3, respectively) compared to those of HA30, respectively. In the realm of HA-based biomaterials, a high resistance to external stress penetration is an important goal for removing the application constraints in a complex intraD

DOI: 10.1021/acssuschemeng.7b04192 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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ACS Sustainable Chemistry & Engineering corporeal environment.19,26 Providing high-efficiency mechanical property improvements for PLA, the novel HA@GO nanostructures apparently stand out among the traditional HA nanofillers, as exemplified by a gradual decline in tensile strength from 64.5 MPa for pure PLA to 50.6 MPa for composites containing 30 wt % HA.46 Deformation mechanisms underlying the mechanical robustness of HA@GO-reinforced PLA composites were appraised from the perspective of microstructural evolution involving deformation-induced nanofibrillation and cavitation (Figure 7).

In addition to remarkable enhancements in mechanical properties, HA@GO significantly enhanced osteoblast growth and proliferation on the nanocomposite surfaces, as manifested by the observed morphology of the response of osteosarcoma cell line MG-63 with an Olympus FV-1000 confocal microscope (Figure 8a). The MG-63 cells were plated onto the

Figure 7. Reinforcing and toughening mechanisms in PLA/HA@GO nanocomposites. SEM images comparing the fracture surfaces after tensile failure for composites with (a−c) HA and (d−i) HA@GO.

Identical to the brittle mode of fracture widely reported for PLA reinforced with high-strength fillers,47−49 smooth and scalelike fracture surfaces were observed for PLA/HA, suggesting localized breaking and the absence of plastic deformation (Figure 7a−c). Ductile extension acted as the predominant fracture mode in the presence of HA@GO independent of filler contents, leading to the formation of nanosized cavities and even nanofibrils in large quantities (Figure 7d−i). In particular, the fine nanofibrils were featured by oriented alignment along the deformation and an ultrasmall diameter as small as tens of nanometers. The nanofibrils closely adhered to each other, indicating the creation of a tight linkage between the neighboring nanofibrils in concert with an increasing level of deformation. This was accompanied by the deformation-induced nanovoids enclosing the nanofibrils, as well as the tapered tips at the fracture ends of nanofibrils, both of which favored vast energy dissipation by transferring and redistributing the penetrating stress.50 As distinguished from the catastrophic cracks or cavities usually found in incompatible blends51 or poorly cohered composites,48 the well-dispersed nanocavities likely enabled high extensibility by arresting and localizing the penetrating stress around the nanoscale surfaces of HA@GO. It is important to note that only a small amount of HA closely adhered to the matrix was observed, suggesting that a majority of HA nanowhiskers and GO nanosheets were intimately embedded in the host matrix and involved in the elongational flow within the nanofibrils. The HA@GO-enabled microstructural evolution that pointed to a series of energydissipating and flexibility-imparting mechanisms should be responsible for remarkable enhancements in the resistance to stress penetration, favorably contributing to the evasion of the strength−ductility trade-off dilemma.52

Figure 8. Cell adhesion on the nanocomposite films. (a) Fluorescence images of F-actin and nuclei stained with Rhodamine Phalloidin and DAPI in MG-63 cells on nanocomposite surfaces. Scale bars denote 25 μm for all images. (b) Intensity plots of the areas outlined by straight lines marked with the triangles in panel a.

nanocomposite films in a 12-well plate. After adhesion, the cells were fixed in 4% paraformaldehyde and stained with Rhodamine Phalloidin and DAPI. A higher density of cells existed with the lamellipodial protrusion growing on HA30 and HG30 compared to that of the pure PLA counterpart, which was tightly spatiotemporally coupled to adhesion. To determine the effects of the GO nanosheets, we illustrated the F-actin distribution in cells among the different groups with the intensity plots of the Phalloidin. F-Actin was distributed at the cell edge in HA30 and HG30 groups, while it showed a cytoplasmic distribution for pure PLA (Figure 8b). After addition of HA nanowhiskers with a similar composition of the bone inorganic phase, it is apparent that cell adhesion on PLA nanocomposites was enhanced, primarily resulting from the increase in hydrophilicity, surface roughness, the number of cell adhesion sites, and affinity for osteoblast cells.53 The wellexfoliated HA@GO was ready to provide bioactive attachment sites for the osteoblast cells, giving rise to the elongated lamellipodia and pseudopodia.54 This mechanism could be further enhanced by enhancing the surface energy by incorporation of GO nanosheets, which may facilitate the anchoring interaction with neighboring cells.55 E

DOI: 10.1021/acssuschemeng.7b04192 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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establishing a facile method for controlling the surface properties of GO nanosheets. Being preferentially nucleated and accommodated at GO surfaces, the highly crystalline HA nanowhiskers (20 nm diameter and 150 nm length) were characterized by coherent bonding with the host nanosheets. The strong GO−HA interactions, coupled with the high density of oxygen functional groups, endowed the HA@GO with good exfoliation and intimate interactions in the PLA matrix. Inheriting excellent biocompatibility of HA and remarkable strength of GO, the PLA/HA@GO nanocomposites exhibited an exceptional combination of prominent cytocompatibility with osteoblast cells and high mechanical strength and toughness. As an example, HG30 exhibited a >85% increase in cell viability compared to that of the normal PLA/HA counterpart, as accompanied by 2- and 7.9-fold increases in the tensile strength and toughness, respectively (105 MPa and 2.9 MJ/m3, respectively). The biomineralization methodology signifies a high-efficiency and low-cost approach to controlling the GO properties, thus empowering a highperformance and environmentally benign nanocomposite campaign that is not wedded to the traditional GO or graphene nanosheets. The versatility of this method should allow homogeneous doping of biologically beneficial ions (e.g., Si or Na ions) in the apatite structure for on-demand function.

To determine the effects of HA@GO nanostructures on cell viability, the MTT colorimetric assay was used to evaluate MG63 cell viability on the nanocomposite films. In brief, 1 × 104 MG-63 cells were seeded into the 12-well plates with a size of 10 mm × 10 mm for the nanocomposite films and incubated for 24 h. MTT was added to the well at a final concentration of 500 μg/mL for another 4 h incubation, after which 1 mL of dimethyl sulfoxide was added to each well. The absorbance was recorded by using the microplate reader at 490 nm. As shown in Figure 9, osteoblast cells cultured on pure PLA were characterized by the lowest inferior cell viability, due to

Figure 9. MTT assay of cells that proliferated on the surfaces of composite films.

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ASSOCIATED CONTENT

S Supporting Information *

the intrinsically inferior ability to induce cell growth and the absence of bioactive sites for cell attachment.53,56 With the existence of 10 and 20 wt % HA, the level of cell growth modestly increased by approximately 20%, likely resulting from the support of mineral sources and increases in surface roughness from HA particles.57 However, increasing the HA content to 30 wt % suppressed the cell viability to a level close to that of pure PLA. This was presumably due to the distinct local agglomeration of HA (Figure 4a), on which the cell membrane may be punctured by the rather coarse HA clusters58 and the cell growth may be restrained with a limited organic phase.59 Remarkable promotion of cell adhesion and proliferation was observed for PLA/HA@GO, showing a >85% increase in cell viability for HG10 and HG30 compared to those o the PLA/HA counterparts. The complete exfoliation and proper dispersion in the PLA matrix endowed the HA@ GO nanostructures with a high surface energy to anchor the adhesion of MG-63 cells and great bioactivity to speed the proliferation.55 This mechanism could be further enhanced by the homogeneous phase structure, benefiting cell migration and cell spreading over the film surfaces that were identical to those observed for plentiful actin stress fiber throughout the cytoplasm of osteoblast cells (Figure 8a). Additional benefits of PLA/HA@GO nanocomposites for bone tissue regeneration were associated with the increased degradability, conferring rapid proliferation of osteoblast cells accompanied by proper degradation of the host materials. The unprecedented combination of mechanical robustness and cytocompatibility confers great promise in the biomedical field (e.g., fast bone tissue regeneration) upon the hybrid system. The design principles of these materials are significant for engendering orthopedic and dental implant formulations with improved osteointegration performances.

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssuschemeng.7b04192. Experimental details, SEM image and XRD profiles of HA and HA@GO, TEM iamge and XRD curve of GO, FTIR spectra and EDS microanalysis of GO, HA, and HA@GO, SEM images of HG30, DSC heating data and FTIR spectra of nanocomposite films, tensile behavior of pure PLA, and detailed tensile properties of composite films (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Chen Chen: 0000-0002-9632-045X Li Zhang: 0000-0002-0324-5092 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (51673131), the Seedling Project of Scientific and Technological Innovation of Sichuan Province (2016079), and the State Key Laboratory of Medicinal Chemical Biology.

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REFERENCES

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CONCLUSIONS Microwave-assisted mineralization was used to achieve in situ synthesis of HA nanowhiskers at GO surfaces (HA@GO), F

DOI: 10.1021/acssuschemeng.7b04192 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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DOI: 10.1021/acssuschemeng.7b04192 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX