Graphene Oxide Induces Ester Bonds Hydrolysis of Poly-l-lactic Acid Scaffold to Accelerate Degradation

Cijun Shuai, Yang Li, Wenjing Yang, Li Yu, Youwen Yang, Shuping Peng, Pei Feng

Article ID: 249
Vol 6, Issue 1, 2020, Article identifier:249

VIEWS - 668 (Abstract) 151 (PDF)


Poly-l-lactic acid (PLLA) possesses good biocompatibility and bioabsorbability as scaffold material, while slow degradation rate limits its application in bone tissue engineering. In this study, graphene oxide (GO) was introduced into the PLLA scaffold prepared by selective laser sintering to accelerate degradation. The reason was that GO with a large number of oxygencontaining functional groups attracted water molecules and transported them into scaffold through the interface microchannels formed between lamellar GO and PLLA matrix. More importantly, hydrogen bonding interaction between the functional groups of GO and the ester bonds of PLLA induced the ester bonds to deflect toward the interfaces, making water molecules attack the ester bonds and thereby breaking the molecular chain of PLLA to accelerate degradation. As a result, some micropores appeared on the surface of the PLLA scaffold, and mass loss was increased from 0.81% to 4.22% after immersing for 4 weeks when 0.9% GO was introduced. Besides, the tensile strength and compressive strength of the scaffolds increased by 24.3% and 137.4%, respectively, due to the reinforced effect of GO. In addition, the scaffold also demonstrated good bioactivity and cytocompatibility.


Poly-l-lactic acid scaffold, GO, Degradation property, Ester bonds hydrolysis

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An J, Teoh JE, Suntornnond R, et al., 2015, Design and 3D Printing of Scaffolds and Tissues. Engineering, 1:261–268.

Liu F, Mishbak H, Bartolo PJ, 2019, Hybrid Polycaprolactone/Hydrogel Scaffold Fabrication and in-process Plasma Treatment Using PABS. Int J Bioprint, 5:174.

Cardoso, GB, Perea, GN, D’Avila, MA, et al., 2011, Initial Study of Electrospinning PCL/PLLA Blends. Adv Mater Phys Chem, 1:94–98.

Saito Y, Minami K, Kobayashi M, et al., 2002, New Tubular Bioabsorbable Knitted Airway Stent: Biocompatibility and Mechanical Strength. J Thorac Cardiovasc Surg, 123:161–167. DOI: 10.1067/mtc.2002.118503.

Shuai C, Yang W, He C, et al., 2020, A Magnetic Microenvironment in Scaffolds for Stimulating Bone Regeneration. Mater Des, 185:108275. DOI: 10.1016/j.matdes.2019.108275.

Weng Y, Jin Y, Meng Q, et al., 2013, Biodegradation Behavior of Poly (Butylene Adipate-co-terephthalate) (PBAT), Poly (Lactic Acid)(PLA), and their Blend under Soil Conditions. Polym Test, 32:918–926. DOI: 10.1016/j.polymertesting.2013.05.001.

Shuai C, Li Y, Feng P, et al., 2019, Montmorillonite Reduces Crystallinity of Poly-l-lactic Acid Scaffolds to Accelerate Degradation. Polym Adv Technol, 30:2425–2435. DOI: 10.1002/pat.4690.

Tanaka M, Tanaka H, Hojo M, et al., 2019, Change in Deformation/Fracture Behavior of Interface-controlled HAP/PLLA Composites by Hydrolysis, Proceedings of the 17th International Conference on Composite Materials, CDROM.

Yang Y, He C, Dianyu E, et al., 2019, Mg Bone Implant: Features, Developments and Perspectives. Mater Des, 2019:108259.

Lee JH, Park TG, Park HS, et al., 2003, Thermal and Mechanical Characteristics of Poly(L-lactic acid) Nanocomposite Scaffold. Biomaterials, 24:2773–2778. DOI: 10.1016/s0142-9612(03)00080-2.

Chen X, Wu X, Fan Z, et al., 2018, Biodegradable Poly (Trimethylene carbonate-b-(L-lactide-ran-glycolide) Terpolymers with Tailored Molecular Structure and Advanced Performance. Polym Adv Technol, 29:1684–1696. DOI: 10.1002/pat.4272.

Shuai C, Yang Y, Feng P, et al., 2018, A Multi-scale Porous Scaffold Fabricated by a Combined Additive Manufacturing and Chemical Etching Process for Bone Tissue Engineering. Int J Bioprint, 4:133. DOI: 10.18063/ijb.v4i1.133.

Shie MY, Fang HY, Lin YH, et al., 2019, Application of Piezoelectric Cells Printing on Three-dimensional Porous Bioceramic Scaffold for Bone Regeneration. Int J Bioprint, 5:210. DOI: 10.18063/ijb.v5i2.210.

Yang Y, Wang G, Liang H, et al., 2019, Additive manufacturing of bone scaffolds. Int J Bioprint, 5:184.

Ji JH, Park IS, Kim YK, et al., 2015, Influence of Heat Treatment on Biocorrosion and Hemocompatibility of Biodegradable Mg-35Zn-3Ca Alloy. Adv Mater Sci Eng, 17:1–10. DOI: 10.1155/2015/318696.

Kang Y, Chen P, Shi X, et al., 2018, Multilevel Structural Stereocomplex Polylactic Acid/collagen Membranes by Pattern Electrospinning for Tissue Engineering. Polymer, 156:250–260. DOI: 10.1016/j.polymer.2018.10.009.

Buwalda SJ, Dijkstra PJ, Calucci L, et al., 2019, Influence of Amide versus Ester Linkages on the Properties of Eight-Armed PEG-PLA Star Block Copolymer Hydrogels. Biomacromolecules, 11:224–232. DOI: 10.1021/bm901080d.

Kontakis GM, Pagkalos JE, Tosounidis TI, et al., 2007, Bioabsorbable Materials in Orthopaedics. Acta Orthop Belg, 73:159–169.

Shuai C, Zan J, Yang Y, et al., 2019, Surface Modification Enhances Interfacial Bonding in PLLA/MgO Bone Scaffold. Mater Sci Eng C, 108:110486. DOI: 10.1016/j.msec.2019.110486.

Ding L, Wei Y, Wang Y, et al., 2017, A Two-Dimensional Lamellar Membrane: MXene Nanosheet Stacks. Angew Chem Int Ed Engl, 56:1825–1829. DOI: 10.1002/anie.201609306.

Shen J, Hu Y, Shi M, et al., 2009, Fast and Facile Preparation of Graphene Oxide and Reduced Graphene Oxide Nanoplatelets. Chem Mater, 21:3514–3520. DOI: 10.1021/cm901247t.

Wang G, Qi F, Yang W, et al., 2019, Crystallinity and Reinforcement in Poly-l-lactic Acid Scaffold Induced by Carbon Nanotubes. Adv Polym Technol, 2019:8625325.

Yoon OJ, Sohn IY, Kim DJ, et al., Enhancement of Thermomechanical Properties of poly(D,L-lactic-co-glycolicacid) and Graphene Oxide Composite Films for Scaffolds. Macromol Res, 20:789–794. DOI: 10.1007/s13233-012-0116-0.

He S, Yang S, Zhang Y, Li X, et al., 2019, LncRNA ODIR1 Inhibits Osteogenic Differentiation of hUC-MSCs through the FBXO25/H2BK120ub/H3K4me3/OSX Axis. Cell Death Dis, 10:1–16. DOI: 10.1038/s41419-019-2148-2.

Depan D, Girase B, Shah JS, et al., 2011, 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, 7:3432–3445. DOI: 10.1016/j.actbio.2011.05.019.

Xiong G, Luo H, Zuo G, et al., Novel Porous Graphene Oxide and Hydroxyapatite Nanosheets-reinforced Sodium Alginate Hybrid Nanocomposites for Medical Applications. Mater Charact, 107:419–425. DOI: 10.1016/j.matchar.2015.07.016.

Chen J, Shi X, Ren L, et al., 2016, Graphene Oxide/PVA Inorganic/Organic Interpenetrating Hydrogels with Excellent Mechanical Properties and Biocompatibility. Carbon, 111:18–27. DOI: 10.1016/j.carbon.2016.07.038.

Zhao X, Zhang Q, Chen D, et al., 2010, Enhanced Mechanical Properties of Graphene-Based Poly(vinyl alcohol) Composites. Macromolecules, 44:2392–2392. DOI: 10.1021/ma200335d.

Wang K, Ruan J, Song H, et al., 2011, Biocompatibility of Graphene Oxide. Nanoscale Res Lett, 6:1–8.

Gao C, Yao M, Shuai C, et al., 2019, Nano-SiC Reinforced Zn Biocomposites Prepared via Laser Melting: Microstructure, Mechanical Properties and Biodegradability. J Mater Sci Technol, 35:2608–2617. DOI: 10.1016/j.jmst.2019.06.010.

Rodríguez-Lozano FJ, García-Bernal D, Aznar-Cervantes S, et al., 2014, Effects of Composite Films of Silk Fibroin and Graphene Oxide on the Proliferation, Cell Viability and Mesenchymal Phenotype of Periodontal Ligament Stem Cells. J Mater Sci Mater Med, 25:2731–2741. DOI: 10.1007/s10856-014-5293-2.

Li W, Xu Z, Chen L, et al., 2014, A Facile Method to Produce Graphene Oxide-g-poly (L-lactic acid) as an Promising Reinforcement for PLLA Nanocomposites. Chem Eng J, 237:291–299. DOI: 10.1016/j.cej.2013.10.034.

Zhang K, Zheng H, Liang S, et al., 2016, Aligned PLLA Nanofibrous Scaffolds Coated with Graphene Oxide for Promoting Neural Cell Growth. Acta Biomater, 37:131–142. DOI: 10.1016/j.actbio.2016.04.008.

Pan LH, Kuo SH, Lin TY, et al., 2017, An Electrochemical Biosensor to Simultaneously Detect VEGF and PSA for Early Prostate Cancer Diagnosis Based on Graphene Oxide/ssDNA/PLLA Nanoparticles. Biosens Bioelectron, 89:598–605. DOI: 10.1016/j.bios.2016.01.077.

Chen Q, Mangadlao JD, Wallat J, et al., 2017, 3D Printing Biocompatible Polyurethane/Poly (Lactic Acid)/Graphene Oxide Nanocomposites: Anisotropic Properties. ACS Appl Mater Interfaces, 9:4015–4023. DOI: 10.1021/acsami.6b11793.

Yuan S, Shen F, Chua CK, et al., 2019, Polymeric Composites for Powder-based Additive Manufacturing: Materials and Applications. Prog Polym Sci, 91:141–168. DOI: 10.1016/j.progpolymsci.2018.11.001.

Lee JY, An J, Chua CK, 2017, Fundamentals and Applications of 3D Printing for Novel Materials. Appl Mater Today, 7:120–133.

Zhuang P, Sun AX, An J, et al., 2018, 3D Neural Tissue Models: From Spheroids to Bioprinting. Biomaterials, 154:113–133. DOI: 10.1016/j.biomaterials.2017.10.002.

Mir TA, Iwanaga S, Kurooka T, et al., 2019, Biofabrication Offers Future Hope for Tackling Various Obstacles and Challenges in Tissue Engineering and Regenerative Medicine: A Perspective. Int J Bioprint, 5:153. DOI: 10.18063/ijb.v5i1.153.

Ng WL, Chua CK, Shen YF, 2019, Print me an Organ! Why we are not there yet. Prog Polym Sci, 97:101145. DOI: 10.1016/j.progpolymsci.2019.101145.

Lee JM, Sing SL, Zhou M, et al., 2018, 3D Bioprinting Processes: A Perspective on Classification and Terminology.Int J Bioprint, 4:151. DOI: 10.18063/ijb.v4i2.151.

Zhuang P, Ng WL, An J, et al., 2019, Layer-by-Layer Ultraviolet Assisted Extrusion-based (UAE) Bioprinting of Hydrogel Constructs with High Aspect Ratio for Soft Tissue Engineering Applications. PLoS One, 14:e0216776. DOI: 10.1371/journal.pone.0216776.

Lins LC, Wianny F, Livi S, et al., Development of Bioresorbable Hydrophilic-hydrophobic Electrospun Scaffolds for Neural Tissue Engineering. Biomacromolecules, 17:3172–3187. DOI: 10.1021/acs.biomac.6b00820.

Gao C, Yao M, Li S, et al., 2019, Highly Biodegradable and Bioactive Fe-Pd-Bredigite Biocomposites Prepared by Selective Laser Melting. J Adv Res, 20:91–104. DOI: 10.1016/j.jare.2019.06.001.

Wei G, Ma PX, 2004, Structure and Properties of Nano-Hydroxyapatite/Polymer Composite Scaffolds for Bone Tissue Engineering. Biomaterials, 25:4749–4757. DOI: 10.1016/j.biomaterials.2003.12.005.

Xia W, Chang J, 2010, Bioactive Glass Scaffold with Similar Structure and Mechanical Properties of Cancellous Bone. J Biomed Mater Res Part B Appl Biomater, 95:449–455. DOI: 10.1002/jbm.b.31736.

Feng P, Kong Y, Yu L, et al., 2019, Molybdenum Disulfide Nanosheets Embedded with Nanodiamond Particles: Codispersion Nanostructures as Reinforcements for Polymer Scaffolds. Appl Mater Today, 17:216–226. DOI: 10.1016/j.apmt.2019.08.005.

Geng LH, Peng XF, Jing X, et al., Investigation of Poly(llactic acid)/Graphene Oxide Composites Crystallization and Nanopore Foaming Behaviors via Supercritical Carbon Dioxide Low Temperature Foaming. J Mater Res, 31:348–359. DOI: 10.1557/jmr.2016.13.

Morales-Narváez E, Baptista-Pires L, Zamora-Gálvez A, et al., 2017, Graphene-Based Biosensors: Going Simple. Adv Mater, 29:1604905. DOI: 10.1002/adma.201604905.

Kaniyoor A, Baby TT, Ramaprabhu S, 2010, Graphene Synthesis via Hydrogen Induced Low Temperature Exfoliation of Graphite Oxide. J Mater Chem, 20:8467–8460. DOI: 10.1039/c0jm01876g.

Eckhart KE, Holt BD, Laurencin MG, et al., 2019, Covalent Conjugation of Bioactive Peptides to Graphene Oxide for Biomedical Applications. Biomater Sci, 7:3876–3885. DOI: 10.1039/c9bm00867e.

Zhang P, Wang BT, Gao D, et al., The Study on the Mechanical Properties of Poly (Lactic Acid)/Straw Fiber Composites. Appl Mech Mater, 2012:312–315.

Todo M, Park SD, Arakawa K, et al., 2006, Relationship between Microstructure and Fracture Behavior of Bioabsorbable HA/PLLA Composites. Compos Part A Appl Sci Manuf, 37:2221–2225. DOI: 10.1016/j.compositesa.2005.10.001.

Yang Y, He C, Dianyu E, et al., 2019, Mg Bone Implant: Features, Developments and Perspectives. Mater Des, 185:108259. DOI: 10.1016/j.matdes.2019.108259.

Shuai C, Liu G, Yang Y, et al., 2020, Functionalized BaTiO3 Enhances Piezoelectric Effect towards Cell Response of Bone Scaffold. Colloids Surf B Biointerfaces, 185:110587. DOI: 10.1016/j.colsurfb.2019.110587.

Zhou Z, Liu L, Liu Q, et al., 2012, Effect of Surface Modification of Bioactive Glass on Properties of Poly-L-Lactide Composite Materials. J Macromol Sci Part B, 51:1637–1646. DOI: 10.1080/00222348.2012.672295.

Alexa A, Rahnenführer J, Lengauer TR, 2006, Improved Scoring of Functional Groups from Gene Expression Data by Decorrelating GO Graph Structure. Bioinformatics, 22:1600–1607. DOI: 10.1093/bioinformatics/btl140.

Shuai C, Cheng Y, Yang Y, et al., 2019, Laser Additive Manufacturing of Zn-2Al Part for Bone Repair: Formability, Microstructure and Properties. J Alloys Compd, 798:606–615. DOI: 10.1016/j.jallcom.2019.05.278.

Yang X, Li X, Ma X, et al., 2014, Carbonaceous Impurities Contained in Graphene Oxide/Reduced Graphene Oxide Dominate their Electrochemical Capacitances. Electroanalysis, 26:139–146. DOI: 10.1002/elan.201300128.

Wang H, Zhao S, Xiao W, et al., 2016, Influence of Cu Doping in Borosilicate Bioactive Glass and the Properties of its Derived Scaffolds. Mater Sci Eng C, 58:194–203. DOI: 10.1016/j.msec.2015.08.027.

Suntornnond R, An J, Chua CK, 2017, Roles of Support Materials in 3D Bioprinting-Present and Future. Int J Bioprint, 3:321–328. DOI: 10.18063/ijb.2017.01.006.



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