Layer-by-layer decorated herbal cell compatible scaffolds for bone tissue engineering: A synergistic effect of graphene oxide and Cissus quadrangularis
Restricted accessResearch articleFirst published online January, 2020
Layer-by-layer decorated herbal cell compatible scaffolds for bone tissue engineering: A synergistic effect of graphene oxide and Cissus quadrangularis
Among various bone regenerative and repair methods, use of osteoinductive scaffold as bone grafts/substitute has gained wide importance worldwide. To develop such osteoinductive scaffold that is more natural and which spontaneously stimulates osteoblast formation without any differentiation media, we prepared electrospun poly ε-caprolactone scaffold which is further modified by means of layer-by-layer method using Cissus quadrangularis callus culture extract and graphene oxide (PCL-GO-CQ). The modified PCL-GO-CQ scaffold was compared with plain poly ε-caprolactone scaffold and poly ε-caprolactone coated only with graphene oxide. Physical properties, such as roughness, wettability, yield strength and tensile strength, of PCL-GO-CQ scaffold were found to be superior. Also, PCL-GO-CQ scaffold showed more in vitro cell compatibility with enhanced cellular proliferation on its surface. Presence of graphene oxide and Cissus quadrangularis callus in scaffold helped in the differentiation of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells into osteogenic lineage without any differentiation media in less than 20 days. The synergistic effect of Cissus quadrangularis callus extract and graphene oxide in PCL-GO-CQ scaffold enhanced osteoblastic differentiation, osteoconduction and osteoinduction potential of scaffolds making them highly potential in bone regeneration and bone tissue engineering applications.
MaroltDKnezevicMNovakovicGV.Bone tissue engineering with human stem cells. Stem Cell Res Ther2010; 1: 10.
2.
SowjanyaJASinghJMohitaT, et al. Biocomposite scaffolds containing chitosan/alginate/nano-silica for bone tissue engineering. Colloids Surf B Biointerfaces2013; 109: 294–300.
3.
VenkatesanJBhatnagarIKimS-K.Chitosan-alginate biocomposite containing fucoidan for bone tissue engineering. Mar Drugs2014; 12: 300–316.
4.
KashteSJaiswalAKKadamS.Artificial bone via bone tissue engineering: current scenario and challenges. Tissue Eng Regen Med2017; 14: 1–14.
5.
AlvesADuarteARCManoJF, et al. PDLLA enriched with ulvan particles as a novel 3D porous scaffold targeted for bone engineering. J Supercrit Fluids2012; 65: 32–38.
6.
RajzerIMenaszekEKwiatkowskiR, et al. Bioactive nanocomposite PLDL/nano-hydroxyapatite electrospun membranes for bone tissue engineering. J Mater Sci Mater Med2014; 25: 1239–1247.
7.
LiuXMaP.Polymeric scaffolds for bone tissue engineering. Ann Biomed Eng2004; 32: 477–486.
8.
QianJXuWYongX, et al. Fabrication and in vitro biocompatibility of biomorphic PLGA/nHA composite scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl2014; 36: 95–101.
9.
ChuenjitkuntawornBOsathanonTNowwaroteN, et al. The efficacy of polycaprolactone/hydroxyapatite scaffold in combination with mesenchymal stem cells for bone tissue engineering. J Biomed Mater Res A2015; 104: 264–271.
10.
RenKWangYSunT, et al. Electrospun PCL/gelatin composite nanofiber structures for effective guided bone regeneration membranes. Mater Sci Eng C2017; 78: 324–332.
11.
ChakrapaniVYKumarTSSRajDK, et al. Electrospun cytocompatible polycaprolactone blend composite with enhanced wettability for bone tissue engineering. J Nanosci Nanotechnol2017; 17: 2320–2328.
12.
SonYJKimHSYooHS.Layer-by-layer surface decoration of electrospun nanofibrous meshes for air–liquid interface cultivation of epidermal cells. RSC Adv2016; 6: 114061–114068.
13.
GallagherWMLynchIAllenLT, et al. Molecular basis of cell-biomaterial interaction: insights gained from transcriptomic and proteomic studies. Biomaterials2006; 27: 5871–5882.
14.
YangSLeongKFDuZ, et al. The design of scaffolds for use in tissue engineering. Part I. Traditional factors. Tissue Eng2001; 7: 679–689.
15.
ChenWMcCarthyTJ.Layer-by-layer deposition: a tool for polymer surface modification. Marcomolecules1997; 9297: 78–86.
16.
LiYChoiMCJeongKM, et al. Layer-by-layer assembly of graphene on polyimide films via thermal imidization and synchronous reduction of graphene oxide. Macromol Res2017; 25: 496–499.
17.
HeXWuLLWangJJ, et al. Layer-by-layer assembly deposition of graphene oxide on poly(lactic acid) films to improve the barrier properties. High Perform Polym2015; 27: 318–325.
18.
YuPBaoRYShiXJ, et al. Self-assembled high-strength hydroxyapatite/graphene oxide/chitosan composite hydrogel for bone tissue engineering. Carbohydr Polym2017; 155: 507–515.
19.
LuoYShenHFangY, 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 Interfaces2015; 7: 6331–6339.
20.
KaurTThirugnanamAPramanikK.Effect of carboxylated graphene nanoplatelets on mechanical and in-vitro biological properties of polyvinyl alcohol nanocomposite scaffolds for bone tissue engineering. Mater Today Commun2017; 12: 34–42.
21.
MaHSuWTaiZ, et al. Preparation and cytocompatibility of polylactic acid/hydroxyapatite/graphene oxide nanocomposite fibrous membrane. Chinese Sci Bull2012; 57: 3051–3058.
22.
QiWYuanWYanJ, et al. Growth and accelerated differentiation of mesenchymal stem cells on graphene oxide/poly-l-lysine composite films. J Mater Chem B2014; 2: 5461–5467.
23.
ZhangQLiKYanJ, et al. Graphene coating on the surface of CoCrMo alloy enhances the adhesion and proliferation of bone marrow mesenchymal stem cells. Biochem Biophys Res Commun2018; 497: 1011–1017.
24.
QiuJGuoJGengH, et al. Three-dimensional porous graphene nanosheets synthesized on the titanium surface for osteogenic differentiation of rat bone mesenchymal stem cells. Carbon2017; 125: 227–235.
25.
JaidevLRKumarSChatterjeeK.Multi-biofunctional polymer graphene composite for bone tissue regeneration that elutes copper ions to impart angiogenic, osteogenic and bactericidal properties. Colloids Surf B Biointerfaces2017; 159: 293–302.
26.
MishraGSrivastavaSNagoriBP.Pharmacological and therapeutic activity of Cissus quadrangularis: an overview. Int J PharmTech Res2010; 2: 1298–1310.
27.
DekaDKLahonLCSaikiaA, et al. Effect of Cissus quadrangularis in accelerating healing process of experimentally fractured radius-ulna of dog: a preliminary study. Indian J Pharmacol1994; 26: 44–45.
28.
RaoMSBhagath KumarPNarayana SwamyVB, et al. Cissus quadrangularis plant extract enhances the development of cortical bone and trabeculae in the fetal femur. Pharmacologyonline2007; 3: 190–202.
29.
PotuBKRaoMSKuttyNG, et al. Petroleum ether extract of Cissus quadrangularis (LINN) stimulates the growth of fetal bone during intra uterine developmental period: a morphometric analysis. Clinics2008; 63: 815–820.
30.
SuganyaSVenugopalJRamakrishnaS, et al. Herbally derived polymeric nanofibrous scaffolds for bone tissue regeneration. J Appl Polym Sci2014; 131: 1–11.
31.
SinghNSinghVSinghR, et al. Osteogenic potential of cissus qudrangularis assessed with osteopontin expression. Natl J Maxillofac Surg2013; 4: 52–56.
32.
ParvathiKKrishnanAGAnithaA, et al. Poly(L-lactic acid) nanofibers containing Cissus quadrangularis induced osteogenic differentiation in vitro. Int J Biol Macromol2018; 110: 514–521.
33.
ZhouTLiGLinS, et al. Electrospun poly(3-hydroxybutyrate-co-4-hydroxybutyrate)/graphene oxide scaffold: enhanced properties and promoted in vivo bone repair in rats. ACS Appl Mater Interfaces2017; 9: 42589–42600.
34.
KadamSBhondeR.Islet neogenesis from the constitutively nestin expressing human umbilical cord matrix derived mesenchymal stem cell. Islets2010; 2: 112–120.
35.
JaiswalAKKadamSSSoniVP, et al. Improved functionalization of electrospun PLLA/gelatin scaffold by alternate soaking method for bone tissue engineering. Appl Surf Sci2013; 268: 477–488.
36.
ThadavirulNPavasantPSupapholP.Fabrication and evaluation of polycaprolactone–poly(hydroxybutyrate) or poly(3-hydroxybutyrate-co-3-hydroxyvalerate) dual-leached porous scaffolds for bone tissue engineering applications. Macromol Mater Eng2017; 302: 1600289.
37.
TsaiK-YLinH-YChenY-W, et al. Laser sintered magnesium-calcium silicate/poly-ε-caprolactone scaffold for bone tissue engineering. Materials2017; 10: 65–72.
38.
ChhabraHKumbharJRajwadeJ, et al. Three-dimensional scaffold of gelatin-poly(methyl vinyl ether-alt-maleic anhydride) for regenerative medicine: proliferation and differentiation of mesenchymal stem cells. J Bioact Compat Polym2016; 31: 273–290.
39.
GargPMalikCP.Multiple shoot formation and efficient root induction in Cissus quadrangularis. Int J Pharm Clin Res2012; 4: 4–10.
40.
MehtaRTewarePS. In vitro Callus Induction from Stem Explants of Cissus quadrangularis L. (Hadjod)Int J Ayurvedic Herb Med2012; 2: 229–233.
41.
SissonKZhangCFarach-CarsonMC, et al. Fiber diameters control osteoblastic cell migration and differentiation in electrospun gelatin. J Biomed Mater Res A2010; 94: 1312–1320.
42.
NoriegaSEHasanovaGISchneiderMJ, et al. Effect of fiber diameter on the spreading, proliferation and differentiation of chondrocytes on electrospun chitosan matrices. Cells Tissues Organs2012; 195: 207–221.
43.
NayakTRAndersenHMakamVS, et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano2011; 5: 4670–4678.
44.
DeligianniDKatsalaNLadasS, et al. Effect of surface roughness of the titanium alloy Ti–6Al–4V on human bone marrow cell response and on protein adsorption. Biomaterials2001; 22: 1241–1251.
45.
YangMZhuSChenY, et al. Studies on bone marrow stromal cells affinity of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). Biomaterials2004; 25: 1365–1373.
46.
MisraSKAnsariTMohnD, et al. Effect of nanoparticulate bioactive glass particles on bioactivity and cytocompatibility of poly(3-hydroxybutyrate) composites. J R Soc Interface2010; 7: 453–465.
47.
LeeEJLeeJHShinYC, et al. Graphene oxide-decorated PLGA/collagen hybrid fiber sheets for application to tissue engineering scaffolds. Biomater Res2014; 18: 18–24.
48.
BhullarSKRanaDLekesizH, et al. Design and fabrication of auxetic PCL nanofiber membranes for biomedical applications. Mater Sci Eng C Mater Biol Appl2017; 81: 334–340.
49.
PersenaireOAlexandreMDegéePA, et al. Mechanisms and kinetics of thermal degradation of poly(ε-caprolactone). Biomacromolecules2001; 2: 288–294.
50.
PintoAMMoreiraSGonçalvesIC, et al. Biocompatibility of poly(lactic acid) with incorporated graphene-based materials. Colloids Surfaces B Biointerfaces2013; 104: 229–238.
51.
SunHZhuFHuQ, et al. Controlling stem cell-mediated bone regeneration through tailored mechanical properties of collagen scaffolds. Biomaterials2014; 35: 1176–1184.
52.
LinCYKikuchiNHollisterSJ.A novel method for biomaterial scaffold internal architecture design to match bone elastic properties with desired porosity. J Biomech2004; 37: 623–636.
53.
Tarik ArafatMGibsonILiX. State of the art and future direction of additive manufactured scaffolds-based bone tissue engineering. Rapid Prototyp J2014; 20: 13–26.
54.
WangJYuX.Preparation, characterization and in vitro analysis of novel structured nanofibrous scaffolds for bone tissue engineering. Acta Biomater2010; 6: 3004–3012.
55.
LeeWCLimCHShiH, et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano2011; 5: 7334–7341.
56.
FelkaTSchferRDe ZwartP, et al. Animal serum-free expansion and differentiation of human mesenchymal stromal cells. Cytotherapy2010; 12: 143–153.
57.
WangJLiuDGuoB, et al. Role of biphasic calcium phosphate ceramic-mediated secretion of signaling molecules by macrophages in migration and osteoblastic differentiation of MSCs. Acta Biomater2017; 51: 447–460.
58.
HungPSKuoYCChenHG, et al. Detection of osteogenic differentiation by differential mineralized matrix production in mesenchymal stromal cells by Raman spectroscopy. PLoS ONE2013; 8: e65438.
59.
YamamotoNFuruyaKHanadaK.Progressive development of the osteoblast phenotype during differentiation of osteoprogenitor cells derived from fetal rat calvaria: model for in vitro bone formation. Biol Pharm Bull2002; 25: 509–515.
60.
AçilYGhoniemAAWiltfangJ, et al. Optimizing the osteogenic differentiation of human mesenchymal stromal cells by the synergistic action of growth factors. J Craniomaxillofac Surg2014; 42: 2002–2009.
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