Effect of changes in the surface chemistry and topography of poly(2-hydroxyethyl methacrylate) on the in vitro attachment of human corneal epithelial cells
Restricted accessResearch articleFirst published online May, 2018
Effect of changes in the surface chemistry and topography of poly(2-hydroxyethyl methacrylate) on the in vitro attachment of human corneal epithelial cells
The effects on cell adhesion induced by changes in the topography and chemistry of poly(2-hydroxyethyl methacrylate) hydrogel surfaces were investigated in vitro using the human corneal epithelial cell line, HCE-T. Poly(2-hydroxyethyl methacrylate) surfaces with a lotus-leaf-like topography and poly(2-hydroxyethyl methacrylate) surfaces with a flat topography, but functionalized with the cell-adhesive peptide sequence Arg–Gly–Asp, both enhanced attachment of HCE-T cells as compared to flat, non-functionalized poly(2-hydroxyethyl methacrylate) surfaces. However, the simultaneous existence on the same poly(2-hydroxyethyl methacrylate) surface of Arg–Gly–Asp motifs and of lotus-leaf-like topographical patterns led to an apparently antagonistic effect reflected in reduced cell attachment. The study provided additional evidence of the complexity of the cell–biomaterial interactions.
GumbinerBM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell1996; 84: 345–357.
2.
HynesROZhaoQ.The evolution of cell adhesion. J Cell Biol2000; 150: F89–F96.
3.
SuhWHAnanthanarayananBTirrellM.Molecular engineering of peptides for cellular adhesion control. In:ZengH (ed.) Polymer adhesion, friction, and lubrication. New York: Wiley, 2013, pp. 283–317.
HorbettTA. Protein adsorption on biomaterials. In: CooperSLPeppasNAHoffmanASet al. (eds) Biomaterials: interfacial phenomena and applications. Washington, DC: ACS, 1982, pp. 233–244.
8.
CurtisASGForresterJV. The competitive effects of serum proteins on cell adhesion. J Cell Sci1984; 71: 17–35.
9.
TamadaYIkadaQ.Effect of preadsorbed proteins on cell adhesion to polymer surfaces. J Colloid Interface Sci1993; 155: 334–339.
10.
HorbettTAKlumbLA.Cell culturing: surface aspects and considerations. In: BrashJLWojciechowskiPW (eds) Interfacial phenomena and bioproducts. New York: Marcel Dekker, 1996, pp. 351–445.
11.
WojciechowskiPW.Transport and adsorption of cells and proteins at interfaces. In: BrashJLWojciechowskiPW (eds) Interfacial phenomena and bioproducts. New York: Marcel Dekker, 1996, pp. 209–229.
12.
WilsonCJCleggRELeavesleyDIet al. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng2005; 11: 1–18.
13.
HerselUDahmenCKesslerH.RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials2003; 24: 4385–4415.
14.
HuangJGräterSVCorbelliniFet al. Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett2009; 9: 1111–1116.
15.
RoachPParkerTGadegaardNet al. Surface strategies for control of neuronal cell adhesion: a review. Surf Sci Rep2010; 65: 145–173.
PaulNRJacquemetGCaswellPT.Endocytic trafficking of integrins in cell migration. Curr Biol2015; 25: R1092–R1105.
20.
PanLZhaoYYuanZet al. Research advances on structure and biological functions of integrins. Springerplus2016; 5: 1094.
21.
StreuliCH.Integrins as architects of cell behavior. Mol Biol Cell2016; 27: 2885–2888.
22.
WangYNiH.Fibronectin maintains the balance between hemostasis and thrombosis. Cell Mol Life Sci2016; 73: 3265–3277.
23.
ZeltzCGullbergD.The integrin-collagen connection – a glue for tissue repair?J Cell Sci2016; 129: 653–664.
24.
PierschbacherMDRuoslahtiE.Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature1984; 309: 30–33.
25.
RuoslahtiEPierschbacherMD.New perspectives in cell adhesion: RGD and integrins. Science1987; 238: 491–497.
StaatzWDFokKFZutterMMet al. Identification of a tetrapeptide recognition sequence for the α2β1 integrin in collagen. J Biol Chem1991; 266: 7363–7367.
28.
RuoslahtiE.RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol1996; 12: 697–715.
29.
HarrisonRG.Observations on the living developing nerve fiber. Exp Biol Med1906; 4: 140–143.
30.
LoebLFleisherMS.On the factors which determine the movements of tissues in culture media. J Med Res1917; 37: 75–99.
31.
WeissP.Nerve patterns: the mechanics of nerve growth. Growth1941; 5: 163–203.
32.
CurtisASGVardeM. Control of cell behavior: topological factors. J Natl Cancer Inst1964; 33: 15–26.
33.
CurtisASGForresterJVMcInnesCet al. Adhesion of cells to polystyrene surfaces. J Cell Biol1983; 97: 1500–1506.
34.
CurtisAWilkinsonC.Topographical control of cells. Biomaterials1997; 18: 1573–1583.
35.
CurtisASWilkinsonCD.Reactions of cells to topography. J Biomater Sci Polym Ed1998; 9: 1313–1329.
36.
DunnGAHeathJP.A new hypothesis of contact guidance in tissue cells. Exp Cell Res1976; 101: 1–14.
37.
DunnGABrownAF.Alignment of fibroblasts on grooved surfaces described by a simple geometric transformation. J Cell Sci1986; 83: 313–340.
38.
SinghviRStephanopoulosGWangDI.Effects of substratum morphology on cell physiology. Biotechnol Bioeng1994; 43: 764–471.
39.
FlemmingRGMurphyCJAbramsGAet al. Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials1999; 20: 573–588.
40.
TeixeiraAIAbramsGABerticsPJet al. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci2003; 116: 1881–1892.
41.
SniadeckiNJDesaiRARuizSAet al. Nanotechnology for cell-substrate interactions. Ann Biomed Eng2006; 34: 59–74.
42.
FraserSATingYHMallonKSet al. Sub-micron and nanoscale feature depth modulates alignment of stromal fibroblasts and corneal epithelial cells in serum-rich and serum-free media. J Biomed Mater Res A2008; 86: 725–735.
43.
MartinezEEngelEPlanellJAet al. Effects of artificial micro- and nano-structured surfaces on cell behaviour. Ann Anat2009; 191: 126–135.
44.
Hoffman-KimDMitchelJABellamkondaRV.Topography, cell response, and nerve regeneration. Annu Rev Biomed Eng2010; 12: 203–231.
45.
KilianKABugarijaBLahnBTet al. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A2010; 107: 4872–4877.
46.
WilsonSLWimpennyIAhearneMet al. Chemical and topographical effects on cell differentiation and matrix elasticity in a corneal stromal layer model. Adv Funct Mater2012; 22: 3641–3649.
47.
AhearneM.Introduction to cell-hydrogel mechanosensing. Interface Focus2014; 4: 20130038.
48.
ChirilaTVVijayasekaranSHorneRet al. Interpenetrating polymer network (IPN) as a permanent joint between the elements of a new type of artificial cornea. J Biomed Mater Res1994; 28: 745–753.
ChirilaTV.An overview of the development of artificial corneas with porous skirts and the use of PHEMA for such an application. Biomaterials2001; 22: 3311–3317.
51.
HicksCRCrawfordGJLouXet al. Corneal replacement using a synthetic hydrogel cornea, AlphaCor™: device, preliminary outcomes and complications. Eye2003; 17: 385–392.
52.
HicksCRClaytonABVijayasekaranSet al. Development of a poly(2-hydroxyethyl methacrylate) orbital implant allowing direct muscle attachment and tissue ingrowth. Ophthal Plast Reconstr Surg1999; 15: 326–332.
53.
MinettTWTigheBJLydonMJet al. Requirements for cell spreading on polyHEMA coated culture substrates. Cell Biol Int Rep1984; 8: 151–159.
54.
LydonMJMinettTWTigheBJ.Cellular interactions with synthetic polymer surfaces in culture. Biomaterials1985; 6: 396–402.
55.
LydonMJ.Synthetic hydrogels as substrata for cell adhesion studies. Br Polym J1986; 18: 22–27.
Van WachemPBHogtAHBeugelingTet al. Adhesion of cultured human endothelial cells onto methacrylate polymers with varying surface wettability and charge. Biomaterials1987; 8: 323–328.
58.
HollyFJRefojoMF. Wettability of hydrogels. I. Poly (2-hydroxyethyl methacrylate). J Biomed Mater Res1975; 9: 315–326.
59.
De RosaMCarteniMPetilloOet al. Cationic polyelectrolyte hydrogel fosters fibroblast spreading, proliferation, and extracellular matrix production: implications for tissue engineering. J Cell Physiol2004; 198: 133–143.
60.
Guiseppi-ElieADongCDinuCZ.Crosslink density of a biomimetic poly(HEMA)-based hydrogel influences growth and proliferation of attachment dependent RMS 13 cells. J Mater Chem2012; 22: 19529–19539.
61.
PatersonSMShadforthAMAShawJAet al. Improving the cellular invasion into PHEMA sponges by incorporation of the RGD peptide ligand: the use of copolymerization as a means to functionalize PHEMA sponges. Mater Sci Eng C Mater Biol Appl2013; 33: 4917–4922.
62.
McAuslanBRJohnsonG.Cell responses to biomaterials. I: adhesion and growth of vascular endothelial cells on poly(hydroxyethyl methacrylate) following surface modification by hydrolytic etching. J Biomed Mater Res1987; 21: 921–935.
ZainuddinBarnardZKeenIet al. PHEMA hydrogels modified through the grafting of phosphate groups by ATRP support the attachment and growth of human corneal epithelial cells. J Biomater Appl2008; 23: 147–168.
65.
KubinováSHorákDKozubenkoNet al. The use of superporous Ac-CGGASIKVAVS-OH-modified PHEMA scaffolds to promote cell adhesion and the differentiation of human fetal neural precursors. Biomaterials2010; 31: 5966–5975.
BryndaEHouskaMKysilkaJet al. Surface modification of hydrogels based on poly(2-hydroxyethyl methacrylate) with extracellular matrix proteins. J Mater Sci Mater Med2009; 20: 909–915.
68.
PatelAMequanintK.Synthesis and characterization of polyurethane-block-poly(2-hydroxyethyl methacrylate) hydrogels and their surface modification to promote cell affinity. J Bioact Compat Polym2011; 26: 114–129.
69.
GuvendirenMBurdickJA.The control of stem cell morphology and differentiation by hydrogel surface wrinkles. Biomaterials2010; 31: 6511–6518.
70.
ZainuddinChirilaTVBarnardZet al. F2 excimer laser (157 nm) radiation modification and surface ablation of PHEMA hydrogels and the effects on bioactivity: surface attachment and proliferation of human corneal epithelial cells. Radiat Phys Chem2011; 80: 219–229.
71.
De GiglioECafagnaDGiangregorioMMet al. PHEMA-based thin hydrogel films for biomedical applications. J Bioact Compat Polym2011; 26: 420–434.
72.
Santander-BorregoMTaranEShadforthAMAet al. Hydrogels with lotus leaf topography: investigating surface properties and cell adhesion. Langmuir2017; 33: 485–493.
73.
BarthlottWNeinhuisC.Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta1997; 202: 1–8.
74.
SolgaACermanZStrifflerBFet al. The dream of staying clean: lotus and biomimetic surfaces. Bioinspir Biomim2007; 2: S126–S134.
75.
Santander-BorregoMGreenDWChirilaTVet al. Click functionalization of methacrylate-based hydrogels and their cellular response. J Polym Sci A: Polym Chem2014; 52: 1781–1789.
76.
TsarevskyNVBencherifSMatyjaszewskiK.Graft copolymers by a combination of ATRP and two different consecutive click reactions. Macromolecules2007; 40: 4439–4445.
77.
Araki-SasakiKOhashiYSasabeTet al. An SV40-immortalized human corneal epithelial cell line and its characterization. Invest Ophthalmol Vis Sci1995; 36: 614–621.
78.
KruszewskiFHWalkerTLDiPasqualeLC.Evaluation of a human corneal epithelial cell line as an in vitro model for assessing ocular irritation. Fundam Appl Toxicol1997; 36: 130–140.
79.
ToropainenERantaVPTalvitieAet al. Culture model of human corneal epithelium for prediction of ocular drug absorption. Invest Ophthalmol Vis Sci2001; 42: 2942–2948.
80.
BeckerUEhrhardtCDaumNet al. Expression of ABC-transporters in human corneal tissue and the transformed cell line, HCE-T. J Ocul Pharmacol Ther2007; 23: 172–181.
81.
ReichlS.Cell culture models of the human cornea – a comparative evaluation of their usefulness to determine ocular drug absorption in-vitro. J Pharm Pharmacol2008; 60: 299–307.
82.
MassiaSPHubbellJA.Covalently attached GRGD on polymer surfaces promotes biospecific adhesion of mammalian cells. Ann N Y Acad Sci1990; 589: 261–270.
83.
MeiYBeersKLByrdHCMet al. Solid-phase ATRP synthesis of peptide-polymer hybrids. J Am Chem Soc2004; 126: 3472–3476.
84.
KaruriNWLiliensiekSTeixeiraAIet al. Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells. J Cell Sci2004; 117: 3153–3164.
85.
LiliensiekSJCampbellSNealeyPFet al. The scale of substratum topographic features modulates proliferation of corneal epithelial cells and corneal fibroblasts. J Biomed Mater Res A2006; 79: 185–192.
86.
MassiaSPHubbellJA.Covalent surface immobilization of Arg-Gly-Asp- and Tyr-Ile-Gly-Ser-Arg-containing peptides to obtain well-defined cell-adhesive substrates. Anal Biochem1990; 187: 292–301.
87.
MassiaSPHubbellJA.Human endothelial cell interactions with surface-coupled adhesion peptides on a nonadhesive glass substrate and two polymeric biomaterials. J Biomed Mater Res1991; 25: 223–242.
88.
MassiaSPHubbellJA.An RGD spacing of 440 nm is sufficient for integrin αvβ3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation. J Cell Biol1991; 114: 1089–1100.
89.
HernDLHubbellJA.Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J Biomed Mater Res1998; 39: 266–276.
90.
ElbertDLHubbellJA.Conjugate addition reactions combined with free-radical cross-linking for the design of materials for tissue engineering. Biomacromolecules2001; 2(2): 430–441.
91.
Le SauxGMagenauABöckingTet al. The relative importance of topography and RGD ligand density for endothelial cell adhesion. PLoS ONE2011; 6: e21869.
