Collagen/PEO/gold nanofibrous matrices for skin tissue engineering

As a novel approach in skin tissue engineering, gold nanoparticles (AuNPs) were synthesized and incorporated at different concentrations into collagen/PEO nanofibrous matrices in this study. The group containing 14.27 ppm AuNPs (CM-Au) had the best nanofibrous morphology. CM-Au was cross-linked with glutaraldehyde vapor (CM-AuX). All groups were disrupted in collagenase in 2 h, but cross-linked groups and Matriderm1397904493 resisted hydrolytic degradation for 7 and 14 days, respectively. Due to its small pores and dense structure, lower water swelling results (7.26 ± 2.62 g/g) were obtained for CM-AuX than Matriderm (17.51 ± 1.97 g/g). CM-Au and Matriderm had statistically similar tensile strength and elastic modulus, but elongation at break of CM-Au (over 100%) was significantly better than that of Matriderm. After cross-linking, tensile strength and elastic modulus of collagen matrix was further improved. AuNPs (37 and 42 nm) seemed to be nontoxic on 3T3 fibroblasts and keratinocytes for different time periods. CM-AuX scaffold extracts were also nontoxic for 3T3 fibroblasts and keratinocytes. The L929 cell attachment and proliferation on CM-AuX were comparable with Matriderm, indicating good in vitro biocompatibility. As a whole, collagen matrices incorporated with AuNPs are potential biomaterial candidates for skin tissue engineering.

PDF

___

Agarwal S, Mishra P, Shivange G, Kodipelli N, Moros M, de la Fuente JM, Anindya R (2015). Citrate-capped gold nanoparticles for the label-free detection of ubiquitin C-terminal hydrolase-1. Analyst 140: 1166–1173.
Baker BM, Gee AO, Metter RB, Nathan AS, Marklein RA, Burdick JA, Mauck RL (2008). The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials 29: 2348–2358.
Balasubramani G, Ramkumar R, Krishnaveni N, Pazhanimuthu A, Natarajan T, Sowmiya R, Perumal P (2015). Structural characterization, antioxidant and anticancer properties of gold nanoparticles synthesized from leaf extract (decoction) of Antigonon leptopus Hook. & Arn. J Trace Elem Med Biol 30: 83–89.
Buttafoco L, Kolkman NG, Engbers-Buijtenhuijs P (2006). Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials 27: 724–734.
Castaneda L, Valle J, Yang N, Pluskat S, Slowinska K (2008). Collagen cross-linking with Au nanoparticles. Biomacromolecules 9: 3383–3388.
Chakrapani VY, Gnanamani A (2012). Electrospinning of type I collagen and PCL nanofibers using acetic acid. J Appl Polym Sci 125: 3221–3227.
Chang MC, Tanaka J (2002). FT-IR study for hydroxyapatite/ collagen nanocomposite cross-linked by glutaraldehyde. Biomaterials 23: 4811–4818.
Charulatha V, Rajaram A (2003). Influence of different cross-linking treatments on the physical properties of collagen membranes. Biomaterials 24: 759–767.
Chen JP, Chang GY, Chen JK (2008). Electrospun collagen/chitosan nanofibrous membrane as wound dressing. Colloid Surface A 313–314: 183–188.
Cozad M, Bachman S, Grant S (2011). Assessment of decellularized porcine diaphragm conjugated with gold nanomaterials as a tissue scaffold for wound healing. J Biomed Mater Res A 99: 426–434.
Cui Q, Yashchenok A, Zhang L, Li L, Masic A, Wienskol G, Möhwald H, Bargheer M (2014). Fabrication of bifunctional gold/gelatin hybrid nanocomposites and their application. ACS Appl Mater Interfaces 6: 1999–2002.
Deeken CR, Fox DB, Bachman SL, Ramshaw BJ, Grant SA (2011). Characterization of bionanocomposite scaffolds comprised of amine-functionalized gold nanoparticles and silicon carbide nanowires crosslinked to an acellular porcine tendon. J Biomed Mater Res B 97: 334–344.
Dong B, Arnoult O, Wnek GE (2009). Electrospinning of collagen nanofiber scaffolds from benign solvents. Macromol. Rapid Commun 30: 539–542.
Duan H, Feng B, Guo X, Wang J, Zhao L, Zhou G, Liu W, Cao Y, Zhang W (2013). Engineering of epidermis skin grafts using electrospun nanofibrous gelatin/polycaprolactone membranes. Int J Nanomed 8: 2077–2084.
Duan X, Sheardown H (2006). Dendrimer crosslinked collagen as a corneal tissue engineering scaffold: mechanical properties and corneal epithelial cell interactions. Biomaterials 27: 4608–4617.
Ehmann HMA, Breitwieser D, Winter S, Gspan C, Koraimann G, Maver U, Sega M, Köstler S, Stana-Kleinschek K, Spirk S et al. (2015). Gold nanoparticles in the engineering of antibacterial and anticoagulant surfaces. Carbohyd Polym 117: 34–42.
Fathi-Azarbayjani A, Qun L, Chan YW, Chan SY (2010). Novel vitamin and gold-loaded nanofiber facial mask for topical delivery. Aaps Pharmscitech 11: 1164–1170.
Fischer RL, McCoy MG, Grant SA (2012). Electrospinning collagen and hyaluronic acid nanofiber meshes. J Mater Sci-Mater M 23: 1645–1654.
Fleischer S, Shevach M, Feiner R, Dvir T (2014). Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues. Nanoscale 6: 9410–9414.
Frens G (1973). Controlled nucleation for regulation of particle-size in monodisperse gold suspensions. Nature Physical Science 241: 20–22.
Goodman CM, McCusker CD, Yilmaz T (2004). Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chem 157: 897–900.
Gopalakrishnan R, Azhagiya Singam ER, Vijaya Sundar J, Subramanian V (2015). Interaction of collagen like peptides with gold nanosurfaces: a molecular dynamics investigation. Phys Chem Chem Phys 17: 5172–5186.
Grant DN, Benson J, Cozad MJ, Whelove OE, Bachman SL, Ramshaw BJ, Grant DA, Grant SA (2011). Conjugation of gold nanoparticles to polypropylene mesh for enhanced biocompatibility. J Mater Sci-Mater M 22: 2803–2812.
Grant SA, Spradling CS, Grant DN, Fox DB, Jimenez L, Grant DA, Rone RJ (2014). Assessment of the biocompatibility and stability of a gold nanoparticle collagen bioscaffold. J Biomed Mater Res A 102: 332–339.
Higuchi A, Tsukamoto Y (2004). Cell separation of hepatocytes and fibroblasts through surface-modified polyurethane membranes. J Biomed Mater Res A 71: 470–479.
Hsu FY, Hung YS, Liou HM, Shen CH (2010). Electrospun hyaluronate–collagen nanofibrous matrix and the effects of varying the concentration of hyaluronate on the characteristics of foreskin fibroblast cells. Acta Biomater 6: 2140–2147
Huang GP, Shanmugasundaram S (2015). An investigation of common crosslinking agents on the stability of electrospun collagen scaffolds. J Biomed Mater Res A 103: 762–771.
Huang L, Nagapudi K, Apkarian RP (2001). Engineered collagen– PEO nanofibers and fabrics. J Biomat Sci-Polym E 12: 979–993.
Hung HS, Chang CH, Chang CJ, Tang CM, Kao WC, Lin SZ, Hsieh HH, Chu MY, Sun WS, Hsu SH (2014). In vitro study of a novel nanogold-collagen composite to enhance the mesenchymal stem cell behavior for vascular regeneration. PLoS ONE 9: e104019.
Jin HJ, Chen J, Karageorgiou V, Altman GH, Kaplan DL (2004). Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials 25: 1039–1047.
Jung D, Minami I, Patel S, Lee J, Jiang B, Yuan Q, Li L, Kobayashi S, Chen Y, Lee KB et al. (2012). Incorporation of functionalized gold nanoparticles into nanofibers for enhanced attachment and differentiation of mammalian cells. J Nanobiotechnology 10: 23.
Kimling J, Maier M, Okenve B, Kotaidis V, Ballot H, Plech A (2006). Turkevich method for gold nanoparticle synthesis revisited. J Phys Chem B 110:15700–15707.
Ko WK, Heo DN, Moon HJ, Lee SJ, Bae MS, Lee JB, Sun IC, Jeon HB, Park HK, Kwon IK (2015). The effect of gold nanoparticle size on osteogenic differentiation of adipose-derived stem cells. J Colloid Interf Sci 438: 68–76.
Lee CH, Chang SH, Chen WJ, Hung KC, Lin YH (2015). Augmentation of diabetic wound healing and enhancement of collagen content using nanofibrous glucophage-loaded collagen/PLGA scaffold membranes. J Colloid Interf Sci 439: 88–97.
Li X, Robinson SM, Gupta A, Saha K, Jiang Z, Moyano DF, Sahar A, Riley MA, Rotello VM (2014). Functional gold nanoparticles as potent antimicrobial agents against multi-drug-resistant bacteria. ACS Nano 8: 10682–10686.
Lin HY, Kuo YJ, Chang SH, Ni T (2013). Characterization of electrospun nanofiber matrices made of collagen blends as potential skin substitutes. Biomed Mater 8: 025009.
Liu SJ, Kau YC, Chou CY, Chen JK, Wu RC (2010). Electrospun PLGA/collagen nanofibrous membrane as early-stage wound dressing. J Membrane Sci 355: 53–55.
Lowery JL, Datta N, Rutledge GC (2010). Effect of fiber diameter, pore size and seeding method on growth of human dermal fibroblasts in electrospun poly(epsilon-caprolactone) fibrous mats. Biomaterials 31: 491–504.
Lu S, Xia D, Huang G, Jing H, Wang Y, Gu H (2010). Concentration effect of gold nanoparticles on proliferation of keratinocytes. Colloid Surface B 81: 406–411.
Manjumeena R, Elakkiya T, Duraibabu D, Feroze Ahamed A, Kalaichelvan P, Venkatesan R (2015). “Green” biocompatible organic-inorganic hybrid electrospun nanofibers for potential biomedical applications. J Biomater Appl 29: 1039–1055.
Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002). Electrospinning of collagen nanofibers. Biomacromolecules 3: 232–238.
McKeon‐Fischer KD, Freeman JW (2011). Characterization of electrospun poly(L‐lactide) and gold nanoparticle composite scaffolds for skeletal muscle tissue engineering. J Tissue Eng Regen M 5: 560–568.
Obaid G, Chambrier I, Cook MJ, Russell DA (2015). Cancer targeting with biomolecules: a comparative study of photodynamic therapy efficacy using antibody or lectin conjugated phthalocyanine-PEG gold nanoparticles. Photochem Photobiol Sci 14: 737–747.
Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen‐Dechent W (2007). Size‐dependent cytotoxicity of gold nanoparticles. Small 3: 1941–1949.
Patra HK, Banerjee S, Chaudhuri U, Lahiri P, Dasgupta A (2007). Cell selective response to gold nanoparticles. Nanomed Nanotechnol 3: 111–119.
Paviolo C, Chon JW, Clayton AH (2015). Inhibiting EGFR clustering and cell proliferation with gold nanoparticles. Small 11: 1638– 1643.
Ravichandran R, Sridhar R, Venugopal JR, Sundarrajan S, Mukherjee S, Ramakrishna S (2014). Gold nanoparticle loaded hybrid nanofibers for cardiogenic differentiation of stem cells for infarcted myocardium regeneration. Macromol Biosci 14: 515–525.
Regiel-Futyra A, Kus-Liśkiewicz M, Sebastian V, Irusta S, Arruebo M, Stochel G, Kyzioł A (2015). Development of noncytotoxic chitosan-gold nanocomposites as efficient antibacterial materials. ACS Appl Mater Interfaces 7: 1087–1099.
Rho KS, Jeong L, Lee G, Seo BM, Park YJ, Hong SD (2006). Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing. Biomaterials 27: 1452–1461.
Sanna V, Pala N, Dessì G, Manconi P, Mariani A, Dedola S, Rassu M, Crosio C, Iaccarino C, Sechi M (2014). Single-step green synthesis and characterization of gold-conjugated polyphenol nanoparticles with antioxidant and biological activities. Int J Nanomed 9: 4935–4951.
Schlinkert P, Casals E, Boyles M, Tischler U, Hornig E, Tran N, Zhao J, Himly M, Riediker M, Oostingh G et al. (2015). The oxidative potential of differently charged silver and gold nanoparticles on three human lung epithelial cell types. J Nanobiotechnology 13: 1.
Shevach M, Fleischer S, Shapira A, Dvir T (2014). Gold nanoparticle-decellularized matrix hybrids for cardiac tissue engineering. Nano Lett 14: 5792–5796.
Silveira PCL, Venâncio M, Souza PS, Victor EG, de Souza Notoya F, Paganini CS, Streck EL, da Silva L, Pinho RA, Paula MMS (2014). Iontophoresis with gold nanoparticles improves mitochondrial activity and oxidative stress markers of burn wounds. Mater Sci Eng C Mater Biol Appl 44: 380–385.
Silver F (1994). Biomaterials, Medical Devices and Tissue Engineering: An Integrated Approach. 1st ed. London, UK: Chapman and Hall.
Sionkowska A, Kozłowska J (2010). Characterization of collagen/ hydroxyapatite composite sponges as a potential bone substitute. Int J Biol Macromol 47: 483–487.
Wang S, Lu W, Tovmachenko O, Rai US, Yu H (2008). Challenge in understanding size and shape dependent toxicity of gold nanomaterials in human skin keratinocytes. Chem Phys Lett 463: 145–149.
Whelove OE, Cozad MJ, Lee BD, Sengupta S, Bachman SL, Ramshaw BJ, Grant SA (2011). Development and in vitro studies of a polyethylene terephthalate-gold nanoparticle scaffold for improved biocompatibility. J Biomed Mater Res B 99: 142–149.
Wittaya-Areekul S, Prahsarn C (2006). Development and in vitro evaluation of chitosan–polysaccharides composite wound dressings. Int J Pharm 313:123–128.
Zhang M, Wang J, Xu W, Luan J, Li X, Zhang Y, Dong H (2015). The mechanical property of Rana chensinensis skin collagen/poly (L-lactide) fibrous membrane. Mater Lett 139: 647–470.
Zhou T, Wang N, Xue Y, Ding T, Liu X, Mo X, Sun J (2015). Development of biomimetic tilapia collagen nanofibers for skin regeneration through inducing keratinocytes differentiation and collagen synthesis of dermal fibroblasts. ACS Appl Mater Interfaces 7: 3253–3262.
Zhou Y, Kong Y, Kundu S, Cirillo J, Liang H (2012). Antibacterial activities of gold and silver nanoparticles against Escherichia coli and bacillus Calmette-Guérin. J Nanobiotechnology 10: 19