Murat DEMİRBİLEK, Selçuk AKTÜRK, Nelisa LAÇİN TÜRKOĞLU

N-Acetylglucoseamine modified alginate sponges as scaffolds for skin tissue engineering

In the treatment of dermal wounds, wound-dressing materials prepared from natural mucopolysaccharides are widely used because of their advantages such as nonirritation, nontoxicity, and ease in topical application. In the present study, alginate hydrogels modified with N-acetyl glucose amine (NAG) were prepared as wound-dressing material. Physical, chemical, thermal, and mechanical properties of the hydrogels were studied. Cytotoxicity of the hydrogels on endothelial (HUVEC) and keratinocyte (HaCaT) cells were examined. Anti- and proinflammatory cytokine levels of human monocyte-macrophage cells (THP-1) stimulated with hydrogels were determined. According to the results, increasing the NAG concentration led to an increase in the swelling and nitrogen ratios in the hydrogels. Additionally, increasing the NAG concentration decreased elastic modulus and degradation time. Hydrogels were not cytotoxic on HaCaT and HUVEC cells. It stimulated IL-10 and TNF-alpha levels at a small rate.

PDF

___

Asada M, Sugie M, Inoue M, Nakagomı K, Hongo S, Murata K, Tomizuka N (1997). Inhibitory effect of alginic acids on hyaluronidase and on histamine release from mast cells. Biosci Biotech Bioch 61: 1030-1032.
Ates A, Kinikli G, Turgay M, Duman M (2004). The efficacy of viscosupplementation therapy with sodium hyaluronate in patients with knee osteoarthritis. Turk J Geriatr 7: 21-24.
Balakrishnan B, Mohanty M, Umashankar P, Jayakrishnan A (2005). Evaluation of an in situ forming hydrogel wound dressing based on oxidized alginate and gelatin. Biomaterials 26: 6335-6342.
Boeckel DG, Shinkai RSA, Grossi ML, Teixeira ER (2014). In vitro evaluation of cytotoxicity of hyaluronic acid as an extracellular matrix on OFCOL II cells by the MTT assay. Oral Surg Oral Med Oral Pathol Oral Radiol 117: 423-428.
Boehler RM, Graham JG, Shea LD (2011). Tissue engineering tools for modulation of the immune response. Biotechniques 51: 239-244.
Catanzano O, Desposito V, Acierno S, Ambrosio M, De Caro C, Avagliano C, Ungaro F (2015). Alginatehyaluronan composite hydrogels accelerate wound healing process. Carbohydr Polym 131: 407-414.
Chang C, Duan B, Zhang L (2009). Fabrication and characterization of novel macroporous cellulosealginate hydrogels. Polymer 50: 5467-5473.
Chaudhuri O, Gu L, Darnell M, Klumpers D, Bencherif SA, Weaver JC, Mooney DJ (2015). Substrate stress relaxation regulates cell spreading. Nat Commun 6: 7365-7372.
Croce M, Boraldi F, Quaglino D, Tiozzo R, Pasquali-Ronchetti I (2003). Hyaluronan uptake by adult human skin fibroblasts in vitro. Eur J Histochem 47: 63-73.
Croce M, Dyne K, Boraldi F, Quaglino D, Cetta G, Tiozzo R, Ronchetti IP (2001). Hyaluronan affects protein and collagen synthesis by in vitro human skin fibroblasts. Tissue Cell 33: 326-331.
Das D, Pal S (2015). Modified biopolymer-dextrin based crosslinked hydrogels: application in controlled drug delivery. RSC Adv 5: 25014-25050.
Demidova-Rice TN, Hamblin MR, Herman IM (2012). Acute and impaired wound healing: pathophysiology and current methods for drug delivery, part 1: normal and chronic wounds: biology, causes, and approaches to care. Adv Skin Wound Care 25: 304-314.
Draget KI, Skjåk-Bræk G, Smidsrød O (1997). Alginate based new materials. Int J Biol Macromol 21: 47-55.
Dvir-Ginzberg M, Gamlieli-Bonshtein I, Agbaria R, Cohen S (2003). Liver tissue engineering within alginate scaffolds: effects of cell-seeding density on hepatocyte viability, morphology, and function. Tissue Eng 9: 757-766.
Franz S, Rammelt S, Scharnweber D, Simon JC (2011). Immune responses to implantsa review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32: 6692-6709.
Fundueanu G, Nastruzzi C, Carpov A, Desbrieres J, Rinaudo M (1999). Physico-chemical characterization of Ca-alginate microparticles produced with different methods. Biomaterials 20: 1427-1435.
Grellner W, Georg T, Wilske J (2000). Quantitative analysis of proinflammatory cytokines (IL-1β, IL-6, TNF-α) in human skin wounds. Forensic Sci Int 113: 251-264.
Harper BA (2013). Understanding interactions in wet alginate film formation used for in-line food processes. PhD Thesis, University of Guelph, Ontario, Canada.
Hashimoto T, Suzuki Y, Tanihara M, Kakimaru Y, Suzuki K (2004). Development of alginate wound dressings linked with hybrid peptides derived from laminin and elastin. Biomaterials 25: 1407-1414.
Hsu SH, Whu SW, Hsieh SC, Tsai CL, Chen DC, Tan TS (2004). Evaluation of chitosan‐alginate‐hyaluronate complexes modified by an RGD‐containing protein as tissue‐engineering scaffolds for cartilage regeneration. Artif Organs 28: 693-703.
Jahn M, Baynes JW, Spiteller G (1999). The reaction of hyaluronic acid and its monomers, glucuronic acid and N-acetylglucosamine, with reactive oxygen species. Carbohydr Res 321: 228-234.
Kaklamani G, Cheneler D, Grover LM, Adams MJ, Bowen J (2014). Mechanical properties of alginate hydrogels manufactured using external gelation. J Mech Behav Biomed Mater 36: 135- 142.
Kataria K, Gupta A, Rath G, Mathur R, Dhakate S (2014). In vivo wound healing performance of drug loaded electrospun composite nanofibers transdermal patch. Int J Pharm 469: 102- 110.
Kim JO, Park JK, Kim JH, Jin SG, Yong CS, Li DX, Lyoo WS (2008). Development of polyvinyl alcoholsodium alginate gel-matrixbased wound dressing system containing nitrofurazone. Int J Pharm 359: 79-86.
Komine M, Rao LS, Kaneko T, Tomic-Canic M, Tamaki K, Freedberg IM, Blumenberg M (2000). Inflammatory versus proliferative processes in epidermis tumor necrosis factor α induces k6b keratin synthesis through a transcriptional complex containing NFκB and C/EBPβ. J Biol Chem 275: 32077-32088.
Laus R, Costa TG, Szpoganicz B, Fávere VT (2010). Adsorption and desorption of Cu (II), Cd (II) and Pb (II) ions using chitosan crosslinked with epichlorohydrin-triphosphate as the adsorbent. J Hazard Mater 183: 233-241.
Lee JS, Lee SU, Che CY, Lee JE (2015). Comparison of cytotoxicity and wound healing effect of carboxymethylcellulose and hyaluronic acid on human corneal epithelial cells. Int J Ophthalmol 8: 215- 221.
Lee KY, Mooney DJ (2012). Alginate: properties and biomedical applications. Prog Polym Sci 37: 106-126.
Li Z, Ramay HR, Hauch KD, Xiao D, Zhang M (2005). Chitosan alginate hybrid scaffolds for bone tissue engineering. Biomaterials 26: 3919-3928.
Maia F, da Silva J, do Amaral F, Martin A, Lobo A, Soares L (2013). Morphological and chemical evaluation of bone with apatitecoated Al2O3 implants as scaffolds for bone repair. Cerâmica 59: 533-538.
Martinez FO, Gordon S (2014). The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6: 12703-12728.
McKee CM, Penno MB, Cowman M, Burdick MD, Strieter RM, Bao C, Noble PW (1996). Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 98: 2403-2416.
Mohan N, Nair PD (2005). Novel porous, polysaccharide scaffolds for tissue engineering applications. Trends Biomater Artif Organs 18: 219-224.
Noble PW, McKee CM, Cowman M, Shin HS (1996). Hyaluronan fragments activate an NF-kappa B/I-kappa B alpha autoregulatory loop in murine macrophages. J Exp Med 183: 2373-2378.
Olutoye OO, Cohen IK (1996). Fetal wound healing: an overview. Wound Repair Regen 4: 66-74.
Rowley JA, Madlambayan G, Mooney DJ (1999). Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20: 45-53.
Sarmento B, Ferreira D, Veiga F, Ribeiro A (2006). Characterization of insulin-loaded alginate nanoparticles produced by ionotropic pre-gelation through DSC and FTIR studies. Carbohydr Polym 66: 1-7.
Sheehan KM, DeLott LB, West RA, Bonnema JD, DeHeer DH (2004). Hyaluronic acid of high molecular weight inhibits proliferation and induces cell death in U937 macrophage cells. J Life Sci 75: 3087-3102.
Simmons CA, Alsberg E, Hsiong S, Kim WJ, Mooney DJ (2004). Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35: 562-569.
Sinha M, Banik RM, Haldar C, Maiti P (2013). Development of ciprofloxacin hydrochloride loaded poly (ethylene glycol)/ chitosan scaffold as wound dressing. J Porous Mater 20: 799- 807.
Soares J, Santos J, Chierice G, Cavalheiro E (2004). Thermal behavior of alginic acid and its sodium salt. Eclet Quím 29: 57-64.
Straccia MC, dAyala GG, Romano I, Oliva A, Laurienzo P (2015). Alginate hydrogels coated with chitosan for wound dressing. Mar Drugs 13: 2890-2908.
Trif M, Ansorge-Schumacher M, Socaciu C (2007). Application of FTIR Spectroscopy for determination of oxidation of encapsulated sea buckthorn oil. XVth International Workshop on Bioencapsulation. Vienna, Austria, pp. 3-7.
Unemori E, Hibbs M, Amento E (1991). Constitutive expression of a 92-kD gelatinase (type V collagenase) by rheumatoid synovial fibroblasts and its induction in normal human fibroblasts by inflammatory cytokines. J Clin Invest 88: 1656-1662.
Walker M, Hobot J, Newman G, Bowler P (2003). Scanning electron microscopic examination of bacterial immobilisation in a carboxymethyl cellulose (AQUACEL®) and alginate dressings. Biomaterials 24: 883-890.
Wallace HJ, Stacey MC (1998). Levels of tumor necrosis factor-α (TNF-α) and soluble TNF receptors in chronic venous leg ulcerscorrelations to healing status. J Invest Dermatol 110: 292-296.
Werner S, Peters KG, Longaker MT, Fuller-Pace F, Banda MJ, Williams LT (1992). Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc Natl Acad Sci 89: 6896-6900.
Wiegand C, Heinze T, Hipler UC (2009). Comparative in vitro study on cytotoxicity, antimicrobial activity, and binding capacity for pathophysiological factors in chronic wounds of alginate and silver‐containing alginate. Wound Repair Regen 17: 511-521.
Xie L, Jiang M, Dong X, Bai X, Tong J, Zhou J (2012). Controlled mechanical and swelling properties of poly (vinyl alcohol)/ sodium alginate blend hydrogels prepared by freezethaw followed by Ca2+ crosslinking. J Appl Polym Sci 124: 823-831.
Zhang C, Jia Z (2010). Preparation of porous chitosan microsphere absorbent and research on its absorption ability for Cu2+ and Zn2+. International Journal of Chemistry 2: 113-120.