Fabrication and characterization of electrospun laminin-functionalized silk fibroin/poly(ethylene oxide) nanofibrous scaffolds for peripheral nerve regeneration
Mina Rajabi
Department of Polymer, School of Chemical Engineering, College of Engineering, University of Tehran, Tehran, Iran
Search for more papers by this authorCorresponding Author
Masoumeh Firouzi
Tissue Repair Laboratory, Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran
Correspondence to: M. Firouzi; e-mail: [email protected] or P. Zahedi; e-mail: [email protected]Search for more papers by this authorZahra Hassannejad
Pediatric Urology and Regenerative Medicine Research Center, Children's Hospital Medical Center, Tehran University of Medical Sciences, Tehran, Iran
Sina Trauma and Surgery Research Center, Tehran University of Medical Sciences, Tehran, Iran
Search for more papers by this authorIsmaeil Haririan
Department of Pharmaceutical Biomaterials and Medical Biomaterials Research Center, Faculty of Pharmacy and Department of Pharmaceutics, Tehran University of Medical Sciences, Tehran, P. O. Box: 14155-6451 Tehran, Iran
Search for more papers by this authorCorresponding Author
Payam Zahedi
Department of Polymer, School of Chemical Engineering, College of Engineering, University of Tehran, Tehran, Iran
Correspondence to: M. Firouzi; e-mail: [email protected] or P. Zahedi; e-mail: [email protected]Search for more papers by this authorMina Rajabi
Department of Polymer, School of Chemical Engineering, College of Engineering, University of Tehran, Tehran, Iran
Search for more papers by this authorCorresponding Author
Masoumeh Firouzi
Tissue Repair Laboratory, Institute of Biochemistry and Biophysics (IBB), University of Tehran, Tehran, Iran
Correspondence to: M. Firouzi; e-mail: [email protected] or P. Zahedi; e-mail: [email protected]Search for more papers by this authorZahra Hassannejad
Pediatric Urology and Regenerative Medicine Research Center, Children's Hospital Medical Center, Tehran University of Medical Sciences, Tehran, Iran
Sina Trauma and Surgery Research Center, Tehran University of Medical Sciences, Tehran, Iran
Search for more papers by this authorIsmaeil Haririan
Department of Pharmaceutical Biomaterials and Medical Biomaterials Research Center, Faculty of Pharmacy and Department of Pharmaceutics, Tehran University of Medical Sciences, Tehran, P. O. Box: 14155-6451 Tehran, Iran
Search for more papers by this authorCorresponding Author
Payam Zahedi
Department of Polymer, School of Chemical Engineering, College of Engineering, University of Tehran, Tehran, Iran
Correspondence to: M. Firouzi; e-mail: [email protected] or P. Zahedi; e-mail: [email protected]Search for more papers by this authorAbstract
The peripheral nerve regeneration is still one of the major clinical problems, which has received a great deal of attention. In this study, the electrospun silk fibroin (SF)/poly(ethylene oxide) (PEO) nanofibrous scaffolds were fabricated and functionalized their surfaces with laminin (LN) without chemical linkers for potential use in the peripheral nerve tissue engineering. The morphology, surface chemistry, thermal behavior and wettability of the scaffolds were examined to evaluate their performance by means of scanning electron microscopy (SEM), Fourier transform infrared (FTIR) spectroscopy, differential scanning calorimetry (DSC) and water contact angle (WCA) measurements, respectively. The proliferation and viability of Schwann cells onto the surfaces of SF/PEO nanofibrous scaffolds were investigated using SEM and thiazolyl blue (MTT) assay. The results showed an improvement of SF conformation and surface hydrophilicity of SF/PEO nanofibers after methanol and O2 plasma treatments. The immunostaining observation indicated a continuous coating of LN on the scaffolds. Improving the surface hydrophilicity and LN functionalization significantly increased the cell proliferation and this was more prominent after 5 days of culture time. In conclusion, the obtained results revealed that the electrospun LN-functionalized SF/PEO nanofibrous scaffold could be a promising candidate for peripheral nerve tissue regeneration. © 2017 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 106B: 1595–1604, 2018.
REFERENCES
- 1 Kijeńska E, Prabhakaran MP, Swieszkowski W, Kurzydlowski KJ, Ramakrishna S. Interaction of Schwann cells with laminin encapsulated PLCL core–shell nanofibers for nerve tissue engineering. Eur Polym J 2014; 50: 30–38.
- 2 Abbasi N, Soudi S, Hayati-Roodbari N, Dodel M, Soleimani M. The effects of plasma treated electrospun nanofibrous poly (ɛ-caprolactone) scaffolds with different orientations on mouse embryonic stem cell proliferation. Cell J 2014; 16(3): 245–254.
- 3 Griffin J, Delgado-Rivera R, Meiners S, Uhrich KE. Salicylic acid-derived poly (anhydride-ester) electrospun fibers designed for regenerating the peripheral nervous system. J Biomed Mater Res A 2011; 97(3): 230–242.
- 4 Kijeńska E, Prabhakaran MP, Swieszkowski W, Kurzydlowski KJ, Ramakrishna S. Electrospun bio-composite P (LLA-CL)/collagen I/collagen III scaffolds for nerve tissue engineering. J Biomed Mater Res B 2012; 100(4): 1093–1102.
- 5 Cooper A, Bhattarai N, Zhang M. Fabrication and cellular compatibility of aligned chitosan–PCL fibers for nerve tissue regeneration. Carbohydr Polym 2011; 85(1): 149–156.
- 6 Nectow AR, Marra KG, Kaplan DL. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B 2011; 18(1): 40–50.
- 7
Amiraliyan N,
Nouri M,
Kish MH. Structural characterization and mechanical properties of electrospun silk fibroin nanofiber mats. Polym Sci Ser A 2010; 52(4): 407–412.
10.1134/S0965545X10040097 Google Scholar
- 8 Ayutsede J, Gandhi M, Sukigara S, Micklus M, Chen HE, Ko F. Regeneration of Bombyx mori silk by electrospinning. Part 3: Characterization of electrospun nonwoven mat. Polymer 2005; 46(5): 1625–1634.
- 9 Jin HJ, Fridrikh SV, Rutledge GC, Kaplan DL. Electrospinning Bombyx mori silk with poly (ethylene oxide). Biomacromolecules 2002; 3(6): 1233–1239.
- 10 Kim UJ, Park J, Li C, Jin HJ, Valluzzi R, Kaplan DL. Structure and properties of silk hydrogels. Biomacromolecules 2004; 5(3): 786–792.
- 11 Inoue S, Tanaka K, Arisaka F, Kimura S, Ohtomo K, Mizuno S. Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6: 6: 1 molar ratio. J Biol Chem 2000; 275(51): 40517–40528.
- 12 Chen JP, Chen SH, Lai GJ. Preparation and characterization of biomimetic silk fibroin/chitosan composite nanofibers by electrospinning for osteoblasts culture. Nanoscale Res Lett 2012; 7(170): 1–11.
- 13 Sashina ES, Bochek AM, Novoselov NP, Kirichenko DA. Structure and solubility of natural silk fibroin. Russ J Appl Chem 2006; 79(6): 869–876.
- 14 Jin HJ, Kaplan DL. Mechanism of silk processing in insects and spiders. Nature 2003; 424(6952): 1057–1061.
- 15 Motta A, Fambri L, Migliaresi C. Regenerated silk fibroin films: Thermal and dynamic mechanical analysis. Macromol Chem Phys 2002; 203(10–11): 1658–1665.
- 16 Leal-Egaña A, Scheibel T. Interactions of cells with silk surfaces. J Mater Chem 2012; 22(29): 14330–14336.
- 17 López-Pérez PM, Da Silva RMP, Sousa RA, Pashkuleva I, Reis RL. Plasma-induced polymerization as a tool for surface functionalization of polymer scaffolds for bone tissue engineering: An in vitro study. Acta Biomater 2010; 6(9): 3704–3712.
- 18
Wang S,
Zhang Y,
Wang H,
Dong Z. Preparation, characterization and biocompatibility of electrospinning heparin-modified silk fibroin nanofibers. Int J Biol Macromol 2011; 48(2): 345–353.
10.1016/j.ijbiomac.2010.12.008 Google Scholar
- 19 Estrada V, Tekinay AB, Muller HW. Neural ECM mimetics. Prog Brain Res 2014; 214: 391–413.
- 20
Colognato H,
Yurchenco PD. Form and function: The laminin family of heterotrimers. Dev Dyn 2000; 218(2): 213–234.
10.1002/(SICI)1097-0177(200006)218:2<213::AID-DVDY1>3.0.CO;2-R CAS PubMed Web of Science® Google Scholar
- 21
Mey J,
Brook G,
Hodde D,
Kriebel A. Electrospun fibers as substrates for peripheral nerve regeneration. In: R Jayakumar, S Nair, editors. Biomedical Applications of Polymeric Nanofibers. Heidelberg/Berlin: Springer; 2011. pp 131–170.
10.1007/12_2011_122 Google Scholar
- 22 Neal RA, McClugage SG III, Link MC, Sefcik LS, Ogle RC, Botchwey EA. Laminin nanofiber meshes that mimic morphological properties and bioactivity of basement membranes. Tissue Eng Part C 2008; 15(1): 11–21.
- 23
Zander NE,
Beebe TP Jr. Immobilized laminin concentration gradients on electrospun fiber scaffolds for controlled neurite outgrowth. Biointerphases 2014; 9(1): 011003.
10.1116/1.4857295 Google Scholar
- 24 Neal RA, Tholpady SS, Foley PL, Swami N, Ogle RC, Botchwey EA. Alignment and composition of laminin–polycaprolactone nanofiber blends enhance peripheral nerve regeneration. J Biomed Mater Res A 2012; 100(2): 406–423.
- 25 Tresco PA. Tissue engineering strategies for nervous system repair. Prog Brain Res 2000; 128: 349–363.
- 26 Hsu SH, Kuo WC, Chen YT, Yen CT, Chen YF, Chen KS, Huang WC, Cheng H. New nerve regeneration strategy combining laminin-coated chitosan conduits and stem cell therapy. Acta Biomater 2013; 9(5): 6606–6615.
- 27 Chen Z-L, Strickland S. Laminin γ1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J Cell Biol 2003; 163(4): 889–899.
- 28 Jeong L, Yeo IS, Kim HN, Yoon YI, Jang DH, Jung SY, Min BM, Park WH. Plasma-treated silk fibroin nanofibers for skin regeneration. Int J Biol Macromol 2009; 44(3): 222–228.
- 29 Li S, Wu H, Hu XD, Tu CQ, Pei FX, Wang GL, Lin W, Fan HS. Preparation of electrospun PLGA-silk fibroin nanofibers-based nerve conduits and evaluation in vivo. Artif Cell Blood Subtitutes Biotechnol 2012; 40(1–2): 171–178.
- 30 Li D, Frey MW, Joo YL. Characterization of nanofibrous membranes with capillary flow porometry. J Membr Sci 2006; 286(1): 104–114.
- 31 Firouzi M, Sabouni F, Deezagi A, Pirbasti ZH, Poorrajab F, Rahimi-Movaghar V. Schwann cell apoptosis and p75NTR siRNA. Iran J Allergy Asthma Immunol 2011; 10(1): 53–59.
- 32 Nategh M, Firouzi M, Naji-Tehrani M, Zanjani LO, Hassannejad Z, Nabian MH, Zadegan SA, Karimi M, Rahimi-Movaghar V. Subarachnoid space transplantation of Schwann and/or olfactory ensheathing cells following severe spinal cord injury fails to improve locomotor recovery in rats. Acta Med Iran 2016; 54(9): 562–569.
- 33 Boulet-Audet M, Vollrath F, Holland C. Identification and classification of silks using infrared spectroscopy. J Exp Biol 2015; 218(19): 3138–3149.
- 34 Lawrence BD. Methods to Produce Silk Fibroin Film Biomaterials for Applications in Corneal Tissue Regeneration. Medford, MA: Tufts University; 2008. p 134.
- 35 Wang HY, Zhang YQ. Effect of regeneration of liquid silk fibroin on its structure and characterization. Soft Matter 2013; 9(1): 138–145.
- 36 Min BM, Jeong L, Lee KY, Park WH. Regenerated silk fibroin nanofibers: Water vapor-induced structural changes and their effects on the behavior of normal human cells. Macromol Biosci 2006; 6(4): 285–292.
- 37 Yang Y, Chen X, Ding F, Zhang P, Liu J, Gu X. Biocompatibility evaluation of silk fibroin with peripheral nerve tissues and cells in vitro. Biomaterials 2007; 28(9): 1643–1652.
- 38 Cao H, Chen X, Huang L, Shao Z. Electrospinning of reconstituted silk fiber from aqueous silk fibroin solution. Mater Sci Eng C 2009; 29(7): 2270–2274.
- 39 Ramsey WS, Hertl W, Nowlan ED, Binkowski NJ. Surface treatments and cell attachment. In Vitro Cell Dev Biol Plant 1984; 20(10): 802–808.
- 40
Aumailley M,
Smyth N. The role of laminins in basement membrane function. J Anat 1998; 193(1): 1–21.
10.1046/j.1469-7580.1998.19310001.x Google Scholar
- 41 Prabhakaran MP, Venugopal J, Chan CK, Ramakrishna S. Surface modified electrospun nanofibrous scaffolds for nerve tissue engineering. Nanotechnology 2008; 19(45): 455102.