Electrical stimulation of nerve cells using conductive nanofibrous scaffolds for nerve tissue engineering

Tissue Engineering - Part A

Volumn 15, Issue 11, 2009, Pages 3605-3619

  Ghasemi Mobarakeh, Laleh ^a,b,c,d   Prabhakaran, Molamma P ^a   Morshed, Mohammad ^b   Nasr Esfahani, Mohammad Hossein ^d   Ramakrishna, Seeram ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b ISFAHAN UNIVERSITY OF TECHNOLOGY   (Iran)

^c ISLAMIC AZAD UNIVERSITY   (Iran)

^d ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

BIODEGRADATION; CELL CULTURE; CELL PROLIFERATION; DOPING (ADDITIVES); FOURIER TRANSFORM INFRARED SPECTROSCOPY; MECHANICAL PROPERTIES; NANOFIBERS; POLYANILINE; SCAFFOLDS; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; X RAY PHOTOELECTRON SPECTROSCOPY;

BALANCED PROPERTY; CONDUCTIVE NANOFIBERS; DOPED POLYANILINE; ELECTRICAL PROPERTY; ELECTRICAL STIMULATIONS; ELECTROSPUNS; ENHANCED CONDUCTIVITY; FIBER DIAMETERS; FOURIER TRANSFORM INFRARED; IN-VITRO; NANOFIBROUS SCAFFOLDS; NERVE CELLS; NERVE REGENERATION; NERVE TISSUE ENGINEERING; NEURITE OUTGROWTH; POLY(E-CAPROLACTONE); STEM CELL; SULFOPHENYL; X-RAY PHOTOELECTRON SPECTROSCOPY SPECTRA;

ELECTRIC PROPERTIES;

GELATIN; MOLECULAR SCAFFOLD; NANOFIBER; POLYANILINE; POLYCAPROLACTONE;

ARTICLE; BIODEGRADABILITY; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CELL STRUCTURE; CONDUCTANCE; CONTROLLED STUDY; ELECTROSTIMULATION; HYDROPHILICITY; INFRARED RADIATION; INFRARED SPECTROSCOPY; NERVE CELL STIMULATION; NERVE REGENERATION; NERVOUS TISSUE; NEURAL STEM CELL; NITROBLUE TETRAZOLIUM TEST; POROSITY; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TENSILE STRENGTH; TISSUE ENGINEERING; ULTRAVIOLET SPECTROSCOPY; X RAY PHOTOELECTRON SPECTROSCOPY;

EID: 72649100133     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0689     Document Type: Article

References (82)

1. Schmidt, C.E., Shastri, V.R., Vacanti, J.P., and Langer, R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc Natl Acad Sci USA 94, 8948, 1997.
2. Schmidt, C.E., and Leach, J.B. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng 5, 293, 2003.
3. Yang, F., Murugan, R., Ramakrishna, S., Wang, X., Mac, Y.X., and Wang, S. Fabrication of nano-structured porous PLLA scaffold intended for nerve tissue engineering. Biomaterials 25, 1891, 2004.
4. Yang, F., Xu, C.Y., Kotaki, M., Wang, S., and Ramakrishna, S. Characterization of neural, stem cells on electrospun poly(L-lactic acid) nanofibrous scaffold. J Biomater Sci Polym Ed 15, 1483, 2004.
5. Valentini, R.F., Vargo, T.G., Jr., J.A.G., and Aebischer, P. Electrically charged polymeric substrates enhance nerve fibre outgrowth in vivo. Biomaterials 13, 183, 1992.
6. Shi, G., Zhang, Z., and Rouabhia, M. The regulation of cell functions electrically using biodegradable polypyrrole-polylactide conductors. Biomaterials 9, 3792, 2003.
7. Sun, S., Titushkin, I., and Cho, M. Regulation of mesenchy-mal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry 69, 133, 2006.
8. Rivers, T.J., Hudson, T.W., and Schmidt, C.E. Synthesis of a novel biodegradable electrically conducting polymer for biomedical applications. Adv Funct Mater 12, 33, 2002.
9. Chronakis, I.S., Grapenson, S., and Jakob, A. Conductive polypyrrole nanofibers via electrospinning: electrical and morphological properties. Polymer 47, 1597, 2006.
10. Wong, J.Y., Langer, R., and Ingberi, D.E. Electrically conducting polymers can noninvasively control the shape and growth of mammalian cells. Proc Natl Acad Sci USA 91, 3201, 1994.
11. Shi, G., Rouabhia, M., Wang, Z., Dao, L.H., and Zhang, Z. A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide. Biomaterials 25, 2477, 2004.
12. Li, M., Guo, Y., Wei, Y., MacDiarmid, A.G., and Lelkes, P.I. Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials 27, 2705, 2006.
13. Jeong, S.I., Jun, I.D., Choi, M.J., Nho, Y.C., Lee, Y.M., and Shin, H. Development of electroactive and elastic nanofibers that contain polyaniline and poly (L-lactide-co-e-caprolactone) for the control of cell adhesion. Macromol Biosci 8, 627, 2008.
14. Bidez, P.R., Li, S., Macdiarmid, A.G., Venancio, E.C., Wei, Y., and Lelkes, P.I. Polyaniline, an electroactive polymer, supports adhesion and proliferation of cardiac myoblasts. J Biomater Sci Polym Ed 17, 199, 2006.
15. Li, D.F., Wang, W., Wang, H.J., Jia, X.S., and Wang, J.Y. Polyaniline films with nanostructure used as neural probe coating surfaces. Appl Surface Sci 255, 581, 2008.
16. Guimarda, N.K., Gomezb, N., and Schmidt, C.E. Conducting polymers in biomedical engineering. Prog Polym Sci 32, 876, 2007.
17. Kamalesh, S., Tan, P., Wang, J., Lee, T., Kang, E.T., and Wang, C.H. Biocompatibility of electroactive polymers in tissues. J Biomed Mater Res 52, 467, 2000.
18. Mattioli-Belmonte, M., Giavaresi, G., Biagini, G., Virgili, L., Giacomini, M., Fini, M., Giantomassi, F., Natali, D., Torri-celli, P., and Giardino, R. Tailoring biomaterial compatibility: in vivo tissue response versus in vitro cell behavior. Int J Artif Organs 26, 1077, 2003.
19. Shi, G., Rouabhia, M., Meng, S., and Zhang, Z. Electrical stimulation enhances viability of human cutaneous fibro-blasts on conductive biodegradable substrates. J Biomed Mater Res Part A 84A, 1026, 2007.
20. Liu, Y., Liu, X., Chen, J., Gilmore, K.J., and Wallace, G.G. 3D Bio-nanofibrous PPy/SIBS mats as platforms for cell cul-turing. Chem Commun 32, 3729, 2008.
21. Ghasemi-Mobarakeh, L., Prabhakaran, M.P., Morshed, M., Nasr-Esfahani, M.H., and Ramakrishna, S. Electrospun poly (e-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29, 4532, 2008.
22. Hopkins, A.R., and Rasmussen, P.G. Characterization of solution and solid state properties of undoped and doped polyanilines processed from hexafluoro-2-propanol. Macromolecules 29, 7838, 1996.
23. Blacher, S., Maquet, V., Schils, F., Martin, D., Schoenen, J., Moonen, G., Jérôme, R., and Pirard, J.P. Image analysis of the axonal ingrowth into poly(d,l-lactide) porous scaffolds in relation to the 3-D porous structure. Biomaterials 24, 1033, 2003.
24. Seidlits, S.K., Lee, J.Y., and Schmidt, C.E. Nanostructured scaffolds for neural applications. Nanomedicine 3, 183, 2008.
25. Bini, T.B., Gao, S., Wang, S., and Ramakrishna, S. Poly (L-lactide-co-glycolide) biodegradable microfibers and elec-trospun nanofibers for nerve tissue engineering: an in vitro study. J Mater Sci 41, 6453, 2006.
26. Schnell, E., Klinkhammer, K., Balzer, S., Brook, G., Kleeb, D., Dalton, P., and Mey, J. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-e-capro-lactone and a collagen/poly-e- caprolactone blend. Biomaterials 28, 3012, 2007.
27. Xu, C.Y., Inai, R., Kotaki, M., and Ramakrishna, S. Aligned biodegradable nanofibrous structure: a potential scaffold for blood vessel engineering. Biomaterials 25, 877, 2004.
28. Lee, C.H., Shin, H.J., Cho, I.H., Kang, Y.M., Kim, I.A., Park, K.D., and Shin, J.W. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 26, 1261, 2005.
29. Yang, F., Murugan, R., Wang, S., and Ramakrishna, S. Electrospinning of nano/micro scale poly(L-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26, 2603, 2005.
30. Patel, N., and Poo, M.M. Orientation of neurite growth by extracellar electric fields. J Neurosci 2, 483, 1982.
31. Freeman, J.A., Manis, P.B., Snipes, G.J., Mayes, B.N., Samson, P.C., Jr., Wikswo, J.P., and Freeman, D.B. Steady growth cone currents revealed by a novel circularly vibrating probe: a possible mechanism underlying neurite growth. J Neurosci 13, 257, 1985.
32. Sisken, B.F., Kanje, M., Lundborg, G., Herbst, E., and Kurtz, W. Stimulation of rat sciatic nerve regeneration with pulsed electromagnetic fields. Brain Res 485, 309, 1989.
33. Kotwal, A., and Schmid, C.E. Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials. Biomaterials 22, 1055, 2001.
34. Pomfret, S.J., Adams, P.N., Comfort, N.P., and Monkmana, A.P. Electrical and mechanical properties of polyaniline fibres produced by a one-step wet spinning. Polymer 41, 2265, 2000.
35. Yu, Q.Z., Shi, M.M., Deng, M., Wang, M., and Chena, H.Z. Morphology and conductivity of polyaniline sub-micron fibers prepared by electrospinning. Mater Sci Eng B 150, 70, 2008.
36. Norris, I.D., Shaker, M.M., Ko, F.K., and MacDiarmid, A.G. Electrostatic fabrication of ultrafine conducting fibers: polyaniline/polyethylene oxide blends. Synth Met 114, 109, 2000.
37. Veluru, J.B., Satheesh, K.K., Trivedi, D.C., Ramakrishna, M.V., and Srinivasan, N.T. Electrical properties of electro-spun fibers of PANI-PMMA composites. J Eng Fibers Fabrics 2, 25, 2007.
38. León, M.J.D. Electrospinning Nanofibers of Polyaniline and Polyaniline/Polystyrene and Polyethylene Oxide) Blends, Proceeding of The National Conference On Undergraduate Research, University of Kentucky, Lexington, Kentucky, 2001.
39. Bishop, A., and Gouma, P. Leuco-emeraldine based polyaniline-poly-vinyl- pyrrolidone electrospun composites and bio-composites: a preliminary study of sensing behavior. Rev Adv Mater Sci 10, 209, 2005.
40. Desai, K., Lee, J.S., and Sung, C. Nanocharacterization of electrospun nanofibers of polyaniline/poly methyl methac-rylate blends using SEM, TEM and AFM. Microsc Microanal 10, 556, 2004.
41. Koh, H.S., Yong, T., Chan, C.K., and Ramakrishna, S. Enhancement of neurite outgrowth using nano-structured scaffolds coupled with laminin. Biomaterials 29, 3574, 2008.
42. Cheng, M., Deng, J., Yang, F., Gong, Y., Zhao, N., and Zhang, X. Study on physical properties and nerve cell affinity of composite films from chitosan and gelatin solutions. Biomaterials 24, 2871, 2003.
43. Kim, C.H., Khil, M.S., Kim, H.Y., Lee, H.U., and Jahng, K.Y. An improved hydrophilicity via electrospinning for enhanced cell attachment and proliferation. J Biomed Mater Res B Appl Biomater 78B, 283, 2006.
44. Li, W.J., Cooper, J.R., Mauck, R.L., and Tuan, R.S. Fabrication and characterization of six electrospun poly(a-hydro-xyester)-based nanofibrous scaffolds for tissue engineering applications. Acta Biomater 2, 377, 2006.
45. Lee, C.Y., and Kil, J.K. Hydrophilic property by contact angle change of ion implanted polycarbonate. Rev Sci In-strum 79, 02C508, 2008.
46. Corey, J.M., Gertz, C.C., Wang, B.S., Birrell, L.K., Johnson, S.L., Martin, D.C., and Feldman, E.L. The design of electro-spun PLLA nanofiber scaffolds compatible with serum-free growth of primary motor and sensory neurons. Acta Biomater 4, 863, 2008.
47. Huangm, S.C., Ball, I.J., and Kaner, R.B. Polyaniline membranes for pervaporation of carboxylic acids and water. Macromolecules 31, 5456, 1998.
48. Lubentsov, B., Timofeeva, O., Saratovskikh, S., Krinichnyi, V., Pelekh, A., Dmitrenko, V., and Khidekel, M. The study of conducting polymer interaction with gaseous substances IV. The water content influence on polyaniline crystal structure and conductivity. Synth Met 47, 187, 1992.
49. Alix, A., Lemoine, V., Nechtschein, M., Travers, J.P., and Menardo, C. Water absorption study in polyaniline. Synth Met 29, E457, 1989.
50. Gomes, M.E., Holtorf, H.L., Reis, R.L., and Mikos, A.G. Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng 12, 801, 2006.
51. Guixin, S., and Qing, C. Polym. Fabrication and biocom-patibility of cell scaffolds of poly(L-lactic acid) and poly(L-lactic-co-glycolic acid). Adv Technol 13, 227, 2002.
52. Wang, S., Yaszemski, M.J., Knight, A.M., Gruetzmacher, J.A., Windebank, A.J., and Lu, L. Photo-crosslinked poly(e-caprolactone fumarate) networks for guided peripheral nerve regeneration: material properties and preliminary biological evaluations. Acta Biomaterialia 5, 1531, 2009.
53. Hudson, T.W., Evans, G.R., and Schmidt, C.E. Engineering strategies for peripheral nerve repair. Clin Plast Surg 26, 617, 1999.
54. RodrmHguez, J., GoHmez, N., Perego, G., and Navarro, X. Highly permeable polylactide-caprolactone nerve guides enhance peripheral nerve regeneration through long gaps. Biomaterials 20, 1489, 1999.
55. Borschel, G.H., Kia, K.F., Kuzon, W.M., and Dennis, R.G. Mechanical properties of acellular peripheral nerve. J Surg Res 114, 133, 2003.
56. Plikk, P., Malberg, S., and Albertsson, A.C. Design of re-sorbable porous tubular copolyester scaffolds for use in nerve regeneration. Biomacromolecules 10, 1259, 2009.
57. Laska, J., Zak, K., and Pron, A. Conducting blends of poly-aniline with conventional polymers. Synth Met 84, 117, 1997.
58. Sukitpaneenit, P., Thanpitcha, T., Sirivat, A., Weder, C., and Rujiravanit, R. Electrical conductivity and mechanical properties of polyaniline/natural rubber composite fibers. J Appl Polym Sci 106, 4038, 2007.
59. Wang, Y., Serrano, S., and Santiago-Aviles, J.J. Conductivity measurement of electrospun PAN-based carbon nanofiber. J Mater Sci Lett 21, 1055, 2002.
60. Zhu, Y., Lim, X., Chea Sim, M., Lim, C.T., and Sow, C.H. Versatile transfer of aligned carbon nanotubes with poly-dimethylsiloxane as the intermediate. Nanotechnology 19, 325304, 2008.
61. Nelson, R.M., Hayes, K.W., and Currier, D.B. Clinical Electrotherapy (chapter 1). Stamford, CT: Appleton & Lange, University of Michigan, 1999.
62. Wallace, G.G., Spinks, G.M., Kane-Maguire, L.A.P., and Teasdale, P.R. Conductive Electroactive Polymers: Intelligent Polymer Systems, third edition. Taylor and Francis, London 2008.
63. Laska, J. Conformations of polyaniline in polymer blends. J Mol Struct 701, 13, 2004.
64. Xis, Y., Wiesinger, J.M., and MacDiarmid, A.G. Cam-phorsulfonic acid fully doped polyaniline emeraldine salt: conformations in different solvents studied by an ultraviolet/visible/near-infrared spectroscopic method. Chem Mater 7, 443, 1995.
65. Kulszewicz-Bajer, I., Wielgus, I., Pron, A., and Rannou, P. Protonation of polyaniline in hexafluoro-2-propanol, spec-troscopic investigation. Macromolecules 30, 7091, 1997.
66. Veraa, R., Romerob, H., and Ahumada, E. Synthesis and characterization of polyaniline and poly ortho methoxyani-line behavior against carbon steel corrosion. J Chilean Chem Soc 48, publish online, 2003.
67. Rivers, T.J., Hudson, T.W., and Schmidt, C.E. Synthesis of a novel, biodegradable electrically conducting polymer for biomedical applications. Adv Funct Mater 12, 33, 2002.
68. Kim, Y.J., and Kwon, O.H. Crosslinked gelatin nanofibers and their potential for tissue engineering. Key Eng Mater 342, 169, 2007.
69. Kozlov, P.V., and Burdygina, G.I. The structure and properties of solid gelatin and the principles of their modification. Polymer 24, 651, 1983.
70. Zhang, Y.Z., Venugopal, J., Huang, Z.M., Lim, C.T., and Ramakrishna, S. Crosslinking of the electrospun gelatin nanofibers. Polymer 47, 2911, 2006.
71. McGuigan, A.P., and Sefton, M.V. Modular tissue engineering: fabrication of a gelatin-based construct. J Tissue Eng Regen Med 1, 136, 2007.
72. Sakai, S., Hashimoto, I., and Kawakami, K. Synthesis of an agarose-gelatin conjugate for use as a tissue engineering scaffold. J Biosci Bioeng 103, 22, 2007.
73. Broderick, E.P., O'Halloran, D.M., Rochev, Y.A., Griffin, M., Collighan, R.J., and Pandit, A.S. Enzymatic stabilization of gelatin-based scaffolds. J Biomed Mater Res 72B, 37, 2005.
74. Yung, C.W., Wu, L.Q., Tullman, J.A., Payne, G.F., Bentley, W.E., and Barbari, T.A. Transglutaminase crosslinked gelatin as a tissue engineering scaffold. J Biomed Mater Res A 83A, 1039, 2007.
75. Li, M., Mondrinos, M.J., Chen, X., Gandhi, M.R., Ko, F.K., and Lelkes, P.I. Co-electrospun poly (lactide-co-glycolide), gelatin, and elastin blends for tissue engineering scaffolds. J Biomed Mater Res A 79A, 963, 2006.
76. Coombes, A.G.A., Verderio, E., Shaw, B., Li, X., Griffin, M., and Downes, S. Biocomposites of non-crosslinked natural and synthetic polymers. Biomaterials 23, 2113, 2002.
77. Zhang, Y., Ouyang, H., Lim, C.T., Ramakrishna, S., and Huang, Z.M. Electrospinning of gelatin fibers and gelatin/pcl composite fibrous scaffolds. J Biomed Mater Res 72B, 156, 2005.
78. McCaig, C.D., Rajnicek, A.M., Song, B., and Zhao, M. Controlling cell behavior electrically: current views and future potential. Physiol Rev 85, 943, 2005.
79. Green, R.A., Lovell, N.H., Wallace, G.G., and Poole-Warren, L.A. Conducting polymers for neural interfaces: challenges in developing an effective long-term implant. Biomaterials 29, 3393, 2008.
80. Traynor, A.E., and Tischler, A.S. Phospholipases elevate cyclic AMP levels and promote neurite extension in a clonal nerve cell line. Brain Res 316, 197, 1984.
81. Kitchen, S., ed. Electrotherapy: Evidence-Based Practice. New York: Churchill Livingstone, 2002.
82. Matthews, G. Cellular Physiology of Nerve and Muscle, fourth edition. Blackwell Science Ltd., Malden, MA, 2003