Material properties and electrical stimulation regimens of polycaprolactone fumarate-polypyrrole scaffolds as potential conductive nerve conduits

Acta Biomaterialia

Volumn 7, Issue 3, 2011, Pages 944-953

  Moroder, Philipp ^b   Runge, M Brett ^a   Wang, Huan ^a   Ruesink, Terry ^a   Lu, Lichun ^a   Spinner, Robert J ^a   Windebank, Anthony J ^a   Yaszemski, Michael J ^a  

^a MAYO CLINIC   (United States)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Electrical stimulation; Nerve; PC12 cells; Polycaprolactone fumarate; Polypyrrole

Indexed keywords

BIOMECHANICS; CELLS; CYTOLOGY; FLUORESCENCE MICROSCOPY; NEURONS; POLYCAPROLACTONE; SCAFFOLDS (BIOLOGY);

CELLULAR MORPHOLOGY; ELECTRICAL STIMULATIONS; FREQUENCY CURRENT; MECHANICAL AND ELECTRICAL PROPERTIES; NERVE; NERVE CONDUITS; NEURITES; PC12 CELLS; PHYSIOLOGICAL CONDITION; POLYCAPROLACTONE FUMARATE;

POLYPYRROLES;

BIOMATERIAL; FUMARIC ACID DERIVATIVE; POLYCAPROLACTONE; POLYCAPROLACTONE FUMARATE; POLYPYRROLE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL STRUCTURE; CONTROLLED STUDY; ELECTROSTIMULATION; FLUORESCENCE MICROSCOPY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SURFACE PROPERTY;

EID: 79251645848     PISSN: 17427061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actbio.2010.10.013     Document Type: Article

References (62)

1. J. Isaacs Treatment of acute peripheral nerve injuries: current concepts J Hand Surg Am 35 2010 491 497
2. A.A. Al-Majed, C.M. Neumann, T.M. Brushart, and T. Gordon Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration J Neurosci 20 2000 2602 2608
3. G.R. Evans Challenges to nerve regeneration Semin Surg Oncol 19 2000 312 318
4. D. Yucel, G.T. Kose, and V. Hasirci Polyester based nerve guidance conduit design Biomaterials 31 2010 1596 1603
5. Chiono V, Vozzi G, Vozzi F, Salvadori C, Dini F, Carlucci F, et al. Melt-extruded guides for peripheral nerve regeneration. Part I. Poly(epsilon-caprolactone). Biomed Microdevices 2009;May:Epub.
6. S.W. Kemp, S. Syed, W. Walsh, D.W. Zochodne, and R. Midha Collagen nerve conduits promote enhanced axonal regeneration, Schwann cell association, and neovascularization compared to silicone conduits Tissue Eng Part A 15 2009 1975 1988
7. G.C. de Ruiter, I.A. Onyeneho, E.T. Liang, M.J. Moore, A.M. Knight, and M.J.A. Malessy Methods for in vitro characterization of multichannel nerve tubes J Biomed Mater Res A 84 2007 643 651
8. G.C. de Ruiter, R.J. Spinner, M.J.A. Malessy, M.J. Moore, E.J. Sorenson, and B.L. Currier Accuracy of motor axon regeneration across autograft, single-lumen, and multichannel poly(lactic-co-glycolic acid) nerve tubes Neurosurgery 63 2008 144 155
9. G.C.W. de Ruiter, M.J.A. Malessy, A.O. Alaid, R.J. Spinner, J.K. Engelstad, and E.J. Sorenson Misdirection of regenerating motor axons after nerve injury and repair in the rat sciatic nerve model Exp Neurol 211 2008 339 350
10. M.J. Moore, J.A. Friedman, E.B. Lewellyn, S.M. Mantilla, A.J. Krych, and S. Ameenuddin Multiple-channel scaffolds to promote spinal cord axon regeneration Biomaterials 27 2006 419 429
11. S. Wang, M.J. Yaszemski, A.M. Knight, J.A. Gruetzmacher, A.J. Windebank, and L. Lu Photo-crosslinked poly(-caprolactone fumarate) networks for guided peripheral nerve regeneration: material properties and preliminary biological evaluations Acta Biomater 5 2009 1531 1542
12. S. Wang, L. Lu, J.A. Gruetzmacher, B.L. Currier, and M.J. Yaszemski Synthesis and characterizations of biodegradable and crosslinkable poly(-caprolactone fumarate), poly(ethylene glycol fumarate), and their amphiphilic copolymer Biomaterials 27 2006 832 841
13. X.K. Li, S.X. Cai, B. Liu, Z.L. Xu, X.Z. Dai, and K.W. Ma Characteristics of PLGA-gelatin complex as potential artificial nerve scaffold Colloids Surf B Biointerfaces 57 2007 198 203
14. M. Sun, P.J. Kingham, A.J. Reid, S.J. Armstrong, G. Terenghi, and S. Downes In vitro and in vivo testing of novel ultrathin PCL and PCL/PLA blend films as peripheral nerve conduit J Biomed Mater Res A 93 2010 1470 1481
15. S. Madduri, K. Feldman, T. Tervoort, M. Papaloizos, and B. Gander Collagen nerve conduits releasing the neurotrophic factors GDNF and NGF J Control Release 143 2010 168 174
16. S. Madduri, M. Papaloizos, and B. Gander Trophically and topographically functionalized silk fibroin nerve conduits for guided peripheral nerve regeneration Biomaterials 31 2010 2323 2334
17. G. Piquilloud, T. Christen, L.A. Pfister, B. Gander, and M.Y. Papaloizos Variations in glial cell line-derived neurotrophic factor release from biodegradable nerve conduits modify the rate of functional motor recovery after rat primary nerve repairs Eur J Neurosci 26 2007 1109 1117
18. T.M. Brushart, P.N. Hoffman, R.M. Royall, B.B. Murinson, C. Witzel, and T. Gordon Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron J Neurosci 22 2002 6631 6638
19. T. Gordon, E. Udina, V.M. Verge, and E.I. de Chaves Brief electrical stimulation accelerates axon regeneration in the peripheral nervous system and promotes sensory axon regeneration in the central nervous system Motor Control 13 2009 412 441
20. N.M. Geremia, T. Gordon, T.M. Brushart, A.A. Al-Majed, and V.M.K. Verge Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression Exp Neurol 205 2007 347 359
21. D.D. Ateh, H.A. Navsaria, and P. Vadgama Polypyrrole-based conducting polymers and interactions with biological tissues J R Soc Interface 3 2006 741 752
22. S.J. Chen, D.Y. Wand, C.W. Yuan, X.D. Wany, P.Y. Zhang, and X.S. Gu Template synthesis of the polypyrrole tube and its bridging in vivo sciatic nerve regeneration J Mater Sci Lett 19 2000 2157 2159
23. N. Gomez, J.Y. Lee, J.D. Nickels, and C.E. Schmidt Micropatterned polypyrrole: a combination of electrical and topographical characteristics for the stimulation of cells Adv Funct Mater 17 2007 1645 1653
24. N. Gomez, and C.E. Schmidt Nerve growth factor-immobilized polypyrrole: bioactive electrically conducting polymer for enhanced neurite extension J Biomed Mater Res A 81 2007 135 149
25. J.-W. Lee, F. Serna, J. Nickels, and C.E. Schmidt Carboxylic acid-functionalized conductive polypyrrole as a bioactive platform for cell adhesion Biomacromolecules 7 2006 1692 1695
26. J.-W. Lee, F. Serna, and C.E. Schmidt Carboxy-endcapped conductive polypyrrole: biomimetic conducting polymer for cell scaffolds and electrodes Langmuir 22 2006 9816 9819
27. C. Mao, A. Zhu, Q. Wu, X. Chen, J. Kim, and J. Shen New biocompatible polypyrrole-based films with good blood compatibility and high electrical conductivity Colloids Surf B Biointerfaces 67 2008 41 45
28. K.G. Neoh, K.K.S. Lau, V.V.T. Wang, E.T. Kang, and K.L. Tan Structure and degradation behavior of polypyrrole doped with sulfonate anions and different sizes subject to undoping-redoping cycles Chem Mater 8 1996 167 172
29. R. Olayo, C. Rios, H. Salgado-Ceballos, G.J. Cruz, J. Morales, and M.G. Olayo Tissue spinal cord response in rats after implants of polypyrrole and polyethylene glycol obtained by plasma J Mater Sci Mater Med 19 2008 817 826
30. G. Shi, Z. Zhang, and M. Rouabhia The regulation of cell functions electrically using biodegradable polypyrrole-polylactide conductors Biomaterials 29 2008 3792 3798
31. G. Shustak, M. Gadzinowski, S. Slomkowski, A.J. Domb, and D. Mandler A novel electrochemically synthesized biodegradable thin film of polypyrrole-polyethyleneglycol-polylactic acid nanoparticles New J Chem 31 2007 163 168
32. X. Wang, X. Gu, C. Yuan, S. Chen, P. Zhang, and T. Zhang Evaluation of biocompatibility of polypyrrole in vitro and in vivo J Biomed Mater Res A 68 2003 411 422
33. J.Y. Lee, C.A. Bashur, A.S. Goldstein, and C.E. Schmidt Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications Biomaterials 30 2009 4325 4335
34. G. Shi, M. Rouabhia, Z. Wang, L.H. Dao, and Z. Zhang A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide Biomaterial 25 2004 2477 2488
35. A. Abarrategi, M.C. Gutierrez, C. Moreno-Vicente, M.J. Hortiguela, V. Ramos, and J.L. Lopez-Lacomba Multiwall carbon nanotube scaffolds for tissue engineering purposes Biomaterials 29 2008 94 102
36. S.L. Edwards, J.S. Church, J.A. Werkmeister, and J.A. Ramshaw Tubular micro-scale multiwalled carbon nanotube-based scaffolds for tissue engineering Biomaterials 30 2009 1725 1731
37. J.S. Park, K. Park, H.T. Moon, D.G. Woo, H.N. Yang, and K.-H. Park Electrical pulsed stimulation of surfaces homogeneously coated with gold nanoparticles to induce neurite outgrowth of PC12 cells Langmuir 25 2009 451 457
38. N.K. Guimard, N. Gomez, and C.E. Schmidt Conducting polymers in biomedical engineering Prog Polym Sci 32 2007 876 921
39. M.B. Runge, M. Dadsetan, J. Baltrusaitis, A.M. Knight, T. Ruesink, and E.A. Lazcano The development of electrically conductive polycaprolactone fumarate-polypyrrole composite materials for nerve regeneration Biomaterials 31 2010 5916 5926
40. H. Durgam, S. Sapp, C. Deister, Z. Khaing, E. Chang, and S. Luebben Novel Degradable co-polymers of polypyrrole support cell proliferation and enhance neurite out-growth with electrical stimulation J Biomater Sci Polym Ed 21 2010 1265 1282
41. J. Huang, X. Hu, L. Lu, Z. Ye, Q. Zhang, and Z. Luo Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers J Biomed Mater Res Part A 93 2010 164 174
42. L. Yao, S. Wang, W. Cui, R. Sherlock, C. O'Connell, and G. Damodaran Effect of functionalized micropatterned PLGA on guided neurite growth Acta Biomater 5 2009 580 588
43. S. Wang, D.H. Kempen, N.K. Simha, J.L. Lewis, A.J. Windebank, and M.J. Yaszemski Photo-cross-linked hybrid polymer networks consisting of poly(propylene fumarate) and poly(caprolactone fumarate): controlled physical properties and regulated bone and nerve cell responses Biomacromolecules 9 2008 1229 1241
44. J.B. Leach, X.Q. Brown, J.G. Jacot, P.A. Dimilla, and J.Y. Wong Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity J Neural Eng 4 2007 26 34
45. S. Wang, M.J. Yaszemski, J.A. Gruetzmacher, and L. Lu Photo-crosslinked poly(-caprolactone fumarate) networks: roles of crystallinity and crosslinking density in determining mechanical properties Polymer 49 2008 5692 5699
46. G.C. de Ruiter, M.J. Malessy, M.J. Yaszemski, A.J. Windebank, and R.J. Spinner Designing ideal conduits for peripheral nerve repair Neurosurg Focus 26 2009 E5
47. W.F. den Dunnen, B. van der Lei, P.H. Robinson, A. Holwerda, A.J. Pennings, and J.M. Schakenraad Biological performance of a degradable poly(lactic acid-epsilon-caprolactone) nerve guide: influence of tube dimensions J Biomed Mater Res 29 1995 757 766
48. Z. Zhang, M. Rouabhia, Z. Wang, C. Roberge, G. Shi, and P. Roche Electrically conductive biodegradable polymer composite for nerve regeneration: electricity-stimulated neurite outgrowth and axon regeneration Artif Organs 31 2007 13 22
49. T. Gordon, T.M. Brushart, and K.M. Chan Augmenting nerve regeneration with electrical stimulation Neurol Res 30 2008 1012 1022
50. T. Gordon, K.M. Chan, O.A. Sulaiman, E. Udina, N. Amirjani, and T.M. Brushart Accelerating axon growth to overcome limitations in functional recovery after peripheral nerve injury Neurosurgery 65 2009 A132 A144
51. P. Ahlborn, M. Schachner, and A. Irintchev One hour electrical stimulation accelerates functional recovery after femoral nerve repair Exp Neurol 208 2007 137 144
52. C.E. Schmidt, V.R. Shastri, J.P. Vacanti, and R. Langer Stimulation of neurite outgrowth using an electrically conductive polymer Proc Natl Acad Sci USA 94 1997 8948 8953
53. A. Kotwal, and C.E. Schmidt Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials Biomaterials 22 2001 1055 1064
54. N.B. Patel, and M.M. Poo Perturbation of the direction of neurite growth by pulsed and focal electric fields J Neurosci 4 1984 2939 2947
55. N. Patel, and M.M. Poo Orientation of neurite growth by extracellular electric fields J Neurosci 2 1982 483 496
56. J. Li, H. McNally, and R. Shi Enhanced neurite alignment on micro-patterned poly-l-lactic acid films J Biomed Mater Res A 87 2008 392 404
57. M.J. Mahoney, R.R. Chen, J. Tan, and W.M. Saltzman The influence of microchannels on neurite growth and architecture Biomaterials 26 2005 771 778
58. J.M. Corey, D.Y. Lin, K.B. Mycek, Q. Chen, S. Samuel, and E.L. Feldman Aligned electrospun nanofibers specify the direction of dorsal root ganglia neurite growth J Biomed Mater Res A 83 2007 636 645
59. E. Schnell, K. Klinkhammer, S. Balzer, G. Brook, D. Klee, and P. Dalton Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend Biomaterials 28 2007 3012 3025
60. L. Erskine, and C.D. McCaig Growth cone neurotransmitter receptor activation modulates electric field-guided nerve growth Dev Biol 171 1995 330 339
61. R.W. Davenport, and C.D. McCaig Hippocampal growth cone responses to focally applied electric fields J Neurobiol 24 1993 89 100
62. R.J. Cork, M.E. McGinnis, J. Tsai, and K.R. Robinson The growth of PC12 neurites is biased towards the anode of an applied electrical field J Neurobiol 25 1994 1509 1516