Silk-tropoelastin protein films for nerve guidance

Acta Biomaterialia

Volumn 14, Issue , 2015, Pages 1-10

  White, James D ^a   Wang, Siran ^a   Weiss, Anthony S ^b   Kaplan, David L ^a  

^a Tufts University   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Elastin; Nerve guide; Nerve regeneration; Protein blends; Silk

Indexed keywords

AMINO ACIDS; BIOMATERIALS; CELLS; DISEASE CONTROL; ELECTROPHYSIOLOGY; NEURONS; RECOMBINANT PROTEINS; SILICONES; THIN FILMS;

CELL PROCESS; NERVE GUIDE; NERVE REGENERATION; NEURITE EXTENSION; PERIPHERAL NERVE REGENERATION; PROTEIN BLEND; PROTEIN FILMS; SCHWANN CELLS; SILK; TROPOELASTIN;

CYTOLOGY;

DIMETICONE; FIBRONECTIN; LAMININ; NANOFILM; POLY DEXTRO LYSINE; SILK FIBROIN; SILK TROPOELASTIN PROTEIN FILM; TROPOELASTIN; UNCLASSIFIED DRUG; SILK; TUBULIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIODEGRADABILITY; BRAIN CELL; CELL ACTIVITY; CELL ADHESION; CELL DENSITY; CELL ELONGATION; CELL PROLIFERATION; CELL SURFACE; CELL VIABILITY; CHICK; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MEMBRANE STEADY POTENTIAL; MYELINATION; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPINAL CORD NERVE CELL; SPINAL GANGLION; STRUCTURE ACTIVITY RELATION; SURFACE CHARGE; ANIMAL; BOMBYX; CELL SURVIVAL; CHICK EMBRYO; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOLECULAR WEIGHT; NEURITE; PROCEDURES; STAINING; TISSUE REGENERATION;

ACTION POTENTIALS; ANIMALS; BOMBYX; CELL PROLIFERATION; CELL SURVIVAL; CHICK EMBRYO; GANGLIA, SPINAL; GUIDED TISSUE REGENERATION; HUMANS; MOLECULAR WEIGHT; NERVE REGENERATION; NEURITES; RATS; SCHWANN CELLS; SILK; STAINING AND LABELING; TROPOELASTIN; TUBULIN;

EID: 84921866483     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.11.045     Document Type: Article

References (60)

1. Noble J, Munro CA, Prasad VS, Midha R. Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. J Trauma 1998;45:116-22.
2. Gu X, Ding F, Yang Y, Jie Liu. Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog Neurobiol 2011;93:204-30.
3. Scholz T, Krichevsky A, Sumarto A, Jaffurs D, Wirth GA, Paydar K, et al. Peripheral nerve injuries: an international survey of current treatments and future perspectives. J Reconstr Microsurg 2009;25(6):339-44.
4. Battiston B, Raimondo S, Tos P, Gaidano V, Audisio C, Scevola A, et al. Tissue engineering of peripheral nerves. Int Rev Neurobiol 2009:227-49.
5. Thorsen F, Rosberg HE, Steen Carlsson K, Dahlin LB. Digital nerve injuries: epidemiology, results, costs, and impact on daily life. J Plast Surg Hand Surg 2012;42(3-4):184-90.
6. Isaacs J. Major peripheral nerve injuries. Hand Clin 2013;3:371-82.
7. Cunha C, Panseri S, Antonini S. Emerging nanotechnology approaches in tissue engineering for peripheral nerve regeneration. Nanomedicine: NBM 2011;7:50-9.
8. Nectow AR, Marra KG, Kaplan DL. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B Rev 2012;1:40-50.
9. Taras JS, Jacoby SM, Lincoski CJ. Reconstruction of digital nerves with collagen conduits. J Hand Surg Am 2011;36(9):1441-6.
10. Wang H, Zhao Q, Zhao W, Liu Q, Gu X, Yang Y. Repairing rat sciatic nerve injury by a nerve-growth-factor-loaded chitosan-based nerve conduit. Biotechnol Appl Biochem 2012;59(5):388-94.
11. Yang Y, Ding F, Wu J, Hu W, Liu W, Liu J, et al. Development and evaluation of silk fibroin-based nerve grafts for peripheral nerve regeneration. Biomaterials 2007;28:5526-35.
12. Reid AJ, de Luca AC, Faroni A, Downes S, Sun M, Terenghi G, et al. Long term peripheral nerve regeneration using a novel PCL nerve conduit. Neurosci Lett 2013;544:125-30.
13. Suwantong O, Waheetorncheepsawat S, Sanchavanakit P, Pavasant P, Cheepsunthorn T, Bunaprasert T, et al. In vitro biocompatibility of electrospun poly(3-hydroxybutyrate) and poly(3-hydroxybutyrate-co-hydroxyvalerate) fiber mats. Int J Biol Macromol 2007;40:217-23.
14. Lu MC, Huang YT, Lin JH, Yao CH, Lou CW, Tsai CC, et al. Evaluation of a multilayer microbraided polylactic acid fiber-reinforced conduit for peripheral nerve regeneration. J Mater Sci Mater Med 2009;20(5):1175-80.
15. de Boer R, Knight AM, Borntraeger A, Herbert-Blouin MN, Spinner RJ, Malessy MJ, et al. Rat sciatic nerve repair with a poly-lactic-co-glycolic acid scaffold and nerve growth factor releasing microspheres. Microsurgery 2011;31(4):293-302.
16. Chiono V, Sartori S, Rechichi A, Tonda-Turo C, Vozzi G, Vozzi F, et al. Poly(ester urethane) guides for peripheral nerve regeneration. Macromol Biosci 2011;11(2):245-56.
17. Bertleff MJ, Meek MF, Nicolai JP. A prospective clinical evaluation of biodegradable neurolac nerve guides for sensory nerve repair in the hand. J Hand Surg Am 2005;30(3):513-8.
18. Agnew SP, Dumanian GA. Technical use of synthetic conduits for nerve repair. J Hand Surg 2010;35(5):838-41.
19. Archibald SJ, Shefner J, Krarup C, Madison RD. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. J Neurosci 1995;15(5):4109-23.
20. Clements IP, Kim Y, English AW, Lu X, Chung A, Bellamkonda RV. Thin-film enhanced nerve guidance channels for peripheral nerve repair. Biomaterials 2009;30(23-24):3834-46.
21. Hu X, Wang X, Rnjak J, Weiss AS, Kaplan DL. Biomaterials derived from silk-tropoelastin protein systems. Biomaterials 2010;31:8121-31.
22. Hu X, Tang-Schomer MD, Huang W, Xia X, Weiss AS, Kaplan DL. Charge-tunable autoclaved silk-tropoelastin protein alloys that control neuron cell responses. Adv Funct Mater 2013;23(31):3875-84.
23. Lin YC, Ramadan M, Hronik-Tupaj M, Kaplan DL, Philips BJ, Sivak W, et al. Spatially controlled delivery of neurotrohic factors in silk fibroin-based nerve conduits for peripheral nerve repair. Ann Plast Surg 2011;67(2):147-55.
24. Mithieux SM, Wise SG, Weiss AS. Tropoelastin - A multifaceted naturally smart material. Adv Drug Deliv Rev 2013;65:421-8.
25. Bax DV, Rodgers UR, Bilek MM, Weis AS. Cell adhesion to tropoelastin is mediated via the C-terminal GRKRK motif and integrin alphaVbeta3. J Biol Chem 2009;284(42):28616-23.
26. Broekelmann TJ, Kozel BA, Ishibaschi H, Werneck CC, Keeley FW, Zhang L, et al. Tropoelastin interacts with cell-surface glycosaminoglycans via its COOH-terminal domain. J Biol Chem 2005;280(49):40939-47.
27. Akhtar K, Broekelmann TJ, Song H, Turk J, Brett TJ, Mecham RP, et al. Oxidative modifications of the C-terminal domain of tropoelastin prevent cell binding. J Biol Chem 2011;286(15):13574-82.
28. Bax DV, Liu SJ, McKenzie DR, Bilek MM, Weiss AS. Tropoelastin switch and modulated endothelial cell binding to PTFE. BioNanoScience 2011;1:123-7.
29. Ho C, O'Leary ME. Single-cell analysis of sodium channel expression in dorsal root ganglion neurons. Mol Cell Neurosci 2011;46(1):159-66.
30. Wray LS, Hu X, Gallego J, Georgakoudi I, Omenetto FG, Schmidt D, et al. Effect of processing on silk-based biomaterials: reproducibility and biocompatibility. J Biomed Mater Res B: Appl Biomater 2011;99(1):89-101.
31. Wise SG, Weiss AS. Tropoelastin. Int J Biochem Cell Biol 2009;41:494-7.
32. Martin SL, Vrhovski B, Weiss AS. Total synthesis and expression in Escherichia coli of a gene encoding human tropoelastin. Gene 1995;154:159-66.
33. Jin H-J, Park J, Karageorgiou V, Kim U-J, Valluzzi R, Cebe P, et al. Water-stable silk films with reduced β-sheet content. Adv Funct Mater 2005;15(8):1241-7.
34. Dichter MA, Fischbach GD. The action potential of chick dorsal root ganglion neurones maintained in cell culture. J Physiol 1977;267(2):281-98.
35. Meijering E, Jacob M, Saria JCF, Steiner P, Hirling H, Unser M. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry Part A 2004;58(2):167-76.
36. Hamill OP, Marty A, Neher E, Sackmann B, Sigworth FJ. Improved patch-clamp techniques for high resolution recording from cells and cell free membrane patches. Pflugers Archiv 1981;391(2):85-100.
37. Hu X, Park S-H, Gil ES, Xia X-X, Weiss AS, Kaplan DL. The influence of elasticity and surface roughness on myogenic and osteogenic differentiation of cells on silk-elastin biomaterials. Biomaterials 2011;32:8979-89.
38. Borschel GH, Kia KF, Kuzon WM, Dennis RG. Mechanical properties of acellular peripheral nerve. J Surg Res 2003;114:133-9.
39. Swindle-Reilly KE, Papke JB, Kutosky HP, Throm A, Hammer JA, Harkins AB, et al. The impact of laminin on 3D neurite extension in collagen gels. J Neural Eng 2012;9(4):046007.
40. Willits RK, Skornia SL. Effect of collagen gel stiffness on neurite extension. J Biomater Sci Polym Edn 2004;15(12):1521-31.
41. Blewitt MJ, Willits RK. The effect of soluble peptide sequences on neurite extension on 2D collagen substrates and within 3D collagen gels. Ann Biomed Eng 2007;35(12):2159-67.
42. Balgude AP, Yu X, Szymanski A, Bellamkonda RV. Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 2001;22(10):1077-84.
43. Hopkins AM, Laporte L, Tortelli F, Spedden E, Staii C, Atherton TJ, et al. Silk hydrogels as soft substrates for neural tissue engineering. Adv Funct Mater 2013;23(41):5140-9.
44. Spedden E, White JD, Naumova EN, Kaplan DL, Staii C. Elasticity maps of living neurons measured by combined fluorescence and atomic force microscopy. Biophys J 2012;103(5):868-77.
45. Loverde JR, Oxoka VC, Aquino R, Lin L, Pfister BJ. Live imaging of axon stretch growth in embryonic and adult neurons. J Neurotrauma 2011;28(11):2389-403.
46. Dadsetan M, Knight AM, Lu L, Windebank AJ, Yaszemski MJ. Stimulation of neurite outgrowth using positively charged hydrogels. Biomaterials 2009;30(23-24):3874-81.
47. Zhou Z, Yu P, Geller HM, Ober CK. The role of hydrogels with tethered acetylcholine functionality on the adhesion and viability of hippocampal neurons and glial cells. Biomaterials 2012;33(8):2473-81.
48. Lee DY, Choi BH, Park JH, Zhu SJ, Kim BY, Huh JY, et al. Nerve regeneration with the use of a poly(L-lactide-co-glycolic acid)-coated collagen tube filled with collagen gel. J Craniomaxillofac Surg 2006;34(1):50-6.
49. Rogers SL, Letourneau PC, Palm SL, McCarthy J, Furcht LT. Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin. Dev Biol 1983;98(1):212-20.
50. Zuidema JM, Pap MM, Jaroch DB, Morrison FA, Gilbert RJ. Fabrication and charaterization of tunable poysaccharide hydrogel blends for neural repair. Acta Biomater 2011;7:1634-43.
51. Cheng C-M, LeDuc PR, Lin Y-W. Localized bimodal response of neurite extensions and structural proteins in dorsal-root ganglion neurons with controlled polydimethylsiloxane substrate stiffness. J Biomech 2011;44:856-62.
52. Bunge RP. The role of the Schwann cell in trophic support and regeneration. J Neurol 1994;242:S19-21.
53. Koppes AN, Nordberg AL, Paolilo GM, Goodsell NM, Darwish HA, Zhang L, et al. Electrical stimulation of Schwann cells promotes sustained increases in neurite outgrowth. Tissue Eng Part A 2014;20(3-4):494-506.
54. Nave KA. Myelination and support of axonal integrity by glia. Nature 2010;468:244-52.
55. Gu Y, Ji Y, Zhao Y, Liu Y, Ding F, Gu X, et al. The influence of substrate stiffness on the behavior and functions of Schwann cells in culture. Biomaterials 2012;33:6672-81.
56. Thaxton C, Bott M, Walker B, Sparrow A, Lambert S, Fernandez-Valle C. Schwannomin/merlin promotes Schwann cell elongation and influences myelin segment length. Mol Cell Neurosci 2011;47(1):1-9.
57. Thompsen DM, Buettner HM. Neurite outgrowth is directed by schwann cell alignment in the absence of other guidance cues. Ann Biomed Eng 2006;34(1):161-8.
58. Hronik-Tupaj M, Raja WK, Tang-Schomer M, Omenetto FG, Kaplan DL. Neural responses to electrical stimulation on patterned silk films. J Biomed Mater Res A 2013;101(9):2559-72.
59. Yang J. Zorumski CF Elevated potassium shortens action potential duration by altering outward currents in chick dorsal root ganglia neurons. J Neurobiol 1990;21(4):661-71.
60. Shakhbazau A, Kawasoe J, Hoyng SA, Kumar R, van Minnen J, Verhaagen J, et al. Early regenerative effects of NGF-transduced Schwann cells in peripheral nerve repair. Mol Cell Neurosci 2012;50(1):103-12.