Electrical and neurotrophin enhancement of neurite outgrowth within a 3D collagen scaffold

Annals of Biomedical Engineering

Volumn 42, Issue 6, 2014, Pages 1282-1291

  Adams, Robert D ^a   Rendell, Sara R ^a   Counts, Lauren R ^a   Papke, Jason B ^a   Willits, Rebecca K ^b   Harkins, Amy B ^a,c  

^a SAINT LOUIS UNIVERSITY   (United States)

^b University of Akron   (United States)

^c Saint Louis University   (United States)

Author keywords

Brain derived neurotrophic factor; Collagen scaffold; Dorsal root ganglion; Electrical stimulation; Nerve growth factor; Neurite growth

Indexed keywords

COLLAGEN; ENZYME INHIBITION; SCAFFOLDS; THREE DIMENSIONAL;

BRAIN-DERIVED NEUROTROPHIC FACTORS; COLLAGEN SCAFFOLDS; DORSAL ROOT GANGLIA; ELECTRICAL STIMULATIONS; NERVE GROWTH FACTOR; NEURITE GROWTH;

NEURONS;

BRAIN DERIVED NEUROTROPHIC FACTOR; COLLAGEN; NERVE GROWTH FACTOR; NEUROTROPHIN;

ANIMAL CELL; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; ELECTROSTIMULATION; EMBRYO; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; SPINAL GANGLION; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; METABOLISM; NEURITE; TISSUE SCAFFOLD;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CHICK EMBRYO; COLLAGEN; ELECTRIC STIMULATION; GANGLIA, SPINAL; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; NEURITES; TISSUE SCAFFOLDS;

EID: 84900014713     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-014-1001-0     Document Type: Article

References (43)

1. Al-Majed, A. A., T. M. Brushart, and T. Gordon. Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur. J. Neurosci. 12:4381-4390, 2000.
2. Al-Majed, A. A., C. M. Neumann, T. M. Brushart, and T. Gordon. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J. Neurosci. 20:2602-2608, 2000.
3. Bamji, S. X., M. Majdan, C. D. Pozniak, D. J. Belliveau, R. Aloyz, J. Kohn, C. G. Causing, and F. D. Miller. The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J. Cell Biol. 140:911-923, 1998.
4. Bell, J. H., and J. W. Haycock. Next generation nerve guides: materials, fabrication, growth factors, and cell delivery. Tissue Eng. Part B Rev. 18:116-128, 2012.
5. Blewitt, M. J., and R. K. Willits. The effect of soluble peptide sequences on neurite extension on 2D collagen substrates and within 3D collagen gels. Ann. Biomed. Eng. 35:2159-2167, 2007.
6. Brown, B. R., M. E. Hughes, and C. Russo. Thermoelectricity in natural and synthetic hydrogels. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 70:031917, 2004.
7. Chang, Y. J., C. M. Hsu, C. H. Lin, M. S. Lu, and L. Chen. Electrical stimulation promotes nerve growth factorinduced neurite outgrowth and signaling. Biochim. Biophys. Acta 4130-6:2013, 1830.
8. Chao, M. V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4:299-309, 2003.
9. Cheng, X., U. A. Gurkan, C. J. Dehen, M. P. Tate, H. W. Hillhouse, G. J. Simpson, and O. Akkus. An electrochemical fabrication process for the assembly of anisotropically oriented collagen bundles. Biomaterials 29:3278-3288, 2008.
10. Corredor, R. G., and J. L. Goldberg. Electrical activity enhances neuronal survival and regeneration. J. Neural Eng. 6:055001, 2009.
11. Davies, A. M., H. Thoenen, and Y. A. Barde. The response of chick sensory neurons to brain-derived neurotrophic factor. J. Neurosci. 6:1897-1904, 1986.
12. Dubey, N., P. C. Letourneau, and R. T. Tranquillo. Guided neurite elongation and Schwann cell invasion into magnetically aligned collagen in simulated peripheral nerve regeneration. Exp. Neurol. 158:338-350, 1999.
13. Elsdale, T., and J. Bard. Collagen substrata for studies on cell behavior. J. Cell Biol. 54:626-637, 1972.
14. English, A. W., W. Meador, and D. I. Carrasco. Neurotrophin- 4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur. J. Neurosci. 21:2624-2634, 2005.
15. Geller, H. M., and J. W. Fawcett. Building a bridge: engineering spinal cord repair. Exp. Neurol. 174:125-136, 2002.
16. Geremia, N. M., T. Gordon, T. M. Brushart, A. A. Al-Majed, and V. M. Verge. Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Exp. Neurol. 205:347-359, 2007.
17. Gordon, T., O. Sulaiman, and J. G. Boyd. Experimental strategies to promote functional recovery after peripheral nerve injuries. J. Peripher. Nerv. Syst. 8:236-250, 2003.
18. Greenebaum, B., C. H. Sutton, M. S. Vadula, J. H. Battocletti, T. Swiontek, J. DeKeyser, and B. F. Sisken. Effects of pulsed magnetic fields on neurite outgrowth from chick embryo dorsal root ganglia. Bioelectromagnetics 17:293-302, 1996.
19. Gross, D., L. M. Loew, and W. W. Webb. Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys. J. 50:339-348, 1986.
20. Hart, A., G. Terenghi, and M. Wiberg. Tissue engineering for peripheral nerve regeneration. In: Tissue Engineering, edited by N. Pallua, and C. V. Suscheck. Berlin: Springer, 2011, pp. 245-262.
21. Hory-Lee, F., M. Russell, R. M. Lindsay, and E. Frank. Neurotrophin 3 supports the survival of developing muscle sensory neurons in culture. Proc. Natl Acad. Sci. U.S.A. 90:2613-2617, 1993.
22. Koppes, A. N., A. M. Seggio, and D. M. Thompson. Neurite outgrowth is significantly increased by the simultaneous presentation of Schwann cells and moderate exogenous electric fields. J. Neural Eng. 8:046023, 2011.
23. Kuntz, R. M., and W. M. Saltzman. Neutrophil motility in extracellular matrix gels: mesh size and adhesion affect speed of migration. Biophys. J. 72:1472-1480, 1997.
24. Longair, M. H., D. A. Baker, and J. D. Armstrong. Simple Neurite Tracer: open source software for reconstruction, visualization and analysis of neuronal processes. Bioinformatics 27:2453-2454, 2011.
25. Macias, M. Y., J. H. Battocletti, C. H. Sutton, F. A. Pintar, and D. J. Maiman. Directed and enhanced neurite growth with pulsed magnetic field stimulation. Bioelectromagnetics 21:272-286, 2000.
26. Miller, C., S. Jeftinija, and S. Mallapragada. Micropatterned Schwann cell-seeded biodegradable polymer substrates significantly enhance neurite alignment and outgrowth. Tissue Eng. 7:705-715, 2001.
27. Nguyen, H. T., C. Wei, J. K. Chow, L. Nguy, H. K. Nguyen, and C. E. Schmidt. Electric field stimulation through a substrate influences Schwann cell and extracellular matrix structure. J. Neural Eng. 10:046011, 2013.
28. Nguyen, H. T., C. Wei, J. K. Chow, A. Nguyen, J. Coursen, S. Sapp, S. Luebben, E. Chang, R. Ross, and C. E. Schmidt. Electric field stimulation through a biodegradable polypyrrole-co-polycaprolactone substrate enhances neural cell growth. J. Biomed. Mater. Res. A. DOI:10.1002/jbm.a.34925.
29. Nuccitelli, R. Physiological electric fields can influence cell motility, growth, and polarity. In: Advances in Molecular and Cell Biology, edited by R. M. Kenneth. Amsterdam: Elsevier, 1988, pp. 213-233.
30. Parkhurst, M. R., and W. M. Saltzman. Quantification of human neutrophil motility in three-dimensional collagen gels. Effect of collagen concentration. Biophys. J. 61:306-315, 1992.
31. Sauer, H., G. Rahimi, J. Hescheler, and M. Wartenberg. Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J. Cell. Biochem. 75:710-723, 1999.
32. Saygili, E., P. Schauerte, F. Kuppers, L. Heck, J. Weis, C. Weber, R. H. Schwinger, R. Hoffmann, J. W. Schroder, N. Marx, and O. R. Rana. Electrical stimulation of sympathetic neurons induces autocrine/paracrine effects of NGF mediated by TrkA. J. Mol. Cell. Cardiol. 49:79-87, 2010.
33. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona. Fiji: an opensource platform for biological-image analysis. Nat. Methods 9:676-682, 2012.
34. Skaper, S. D. The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol. Disord. Drug Targets 7:46-62, 2008.
35. Skaper, S. D. The neurotrophin family of neurotrophic factors: an overview. Methods Mol. Biol. 846:1-12, 2012.
36. Skaper, S. D., and S. Varon. Maintenance by nerve growth factor of the intracellular sodium environment in spinal sensory and sympathetic ganglionic cells. Brain Res. 197:379-389, 1980.
37. Swindle-Reilly, K. E., J. B. Papke, H. P. Kutosky, A. Throm, J. A. Hammer, A. B. Harkins, and R. K. Willits. The impact of laminin on 3D neurite extension in collagen gels. J. Neural Eng. 9:046007, 2012.
38. Tep, C., T. H. Lim, P. O. Ko, S. Getahun, J. C. Ryu, V. M. Goettl, S. M. Massa, M. Basso, F. M. Longo, and S. O. Yoon. Oral administration of a small molecule targeted to block proNGF binding to p75 promotes myelin sparing and functional recovery after spinal cord injury. J. Neurosci. 33:397-410, 2013.
39. Torbet, J., and M. C. Ronziere. Magnetic alignment of collagen during self-assembly. Biochem. J. 219:1057-1059, 1984.
40. Udina, E., M. Furey, S. Busch, J. Silver, T. Gordon, and K. Fouad. Electrical stimulation of intact peripheral sensory axons in rats promotes outgrowth of their central projections. Exp. Neurol. 210:238-247, 2008.
41. Willits, R. K., and S. L. Skornia. Effect of collagen gel stiffness on neurite extension. J. Biomater. Sci. Polym. Ed. 15:1521-1531, 2004.
42. Wood, M., and R. K. Willits. Short-duration, DC electrical stimulation increases chick embryo DRG neurite outgrowth. Bioelectromagnetics 27:328-331, 2006.
43. Wood, M. D., and R. K. Willits. Applied electric field enhances DRG neurite growth: influence of stimulation media, surface coating and growth supplements. J. Neural Eng. 6:046003, 2009.