Neuronal electrophysiological function and control of neurite outgrowth on electrospun polymer nanofibers are cell type dependent

Tissue Engineering - Part A

Volumn 20, Issue 5-6, 2014, Pages 1089-1095

  Bourke, Justin L ^a   Coleman, Harold A ^a   Pham, Vi ^a   Forsythe, John S ^a   Parkington, Helena C ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; ELECTROPHYSIOLOGY; NANOFIBERS; NEURAL NETWORKS; POLYCAPROLACTONE; SCAFFOLDS (BIOLOGY); SUBSTRATES;

BIOMATERIAL SCAFFOLDS; CENTRAL NERVOUS SYSTEMS; DORSAL ROOT GANGLIA (DRG); ELECTROSPUN POLYMER NANOFIBERS; NANOFIBROUS SCAFFOLDS; PERIPHERAL NERVOUS SYSTEM; SUBSTRATE COMPOSITION; TISSUE ENGINEERING APPLICATIONS;

NEURONS;

ETHYLENEDIAMINE; LAMININ; MOLECULAR SCAFFOLD; NANOFIBER; POLYCAPROLACTONE; POLYMER; POLYSTYRENE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL MATURATION; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSPINNING; EMBRYO; FEMALE; HIPPOCAMPUS; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SPINAL CORD NERVE CELL; SPINAL GANGLION; SYNAPTIC POTENTIAL; TISSUE ENGINEERING; WHOLE CELL PATCH CLAMP;

ANIMALS; ANTIBODIES; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; GANGLIA, SPINAL; HIPPOCAMPUS; MICE; NANOFIBERS; NEURITES; PATCH-CLAMP TECHNIQUES; POLYESTERS; RATS; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84896808022     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0295     Document Type: Article

References (48)

1. Hutmacher, D.W. Biomaterials offer cancer research the third dimension. Nat Mater 9, 90, 2010
2. Lutton, C., and Goss, B. Caring about microenvironments. Nat Biotechnol 26, 613, 2008
3. Edelman, D.B., and Keefer, E.W. A cultural renaissance: In vitro cell biology embraces three-dimensional context. Exp Neurol 192, 1, 2005
4. Kleinfeld, D., Kahler, K.H., and Hockberger, P.E. Controlled outgrowth of dissociated neurons on patterned substrates. J Neurosci 8, 4098, 1988
5. Magnusson, A.K., Linderholm, P., Vieider, C., Ulfendahl, M., and Erlandsson, A. Surface protein patterns govern morphology, proliferation, and expression of cellular markers but have no effect on physiological properties of cortical precursor cells. J Neurosci Res 86, 2363, 2008
6. Heller, D.A., Garga, V., Kelleher, K.J., Lee, T.-C., Mahbubani, S., Sigworth, L.A., et al. Patterned networks of mouse hippocampal neurons on peptide-coated gold surfaces. Biomaterials 26, 883, 2005
7. Xu, T., Gregory, C.A., Molnar, P., Cui, X., Jalota, S., Bhaduri, S.B., et al. Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials 27, 3580, 2006
8. Ma, W., Liu, Q.-Y., Jung, D., Manos, P., Pancrazio, J.J., Schaffner, A.E., et al. Central neuronal synapse formation on micropatterned surfaces. Brain Res Dev Brain Res 111, 231, 1998
9. Liu, Q.-Y., Coulombe, M., Dumm, J., Shaffer, K.M., Schaffner, A.E., Barker, J.L., et al. Synaptic connectivity in hippocampal neuronal networks cultured on micropatterned surfaces. Brain Res Dev Brain Res 120, 223, 2000
10. Thalhammer, A., Edgington, R.J., Cingolani, L.A., Schoepfer, R., and Jackman, R.B. The use of nanodiamond monolayer coatings to promote the formation of functional neuronal networks. Biomaterials 31, 2097, 2010
11. Marti'nez-Ramos, C., Lainez, S., Sancho, F., Garci'a Esparza, M.A., Planells-Cases, R., Garci'a Verdugo, J.M., et al. Differentiation of postnatal neural stem cells into glia and functional neurons on laminin-coated polymeric substrates. Tissue Eng Part A 14, 1365, 2008
12. Stevens, M.M., and George, J.H. Exploring and engineering the cell surface interface. Science 310, 1135, 2005
13. Bölgen, N., Menceloǧ lu, Y.Z., Acatay, K., Vargel, I., and Pisxkin, E. In vitro and in vivo degradation of non-woven materials made of poly(epsilon-caprolactone) nanofibers prepared by electrospinning under different conditions. J Biomater Sci Polym Ed 16, 1537, 2005
14. Horne, M.K., Nisbet, D.R., Forsythe, J.S., and Parish, C.L. Three-dimensional nanofibrous scaffolds incorporating immobilized BDNF promote proliferation and differentiation of cortical neural stem cells. Stem Cells Dev 19, 843, 2010
15. Nisbet, D.R., Yu, L.M.Y., Zahir, T., Forsythe, J.S., and Shoichet, M.S. Characterization of neural stem cells on electrospun poly(epsilon-caprolactone) submicron scaffolds: Evaluating their potential in neural tissue engineering. J Biomater Sci Polym Ed 19, 623, 2008
16. Irons, H.R., Cullen, D.K., Shapiro, N.P., Lambert, N.A., Lee, R.H., and Laplaca, M.C. Three-dimensional neural constructs: A novel platform for neurophysiological investigation. J Neural Eng 5, 333, 2008
17. Ma, W., Fitzgerald, W., Liu, Q.-Y., O'Shaughnessy, T.J., Maric, D., Lin, H.J., et al. CNS stem and progenitor cell differentiation into functional neuronal circuits in threedimensional collagen gels. Exp Neurol 190, 276, 2004
18. O'Shaughnessy, T.J., Lin, H.J., and Ma, W. Functional synapse formation among rat cortical neurons grown on threedimensional collagen gels. Neurosci Lett 340, 169, 2003
19. Xu, T., Molnar, P., Gregory, C., Das, M., Boland, T., and Hickman, J.J. Electrophysiological characterization of embryonic hippocampal neurons cultured in a 3D collagen hydrogel. Biomaterials 30, 4377, 2009
20. Mendonça, G., Mendonça, D.B.S., Simöes, L.G.P., Araú jo, A.L., Leite, E.R., Duarte, W.R., et al. The effects of implant surface nanoscale features on osteoblast-specific gene expression. Biomaterials 30, 4053, 2009
21. Shao, H.-J., Lee, Y.-T., Chen, C.-S., Wang, J.-H., and Young, T.-H. Modulation of gene expression and collagen production of anterior cruciate ligament cells through cell shape changes on polycaprolactone/chitosan blends. Biomaterials 31, 4695, 2010
22. Chew, S.Y., Mi, R., Hoke, A., and Leong, K.W. The effect of the alignment of electrospun fibrous scaffolds on Schwann cell maturation. Biomaterials 29, 653, 2008
23. Shahbazi, E., Kiani, S., Gourabi, H., and Baharvand, H. Electrospun nanofibrillar surfaces promote neuronal differentiation and function from human embryonic stem cells. Tissue Eng Part A 17, 3021, 2011
24. Xu, H., Bai, J., Meng, J., Hao, W., Xu, H., and Cao, J.-M. Multi-walled carbon nanotubes suppress potassium channel activities in PC12 cells. Nanotechnology 20, 285102, 2009
25. Park, K.H., Chhowalla, M., Iqbal, Z., and Sesti, F. Singlewalled carbon nanotubes are a new class of ion channel blockers. J Biol Chem 278, 50212, 2003
26. Lovat, V., Pantarotto, D., Lagostena, L., Cacciari, B., Grandolfo, M., Righi, M., et al. Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett 5, 1107, 2005
27. Cellot, G., Cilia, E., Cipollone, S., Rancic, V., Sucapane, A., Giordani, S., et al. Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nat Nanotechnol 4, 126, 2009
28. Ho, C., and O'Leary, M.E. Single-cell analysis of sodium channel expression in dorsal root ganglion neurons. Mol Cell Neurosci 46, 159, 2011
29. Scroggs, R.S., and Fox, A.P. Calcium current variation between acutely isolated adult rat dorsal root ganglion neurons of different size. J Physiol (Lond) 445, 639, 1992
30. Scroggs, R.S., Todorovic, S.M., Anderson, E.G., and Fox, A.P. Variation in IH, IIR, and ILEAK between acutely isolated adult rat dorsal root ganglion neurons of different size. J Neurophysiol 71, 271, 1994
31. Villiere, V., and McLachlan, E.M. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol 76, 1924, 1996
32. Caffrey, J.M., Eng, D.L., Black, J.A., Waxman, S.G., and Kocsis, J.D. Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592, 283, 1992
33. Xie, J., MacEwan, M.R., Li, X., Sakiyama-Elbert, S.E., and Xia, Y. Neurite outgrowth on nanofiber scaffolds with different orders, structures, and surface properties. ACS Nano 3, 1151, 2009
34. Schnell, E., Klinkhammer, K., Balzer, S., Brook, G., Klee, D., Dalton, P., et al. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials 28, 3012, 2007
35. Daud, M.F.B., Pawar, K.C., Claeyssens, F., Ryan, A.J., and Haycock, J.W. An aligned 3D neuronal-glial co-culture model for peripheral nerve studies. Biomaterials 33, 5901, 2012
36. Corey, J.M., Lin, D.Y., Mycek, K.B., Chen, Q., Samuel, S., Feldman, E.L., et al. Aligned electrospun nanofibers specify the direction of dorsal root ganglia neurite growth. J Biomed Mater Res A 83, 636, 2007
37. Wang, H.B., Mullins, M.E., Cregg, J.M., McCarthy, C.W., and Gilbert, R.J. Varying the diameter of aligned electrospun fibers alters neurite outgrowth and Schwann cell migration. Acta Biomater 6, 2970, 2010
38. Eubanks, J.H., Perez-Velazquez, J.L., Kerr, R.G., Carlen, P.L., Mills, L.R., and Jones, O.T. Three distinct neuronal phenotypes exist in embryonic rat hippocampal neurons cultured in basic fibroblast growth factor. Neurosci Lett 204, 5, 1996
39. Bi, G.Q., and Poo, M.M. Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18, 10464, 1998
40. Tao, H., Zhang, L.I., Bi, G., and Poo, M. Selective presynaptic propagation of long-Term potentiation in defined neural networks. J Neurosci 20, 3233, 2000
41. Wang, H.-X., Gerkin, R.C., Nauen, D.W., and Bi, G.-Q. Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat Neurosci 8, 187, 2005
42. Nagata, I., and Nakatsuji, N. Rodent CNS neuroblasts exhibit both perpendicular and parallel contact guidance on the aligned parallel neurite bundle. Development 112, 581, 1991
43. Nagata, I., Kawana, A., and Nakatsuji, N. Perpendicular contact guidance of CNS neuroblasts on artificial microstructures. Development 117, 401, 1993
44. Fozdar, D.Y., Lee, J.Y., Schmidt, C.E., and Chen, S. Hippocampal neurons respond uniquely to topographies of various sizes and shapes. Biofabrication 2, 035005, 2010
45. Lee, J.Y., Bashur, C.A., Gomez, N., Goldstein, A.S., and Schmidt, C.E. Enhanced polarization of embryonic hippocampal neurons on micron scale electrospun fibers. J Biomed Mater Res A 92, 1398, 2010
46. Larsson, K., Brisby, H., Johansson, B.R., Runesson, E., and Rydevik, B. Electron microscopy analysis of neurites extending from dorsal root ganglia in vitro following exposure to intervertebral disc cells. Cells Tissues Organs (Print) 196, 82, 2012
47. Arhem, P., Klement, G., and Blomberg, C. Channel density regulation of firing patterns in a cortical neuron model. Biophys J 90, 4392, 2006
48. Arhem, P., and Blomberg, C. Ion channel density and threshold dynamics of repetitive firing in a cortical neuron model. BioSystems 89, 117, 2007