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Approaches for Neural Tissue Regeneration

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Abstract

There is currently no treatment for neurodegenerative diseases such as Parkinson’s or Alzheimer’s diseases. While spinal cord injury has no treatment either, nerve injuries are being treated with autologous grafts, a procedure that in turn translates into a loss of function in the donor area. The development of therapies for these pathologies has become urgent as population keeps on ageing. A promising direction of investigation is the use of regenerative techniques to re-grow healthy and functional tissue in the injured area. In this review article, various approaches currently investigated to promote neural regeneration are covered. Those include approaches based on (and many times combining) stem cell therapy, scaffolds made of hydrogel, electrospun fibers and conductive materials as well as the use of soluble or non-diffusible growth factors.

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References

  1. Di Carlo, A. (2009). Human and economic burden of stroke. Age and Ageing, 38(1), 4–5.

    PubMed  Google Scholar 

  2. Spinal cord injury facts and figures at a glance. Journal of Spinal Cord Medicine, 35(6), 480–481 (2012).

  3. Ford, B. (2010). Parkinson’s disease Q & A, sixth edition.

  4. May, M., Sobol, S. M., & Mester, S. J. (1991). Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy. Otolaryngology – Head and Neck Surgery, 104(6), 818–825.

    CAS  PubMed  Google Scholar 

  5. Brooks, D. N., Weber, R. V., Chao, J. D., et al. (2012). Processed nerve allografts for peripheral nerve reconstruction: a multicenter study of utilization and outcomes in sensory, mixed, and motor nerve reconstructions. Microsurgery, 32(1), 1–14.

    PubMed  Google Scholar 

  6. Dellon, A. L., & Mackinnon, S. E. (1988). An alternative to the classical nerve graft for the management of the short nerve gap. Plastic and Reconstructive Surgery, 82(5), 849–856.

    CAS  PubMed  Google Scholar 

  7. Montastruc, J. L., Rascol, O., & Senard, J. M. (1999). Treatment of Parkinson’s disease should begin with a dopamine agonist. Movement Disord, 14(5), 725–730.

    CAS  PubMed  Google Scholar 

  8. Sugaya, K., & Merchant, S. (2008). How to approach Alzheimer’s disease therapy using stem cell technologies. Journal of Alzheimer’s Disease, 15(2), 241–254.

    CAS  PubMed  Google Scholar 

  9. Miller, R. H. (2006). The promise of stem cells for neural repair. Brain Research, 1091(1), 258–264.

    CAS  PubMed  Google Scholar 

  10. Hwang, W., Alvarez-Buylla, A., & Lim, D. (2012). Glial nature of adult neural stem cells: neurogenic competence in adult astrocytes. In M. S. Rao, M. Carpenter, & M. C. Vemuri (Eds.), Neural development and stem cells (pp. 149–172). New York: Springer.

    Google Scholar 

  11. Pawitan, J. A. (2011). Prospect of cell therapy for Parkinson’s disease. Anat Cell Biol, 44(4), 256–264.

    PubMed Central  PubMed  Google Scholar 

  12. Joyce, N., Annett, G., Wirthlin, L., Olson, S., Bauer, G., & Nolta, J. A. (2010). Mesenchymal stem cells for the treatment of neurodegenerative disease. Regenerative Medicine, 5(6), 933–946.

    PubMed Central  PubMed  Google Scholar 

  13. Kassis, I., Grigoriadis, N., Gowda-Kurkalli, B., et al. (2008). Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Archives of Neurology, 65(6), 753–761.

    PubMed  Google Scholar 

  14. Aizman, I., Tate, C. C., Mcgrogan, M., & Case, C. C. (2009). Extracellular matrix produced by bone marrow stromal cells and by their derivative, SB623 cells, supports neural cell growth. Journal of Neuroscience Research, 87(14), 3198–3206.

    CAS  PubMed  Google Scholar 

  15. Cummings, B. J., Uchida, N., Tamaki, S. J., et al. (2005). Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proceedings of the National Academy of Sciences of the United States of America, 102(39), 14069–14074.

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Borlongan, C. V., Tajima, Y., Trojanowski, J. Q., Lee, V. M., & Sanberg, P. R. (1998). Transplantation of cryopreserved human embryonal carcinoma-derived neurons (NT2N cells) promotes functional recovery in ischemic rats. Experimental Neurology, 149(2), 310–321.

    CAS  PubMed  Google Scholar 

  17. Heine, W., Conant, K., Griffin, J. W., & Hoke, A. (2004). Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Experimental Neurology, 189(2), 231–240.

    CAS  PubMed  Google Scholar 

  18. Munoz, J. R., Stoutenger, B. R., Robinson, A. P., Spees, J. L., & Prockop, D. J. (2005). Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proceedings of the National Academy of Sciences of the United States of America, 102(50), 18171–18176.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Hansmann, F., Pringproa, K., Ulrich, R, et al. (2012). Highly malignant behavior of a murine oligodendrocyte precursor cell line following transplantation into the demyelinated and non-demyelinated central nervous system. Cell Transplant.

  20. Sulaiman, O. A., & Gordon, T. (2002). Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia, 37(3), 206–218.

    PubMed  Google Scholar 

  21. Kobayashi, N. R., Fan, D. P., Giehl, K. M., Bedard, A. M., Wiegand, S. J., & Tetzlaff, W. (1997). BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Talpha1-tubulin mRNA expression, and promote axonal regeneration. Journal of Neuroscience, 17(24), 9583–9595.

    CAS  PubMed  Google Scholar 

  22. Boyd, J. G., & Gordon, T. (2003). Glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Experimental Neurology, 183(2), 610–619.

    CAS  PubMed  Google Scholar 

  23. Grassi, M., & Grassi, G. (2005). Mathematical modelling and controlled drug delivery: matrix systems. Current Drug Delivery, 2(1), 97–116.

    CAS  PubMed  Google Scholar 

  24. He, J., Zhong, C., & Mi, J. (2005). Modeling of drug release from bioerodible polymer matrices. Drug Delivery, 12(5), 251–259.

    CAS  PubMed  Google Scholar 

  25. Sackett, C. K., & Narasimhan, B. (2011). Mathematical modeling of polymer erosion: consequences for drug delivery. International Journal of Pharmaceutics, 418(1), 104–114.

    CAS  PubMed  Google Scholar 

  26. Xia, L., Wan, H., Hao, S. Y., et al. (2013). Co-transplantation of neural stem cells and Schwann cells within poly (L-lactic-co-glycolic acid) scaffolds facilitates axonal regeneration in hemisected rat spinal cord. Chinese Medical Journal, 126(5), 909–917.

    PubMed  Google Scholar 

  27. Tosi, G., Bortot, B., Ruozi, B., et al. (2013). Potential use of polymeric nanoparticles for drug delivery across the blood–brain barrier. Current Medicinal Chemistry.

  28. Caicco, M. J., Cooke, M. J., Wang, Y., Tuladhar, A., Morshead, C. M., & Shoichet, M. S. (2013). A hydrogel composite system for sustained epi-cortical delivery of Cyclosporin A to the brain for treatment of stroke. Journal of Controlled Release, 166(3), 197–202.

    CAS  PubMed  Google Scholar 

  29. Han, J., Lazarovici, P., Pomerantz, C., Chen, X., Wei, Y., & Lelkes, P. I. (2011). Co-electrospun blends of PLGA, gelatin, and elastin as potential nonthrombogenic scaffolds for vascular tissue engineering. Biomacromolecules, 12(2), 399–408.

    CAS  PubMed  Google Scholar 

  30. Wang, Y., Wei, Y. T., Zu, Z. H., et al. (2011). Combination of hyaluronic acid hydrogel scaffold and PLGA microspheres for supporting survival of neural stem cells. Pharmaceutical Research, 28(6), 1406–1414.

    CAS  PubMed  Google Scholar 

  31. Tzeng, S. Y., & Lavik, E. B. (2010). Photopolymerizable nanoarray hydrogels deliver CNTF and promote differentiation of neural stem cells. Soft Matter, 6(10), 2208–2215.

    CAS  Google Scholar 

  32. Bertram, J. P., Rauch, M. F., Chang, K., & Lavik, E. B. (2010). Using polymer chemistry to modulate the delivery of neurotrophic factors from degradable microspheres: delivery of BDNF. Pharmaceutical Research, 27(1), 82–91.

    CAS  PubMed  Google Scholar 

  33. Han, N., Johnson, J., Lannutti, J. J., & Winter, J. O. (2012). Hydrogel-electrospun fiber composite materials for hydrophilic protein release. Journal of Controlled Release, 158(1), 165–170.

    CAS  PubMed  Google Scholar 

  34. Puppi, D., Piras, A. M., Detta, N., Dinucci, D., & Chiellini, F. (2010). Poly(lactic-co-glycolic acid) electrospun fibrous meshes for the controlled release of retinoic acid. Acta Biomaterialia, 6(4), 1258–1268.

    CAS  PubMed  Google Scholar 

  35. Wang, C. Y., Liu, J. J., Fan, C. Y., Mo, X. M., Ruan, H. J., & Li, F. F. (2012). The effect of aligned core-shell nanofibres delivering NGF on the promotion of sciatic nerve regeneration. Journal of Biomaterials Science, Polymer Edition, 23(1–4), 167–184.

    CAS  Google Scholar 

  36. Seyednejad, H., Ji, W., Yang, F., et al. (2012). Coaxially electrospun scaffolds based on hydroxyl-functionalized poly(epsilon-caprolactone) and loaded with VEGF for tissue engineering applications. Biomacromolecules, 13(11), 3650–3660.

    CAS  PubMed  Google Scholar 

  37. Wang, Y., Cooke, M. J., Morshead, C. M., & Shoichet, M. S. (2012). Hydrogel delivery of erythropoietin to the brain for endogenous stem cell stimulation after stroke injury. Biomaterials, 33(9), 2681–2692.

    CAS  PubMed  Google Scholar 

  38. Gardette, R., Courtois, M., & Bisconte, J. C. (1982). Prenatal development of mouse central nervous structures: time of neuron origin and gradients of neuronal production. A radioautographic study. Journal für Hirnforschung, 23(4), 415–431.

    CAS  PubMed  Google Scholar 

  39. Altman, J., & Bayer, S. A. (1979). Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. Journal of Comparative Neurology, 188(3), 455–471.

    CAS  PubMed  Google Scholar 

  40. Luo, L., & Flanagan, J. G. (2007). Development of continuous and discrete neural maps. Neuron, 56(2), 284–300.

    CAS  PubMed  Google Scholar 

  41. Gillespie, L. N., Clark, G. M., Bartlett, P. F., & Marzella, P. L. (2003). BDNF-induced survival of auditory neurons in vivo: cessation of treatment leads to accelerated loss of survival effects. Journal of Neuroscience Research, 71(6), 785–790.

    CAS  PubMed  Google Scholar 

  42. Keenan, T. M., Grinager, J. R., Procak, A. A., & Svendsen, C. N. (2012). In vitro localization of human neural stem cell neurogenesis by engineered FGF-2 gradients. Integr Biol (Camb), 4(12), 1522–1531.

    CAS  Google Scholar 

  43. Dodla, M. C., & Bellamkonda, R. V. (2008). Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps. Biomaterials, 29(1), 33–46.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Shi, J., Wang, L., Zhang, F., et al. (2010). Incorporating protein gradient into electrospun nanofibers as scaffolds for tissue engineering. ACS Applied Materials & Interfaces, 2(4), 1025–1030.

    CAS  Google Scholar 

  45. Kunze, A., Valero, A., Zosso, D., & Renaud, P. (2011). Synergistic NGF/B27 gradients position synapses heterogeneously in 3D micropatterned neural cultures. PLoS One, 6(10), e26187.

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Krewson, C. E., Klarman, M. L., & Saltzman, W. M. (1995). Distribution of nerve growth factor following direct delivery to brain interstitium. Brain Research, 680(1–2), 196–206.

    CAS  PubMed  Google Scholar 

  47. Saltzman, W. M., Mak, M. W., Mahoney, M. J., Duenas, E. T., & Cleland, J. L. (1999). Intracranial delivery of recombinant nerve growth factor: release kinetics and protein distribution for three delivery systems. Pharmaceutical Research, 16(2), 232–240.

    CAS  PubMed  Google Scholar 

  48. Mahoney, M. J., Krewson, C., Miller, J., & Saltzman, W. M. (2006). Impact of cell type and density on nerve growth factor distribution and bioactivity in 3-dimensional collagen gel cultures. Tissue Engineering, 12(7), 1915–1927.

    CAS  PubMed  Google Scholar 

  49. Sirianni, R. W., Olausson, P., Chiu, A. S., Taylor, J. R., & Saltzman, W. M. (2010). The behavioral and biochemical effects of BDNF containing polymers implanted in the hippocampus of rats. Brain Research, 1321, 40–50.

    CAS  PubMed  Google Scholar 

  50. Shanbhag, M. S., Lathia, J. D., Mughal, M. R., et al. (2010). Neural progenitor cells grown on hydrogel surfaces respond to the product of the transgene of encapsulated genetically engineered fibroblasts. Biomacromolecules.

  51. Dey, N. D., Bombard, M. C., Roland, B. P., et al. (2010). Genetically engineered mesenchymal stem cells reduce behavioral deficits in the YAC 128 mouse model of Huntington’s disease. Behavioural Brain Research, 214(2), 193–200.

    CAS  PubMed  Google Scholar 

  52. Zeng, X., Cai, J., Chen, J., et al. (2004). Dopaminergic differentiation of human embryonic stem cells. Stem Cells, 22(6), 925–940.

    CAS  PubMed  Google Scholar 

  53. Tuszynski, M. H., Thal, L., Pay, M., et al. (2005). A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nature Medicine, 11(5), 551–555.

    CAS  PubMed  Google Scholar 

  54. Sharp, K. G., Dickson, A. R., Marchenko, S. A., et al. (2012). Salmon fibrin treatment of spinal cord injury promotes functional recovery and density of serotonergic innervation. Experimental Neurology, 235(1), 345–356.

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Woerly, S., Doan, V. D., Sosa, N., De Vellis, J., & Espinosa-Jeffrey, A. (2004). Prevention of gliotic scar formation by NeuroGel allows partial endogenous repair of transected cat spinal cord. Journal of Neuroscience Research, 75(2), 262–272.

    CAS  PubMed  Google Scholar 

  56. Kwak, Y. D., Brannen, C. L., Qu, T., et al. (2006). Amyloid precursor protein regulates differentiation of human neural stem cells. Stem Cells and Development, 15(3), 381–389.

    CAS  PubMed  Google Scholar 

  57. Park, J., Lim, E., Back, S., Na, H., Park, Y., & Sun, K. (2010). Nerve regeneration following spinal cord injury using matrix metalloproteinase-sensitive, hyaluronic acid-based biomimetic hydrogel scaffold containing brain-derived neurotrophic factor. Journal of Biomedical Materials Research. Part A, 93(3), 1091–1099.

    PubMed  Google Scholar 

  58. Yu, L., & Ding, J. (2008). Injectable hydrogels as unique biomedical materials. Chemical Society Reviews, 37(8), 1473–1481.

    CAS  PubMed  Google Scholar 

  59. Rickett, T. A., Amoozgar, Z., Tuchek, C. A., Park, J., Yeo, Y., & Shi, R. (2011). Rapidly photo-cross-linkable chitosan hydrogel for peripheral neurosurgeries. Biomacromolecules, 12(1), 57–65.

    CAS  PubMed  Google Scholar 

  60. Peppas, N. A., Hilt, J. Z., Khademhosseini, A., & Langer, R. (2006). Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Advanced Materials, 18, 1345–1360.

    CAS  Google Scholar 

  61. Zuidema, J. M., Pap, M. M., Jaroch, D. B., Morrison, F. A., & Gilbert, R. J. (2011). Fabrication and characterization of tunable polysaccharide hydrogel blends for neural repair. Acta Biomaterialia, 7(4), 1634–1643.

    CAS  PubMed  Google Scholar 

  62. Banerjee, A., Arha, M., Choudhary, S., et al. (2009). The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials, 30(27), 4695–4699.

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Yi, X., Jin, G., Tian, M., Mao, W., & Qin, J. (2011). Porous chitosan scaffold and ngf promote neuronal differentiation of neural stem cells in vitro. Neuro Endocrinology Letters, 32(5), 705–710.

    CAS  PubMed  Google Scholar 

  64. Pfister, L. A., Papaloizos, M., Merkle, H. P., & Gander, B. (2007). Hydrogel nerve conduits produced from alginate/chitosan complexes. Journal of Biomedical Materials Research. Part A, 80(4), 932–937.

    PubMed  Google Scholar 

  65. Macaya, D., & Spector, M. (2012). Injectable hydrogel materials for spinal cord regeneration: a review. Biomedical Materials, 7(1), 012001.

    CAS  PubMed  Google Scholar 

  66. Song, B., Song, J., Zhang, S., et al. (2012). Sustained local delivery of bioactive nerve growth factor in the central nervous system via tunable diblock copolypeptide hydrogel depots. Biomaterials, 33(35), 9105–9116.

    CAS  PubMed  Google Scholar 

  67. Wang, Y., Qi, F., Zhu, S., et al. (2013). A synthetic oxygen carrier in fibrin matrices promotes sciatic nerve regeneration in rats. Acta Biomaterialia.

  68. Perale, G., Rossi, F., Santoro, M., et al. (2012). Multiple drug delivery hydrogel system for spinal cord injury repair strategies. Journal of Controlled Release, 159(2), 271–280.

    CAS  PubMed  Google Scholar 

  69. Woerly, S., Pinet, E., De Robertis, L., et al. (1998). Heterogeneous PHPMA hydrogels for tissue repair and axonal regeneration in the injured spinal cord. Journal of Biomaterials Science, Polymer Edition, 9(7), 681–711.

    CAS  Google Scholar 

  70. Doshi, J., & Reneker, D. H. (1995). Electrospinning process and applications of electrospun fibers. Journal of Electrostatics, 35(2–3), 151–160.

    CAS  Google Scholar 

  71. Ramakrishna, S. (2005). An introduction to electrospinning and nanofibers. World Scientific Publishing Company.

  72. Alhosseini, S. N., Moztarzadeh, F., Mozafari, M., et al. (2012). Synthesis and characterization of electrospun polyvinyl alcohol nanofibrous scaffolds modified by blending with chitosan for neural tissue engineering. International Journal of Nanomedicine, 7, 25–34.

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Zong, X., Bien, H., Chung, C. Y., et al. (2005). Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials, 26(26), 5330–5338.

    CAS  PubMed  Google Scholar 

  74. Boland, E. D., Wnek, G. E., Simpson, D. G., Pawlowski, K. J., & Bowlin, G. L. (2001). Tailoring tissue engineering scaffolds using electrostatic processing techniques: a study of poly(glycolic acid) electrospinning. Journal of Macromolecular Science, Part A, 38(12), 1231–1243.

    Google Scholar 

  75. Subramanian, A., Krishnan, U. M., & Sethuraman, S. (2011). Fabrication of uniaxially aligned 3D electrospun scaffolds for neural regeneration. Biomedical Materials, 6(2), 025004.

    PubMed  Google Scholar 

  76. Ma, Z., Lan, Z., Matsuura, T., & Ramakrishna, S. (2009). Electrospun polyethersulfone affinity membrane: membrane preparation and performance evaluation. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 877(29), 3686–3694.

    CAS  PubMed  Google Scholar 

  77. Yao, L., O’brien, N., Windebank, A., & Pandit, A. (2009). Orienting neurite growth in electrospun fibrous neural conduits. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 90(2), 483–491.

    Google Scholar 

  78. Christopherson, G. T., Song, H., & Mao, H. Q. (2009). The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials, 30(4), 556–564.

    CAS  PubMed  Google Scholar 

  79. Wang, J., Ye, R., Wei, Y., et al. (2012). The effects of electrospun TSF nanofiber diameter and alignment on neuronal differentiation of human embryonic stem cells. Journal of Biomedical Materials Research. Part A, 100(3), 632–645.

    PubMed  Google Scholar 

  80. Corey, J. M., Gertz, C. C., Wang, B. S., et al. (2008). The design of electrospun PLLA nanofiber scaffolds compatible with serum-free growth of primary motor and sensory neurons. Acta Biomaterialia, 4(4), 863–875.

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Nisbet, D. R., Rodda, A. E., Horne, M. K., Forsythe, J. S., & Finkelstein, D. I. (2009). Neurite infiltration and cellular response to electrospun polycaprolactone scaffolds implanted into the brain. Biomaterials, 30(27), 4573–4580.

    CAS  PubMed  Google Scholar 

  82. Koh, H. S., Yong, T., Chan, C. K., & Ramakrishna, S. (2008). Enhancement of neurite outgrowth using nano-structured scaffolds coupled with laminin. Biomaterials, 29(26), 3574–3582.

    CAS  PubMed  Google Scholar 

  83. Kim, H. W., Yu, H. S., & Lee, H. H. (2008). Nanofibrous matrices of poly(lactic acid) and gelatin polymeric blends for the improvement of cellular responses. Journal of Biomedical Materials Research. Part A, 87(1), 25–32.

    PubMed  Google Scholar 

  84. Han, N., Rao, S. S., Johnson, J., et al. (2011). Hydrogel-electrospun fiber mat composite coatings for neural prostheses. Front Neuroeng, 4, 2.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Huang, S.-H., Chien, T.-C., & Hung, K.-Y. (2011). Selective deposition of electrospun alginate-based nanofibers onto cell-repelling hydrogel surfaces for cell-based microarrays. Current Nanoscience, 7(2), 267–274.

    CAS  Google Scholar 

  86. Nakaji-Hirabayashi, T., Kato, K., & Iwata, H. (2012). Improvement of neural stem cell survival in collagen hydrogels by incorporating laminin-derived cell adhesive polypeptides. Bioconjugate Chemistry, 23(2), 212–221.

    CAS  PubMed  Google Scholar 

  87. Han, Q., Sun, W., Lin, H., et al. (2009). Linear ordered collagen scaffolds loaded with collagen-binding brain-derived neurotrophic factor improve the recovery of spinal cord injury in rats. Tissue Engineering. Part A, 15(10), 2927–2935.

    CAS  PubMed  Google Scholar 

  88. Egawa, E. Y., Kato, K., Hiraoka, M., Nakaji-Hirabayashi, T., & Iwata, H. (2011). Enhanced proliferation of neural stem cells in a collagen hydrogel incorporating engineered epidermal growth factor. Biomaterials, 32(21), 4737–4743.

    CAS  PubMed  Google Scholar 

  89. Gamez Sazo, R. E., Maenaka, K., Gu, W., Wood, P. M., & Bunge, M. B. (2012). Fabrication of growth factor- and extracellular matrix-loaded, gelatin-based scaffolds and their biocompatibility with Schwann cells and dorsal root ganglia. Biomaterials, 33(33), 8529–8539.

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Wang, H., Zhao, Q., Zhao, W., Liu, Q., Gu, X., & Yang, Y. (2012). Repairing rat sciatic nerve injury by a nerve-growth-factor-loaded, chitosan-based nerve conduit. Biotechnology and Applied Biochemistry, 59(5), 388–394.

    CAS  PubMed  Google Scholar 

  91. Yoo, H. S., Kim, T. G., & Park, T. G. (2009). Surface-functionalized electrospun nanofibers for tissue engineering and drug delivery. Advanced Drug Delivery Reviews, 61(12), 1033–1042.

    CAS  PubMed  Google Scholar 

  92. Cho, Y. I., Choi, J. S., Jeong, S. Y., & Yoo, H. S. (2010). Nerve growth factor (NGF)-conjugated electrospun nanostructures with topographical cues for neuronal differentiation of mesenchymal stem cells. Acta Biomaterialia, 6(12), 4725–4733.

    CAS  PubMed  Google Scholar 

  93. Horne, M. K., Nisbet, D. R., Forsythe, J. S., & Parish, C. L. (2010). Three-dimensional nanofibrous scaffolds incorporating immobilized BDNF promote proliferation and differentiation of cortical neural stem cells. Stem Cells and Development, 19(6), 843–852.

    CAS  PubMed  Google Scholar 

  94. Belisle, J. M., Correia, J. P., Wiseman, P. W., Kennedy, T. E., & Costantino, S. (2008). Patterning protein concentration using laser-assisted adsorption by photobleaching, LAPAP. Lab on a Chip, 8(12), 2164–2167.

    CAS  PubMed  Google Scholar 

  95. Lin, H., Chen, B., Wang, B., Zhao, Y., Sun, W., & Dai, J. (2006). Novel nerve guidance material prepared from bovine aponeurosis. Journal of Biomedical Materials Research. Part A, 79(3), 591–598.

    PubMed  Google Scholar 

  96. Cao, J., Sun, C., Zhao, H., et al. (2011). The use of laminin modified linear ordered collagen scaffolds loaded with laminin-binding ciliary neurotrophic factor for sciatic nerve regeneration in rats. Biomaterials, 32(16), 3939–3948.

    CAS  PubMed  Google Scholar 

  97. Xie, J., Macewan, M. R., Ray, W. Z., Liu, W., Siewe, D. Y., & Xia, Y. (2010). Radially aligned, electrospun nanofibers as dural substitutes for wound closure and tissue regeneration applications. ACS Nano, 4(9), 5027–5036.

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Park, J. S., Yang, H. N., Woo, D. G., et al. (2012). Exogenous Nurr1 gene expression in electrically-stimulated human MSCs and the induction of neurogenesis. Biomaterials, 33(29), 7300–7308.

    CAS  PubMed  Google Scholar 

  99. Huang, J., Lu, L., Zhang, J., et al. (2012). Electrical stimulation to conductive scaffold promotes axonal regeneration and remyelination in a rat model of large nerve defect. PLoS One, 7(6), e39526.

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Mckasson, M. J., Huang, L., & Robinson, K. R. (2008). Chick embryonic Schwann cells migrate anodally in small electrical fields. Experimental Neurology, 211(2), 585–587.

    PubMed Central  PubMed  Google Scholar 

  101. Xie, J., Macewan, M. R., Willerth, S. M., et al. (2009). Conductive core-sheath nanofibers and their potential application in neural tissue engineering. Advanced Functional Materials, 19(14), 2312–2318.

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Lee, J. Y., Bashur, C. A., Goldstein, A. S., & Schmidt, C. E. (2009). Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials, 30(26), 4325–4335.

    CAS  PubMed Central  PubMed  Google Scholar 

  103. Lee, J. Y., Bashur, C. A., Milroy, C. A., Forciniti, L., Goldstein, A. S., & Schmidt, C. E. (2012). Nerve growth factor-immobilized electrically conducting fibrous scaffolds for potential use in neural engineering applications. IEEE Transactions on Nanobioscience, 11(1), 15–21.

    PubMed  Google Scholar 

  104. Wang, S., Zhao, Y., Shen, M., & Shi, X. (2012). Electrospun hybrid nanofibers doped with nanoparticles or nanotubes for biomedical applications. Therapeutic Delivery, 3(10), 1155–1169.

    CAS  PubMed  Google Scholar 

  105. Huang, Y. J., Wu, H. C., Tai, N. H., Wang, T. W. (2012). Carbon nanotube rope with electrical stimulation promotes the differentiation and maturity of neural stem cells. Small.

  106. Kabiri, M., Soleimani, M., Shabani, I., et al. (2012). Neural differentiation of mouse embryonic stem cells on conductive nanofiber scaffolds. Biotechnological Letters, 34(7), 1357–1365.

    CAS  Google Scholar 

  107. Miao, J., Miyauchi, M., Dordick, J. S., & Linhardt, R. J. (2012). Preparation and characterization of electrospun core sheath nanofibers from multi-walled carbon nanotubes and poly(vinyl pyrrolidone). Journal of Nanoscience and Nanotechnology, 12(3), 2387–2393.

    CAS  PubMed  Google Scholar 

  108. Hwang, J. Y., Shin, U. S., Jang, W. C., Hyun, J. K., Wall, I. B., & Kim, H. W. (2013). Biofunctionalized carbon nanotubes in neural regeneration: a mini-review. Nanoscale, 5(2), 487–497.

    CAS  PubMed  Google Scholar 

  109. Huang, Y. J., Wu, H. C., Tai, N. H., & Wang, T. W. (2012). Carbon nanotube rope with electrical stimulation promotes the differentiation and maturity of neural stem cells. Small, 8(18), 2869–2877.

    CAS  PubMed  Google Scholar 

  110. Sabri, F., Cole, J. A., Scarbrough, M. C., & Leventis, N. (2012). Investigation of polyurea-crosslinked silica aerogels as a neuronal scaffold: a pilot study. PLoS One, 7(3), e33242.

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Joo, N. Y., Knowles, J. C., Lee, G. S., et al. (2012). Effects of phosphate glass fiber-collagen scaffolds on functional recovery of completely transected rat spinal cords. Acta Biomaterialia, 8(5), 1802–1812.

    CAS  PubMed  Google Scholar 

  112. Uemura, M., Refaat, M. M., Shinoyama, M., Hayashi, H., Hashimoto, N., & Takahashi, J. (2010). Matrigel supports survival and neuronal differentiation of grafted embryonic stem cell-derived neural precursor cells. Journal of Neuroscience Research, 88(3), 542–551.

    CAS  PubMed  Google Scholar 

  113. Widhe, M., Bysell, H., Nystedt, S., et al. (2010). Recombinant spider silk as matrices for cell culture. Biomaterials, 31(36), 9575–9585.

    CAS  PubMed  Google Scholar 

  114. Lewicka, M., Hermanson, O., & Rising, A. U. (2012). Recombinant spider silk matrices for neural stem cell cultures. Biomaterials, 33(31), 7712–7717.

    CAS  PubMed  Google Scholar 

  115. Assal, Y., Mie, M., & Kobatake, E. (2013). The promotion of angiogenesis by growth factors integrated with ECM proteins through coiled-coil structures. Biomaterials, 34(13), 3315–3323.

    CAS  PubMed  Google Scholar 

  116. Shaikh Mohammed, J., Decoster, M. A., & Mcshane, M. J. (2006). Fabrication of interdigitated micropatterns of self-assembled polymer nanofilms containing cell-adhesive materials. Langmuir, 22(6), 2738–2746.

    PubMed  Google Scholar 

  117. Beduer, A., Vieu, C., Arnauduc, F., Sol, J. C., Loubinoux, I., & Vaysse, L. (2012). Engineering of adult human neural stem cells differentiation through surface micropatterning. Biomaterials, 33(2), 504–514.

    CAS  PubMed  Google Scholar 

  118. Ruiz, A., Buzanska, L., Gilliland, D., et al. (2008). Micro-stamped surfaces for the patterned growth of neural stem cells. Biomaterials, 29(36), 4766–4774.

    CAS  PubMed  Google Scholar 

  119. Ilkhanizadeh, S., Teixeira, A. I., & Hermanson, O. (2007). Inkjet printing of macromolecules on hydrogels to steer neural stem cell differentiation. Biomaterials, 28(27), 3936–3943.

    CAS  PubMed  Google Scholar 

  120. Xu, T., Gregory, C. A., Molnar, P., et al. (2006). Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials, 27(19), 3580–3588.

    CAS  PubMed  Google Scholar 

  121. Choi, Y. K., Cho, H., Seo, Y. K., Yoon, H. H., Park, J. K. (2012). Stimulation of sub-sonic vibration promotes the differentiation of adipose tissue-derived mesenchymal stem cells into neural cells. Life Sciences.

  122. Chang, Y. J., Tsai, C. J., Tseng, F. G., Chen, T. J., Wang, T. W. (2012). Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior. Nanomedicine.

  123. Leong, W. S., Wu, S. C., Pal, M., et al. (2012). Cyclic tensile loading regulates human mesenchymal stem cell differentiation into neuron-like phenotype. Journal of Tissue Engineering and Regenerative Medicine.

  124. Shen, C. C., Yang, Y. C., Huang, T. B., Chan, S. C., Liu, B. S. (2013). Neural regeneration in a novel nerve conduit across a large gap of the transected sciatic nerve in rats with low-level laser phototherapy. Journal of Biomedical Materials Research Part A.

  125. Alleva, E., & Francia, N. (2009). Psychiatric vulnerability: suggestions from animal models and role of neurotrophins. Neuroscience and Biobehavioral Reviews, 33(4), 525–536.

    CAS  PubMed  Google Scholar 

  126. Bella, A. J., Lin, G., Lin, C. S., Hickling, D. R., Morash, C., & Lue, T. F. (2009). Nerve growth factor modulation of the cavernous nerve response to injury. The Journal of Sexual Medicine, 6(Suppl 3), 347–352.

    PubMed Central  PubMed  Google Scholar 

  127. Mwizerwa, O., Das, P., Nagy, N., Akbareian, S. E., Mably, J. D., & Goldstein, A. M. (2011). Gdnf is mitogenic, neurotrophic, and chemoattractive to enteric neural crest cells in the embryonic colon. Developmental Dynamics, 240(6), 1402–1411.

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Studer, L., Csete, M., Lee, S. H., et al. (2000). Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. Journal of Neuroscience, 20(19), 7377–7383.

    CAS  PubMed  Google Scholar 

  129. Cooke, M. J., Wang, Y., Morshead, C. M., & Shoichet, M. S. (2011). Controlled epi-cortical delivery of epidermal growth factor for the stimulation of endogenous neural stem cell proliferation in stroke-injured brain. Biomaterials, 32(24), 5688–5697.

    CAS  PubMed  Google Scholar 

  130. Ye, W., Shimamura, K., Rubenstein, J. L., Hynes, M. A., & Rosenthal, A. (1998). FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell, 93(5), 755–766.

    CAS  PubMed  Google Scholar 

  131. Hsieh, J., Aimone, J. B., Kaspar, B. K., Kuwabara, T., Nakashima, K., & Gage, F. H. (2004). IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. Journal of Cell Biology, 164(1), 111–122.

    CAS  PubMed  Google Scholar 

  132. Vincent, A. M., Mobley, B. C., Hiller, A., & Feldman, E. L. (2004). IGF-I prevents glutamate-induced motor neuron programmed cell death. Neurobiology of Disease, 16(2), 407–416.

    CAS  PubMed  Google Scholar 

  133. Cheng, B., Maffi, S. K., Martinez, A. A., Acosta, Y. P., Morales, L. D., & Roberts, J. L. (2011). Insulin-like growth factor-I mediates neuroprotection in proteasome inhibition-induced cytotoxicity in SH-SY5Y cells. Molecular and Cellular Neuroscience, 47(3), 181–190.

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Arruda, J. L., Colburn, R. W., Rickman, A. J., Rutkowski, M. D., & Deleo, J. A. (1998). Increase of interleukin-6 mRNA in the spinal cord following peripheral nerve injury in the rat: potential role of IL-6 in neuropathic pain. Brain Research. Molecular Brain Research, 62(2), 228–235.

    CAS  PubMed  Google Scholar 

  135. Ma, Q., Sommer, L., Cserjesi, P., & Anderson, D. J. (1997). Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. Journal of Neuroscience, 17(10), 3644–3652.

    CAS  PubMed  Google Scholar 

  136. Ma, Q., Fode, C., Guillemot, F., & Anderson, D. J. (1999). Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes and Development, 13(13), 1717–1728.

    CAS  PubMed  Google Scholar 

  137. Liu, Z., Gao, W., Wang, Y., Zhang, W., Liu, H., & Li, Z. (2011). Neuregulin-1beta regulates outgrowth of neurites and migration of neurofilament 200 neurons from dorsal root ganglial explants in vitro. Peptides, 32(6), 1244–1248.

    CAS  PubMed  Google Scholar 

  138. Kaka, G. R., Tiraihi, T., Delshad, A., Arabkheradmand, J., & Kazemi, H. (2012). In vitro differentiation of bone marrow stromal cells into oligodendrocyte-like cells using triiodothyronine as inducer. International Journal of Neuroscience, 122(5), 237–247.

    CAS  PubMed  Google Scholar 

  139. Lowry, N., Goderie, S. K., Lederman, P., et al. (2012). The effect of long-term release of Shh from implanted biodegradable microspheres on recovery from spinal cord injury in mice. Biomaterials, 33(10), 2892–2901.

    CAS  PubMed  Google Scholar 

  140. Jia, C., Cussen, A. R., & Hegg, C. C. (2011). ATP differentially upregulates fibroblast growth factor 2 and transforming growth factor alpha in neonatal and adult mice: effect on neuroproliferation. Neuroscience, 177, 335–346.

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Park, S., Lee, K. S., Lee, Y. J., et al. (2004). Generation of dopaminergic neurons in vitro from human embryonic stem cells treated with neurotrophic factors. Neuroscience Letters, 359(1–2), 99–103.

    CAS  PubMed  Google Scholar 

  142. Herz, J., Reitmeir, R., Hagen, S. I., et al. (2012). Intracerebroventricularly delivered VEGF promotes contralesional corticorubral plasticity after focal cerebral ischemia via mechanisms involving anti-inflammatory actions. Neurobiology of Disease, 45(3), 1077–1085.

    CAS  PubMed  Google Scholar 

  143. Ojha, S. S., Stevens, D. R., Hoffman, T. J., et al. (2008). Fabrication and characterization of electrospun chitosan nanofibers formed via templating with polyethylene oxide. Biomacromolecules, 9(9), 2523–2529.

    CAS  PubMed  Google Scholar 

  144. Del Gaudio, C., Bianco, A., Folin, M., Baiguera, S., & Grigioni, M. (2009). Structural characterization and cell response evaluation of electrospun PCL membranes: micrometric versus submicrometric fibers. Journal of Biomedical Materials Research. Part A, 89(4), 1028–1039.

    PubMed  Google Scholar 

  145. Jeong, S. I., Jun, I. D., Choi, M. J., Nho, Y. C., Lee, Y. M., & Shin, H. (2008). Development of electroactive and elastic nanofibers that contain polyaniline and poly(L-lactide-co-epsilon-caprolactone) for the control of cell adhesion. Macromolecular Bioscience, 8(7), 627–637.

    CAS  PubMed  Google Scholar 

  146. Chen, R., Huang, C., Ke, Q., He, C., Wang, H., & Mo, X. (2010). Preparation and characterization of coaxial electrospun thermoplastic polyurethane/collagen compound nanofibers for tissue engineering applications. Colloids and Surfaces B: Biointerfaces, 79(2), 315–325.

    CAS  PubMed  Google Scholar 

  147. Jeong, S. I., Ko, E. K., Yum, J., Jung, C. H., Lee, Y. M., & Shin, H. (2008). Nanofibrous poly(lactic acid)/hydroxyapatite composite scaffolds for guided tissue regeneration. Macromolecular Bioscience, 8(4), 328–338.

    CAS  PubMed  Google Scholar 

  148. Li, M., Guo, Y., Wei, Y., Macdiarmid, A. G., & Lelkes, P. I. (2006). Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials, 27(13), 2705–2715.

    CAS  PubMed  Google Scholar 

  149. Lee, Y. S., Collins, G., & Livingston Arinzeh, T. (2011). Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomaterialia, 7(11), 3877–3886.

    CAS  PubMed  Google Scholar 

  150. Caroni, P., & Grandes, P. (1990). Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. Journal of Cell Biology, 110(4), 1307–1317.

    CAS  PubMed  Google Scholar 

  151. Mey, J., & Thanos, S. (1993). Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Research, 602(2), 304–317.

    CAS  PubMed  Google Scholar 

  152. Li, B. H., Kim, S. M., Yoo, S. B., Kim, M. J., Jahng, J. W., & Lee, J. H. (2012). Recombinant human nerve growth factor (rhNGF-beta) gene transfer promotes regeneration of crush-injured mental nerve in rats. Oral Surg Oral Med Oral Pathol Oral Radiol, 113(3), e26–e34.

    PubMed  Google Scholar 

  153. Neuhuber, B., Timothy Himes, B., Shumsky, J. S., Gallo, G., & Fischer, I. (2005). Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Research, 1035(1), 73–85.

    CAS  PubMed  Google Scholar 

  154. Luo, J., Zhang, H. T., Jiang, X. D., Xue, S., & Ke, Y. Q. (2009). Combination of bone marrow stromal cell transplantation with mobilization by granulocyte-colony stimulating factor promotes functional recovery after spinal cord transection. Acta Neurochirurgica (Wien), 151(11), 1483–1492.

    Google Scholar 

  155. Magnaghi, V., Conte, V., Procacci, P., et al. (2011). Biological performance of a novel biodegradable polyamidoamine hydrogel as guide for peripheral nerve regeneration. Journal of Biomedical Materials Research. Part A, 98(1), 19–30.

    PubMed  Google Scholar 

  156. Liu, T., Xu, J., Chan, B. P., & Chew, S. Y. (2012). Sustained release of neurotrophin-3 and chondroitinase ABC from electrospun collagen nanofiber scaffold for spinal cord injury repair. Journal of Biomedical Materials Research. Part A, 100(1), 236–242.

    PubMed  Google Scholar 

  157. Jain, A., Kim, Y. T., Mckeon, R. J., & Bellamkonda, R. V. (2006). In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury. Biomaterials, 27(3), 497–504.

    CAS  PubMed  Google Scholar 

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Acknowledgments

Authors wish to thank the National Sciences and Engineering Research Council of Canada (NSERC) and New World Laboratories Inc. for their financial support through a Research and Development Collaborative grant.

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Binan, L., Ajji, A., De Crescenzo, G. et al. Approaches for Neural Tissue Regeneration. Stem Cell Rev and Rep 10, 44–59 (2014). https://doi.org/10.1007/s12015-013-9474-z

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