Neural Tissue Engineering (original) (raw)
Abstract
Tissue engineering is the use of engineering methods to replace, replicate, or improve biological tissues. Neural tissue engineering involves the integrated use of biomaterials, cellular engineering, and drug delivery technologies with the purpose of protecting, repairing, or regenerating cells and tissues of the nervous system. Through the introduction of biochemical, topographic, immunomodulatory, and other types of cues, tissues can be therapeutically controlled to direct growth and tissue function in order to overcome biological constraints on tissue repair and regeneration. These strategies can be applied when injury or disease occurs in the brain, spinal cord, for damaged peripheral nerves, or to improve chronic functionality of implantable neural interfaces. In this chapter, we present an overview of neural tissue engineering using examples of therapeutic systems including nerve conduits, implantable hydrogels, delivery of neurotrophic factors and stem cells, genetic approaches to tissue engineering, immunomodulation, and electrical stimulation.
Loading Preview
Sorry, preview is currently unavailable. You can download the paper by clicking the button above.
References (214)
- B. Tasic, Z. Yao, L.T. Graybuck, K.A. Smith, T.N. Nguyen, D. Bertagnolli, J. Goldy, E. Garren, M.N. Economo, S. Viswanathan, O. Penn, T. Bakken, V. Menon, J. Miller, O. Fong, K.E. Hirokawa, K. Lathia, C. Rimorin, M. Tieu, R. Larsen, T. Casper, E. Barkan, M. Kroll, S. Parry, N.V. Shapovalova, D. Hirschstein, J. Pendergraft, H.A. Sullivan, T.K. Kim, A. Szafer, N. Dee, P. Groblewski, I. Wicker- sham, A. Cetin, J.A. Harris, B.P. Levi, S.M. Sunkin, L. Madisen, T.L. Daigle, L. Looger, A. Bernard, J. Phillips, E. Lein, M. Hawrylycz, K. Svoboda, A.R. Jones, C. Koch, H. Zeng, Shared and distinct transcriptomic cell types across neocortical areas. Nature 563, 72-78 (2018)
- C.H. Tischbirek, T. Noda, M. Tohmi, A. Birkner, I. Nelken, A. Konnerth, In vivo functional mapping of a cortical column at single-neuron resolution. Cell Rep. 27(5), 1319-1326 (2019)
- N.J. Abbott, L. Ronnback, E. Hansson, Astrocyte- endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7(1), 41-53 (2006)
- A. Aspelund, S. Antila, S.T. Proulx, T.V. Karlsen, S. Karaman, M. Detmar, H. Wiig, K. Alitalo, A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212(7), 991-999 (2015)
- J.J. Iliff, M. Wang, Y. Liao, B.A. Plogg, W. Peng, G.A. Gundersen, H. Benveniste, G.E. Vates, R. Deane, S.A. Goldman, E.A. Nagelhus, M. Neder- gaard, A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 4(147), 147ra111 (2012)
- A. Louveau, I. Smirnov, T.J. Keyes, J.D. Eccles, S.J. Rouhani, J.D. Peske, N.C. Derecki, D. Castle, J.W. Mandell, K.S. Lee, T.H. Harris, J. Kipnis, Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560), 337 (2015)
- M.V. Sofroniew, Reactive astrocytes in neural re- pair and protection. Neuroscientist 11(5), 400-407 (2005)
- M. Eddleston, L. Mucke, Molecular profile of reac- tive astrocytes-implications for their role in neuro- logic disease. Neuroscience 54(1), 15-36 (1993)
- J. Silver, J.H. Miller, Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5(2), 146-156 (2004)
- J.M. Brown, J. Xia, B. Zhuang, K.S. Cho, C.J. Rogers, C.I. Gama, M. Rawat, S.E. Tully, N. Ue- tani, D.E. Mason, M.L. Tremblay, E.C. Peters, O. Habuchi, D.F. Chen, L.C. Hsieh-Wilson, A sulfated carbohydrate epitope inhibits axon regeneration af- ter injury. Proc. Natl. Acad. Sci. 109(13), 4768-4773 (2012)
- L. Karumbaiah, S. Anand, R. Thazhath, Y. Zhong, R.J. McKeon, R.V. Bellamkonda, Targeted down- regulation of N-acetylgalactosamine 4-sulfate 6- O-sulfotransferase significantly mitigates chon- droitin sulfate proteoglycan-mediated inhibition. Glia 59(6), 981-996 (2011)
- S.E. Tully, R. Mabon, C.I. Gama, S.M. Tsai, X. Liu, L.C. Hsieh-Wilson, A chondroitin sulfate small molecule that stimulates neuronal growth. J. Am. Chem. Soc. 126(25), 7736-7737 (2004)
- A. Nimmerjahn, F. Kirchhoff, F. Helmchen, Rest- ing microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726), 1314-1318 (2005)
- F. Aloisi, Immune function of microglia. Glia 36(2), 165-179 (2001)
- D. Giulian, Ameboid microglia as effectors of in- flammation in the central nervous system. J. Neu- rosci. Res. 18(1), 155-171 (1987). 132-153
- W.J. Streit, M.B. Graeber, G.W. Kreutzberg, Func- tional plasticity of microglia: A review. Glia 1(5), 301-307 (1988)
- R.P. Bunge, M.B. Bunge, Rish, Electron micro- scopic study of demyelination in an experimentally induced lesion in adult cat spinal cord. J. Biophys. Biochem. Cytol. 7, 685-696 (1960)
- M. Bradl, H. Lassmann, Biology and pathology. Acta Neuropathol. 119(1), 37-53 (2010)
- C. French-Constant, J. Camara, Lessons from oligo- dendrocyte biology on promoting repair in multiple sclerosis. J. Neurol. 254, 15-22 (2007)
- I. Glezer, A. Lapointe, S. Rivest, Innate immunity triggers oligodendrocyte progenitor reactivity and confines damages to brain injuries. FASEB J. 20(6), 750-752 (2006)
- V. Bartanusz, D. Jezova, B. Alajajian, M. Digicayli- oglu, The blood-spinal cord barrier: Morphology and clinical implications. Ann. Neurol. 70(2), 194- 206 (2011)
- M.M. Rich, J.W. Lichtman, In vivo visualization of pre-and postsynaptic changes during synapse elim- ination in reinnervated mouse muscle. J. Neurosci. 9(5), 1781-1805 (1989)
- C. Birchmeier, K.A. Nave, Neuregulin-1, a key ax- onal signal that drives Schwann cell growth and differentiation. Glia 56(14), 1491-1497 (2008)
- M. Abercrombie, M.L. Johnson, The outwander- ing of cells in tissue cultures of nerves undergoing Wallerian degeneration. J. Exp. Biol. 19, 266-283 (1942)
- Y.J. Son, W.J. Thompson, Schwann cell processes guide regeneration of peripheral axons. Neuron 14(1), 125-132 (1995)
- M.J. Politis, K. Ederle, P.S. Spencer, Tropism in nerve regeneration in vivo. Attraction of regenerat- ing axons by diffusible factors derived from cells in distal nerve stumps of transected peripheral nerves. Brain Res. 253(1-2), 1-12 (1982)
- C. Ide, K. Tohyama, R. Yokota, T. Nitatori, S. On- odera, Schwann cell basal lamina and nerve regen- eration. Brain Res. 288(1-2), 61-75 (1983)
- A.B. Peterson, L. Xu, J. Daugherty, M.J. Breiding, Surveillance report of traumatic brain injury-related emergency department visits, hospitalizations, and deaths, United States, 2014 (2019)
- C.A. Taylor, J.M. Bell, M.J. Breiding, L. Xu, Trau- matic brain injury-related emergency department visits, hospitalizations, and deaths-United States, 2007 and 2013. MMWR Surveill. Summ. 66(9), 1 (2017)
- C. Werner, K. Engelhard, Pathophysiology of trau- matic brain injury. Br. J. Anaesth. 99(1), 4-9 (2007)
- J.W. Rowland, G.W. Hawryluk, B. Kwon, M.G. Fehlings, Current status of acute spinal cord injury pathophysiology and emerging therapies: Promise on the horizon. Neurosurg. Focus. 25(5), E2 (2008)
- M.T. Filbin, Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4(9), 703-713 (2003)
- Z. He, V. Koprivica, The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27, 341- 368 (2004)
- M.A. Anderson, J.E. Burda, Y. Ren, Y. Ao, T.M. O'Shea, R. Kawaguchi, G. Coppola, B.S. Khakh, T.J. Deming, M.V. Sofroniew, Astrocyte scar forma- tion aids central nervous system axon regeneration. Nature 532(7598), 195 (2016)
- S. Ramón y Cajal, Degeneration and Regeneration of the Nervous System (Oxford University Press, London, 1928)
- S. David, A.J. Aguayo, Axonal elongation into pe- ripheral nervous system "bridges" after central ner- vous system injury in adult rats. Science 214(4523), 931-933 (1981)
- V.J. Tom, M.P. Steinmetz, J.H. Miller, C.M. Doller, J. Silver, Studies on the development and behavior of the dystrophic growth cone, the hallmark of re- generation failure, in an in vitro model of the glial scar and after spinal cord injury. J. Neurosci. 24(29), 6531-6539 (2004)
- J. Noble, C.A. Munro, V.S. Prasad, R. Midha, Anal- ysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. J. Trauma 45(1), 116-122 (1998)
- M.G. Burnett, E.L. Zager, Pathophysiology of pe- ripheral nerve injury: A brief review. Neurosurg. Focus. 16(5), E1 (2004)
- J.A. Kouyoumdjian, Peripheral nerve injuries: A ret- rospective survey of 456 cases. Muscle Nerve 34(6), 785-788 (2006)
- B. Malik, M. Stillman, Chemotherapy-induced pe- ripheral neuropathy. Curr. Pain Headache Rep. 12(3), 165-174 (2008)
- A. Hartemann, N. Attal, D. Bouhassira, I. Dumont, H. Gin, S. Jeanne, G. Said, J.L. Richard, Painful diabetic neuropathy: Diagnosis and management. Diabetes Metab. 37(5), 377-388 (2011)
- H.J. Seddon, Three types of brain injury. Brain 66, 237-288 (1943)
- V. Mukhatyar, L. Karumbaiah, J. Yeh, R. Bel- lamkonda, Tissue engineering strategies designed to facilitate the endogenous regenerative potential of peripheral nerves. Adv. Mater. 21(46), 4670-4679 (2009)
- R.P. Bunge, Expanding roles for the Schwann cell: Ensheathment, myelination, trophism and re- generation. Curr. Opin. Neurobiol. 3(5), 805-809 (1993)
- J.L. Salzer, R.P. Bunge, Studies of Schwann cell pro- liferation. I. an analysis in tissue culture of prolifer- ation during development, Wallerian degeneration, and direct injury. J. Cell Biol. 84(3), 739-752 (1980)
- F.J. Vingerhoets, J.G. Villemure, P. Temperli, C. Pollo, E. Pralong, J. Ghika, Subthalamic DBS re- places levodopa in Parkinson's disease: Two-year follow-up. Neurology 58(3), 396-401 (2002)
- T.D. Kozai, A.S. Jaquins-Gerstl, A.L. Vazquez, A.C. Michael, X.T. Cui, Brain tissue responses to neural implants impact signal sensitivity and intervention strategies. ACS Chem. Neurosci. 6(1), 48-67 (2015)
- T. Saxena, L. Karumbaiah, E.A. Gaupp, R. Patkar, K. Patil, M. Betancur, G.B. Stanley, R.V. Bel- lamkonda, The impact of chronic blood-brain bar- rier breach on intracortical electrode function. Bio- materials 34(20), 4703-4713 (2013)
- W. Shen, L. Karumbaiah, X. Liu, T. Saxena, S. Chen, R. Patkar, R.V. Bellamkonda, M.G. Allen, Extracellular matrix-based intracortical microelec- trodes: Toward a microfabricated neural interface based on natural materials. Microsyst. Nanoeng. 1, 15010 (2015)
- G. Lundborg, R.H. Gelberman, F.M. Longo, H.C. Powell, S. Varon, In vivo regeneration of cut nerves encased in silicone tubes: Growth across a six- millimeter gap. J. Neuropathol. Exp. Neurol. 41(4), 412-422 (1982)
- Z.L. Shen, F. Lassner, M. Becker, G.F. Walter, A. Bader, A. Berger, Viability of cultured nerve grafts: An assessment of proliferation of Schwann cells and fibroblasts. Microsurgery 19(8), 356-363 (1999)
- L.J. Chamberlain, I.V. Yannas, A. Arrizabalaga, H.P. Hsu, T.V. Norregaard, M. Spector, Early peripheral nerve healing in collagen and silicone tube implants: Myofibroblasts and the cellular response. Biomate- rials 19(15), 1393-1403 (1998a)
- L.J. Chamberlain, I.V. Yannas, H.P. Hsu, G. Strichartz, M. Spector, Collagen-GAG substrate en- hances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp. Neurol. 154(2), 315-329 (1998b)
- S.T. Li, S.J. Archibald, C. Krarup, R.D. Madison, Peripheral nerve repair with collagen conduits. Clin. Mater. 9(3-4), 195-200 (1992)
- A. Bozkurt, R. Deumens, C. Beckmann, L. Olde Damink, F. Schugner, I. Heschel, B. Sellhaus, J. Weis, W. Jahnen-Dechent, G.A. Brook, N. Pallua, In vitro cell alignment obtained with a Schwann cell enriched microstructured nerve guide with longitu- dinal guidance channels. Biomaterials 30(2), 169- 179 (2009)
- L. Ghasemi-Mobarakeh, M.P. Prabhakaran, M. Mor- shed, M.H. Nasr-Esfahani, S. Ramakrishna, Elec- trospun poly(epsilon-caprolactone)/gelatin nanofi- brous scaffolds for nerve tissue engineering. Bioma- terials 29(34), 4532-4539 (2008)
- T.J. Galla, S.V. Vedecnik, J. Halbgewachs, S. Stein- mann, C. Friedrich, G.B. Stark, Fibrin/Schwann cell matrix in poly-epsilon-caprolactone conduits enhances guided nerve regeneration. Int. J. Artif. Organs 27(2), 127-136 (2004)
- D.F. Kalbermatten, P.J. Kingham, D. Mahay, C. Mantovani, J. Pettersson, W. Raffoul, H. Balcin, G. Pierer, G. Terenghi, Fibrin matrix for suspension of regenerative cells in an artificial nerve conduit. J. Plast. Reconstr. Aesthet. Surg. 61(6), 669-675 (2008)
- D.F. Kalbermatten, J. Pettersson, P.J. Kingham, G. Pierer, M. Wiberg, G. Terenghi, New fibrin conduit for peripheral nerve repair. J. Reconstr. Microsurg. 25(1), 27-33 (2009)
- A.P. Balgude, X. Yu, A. Szymanski, R.V. Bel- lamkonda, Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 22(10), 1077-1084 (2001)
- G.P. Dillon, X. Yu, A. Sridharan, J.P. Ranieri, R.V. Bellamkonda, The influence of physical structure and charge on neurite extension in a 3D hydrogel scaffold. J. Biomater. Sci. Polym. Ed. 9(10), 1049- 1069 (1998)
- M.C. Dodla, R.V. Bellamkonda, Differences be- tween 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 (2008)
- R.O. Labrador, M. Buti, X. Navarro, Peripheral nerve repair: Role of agarose matrix density on functional recovery. Neuroreport 6(15), 2022-2026 (1995)
- S. Amado, M.J. Simoes, P.A. Armada da Silva, A.L. Luis, Y. Shirosaki, M.A. Lopes, J.D. Santos, F. Freg- nan, G. Gambarotta, S. Raimondo, M. Fornaro, A.P. Veloso, A.S. Varejao, A.C. Mauricio, S. Geuna, Use of hybrid chitosan membranes and N1E-115 cells for promoting nerve regeneration in an axonotmesis rat model. Biomaterials 29(33), 4409-4419 (2008)
- M.E. Chavez-Delgado, J. Mora-Galindo, U. Gomez- Pinedo, A. Feria-Velasco, S. Castro-Castaneda, F.A. Lopez-Dellamary Toral, S. Luquin-De Anda, L.M. Garcia-Segura, J. Garcia-Estrada, Facial nerve re- generation through progesterone-loaded chitosan prosthesis. A preliminary report. J Biomed Mater Res B Appl Biomater 67(2), 702-711 (2003)
- M. Patel, L. Mao, B. Wu, P. VandeVord, GDNF blended chitosan nerve guides: An in vivo study. J. Biomed. Mater. Res. A 90(1), 154-165 (2009)
- A. Mosahebi, M. Simon, M. Wiberg, G. Terenghi, A novel use of alginate hydrogel as Schwann cell matrix. Tissue Eng. 7(5), 525-534 (2001)
- Y. Sakai, Y. Matsuyama, K. Takahashi, T. Sato, T. Hattori, S. Nakashima, N. Ishiguro, New arti- ficial nerve conduits made with photocrosslinked hyaluronic acid for peripheral nerve regeneration. Biomed. Mater. Eng. 17(3), 191-197 (2007)
- B.R. Seckel, D. Jones, K.J. Hekimian, K.K. Wang, D.P. Chakalis, P.D. Costas, Hyaluronic acid through a new injectable nerve guide delivery system en- hances peripheral nerve regeneration in the rat. J. Neurosci. Res. 40(3), 318-324 (1995)
- P. Aebischer, V. Guenard, S.R. Winn, R.F. Valentini, P.M. Galletti, Blind-ended semipermeable guidance channels support peripheral nerve regeneration in the absence of a distal nerve stump. Brain Res. 454(1-2), 179-187 (1988)
- S. Atzet, S. Curtin, P. Trinh, S. Bryant, B. Ratner, Degradable poly(2-hydroxyethyl methacrylate)-co- polycaprolactone hydrogels for tissue engineering scaffolds. Biomacromolecules 9(12), 3370-3377 (2008)
- Y.T. Kim, V.K. Haftel, S. Kumar, R.V. Bellamkonda, The role of aligned polymer fiber-based constructs in the bridging of long peripheral nerve gaps. Bio- materials 29(21), 3117-3127 (2008)
- I.P. Clements, Y.T. Kim, A.W. English, X. Lu, A. Chung, R.V. Bellamkonda, Thin-film enhanced nerve guidance channels for peripheral nerve repair. Biomaterials 30(23-24), 3834-3846 (2009)
- D.M. Thompson, H.M. Buettner, Oriented Schwann cell monolayers for directed neurite outgrowth. Ann. Biomed. Eng. 32(8), 1120-1130 (2004)
- D.J. Bryan, J.B. Tang, A.H. Holway, K.M. Rieger- Christ, D.J. Trantolo, D.L. Wise, I.C. Summerhayes, Enhanced peripheral nerve regeneration elicited by cell-mediated events delivered via a bioresorbable PLGA guide. J. Reconstr. Microsurg. 19(2), 125- 134 (2003)
- W.F. Den Dunnen, B. Van der Lei, J.M. Schaken- raad, E.H. Blaauw, I. Stokroos, A.J. Pennings, P.H. Robinson, Long-term evaluation of nerve regenera- tion in a biodegradable nerve guide. Microsurgery 14(8), 508-515 (1993)
- G.R. Evans, K. Brandt, M.S. Widmer, L. Lu, R.K. Meszlenyi, P.K. Gupta, A.G. Mikos, J. Hodges, J. Williams, A. Gurlek, A. Nabawi, R. Lohman, C.W. Patrick Jr., In vivo evaluation of poly (L-lactic acid) porous conduits for peripheral nerve regeneration. Biomaterials 20(12), 1109-1115 (1999)
- H. Molander, Y. Olsson, O. Engkvist, S. Bowald, I. Eriksson, Regeneration of peripheral nerve through a polyglactin tube. Muscle Nerve 5(1), 54-57 (1982)
- A. Valero-Cabre, K. Tsironis, E. Skouras, G. Perego, X. Navarro, W.F. Neiss, Superior muscle reinnerva- tion after autologous nerve graft or poly-L-lactide- epsilon-caprolactone (PLC) tube implantation in comparison to silicone tube repair. J. Neurosci. Res. 63(2), 214-223 (2001)
- D. Pankajakshan, L.P. Philipose, M. Palakkal, K. Krishnan, L.K. Krishnan, Development of a fibrin composite-coated poly(epsilon-caprolactone) scaf- fold for potential vascular tissue engineering appli- cations. J Biomed Mater Res B Appl Biomater 87(2), 570-579 (2008)
- A.K. Ekaputra, G.D. Prestwich, S.M. Cool, D.W. Hutmacher, Combining electrospun scaffolds with electrosprayed hydrogels leads to three-dimensional cellularization of hybrid constructs. Biomacro- molecules 9(8), 2097-2103 (2008)
- S. Panseri, C. Cunha, J. Lowery, U. Del Carro, F. Taraballi, S. Amadio, A. Vescovi, F. Gelain, Elec- trospun micro-and nanofiber tubes for functional nervous regeneration in sciatic nerve transections. BMC Biotechnol. 8, 39 (2008)
- M.P. Prabhakaran, J.R. Venugopal, T.T. Chyan, L.B. Hai, C.K. Chan, A.Y. Lim, S. Ramakrishna, Electro- spun biocomposite nanofibrous scaffolds for neural tissue engineering. Tissue Eng. Part A 14(11), 1787- 1797 (2008)
- C.M. Valmikinathan, J. Tian, J. Wang, X. Yu, Novel nanofibrous spiral scaffolds for neural tissue engi- neering. J. Neural Eng. 5(4), 422-432 (2008)
- E.L. Whitlock, S.H. Tuffaha, J.P. Luciano, Y. Yan, D.A. Hunter, C.K. Magill, A.M. Moore, A.Y. Tong, S.E. Mackinnon, G.H. Borschel, Processed allo- grafts and type I collagen conduits for repair of peripheral nerve gaps. Muscle Nerve 39(6), 787-799 (2009)
- A. Jain, Y.T. Kim, R.J. McKeon, R.V. Bellamkonda, 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 (2006)
- Y. Zhong, R.V. Bellamkonda, Biomaterials for the central nervous system. J. R. Soc. Interface 5(26), 957-975 (2008)
- S. Carbonetto, M.M. Gruver, D.C. Turner, Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J. Neurosci. 3(11), 2324-2335 (1983)
- J.M. Thompson, D.J. Pelto, Attachment, survival and neurite extension of chick embryo retinal neu- rons on various culture substrates. Dev. Neurosci. 5(5-6), 447-457 (1982)
- E.A. Joosten, P.R. Bar, W.H. Gispen, Collagen im- plants and cortico-spinal axonal growth after mid- thoracic spinal cord lesion in the adult rat. J. Neu- rosci. Res. 41(4), 481-490 (1995)
- D.A. Houweling, A.J. Lankhorst, W.H. Gispen, P.R. Bar, E.A. Joosten, Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp. Neurol. 153(1), 49-59 (1998a)
- D.A. Houweling, J.T. van Asseldonk, A.J. Lankhorst, F.P. Hamers, D. Martin, P.R. Bar, E.A. Joosten, Local application of collagen containing brain-derived neurotrophic factor decreases the loss of function after spinal cord injury in the adult rat. Neurosci. Lett. 251(3), 193-196 (1998b)
- M.C. Jimenez Hamann, C.H. Tator, M.S. Shoichet, Injectable intrathecal delivery system for localized administration of EGF and FGF-2 to the injured rat spinal cord. Exp. Neurol. 194(1), 106-119 (2005)
- D. Gupta, C.H. Tator, M.S. Shoichet, Fast-gelling in- jectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 27(11), 2370-2379 (2006)
- W.M. Tian, S.P. Hou, J. Ma, C.L. Zhang, Q.Y. Xu, I.S. Lee, H.D. Li, M. Spector, F.Z. Cui, Hyaluronic acid-poly-D-lysine-based three-dimensional hydro- gel for traumatic brain injury. Tissue Eng. 11(3-4), 513-525 (2005)
- R. Bellamkonda, J.P. Ranieri, P. Aebischer, Laminin oligopeptide derivatized agarose gels allow three- dimensional neurite extension in vitro. J. Neurosci. Res. 41(4), 501-509 (1995a)
- R. Bellamkonda, J.P. Ranieri, N. Bouche, P. Aebis- cher, Hydrogel-based three-dimensional matrix for neural cells. J. Biomed. Mater. Res. 29(5), 663-671 (1995b)
- X. Yu, G.P. Dillon, R.B. Bellamkonda, A laminin and nerve growth factor-laden three-dimensional scaffold for enhanced neurite extension. Tissue Eng. 5(4), 291-304 (1999)
- H. Lee, R.J. McKeon, R.V. Bellamkonda, Sustained delivery of thermostabilized chABC enhances ax- onal sprouting and functional recovery after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 107(8), 3340-3345 (2010)
- A. Jain, R.J. McKeon, S.M. Brady-Kalnay, R.V. Bel- lamkonda, Sustained delivery of activated rho GT- Pases and BDNF promotes axon growth in CSPG- rich regions following spinal cord injury. PLoS One 6(1), e16135 (2011)
- F.H. Hausheer, R.L. Schilsky, S. Bain, E.J. Berghorn, F. Lieberman, Diagnosis, management, and evaluation of chemotherapy-induced peripheral neuropathy. Semin. Oncol. 33(1), 15-49 (2006)
- S. Koutsopoulos, L.D. Unsworth, Y. Nagai, S. Zhang, Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold. Proc. Natl. Acad. Sci. U. S. A. 106(12), 4623-4628 (2009)
- H. Cao, T. Liu, S.Y. Chew, The application of nanofi- brous scaffolds in neural tissue engineering. Adv. Drug Deliv. Rev. 61(12), 1055-1064 (2009)
- A.E. Wurmser, K. Nakashima, R.G. Summers, N. Toni, K.A. D'Amour, D.C. Lie, F.H. Gage, Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 430(6997), 350-356 (2004)
- Y. Ziv, H. Avidan, S. Pluchino, G. Martino, M. Schwartz, Synergy between immune cells and adult neural stem/progenitor cells promotes functional re- covery from spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 103(35), 13174-13179 (2006)
- R.G. Ellis-Behnke, Y.X. Liang, S.W. You, D.K. Tay, S. Zhang, K.F. So, G.E. Schneider, Nano neuro knit- ting: Peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc. Natl. Acad. Sci. 103(13), 5054-5059 (2006)
- J. Guo, H. Su, Y. Zeng, Y.X. Liang, W.M. Wong, R.G. Ellis-Behnke, K.F. So, W. Wu, Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold. Nanomedicine 3(4), 311-321 (2007)
- V.M. Tysseling-Mattiace, V. Sahni, K.L. Niece, D. Birch, C. Czeisler, M.G. Fehlings, S.I. Stupp, J.A. Kessler, Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J. Neurosci. 28(14), 3814-3823 (2008)
- E.C. Tsai, P.D. Dalton, M.S. Shoichet, C.H. Tator, Synthetic hydrogel guidance channels facilitate re- generation of adult rat brainstem motor axons after complete spinal cord transection. J. Neurotrauma 21(6), 789-804 (2004)
- Y. Katayama, R. Montenegro, T. Freier, R. Midha, J.S. Belkas, M.S. Shoichet, Coil-reinforced hydrogel tubes promote nerve regeneration equivalent to that of nerve autografts. Biomaterials 27(3), 505-518 (2006)
- S. Woerly, E. Pinet, L. De Robertis, M. Bousmina, G. Laroche, T. Roitback, L. Vargova, E. Sykova, Heterogeneous PHPMA hydrogels for tissue repair and axonal regeneration in the injured spinal cord. J. Biomater. Sci. Polym. Ed. 9(7), 681-711 (1998)
- F.Z. Cui, W.M. Tian, Y.W. Fan, S.P. Hou, Q.Y. Xu, I.S. Lee, Cerebrum repair with PHPMA hydro- gel immobilized with neurite-promoting peptides in traumatic brain injury of adult rat model. J. Bioact. Compat. Polym. 18, 413-432 (2003)
- S. Woerly, E. Pinet, L. de Robertis, D. Van Diep, M. Bousmina, Spinal cord repair with PHPMA hydro- gel containing RGD peptides (NeuroGel). Biomate- rials 22(10), 1095-1111 (2001)
- D. Mortisen, M. Peroglio, M. Alini, D. Eglin, Tai- loring thermoreversible hyaluronan hydrogels by "click" chemistry and RAFT polymerization for cell and drug therapy. Biomacromolecules 11(5), 1261- 1272 (2010)
- N. Comolli, B. Neuhuber, I. Fischer, A. Lowman, In vitro analysis of PNIPAAm-PEG, a novel, injectable scaffold for spinal cord repair. Acta Biomater. 5(4), 1046-1055 (2009)
- L.L. Jones, M. Oudega, M.B. Bunge, M.H. Tuszyn- ski, Neurotrophic factors, cellular bridges and gene therapy for spinal cord injury. J. Physiol. 533(Pt 1), 83-89 (2001)
- C.E. Schmidt, J.B. Leach, Neural tissue engineering: Strategies for repair and regeneration. Annu. Rev. Biomed. Eng. 5, 293-347 (2003)
- R. Heumann, D. Lindholm, C. Bandtlow, M. Meyer, M.J. Radeke, T.P. Misko, E. Shooter, H. Thoenen, Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve dur- ing development, degeneration, and regeneration: Role of macrophages. Proc. Natl. Acad. Sci. U. S. A. 84(23), 8735-8739 (1987)
- Y. Murakami, S. Furukawa, A. Nitta, Y. Furukawa, Accumulation of nerve growth factor protein at both rostral and caudal stumps in the transected rat spinal cord. J. Neurol. Sci. 198(1-2), 63-69 (2002)
- M. Oudega, T. Hagg, Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp. Neurol. 140(2), 218-229 (1996)
- J. Bloch, E.G. Fine, N. Bouche, A.D. Zurn, P. Ae- bischer, Nerve growth factor-and neurotrophin-3- releasing guidance channels promote regeneration of the transected rat dorsal root. Exp. Neurol. 172(2), 425-432 (2001)
- M.S. Ramer, J.V. Priestley, S.B. McMahon, Func- tional regeneration of sensory axons into the adult spinal cord. Nature 403(6767), 312-316 (2000)
- E.G. Fine, I. Decosterd, M. Papaloizos, A.D. Zurn, P. Aebischer, GDNF and NGF released by synthetic guidance channels support sciatic nerve regenera- tion across a long gap. Eur. J. Neurosci. 15(4), 589- 601 (2002)
- I.H. Whitworth, R.A. Brown, C.J. Dore, P. Anand, C.J. Green, G. Terenghi, Nerve growth factor enhances nerve regeneration through fibronectin grafts. J. Hand Surg. (Br.) 21(4), 514-522 (1996)
- N.R. Krenz, S.O. Meakin, A.V. Krassioukov, L.C. Weaver, Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury. J. Neurosci. 19(17), 7405-7414 (1999)
- M.I. Romero, N. Rangappa, M.G. Garry, G.M. Smith, Functional regeneration of chronically in- jured sensory afferents into adult spinal cord af- ter neurotrophin gene therapy. J. Neurosci. 21(21), 8408-8416 (2001)
- S. Braun, B. Croizat, M.C. Lagrange, J.M. Warter, P. Poindron, Neurotrophins increase motoneurons' ability to innervate skeletal muscle fibers in rat spinal cord-human muscle cocultures. J. Neurol. Sci. 136(1-2), 17-23 (1996)
- C.E. Henderson, W. Camu, C. Mettling, A. Gouin, K. Poulsen, M. Karihaloo, J. Rullamas, T. Evans, S.B. McMahon, M.P. Armanini, et al., Neu- rotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363(6426), 266-270 (1993)
- R. Grill, K. Murai, A. Blesch, F.H. Gage, M.H. Tuszynski, Cellular delivery of neurotrophin-3 pro- motes corticospinal axonal growth and partial func- tional recovery after spinal cord injury. J. Neurosci. 17(14), 5560-5572 (1997a)
- K.M. Giehl, W. Tetzlaff, BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corti- cospinal neurons in vivo. Eur. J. Neurosci. 8(6), 1167-1175 (1996)
- Q. Yin, G.J. Kemp, L.G. Yu, S.C. Wagstaff, S.P. Fro- stick, Neurotrophin-4 delivered by fibrin glue pro- motes peripheral nerve regeneration. Muscle Nerve 24(3), 345-351 (2001)
- M. Sendtner, P. Carroll, B. Holtmann, R.A. Hughes, H. Thoenen, Ciliary neurotrophic factor. J. Neuro- biol. 25(11), 1436-1453 (1994)
- N.M. Oyesiku, J.N. Wilcox, D.J. Wigston, Changes in expression of ciliary neurotrophic factor (CNTF) and CNTF-receptor alpha after spinal cord injury. J. Neurobiol. 32(3), 251-261 (1997)
- J.H. Ye, J.D. Houle, Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neu- rons. Exp. Neurol. 143(1), 70-81 (1997)
- J.P. Newman, A.N. Verity, S. Hawatmeh, W.E. Fee Jr., D.J. Terris, Ciliary neurotrophic factors enhances peripheral nerve regeneration. Arch. Otolaryngol. Head Neck Surg. 122(4), 399-403 (1996)
- M. Sendtner, G.W. Kreutzberg, H. Thoenen, Ciliary neurotrophic factor prevents the degeneration of mo- tor neurons after axotomy. Nature 345(6274), 440- 441 (1990)
- S.W. Levison, M.H. Ducceschi, G.M. Young, T.L. Wood, Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp. Neu- rol. 141(2), 256-268 (1996)
- C.G. Winter, Y. Saotome, S.W. Levison, D. Hirsh, A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 92(13), 5865-5869 (1995)
- J.V. Priestley, M.S. Ramer, V.R. King, S.B. McMa- hon, R.A. Brown, Stimulating regeneration in the damaged spinal cord. J. Physiol. Paris 96(1-2), 123- 133 (2002)
- A. Buj-Bello, V.L. Buchman, A. Horton, A. Rosen- thal, A.M. Davies, GDNF is an age-specific survival factor for sensory and autonomic neurons. Neuron 15(4), 821-828 (1995)
- C.E. Henderson, H.S. Phillips, R.A. Pollock, A.M. Davies, C. Lemeulle, M. Armanini, L. Simmons, B. Moffet, R.A. Vandlen, L.C. Simpson, et al., GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266(5187), 1062-1064 (1994)
- J. Altman, G.D. Das, Autoradiographic and histo- logical evidence of postnatal hippocampal neuro- genesis in rats. J. Comp. Neurol. 124(3), 319-335 (1965)
- J. Altman, Autoradiographic and histological stud- ies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137(4), 433-457 (1969)
- B.A. Reynolds, S. Weiss, Generation of neurons and astrocytes from isolated cells of the adult mam- malian central nervous system. Science 255(5052), 1707-1710 (1992)
- L.J. Richards, T.J. Kilpatrick, P.F. Bartlett, De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. U. S. A. 89(18), 8591- 8595 (1992)
- J.G. Emsley, B.D. Mitchell, S.S. Magavi, P. Arlotta, J.D. Macklis, The repair of complex neuronal cir- cuitry by transplanted and endogenous precursors. NeuroRx 1(4), 452-471 (2004)
- J.W. McDonald, X.Z. Liu, Y. Qu, S. Liu, S.K. Mickey, D. Turetsky, D.I. Gottlieb, D.W. Choi, Transplanted embryonic stem cells survive, differen- tiate and promote recovery in injured rat spinal cord. Nat. Med. 5(12), 1410-1412 (1999)
- F. Erdo, C. Buhrle, J. Blunk, M. Hoehn, Y. Xia, B. Fleischmann, M. Focking, E. Kustermann, E. Kolossov, J. Hescheler, K.A. Hossmann, T. Trapp, Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J. Cereb. Blood Flow Metab. 23(7), 780-785 (2003)
- Q. Cao, R.L. Benton, S.R. Whittemore, Stem cell repair of central nervous system injury. J. Neurosci. Res. 68(5), 501-510 (2002)
- M. Romero-Ramos, P. Vourc'h, H.E. Young, P.A. Lucas, Y. Wu, O. Chivatakarn, R. Zaman, N. Dunkelman, M.A. el-Kalay, M.F. Chesselet, Neu- ronal differentiation of stem cells isolated from adult muscle. J. Neurosci. Res. 69(6), 894-907 (2002)
- J.R. Sanchez-Ramos, Neural cells derived from adult bone marrow and umbilical cord blood. J. Neurosci. 69(6), 880-893 (2002)
- R. Galli, A. Gritti, L. Bonfanti, A.L. Vescovi, Neural stem cells: An overview. Circ. Res. 92(6), 598-608 (2003)
- T. Vierbuchen, A. Ostermeier, Z.P. Pang, Y. Kokubu, T.C. Südhof, M. Wernig, Direct conversion of fi- broblasts to functional neurons by defined factors. Nature 463(7284), 1035 (2010)
- Z. Guo, L. Zhang, Z. Wu, Y. Chen, F. Wang, G. Chen, In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model. Cell Stem Cell 14(2), 188-202 (2014)
- W. Niu, T. Zang, Y. Zou, S. Fang, D.K. Smith, R. Bachoo, C.L. Zhang, In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat. Cell Biol. 15(10), 1164 (2013)
- U. Pfisterer, A. Kirkeby, O. Torper, J. Wood, J. Nelander, A. Dufour, A. Björklunder, O. Lindvall, J. Jakobsson, M. Parmar, Direct conversion of hu- man fibroblasts to dopaminergic neurons. Proc. Natl. Acad. Sci. 108(25), 10343-10348 (2011)
- O. Torper, U. Pfisterer, D.A. Wolf, M. Pereira, S. Lau, J. Jakobsson, A. Björklund, S. Grealish, M. Parmar, Generation of induced neurons via direct conversion in vivo. Proc. Natl. Acad. Sci. 110(17), 7038-7043 (2013)
- M.M. Dong, T.H. Yi, Stem cell and peripheral nerve injury and repair. Facial Plast. Surg. 26(5), 421-427 (2010)
- H.S. Keirstead, T. Ben-Hur, B. Rogister, M.T. O'Leary, M. Dubois-Dalcq, W.F. Blakemore, Polysialylated neural cell adhesion molecule- positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J. Neurosci. 19(17), 7529-7536 (1999)
- J. Yan, L. Xu, A.M. Welsh, G. Hatfield, T. Hazel, K. Johe, V.E. Koliatsos, Extensive neuronal differenti- ation of human neural stem cell grafts in adult rat spinal cord. PLoS Med. 4(2), e39 (2007)
- Y.D. Teng, E.B. Lavik, X. Qu, K.I. Park, J. Ourednik, D. Zurakowski, R. Langer, E.Y. Snyder, Functional recovery following traumatic spinal cord injury me- diated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. U. S. A. 99(5), 3024-3029 (2002)
- H. Ohtaki, J.H. Ylostalo, J.E. Foraker, A.P. Robin- son, R.L. Reger, S. Shioda, D.J. Prockop, Stem/pro- genitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflam- matory/immune responses. Proc. Natl. Acad. Sci. U. S. A. 105(38), 14638-14643 (2008)
- M.I. Betancur, H.D. Mason, M. Alvarado-Velez, P.V. Holmes, R.V. Bellamkonda, L. Karumbaiah, Chon- droitin sulfate glycosaminoglycan matrices promote neural stem cell maintenance and neuroprotection post-traumatic brain injury. ACS Biomater Sci. Eng. 3(3), 420-430 (2017)
- Y.C. Wang, Y.T. Wu, H.Y. Huang, H.I. Lin, L.W. Lo, S.F. Tzeng, C.S. Yang, Sustained intraspinal delivery of neurotrophic factor encapsulated in biodegrad- able nanoparticles following contusive spinal cord injury. Biomaterials 29(34), 4546-4553 (2008)
- A. Blesch, P. Lu, M.H. Tuszynski, Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res. Bull. 57(6), 833-838 (2002)
- R.J. Grill, A. Blesch, M.H. Tuszynski, Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF- secreting cells. Exp. Neurol. 148(2), 444-452 (1997b)
- M.H. Tuszynski, K. Gabriel, F.H. Gage, S. Suhr, S. Meyer, A. Rosetti, Nerve growth factor delivery by gene transfer induces differential outgrowth of sen- sory, motor, and noradrenergic neurites after adult spinal cord injury. Exp. Neurol. 137(1), 157-173 (1996)
- M.H. Tuszynski, D.A. Peterson, J. Ray, A. Baird, Y. Nakahara, F.H. Gage, Fibroblasts genetically mod- ified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord. Exp. Neurol. 126(1), 1-14 (1994)
- P. Lu, A. Blesch, M.H. Tuszynski, Neurotrophism without neurotropism: BDNF promotes survival but not growth of lesioned corticospinal neurons. J. Comp. Neurol. 436(4), 456-470 (2001)
- L.B. Jakeman, P. Wei, Z. Guan, B.T. Stokes, Brain- derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp. Neurol. 154(1), 170-184 (1998)
- D.M. McTigue, P.J. Horner, B.T. Stokes, F.H. Gage, Neurotrophin-3 and brain-derived neurotrophic fac- tor induce oligodendrocyte proliferation and myeli- nation of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18(14), 5354-5365 (1998)
- P. Menei, C. Montero-Menei, S.R. Whittemore, R.P. Bunge, M.B. Bunge, Schwann cells genetically
- J.S. Shumsky, C.A. Tobias, M. Tumolo, W.D. Long, S.F. Giszter, M. Murray, Delayed transplantation of fibroblasts genetically modified to secrete BDNF and NT-3 into a spinal cord injury site is associ- ated with limited recovery of function. Exp. Neurol. 184(1), 114-130 (2003)
- A. Blesch, J.M. Conner, M.H. Tuszynski, Modula- tion of neuronal survival and axonal growth in vivo by tetracycline-regulated neurotrophin expression. Gene Ther. 8(12), 954-960 (2001)
- A. Blesch, M.H. Tuszynski, Cellular GDNF deliv- ery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination. J. Comp. Neurol. 467(3), 403-417 (2003)
- A. Hofmann, G.P. Nolan, H.M. Blau, Rapid retro- viral delivery of tetracycline-inducible genes in a single autoregulatory cassette. Proc. Natl. Acad. Sci. U. S. A. 93(11), 5185-5190 (1996)
- A. Blesch, M.H. Tuszynski, GDNF gene delivery to injured adult CNS motor neurons promotes ax- onal growth, expression of the trophic neuropeptide CGRP, and cellular protection. J. Comp. Neurol. 436(4), 399-410 (2001)
- A. Blesch, M.H. Tuszynski, Transient growth factor delivery sustains regenerated axons after spinal cord injury. J. Neurosci. 27(39), 10535-10545 (2007)
- M. Berry, L. Barrett, L. Seymour, A. Baird, A. Lo- gan, Gene therapy for central nervous system repair. Curr. Opin. Mol. Ther. 3(4), 338-349 (2001a)
- M.A. Barry, W.J. Dower, S.A. Johnston, Toward cell-targeting gene therapy vectors: Selection of cell- binding peptides from random peptide-presenting phage libraries. Nat. Med. 2(3), 299-305 (1996)
- M. Berry, A.M. Gonzalez, W. Clarke, L. Greenlees, L. Barrett, W. Tsang, L. Seymour, J. Bonadio, A. Logan, A. Baird, Sustained effects of gene-activated matrices after CNS injury. Mol. Cell. Neurosci. 17(4), 706-716 (2001b)
- P.A. Dijkhuizen, W.T. Hermens, M.A. Teunis, J. Ver- haagen, Adenoviral vector-directed expression of neurotrophin-3 in rat dorsal root ganglion explants results in a robust neurite outgrowth response. J. Neurobiol. 33(2), 172-184 (1997)
- C. Gravel, R. Gotz, A. Lorrain, M. Sendtner, Ade- noviral gene transfer of ciliary neurotrophic factor and brain-derived neurotrophic factor leads to long- term survival of axotomized motor neurons. Nat. Med. 3(7), 765-770 (1997)
- W.T. Hermens, R.J. Giger, A.J. Holtmaat, P.A. Di- jkhuizen, D.A. Houweling, J. Verhaagen, Transient gene transfer to neurons and glia: Analysis of ade- noviral vector performance in the CNS and PNS. J. Neurosci. Methods 71(1), 85-98 (1997)
- H.J. Federoff, M.D. Geschwind, A.I. Geller, J.A. Kessler, Expression of nerve growth factor in vivo from a defective herpes simplex virus 1 vector pre- vents effects of axotomy on sympathetic ganglia. Proc. Natl. Acad. Sci. U. S. A. 89(5), 1636-1640 (1992)
- M. Yamada, A. Natsume, M. Mata, T. Oligino, J. Goss, J. Glorioso, D.J. Fink, Herpes simplex virus vector-mediated expression of Bcl-2 protects spinal motor neurons from degeneration following root avulsion. Exp. Neurol. 168(2), 225-230 (2001)
- P.D. Robbins, S.C. Ghivizzani, Viral vectors for gene therapy. Pharmacol. Ther. 80(1), 35-47 (1998)
- J.H. Kordower, J. Bloch, S.Y. Ma, Y. Chu, S. Palfi, B.Z. Roitberg, M. Emborg, P. Hantraye, N. Deglon, P. Aebischer, Lentiviral gene transfer to the non- human primate brain. Exp. Neurol. 160(1), 1-16 (1999)
- L. Naldini, U. Blomer, F.H. Gage, D. Trono, I.M. Verma, Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 93(21), 11382-11388 (1996)
- M. Shimamura, R. Morishita, M. Endoh, K. Os- hima, M. Aoki, S. Waguri, Y. Uchiyama, Y. Kaneda, HVJ-envelope vector for gene transfer into central nervous system. Biochem. Biophys. Res. Commun. 300(2), 464-471 (2003)
- G. Murlidharan, K. Sakamoto, L. Rao, T. Corriher, D. Wang, G. Gao, P. Sullivan, A. Asokan, CNS- restricted transduction and CRISPR/Cas9-mediated gene deletion with an engineered AAV vector. Mol. Ther.-Nucleic Acids 5, e338 (2016)
- N. Mokarram, A. Merchant, V. Mukhatyar, G. Patel, R.V. Bellamkonda, Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials 33, 8793-8801 (2012)
- N. Mokarram, K. Dymanus, A. Srinivasan, J.G. Lyon, J. Tipton, J. Chu, A.W. English, R.V. Bel- lamkonda, Immunoengineering nerve repair. Proc. Natl. Acad. Sci. 114(26), E5077-E5084 (2017)
- N.M. Geremia, T. Gordon, T.M. Brushart, A.A. Al- Majed, V.M. Verge, Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Exp. Neurol. 205(2), 347-359 (2007)
- T. Gordon, E. Udina, V.M. Verge, E.I. de Chaves, Brief electrical stimulation accelerates axon regen- eration in the peripheral nervous system and pro- motes sensory axon regeneration in the central ner- vous system. Mot. Control. 13(4), 412-441 (2009)
- O. Steward, E.M. Schuman, Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299-325 (2001)
- W.M. Grill, M.D. Craggs, R.D. Foreman, C.L. Lud- low, J.L. Buller, Emerging clinical applications of electrical stimulation: Opportunities for restoration of function. J. Rehabil. Res. Dev. 38(6), 641-653 (2001a)
- W.M. Grill, J.W. McDonald, P.H. Peckham, W. Heetderks, J. Kocsis, M. Weinrich, At the interface: Convergence of neural regeneration and neural pros- theses for restoration of function. J. Rehabil. Res. Dev. 38(6), 633-639 (2001b)
- C.D. McCaig, A.M. Rajnicek, B. Song, M. Zhao, Controlling cell behavior electrically: Current views and future potential. Physiol. Rev. 85(3), 943-978 (2005)
- W.F. Agnew, D.B. McCreery, Neural Prostheses: Fundamental Studies (Prentice-Hall, Inc., Engle- wood Cliffs, 1990)
- R.B. Borgens, Electrically mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels. Neuroscience 91(1), 251-264 (1999)
- B. Fritsch, J. Reis, K. Martinowich, H.M. Schambra, Y. Ji, L.G. Cohen, B. Lu, Direct current stimula- tion promotes BDNF-dependent synaptic plasticity: Potential implications for motor learning. Neuron 66(2), 198-204 (2010)
- D.J. Guggenmos, M. Azin, S. Barbay, J.D. Mahnken, C. Dunham, P. Mohseni, R.J. Nudo, Restoration of function after brain damage using a neural prosthesis. Proc. Natl. Acad. Sci. 110(52), 21177-21182 (2013)
- C.F.V. Latchoumane, L. Jackson, M.S.E. Sendi, K.F. Tehrani, L.J. Mortensen, S.L. Stice, M. Ghovanloo, L. Karumbaiah, Chronic electrical stimulation pro- motes the excitability and plasticity of ESC-derived neurons following glutamate-induced inhibition in vitro. Sci. Rep. 8(1), 10957 (2018)
- W.A. Nix, H.C. Hopf, Electrical stimulation of re- generating nerve and its effect on motor recovery. Brain Res. 272(1), 21-25 (1983)
- G.C. Roman, H.K. Strahlendorf, P.W. Coates, B.A. Rowley, Stimulation of sciatic nerve regeneration in the adult rat by low-intensity electric current. Exp. Neurol. 98(2), 222-232 (1987)
- S. Pockett, R.M. Gavin, Acceleration of peripheral nerve regeneration after crush injury in rat. Neu- rosci. Lett. 59(2), 221-224 (1985)
- T. Gordon, T.M. Brushart, K.M. Chan, Augmenting nerve regeneration with electrical stimulation. Neu- rol. Res. 30(10), 1012-1022 (2008)
- T.M. Brushart, Motor axons preferentially reinner- vate motor pathways. J. Neurosci. 13(6), 2730-2738 (1993)
- D. Becker, D.S. Gary, E.S. Rosenzweig, W.M. Grill, J.W. McDonald, Functional electrical stimulation helps replenish progenitor cells in the injured spinal cord of adult rats. Exp. Neurol. 222(2), 211-218 (2010)
- T. Sato, T. Fujikado, T.S. Lee, Y. Tano, Direct ef- fect of electrical stimulation on induction of brain- derived neurotrophic factor from cultured retinal Muller cells. Investig. Ophthalmol. Vis. Sci. 49(10), 4641-4646 (2008a)
- T. Sato, T. Fujikado, T. Morimoto, K. Matsushita, T. Harada, Y. Tano, Effect of electrical stimulation on IGF-1 transcription by L-type calcium channels in cultured retinal Muller cells. Jpn. J. Ophthalmol. 52(3), 217-223 (2008b)
- J.L. Goldberg, J.S. Espinosa, Y. Xu, N. Davidson, G.T. Kovacs, B.A. Barres, Retinal ganglion cells do not extend axons by default: Promotion by neu- rotrophic signaling and electrical activity. Neuron 33(5), 689-702 (2002)