Improving the therapeutic efficacy of neural progenitor cell transplantation following spinal cord injury

References

• DeVivo MJ, Go BK, Jackson AB. Overview of the national spinal cord injury statistical center database. J Spinal Cord Med. 2002;25(4):335–338.
   PubMedGoogle Scholar
• Witiw CD, Fehlings MG. Acute spinal cord injury. J Spinal Disord Tech. 2015;28(6):202–210.
   PubMedGoogle Scholar
• Estrada V, Muller HW. Spinal cord injury - there is not just one way of treating it. F1000Prime Rep. 2014;6:84.
   PubMedGoogle Scholar
• Hoh DJ, Mercier LM, Hussey SP, et al. Respiration following spinal cord injury: evidence for human neuroplasticity. Respir Physiol Neurobiol. 2013;189(2):450–464.
   PubMed Web of Science ®Google Scholar
• Hormigo, K.M., Zholudeva, L.V., Spruance V.M. et al. Enhancing neural activity to drive respiratory plasticity following cervical spinal cord injury. Exp Neurol. 2017;287(Pt 2):276-287.
   Web of Science ®Google Scholar
• Volarevic V, Erceg S, Bhattacharya SS, et al. Stem cell-based therapy for spinal cord injury. Cell Transplant. 2013;22(8):1309–1323.
   PubMed Web of Science ®Google Scholar
• Kanno H, Pearse DD, Ozawa H, et al. Schwann cell transplantation for spinal cord injury repair: its significant therapeutic potential and prospectus. Rev Neurosci. 2015;26(2):121–128.
   PubMed Web of Science ®Google Scholar
• Ziege S, Baumgartner W, Wewetzer K. Toward defining the regenerative potential of olfactory Mucosa: establishment of Schwann cell-free adult canine olfactory ensheathing cell preparations suitable for transplantation. Cell Transplant. 2013;22(2):355–367.
   PubMed Web of Science ®Google Scholar
• Avidan, H., Ziv, Y, Pluchino, S, et al. A synergy between T-cell based vaccination and transplantation of neural stem cells in promoting motor recovery after spinal cord injury. Rev Neurosci. 2005;16:S3–S3.
   Web of Science ®Google Scholar
• Lammertse DP. Clinical trials in spinal cord injury: lessons learned on the path to translation. The 2011 International Spinal Cord Society Sir Ludwig Guttmann Lecture. Spinal Cord. 2013;51(1):2–9.
   PubMed Web of Science ®Google Scholar
• Lammertse DP, Jones LAT, Charlifue SB, et al. Autologous incubated macrophage therapy in acute, complete spinal cord injury: results of the phase 2 randomized controlled multicenter trial. Spinal Cord. 2012;50(9):661–671.
   PubMed Web of Science ®Google Scholar
• Thompson FJ, Reier PJ, Uthman B, et al. Neurophysiological assessment of the feasibility and safety of neural tissue transplantation in patients with syringomyelia. J Neurotrauma. 2001;18(9):931–945.
   PubMed Web of Science ®Google Scholar
• Wirth ED 3rd, Reier PJ, Fessler RG, et al. Feasibility and safety of neural tissue transplantation in patients with syringomyelia. J Neurotrauma. 2001;18(9):911–929.
   PubMed Web of Science ®Google Scholar
• Reier PJ. Neural tissue grafts and repair of the injured spinal cord. Neuropathol Appl Neurobiol. 1985;11(2):81–104.
   PubMed Web of Science ®Google Scholar
• Bonner JF, Connors TM, Silverman WF, et al. Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J Neurosci. 2011;31(12):4675–4686.
   PubMed Web of Science ®Google Scholar
• Lepore, A.C., Neuhuber B, Connors TM et al. Long-term fate of neural precursor cells following transplantation into developing and adult CNS. Neuroscience. 2006;142(1):287-304.
   Web of Science ®Google Scholar
• Lu P, Kadoya K, Tuszynski MH. Axonal growth and connectivity from neural stem cell grafts in models of spinal cord injury. Curr Opin Neurobiol. 2014;27:103–109.
   PubMed Web of Science ®Google Scholar
• Lu P, Wang Y, Graham L, et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell. 2012;150(6):1264–1273.
   PubMed Web of Science ®Google Scholar
• Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707–1710.
   PubMed Web of Science ®Google Scholar
• Temple S. Division and differentiation of isolated CNS blast cells in microculture. Nature. 1989;340(6233):471–473.
   PubMed Web of Science ®Google Scholar
• Iyer NR, Huettner JE, Butts JC, et al. Generation of highly enriched V2a interneurons from mouse embryonic stem cells. Exp Neurol. 2016;277:305–316.
   PubMed Web of Science ®Google Scholar
• Iyer NR, Wilems TS, Sakiyama-Elbert SE. Stem cells for spinal cord injury: Strategies to inform differentiation and transplantation. Biotechnol Bioeng. 2016. doi: 10.1002/bit.26074. [Epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Mothe AJ, Tator CH. Review of transplantation of neural stem/progenitor cells for spinal cord injury. Int J Dev Neurosci. 2013;31(7):701–713.
   PubMed Web of Science ®Google Scholar
• Wyatt LA, Keirstead HS. Stem cell-based treatments for spinal cord injury. Prog Brain Res. 2012;201:233–252.
   PubMed Web of Science ®Google Scholar
• Das GD. Neural transplantation in the spinal cord of the adult mammal, in spinal cord reconstruction. Kao CC, Bunge RP, Reier PJ, Editors. New York: Raven Press; 1983. p. 367–396.
   Google Scholar
• Houle JD, Reier PJ. Transplantation of fetal spinal cord tissue into the chronically injured adult rat spinal cord. J Comp Neurol. 1988;269(4):535–547.
   PubMed Web of Science ®Google Scholar
• Jakeman LB, Reier PJ. Axonal projections between fetal spinal cord transplants and the adult rat spinal cord: a neuroanatomical tracing study of local interactions. J Comp Neurol. 1991;307(2):311–334.
   PubMed Web of Science ®Google Scholar
• Lee KZ, Lane MA, Dougherty BJ, et al. Intraspinal transplantation and modulation of donor neuron electrophysiological activity. Exp Neurol. 2014;251:47–57.
   PubMed Web of Science ®Google Scholar
• Reier, P.J., Bregman, B.S., Wujek, J.R., et al. Intraspinal transplantation of fetal spinal cord tissue: an approach toward functional repair of the injured spinal cord, In Development and Plasticity of the Mammalian Spinal Cord, Goldberger ME, Gorio A, Murray M, Editors. 1986, Liviana Press: Padova. 251–269.
   Google Scholar
• Reier PJ, Golder FJ, Bolser DC, et al. Gray matter repair in the cervical spinal cord. Prog Brain Res. 2002;137:49–70.
   PubMed Web of Science ®Google Scholar
• Reier PJ, Houle JD, Jakeman L, et al. Transplantation of fetal spinal cord tissue into acute and chronic hemisection and contusion lesions of the adult rat spinal cord. Prog Brain Res. 1988;78:173–179.
   PubMed Web of Science ®Google Scholar
• Stokes BT, Reier PJ. Fetal grafts alter chronic behavioral outcome after contusion damage to the adult rat spinal cord. Exp Neurol. 1992;116(1):1–12.
   PubMed Web of Science ®Google Scholar
• White TE, Lane MA, Sandhu MS, et al. Neuronal progenitor transplantation and respiratory outcomes following upper cervical spinal cord injury in adult rats. Exp Neurol. 2010;225(1):231–236.
   PubMed Web of Science ®Google Scholar
• Lu P, Jones LL, Snyder EY, et al. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol. 2003;181(2):115–129.
   PubMed Web of Science ®Google Scholar
• Pluchino S, Quattrini A, Brambilla E, et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature. 2003;422(6933):688–694.
   PubMed Web of Science ®Google Scholar
• Bonner JF, Steward O. Repair of spinal cord injury with neuronal relays: from fetal grafts to neural stem cells. Brain Res. 2015;1619:115–123.
   PubMed Web of Science ®Google Scholar
• Harrop JS, Ghobrial GM, Chitale R, et al. Evaluating initial spine trauma response: injury time to trauma center in PA, USA. J Clin Neurosci. 2014;21(10):1725–1729.
   PubMed Web of Science ®Google Scholar
• Kadoya K, Lu P, Nguyen K, et al. Spinal cord reconstitution with homologous neural grafts enables robust corticospinal regeneration. Nat Med. 2016;22(5):479–487.
   PubMed Web of Science ®Google Scholar
• Tarasenko YI, Gao J, Nie L, et al. Human fetal neural stem cells grafted into contusion-injured rat spinal cords improve behavior. J Neurosci Res. 2007;85(1):47–57.
   PubMed Web of Science ®Google Scholar
• Nishimura S, Yasuda A, Iwai H, et al. Time-dependent changes in the microenvironment of injured spinal cord affects the therapeutic potential of neural stem cell transplantation for spinal cord injury. Mol Brain. 2013;6:3.
   PubMed Web of Science ®Google Scholar
• Khazaei M, Siddiqui AM, Fehlings MG. The Potential for iPS-Derived Stem Cells as a Therapeutic Strategy for Spinal Cord Injury: Opportunities and Challenges. J Clin Med. 2014;4(1):37–65.
   PubMed Web of Science ®Google Scholar
• Falnikar A, Hala TJ, Poulsen DJ, et al. GLT1 overexpression reverses established neuropathic pain-related behavior and attenuates chronic dorsal horn neuron activation following cervical spinal cord injury. Glia. 2016;64(3):396–406.
   PubMed Web of Science ®Google Scholar
• Plemel JR, Keough MB, Duncan GJ, et al. Remyelination after spinal cord injury: is it a target for repair? Prog Neurobiol. 2014;117:54–72.
   PubMed Web of Science ®Google Scholar
• Faulkner J, Keirstead HS. Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transpl Immunol. 2005;15(2):131–142.
   PubMed Web of Science ®Google Scholar
• Cloutier F, Siegenthaler MM, Nistor G, et al. Transplantation of human embryonic stem cell-derived oligodendrocyte progenitors into rat spinal cord injuries does not cause harm. Regen Med. 2006;1(4):469–479.
   PubMed Web of Science ®Google Scholar
• Alsanie WF, Niclis JC, Petratos S. Human embryonic stem cell-derived oligodendrocytes: protocols and perspectives. Stem Cells Dev. 2013;22(18):2459–2476.
   PubMed Web of Science ®Google Scholar
• Czepiel M, Boddeke E, Copray S. Human oligodendrocytes in remyelination research. Glia. 2015;63(4):513–530.
   PubMed Web of Science ®Google Scholar
• Priest CA, Manley NC, Denham J, et al. Preclinical safety of human embryonic stem cell-derived oligodendrocyte progenitors supporting clinical trials in spinal cord injury. Regen Med. 2015;10(8):939–958.
   PubMed Web of Science ®Google Scholar
• Myers SA, Bankston AN, Burke DA, et al. Does the preclinical evidence for functional remyelination following myelinating cell engraftment into the injured spinal cord support progression to clinical trials? Exp Neurol. 2016;283:560–572.
   PubMed Web of Science ®Google Scholar
• Watson RA, Yeung TM. What is the potential of oligodendrocyte progenitor cells to successfully treat human spinal cord injury? BMC Neurol. 2011;11:113.
   PubMed Web of Science ®Google Scholar
• Tuszynski MH, Wang Y, Graham L, et al. Neural stem cell dissemination after grafting to CNS injury sites. Cell. 2014;156(3):388–389.
   PubMed Web of Science ®Google Scholar
• Charsar BA, Urban MW, Lepore AC. Harnessing the power of cell transplantation to target respiratory dysfunction following spinal cord injury. Exp Neurol. 2017;287(Pt 2):268-275.
   Web of Science ®Google Scholar
• Sloan SA, Barres BA. Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr Opin Neurobiol. 2014;27:75–81.
   PubMed Web of Science ®Google Scholar
• Li K, Javed E, Hala TJ, et al. Transplantation of glial progenitors that overexpress glutamate transporter GLT1 preserves diaphragm function following cervical SCI. Mol Ther. 2015;23(3):533–548.
   PubMed Web of Science ®Google Scholar
• Falnikar A, Li K, Lepore AC. Therapeutically targeting astrocytes with stem and progenitor cell transplantation following traumatic spinal cord injury. Brain Res. 2015;1619:91–103.
   PubMed Web of Science ®Google Scholar
• Haas C, Neuhuber B, Yamagami T, et al. Phenotypic analysis of astrocytes derived from glial restricted precursors and their impact on axon regeneration. Exp Neurol. 2012;233(2):717–732.
   PubMed Web of Science ®Google Scholar
• Ketschek AR, Haas C, Gallo G, et al. The roles of neuronal and glial precursors in overcoming chondroitin sulfate proteoglycan inhibition. Exp Neurol. 2012;235(2):627–637.
   PubMed Web of Science ®Google Scholar
• Yuan XB, Jin Y, Haas C, et al. Guiding migration of transplanted glial progenitor cells in the injured spinal cord. Sci Rep. 2016;6:22576.
   PubMed Web of Science ®Google Scholar
• Filous AR, Silver J. “Targeting astrocytes in CNS injury and disease: A translational research approach”. Prog Neurobiol. 2016;144:173–187.
   PubMed Web of Science ®Google Scholar
• Li K, Javed E, Scura D, et al. Human iPS cell-derived astrocyte transplants preserve respiratory function after spinal cord injury. Exp Neurol. 2015;271:479–492.
   PubMed Web of Science ®Google Scholar
• Khakh BS, Sofroniew MV. Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci. 2015;18(7):942–952.
   PubMed Web of Science ®Google Scholar
• Faulkner JR, Herrmann JE, Woo MJ, et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci. 2004;24(9):2143–2155.
   PubMed Web of Science ®Google Scholar
• Sofroniew MV. Astrocyte barriers to neurotoxic inflammation. Nat Rev Neurosci. 2015;16(5):249–263.
   PubMed Web of Science ®Google Scholar
• Anderson MA, Burda JE, Ren Y, et al. Astrocyte scar formation aids central nervous system axon regeneration. Nature. 2016;532(7598):195–200.
   PubMed Web of Science ®Google Scholar
• Anderson MA, Ao Y, Sofroniew MV. Heterogeneity of reactive astrocytes. Neurosci Lett. 2014;565:23–29.
   PubMed Web of Science ®Google Scholar
• Davies JE, Pröschel C, Zhang N, et al. Transplanted astrocytes derived from BMP- or CNTF-treated glial-restricted precursors have opposite effects on recovery and allodynia after spinal cord injury. J Biol. 2008;7(7):24.
   PubMedGoogle Scholar
• Hofstetter CP, Holmström NAV, Lilja JA, et al. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci. 2005;8(3):346–353.
   PubMed Web of Science ®Google Scholar
• Mitsui T, Shumsky JS, Lepore AC, et al. Transplantation of neuronal and glial restricted precursors into contused spinal cord improves bladder and motor functions, decreases thermal hypersensitivity, and modifies intraspinal circuitry. J Neurosci. 2005;25(42):9624–9636.
   PubMed Web of Science ®Google Scholar
• Kwon BK, Soril LJJ, Bacon M, et al. Demonstrating efficacy in preclinical studies of cellular therapies for spinal cord injury - how much is enough? Exp Neurol. 2013;248:30–44.
   PubMed Web of Science ®Google Scholar
• Dietz V. Improving outcome of sensorimotor functions after traumatic spinal cord injury. F1000Res 2016;5:1018.
   Google Scholar