An implantable human stem cell-derived tissue-engineered rostral migratory stream for directed neuronal replacement
  • 1.

    Zhao, C., Deng, W. & Gage, F. H. Mechanisms and functional implications of adult neurogenesis. Cell 132, 645–660 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Ming, G.-L. & Song, H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687–702 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 3.

    Lim, D. A. & Alvarez-Buylla, A. The adult ventricular-subventricular zone (V-SVZ) and olfactory bulb (OB) neurogenesis. Cold Spring Harbor Perspect. Biol. 8, a018820 (2016).

  • 4.

    Lledo, P.-M., Merkle, F. T. & Alvarez-Buylla, A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31, 392–400 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 5.

    Brill, M. S. et al. Adult generation of glutamatergic olfactory bulb interneurons. Nat. Neurosci. 12, 1524–1533 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Lazarini, F. & Lledo, P.-M. Is adult neurogenesis essential for olfaction? Trends Neurosci. 34, 20–30 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 7.

    Nam, S. C. et al. Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J. Comp. Neurol. 505, 190–208 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  • 8.

    Kojima, T. et al. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. STEM CELLS N/A-N/A (2010) https://doi.org/10.1002/stem.306.

  • 9.

    Grade, S. et al. Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum. PLoS ONE 8, e55039 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 10.

    Ota, H. et al. Speed control for neuronal migration in the postnatal brain by Gmip-mediated local inactivation of RhoA. Nat. Commun. 5, 4532 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Kaneko, N., Sawada, M. & Sawamoto, K. Mechanisms of neuronal migration in the adult brain. J. Neurochem. 141, 835–847 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 12.

    Dillen, Y., Kemps, H., Gervois, P., Wolfs, E. & Bronckaers, A. Adult neurogenesis in the subventricular zone and its regulation after ischemic stroke: implications for therapeutic approaches. Transl. Stroke Res. https://doi.org/10.1007/s12975-019-00717-8 (2019).

  • 13.

    Fujioka, T., Kaneko, N. & Sawamoto, K. Blood vessels as a scaffold for neuronal migration. Neurochem. Int. 126, 69–73 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Kaneko, N. et al. New neurons use Slit-Robo signaling to migrate through the glial meshwork and approach a lesion for functional regeneration. Sci. Adv. 4, eaav0618 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 15.

    Cleary, M. A., Uboha, N., Picciotto, M. R. & Beech, R. D. Expression of ezrin in glial tubes in the adult subventricular zone and rostral migratory stream. Neuroscience 143, 851–861 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 16.

    Tang, H. et al. Effect of neural precursor proliferation level on neurogenesis in rat brain during aging and after focal ischemia. Neurobiol. Aging 30, 299–308 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 17.

    Lu, J., Manaenko, A. & Hu, Q. Targeting adult neurogenesis for poststroke therapy. Stem Cells Int. 2017, 5868632 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 18.

    Chang, E. H. et al. Traumatic brain injury activation of the adult subventricular zone neurogenic niche. Front. Neurosci. 10, 332 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 19.

    Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963–970 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Parent, J. M., Vexler, Z. S., Gong, C., Derugin, N. & Ferriero, D. M. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802–813 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  • 21.

    Jin, K. et al. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol. Cell. Neurosci. 24, 171–189 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 22.

    Thored, P. et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24, 739–747 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 23.

    Thored, P. et al. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38, 3032–3039 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Yamashita, T. et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 26, 6627–6636 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Liu, X. S. et al. Gene profiles and electrophysiology of doublecortin-expressing cells in the subventricular zone after ischemic stroke. J. Cereb. Blood Flow Metab. 29, 297–307 (2009).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 26.

    Kernie, S. G. & Parent, J. M. Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol. Dis. 37, 267–274 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Young, C. C., Brooks, K. J., Buchan, A. M. & Szele, F. G. Cellular and molecular determinants of stroke-induced changes in subventricular zone cell migration. Antioxid. Redox Signal. 14, 1877–1888 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Lindvall, O. & Kokaia, Z. Neurogenesis following stroke affecting the adult brain. Cold Spring Harbor Perspect. Biol. 7, a019034 (2015).

  • 29.

    Ramaswamy, S., Goings, G. E., Soderstrom, K. E., Szele, F. G. & Kozlowski, D. A. Cellular proliferation and migration following a controlled cortical impact in the mouse. Brain Res. 1053, 38–53 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 30.

    Acosta, S. A. et al. Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS ONE 8, e53376 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Mierzwa, A. J., Sullivan, G. M., Beer, L. A., Ahn, S. & Armstrong, R. C. Comparison of cortical and white matter traumatic brain injury models reveals differential effects in the subventricular zone and divergent Sonic hedgehog signaling pathways in neuroblasts and oligodendrocyte progenitors. ASN Neuro 6, 1759091414551782 (2014).

  • 32.

    Chirumamilla, S., Sun, D., Bullock, M. R. & Colello, R. J. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J. Neurotrauma 19, 693–703 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Chen, X.-H., Iwata, A., Nonaka, M., Browne, K. D. & Smith, D. H. Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J. Neurotrauma 20, 623–631 (2003).

    PubMed  Article  PubMed Central  Google Scholar 

  • 34.

    Zhang, R. L. et al. Reduction of the cell cycle length by decreasing G 1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke. J. Cereb. Blood Flow. Metab. 26, 857–863 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Addington, C. P., Roussas, A., Dutta, D. & Stabenfeldt, S. E. Endogenous repair signaling after brain injury and complementary bioengineering approaches to enhance neural regeneration. Biomark. Insights 10s1, BMI.S20062 (2015).

    Article  Google Scholar 

  • 36.

    Hayashi, Y., Jinnou, H., Sawamoto, K. & Hitoshi, S. Adult neurogenesis and its role in brain injury and psychiatric diseases. J. Neurochem. 147, 584–594 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Ohab, J. J., Fleming, S., Blesch, A. & Carmichael, S. T. A neurovascular niche for neurogenesis after stroke. J. Neurosci. 26, 13007–13016 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 38.

    Wang, Z. et al. Neurogenic niche conversion strategy induces migration and functional neuronal differentiation of neural precursor cells following brain injury. Stem Cells Dev. scd.2019.0147 (2020) https://doi.org/10.1089/scd.2019.0147.

  • 39.

    Kolb, B. et al. Growth factor-stimulated generation of new cortical tissue and functional recovery after stroke damage to the motor cortex of rats. J. Cereb. Blood Flow Metab. 27, 983–997 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 40.

    Schäbitz, W.-R. et al. Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke 38, 2165–2172 (2007).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 41.

    Ma, M. et al. Intranasal delivery of transforming growth factor-beta1 in mice after stroke reduces infarct volume and increases neurogenesis in the subventricular zone. BMC Neurosci. 9, 117 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 42.

    Petraglia, A. L., Marky, A. H., Walker, C., Thiyagarajan, M. & Zlokovic, B. V. Activated protein C is neuroprotective and mediates new blood vessel formation and neurogenesis after controlled cortical impact. Neurosurgery 66, 165–171 (2010). discussion 171-2.

    PubMed  Article  PubMed Central  Google Scholar 

  • 43.

    Popa-Wagner, A. et al. Effects of granulocyte-colony stimulating factor after stroke in aged rats. Stroke 41, 1027–1031 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 44.

    Erlandsson, A., Lin, C. -H. A., Yu, F. & Morshead, C. M. Immunosuppression promotes endogenous neural stem and progenitor cell migration and tissue regeneration after ischemic injury. Exp. Neurol. 230, 48–57 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Yu, S.-J. et al. Local administration of AAV-BDNF to subventricular zone induces functional recovery in stroke rats. PLoS ONE 8, e81750 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 46.

    Clark, A. R., Carter, A. B., Hager, L. E. & Price, E. M. In vivo neural tissue engineering: cylindrical biocompatible hydrogels that create new neural tracts in the adult mammalian brain. Stem Cells Dev. 25, 1109–1118 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 47.

    Gundelach, J. & Koch, M. Redirection of neuroblast migration from the rostral migratory stream into a lesion in the prefrontal cortex of adult rats. Exp. brain Res. 236, 1181–1191 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  • 48.

    Jinnou, H. et al. Radial glial fibers promote neuronal migration and functional recovery after neonatal brain injury. Cell Stem Cell 22, 128–137.e9 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 49.

    Purvis, E. M., O’Donnell, J. C., Chen, H. I. & Cullen, D. K. Tissue engineering and biomaterial strategies to elicit endogenous neuronal replacement in the brain. Front. Neurol. https://doi.org/10.3389/fneur.2020.00344 (2020).

  • 50.

    Cullen, D. K. et al. Microtissue engineered constructs with living axons for targeted nervous system reconstruction. Tissue Eng. Part A 18, 2280–2289 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 51.

    Struzyna, L. A., Katiyar, K. & Cullen, D. K. Living scaffolds for neuroregeneration. Curr. Opin. Solid State Mater. Sci. 18, 308–318 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 52.

    Struzyna, L. A. et al. Rebuilding brain circuitry with living micro-tissue engineered neural networks. Tissue Eng. Part A 21, 2744–2756 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Struzyna, L. A. et al. Tissue engineered nigrostriatal pathway for treatment of Parkinson’s disease. J. Tissue Eng. Regener. Med. 12, 1702–1716 (2018).

    CAS  Article  Google Scholar 

  • 54.

    Adewole, D. O., Das, S., Petrov, D. & Cullen, D. K. Scaffolds for brain tissue reconstruction. In Handbook of Tissue Engineering Scaffold, Vol. 2, 3–29 (ed. Mozafari, M., Sefat, F., and Atala, A.) (Elsevier, 2019).

  • 55.

    Katiyar, K. S., Struzyna, L. A., Das, S. & Cullen, D. K. Stretch growth of motor axons in custom mechanobioreactors to generate long-projecting axonal constructs. J. Tissue Eng. Regener. Med. 13, 2040–2054 (2019).

    CAS  Article  Google Scholar 

  • 56.

    Winter, C. C. et al. Transplantable living scaffolds comprised of micro-tissue engineered aligned astrocyte networks to facilitate central nervous system regeneration. Acta Biomater. 38, 44–58 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Katiyar, K. S. et al. Three-dimensional tissue engineered aligned astrocyte networks to recapitulate developmental mechanisms and facilitate nervous system regeneration. J. Visual. Exp. https://doi.org/10.3791/55848 (2018).

  • 58.

    O’Donnell, J., Katiyar, K., Panzer, K. & Cullen, D. K. A tissue-engineered rostral migratory stream for directed neuronal replacement. Neural Regener. Res. 13, 1327 (2018).

    Article  Google Scholar 

  • 59.

    Ganz, J. et al. Astrocyte-like cells derived from human oral mucosa stem cells provide neuroprotection in vitro and in vivo. Stem cells Transl. Med. 3, 375–386 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 60.

    Panzer, K. V. et al. Tissue engineered bands of büngner for accelerated motor and sensory axonal outgrowth. Front. Bioeng. Biotechnol. 8, 580654 (2020).

  • 61.

    Lois, C. & Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145–1148 (1994).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 62.

    Yin, X. et al. Neurons derived from human induced pluripotent stem cells integrate into rat brain circuits and maintain both excitatory and inhibitory synaptic activities. eneuro 6, ENEURO.0148-19.2019 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Rolfe, A. & Sun, D. Stem cell therapy in brain trauma: implications for repair and regeneration of injured brain in experimental TBI models. In Brain Neurotrauma: Molecular, Neuropsychological, and Rehabilitation Aspects (ed. Kobeissy, F. H.) (CRC Press/Taylor & Francis, 2015).

  • 64.

    Yamashita, T. et al. Novel therapeutic transplantation of induced neural stem cells for stroke. Cell Transplant. 26, 461–467 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 65.

    Xiong, L.-L. et al. Neural stem cell transplantation promotes functional recovery from traumatic brain injury via brain derived neurotrophic factor-mediated neuroplasticity. Mol. Neurobiol. 55, 2696–2711 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 66.

    Kim, K. et al. Epigenetic memory in induced pluripotent stem cells. Nature 467, 285–290 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 67.

    Hickey, K. & Stabenfeldt, S. E. Using biomaterials to modulate chemotactic signaling for central nervous system repair. Biomed. Mater. 13, 044106 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 68.

    Cotman, C. & Berchtold, N. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25, 295–301 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 69.

    Griesbach, G. S., Hovda, D. A., Molteni, R., Wu, A. & Gomez-Pinilla, F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience 125, 129–139 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 70.

    Fon, D. et al. Nanofibrous scaffolds releasing a small molecule BDNF-mimetic for the re-direction of endogenous neuroblast migration in the brain. Biomaterials 35, 2692–2712 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 71.

    Motalleb, R. et al. In vivo migration of endogenous brain progenitor cells guided by an injectable peptide amphiphile biomaterial. J. Tissue Eng. Regener. Med. 12, e2123–e2133 (2018).

    CAS  Article  Google Scholar 

  • 72.

    Ajioka, I. et al. Enhancement of neuroblast migration into the injured cerebral cortex using laminin-containing porous sponge. Tissue Eng. Part A 21, 193–201 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Fujioka, T. et al. β1 integrin signaling promotes neuronal migration along vascular scaffolds in the post-stroke brain. EBioMedicine 16, 195–203 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Gengatharan, A., Bammann, R. R. & Saghatelyan, A. The role of astrocytes in the generation, migration, and integration of new neurons in the adult olfactory bulb. Front. Neurosci. 10, 149 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 75.

    Mason, H. A., Ito, S. & Corfas, G. Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J. Neurosci. 21, 7654–7663 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 76.

    García-Marqués, J., De Carlos, J. A., Greer, C. A. & López-Mascaraque, L. Different astroglia permissivity controls the migration of olfactory bulb interneuron precursors. Glia 58, 218–230 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 77.

    Persson, A., Lindwall, C., Curtis, M. A. & Kuhn, H. G. Expression of ezrin radixin moesin proteins in the adult subventricular zone and the rostral migratory stream. Neuroscience 167, 312–322 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 78.

    Kaneko, N. et al. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron 67, 213–223 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 79.

    Harris, J. P. et al. Advanced biomaterial strategies to transplant preformed micro-tissue engineered neural networks into the brain. J. Neural Eng. 13, 016019 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 80.

    Serruya, M. D. et al. Engineered axonal tracts as “living electrodes” for synaptic-based modulation of neural circuitry. Adv. Funct. Mater. 28, 1701183 (2018).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 81.

    Li, L. et al. Human embryonic stem cells possess immune-privileged properties. Stem Cells 22, 448–456 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 82.

    Zhang, Q. et al. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J. Immunol. (Baltim., Md.: 1950) 183, 7787–7798 (2009).

    CAS  Article  Google Scholar 

  • 83.

    Zhang, Q. et al. Neural crest stem-like cells non-genetically induced from human gingiva-derived mesenchymal stem cells promote facial nerve regeneration in rats. Mol. Neurobiol. 55, 6965–6983 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 84.

    Zhang, Q. et al. 3D bio-printed scaffold-free nerve constructs with human gingiva-derived mesenchymal stem cells promote rat facial nerve regeneration. Sci. Rep. 8, 6634 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 85.

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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