Neuro-immune interactions of neural stem cell transplants: From animal disease models to human trials

Experimental Neurology

Volumn 260, Issue , 2014, Pages 19-32

  Giusto, Elena ^a   Donegà, Matteo ^a   Cossetti, Chiara ^a   Pluchino, Stefano ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Clinical trials; Immune modulation; Neural stem cells; Neuro immune interactions; Stem cell therapy

Indexed keywords

CEREBROVASCULAR ACCIDENT; CLINICAL EFFECTIVENESS; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NEURAL STEM CELL TRANSPLANTATION; NEUROIMMUNOLOGY; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; SPINAL CORD INJURY; ANIMAL; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL TRIAL (TOPIC); CYTOLOGY; DISEASE MODEL; METHODOLOGY; NEURAL STEM CELL; NEURO-IMMUNE INTERACTIONS; STEM CELL TRANSPLANTATION;

CLINICAL TRIALS; IMMUNE MODULATION; NEURAL STEM CELLS; NEURO-IMMUNE INTERACTIONS; STEM CELL THERAPY;

ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; MULTIPLE SCLEROSIS; NEURAL STEM CELLS; STEM CELL TRANSPLANTATION;

EID: 84908365928     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.03.009     Document Type: Review

References (194)

1. Abematsu M., Tsujimura K., Yamano M., Saito M., Kohno K., Kohyama J., Namihira M., Komiya S., Nakashima K. Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury. J. Clin. Invest. 2010, 120:3255-3266.
2. Aboody K., Capela A., Niazi N., Stern J.H., Temple S. Translating stem cell studies to the clinic for CNS repair: current state of the art and the need for a Rosetta Stone. Neuron 2011, 70:597-613.
3. Aharonowiz M., Einstein O., Fainstein N., Lassmann H., Reubinoff B., Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS One 2008, 3:e3145.
4. Allaman I., Belanger M., Magistretti P.J. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci. 2011, 34:76-87.
5. Amariglio N., Hirshberg A., Scheithauer B.W., Cohen Y., Loewenthal R., Trakhtenbrot L., Paz N., Koren-Michowitz M., Waldman D., Leider-Trejo L., Toren A., Constantini S., Rechavi G. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 2009, 6:e1000029.
6. Andres R.H., Choi R., Pendharkar A.V., Gaeta X., Wang N., Nathan J.K., Chua J.Y., Lee S.W., Palmer T.D., Steinberg G.K., Guzman R. The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain. Stroke 2011, 42:2923-2931.
7. Andres R.H., Horie N., Slikker W., Keren-Gill H., Zhan K., Sun G., Manley N.C., Pereira M.P., Sheikh L.A., McMillan E.L., Schaar B.T., Svendsen C.N., Bliss T.M., Steinberg G.K. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 2011, 134:1777-1789.
8. Bacigaluppi M., Pluchino S., Martino G., Kilic E., Hermann D.M. Neural stem/precursor cells for the treatment of ischemic stroke. J. Neurol. Sci. 2008, 265:73-77.
9. Bacigaluppi M., Pluchino S., Peruzzotti-Jametti L., Kilic E., Kilic U., Salani G., Brambilla E., West M.J., Comi G., Martino G., Hermann D.M. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 2009, 132:2239-2251.
10. Bamber N.I., Li H., Lu X., Oudega M., Aebischer P., Xu X.M. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 2001, 13:257-268.
11. Barkhof F., Bruck W., De Groot C.J., Bergers E., Hulshof S., Geurts J., Polman C.H., van der Valk P. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch. Neurol. 2003, 60:1073-1081.
12. Barres B.A., Hart I.K., Coles H.S., Burne J.F., Voyvodic J.T., Richardson W.D., Raff M.C. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 1992, 70:31-46.
13. Ben-Hur T. Immunomodulation by neural stem cells. J. Neurol. Sci. 2008, 265:102-104.
14. Ben-Hur T., Einstein O., Mizrachi-Kol R., Ben-Menachem O., Reinhartz E., Karussis D., Abramsky O. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 2003, 41:73-80.
15. Blakemore W.F. Remyelination of CNS axons by Schwann cells transplanted from the sciatic nerve. Nature 1977, 266:68-69.
16. Blakemore W.F., Crang A.J. Extensive oligodendrocyte remyelination following injection of cultured central nervous system cells into demyelinating lesions in adult central nervous system. Dev. Neurosci. 1988, 10:1-11.
17. Blakemore W.F., Chari D.M., Gilson J.M., Crang A.J. Modelling large areas of demyelination in the rat reveals the potential and possible limitations of transplanted glial cells for remyelination in the CNS. Glia 2002, 38:155-168.
18. Bonner J.F., Blesch A., Neuhuber B., Fischer I. Promoting directional axon growth from neural progenitors grafted into the injured spinal cord. J. Neurosci. Res. 2010, 88:1182-1192.
19. Bonner J.F., Connors T.M., Silverman W.F., Kowalski D.P., Lemay M.A., Fischer I. Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J. Neurosci. 2011, 31:4675-4686.
20. Bottai D., Madaschi L., Di Giulio A.M., Gorio A. Viability-dependent promoting action of adult neural precursors in spinal cord injury. Mol. Med. 2008, 14:634-644.
21. Buhnemann C., Scholz A., Bernreuther C., Malik C.Y., Braun H., Schachner M., Reymann K.G., Dihne M. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain 2006, 129:3238-3248.
22. Butovsky O., Hauben E., Schwartz M. Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7-2 (CD86) and prevention of cyst formation. FASEB J. 2001, 15:1065-1067.
23. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 2006, 31:149-160.
24. Canoll P.D., Musacchio J.M., Hardy R., Reynolds R., Marchionni M.A., Salzer J.L. GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 1996, 17:229-243.
25. Canoll P.D., Kraemer R., Teng K.K., Marchionni M.A., Salzer J.L. GGF/neuregulin induces a phenotypic reversion of oligodendrocytes. Mol. Cell. Neurosci. 1999, 13:79-94.
26. Cao Q.L., Zhang Y.P., Howard R.M., Walters W.M., Tsoulfas P., Whittemore S.R. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp. Neurol. 2001, 167:48-58.
27. Cao Q.L., Howard R.M., Dennison J.B., Whittemore S.R. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp. Neurol. 2002, 177:349-359.
28. Cao W., Yang Y., Wang Z., Liu A., Fang L., Wu F., Hong J., Shi Y., Leung S., Dong C., Zhang J.Z. Leukemia inhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. Immunity 2011, 35:273-284.
29. Capone C., Frigerio S., Fumagalli S., Gelati M., Principato M.C., Storini C., Montinaro M., Kraftsik R., De Curtis M., Parati E., De Simoni M.G. Neurosphere-derived cells exert a neuroprotective action by changing the ischemic microenvironment. PLoS One 2007, 2:e373.
30. Chang A., Tourtellotte W.W., Rudick R., Trapp B.D. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 2002, 346:165-173.
31. Chari D.M., Crang A.J., Blakemore W.F. Decline in rate of colonization of oligodendrocyte progenitor cell (OPC)-depleted tissue by adult OPCs with age. J. Neuropathol. Exp. Neurol. 2003, 62:908-916.
32. Chen J.T., Kuhlmann T., Jansen G.H., Collins D.L., Atkins H.L., Freedman M.S., O'Connor P.W., Arnold D.L. Voxel-based analysis of the evolution of magnetization transfer ratio to quantify remyelination and demyelination with histopathological validation in a multiple sclerosis lesion. NeuroImage 2007, 36:1152-1158.
33. Chen B., Gao X.Q., Yang C.X., Tan S.K., Sun Z.L., Yan N.H., Pang Y.G., Yuan M., Chen G.J., Xu G.T., Zhang K., Yuan Q.L. Neuroprotective effect of grafting GDNF gene-modified neural stem cells on cerebral ischemia in rats. Brain Res. 2009, 1284:1-11.
34. Chen G., Hu Y.R., Wan H., Xia L., Li J.H., Yang F., Qu X., Wang S.G., Wang Z.C. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells and Schwann cells. Chin. Med. J. (Engl.) 2010, 123:2424-2431.
35. Chu K., Kim M., Jeong S.W., Kim S.U., Yoon B.W. Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci. Lett. 2003, 343:129-133.
36. Chu K., Kim M., Jung K.H., Jeon D., Lee S.T., Kim J., Jeong S.W., Kim S.U., Lee S.K., Shin H.S., Roh J.K. Human neural stem cell transplantation reduces spontaneous recurrent seizures following pilocarpine-induced status epilepticus in adult rats. Brain Res. 2004, 1023:213-221.
37. Chu K., Kim M., Park K.I., Jeong S.W., Park H.K., Jung K.H., Lee S.T., Kang L., Lee K., Park D.K., Kim S.U., Roh J.K. Human neural stem cells improve sensorimotor deficits in the adult rat brain with experimental focal ischemia. Brain Res. 2004, 1016:145-153.
38. Coleman M.P., Perry V.H. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 2002, 25:532-537.
39. Compston A. Remyelination of the central nervous system. Mult. Scler. 1996, 1:388-392.
40. Compston A. Remyelination in multiple sclerosis: a challenge for therapy. The 1996 European Charcot Foundation Lecture. Mult. Scler. 1997, 3:51-70.
41. Compston A., Coles A. Multiple sclerosis. Lancet 2002, 359:1221-1231.
42. Cossetti C., Alfaro-Cervello C., Donega M., Tyzack G., Pluchino S. New perspectives of tissue remodelling with neural stem and progenitor cell-based therapies. Cell Tissue Res. 2012, 349:321-329.
43. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 1997, 3:73-76.
44. Cummings B.J., Uchida N., Tamaki S.J., Salazar D.L., Hooshmand M., Summers R., Gage F.H., Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14069-14074.
45. Cusimano M., Biziato D., Brambilla E., Donega M., Alfaro-Cervello C., Snider S., Salani G., Pucci F., Comi G., Garcia-Verdugo J.M., De Palma M., Martino G., Pluchino S. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012, 135:447-460.
46. Daadi M.M., Davis A.S., Arac A., Li Z., Maag A.L., Bhatnagar R., Jiang K., Sun G., Wu J.C., Steinberg G.K. Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury. Stroke 2010, 41:516-523.
47. Darsalia V., Kallur T., Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur. J. Neurosci. 2007, 26:605-614.
48. Ditunno J.F., Little J.W., Tessler A., Burns A.S. Spinal shock revisited: a four-phase model. Spinal Cord 2004, 42:383-395.
49. Donnelly D.J., Popovich P.G. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 2008, 209:378-388.
50. Dyment D.A., Ebers G.C. An array of sunshine in multiple sclerosis. N. Engl. J. Med. 2002, 347:1445-1447.
51. Einstein O., Karussis D., Grigoriadis N., Mizrachi-Kol R., Reinhartz E., Abramsky O., Ben-Hur T. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol. Cell. Neurosci. 2003, 24:1074-1082.
52. Einstein O., Grigoriadis N., Mizrachi-Kol R., Reinhartz E., Polyzoidou E., Lavon I., Milonas I., Karussis D., Abramsky O., Ben-Hur T. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp. Neurol. 2006, 198:275-284.
53. Einstein O., Fainstein N., Vaknin I., Mizrachi-Kol R., Reihartz E., Grigoriadis N., Lavon I., Baniyash M., Lassmann H., Ben-Hur T. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann. Neurol. 2007, 61:209-218.
54. Einstein O., Friedman-Levi Y., Grigoriadis N., Ben-Hur T. Transplanted neural precursors enhance host brain-derived myelin regeneration. J. Neurosci. 2009, 29:15694-15702.
55. Englund U., Bjorklund A., Wictorin K., Lindvall O., Kokaia M. Grafted neural stem cells develop into functional pyramidal neurons and integrate into host cortical circuitry. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:17089-17094.
56. Fainstein N., Vaknin I., Einstein O., Zisman P., Ben Sasson S.Z., Baniyash M., Ben-Hur T. Neural precursor cells inhibit multiple inflammatory signals. Mol. Cell. Neurosci. 2008, 39:335-341.
57. Fischer I. Candidate cells for transplantation into the injured CNS. Prog. Brain Res. 2000, 128:253-257.
58. Fleming J.C., Norenberg M.D., Ramsay D.A., Dekaban G.A., Marcillo A.E., Saenz A.D., Pasquale-Styles M., Dietrich W.D., Weaver L.C. The cellular inflammatory response in human spinal cords after injury. Brain 2006, 129:3249-3269.
59. Flugel A., Berkowicz T., Ritter T., Labeur M., Jenne D.E., Li Z., Ellwart J.W., Willem M., Lassmann H., Wekerle H. Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity 2001, 14:547-560.
60. Franklin R.J. Why does remyelination fail in multiple sclerosis?. Nat. Rev. Neurosci. 2002, 3:705-714.
61. Franklin R.J., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 2008, 9:839-855.
62. Frieler R.A., Meng H., Duan S.Z., Berger S., Schutz G., He Y., Xi G., Wang M.M., Mortensen R.M. Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke 2011, 42:179-185.
63. Fujimoto Y., Abematsu M., Falk A., Tsujimura K., Sanosaka T., Juliandi B., Semi K., Namihira M., Komiya S., Smith A., Nakashima K. Treatment of a mouse model of spinal cord injury by transplantation of human induced pluripotent stem cell-derived long-term self-renewing neuroepithelial-like stem cells. Stem Cells 2012, 30:1163-1173.
64. Glass J.D., Boulis N.M., Johe K., Rutkove S.B., Federici T., Polak M., Kelly C., Feldman E.L. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells 2012, 30:1144-1151.
65. Goldman S.A., Nedergaard M., Windrem M.S. Glial progenitor cell-based treatment and modeling of neurological disease. Science 2012, 338:491-495.
66. Groves A.K., Barnett S.C., Franklin R.J., Crang A.J., Mayer M., Blakemore W.F., Noble M. Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 1993, 362:453-455.
67. Gu Y.L., Yin L.W., Zhang Z., Liu J., Liu S.J., Zhang L.F., Wang T.H. Neurotrophin Expressions in Neural Stem Cells Grafted Acutely to Transected Spinal Cord of Adult Rats Linked to Functional Improvement. Cell. Mol. Neurobiol. 2012, 32:1089-1097.
68. Gupta N., Henry R.G., Strober J., Kang S.M., Lim D.A., Bucci M., Caverzasi E., Gaetano L., Mandelli M.L., Ryan T., Perry R., Farrell J., Jeremy R.J., Ulman M., Huhn S.L., Barkovich A.J., Rowitch D.H. Neural stem cell engraftment and myelination in the human brain. Sci. Transl. Med. 2012, 4:155ra137.
69. Guzman R., De Los Angeles A., Cheshier S., Choi R., Hoang S., Liauw J., Schaar B., Steinberg G. Intracarotid injection of fluorescence activated cell-sorted CD49d-positive neural stem cells improves targeted cell delivery and behavior after stroke in a mouse stroke model. Stroke 2008, 39:1300-1306.
70. Han S.S., Kang D.Y., Mujtaba T., Rao M.S., Fischer I. Grafted lineage-restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp. Neurol. 2002, 177:360-375.
71. Han S.S., Liu Y., Tyler-Polsz C., Rao M.S., Fischer I. Transplantation of glial-restricted precursor cells into the adult spinal cord: survival, glial-specific differentiation, and preferential migration in white matter. Glia 2004, 45:1-16.
72. Harris V.K., Yan Q.J., Vyshkina T., Sahabi S., Liu X., Sadiq S.A. Clinical and pathological effects of intrathecal injection of mesenchymal stem cell-derived neural progenitors in an experimental model of multiple sclerosis. J. Neurol. Sci. 2012, 313:167-177.
73. Hassani Z., O'Reilly J., Pearse Y., Stroemer P., Tang E., Sinden J., Price J., Thuret S. Human neural progenitor cell engraftment increases neurogenesis and microglial recruitment in the brain of rats with stroke. PLoS One 2012, 7:e50444.
74. Hawryluk G.W., Mothe A.J., Chamankhah M., Wang J., Tator C., Fehlings M.G. In vitro characterization of trophic factor expression in neural precursor cells. Stem Cells Dev. 2012, 21:432-447.
75. Hicks, C., Stevanato, L., Stroemer, R.P., Tang, E., Richardson, S., Sinden, J.D., in press. In vivo and in vitro characterization of the angiogenic effect of CTX0E03 human neural stem cells. Cell Transplant [Epub ahead of print].
76. Hill C.E., Proschel C., Noble M., Mayer-Proschel M., Gensel J.C., Beattie M.S., Bresnahan J.C. Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: survival, differentiation, and effects on lesion environment and axonal regeneration. Exp. Neurol. 2004, 190:289-310.
77. Ho C.H., Wuermser L.A., Priebe M.M., Chiodo A.E., Scelza W.M., Kirshblum S.C. Spinal cord injury medicine. 1. Epidemiology and classification. Arch. Phys. Med. Rehabil. 2007, 88:S49-S54.
78. Hofstetter C.P., Holmstrom N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 2005, 8:346-353.
79. Hurtado A., Moon L.D., Maquet V., Blits B., Jerome R., Oudega M. Poly (d, l-lactic acid) macroporous guidance scaffolds seeded with Schwann cells genetically modified to secrete a bi-functional neurotrophin implanted in the completely transected adult rat thoracic spinal cord. Biomaterials 2006, 27:430-442.
80. Hwang D.H., Kim B.G., Kim E.J., Lee S.I., Joo I.S., Suh-Kim H., Sohn S., Kim S.U. Transplantation of human neural stem cells transduced with Olig2 transcription factor improves locomotor recovery and enhances myelination in the white matter of rat spinal cord following contusive injury. BMC Neurosci. 2009, 10:117.
81. Iadecola C., Anrather J. The immunology of stroke: from mechanisms to translation. Nat. Med. 2011, 17:796-808.
82. Imitola J., Raddassi K., Park K.I., Mueller F.J., Nieto M., Teng Y.D., Frenkel D., Li J., Sidman R.L., Walsh C.A., Snyder E.Y., Khoury S.J. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:18117-18122.
83. Ishibashi S., Sakaguchi M., Kuroiwa T., Yamasaki M., Kanemura Y., Shizuko I., Shimazaki T., Onodera M., Okano H., Mizusawa H. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J. Neurosci. Res. 2004, 78:215-223.
84. Iwanami A., Kaneko S., Nakamura M., Kanemura Y., Mori H., Kobayashi S., Yamasaki M., Momoshima S., Ishii H., Ando K., Tanioka Y., Tamaoki N., Nomura T., Toyama Y., Okano H. Transplantation of human neural stem cells for spinal cord injury in primates. J. Neurosci. Res. 2005, 80:182-190.
85. Jeong S.W., Chu K., Jung K.H., Kim S.U., Kim M., Roh J.K. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 2003, 34:2258-2263.
86. Jepson S., Vought B., Gross C.H., Gan L., Austen D., Frantz J.D., Zwahlen J., Lowe D., Markland W., Krauss R. LINGO-1, a transmembrane signaling protein, inhibits oligodendrocyte differentiation and myelination through intercellular self-interactions. J. Biol. Chem. 2012, 287:22184-22195.
87. Jiang Q., Zhang Z.G., Ding G.L., Silver B., Zhang L., Meng H., Lu M., Pourabdillah-Nejed D.S., Wang L., Savant-Bhonsale S., Li L., Bagher-Ebadian H., Hu J., Arbab A.S., Vanguri P., Ewing J.R., Ledbetter K.A., Chopp M. MRI detects white matter reorganization after neural progenitor cell treatment of stroke. NeuroImage 2006, 32:1080-1089.
88. Jin K., Mao X., Xie L., Galvan V., Lai B., Wang Y., Gorostiza O., Wang X., Greenberg D.A. Transplantation of human neural precursor cells in Matrigel scaffolding improves outcome from focal cerebral ischemia after delayed postischemic treatment in rats. J. Cereb. Blood Flow Metab. 2010, 30:534-544.
89. Jin K., Xie L., Mao X., Greenberg M.B., Moore A., Peng B., Greenberg R.B., Greenberg D.A. Effect of human neural precursor cell transplantation on endogenous neurogenesis after focal cerebral ischemia in the rat. Brain Res. 2011, 1374:56-62.
90. Johnson P.J., Tatara A., McCreedy D.A., Shiu A., Sakiyama-Elbert S.E. Tissue-engineered fibrin scaffolds containing neural progenitors enhance functional recovery in a subacute model of SCI. Soft Matter 2010, 6:5127-5137.
91. Kakulas B.A. Neuropathology: the foundation for new treatments in spinal cord injury. Spinal Cord 2004, 42:549-563.
92. Kamei N., Tanaka N., Oishi Y., Hamasaki T., Nakanishi K., Sakai N., Ochi M. BDNF, NT-3, and NGF released from transplanted neural progenitor cells promote corticospinal axon growth in organotypic cocultures. Spine 2007, 32:1272-1278.
93. Karimi-Abdolrezaee S., Eftekharpour E., Wang J., Morshead C.M., Fehlings M.G. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 2006, 26:3377-3389.
94. Karimi-Abdolrezaee S., Eftekharpour E., Wang J., Schut D., Fehlings M.G. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J. Neurosci. 2010, 30:1657-1676.
95. Kelly S., Bliss T.M., Shah A.K., Sun G.H., Ma M., Foo W.C., Masel J., Yenari M.A., Weissman I.L., Uchida N., Palmer T., Steinberg G.K. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11839-11844.
96. Kim S.Y., Cho H.S., Yang S.H., Shin J.Y., Kim J.S., Lee S.T., Chu K., Roh J.K., Kim S.U., Park C.G. Soluble mediators from human neural stem cells play a critical role in suppression of T-cell activation and proliferation. J. Neurosci. Res. 2009, 87:2264-2272.
97. Knight J.C., Scharf E.L., Mao-Draayer Y. Fas activation increases neural progenitor cell survival. J. Neurosci. Res. 2010, 88:746-757.
98. Kokaia Z., Martino G., Schwartz M., Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair?. Nat. Neurosci. 2012, 15:1078-1087.
99. Kusano K., Enomoto M., Hirai T., Tsoulfas P., Sotome S., Shinomiya K., Okawa A. Transplanted neural progenitor cells expressing mutant NT3 promote myelination and partial hindlimb recovery in the chronic phase after spinal cord injury. Biochem. Biophys. Res. Commun. 2010, 393:812-817.
100. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27:2596-2605.
101. Lee H.J., Kim K.S., Park I.H., Kim S.U. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS One 2007, 2:e156.
102. Lee S.T., Chu K., Jung K.H., Kim S.J., Kim D.H., Kang K.M., Hong N.H., Kim J.H., Ban J.J., Park H.K., Kim S.U., Park C.G., Lee S.K., Kim M., Roh J.K. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 2008, 131:616-629.
103. Lee S.I., Kim B.G., Hwang D.H., Kim H.M., Kim S.U. Overexpression of Bcl-XL in human neural stem cells promotes graft survival and functional recovery following transplantation in spinal cord injury. J. Neurosci. Res. 2009, 87:3186-3197.
104. Lepore A.C., Fischer I. Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp. Neurol. 2005, 194:230-242.
105. Lepore A.C., Maragakis N.J. Targeted stem cell transplantation strategies in ALS. Neurochem. Int. 2007, 50:966-975.
106. Lepore A.C., Neuhuber B., Connors T.M., Han S.S., Liu Y., Daniels M.P., Rao M.S., Fischer I. Long-term fate of neural precursor cells following transplantation into developing and adult CNS. Neuroscience 2006, 139:513-530.
107. Li S., Stys P.K. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J. Neurosci. 2000, 20:1190-1198.
108. Lindvall O., Kokaia Z. Stem cell research in stroke: how far from the clinic?. Stroke 2011, 42:2369-2375.
109. Liu Y.P., Lang B.T., Baskaya M.K., Dempsey R.J., Vemuganti R. The potential of neural stem cells to repair stroke-induced brain damage. Acta Neuropathol. 2009, 117:469-480.
110. Lobsiger C.S., Cleveland D.W. Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat. Neurosci. 2007, 10:1355-1360.
111. Lu P., Jones L.L., Snyder E.Y., Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol. 2003, 181:115-129.
112. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 2000, 47:707-717.
113. Macias M.Y., Syring M.B., Pizzi M.A., Crowe M.J., Alexanian A.R., Kurpad S.N. Pain with no gain: allodynia following neural stem cell transplantation in spinal cord injury. Exp. Neurol. 2006, 201:335-348.
114. Martino G., Pluchino S. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 2006, 7:395-406.
115. Martino G., Pluchino S. Neural stem cells: guardians of the brain. Nat. Cell Biol. 2007, 9:1031-1034.
116. Martino G., Franklin R.J., Baron Van Evercooren A., Kerr D.A., G. Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat. Rev. Neurol. 2010, 6:247-255. and Stem Cells in Multiple Sclerosis Consensus.
117. Martino G., Pluchino S., Bonfanti L., Schwartz M. Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiol. Rev. 2011, 91:1281-1304.
118. Mason J.L., Ye P., Suzuki K., D'Ercole A.J., Matsushima G.K. Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J. Neurosci. 2000, 20:5703-5708.
119. McGill T.J., Cottam B., Lu B., Wang S., Girman S., Tian C., Huhn S.L., Lund R.D., Capela A. Transplantation of human central nervous system stem cells - neuroprotection in retinal degeneration. Eur. J. Neurosci. 2012, 35:468-477.
120. Modo M., Stroemer R.P., Tang E., Patel S., Hodges H. Effects of implantation site of stem cell grafts on behavioral recovery from stroke damage. Stroke 2002, 33:2270-2278.
121. Mothe A.J., Zahir T., Santaguida C., Cook D., Tator C.H. Neural stem/progenitor cells from the adult human spinal cord are multipotent and self-renewing and differentiate after transplantation. PLoS One 2011, 6:e27079.
122. Noble L.J., Wrathall J.R. Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 1989, 482:57-66.
123. Nori S., Okada Y., Yasuda A., Tsuji O., Takahashi Y., Kobayashi Y., Fujiyoshi K., Koike M., Uchiyama Y., Ikeda E., Toyama Y., Yamanaka S., Nakamura M., Okano H. Grafted human-induced pluripotent stem-cell-derived neurospheres promote motor functional recovery after spinal cord injury in mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:16825-16830.
124. Noseworthy J.H., Lucchinetti C., Rodriguez M., Weinshenker B.G. Multiple sclerosis. N. Engl. J. Med. 2000, 343:938-952.
125. Oh J.S., Kim K.N., An S.S., Pennant W.A., Kim H.J., Gwak S.J., Yoon D.H., Lim M.H., Choi B.H., Ha Y. Co-transplantation of Mouse Neural Stem Sells (mNSCs) with Adipose Tissue-derived Mesenchymal Stem Sells Improves mNSC Survival in a Rat Spinal Cord Injury Model. Cell Transplant 2010, 20:837-849.
126. Ourednik J., Ourednik V., Lynch W.P., Schachner M., Snyder E.Y. Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat. Biotechnol. 2002, 20:1103-1110.
127. Park K.I., Teng Y.D., Snyder E.Y. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat. Biotechnol. 2002, 20:1111-1117.
128. Park D.H., Eve D.J., Chung Y.G., Sanberg P.R. Regenerative medicine for neurological disorders. ScientificWorldJournal 2010, 10:470-489.
129. Parr A.M., Kulbatski I., Tator C.H. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J. Neurotrauma 2007, 24:835-845.
130. Parr A.M., Kulbatski I., Zahir T., Wang X., Yue C., Keating A., Tator C.H. Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 2008, 155:760-770.
131. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., Sorensen P.S., Bruck W., Lucchinetti C., Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006, 129:3165-3172.
132. Payne N., Siatskas C., Barnard A., Bernard C.C. The prospect of stem cells as multi-faceted purveyors of immune modulation, repair and regeneration in multiple sclerosis. Curr. Stem Cell Res. Ther. 2011, 6:50-62.
133. Pfeifer K., Vroemen M., Blesch A., Weidner N. Adult neural progenitor cells provide a permissive guiding substrate for corticospinal axon growth following spinal cord injury. Eur. J. Neurosci. 2004, 20:1695-1704.
134. Pignataro G., Studer F.E., Wilz A., Simon R.P., Boison D. Neuroprotection in ischemic mouse brain induced by stem cell-derived brain implants. J. Cereb. Blood Flow Metab. 2007, 27:919-927.
135. Pluchino S., Martino G. The therapeutic plasticity of neural stem/precursor cells in multiple sclerosis. J. Neurol. Sci. 2008, 265:105-110.
136. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L., Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 2003, 422:688-694.
137. Pluchino S., Furlan R., Martino G. Cell-based remyelinating therapies in multiple sclerosis: evidence from experimental studies. Curr. Opin. Neurol. 2004, 17:247-255.
138. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., Martinello M., Cattalini A., Bergami A., Furlan R., Comi G., Constantin G., Martino G. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005, 436:266-271.
139. Pluchino S., Gritti A., Blezer E., Amadio S., Brambilla E., Borsellino G., Cossetti C., Del Carro U., Comi G., t Hart B., Vescovi A., Martino G. Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates. Ann. Neurol. 2009, 66:343-354.
140. Pluchino S., Zanotti L., Brambilla E., Rovere-Querini P., Capobianco A., Alfaro-Cervello C., Salani G., Cossetti C., Borsellino G., Battistini L., Ponzoni M., Doglioni C., Garcia-Verdugo J.M., Comi G., Manfredi A.A., Martino G. Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One 2009, 4:e5959.
141. Pluchino S., Cusimano M., Bacigaluppi M., Martino G. Remodelling the injured CNS through the establishment of atypical ectopic perivascular neural stem cell niches. Arch. Ital. Biol. 2010, 148:173-183.
142. Pollock K., Stroemer P., Patel S., Stevanato L., Hope A., Miljan E., Dong Z., Hodges H., Price J., Sinden J.D. A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke. Exp. Neurol. 2006, 199:143-155.
143. Prineas J.W., Barnard R.O., Kwon E.E., Sharer L.R., Cho E.S. Multiple sclerosis: remyelination of nascent lesions. Ann. Neurol. 1993, 33:137-151.
144. Raine C.S., Wu E. Multiple sclerosis: remyelination in acute lesions. J. Neuropathol. Exp. Neurol. 1993, 52:199-204.
145. Rayment E.A., Williams D.J. Concise review: mind the gap: challenges in characterizing and quantifying cell- and tissue-based therapies for clinical translation. Stem Cells 2010, 28:996-1004.
146. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
147. Riley J., Federici T., Polak M., Kelly C., Glass J., Raore B., Taub J., Kesner V., Feldman E.L., Boulis N.M. Intraspinal stem cell transplantation in amyotrophic lateral sclerosis: a phase I safety trial, technical note, and lumbar safety outcomes. Neurosurgery 2012, 71:405-416.
148. Roitberg B.Z., Mangubat E., Chen E.Y., Sugaya K., Thulborn K.R., Kordower J.H., Pawar A., Konecny T., Emborg M.E. Survival and early differentiation of human neural stem cells transplanted in a nonhuman primate model of stroke. J. Neurosurg. 2006, 105:96-102.
149. Rowland J.W., Hawryluk G.W., Kwon B., Fehlings M.G. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg. Focus. 2008, 25:E2.
150. Ruckh J.M., Zhao J.W., Shadrach J.L., van Wijngaarden P., Rao T.N., Wagers A.J., Franklin R.J. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 2012, 10:96-103.
151. Sahni V., Kessler J.A. Stem cell therapies for spinal cord injury. Nat. Rev. Neurol. 2010, 6:363-372.
152. Salazar D.L., Uchida N., Hamers F.P., Cummings B.J., Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in an early chronic spinal cord injury NOD-scid mouse model. PLoS One 2010, 5:e12272.
153. Shen C.C., Lin C.H., Yang Y.C., Chiao M.T., Cheng W.Y., Ko J.L. Intravenous implanted neural stem cells migrate to injury site, reduce infarct volume, and improve behavior after cerebral ischemia. Curr. Neurovasc. Res. 2010, 7:167-179.
154. Sher F., Amor S., Gerritsen W., Baker D., Jackson S.L., Boddeke E., Copray S. Intraventricularly injected Olig2-NSCs attenuate established relapsing-remitting EAE in mice. Cell Transplant 2012, 21:1883-1897.
155. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
156. Steiner R., Huhn S., Koch T., Al-Uzri A., Guillaime D., Sutcliffe T., Vogel H., Selden N. CNS transplantation of purified human neural stem cells in infantile and late-infantile neuronal ceroid lipofuscinoses: summary of the phase I trial. Mol. Genet. Metab. 2010, 99:S35.
157. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat. Med. 2007, 13:139-145.
158. Stoodley M.A. Pathophysiology of syringomyelia. J. Neurosurg. 2000, 92:1069-1070. (author reply 1071-1063).
159. Stroemer P., Patel S., Hope A., Oliveira C., Pollock K., Sinden J. The neural stem cell line CTX0E03 promotes behavioral recovery and endogenous neurogenesis after experimental stroke in a dose-dependent fashion. Neurorehabil. Neural Repair 2009, 23:895-909.
160. Sun C., Zhang H., Li J., Huang H., Cheng H., Wang Y., Li P., An Y. Modulation of the major histocompatibility complex by neural stem cell-derived neurotrophic factors used for regenerative therapy in a rat model of stroke. J. Transl. Med. 2010, 8:77.
161. Syed Y.A., Hand E., Mobius W., Zhao C., Hofer M., Nave K.A., Kotter M.R. Inhibition of CNS remyelination by the presence of semaphorin 3A. J. Neurosci. 2011, 31:3719-3728.
162. Takahashi K., Yasuhara T., Shingo T., Muraoka K., Kameda M., Takeuchi A., Yano A., Kurozumi K., Agari T., Miyoshi Y., Kinugasa K., Date I. Embryonic neural stem cells transplanted in middle cerebral artery occlusion model of rats demonstrated potent therapeutic effects, compared to adult neural stem cells. Brain Res. 2008, 1234:172-182.
163. Takeuchi H., Natsume A., Wakabayashi T., Aoshima C., Shimato S., Ito M., Ishii J., Maeda Y., Hara M., Kim S.U., Yoshida J. Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci. Lett. 2007, 426:69-74.
164. Tamaki S.J., Jacobs Y., Dohse M., Capela A., Cooper J.D., Reitsma M., He D., Tushinski R., Belichenko P.V., Salehi A., Mobley W., Gage F.H., Huhn S., Tsukamoto A.S., Weissman I.L., Uchida N. Neuroprotection of host cells by human central nervous system stem cells in a mouse model of infantile neuronal ceroid lipofuscinosis. Cell Stem Cell 2009, 5:310-319.
165. Tator C.H., Koyanagi I. Vascular mechanisms in the pathophysiology of human spinal cord injury. J. Neurosurg. 1997, 86:483-492.
166. Taylor L., Jones L., Tuszynski M.H., Blesch A. Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 2006, 26:9713-9721.
167. Teng Y.D., Lavik E.B., Qu X., Park K.I., Ourednik J., Zurakowski D., Langer R., Snyder E.Y. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3024-3029.
168. Teng Y.D., Yu D., Ropper A.E., Li J., Kabatas S., Wakeman D.R., Wang J., Sullivan M.P., Redmond D.E., Langer R., Snyder E.Y., Sidman R.L. Functional multipotency of stem cells: a conceptual review of neurotrophic factor-based evidence and its role in translational research. Curr. Neuropharmacol. 2011, 9:574-585.
169. Tobias C.A., Shumsky J.S., Shibata M., Tuszynski M.H., Fischer I., Tessler A., Murray M. Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp. Neurol. 2003, 184:97-113.
170. Tymianski M., Wallace M.C., Spigelman I., Uno M., Carlen P.L., Tator C.H., Charlton M.P. Cell-permeant Ca2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 1993, 11:221-235.
171. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 2008, 8:726-736.
172. Uchida N., Chen K., Dohse M., Hansen K.D., Dean J., Buser J.R., Riddle A., Beardsley D.J., Wan Y., Gong X., Nguyen T., Cummings B.J., Anderson A.J., Tamaki S.J., Tsukamoto A., Weissman I.L., Matsumoto S.G., Sherman L.S., Kroenke C.D., Back S.A. Human neural stem cells induce functional myelination in mice with severe dysmyelination. Sci. Transl. Med. 2012, 4:155ra136.
173. van den Berg M.E., Castellote J.M., Mahillo-Fernandez I., de Pedro-Cuesta J. Incidence of spinal cord injury worldwide: a systematic review. Neuroepidemiology 2010, 34:184-192. (discussion 192).
174. Vroemen M., Aigner L., Winkler J., Weidner N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur. J. Neurosci. 2003, 18:743-751.
175. Wang G., Ao Q., Gong K., Zuo H., Gong Y., Zhang X. Synergistic effect of neural stem cells and olfactory ensheathing cells on repair of adult rat spinal cord injury. Cell Transplant. 2010, 19:1325-1337.
176. Wang M., Zhai P., Chen X., Schreyer D.J., Sun X., Cui F. Bioengineered scaffolds for spinal cord repair. Tissue Eng. Part B Rev. 2011, 17:177-194.
177. Watanabe T., Yamamoto T., Abe Y., Saito N., Kumagai T., Kayama H. Differential activation of microglia after experimental spinal cord injury. J. Neurotrauma 1999, 16:255-265.
178. Wei L., Cui L., Snider B.J., Rivkin M., Yu S.S., Lee C.S., Adams L.D., Gottlieb D.I., Johnson E.M., Yu S.P., Choi D.W. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol. Dis. 2005, 19:183-193.
179. Wilson J.R., Cadotte D.W., Fehlings M.G. Clinical predictors of neurological outcome, functional status, and survival after traumatic spinal cord injury: a systematic review. J. Neurosurg. Spine 2012, 17:11-26.
180. Windrem M.S., Nunes M.C., Rashbaum W.K., Schwartz T.H., Goodman R.A., McKhann G., Roy N.S., Goldman S.A. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 2004, 10:93-97.
181. Windrem M.S., Schanz S.J., Guo M., Tian G.F., Washco V., Stanwood N., Rasband M., Roy N.S., Nedergaard M., Havton L.A., Wang S., Goldman S.A. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008, 2:553-565.
182. Wingerchuk D.M., Lucchinetti C.F., Noseworthy J.H. Multiple sclerosis: current pathophysiological concepts. Lab. Invest. 2001, 81:263-281.
183. Wu W., Chen X., Hu C., Li J., Yu Z., Cai W. Transplantation of neural stem cells expressing hypoxia-inducible factor-1alpha (HIF-1alpha) improves behavioral recovery in a rat stroke model. J. Clin. Neurosci. 2010, 17:92-95.
184. Xiong Y., Zhu J.X., Fang Z.Y., Zeng C.G., Zhang C., Qi G.L., Li M.H., Zhang W., Quan D.P., Wan J. Coseeded Schwann cells myelinate neurites from differentiated neural stem cells in neurotrophin-3-loaded PLGA carriers. Int. J. Nanomedicine 2012, 7:1977-1989.
185. Yan J., Xu L., Welsh A.M., Hatfield G., Hazel T., Johe K., Koliatsos V.E. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med. 2007, 4:e39.
186. Yang J., Jiang Z., Fitzgerald D.C., Ma C., Yu S., Li H., Zhao Z., Li Y., Ciric B., Curtis M., Rostami A., Zhang G.X. Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J. Clin. Invest. 2009, 119:3678-3691.
187. Yang J., Yan Y., Ma C.G., Kang T., Zhang N., Gran B., Xu H., Li K., Ciric B., Zangaladze A., Curtis M., Rostami A., Zhang G.X. Accelerated and enhanced effect of CCR5-transduced bone marrow neural stem cells on autoimmune encephalomyelitis. Acta Neuropathol. 2012, 124:491-503.
188. Yasuda A., Tsuji O., Shibata S., Nori S., Takano M., Kobayashi Y., Takahashi Y., Fujiyoshi K., Hara C.M., Miyawaki A., Okano H.J., Toyama Y., Nakamura M., Okano H. Significance of remyelination by neural stem/progenitor cells transplanted into the injured spinal cord. Stem Cells 2011, 29:1983-1994.
189. Zeng X., Zeng Y.S., Ma Y.H., Lu L.Y., Du B.L., Zhang W., Li Y., Chan W.Y. Bone Marrow Mesenchymal Stem Cells in a Three Dimensional Gelatin Sponge Scaffold Attenuate Inflammation, Promote Angiogenesis and Reduce Cavity Formation in Experimental Spinal Cord Injury. Cell Transplant 2011, 20:1881-1899.
190. Zhang Z.G., Jiang Q., Zhang R., Zhang L., Wang L., Zhang L., Arniego P., Ho K.L., Chopp M. Magnetic resonance imaging and neurosphere therapy of stroke in rat. Ann. Neurol. 2003, 53:259-263.
191. Zhang P., Li J., Liu Y., Chen X., Kang Q., Zhao J., Li W. Human neural stem cell transplantation attenuates apoptosis and improves neurological functions after cerebral ischemia in rats. Acta Anaesthesiol. Scand. 2009, 53:1184-1191.
192. Zhang P., Li J., Liu Y., Chen X., Lu H., Kang Q., Li W., Gao M. Human embryonic neural stem cell transplantation increases subventricular zone cell proliferation and promotes peri-infarct angiogenesis after focal cerebral ischemia. Neuropathology 2011, 31:384-391.
193. Ziv Y., Avidan H., Pluchino S., Martino G., Schwartz M. Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13174-13179.
194. Zujovic V., Doucerain C., Hidalgo A., Bachelin C., Lachapelle F., Weissert R., Stadelmann C., Linington C., Evercooren A.B. Exogenous schwann cells migrate, remyelinate and promote clinical recovery in experimental auto-immune encephalomyelitis. PLoS One 2012, 7:e42667.