Neural stem cells and the quest for restorative neurology

Histology and Histopathology

Volumn 19, Issue 1, 2004, Pages 271-280

  Luque, Juan M ^a   Gimenez y Ribotta M ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

Astrocyte; Brain stroke; Cellular therapy; Ependymocyte; GFAP; Multiple sclerosis; Neurodegeneration; Neurogenesis; Neuroregeneration; Parkinson's disease; Radial glia; Spinal cord injury; Stem cells; Stem niche; Subgranular zone; Subventricular zone

Indexed keywords

CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL TRIAL; HUMAN; MEDICAL LITERATURE; MEDICAL RESEARCH; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROLOGIC DISEASE; NEUROLOGY; NONHUMAN; PARKINSON DISEASE; REVIEW; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; STROKE; TISSUE REPAIR; TREATMENT INDICATION;

ANIMALS; CELL DIFFERENTIATION; CEREBROVASCULAR ACCIDENT; HUMANS; MULTIPLE SCLEROSIS; NEUROLOGY; NEURONS; PARKINSON DISEASE; RESEARCH; SPINAL CORD INJURIES; STEM CELLS;

EID: 1642474370     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (106)

1. Alvarez-Buylla A., Theelen M. and Nottebohm F. (1990). Proliferation "hot spots" in adult avian ventricular zone reveal radial cell division. Neuron 5, 101-109.
2. Alvarez-Buylla A., García-Verdugo J.M. and Tramontin A.D. (2001). A unified hipothesis on the lineage of neural stem cells. Nature Rev. Neurosci. 2, 287-293.
3. Akiyama Y., Honmou O., Kato T., Uede T., Hashi K. and Kocsis J.D. (2001). Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp. Neurol. 167, 27-39.
4. Arenas E. (2002). Stem cells in the treatment of Parkinson's disease. Brain Res. Bull. 57, 795-808.
5. Armstrong R.J. and Barker R.A. (2001). Neurodegeneration: A failure of neuroregeneration? Lancet 358, 1174-1176.
6. Arvidsson A., Collin T., Kirik D., Kokaia Z. and Lindvall O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nature Med. 8, 963-970.
7. Assmus B., Schchinger V., Teupe C., Britten M., Lehmann R., Dobert N., Grunwald F., Aicher A., Urbich C., Martin H., Hoelzer D., Dimmeler S. and Zeiher A.M. (2002). Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106, 3009-3017.
8. Björklund L.M., Sánchez-Pernaute R., Chung S., Andersson T., Chen I.Y., McNaught K.S., Brownell A.L., Jenkins B.G., Wahlestedt C., Kim K.S. and Isacson O. (2002). Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci.USA 99, 2344-2349.
9. Blau H.M., Brazelton T.R. and Weimann J.M. (2001). The evolving concept of a stem cell: Entity or function? Cell 105, 829-841.
10. Brazel C.Y., Romanko M.J., Rothstein R.P. and Levison S.W. (2003). Roles of the mammalian subventricular zone in brain development. Prog. Neurobiol. 69, 49-69.
11. Cairns K. and Finklestein S.P. (2003). Growth factors and stem cells as treatments for stroke recovery. Phys. Med. Rehabil. Clin. N. Am. 14, S135-142.
12. Cao Q.L., Zhang Y.P., Howard R.M., Walters W.M., Tsoulfas P. and Whittemore S.R. (2001). Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord care restricted to a glial lineage. Exp. Neurol. 167, 48-58.
13. Cao Q.L., Howard R.M., Dennison J.B. and Whittemore S.R. (2002). Differentiation of engrafted neuronal-restricted precursors cells is inhibited in the traumatically injured spinal cord. Exp. Neurol. 177, 349-359.
14. Capela A. and Temple S. (2002). LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35, 865-875.
15. Chiasson B.J., Tropepe V., Morshead C.M. and van der Kooy D. (1999). Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J. Neurosci. 19, 4462-4471.
16. Clarke D.L. and Frisen J. (2001). Differentiation potential of adult stem cells. Curr. Opin. Genet. Dev. 11, 575-580.
17. Clarke D.L., Johansson C.B., Wilbertz J., Veress B., Nilsson E., Karlstrom H., Lendhal U. and Frisen J. (2000). Generalized potential of adult neural stem cell. Science 288, 1559-1561.
18. David S. and Lacroix S. (2003). Molecular approaches to spinal cord repair. Annu. Rev. Neurosci. 26, 411-440.
19. DeAzevedo L.C., Fallet C., Moura-Nieto V., Daumas-Duport C., Hedin-Pereira C. and Lent R. (2003). Cortical radial glia cells in human fetuses: Depth-correlated transformation into astrocytes. J. Neurobiol. 55, 288-298.
20. Doetsch F., Caille I., Lim D.A., García-Verdugo J.M. and Alvarez-Buylla A. (1999). SVZ astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
21. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M. and Alvarez-Buylla A. (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36, 1021-1034.
22. Dupin E., Real C., Glavieux-Pardanaud C., Vaigot P., Le Douarin N.M. (2003). Reversal of developmental restrictions in neural crest lineages: Transition from Schwann cells to glial-melanocytic precursors in vitro. Proc. Natl. Acad. Sci. USA 100, 5229-5233.
23. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S, Trojanowski J.Q., Eidelberg D. and Fahn S. (2001). Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719.
24. Frisen J. (2002). Stem cell plasticity? Neuron 35, 415-418.
25. Fuchs E. and Segre J.A. (2000). Stem cells: A new lease on life. Cell 100, 143-155.
26. Gage F.H. (2000). Mammalian neural stem cells. Science 287, 1433-1438.
27. Galli R., Gritti A., Bonfanti L. and Vescovi A.L. (2003). Neural stem cells, an overview. Circ. Res. 92, 598-608.
28. Giménez y Ribotta M. and Privat A. (1998). Biological interventions for spinal cord injury. Curr. Opin. Neurol. 11, 647-654.
29. Giménez y Ribotta M., Langa F., Menet V. and Privat A. (2000). Comparative anatomy of the cerebellar cortex in mice lacking vimentin, GFAP, and both vimentin and GFAP. Glia 31, 69-83.
30. Giménez y Ribotta M., Gaviria M., Menet V. and Privat A. (2002). Strategies for regeneration and repair in spinal cord traumatic injury. Prog. Brain Res. 137, 191-212.
31. Gomi H., Yokoyama T., Fujimoto K., Ikeda T., Katoh A., Itoh T. and Itohara S. (1995). Mice devoid of the glial fibrillary acidic protein develop normally and are susceptible to scrapie prions. Neuron 14, 29-41.
32. Gray G.E. and Sanes J.R. (1992). Lineage of radial glia in the chicken optic tectum. Development 114, 271-283.
33. Hanbury R., Ling Z.D., Wuu J. and Kordower J.H. (2003). GFAP knockout mice have increased levels in GDNF that protect striatal neurons from metabolic and excitotoxic insults. J. Comp. Neurol. 461, 307-316.
34. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A. and Götz M. (2002). Glial cells generate neurons: The role of transcription factor Pax6. Nature Neurosci. 5, 308-315.
35. Hoehn M., Kustermann E., Blunk J., Wiedermann D., Trapp T., Wecker S., Focking M., Arnold H., Hescheler J., Fleischmann B.K., Schwindt W. and Buhrle C. (2002). Monitoring of implanted stem cell migration in vivo: A highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc. Natl. Acad. Sci. USA 99, 16267-16272.
36. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J. and Gage F.H. (2000). Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20, 2218-2228.
37. Horner P.J. and Gage F.H. (2000). Regenerating the damaged central nervous system. Nature 407, 963-970.
38. Imamura T., Kornblum H.I. and Sofroniew M.V. (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci. 23, 2824-2832.
39. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-González X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A. and Verfaillie C.M. (2002a). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49.
40. Jiang Y., Vaessen B., Lenvik T., Blackstad M., Reyes M. and Verfaillie C.M. (2002b). Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle and brain. Exp. Hematol. 30, 896-904.
41. Johansson C.B., Momma S., Clarke D.L., Risling M. and Frisen J. (1999). Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96, 25-34.
42. Kim J.-H., Auerbach JM., Rodríguez-Gómez J.A., Velasco I., Gavin D., Lumelsky N., Lee S.-H., Nguyen J., Sánchez-Pernaute R., Bankiewicz K. and McKay R. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56.
43. Kinouchi R., Takeda M., Yang L., Wilhemsson U., Lundkvist A., Pekny M. and Chen D.F. (2003). Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nature Neurosci. 6, 863-868.
44. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C. and Steindler D.A. (2000). Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl. Acad. Sci. USA 97, 13883-13888.
45. Liedtke W., Eldelmann W., Bieri P.L., Chiu F.C. Cowan N.J., Kucherlapati R. and Raine C.S. (1996). GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17, 607-615.
46. Liedtke W., Edelmann W., Chiu F.-C., Kucherlapati R. and Raine C.S. (1998). Experimental autoimmune encephalomyelitis in mice lacking glial fibrillary acidic protein is characterized by a more severe clinical course and an infiltrative central nervous system lesion. Am. J. Pathol. 152, 251-259.
47. Lindvall O. (2003). Stem cells for cell therapy in Parkinson's disease. Pharmacol. Res. 47, 279-287.
48. Liu S., Qu Y., Stewart T.J., Howard M.J., Chkrabortty S., Holekamp T.F. and McDonald J.W. (2000). Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl. Acad. Sci. USA 97, 6126-6131.
49. Loeffler M. and Roeder I. (2003). Tissue stem cells: Definition, plasticity, heterogeneity, self-organization and models. A conceptual approach. Cells Tissues Organs 171, 8-26.
50. Luque J.M., Morante-Oria J. and Fairén A. (2003). Localization of ApoER2, VLDLR and Dab1 in radial glia: Groundwork for a new model of reelin action during cortical development. Dev. Brain Res. 140, 195-203.
51. Malatesta P., Hartfuss E. and Gotz M. (2000). Isolation of radial glial cells by fluorescent-activated cell sorting reveals neuronal lineage. Development 127, 5253-5263.
52. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F. and Gotz M. (2003). Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 37, 751-764.
53. Marin-Padilla M. (1995). Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocyte in the human cerebral cortex: A Golgi study. J. Comp. Neurol. 357, 554-572.
54. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I. and Choi D.W. (1999). Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med. 5, 1410-1412.
55. McKay R. (1997). Stem cells in the central nervous system. Science 276, 66-71.
56. Menet V., Giménez y Ribotta M., Sandillon F. and Privat A. (2000). GFAP null astrocytes are a favorable substrate for neuronal survival and neurite growth. Glia 31, 267-272.
57. Menet V., Giménez y Ribotta M., Chauvet N., Drian M.J., Lannoy J., Colucci-Guyon E. and Privat A. (2001). Inactivation of the glial fibrillay acidic protein gene, but not that of vimentin, improves neuronal survival and neurite growth by modifying adhesion molecule expression. J. Neurosci. 21, 6147-6158.
58. Menet V., Prieto M., Privat A. and Giménez y Ribotta M. (2003). Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc. Natl. Acad. Sci. USA 100, 8999-9004.
59. Mercier F., Kitasako J.T. and Hatton G.I. (2002). Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network. J. Comp. Neurol. 451, 170-188.
60. Mercier F., Kitasako J.T. and Hatton G.I. (2003). Fractones and other basal laminae in the hypothalamus. J. Comp. Neurol. 455, 324-340.
61. Messing A. and Brenner M. (2003). GFAP: Functional implications gleaned from studies of genetically engineered mice. Glia 43, 87-90.
62. Mi H. and Barres B.A. (1999). Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J. Neurosci. 19, 1049-1061.
63. Miyamura T., Morita N., Baba H., Hase S., Kajimoto T., Tsuji S., Kawata M., Kato I., Mikoshiba K. and Ikenaka K. (1998). Metabolic labelling of a subset of glial cells by UDP-galactose: Implication for astrocyte lineage diversity. J. Neurosci. Res. 52, 173-183.
64. Miyata T., Kawaguchi A., Okano H. and Ogawa M. (2001). Asymmetric inheritance of radial glia fibers by cortical neurons. Neuron 31, 727-741.
65. Modo M., Stroemer R.P., Tang E., Patel S. and Hodges H. (2002). Effects of implantation site of stem cell grafts on behavioural recovery from stroke damage. Stroke 33, 2270-2278.
66. Morrison S., Shah N.M. and Anderson D.J. (1997). Regulatory mechanisms in stem cell biology. Cell 88, 287-298.
67. Morrison S.J. (2001). Neuronal potential and lineage determination by neural stem cells. Curr. Opin. Cell Biol. 13, 666-672.
68. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T. and Nakafuku M. (2002). Regeneration of hippocampal piramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441.
69. Nawashiro F., Brenner M., Fukui S., Shima K. and Hallenbeck J.M. (2002). High susceptibility to cerebral ischemia in GFAP-null mice. J. Cereb. Blood Flow Metab. 20, 1040-1044.
70. Nishimura F., Yoshikawa M., Kanda S., Nonaka M., Yokota H., Shiroi A., Nakase H., Hirabayashi H., Ouji Y., Birumachi J., Ishizaka S. and Sakaki T. (2003). Potential use of embryonic stem cells for the treatment of mouse parkinsonian models: Improved behavior by transplantation of in vitro differentiated dopaminergic neurons from embryonic stem cells. Stem Cells 21, 171-180.
71. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S. and Kriegstein A.R. (2001). Neurons derived from radial glia cells establish radil units in neocortex. Nature 409, 714-720.
72. Nottebohm F. (2002). Neuronal replacement in adult brain. Brain Res. Bull. 57, 737-749.
73. Ogawa Y., Sawamoto K., Miyata T., Miyao S., Watanabe M., Nakamura M., Bregman B.S., Koike M., Uchiyama Y., Toyama Y. and Okano H. (2002). Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adults rats. J Nuurosci. Res. 15, 925-933.
74. Olanow C.W. and Tatton W.G. (1999). Etiology and pathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 22, 123-144.
75. Pekny M., Leveen P., Pekna M., Eliasson C., Berthold C.H., Westemark B. and Betsholtz C. (1995). Mice lacking glial fibrillary acidic protein display astrocytes devoid of intermediate filaments but develop and reproduce normally. EMBO J. 14, 1590-1598.
76. Pekny M., Johansson C.B., Eliasson C., Stakeberg J., Wallen A., Perlmann T., Lendahl U., Betsholtz C. Berthold C.H. and Frisen J. (1999). Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J. Cell Biol. 145, 503-514.
77. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salan G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L. and Martino G. (2003). Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422, 688-694.
78. Potten C.S. and Loeffler M. (1990). Stem cells: Attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020.
79. Rickman M. and Wolff J.R. (1985). Prenatal gliogenesis in the neopallium of the rat. Adv. Anat. Embryol. Cell. Biol. 93, 1-104.
80. Riess P, Zhang C., Saatman K.E., Laurer H.L., Longhi L.G., Raghupathi R., Lenzlinger P.M., Lifschitz J., Boockvar J., Neugebauer E., Snyder E.Y. and McIntosh T.K. (2002). Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery 51, 1043-1052.
81. Roy N.S., Wang S., Jiang L., Kang J., Benraiss S., Harrison-Restelli C., Fraser R.A.R., Couldwell W.T., Kawaguchi A., Okano H., Nedergaard M., Goldman S. (2000). In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nature Med. 6, 271-277.
82. Savitz S.I., Rosenbaum D.M., Dinsmore J.H., Wechsler L.R. and Caplan L.R. (2002). Cell transplantation for stroke. Ann. Neurol. 52, 266-275.
83. Schuldiner M., Itskovitz-Eldor J, and Benvenisty N. (2003). Selective ablation of human embryonic stem cells expressing a "suicide" gene. Stem Cells 21, 257-265.
84. Seaberg R.M. and Van Der Kooy D. (2002). Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784-1793.
85. Seaberg R.M. and Van Der Kooy D. (2003). Stem and progenitor cells: The premature desertion of rigorous definitions. Trends Neurosci. 26, 125-131.
86. Seri B, García-Verdugo J.M., McEwen B.S. and Alvarez-Buylla A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 21, 7153-7160.
87. Shihabuddin L.S., Horner P.J., Ray J. and Gage F.H. (2000). Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 20, 8727-8735.
88. Spradling A., Drummond-Barbosa D. and Kai T. (2001). Stem cells find their niche. Nature 414, 98-104.
89. Steinman L. (2001). Multiple sclerosis: A two stage disease. Nature Immunol. 2, 762-764.
90. Stenman J., Toresson H. and Campbell K. (2003). Identification of two distinct progenitor populations in the lateral ganglionic eminence: Implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23, 167-174.
91. Svendsen C.N. and Smith A.G. (1999). New prospects for human stem-cell therapy in the nervous system. Trends Neurosci. 22, 357-364.
92. Takagi Y., Nozaki K., Takahashi J., Yodoi J., Ishikawa M. and Hashimoto N. (1999). Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice. Brain Res. 831, 283-287.
93. Takahashi M., Arai Y., Kurosawa H., Sueyoshi N. and Shirai S. (2003). Ependymal cell reactions in spinal cord segments after compression injury in adult rat. J. Neuropathol. Exp. Neurol. 62, 185-194.
94. Tamanaki N., Nakamura K., Okamoto K. and Kaneko T. (2001). Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41, 51-60.
95. Temple S. (2001a). Stem cell plasticity - Building the brain of our dreams. Nature Rev. 2, 513-520.
96. Temple S. (2001b). The development of neural stem cells. Nature 414, 112-117.
97. Tropepe V., Hitoshi S., Sirard C., Mak T.W., Rossant J. and Van Der Koody D. (2001). Direct neural fate specification from embryonic stem cells: A primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30, 65-78.
98. Vassilopoulos G., Wang P.R. and Russell D.W. (2003). Transplanted bone marrow regenerates liver by cell fusion. Nature 422, 901-904.
99. Wang X., Willenbring H., Akkari Y., Torimaru Y., Foster M., Al-Dhalimy M., Lagasse E., Finegold M., Olson S. and Grompe M. (2003). Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422, 897-901.
100. Weissman I.L. (2000). Stem cells: Units of development, units of regeneration, and units of evolution. Cell 100, 157-160.
101. Yamamoto S., Yamamoto N., Kitamura T., Nakamura K. and Nakafuku M. (2001). Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp. Neurol. 172, 115-127.
102. Yang M., Stull N.D., Berk M.A., Snyder E.Y. and Iacovitti L. (2002). Neural stem cells spontaneously express dopaminergic traits after transplantation into the intact or 6-hydroxydopamine-lesioned rat. Exp. Neurol. 177, 50-60.
103. Zhan S.-C. (2001). Defining glial cells during CNS development. Nature Rev. Neurosci. 2, 840-843.
104. Zhang Z.G., Zhang L., Jiang Q. and Chopp M. (2002). Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ. Res. 90, 284-288.
105. Zhang Z.G., Jian Q., Zhang R., Zhang L., Wang L., Zhang L., Arniego P., Ho K.-L. and Chopp M. (2003). Magnetic resonance imaging and neurosphere therapy of stroke in rat. Ann. Neurol. 53, 259-263.
106. Zhao L.R., Duan W.M., Reyes M., Keene C.D., Verfaillie C.M. and Low W.C. (2002). Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp. Neurol. 174, 11-20.