Brain regeneration in physiology and pathology: The immune signature driving therapeutic plasticity of neural stem cells

Physiological Reviews

Volumn 91, Issue 4, 2011, Pages 1281-1304

  Martino, Gianvito ^a,b,c,d   Pluchino, Stefano ^a,b,c,d   Bonfanti, Luca ^a,b,c,d   Schwartz, Michal ^a,b,c,d  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF TURIN   (Italy)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; BYSTANDER EFFECT; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROIMMUNOLOGY; NEUROPROTECTION; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STEM CELL NICHE; TISSUE INJURY;

ANIMALS; BRAIN; CELL COMMUNICATION; HUMANS; IMMUNE SYSTEM; NEURAL STEM CELLS; NEURONAL PLASTICITY; REGENERATION; STEM CELL TRANSPLANTATION;

EID: 79959635553     PISSN: 00319333     EISSN: 15221210     Source Type: Journal    
DOI: 10.1152/physrev.00032.2010     Document Type: Review

References (263)

1. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the bloodbrain barrier. Nat Rev Neurosci 7: 41-53, 2006.
2. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97: 12846-12851, 2000.
3. Agata K, Saito Y, Nakajima E. Unifying principles of regeneration I: epimorphosis versus morphallaxis. Dev Growth Differ 49: 73-78, 2007.
4. Agata K, Tanaka T, Kobayashi C, Kato K, Saitoh Y. Intercalary regeneration in planarians. Dev Dyn 226: 308-316, 2003.
5. 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 3: e3145, 2008.
6. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335, 1965.
7. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 41: 683-686, 2004.
8. Archer DR, Cuddon PA, Lipsitz D, Duncan ID. Myelination of the canine central nervous system by glial cell transplantation: a model for repair of human myelin disease. Nat Med 3: 54-59, 1997.
9. 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.
10. Bacigaluppi M, Pluchino S, Jametti LP, Kilic E, Kilic U, Salani G, Brambilla E, West MJ, Comi G, Martino G, Hermann DM. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132: 2239-2251, 2009.
11. Banerjee R, Mosley RL, Reynolds AD, Dhar A, Jackson-Lewis V, Gordon PH, Przedborski S, Gendelman HE. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One 3: e2740, 2008.
12. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70: 31-46, 1992.
13. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, Klinkert WE, Flugel-Koch C, Issekutz TB, Wekerle H, Flugel A. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462: 94-98, 2009.
14. Becker CG, Becker T. Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26: 71-80, 2008.
15. Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci USA 105: 15558-15563, 2008.
16. 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 41: 73-80, 2003.
17. Ben-Hur T, Goldman SA. Prospects of cell therapy for disorders of myelin. Ann NY Acad Sci 1142: 218-249, 2008.
18. Berry M, Hubbard P, Butt AM. Cytology and lineage of NG2-positive glia. J Neurocytol 31: 457-467, 2002.
19. Birnbaum KD, Sanchez A.A. Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710, 2008.
20. Bjorklund A. Cell therapy for Parkinson's disease: problems and prospects. Novartis Found Symp 265: 174-187, 2005.
21. Block GJ, Ohkouchi S, Fung F, Frenkel J, Gregory C, Pochampally R, Dimattia G, Sullivan DE, Prockop DJ. Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1. Stem Cells 27: 670-681, 2009.
22. Borchardt T, Braun T. Cardiovascular regeneration in non-mammalian model systems: what are the differences between newts and man? Thromb Haemost 98: 311-318, 2007.
23. Brockes JP, Kumar A. Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24: 525-549, 2008.
24. Brundin P, Li JY, Holton JL, Lindvall O, Revesz T. Research in motion: the enigma of Parkinson's disease pathology spread. Nat Rev Neurosci 9: 741-745, 2008.
25. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Gotz M. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci USA 105: 3581-3586, 2008.
26. Butovsky O, Kunis G, Koronyo-Hamaoui M, Schwartz M. Selective ablation of bone marrow-derived dendritic cells increases amyloid plaques in a mouse Alzheimer's disease model. Eur J Neurosci 26: 413-416, 2007.
27. Butovsky O, Landa G, Kunis G, Ziv Y, Avidan H, Greenberg N, Schwartz A, Smirnov I, Pollack A, Jung S, Schwartz M. Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116: 905-915, 2006.
28. Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M. Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol Cell Neurosci 29: 381-393, 2005.
29. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, 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 31: 149-160, 2006.
30. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M. Synantocytes: the fifth element. J Anat 207: 695-706, 2005.
31. Cannella B, Hoban CJ, Gao YL, Garcia-Arenas R, Lawson D, Marchionni M, Gwynne D, Raine CS. The neuregulin, glial growth factor 2, diminishes autoimmune demyelination and enhances remyelination in a chronic relapsing model for multiple sclerosis. Proc Natl Acad Sci USA 95: 10100-10105, 1998.
32. Canoll PD, Kraemer R, Teng KK, Marchionni MA, Salzer JL. GGF/neuregulin induces a phenotypic reversion of oligodendrocytes. Mol Cell Neurosci 13: 79-94, 1999.
33. Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL. GGF/ neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17: 229-243, 1996.
34. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827-835, 2004.
35. Cardon M, Ron-Harel N, Cohen H, Lewitus GM, Schwartz M. Dysregulation of kisspeptin and neurogenesis at adolescence link inborn immune deficits to the late onset of abnormal sensorimotor gating in congenital psychological disorders. Mol Psychiatry 15: 415-425, 2010.
36. Carlson BM. Muscle regeneration in amphibians and mammals: passing the torch. Dev Dyn 226: 167-181, 2003.
37. Carlson BM. Some principles of regeneration in mammalian systems. Anat Rec B New Anat 287: 4-13, 2005.
38. Carmeliet P. Blood vessels and nerves: common signals, pathways and diseases. Nat Rev Genet 4: 710-720, 2003.
39. Carro E, Trejo JL, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J Neurosci 21: 5678-5684, 2001.
40. Chen J, Magavi SS, Macklis JD. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci USA 101: 16357-16362, 2004.
41. Chernoff EA, Stocum DL, Nye HL, Cameron JA. Urodele spinal cord regeneration and related processes. Dev Dyn 226: 295-307, 2003.
42. Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, Brown RH Jr, Carroll MC. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci USA 105: 17913-17918, 2008.
43. Choi C, Benveniste EN. Fas ligand/Fas system in the brain: regulator of immune and apoptotic responses. Brain Res 44: 65-81, 2004.
44. Compston A, Coles A. Multiple sclerosis. Lancet 359: 1221-1231, 2002.
45. Conti L, Cattaneo E. Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci 11: 176-187.
46. Conti L, Cattaneo E. Novel and immortalization-based protocols for the generation of neural CNS stem cell lines for gene therapy approaches. Methods Mol Biol 438: 319-332, 2008.
47. Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V, Uccelli A. Human mesenchymal stem cells modulate B cell functions. Blood 107: 367-372, 2006.
48. Corti S, Locatelli F, Papadimitriou D, Del Bo R, Nizzardo M, Nardini M, Donadoni C, Salani S, Fortunato F, Strazzer S, Bresolin N, Comi GP. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 130: 1289-1305, 2007.
49. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249, 2007.
50. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390: 680-683, 1997.
51. Dawson MR, Polito A, Levine JM, Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24: 476-488, 2003.
52. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168: 415-427, 2005.
53. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR, Kipnis J. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207: 1067-1080.
54. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR, Kipnis J. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207: 1067-1080, 2010.
55. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev 13: 543-550, 2003.
56. Doetsch F. The glial identity of neural stem cells. Nat Neurosci 6: 1127-1134, 2003.
57. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716, 1999.
58. Dore-Duffy P. Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14: 1581-1593, 2008.
59. Dore-Duffy P, Katychev A, Wang X, Van Buren E. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 26: 613-624, 2006.
60. Dyment DA, Ebers GC. An array of sunshine in multiple sclerosis. N Engl J Med 347: 1445-1447, 2002.
61. Ehninger D, Kempermann G. Neurogenesis in the adult hippocampus. Cell Tissue Res 331: 243-250, 2008.
62. 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 61: 209-218, 2007.
63. 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 198: 275-284, 2006.
64. 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 24: 1074-1082, 2003.
65. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100: 13632-13637, 2003.
66. Endo T, Yoshino J, Kado K, Tochinai S. Brain regeneration in anuran amphibians. Dev Growth Differ 49: 121-129, 2007.
67. Engelhardt B, Ransohoff RM. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 26: 485-495, 2005.
68. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317, 1998.
69. Espinosa de los Monteros A, Zhao P, Huang C, Pan T, Chang R, Nazarian R, Espejo D, de Vellis J. Transplantation of CG4 oligodendrocyte progenitor cells in the myelindeficient rat brain results in myelination of axons and enhanced oligodendroglial markers. J Neurosci Res 50: 872-887, 1997.
70. Fainstein N, Vaknin I, Einstein O, Zisman P, Ben Sasson SZ, Baniyash M, Ben-Hur T. Neural precursor cells inhibit multiple inflammatory signals. Mol Cell Neurosci 39: 335-341, 2008.
71. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24: 2143-2155, 2004.
72. Fellous TG, Islam S, Tadrous PJ, Elia G, Kocher HM, Bhattacharya S, Mears L, Turnbull DM, Taylor RW, Greaves LC, Chinnery PF, Taylor G, McDonald SA, Wright NA, Alison MR. Locating the stem cell niche and tracing hepatocyte lineages in human liver. Hepatology 49: 1655-1663, 2009.
73. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23: 373-382, 2003.
74. Font E, Garcia-Verdugo JM, Alcantara S, Lopez-Garcia C. Neuron regeneration reverses 3-acetylpyridine-induced cell loss in the cerebral cortex of adult lizards. Brain Res 551: 230-235, 1991.
75. Fowler CD, Liu Y, Wang Z. Estrogen and adult neurogenesis in the amygdala and hypothalamus. Brain Res Rev 57: 342-351, 2008.
76. Franklin RJ. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3: 705-714, 2002.
77. Franklin RJ, French-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9: 839-855, 2008.
78. Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23: 9357-9366, 2003.
79. Gadea A, Aguirre A, Haydar TF, Gallo V. Endothelin-1 regulates oligodendrocyte development. J Neurosci 29: 10047-10062, 2009.
80. Gage FH. Mammalian neural stem cells. Science 287: 1433-1438, 2000.
81. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36: 249-266, 1998.
82. Givogri MI, Galbiati F, Fasano S, Amadio S, Perani L, Superchi D, Morana P, Del Carro U, Marchesini S, Brambilla R, Wrabetz L, Bongarzone E. Oligodendroglial progenitor cell therapy limits central neurological deficits in mice with metachromatic leukodystrophy. J Neurosci 26: 3109-3119, 2006.
83. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3: 23-35, 2003.
84. Goss RJ. Hypertrophy versus hyperplasia. Science 153: 1615-1620, 1966.
85. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8: 481-488, 2007.
86. Gould E, Cameron HA. Regulation of neuronal birth, migration and death in the rat dentate gyrus. Dev Neurosci 18: 22-35, 1996.
87. Greene P. Cell-based therapies in Parkinson's disease. Curr Neurol Neurosci Rep 9: 292-297, 2009.
88. Harty M, Neff AW, King MW, Mescher AL. Regeneration or scarring: an immunologic perspective. Dev Dyn 226: 268-279, 2003.
89. Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M. Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 20: 6421-6430, 2000.
90. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12: 656-670, 2007.
91. Hemmer B, Archelos JJ, Hartung HP. New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 3: 291-301, 2002.
92. Hochedlinger K, Plath K. Epigenetic reprogramming and induced pluripotency. Development 136: 509-523, 2009.
93. Holland EC, Varmus HE. Basic fibroblast growth factor induces cell migration and proliferation after glia-specific gene transfer in mice. Proc Natl Acad Sci USA 95: 1218-1223, 1998.
94. Horner PJ, Thallmair M, Gage FH. Defining the NG2-expressing cell of the adult CNS. J Neurocytol 31: 469-480, 2002.
95. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426: 83-87, 2003.
96. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, Ming GL, Song H, Gallo V. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 13: 541-550.
97. Jaenisch R, Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582, 2008.
98. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99: 11946-11950, 2002.
99. Karman J, Ling C, Sandor M, Fabry Z. Initiation of immune responses in brain is promoted by local dendritic cells. J Immunol 173: 2353-2361, 2004.
100. Kaslin J, Ganz J, Brand M. Proliferation, neurogenesis and regeneration in the nonmammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363: 101-122, 2008.
101. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130: 391-399, 2003.
102. Kendall AL, Rayment FD, Torres EM, Baker HF, Ridley RM, Dunnett SB. Functional integration of striatal allografts in a primate model of Huntington's disease. Nat Med 4: 727-729, 1998.
103. Kipnis J, Cardon M, Avidan H, Lewitus GM, Mordechay S, Rolls A, Shani Y, Schwartz M. Dopamine, through the extracellular signal-regulated kinase pathway, downregulates CD4+ CD25+ regulatory T-cell activity: implications for neurodegeneration. J Neurosci 24: 6133-6143, 2004.
104. Kipnis J, Cohen H, Cardon M, Ziv Y, Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc Natl Acad Sci USA 101: 8180-8185, 2004.
105. Kipnis J, Mizrahi T, Hauben E, Shaked I, Shevach E, Schwartz M. Neuroprotective autoimmunity: naturally occurring CD4+ CD25+ regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci USA 99: 15620-15625, 2002.
106. Kleine TO, Benes L. Immune surveillance of the human central nervous system (CNS): different migration pathways of immune cells through the blood-brain barrier and blood-cerebrospinal fluid barrier in healthy persons. Cytometry A 69: 147-151, 2006.
107. Klimanskaya I, Rosenthal N, Lanza R. Derive and conquer: sourcing and differentiating stem cells for therapeutic applications. Nat Rev Drug Discov 7: 131-142, 2008.
108. Koizumi O, Bode HR. Plasticity in the nervous system of adult hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J Neurosci 11: 2011-2020, 1991.
109. Kokoeva MV, Yin H, Flier JS. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505: 209-220, 2007.
110. Kokoeva MV, Yin H, Flier JS. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310: 679-683, 2005.
111. Koo JW, Duman RS. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA 105: 751-756, 2008.
112. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14: 504-506, 2008.
113. Kornack DR, Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 294: 2127-2130, 2001.
114. Kornek B, Lassmann H. Neuropathology of multiple sclerosis-new concepts. Brain Res Bull 61: 321-326, 2003.
115. Koronyo-Hamaoui M, Ko MK, Koronyo Y, Azoulay D, Seksenyan A, Kunis G, Pham M, Bakhsheshian J, Rogeri P, Black KL, Farkas DL, Schwartz M. Attenuation of AD-like neuropathology by harnessing peripheral immune cells: local elevation of IL-10 and MMP-9. J Neurochem 111: 1409-1424, 2009.
116. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. Hippocampal longterm potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92: 8856-8860, 1995.
117. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32: 149-184, 2009.
118. Kung JW, Forbes SJ. Stem cells and liver repair. Curr Opin Biotechnol 20: 568-574, 2009.
119. Lassmann H. Mechanisms of demyelination and tissue destruction in multiple sclerosis. Clin Neurol Neurosurg 104: 168-171, 2002.
120. Lassmann H, Bruck W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol 17: 210-218, 2007.
121. Lazarov-Spiegler O, Rapalino O, Agranov G, Schwartz M. Restricted inflammatory reaction in the CNS: a key impediment to axonal regeneration? Mol Med Today 4: 337-342, 1998.
122. Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, Kang KM, Hong NH, Kim JH, Ban JJ, Park HK, Kim SU, Park CG, Lee SK, Kim M, Roh JK. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131: 616-629, 2008.
123. Lewitus GM, Cohen H, Schwartz M. Reducing post-traumatic anxiety by immunization. Brain Behav Immun 22: 1108-1114, 2008.
124. Lewitus GM, Schwartz M. Behavioral immunization: immunity to self-antigens contributes to psychological stress resilience. Mol Psychiatry 14: 532-536, 2009.
125. Lewitus GM, Wilf-Yarkoni A, Ziv Y, Shabat-Simon M, Gersner R, Zangen A, Schwartz M. Vaccination as a novel approach for treating depressive behavior. Biol Psychiatry 65: 283-288, 2009.
126. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A, Widner H, Revesz T, Lindvall O, Brundin P. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14: 501-503, 2008.
127. Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 21: 605-631, 2005.
128. Lin G, Chen Y, Slack JM. Regeneration of neural crest derivatives in the Xenopus tadpole tail. BMC Dev Biol 7: 56, 2007.
129. Lindvall O, Kokaia Z. Stem cells in human neurodegenerative disorders-time for clinical translation? J Clin Invest 120: 29-40, 2010.
130. Little MH, Bertram JF. Is there such a thing as a renal stem cell? J Am Soc Nephrol 20: 2112-2117, 2009.
131. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148, 1994.
132. Lois C, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90: 2074-2077, 1993.
133. Lu P, Jones LL, Snyder EY, Tuszynski MH. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 181: 115-129, 2003.
134. Luzzati F, De Marchis S, Fasolo A, Peretto P. Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26: 609-621, 2006.
135. Ma DK, Ming GL, Song H. Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr Opin Neurobiol 15: 514-520, 2005.
136. Madhavan L, Ourednik V, Ourednik J. Neural stem/progenitor cells initiate the formation of cellular networks that provide neuroprotection by growth factor-modulated antioxidant expression. Stem Cells 26: 254-265, 2008.
137. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R, Plath K, Hochedlinger K. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1: 55-70, 2007.
138. Manganas LN, Zhang X, Li Y, Hazel RD, Smith SD, Wagshul ME, Henn F, Benveniste H, Djuric PM, Enikolopov G, Maletic-Savatic M. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318: 980-985, 2007.
139. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, Martinez-Ramirez S, Jimenez-Xarrie E, Marin R, Marti-Vilalta JL, Garcia-Verdugo JM. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 74: 357-365, 2010.
140. Martin P, Parkhurst SM. Parallels between tissue repair and embryo morphogenesis. Development 131: 3021-3034, 2004.
141. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27: 451-483, 2009.
142. Martino G. How the brain repairs itself: new therapeutic strategies in inflammatory and degenerative CNS disorders. Lancet Neurol 3: 372-378, 2004.
143. Martino G, Pluchino S. The therapeutic potential of neural stem cells. Nat Rev Neurosci 7: 395-406, 2006.
144. Mason JL, Ye P, Suzuki K, D'Ercole AJ, Matsushima GK. Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J Neurosci 20: 5703-5708, 2000.
145. Mathieu P, Battista D, Depino A, Roca V, Graciarena M, Pitossi F. The more you have, the less you get: the functional role of inflammation on neuronal differentiation of endogenous and transplanted neural stem cells in the adult brain. J Neurochem 112: 1368-1385.
146. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6: e182, 2008.
147. Mescher AL, Neff AW. Limb regeneration in amphibians: immunological considerations. Sci World J 6 Suppl 1: 1-11, 2006.
148. Mescher AL, Neff AW. Regenerative capacity and the developing immune system. Adv Biochem Eng Biotechnol 93: 39-66, 2005.
149. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 276: 60-66, 1997.
150. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3: 265-278, 2008.
151. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M. Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 5: 49-55, 1999.
152. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765, 2003.
153. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132: 598-611, 2008.
154. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Hoglinger GU, Hirsch EC, Reynolds R, Baron-Van Evercooren A. Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci USA 104: 4694-4699, 2007.
155. Nakanishi K, Aono S, Hirano K, Kuroda Y, Ida M, Tokita Y, Matsui F, Oohira A. Identification of neurite outgrowth-promoting domains of neuroglycan C, a brainspecific chondroitin sulfate proteoglycan, involvement of phosphatidylinositol 3-kinase and protein kinase C signaling pathways in neuritogenesis. J Biol Chem 281: 24970-24978, 2006.
156. Nakatani Y, Kawakami A, Kudo A. Cellular and molecular processes of regeneration, with special emphasis on fish fins. Dev Growth Differ 49: 145-154, 2007.
157. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110: 429-441, 2002.
158. Nishiyama A. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13: 62-76, 2007.
159. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22, 2009.
160. Nottebohm F. The road we travelled: discovery, choreography, and significance of brain replaceable neurons. Ann NY Acad Sci 1016: 628-658, 2004.
161. Nye HL, Cameron JA, Chernoff EA, Stocum DL. Regeneration of the urodele limb: a review. Dev Dyn 226: 280-294, 2003.
162. Nystul TG, Spradling AC. Breaking out of the mold: diversity within adult stem cells and their niches. Curr Opin Genet Dev 16: 463-468, 2006.
163. Ohlstein B, Kai T, Decotto E, Spradling A. The stem cell niche: theme and variations. Curr Opin Cell Biol 16: 693-699, 2004.
164. Okamoto M, Ohsawa H, Hayashi T, Owaribe K, Tsonis PA. Regeneration of retinotectal projections after optic tectum removal in adult newts. Mol Vision 13: 2112-2118, 2007.
165. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317, 2007.
166. Olson JK, Ludovic Croxford J, Miller SD. Innate and adaptive immune requirements for induction of autoimmune demyelinating disease by molecular mimicry. Mol Immunol 40: 1103-1108, 2004.
167. Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY. Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol 20: 1103-1110, 2002.
168. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479-494, 2000.
169. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+ CD25+ T cellmediated suppression by dendritic cells. Science 299: 1033-1036, 2003.
170. Perez-Martin M, Cifuentes M, Grondona JM, Lopez-Avalos MD, Gomez-Pinedo U, Garcia-Verdugo JM, Fernandez-Llebrez P. IGF-I stimulates neurogenesis in the hypothalamus of adult rats. Eur J Neurosci 31: 1533-1548.
171. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Evercooren AB. Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci USA 99: 13211-13216, 2002.
172. Piccini P, Brooks DJ, Bjorklund A, Gunn RN, Grasby PM, Rimoldi O, Brundin P, Hagell P, Rehncrona S, Widner H, Lindvall O. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat Neurosci 2: 1137-1140, 1999.
173. 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 66: 343-354, 2009.
174. Pluchino S, Muzio L, Imitola J, Deleidi M, Alfaro-Cervello C, Salani G, Porcheri C, Brambilla E, Cavasinni F, Bergamaschi A, Garcia-Verdugo JM, Comi G, Khoury SJ, Martino G. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain 131: 2564-2578, 2008.
175. 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 AL, Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694, 2003.
176. 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 JM, Comi G, Manfredi AA, Martino G. Immune regulatory neural stem/ precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One 4: e5959, 2009.
177. 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. Neurospherederived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436: 266-271, 2005.
178. Ponti G, Crociara P, Armentano M, Bonfanti L. Adult neurogenesis without germinal layers: the "atypical" cerebellum of rabbits. Arch Ital Biol 148: 147-158, 2010.
179. Ponti G, Peretto P, Bonfanti L. A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294: 168-180, 2006.
180. Ponti G, Peretto P, Bonfanti L. Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS One 3: e2366, 2008.
181. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494: 415-434, 2006.
182. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, Escribano J, Farinas I. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9: 331-339, 2006.
183. Rampon C, Weiss N, Deboux C, Chaverot N, Miller F, Buchet D, Tricoire-Leignel H, Cazaubon S, Baron-Van Evercooren A, Couraud PO. Molecular mechanism of systemic delivery of neural precursor cells to the brain: assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells 26: 1673-1682, 2008.
184. Ransohoff RM. Immunology: in the beginning. Nature 462: 41-42, 2009.
185. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4: 814-821, 1998.
186. Rehermann MI, Marichal N, Russo RE, Trujillo-Cenoz O. Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J Comp Neurol 515: 197-214, 2009.
187. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2: 141-150, 2008.
188. Robel S, Berninger B, Gotz M. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12: 88-104, 2011.
189. Robert J, Cohen N. Evolution of immune surveillance and tumor immunity: studies in Xenopus. Immunol Rev 166: 231-243, 1998.
190. Rolls A, Shechter R, London A, Segev Y, Jacob-Hirsch J, Amariglio N, Rechavi G, Schwartz M. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med 5: e171, 2008.
191. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 9: 1081-1088, 2007.
192. Rolls A, Shechter R, Schwartz M. The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10: 235-241, 2009.
193. Ron-Harel N, Schwartz M. Immune senescence and brain aging: can rejuvenation of immunity reverse memory loss? Trends Neurosci 32: 367-375, 2009.
194. Ron-Harel N, Segev Y, Lewitus GM, Cardon M, Ziv Y, Netanely D, Jacob-Hirsch J, Amariglio N, Rechavi G, Domany E, Schwartz M. Age-dependent spatial memory loss can be partially restored by immune activation. Rejuvenation Res 11: 903-913, 2008.
195. Rossi F, Cattaneo E. Opinion: neural stem cell therapy for neurological diseases: dreams and reality. Nat Rev Neurosci 3: 401-409, 2002.
196. Roy S, Levesque M. Limb regeneration in axolotl: is it superhealing? Sci World J 6 Suppl 1: 12-25, 2006.
197. Rutkowski MJ, Sughrue ME, Kane AJ, Mills SA, Fang S, Parsa AT. Complement and the central nervous system: emerging roles in development, protection and regeneration. Immunol Cell Biol 88: 781-786.
198. Samstein B, Johnson GB, Platt JL. Toll-like receptor-4 and allograft responses. Transplantation 77: 475-477, 2004.
199. San Miguel-Ruiz JE, Garcia-Arraras JE. Common cellular events occur during wound healing and organ regeneration in the sea cucumber Holothuria glaberrima. BMC Dev Biol 7: 115, 2007.
200. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744, 2004.
201. Sanchez Alvarado A, Kang H. Multicellularity, stem cells, and the neoblasts of the planarian Schmidtea mediterranea. Exp Cell Res 306: 299-308, 2005.
202. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192: 348-356, 2005.
203. Schwartz M, Cohen IR. Autoimmunity can benefit self-maintenance. Immunol Today 21: 265-268, 2000.
204. Schwartz M, Kipnis J. Multiple sclerosis as a by-product of the failure to sustain protective autoimmunity: a paradigm shift. Neuroscientist 8: 405-413, 2002.
205. Schwartz M, Shechter R. Protective autoimmunity functions by intracranial immunosurveillance to support the mind: the missing link between health and disease. Mol Psychiatry 15: 342-354, 2010.
206. Schwartz M, Shechter R. Systemic inflammatory cells fight off neurodegenerative disease. Nat Rev Neurol 6: 405-410, 2010.
207. Schwartz M, Yoles E. Immune-based therapy for spinal cord repair: autologous macrophages and beyond. J Neurotrauma 23: 360-370, 2006.
208. Schwartz M, Ziv Y. Immunity to self and self-maintenance: what can tumor immunology teach us about ALS and Alzheimer's disease? Trends Pharmacol Sci 29: 287-293, 2008.
209. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478: 359-378, 2004.
210. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21: 7153-7160, 2001.
211. Shechter R, Baruch K, Schwartz M, Rolls A. Touch gives new life: mechanosensation modulates spinal cord adult neurogenesis. Mol Psychiatry. 16: 342-352, 2011.
212. Shechter R, London A, Varol C, Raposo C, Cusimano M, Yovel G, Rolls A, Mack M, Pluchino S, Martino G, Jung S, Schwartz M. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med 6: e1000113, 2009.
213. Shechter R, Ronen A, Rolls A, London A, Bakalash S, Young MJ, Schwartz M. Toll-like receptor 4 restricts retinal progenitor cell proliferation. J Cell Biol 183: 393-400, 2008.
214. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304: 1338-1340, 2004.
215. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3: 289-300, 2008.
216. Singla V, Reiter JF. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313: 629-633, 2006.
217. Sohur US, Emsley JG, Mitchell BD, Macklis JD. Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells. Philos Trans R Soc Lond B Biol Sci 361: 1477-1497, 2006.
218. Song HJ, Stevens CF, Gage FH. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5: 438-445, 2002.
219. Sotelo C. Cerebellar synaptogenesis: mutant mice-neuronal grafting. J Physiol 85: 134-144, 1991.
220. Stoick-Cooper CL, Moon RT, Weidinger G. Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 21: 1292-1315, 2007.
221. Suda Y, Suzuki M, Ikawa Y, Aizawa S. Mouse embryonic stem cells exhibit indefinite proliferative potential. J Cell Physiol 133: 197-201, 1987.
222. Suh H, Deng W, Gage FH. Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25: 253-275, 2009.
223. Swanborg RH. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clin Immunol Immunopathol 77: 4-13, 1995.
224. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676, 2006.
225. Tanaka E, Galliot B. Triggering the regeneration and tissue repair programs. Development 136: 349-353, 2009.
226. Tanaka EM, Ferretti P. Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10: 713-723, 2009.
227. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3: 279-288, 2008.
228. Thompson LH, Bjorklund A. Transgenic reporter mice as tools for studies of transplantability and connectivity of dopamine neuron precursors in fetal tissue grafts. Prog Brain Res 175: 53-79, 2009.
229. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38: 3032-3039, 2007.
230. Torok MA, Gardiner DM, Shubin NH, Bryant SV. Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol 200: 225-233, 1998.
231. Tournefier A, Laurens V, Chapusot C, Ducoroy P, Padros MR, Salvadori F, Sammut B. Structure of MHC class I and class II cDNAs and possible immunodeficiency linked to class II expression in the Mexican axolotl. Immunol Rev 166: 259-277, 1998.
232. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338: 278-285, 1998.
233. Trejo JL, Carro E, Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21: 1628-1634, 2001.
234. Umesono Y, Agata K. Evolution and regeneration of the planarian central nervous system. Dev Growth Differ 51: 185-195, 2009.
235. Van Noort JM, Bsibsi M. Toll-like receptors in the CNS: implications for neurodegeneration and repair. Prog Brain Res 175: 139-148, 2009.
236. Walker MR, Patel KK, Stappenbeck TS. The stem cell niche. J Pathol 217: 169-180, 2009.
237. Watanabe H, Hoang VT, Mattner R, Holstein TW. Immortality and the base of multicellular life: lessons from cnidarian stem cells. Semin Cell Dev Biol 20: 1114-1125, 2009.
238. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Cell 100: 157-168, 2000.
239. Wernig M, Meissner A, Cassady JP, Jaenisch R. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell 2: 10-12, 2008.
240. Whitehead GG, Makino S, Lien CL, Keating MT. fgf20 is essential for initiating zebrafish fin regeneration. Science 310: 1957-1960, 2005.
241. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann G, 2nd Roy NS, Goldman SA. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 10: 93-97, 2004.
242. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2: 553-565, 2008.
243. Wingerchuk DM, Lucchinetti CF, Noseworthy JH. Multiple sclerosis: current pathophysiological concepts. Lab Invest 81: 263-281, 2001.
244. Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C, Braun A, Blankenstein T, Kempermann G. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol 182: 3979-3984, 2009.
245. Wujek JR, Bjartmar C, Richer E, Ransohoff RM, Yu M, Tuohy VK, Trapp BD. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J Neuropathol Exp Neurol 61: 23-32, 2002.
246. Xu L, Yan J, Chen D, Welsh AM, Hazel T, Johe K, Hatfield G, Koliatsos VE. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 82: 865-875, 2006.
247. Yan X, Owens DM. The skin: a home to multiple classes of epithelial progenitor cells. Stem cell rev 4: 113-118, 2008.
248. Yang J, Jiang Z, Fitzgerald DC, Ma C, Yu S, Li H, Zhao Z, Li Y, Ciric B, Curtis M, Rostami A, Zhang GX. Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J Clin Invest 119: 3678-3691, 2009.
249. Yannas IV. Similarities and differences between induced organ regeneration in adults and early foetal regeneration. J Royal Soc Interface/Royal Soc 2: 403-417, 2005.
250. Yao DL, Liu X, Hudson LD, Webster HD. Insulin-like growth factor I treatment reduces demyelination and up-regulates gene expression of myelin-related proteins in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 92: 6190-6194, 1995.
251. Yao DL, Liu X, Hudson LD, Webster HD. Insulin-like growth factor-I given subcutaneously reduces clinical deficits, decreases lesion severity and upregulates synthesis of myelin proteins in experimental autoimmune encephalomyelitis. Life Sci 58: 1301-1306, 1996.
252. Yasuhara T, Borlongan CV, Date I. Ex vivo gene therapy: transplantation of neurotrophic factor-secreting cells for cerebral ischemia. Front Biosci 11: 760-775, 2006.
253. Yasuhara T, Matsukawa N, Hara K, Yu G, Xu L, Maki M, Kim SU, Borlongan CV. Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J Neurosci 26: 12497-12511, 2006.
254. Yoles E, Hauben E, Palgi O, Agranov E, Gothilf A, Cohen A, Kuchroo V, Cohen IR, Weiner H, Schwartz M. Protective autoimmunity is a physiological response to CNS trauma. J Neurosci 21: 3740-3748, 2001.
255. Yong VW, Rivest S. Taking advantage of the systemic immune system to cure brain diseases. Neuron 64: 55-60, 2009.
256. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106: 1755-1761, 2005.
257. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6: 578-590.
258. Zhang W, Lee WH, Triarhou LC. Grafted cerebellar cells in a mouse model of hereditary ataxia express IGF-I system genes and partially restore behavioral function. Nat Med 2: 65-71, 1996.
259. 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 USA 103: 13174-13179, 2006.
260. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9: 268-275, 2006.
261. Ziv Y, Schwartz M. Immune-based regulation of adult neurogenesis: implications for learning and memory. Brain Behav Immun 22: 167-176, 2008.
262. Ziv Y, Schwartz M. Orchestrating brain-cell renewal: the role of immune cells in adult neurogenesis in health and disease. Trends Mol Med 14: 471-478, 2008.
263. Zupanc GK, Zupanc MM. New neurons for the injured brain: mechanisms of neuronal regeneration in adult teleost fish. Regenerative Med 1: 207-216, 2006.