Neurodegeneration and cell replacement

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1489, 2008, Pages 153-170

  Ormerod, Brandi K ^a   Palmer, Theo D ^a   Caldwell, Maeve A ^b,c  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Adult neural stem cells; Foetal stem cells; Human embryonic stem cells; Immunology; Neurodegenerative disease

Indexed keywords

BRAIN; DEVELOPMENTAL BIOLOGY; IMMUNE SYSTEM; NERVOUS SYSTEM DISORDER; NEUROLOGY;

ANIMALIA;

EID: 36448992620     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.2018     Document Type: Review

References (173)

1. Abeliovich, A. et al. 2000 Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239-252. (doi:10.1016/S0896-6273(00)80886-7)
2. Aberg, M. A., Aberg, N. D., Hedbacker, H., Oscarsson, J. & Eriksson, P. S. 2000 Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20, 2896-2903.
3. Aebischer, P. et al. 1996 Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients. Nat. Med. 2, 696-699. (doi:10.1038/nm0696-696)
4. ALS CNTF Group 1996 A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. ALS CNTF Treatment Study Group. Neurology 46, 1244-1249.
5. Alvarez-Buylla, A. & Lim, D. A. 2004 For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686.
6. Alvarez-Buylla, A. & Garcia-Verdugo, J. M. 2002 Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
7. Amit, M., Carpenter, M. K., Inokuma, M. S., Chiu, C. P., Harris, C. P., Waknitz, M. A., Itskovitz-Eldor, J. & Thomson, J. A. 2000 Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev. Biol. 227, 271-278. (doi:10.1006/dbio.2000.9912)
8. Arase, K., Saijo, K., Watanabe, H., Konno, A., Arase, H. & Saito, T. 1999 Ablation of a specific cell population by the replacement of a uniquely expressed gene with a toxin gene. Proc. Natl Acad. Sci. USA 96, 9264-9268. (doi:10.1073/pnas.96.16.9264)
9. Arsenijevic, Y., Villemure, J. G., Brunet, J. F., Bloch, J. J., Deglon, N., Kostic, C., Zurn, A. & Aebischer, P. 2001 Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp. Neurol. 170, 48-62. (doi:10.1006/exnr.2001.7691)
10. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. 2002 Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970. (doi:10.1038/nm747)
11. Barker, R. A. & Widner, H. 2004 Immune problems in central nervous system cell therapy. NeuroRx 1, 472-481. (doi:10.1602/neurorx.1.4. 472)
12. Beal, M. F. 2001 Experimental models of Parkinson's disease. Nat. Rev. Neurosci. 2, 325-334. (doi:10.1038/35072550)
13. Behrstock, S. & Svendsen, C. N. 2004 Combining growth factors, stem cells, and gene therapy for the aging brain. Ann. N. Y. Acad. Sci. 1019, 5-14. (doi:10.1196/annals.1297.002)
14. Ben-Hur, T., Idelson, M., Khaner, H., Pera, M., Reinhartz, E., Itzik, A. & Reubinoff, B. E. 2004 Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells 22, 1246-1255. (doi:10.1634/stemcells.2004-0094)
15. Betarbet, R., Sherer, T. B., MacKenzie, G., Garcia-Osuna, M., Panov, A. V. & Greenamyre, J. T. 2000 Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306. (doi:10.1038/81834)
16. Bjorklund, L. M. et al. 2002 Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl Acad. Sci. USA 99, 2344-2349. (doi:10.1073/pnas. 022438099)
17. Blesch, A. & Tuszynski, M. H. 2004 Gene therapy and cell transplantation for Alzheimer's disease and spinal cord injury. Yonsei Med. J. 45(Suppl.), 28-31.
18. Bloch, J. et al. 2004 Neuroprotective gene therapy for Huntington's disease, using polymer-encapsulated cells engineered to secrete human ciliary neurotrophic factor: results of a phase I study. Hum. Gene Ther. 15, 968-975. (doi:10.1089/hum.2004.15.968)
19. Block, M. L. & Hong, J. S. 2005 Microglia and inflammationmediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76, 77-98. (doi:10.1016/j.pneurobio.2005.06.004)
20. Bongso, A. & Richards, M. 2004 History and perspective of stem cell research. Best. Pract. Res. Clin. Obstet. Gynaecol. 18, 827-842. (doi:10.1016/j.bpobgyn.2004.09.002)
21. Bradley, J. A., Bolton, E. M. & Pedersen, R. A. 2002 Stem cell medicine encounters the immune system. Nat. Rev. Immunol. 2, 859-871. (doi:10.1038/nri934)
22. Bunge, M. B. & Pearse, D.D. 2003 Transplantation strategies to promote repair of the injured spinal cord. J. Rehabil. Res. Dev. 40, 55-62.
23. Burns, R. S., Chiueh, C. C., Markey, S. P., Ebert, M. H., Jacobowitz, D. M. & Kopin, I. J. 1983 A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc. Natl Acad. Sci. USA 80, 4546-4550. (doi:10.1073/pnas.80.14.4546)
24. Caldwell, M. A. & Svendsen, C. N. 1998 Heparin, but not other proteoglycans potentiates the mitogenic effects of FGF-2 on mesencephalic precursor cells. Exp. Neurol. 152, 1-10. (doi:10.1006/exnr.1998. 6815)
25. Caldwell, M. A., He, X., Wilkie, N., Pollack, S., Marshall, G., Wafford, K. A. & Svendsen, C. N. 2001 Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 19, 475-479. (doi:10.1038/88158)
26. Carpenter,M.K., Cui, X.,Hu, Z. Y., Jackson, J., Sherman, S., Seiger, A. & Wahlberg, L. U. 1999 In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158, 265-278. (doi:10.1006/exnr.1999.7098)
27. Chandran, S., Hunt, D., Joannides, A., Zhao, C., Compston, A. & Franklin, R. J. M. 2007 Myelin repair: the role of stem and precursor cells in multiple sclerosis. Phil. Trans. R. Soc. B 363, 171-183. (doi:10.1098/rstb.2006.2019)
28. Chen, J., Magavi, S. S. & Macklis, J. D. 2004 Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl Acad. Sci. USA 101, 16 357-16 362. (doi:10.1073/pnas. 0406795101)
29. Clarkson, E. D. 2001 Fetal tissue transplantation for patients with Parkinson's disease: a database of published clinical results. Drugs Aging 18, 773-785. (doi:10.2165/00002512-200118100-00006)
30. Corti, O., Sabate, O., Horellou, P., Colin, P., Dumas, S., Buchet, D., Buc-Caron, M. H. & Mallet, J. 1999 A single adenovirus vector mediates doxycycline-controlled expression of tyrosine hydroxylase in brain grafts of human neural progenitors. Nat. Biotechnol. 17, 349-354. (doi:10.1038/7901)
31. Costantini, L. C., Bakowska, J. C., Breakefield, X. O. & Isacson, O. 2000 Gene therapy in the CNS. Gene Ther. 7, 93-109. (doi:10.1038/sj.gt.3301119)
32. Cowan, C. A. et al. 2004 Derivation of embryonic stem-cell lines from human blastocysts. N. Engl. J. Med. 350, 1353-1356. (doi:10.1056/NEJMsr040330)
33. Crain,B. J.,Tran, S.D.&Mezey, E. 2005Transplanted human bone marrow cells generate new brain cells. J. Neurol. Sci. 233, 121-123. (doi:10.1016/j.jns.2005.03.017)
34. Cummings, B. J., Uchida, N., Tamaki, S. J., Salazar, D. L., Hooshmand, M., Summers, R., Gage, F. H. & Anderson, A. J. 2005 Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl Acad. Sci. USA 102, 14 069-14 074. (doi:10.1073/pnas. 0507063102)
35. de Almeida, L. P., Zala, D., Aebischer, P. & Deglon, N. 2001 Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease. Neurobiol. Dis. 8, 433-446. (doi:10.1006/nbdi.2001.0388)
36. Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D. & Malenka, R. C. 2004 Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535-552. (doi:10.1016/S0896- 6273(04)00266-1)
37. Drukker, M., Katz, G., Urbach, A., Schuldiner, M., Markel, G., Itskovitz-Eldor, J., Reubinoff, B., Mandelboim, O. & Benvenisty, N. 2002 Characterization of the expression of MHC proteins in human embryonic stem cells. Proc. Natl Acad. Sci. USA 99, 9864-9869. (doi:10.1073/pnas.142298299)
38. Dunnett, S. B. & Rosser, A. E. 2004 Cell therapy in Huntington's disease. NeuroRx 1, 394-405. (doi:10.1602/neurorx.1.4.394)
39. Dziewczapolski, G., Lie, D. C., Ray, J., Gage, F. H. & Shults, C. W. 2003 Survival and differentiation of adult ratderived neural progenitor cells transplanted to the striatum of hemiparkinsonian rats. Exp. Neurol. 183, 653-664. (doi:10.1016/S0014-4886(03)00212-7)
40. Ebadi, M. et al. 1997 Neurotrophins and their receptors in nerve injury and repair. Neurochem. Int. 30, 347-374. (doi:10.1016/S0197-0186(96)00071-X)
41. Ekdahl, C. T., Claasen, J. H., Bonde, S., Kokaia, Z. & Lindvall, O. 2003 Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl Acad. Sci. USA 100, 13 632-13 637. (doi:10.1073/pnas.2234031100)
42. Emsley, J. G., Mitchell, B. D., Kempermann, G. & Macklis, J. D. 2005 Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 75, 321-341. (doi:10.1016/j.pneurobio.2005.04.002)
43. Escolar, M. L. et al. 2005 Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. N. Engl. J. Med. 352, 2069-2081. (doi:10.1056/NEJMoa042604)
44. Eslamboli, A., Georgievska, B., Ridley, R. M., Baker, H. F., Muzyczka, N., Burger, C., Mandel, R. J., Annett, L. & Kirik, D. 2005 Continuous low-level glial cell line-derived neurotrophic factor delivery using recombinant adenoassociated viral vectors provides neuroprotection and induces behavioral recovery in a primate model of Parkinson's disease. J. Neurosci. 25, 769-777. (doi:10.1523/JNEUROSCI.4421-04.2005)
45. Fabel, K., Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C. J. & Palmer, T. D. 2003 VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812. (doi:10.1111/j.1460-9568.2003.03041.x)
46. Fouad, K., Dietz, V. & Schwab, M. E. 2001 Improving axonal growth and functional recovery after experimental spinal cord injury by neutralizing myelin associated inhibitors. Brain Res. Brain Res. Rev. 36, 204-212. (doi:10.1016/S0165-0173(01)00096-0)
47. Franklin, R. J. 2002 Why does remyelination fail in multiple sclerosis? Nat. Rev. Neurosci. 3, 705-714. (doi:10.1038/nrn917)
48. Freed, C. R. et al. 2001 Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719. (doi:10.1056/NEJM200103083441002)
49. Freeman, T. B. 1997 From transplants to gene therapy for Parkinson's disease. Exp. Neurol. 144, 47-50. (doi:10.1006/exnr.1996.6387)
50. Fricker, R. A., Carpenter, M. K., Winkler, C., Greco, C., Gates, M. A. & Bjorklund, A. 1999 Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci. 19, 5990-6005.
51. Friedman, W. J. 2000 Neurotrophins induce death of hippocampal neurons via the p75 receptor. J. Neurosci. 20, 6340-6346.
52. Gage, F. H. 2002 Neurogenesis in the adult brain. J. Neurosci. 22, 612-613.
53. Gage, F. H. 2003 Brain, repair yourself. Sci. Am. 289, 46-53.
54. Gage, F. H., Coates, P. W., Palmer, T. D., Kuhn, H. G., Fisher, L. J., Suhonen, J. O., Peterson, D. A., Suhr, S. T. & Ray, J. 1995 Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl Acad. Sci. USA 92, 11 879-11 883. (doi:10.1073/pnas.92.25.11879)
55. Gash, D. M., Zhang, Z. & Gerhardt, G. 1998 Neuroprotective and neurorestorative properties of GDNF. Ann. Neurol. 44, S121-S125.
56. Giebel, L. B. 2005 Stem cells - a hard sell to investors. Nat. Biotechnol. 23, 798-800. (doi:10.1038/nbt0705-798)
57. Gill, S. S., Patel, N. K., Hotton, G. R., O'Sullivan, K., McCarter, R., Bunnage, M., Brooks, D. J., Svendsen, C. N. & Heywood, P. 2003 Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 9, 589-595. (doi:10.1038/nm850)
58. Gould, E. & Gross, C. G. 2002 Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619-623.
59. Gould, E. & Tanapat, P. 1997 Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80, 427-436. (doi:10.1016/S0306-4522(97)00127-9)
60. Grados-Munro, E. M. & Fournier, A. E. 2003 Myelin-associated inhibitors of axon regeneration. J. Neurosci. Res. 74, 479-485. (doi:10.1002/jnr.10803)
61. Grondin, R. et al. 2002 Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125, 2191-2201. (doi:10.1093/brain/awf234)
62. Hagg, T. & Varon, S. 1993 Ciliary neurotrophic factor prevents degeneration of adult rat substantia nigra dopaminergic neurons in vivo. Proc. Natl Acad. Sci. USA 90, 6315-6319. (doi:10.1073/pnas.90.13. 6315)
63. Henderson, J. T., Seniuk,N. A., Richardson, P. M., Gauldie, J. & Roder, J. C. 1994 Systemic administration of ciliary neurotrophic factor induces cachexia in rodents. J. Clin. Invest. 93, 2632-2638.
64. Hoehn, B. D., Palmer, T. D. & Steinberg, G. K. 2005 Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 36, 2718-2724. (doi:10.1161/01.STR.0000190020.30282.cc)
65. Hoffman, L. M. & Carpenter, M. K. 2005 Characterization and culture of human embryonic stem cells. Nat. Biotechnol. 23, 699-708. (doi:10.1038/nbt1102)
66. Hwang, W. S. et al. 2004 Evidence of a pluripotent human embryonic stem cell line derived from a cloned blastocyst. Science 303, 1669-1674.
67. Iacopino, A. M. & Christakos, S. 1990 Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc. Natl Acad. Sci. USA 87, 4078-4082. (doi:10.1073/pnas.87.11.4078)
68. Imitola, J. et al. 2004 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. USA 101, 18 117-18 122. (doi:10.1073/pnas.0408258102)
69. Ito, H., Goto, S., Sakamoto, S. & Hirano, A. 1992 Calbindin-D28k in the basal ganglia of patients with parkinsonism. Ann. Neurol. 32, 543-550. (doi:10.1002/ana.410320410)
70. Jain, M., Armstrong, R. J., Tyers, P., Barker, R. A. & Rosser, A. E. 2003 GABAergic immunoreactivity is predominant in neurons derived from expanded human neural precursor cells in vitro. Exp. Neurol. 182, 113-123. (doi:10.1016/S0014-4886(03)00055-4)
71. Joannides, A., Gaughwin, P., Schwiening, C., Majed, H., Sterling, J., Compston, A. & Chandran, S. 2004 Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet 364, 172-178. (doi:10.1016/S0140-6736(04)16630-0)
72. Kaspar, B. K., Llado, J., Sherkat, N., Rothstein, J. D. & Gage, F. H. 2003 Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301, 839-842. (doi:10.1126/science.1086137)
73. Kaspar, B. K., Frost, L. M., Christian, L., Umapathi, P. & Gage, F. H. 2005 Synergy of insulin-like growth factor-1 and exercise in amyotrophic lateral sclerosis. Ann. Neurol. 57, 649-655. (doi:10.1002/ana.20451)
74. Keirstead, H. S., Nistor, G., Bernal, G., Totoiu, M., Cloutier, F., Sharp, K. & Steward, O. 2005 Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25, 4694-4705. (doi:10.1523/JNEUROSCI.0311-05.2005)
75. Kempermann, G. & Gage, F. H. 2000 Neurogenesis in the adult hippocampus. Novartis Found. Symp. 231, 220-235.
76. Kirik, D., Georgievska, B. & Bjorklund, A. 2004 Localized striatal delivery of GDNF as a treatment for Parkinson disease. Nat. Neurosci. 7, 105-110. (doi:10.1038/nn1175)
77. Klein, S. M., Behrstock, S., McHugh, J., Hoffmann, K., Wallace, K., Suzuki, M., Aebischer, P. & Svendsen, C. N. 2005 GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum. Gene Ther. 16, 509-521. (doi:10.1089/hum.2005.16.509)
78. Kokai, L. E., Rubin, J. P. & Marra, K. G. 2005 The potential of adipose-derived adult stem cells as a source of neuronal progenitor cells. Plast. Reconstr. Surg. 116, 1453-1460. (doi:10.1097/01.prs. 0000182570.62814.e3)
79. Kordower, J. H. et al. 1995 Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N. Engl. J. Med. 332, 1118-1124. (doi:10.1056/NEJM199504273321702)
80. Kordower, J. H., Goetz, C. G., Freeman, T. B. & Olanow, C. W. 1997 Dopaminergic transplants in patients with Parkinson's disease: neuroanatomical correlates of clinical recovery. Exp. Neurol. 144, 41-46. (doi:10.1006/exnr.1996.6386)
81. Kordower, J. H., Isacson, O. & Emerich, D. F. 1999a Cellular delivery of trophic factors for the treatment of Huntington's disease: is neuroprotection possible? Exp. Neurol. 159, 4-20. (doi:10.1006/exnr.1999.7156)
82. Kordower, J. H. et al. 1999b Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson's disease. Ann. Neurol. 46, 419-424. (doi:10.1002/1531-8249 (199909)46:3〈419::AID-ANA21〉3.0.CO;2-Q)
83. Kordower, J. H. et al. 2000 Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 290, 767-773. (doi:10.1126/science.290.5492.767)
84. Kraus, K. H. 1996 The pathophysiology of spinal cord injury and its clinical implications. Semin. Vet. Med. Surg. (Small Anim) 11, 201-207.
85. Krivit, W. 2004 Allogeneic stem cell transplantation for the treatment of lysosomal and peroxisomal metabolic diseases. Springer Semin. Immunopathol. 26, 119-132.
86. Krivit, W. et al. 1998 Hematopoietic stem-cell transplantation in globoid-cell leukodystrophy. N. Engl. J. Med. 338, 1119-1126. (doi:10.1056/NEJM199804163381605)
87. Land,W. G. 2005 The role of postischemic reperfusion injury and other nonantigen-dependent inflammatory pathways in transplantation. Transplantation 79, 505-514. (doi:10.1097/01.TP.0000153160.82975. 86)
88. Langston, J.W. & Ballard Jr, P. A. 1983 Parkinson's disease in a chemist working with 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. N. Engl. J. Med. 309, 310.
89. Lassmann, H., Bruck, W. & Lucchinetti, C. 2001 Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy. Trends Mol. Med. 7, 115-121. (doi:10.1016/S1471-4914(00)01909-2)
90. Le Belle, J. E. & Svendsen, C. N. 2002 Stem cells for neurodegenerative disorders: where can we go from here? BioDrugs 16, 389-401. (doi:10.2165/00063030-200216060-00001)
91. Le Belle, J. E., Caldwell, M. A. & Svendsen, C. N. 2004 Improving the survival of human CNS precursor-derived neurons after transplantation. J. Neurosci. Res. 76, 174-183.
92. Leventhal, C., Rafii, S., Rafii, D., Shahar, A. & Goldman, S. A. 1999 Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell Neurosci. 13, 450-464. (doi:10.1006/mcne.1999.0762)
93. Lewthwaite, A. J. & Nicholl, D. J. 2005 Genetics of parkinsonism. Curr. Neurol. Neurosci. Rep. 5, 397-404.
94. Li, X. J., Du, Z.W., Zarnowska, E.D., Pankratz, M., Hansen, L. O., Pearce, R. A. & Zhang, S. C. 2005 Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 23, 215-221. (doi:10.1038/nbt1063)
95. Lin, J. C. & Rosenthal, A. 2003 Molecular mechanisms controlling the development of dopaminergic neurons. Semin. Cell Dev. Biol. 14, 175-180. (doi:10.1016/S1084-9521(03)00009-0)
96. Lindvall, O. & Bjorklund, A. 2004 Cell therapy in Parkinson's disease. NeuroRx 1, 382-393. (doi:10.1602/neurorx.1.4.382)
97. Lindvall, O., Rehncrona, S., Brundin, P. & Gustavii, B. 1989 Human fetal dopamine neurons grafted into the striatum in two patients with severe Parkinson's disease. Arch. Neurol. 46, 615-631.
98. Lledo, P. M., Saghatelyan, A. & Lemasson, M. 2004 Inhibitory interneurons in the olfactory bulb: from development to function. Neuroscientist 10, 292-303. (doi:10.1177/1073858404263460)
99. Love, S., Plaha, P., Patel, N. K., Hotton, G. R., Brooks, D. J. & Gill, S. S. 2005 Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain. Nat. Med. 11, 703-704. (doi:10.1038/nm0705-703)
100. Ma, D. K., Ming, G. L. & Song, H. 2005 Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr. Opin. Neurobiol. 15, 514-520. (doi:10.1016/j.conb.2005.08.003)
101. Magavi, S. S., Leavitt, B. R. & Macklis, J. D. 2000 Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951-955. (doi:10.1038/35016083)
102. Maier, K. et al. 2004 Ciliary neurotrophic factor protects retinal ganglion cells from secondary cell death during acute autoimmune optic neuritis in rats. Brain Pathol. 14, 378-387.
103. Maitra, A. et al. 2005 Genomic alterations in cultured human embryonic stem cells. Nat. Genet. 37, 1099-1103. (doi:10.1038/ng1631)
104. Mann, D. M. 1996 Pyramidal nerve cell loss in Alzheimer's disease. Neurodegeneration 5, 423-427. (doi:10.1006/neur.1996.0057)
105. Marchetti, B. & Abbracchio, M. P. 2005 To be or not to be (inflamed) - is that the question in anti-inflammatory drug therapy of neurodegenerative disorders? Trends Pharmacol. Sci. 26, 517-525. (doi:10.1016/j.tips.2005.08.007)
106. Massengale, M., Wagers, A. J., Vogel, H. & Weissman, I. L. 2005 Hematopoietic cells maintain hematopoietic fates upon entering the brain. J. Exp. Med. 201, 1579-1589. (doi:10.1084/jem.20050030)
107. McGee, A. W. & Strittmatter, S. M. 2003 The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci. 26, 193-198. (doi:10.1016/S0166-2236(03)00062-6)
108. Mendez, I., Sanchez-Pernaute, R., Cooper, O., Vinuela, A., Ferrari, D., Bjorklund, L., Dagher, A. & Isacson, O. 2005 Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease. Brain 128, 1498-1510. (doi:10.1093/brain/awh510)
109. Menendez, P., Wang, L., Chadwick, K., Li, L. & Bhatia, M. 2004 Retroviral transduction of hematopoietic cells differentiated from human embryonic stem cell-derived CD45(neg)PFV hemogenic precursors. Mol. Ther. 10, 1109-1120. (doi:10.1016/j.ymthe.2004.08.016)
110. Miller, R. G., Bryan, W. W., Dietz, M. A., Munsat, T. L., Petajan, J. H., Smith, S. A. & Goodpasture, J. C. 1996a Toxicity and tolerability of recombinant human ciliary neurotrophic factor in patients with amyotrophic lateral sclerosis. Neurology 47, 1329-1331.
111. Miller, R. G. et al. 1996b A placebo-controlled trial of recombinant human ciliary neurotrophic (rhCNTF) factor in amyotrophic lateral sclerosis. rhCNTF ALS Study Group. Ann. Neurol. 39, 256-260. (doi:10.1002/ana.410390215)
112. Mitchell, A. J., ito-Leon, J., Gonzalez, J. M. & Rivera-Navarro, J. 2005 Quality of life and its assessment in multiple sclerosis: integrating physical and psychological components of wellbeing. Lancet Neurol. 4, 556-566. (doi:10.1016/S1474-4422(05)70166-6)
113. Mittoux, V. et al. 2000 Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum. Gene Ther. 11, 1177-1187. (doi:10.1089/ 10430340050015220)
114. Monje, M. L., Mizumatsu, S., Fike, J. R. & Palmer, T. D. 2002 Irradiation induces neural precursor-cell dysfunction. Nat. Med. 8, 955-962. (doi:10.1038/nm749)
115. Monje, M. L., Toda, H. & Palmer, T. D. 2003 Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765. (doi:10.1126/science.1088417)
116. Nagano, I., Ilieva, H., Shiote, M., Murakami, T., Yokoyama, M., Shoji, M. & Abe, K. 2005 Therapeutic benefit of intrathecal injection of insulin-like growth factor-1 in a mouse model of amyotrophic lateral sclerosis. J. Neurol. Sci. 235, 61-68. (doi:10.1016/j.jns.2005.04.011)
117. Nakatomi, H., Kuriu, T., Okabe, S., Yamamoto, S., Hatano, O., Kawahara, N., Tamura, A., Kirino, T. & Nakafuku, M. 2002 Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441. (doi:10.1016/S0092-8674(02) 00862-0)
118. Neufeld, E. F. & Munzer, J. 2001 The mucopolysaccharides, 8th edn, pp. 3421-3452. New York, NY: McGraw-Hill.
119. Nikkhah, G., Olsson, M., Eberhard, J., Bentlage, C., Cunningham, M. G. & Bjorklund, A. 1994 A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63, 57-72.
120. Nunes, M. C., Roy,N. S., Keyoung,H. M., Goodman, R. R., McKhann, G., Jiang, L., Kang, J., Nedergaard, M. & Goldman, S. A. 2003 Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat. Med. 9, 439-447. (doi:10.1038/nm837)
121. Nutt, J. G. et al. 2003 Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60, 69-73.
122. Olanow, C. W. et al. 2003 A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann. Neurol. 54, 403-414. (doi:10.1002/ana.10720)
123. Olsson, M., Nikkhah, G., Bentlage, C. & Bjorklund, A. 1995 Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15, 3863-3875.
124. Orth, M. & Tabrizi, S. J. 2003 Models of Parkinson's disease. Mov. Disord. 18, 729-737. (doi:10.1002/mds.10447)
125. Ortiz-Gonzalez, X. R., Keene, C. D., Verfaillie, C. M. & Low, W. C. 2004 Neural induction of adult bone marrow and umbilical cord stem cells. Curr. Neurovasc. Res. 1, 207-213. (doi:10.2174/1567202043362342)
126. Palmer, T. D., Ray, J. & Gage, F. H. 1995 FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell Neurosci. 6, 474-486. (doi:10.1006/mcne.1995. 1035)
127. Palmer, T. D., Willhoite, A. R. & Gage, F. H. 2000 Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494. (doi:10.1002/1096-9861(20001002)425:4 〈479::AID-CNE2〉3.0.CO;2-3)
128. Palmer, T. D., Schwartz, P. H., Taupin, P., Kaspar, B., Stein, S. A. & Gage, F. H. 2001 Cell culture. Progenitor cells from human brain after death. Nature 411, 42-43. (doi:10.1038/35075141)
129. Parent, J. M., Vexler, Z. S., Gong, C., Derugin, N. & Ferriero, D. M. 2002 Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802-813. (doi:10.1002/ana.10393)
130. Park, C. H. et al. 2005 In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J. Neurochem. 92, 1265-1276. (doi:10.1111/j.1471-4159.2004.03006.x)
131. Patel, N. K., Bunnage, M., Plaha, P., Svendsen, C. N., Heywood, P. & Gill, S. S. 2005 Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: a two-year outcome study. Ann. Neurol. 57, 298-302. (doi:10.1002/ana.20374)
132. Penn, R. D., Kroin, J. S., York, M. M. & Cedarbaum, J. M. 1997 Intrathecal ciliary neurotrophic factor delivery for treatment of amyotrophic lateral sclerosis (phase I trial). Neurosurgery 40, 94-99. (doi:10.1097/00006123-199701000-00021)
133. Perrier, A. L., Tabar, V., Barberi, T., Rubio, M. E., Bruses, J., Topf, N., Harrison, N. L. & Studer, L. 2004 Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl Acad. Sci. USA 101, 12 543-12 548. (doi:10.1073/pnas.0404700101)
134. Peschanski, M., Bachoud-Levi, A. C. & Hantraye, P. 2004 Integrating fetal neural transplants into a therapeutic strategy: the example of Huntington's disease. Brain 127, 1219-1228. (doi:10.1093/brain/ awh145)
135. Peters, C. et al. 1996 Outcome of unrelated donor bone marrow transplantation in 40 children with Hurler syndrome. Blood 87, 4894-4902.
136. Rabin, S. 2005 The gatekeepers of hES cell products. Nat. Biotechnol. 23, 817-819. (doi:10.1038/nbt0705-817)
137. Reubinoff, B. E., Pera, M. F., Fong, C. Y., Trounson, A. & Bongso, A. 2000 Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 18, 399-404. (doi:10.1038/74447)
138. Reubinoff, B. E., Itsykson, P., Turetsky, T., Pera, M. F., Reinhartz, E., Itzik, A. & Ben-Hur, T. 2001 Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 19, 1134-1140. (doi:10.1038/nbt1201-1134)
139. Richards, M., Fong, C. Y., Chan, W. K., Wong, P. C. & Bongso, A. 2002 Human feeders support prolonged undifferentiated growth of human inner cell masses and embryonic stem cells. Nat. Biotechnol. 20, 933-936. (doi:10.1038/nbt726)
140. Richardson, P. M. 1994 Ciliary neurotrophic factor: a review. Pharmacol. Ther. 63, 187-198. (doi:10.1016/0163-7258(94)90045-0)
141. Roy, N. S. et al. 2000 In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat. Med. 6, 271-277. (doi:10.1038/73119)
142. Sanchez-Pernaute, R., Studer, L., Ferrari, D., Perrier, A., Lee, H., Vinuela, A. & Isacson, O. 2005 Long-term survival of dopamine neurons derived from parthenogenetic primate embryonic stem cells (cyno-1) after transplantation. Stem Cells 23, 914-922. (doi:10.1634/stemcells. 2004-0172)
143. Sauer, H. & Oertel, W. H. 1994 Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 59, 401-415. (doi:10.1016/0306-4522(94) 90605-X)
144. Schmidt, A., Bockmann, M., Stoll, A., Racek, T. & Putzer, B. M. 2005 Analysis of adenovirus gene transfer into adult neural stem cells. Virus Res. 114, 45-53. (doi:10.1016/j.virusres.2005.05.010)
145. Schwab, M. E. & Bartholdi, D. 1996 Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370.
146. Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N., Vincent, P., Pumiglia, K. & Temple, S. 2004 Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340. (doi:10.1126/science.1095505)
147. Simon, H. H., Bhatt, L., Gherbassi,D., Sgado, P. & Alberi, L. 2003 Midbrain dopaminergic neurons: determination of their developmental fate by transcription factors. Ann. N. Y. Acad. Sci. 991, 36-47.
148. Singh, R. N., Nakano, T., Xuing, L., Kang, J., Nedergaard, M. & Goldman, S. A. 2005 Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp. Neurol. 196, 224-234. (doi:10.1016/j.expneurol.2005.06.021)
149. Slevin, J. T., Gerhardt, G. A., Smith, C. D., Gash, D. M., Kryscio, R. & Young, B. 2005 Improvement of bilateral motor functions in patients with Parkinson disease through the unilateral intraputaminal infusion of glial cell line-derived neurotrophic factor. J. Neurosurg. 102, 216-222.
150. Song, H., Stevens, C. F. & Gage, F. H. 2002 Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44. (doi:10.1038/417039a)
151. Sonntag, K. C. et al. 2005 Context-dependent neuronal differentiation and germ layer induction of Smad4-/-and Cripto-/- embryonic stem cells. Mol. Cell Neurosci. 28, 417-429. (doi:10.1016/j.mcn.2004. 06.003)
152. Spalding, K. L., Bhardwaj, R. D., Buchholz, B. A., Druid, H. & Frisen, J. 2005 Retrospective birth dating of cells in humans. Cell 122, 133-143. (doi:10.1016/j.cell.2005.04.028)
153. Staba, S. L. et al. 2004 Cord-blood transplants from unrelated donors in patients with Hurler's syndrome. N. Engl. J. Med. 350, 1960-1969. (doi:10.1056/NEJMoa032613)
154. Svendsen, C. N., Clarke,D. J., Rosser, A. E. & Dunnett, S. B. 1996 Survival and differentiation of rat and human epidermal growth factor-responsive precursor cells following grafting into the lesioned adult central nervous system. Exp. Neurol. 137, 376-388. (doi:10.1006/exnr.1996.0039)
155. Svendsen, C. N., ter Borg, M. G., Armstrong, R. J., Rosser, A. E., Chandran, S., Ostenfeld, T. & Caldwell, M. A. 1998 A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 85, 141-152. (doi:10.1016/S0165-0270(98)00126-5)
156. Tabar, V., Panagiotakos, G., Greenberg, E. D., Chan, B. K., Sadelain, M., Gutin, P. H. & Studer, L. 2005 Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat. Biotechnol. 23, 601-606. (doi:10.1038/nbt1088)
157. Tanapat, P., Galea, L. A. & Gould, E. 1998 Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci. 16, 235-239. (doi:10.1016/S0736-5748(98) 00029-X)
158. Tanapat, P., Hastings, N. B., Reeves, A. J. & Gould, E. 1999 Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19, 5792-5801.
159. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. & Jones, J. M. 1998 Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147. (doi:10.1126/science.282.5391.1145)
160. Toma, J. G., McKenzie, I. A., Bagli, D. & Miller, F. D. 2005 Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23, 727-737. (doi:10.1634/stemcells.2004-0134)
161. Ungerstedt, U. 1971 Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. Acta Physiol. Scand. 367(Suppl.), 49-68.
162. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D. & Gage, F. H. 2002 Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. (doi:10.1038/4151030a)
163. Verma, P. & Fawcett, J. 2005 Spinal cord regeneration. Adv. Biochem. Eng Biotechnol. 94, 43-66.
164. Vescovi, A. L., Gritti, A., Galli, R. & Parati, E. A. 1999 Isolation and intracerebral grafting of nontransformed multipotential embryonic human CNS stem cells. J. Neurotrauma 16, 689-693.
165. Wallen, A. & Perlmann, T. 2003 Transcriptional control of dopamine neuron development. Ann. N. Y. Acad. Sci. 991, 48-60.
166. Wang, L., Zhang, Z.,Wang, Y., Zhang, R. & Chopp,M. 2004 Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35, 1732-1737. (doi:10.1161/01.STR.0000132196.49028.a4)
167. Wenger, D. A., Suzuki, K. & Suzuki, Y. 2001 Galactosylceramide lipidosis: globoid cell leukodystrophy (Krabbe disease), 8th edn, pp. 3669-3694. New York, NY: McGraw Hill.
168. Wharton, S. & Ince, P. G. 2003 Pathology of motor neuron disorders, pp. 17-50. Philadelphia, PA: Butterworth-Heinemann.
169. Windrem, M. S., Nunes, M. C., Rashbaum,W. K., Schwartz, T. H., Goodman, R. A., McKhann, G., Roy, N. S. & Goldman, S. A. 2004 Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 10, 93-97. (doi:10.1038/nm974)
170. Winkler, C., Kirik, D. & Bjorklund, A. 2005 Cell transplantation in Parkinson's disease: how can we make it work? Trends Neurosci. 28, 86-92. (doi:10.1016/j.tins.2004.12.006)
171. Wu, P., Ye, Y. & Svendsen, C. N. 2002 Transduction of human neural progenitor cells using recombinant adeno-associated viral vectors. Gene Ther. 9, 245-255. (doi:10.1038/sj.gt.3301646)
172. Yamada, T., McGeer, P. L., Baimbridge, K. G. & McGeer, E. G. 1990 Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res. 526, 303-307. (doi:10.1016/0006-8993(90)91236-A)
173. Zhang, S. C., Wernig, M., Duncan, I. D., Brustle, O. & Thomson, J. A. 2001 In vitro differentiationof transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133. (doi:10.1038/nbt1201-1129)