Stem cell therapy for Parkinson's disease

Expert Review of Neurotherapeutics

Volumn 7, Issue 6, 2007, Pages 667-675

  Takahashi, Jun ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Dopaminergic; Embryonic stem cell; Neural stem cell; Neuron; Transplantation

Indexed keywords

CELL SPECIFICITY; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PARKINSON DISEASE; PRIMATE; REVIEW; STEM CELL TRANSPLANTATION;

ANIMALS; BIOMEDICAL RESEARCH; CLINICAL TRIALS; HUMANS; PARKINSON DISEASE; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE ENGINEERING; TREATMENT OUTCOME;

EID: 34250342147     PISSN: 14737175     EISSN: 17448360     Source Type: Journal    
DOI: 10.1586/14737175.7.6.667     Document Type: Review

References (68)

1. Olanow CW, Tatton WG. Etiology and pathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 22, 123-144 (2000).
2. Bergman H, Deuschl G. Pathophysiology of Parkinson's disease: from clinical neurology to basic neuroscience and back. Mov. Disord. 17(Suppl. 3), S28-S40 (2002).
3. Dostrovsky JO, Hutchison WD, Lozano AM. The globus pallidus, deep brain stimulation, and Parkinson's disease. Neuroscientist 8, 284-290 (2002).
4. Miyasaki JM, Martin W, Suchowersky O, Weiner WJ, Lang AE. Practice parameter: initiation of treatment for Parkinson's disease: an evidence-based review: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 58, 11-17 (2002).
5. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders - how to make it work. Nat. Med. 10, S42-S50 (2004).
6. Gage FH. Mammalian neural stem cells. Science 287, 1433-1438 (2000).
7. Doetsch FA. A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 13, 543-550 (2003).
8. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl Acad. Sci. USA 78, 7634-7638 (1981).
9. Hauser RA, Freeman TB, Snow BJ et al. Long-term evaluation of bilateral fetal nigral transplantation in Parkinson disease. Arch. Neurol. 56, 179-187 (1999).
10. Piccini P, Brooks DJ, Björklund A et al. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat. Neurosci. 2, 1137-1140 (1999).
11. Lindvall O, Hagell P. Clinical observations after neural transplantation in Parkinson's disease. Prog. Brain Res. 127, 299-320 (2000).
12. Freed CR, Greene PE, Breeze RE et al. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719 (2001). • First report of a double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease (PD).
13. Olanow CW, Goetz CG, Kordower JH et al. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann. Neurol. 54, 403-414 (2003).
14. Ma Y, Feigin A, Dhawan V et al. Dyskinesia after fetal cell transplantation for parkinsonism: a positron emission tomography (PET) study. Ann. Neurol. 52, 628-634 (2002).
15. Mukhida K, Baker KA, Sadi D, Mendez I. Enhancement of sensorimotor behavioral recovery in hemiparkinsonian rats with intrastriatal, intranigral, and intrasubthalamic nucleus dopaminergic transplants. J. Neurosci. 21, 3521-3530 (2001).
16. Mendez I, Sanchez-Pernaute R, Cooper O et al. 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 (2005).
17. Carpenter MK, Cui X, Hu Z-Y et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158, 265-278 (1999).
18. Ostenfeld T, Caldwell MA, Prowse KR, Linskens MH, Jauniaux E, Svendsen CN. Human neural precursor cells express low levels of telomerase in vitro and show diminishing cell proliferation with extensive axonal outgrowth following transplantation. Exp. Neurol. 164, 215-226 (2000).
19. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. Progenitor cells from human brain after death. Nature 411, 42-43 (2001).
20. Vescovi AL, Parati EA, Gritti A et al. Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of trans-plantable human neural stem cell lines by epigenetic stimulation. Exp. Neurol. 156, 71-83 (1999).
21. Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Björklund A. Site-specific migration and neural differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci. 19, 5990-6005 (1999).
22. Hitoshi S, Tropepe V, Ekker M, van der Kooy D. Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development 129, 233-244 (2002).
23. Jain M, Armstrong RJ, Tyers P, Barker RA, Rosser AE. GABAergic immunoreactivity is predominant in neurons derived from expanded human neural precursor cells in vitro. Exp. Neurol. 182, 113-123 (2003).
24. Ostenfeld T, Joly E, Tai Y-T et al. Regional specification of rodent and human neurospheres. Dev. Brain Res. 134, 43-55 (2002).
25. Storch A, Paul G, Csete M et al. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp. Neurol. 170, 317-325 (2001).
26. Sánchez-Pernaute R, Studer L, Bankiewicz KS, Major EO, McKay RD. in vitro generation and transplantation of precursor-derived human dopamine neurons. J. Neurosci. Res. 65, 284-288 (2001).
27. Horiguchi S, Takahashi J, Kishi Y et al. Neural precursor cells derived from human embryonic brain retain regional specificity. J. Neurosci. Res. 75, 817-824 (2004).
28. Lee S-H, Lumelsky N, Studer L, Auerbach JM, McKay RD. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotech. 18, 675-679 (2000). • One of the first pieces of evidence for the generation of dopaminergic (DA) neurons from mouse embryonic stem cells (ESCs).
29. Kawasaki H, Mizuseki K, Nishikawa S et al. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40 (2000). • One of the first pieces of evidence for the generation of DA neurons from mouse ESCs.
30. Björklund LM, Sánchez-Pernaute R, Chung S et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl Acad. Sci. USA 99, 2344-2349 (2002). •• First report demonstrating functional improvement by transplantation of mouse ESC-derived DA neurons.
31. Kim J-H, Auerbach JM, Rodriguez-Gómez J et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56 (2002).
32. Barberi T, Klivenyi P, Calingasan NY et al. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotech. 21, 1200-1207 (2003).
33. Takagi Y, Takahashi J, Saiki H et al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J. Clin. Invest. 115, 102-109 (2005). •• First evidence demonstrating functional improvement by transplantation of primate ESC-derived DA neurons into monkey PD models.
34. Deacon T, Dinsmore J, Constantini LC, Ratliff J, Isacson O. Blastula-stage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp. Neurol. 149, 28-41 (1998).
35. Ying QL, Stavridis M, Griffiths D, Li M, Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monocultures. Nat. Biotech. 21, 183-186 (2003).
36. Ben-Hur T, Idelson M, Khaner H et al. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in parkinsonian rats. Stem Cells 22, 1246-1255 (2004).
37. Reubinoff BE, Itsykson P, Turetsky T et al. Neural progenitors from human embryonic stem cells. Nat. Biotech. 19, 1134-1140 (2001).
38. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotech. 19, 1129-1133 (2001).
39. Erdö F, Bührle C, Blunk J et al. Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J. Cereb. Blood Flow Metab. 23, 780-785 (2003).
40. Nishimura F, Yoshikawa M, Kanda S et al. 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 (2003).
41. Fukuda H, Takahashi J, Watanabe K et al. FACS-based purification of ES cell-derived neural precursors averts tumor formation after transplantation. Stem Cells 24, 763-771 (2006).
42. Chung S, Shin BS, Hedlund E et al. Genetic selection of sox1GFP-expressing neural precursors removes residual tumorigenic pluripotent stem cells and attenuates tumor formation after transplantation. J. Neurochem. 97, 1467-1480 (2006).
43. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG. Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J. Cell Biol. 167, 723-734 (2004).
44. Schierle GS, Hansson O, Leist M, Nicotera P, Widner H, Brundin P. Caspase inhibition reduces apoptosis and increases survival of nigral transplants. Nat. Med. 5, 97-100 (1999).
45. Perrier AL, Tabar V, Barberi T et al. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl Acad. Sci. USA 101, 12543-12548 (2004).
46. Zeng X, Cai J, Chen J et al. Dopaminergic differentiation of human embryonic stem cells. Stem Cells 22, 925-940 (2004).
47. Schulz TC, Noggle SA, Palmarini GM et al. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells 22, 1218-1238 (2004).
48. Yan Y, Yang D, Zarnowska ED et al. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23, 781-790 (2005).
49. Park CH, Minn YK, Lee JY et al. In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J. Neurochem. 92, 1265-1276 (2005).
50. Brederlau A, Correia AS, Anisimov SV et al. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells 24, 1433-1440 (2006).
51. Ueno M, Matsumura M, Watanabe K et al. Neural conversion of ES cells by an inductive activity on human amniotic membrane matrix. Proc. Natl Acad. Sci. USA 103, 9554-9559 (2006).
52. Roy NS, Cleren C, Singh SK, Yang L, Beal MF, Goldman SA. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12, 1259-1268 (2006).
53. Sonntag KC, Pruszak J, Yoshizaki T, van Arensbergen J, Sanchez-Pernaute R, Isacson O. Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the BMP antagonist Noggin. Stem Cells 25, 411-418 (2007).
54. Dezawa M, Kanno H, Hoshino M et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J. Clin. Invest. 113, 1701-1710 (2004).
55. Medicetty S, Bledsoe AR, Fahrenholtz CB, Troyer D, Weiss ML. Transplantation of pig stem cells into rat brain: proliferation during the first 8 weeks. Exp. Neurol. 190, 32-41 (2004).
56. Lie DC, Colamarino SA, Song HJ. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375 (2005).
57. Arvidsson A, Collin T, Kirik D et al. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970 (2002).
58. Parent JM, Vexler ZS, Gong C et al. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802-813 (2002).
59. Jin K, Sun Y, Xie L et al. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol. Cell. Neurosci. 24, 171-189 (2003).
60. Nakatomi H, Kuriu T, Okabe S et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441 (2002).
61. Curtis MA, Penney EB, Pearson AG et al. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl Acad. Sci. USA 100, 9023-9027 (2003).
62. Jin K, Peel AL, Mao XO et al. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl Acad. Sci. USA 101, 343-347 (2004).
63. Zhao M, Momma S, Delfani K et al. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl Acad. Sci. USA 100, 7925-7930 (2003).
64. Cooper O, and Isacson O. Intrastriatal transforming growth factor a delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J. Neurosci. 24, 8924-8931 (2004).
65. Chen Y, Ai Y, Slevin JR, Maley BE, Gash DM. Progenitor proliferation in the adult hippocampus and substantia nigra induced by glial cell line-derived neurotrophic factor. Exp. Neurol. 196, 87-95 (2005).
66. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc. Natl Acad. Sci. USA 101, 10177-10182 (2004).
67. Kanatsu-Shinohara M, Inoue K, Lee J et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell 119, 1001-1012 (2004).
68. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006). •• Report of pluripotent stem cells derived from self-cells.