Current advances in the treatment of Parkinson's disease with stem cells

Current Neurovascular Research

Volumn 4, Issue 2, 2007, Pages 99-109

  Trzaska, Katarzyna A ^a,b   Rameshwar, Pranela ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Cell replacement; Development; Dopamine; Neural repair; Parkinson's disease; Stem cells; Transplantation

Indexed keywords

BRAIN DEGENERATION; CLINICAL FEATURE; DISEASE COURSE; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; HUMAN; LOCOMOTION; MESENCEPHALON; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYME; MICROENVIRONMENT; NERVOUS TISSUE; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SUBSTANTIA NIGRA;

ANIMALS; CELL DIFFERENTIATION; DOPAMINE; HUMANS; MODELS, BIOLOGICAL; NEURONS; PARKINSON DISEASE; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 34248177735     PISSN: 15672026     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720207780637199     Document Type: Review

References (120)

1. Alhadlaq, A, Mao, JJ. (2004) Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev 13: 436-448.
2. Andersson, E, Tryggvason, U, Deng, Q, Friling, S, Alekseenko, Z, Robert, B, Perlmann, T, Ericson, J. (2006) Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124: 393-405.
3. Andersson, E, Jensen, JB, Parmar, M, Guillemot, F, Bjorklund, A. (2006) Development of the mesencephalic dopaminergic neuron system is compromised in the absence of neurogenin 2. Development 133: 507-516.
4. Ang, SL. (2006) Transcriptional control of midbrain dopaminergic neuron development. Development 133: 3499-3506.
5. Angelopoulou, M, Novelli, E, Grove, JE, Rinder, HM, Civin, C, Cheng, L, Krause, DS. (2003) Cotransplantation of human mesenchymal stem cells enhances human myelopoiesis and megakaryocytopoiesis in NOD/SCID mice. Exp Hematol 31: 413-420.
6. Arenas, E. (2005) Engineering a dopaminergic phenotype in stem/precursor cells: role of Nurr1, glia-derived signals, and Wnts. Ann N Y Acad Sci 1049: 51-66.
7. Barker, RA, Widner, H. (2004) Immune problems in central nervous system cell therapy. NeuroRx 1: 472-481.
8. Barry, FP. (2003) Biology and clinical applications of mesenchymal stem cells. Birth Defects Res C Embryo Today 69: 250-256.
9. Barzilai, A, Melamed E, Shirvan, A. (2001) Is there a rationale for neuroprotection against dopamine toxicity in Parkinson's disease? Cell Mol Neurobiol 21: 215-235.
10. Ben-Hur, T, Idelson, M, Khaner, H, Pera, M, Reinhartz, E, Itzik, A, Reubinoff, BE. (2004) Transplanatation of human embryonic stem cellderived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells 22: 1246-1255.
11. Bianco, P, Riminucci, M, Gronthos, S, Robey, PG. (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19: 180-192.
12. Bjorklund, LM, Sanchez-Pernaute, R, Chung, S, Andersson, T, Chen, IY, McNaught, KSP, Brownell, AL, Jenkins, BG, Wahlestedt, C, Kim, KS, Isacson, O. (2002) Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99: 2344-2349.
13. Brederlau, A, Correia, AS, Anisimov, SV, Elmi, M, Paul, G, Roybon, L, Morizane, A, Bergquist, F, Riebe, I, Nannmark, U, Carta, M, Hanse, E, Takahashi, J, Sasai, Y, Funa, K, Brundin, P, Eriksson, PS, Li, JY. (2006) 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.
14. Buytaert-Hoefen, KA, Alvarez, E, Freed, CR. (2004) Generation of tyrosine hydroxylase positive neurons from human embryonic stem cells after coculture with cellular substrates and exposure to GDNF. Stem Cells 22: 669-674.
15. Caplan, AI, Bruder, SP. (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7: 259-264.
16. Carvey, PM, Ling, ZD, Sortwell, CE, Pitzer, MR, McGuire, SO, Storch, A, Collier, TJ. (2001) A clonal line of mesencephalic progenitor cells converted to dopamine neurons by hematopoietic cytokines: a source of cells for transplantation in Parkinson's disease. Exp Neurol 171: 98-108.
17. Castelo-Branco, G, Wagner, J, Rodriguez, FJ, Kele, J, Sousa, K, Rawal, N, Pasolli, HA, Fuchs, E, Kitajewski, J, Arenas, E. (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci U S A 100: 12747-12752.
18. Castelo-Branco, G, Arenas, E. (2006) Function of Wnts in dopaminergic neuron development. Neurodegener Dis 3: 5-11.
19. Chiu, AY, Hall, ZW. (2006) Stem cell research: the California experience. J Neurosci 26: 6661-6663.
20. Cho, KJ, Trzaska, KA, Greco, SJ, McArdle, J, Wang, FS, Ye, JH, Rameshwar, P. (2005) Neurons derived from human mesenchymal stem cells show synaptic transmission and can be induced to produce the neurotransmitter substance P by interleukin-1 alpha. Stem Cells 23: 383-391.
21. Chung, S, Shin, BS, Hwang, M, Lardaro, T, Kang, UJ, Isacson, O, Kim, KS. (2006) Neural precursors derived from embryonic stem cells, but not those from fetal ventral mesencephalon, maintain the potential to differentiate into dopaminergic neurons after expansion in vitro. Stem Cells 24: 1583-1593.
22. Cizkova, D, Rosocha, J, Vanicky, I, Jergova, S, Cizek, M. (2006) Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol Neurobiol 26:1165-1178.
23. Correia, AS, Anisimov, SV, Li, JY, Brundin, P. (2005) Stem cell-based therapy for Parkinson's disease. Ann Med 37: 487-498.
24. Crigler, L, Robey, RC, Asawachaicharn, A, Gaupp, D, Phinney, DG. (2006) Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 198: 54-64.
25. Daadi, MM, Weiss, S. (1999) Generation of tyrosine hydroxylase-producing neurons from precursors of the embryonic and adult forebrain. J Neurosci 19: 4484-4497.
26. de Hemptinne, I, Vermeiren, C, Maloteaux, JM, Hermans, E. (2004) Induction of glial glutamate transporters in adult mesenchymal stem cells. J Neurochem 91: 155-166.
27. Deacon, T, Dinsmore, J, Costantini, LC, Ratliff, J, Isacson, O. (1998) Blastulastage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp Neurol 149: 28-41.
28. Dearry, A, Gingrich, JA, Falardeau, P, Fremeau, RT, Jr., Bates, MD, Caron, MG. (1990) Molecular cloning and expression of the gene for a human D1 dopamine receptor. Nature 347: 72-76.
29. Deng, J, Peterson, BE, Steindler, DA, Jorgensen, ML, Laywell, ED. (2006) Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24: 1054-1064.
30. Dezawa, M, Kanno, H, Hoshino, M, Cho, H, Matsumoto, N, Itokazu, Y, Tajima, N, Yamada, H, Sawada, H, Ishikawa, H, Mimura, T, Kitada, M, Suzuki, Y, Ide, C. (2004) Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest 113: 1701-1710.
31. Dziewczapolski, G, Lie, DC, Ray, J, Gage, FH, Schuls, CW. (2003) Survival and differentiation of adult rat-derived neural progenitor cells transplanted to the striatum of hemiparkinsonian rats. Exp Neurol 183: 653-664.
32. Fallon, J, Reid, S, Kinyamu, R, Opole, I, Opole, R, Baratta, J, Korc, M, Endo, TL, Duong, A, Nguyen, G, Karkehabadhi, M, Twardzik, D, Loughlin, S. (2000) In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 97: 14686-14691.
33. Freed, CR, Greene, PE, Breeze, RE, Tsai, WY, DuMouchel, W, Kao, R, Dillon, S, Winfield, H, Culver, S, Trojanowski, JQ, Eidelberg, D, Fahn, S. (2001) Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 344: 710-719.
34. Frielingsdorf, H, Schwarz, K, Brudin, P, Mohapel, P. (2004) No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 101: 10177-10182.
35. Fu, YS, Cheng, YC, Lin, MY, Cheng, H, Chu, PM, Chou, SC, Shih, YH, Ko, MH, Sung, MS. (2006) Conversion of human umbilical cord mesenchymal stem cells in Wharton's jelly to dopaminergic neurons in vitro - potential therapeutic application for Parkinsonism. Stem Cells 24: 115-124.
36. Grothe, C, Timmer, M, Scholz, T, Winkler, C, Nikkhah, G, Claus, P, Itoh, N, Arenas, E. (2004) Fibroblast growth factor-20 promotes the differentiation of Nurr1-overexpressing neural stem cells into tyrosine hydroxylase-positive neurons. Neurobiol Dis 17: 163-170.
37. Guo, L, Yin, F, Meng, HQ, Ling, L, Hu-He, TN, Li, P, Zhang, CX, Yu, S, Duan, CS, Fan, HX. (2005) Differentiation of mesenchymal stem cells into dopaminergic neuron-like cells in vitro. Biomed Environ Sci 18: 36-42.
38. Hagell, P, Piccini, P, Bjorklund, A, Brundin, P, Rehncrona, S, Widner, H, Crabb, L, Pavese, N, Oertel, WH, Quinn, N, Brooks, DJ, Lindvall, O. (2002) Dyskenesias following neural transplantation in Parkinson's disease. Nat Neurosci 5: 627-628.
39. Hermann, A, Maisel, M, Wegner, F, Liebau, S, Kim, DW, Gerlach, M, Schwarz, J, Kim, KS, Storch, A. (2006) Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 24: 949-964.
40. Hellmann, MA, Panet, H, Barhum, Y, Melamed, E, Offen, D. (2006) Increased survival and migration of engrafted mesenchymal bone marrow stem cells in 6-hydroxydopamine-lesioned rodents. Neurosci Lett 395: 124-128.
41. Hermanson, E, Joseph, B, Castro, D, Lindqvist, E, Aarnisalo, P, Wallen, A, Benoit, G, Hengerer, B, Olson, L, Perlmann, T. (2003) Nurr1 regulates dopamine synthesis and storage in MN9D dopamine cells. Exp Cell Res 288: 324-334.
42. Isacson, O, Bjorklund, LM, Schumacher, JM. (2003) Toward full restoration of synaptic and terminal function of the dopaminergic system in Parkinson's disease by stem cells. Ann Neurol 53(Suppl 3): S135-146; discussion S146-138.
43. Jankovic, J, Chen, S, Le, WD. (2005) The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Prog Neurobiol 77: 128-138.
44. Jiang, Y, Jahagirdar, BN, Reinhardt, RL, Schwartz, RE, Keene, CD, Ortiz-Gonzalez, XR, Reyes, M, Lenvik, T, Lund, T, Blackstad, M, Du, J, Aldrich, S, Lisberg, A, Low, WC, Largaespada, DA, Verfaillie, CM. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49.
45. Kawasaki, H, Mizuseki, K, Nishikawa, S, Kaneko, S, Kuwana, Y, Nakanishi, S, Nishikawa, SI, Sasai, Y. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28: 31-40.
46. Kawasaki, H, Suemori, H, Mizuseki, K, Watanabe, K, Urano, F, Ichinose, H, Haruta, M, Takahashi, M, Yoshikawa, K, Nishikawa, S, Nakatsuji, N, Sasai, Y. (2002) Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc Natl Acad Sci U S A 99: 1580-1585.
47. Kele, J, Simplicio, N, Ferri, AL, Mira, H, Guillemot, F, Arenas, E, Ang, SL. (2006) Neurogenin 2 is required for the development of ventral midbrain dopaminergic neurons. Development 133: 495-505.
48. Kern, S, Eichler, H, Stoeve, J, Kluter, H, Bieback, K. (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24: 1294-1301.
49. Kim, JH, Auerbach, JM, Rodriguez-Gomez, JA, Velasco, I, Gavin, D, Lumelsky, N, Lee, SH, Nguyen, J, Sanchez-Pernaute, R, Bankiewicz, K, McKay, R. (2002) Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418: 50-56.
50. Kim, DW, Chung, S, Hwang, M, Ferree, A, Tsai, HC, Park, JJ, Chung, S, Nam, TS, Kang, UJ, Isacson, O, Kim, KS. (2006) Stromal cell-derived inducing activity, Nurr1, and signaling molecules synergistically induce dopaminergic neurons from mouse embryonic stem cells. Stem Cells 24: 557-567.
51. Klein, C, Schlossmacher, MG. (2006) The genetics of Parkinson's disease: Implications for neurological care. Nat Clin Pract Neurol 2: 136-146.
52. Kodama, H, Hagiwara, H, Sudo, H, Amagai, Y, Yokota, T, Arai, N, Kitamura, Y. (1986) MC3T3-G2/PA6 preadipocytes support in vitro proliferation of hemopoietic stem cells through a mechanism different from that of interleukin 3. J Cell Physiol 129: 20-26.
53. Kondo, T, Johnson, SA, Yoder, MC, Romand, R, Hashino, E. (2005) Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc Natl Acad Sci U S A 102: 4789-4794.
54. Kordower, JH, Freeman, TB, Snow, BJ, Vingerhoets, FJ, Mufson, EJ, Sanberg, PR, Hauser, RA, Smith, DA, Nauert, GM, Perl, DP, Olanow, CW. (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.
55. Krampera, M, Pasini, A, Pizzolo, G, Cosmi, L, Romagnani, S, Annunziato, F. (2006) Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr Opin Pharmacol 6: 435-441.
56. Le Blanc, K, Rasmusson, I, Sundberg, B, Gotherstrom, C, Hassan, M, Uzunel, M, Ringden, O. (2004) Treatment of severe acute graft-versushost disease with third party haploidentical mesenchymal stem cells. Lancet 363: 1439-1441.
57. Lee, MA, Lee, HS, Lee, HS, Cho, KG, Jin, BK, Sohn, S, Lee YS, Ichinose, H, Kim, SU. (2002) Overexpression of midbrain-specific transcription factor Nurr1 modifies susceptibility of mouse neural stem cells to neurotoxins. Neurosci Lett 333: 74-78.
58. Lee, SH, Lumelsky, N, Studer, L, Auerbach, JM, McKay, RD. (2000) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 18: 675-679.
59. Li, F, Chong, ZZ, Maiese, K. (2005) Vital elements of the Wnt-Frizzled signaling pathway in the nervous system. Curr Neurovasc Res 2: 331-340.
60. Li, Y, Chen, J, Wang, L, Zhang, L, Lu, M, Chopp, M. (2001) Intracerebral transplantation of bone marrow stromal cells in a 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. Neurosci Lett 315: 67-70.
61. Lie, DC, Dziewczapolski, G, Willhoite, AR, Kaspar, BK, Shults, CW, Gage, FH. (2002) The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 22: 6639-6649.
62. Lin, JC, Rosenthal, A. (2003) Molecular mechanisms controlling the development of dopaminergic neurons. Semin Cell Dev Biol 14: 175-180.
63. Lindvall, O, Kokaia, Z, Martinez-Serrano, A. (2004) Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 10 (Suppl): S42-50.
64. Liste, I, Navarro, B, Johansen, J, Bueno, C, Villa, A, Johansen, TE, Martinez-Serrano, A. (2004) Low-level tyrosine hydroxylase (TH) expression allows for the generation of stable TH+ cell lines of human neural stem cells. Hum Gene Ther 15: 13-20.
65. Liste, I, Garcia-Garcia, E, Martinez-Serrano, A. (2004) The generation of dopaminergic neurons by human neural stem cells is enhanced by Bcl-XL, both in vitro and in vivo. J Neurosci 24: 10786-10795.
66. Martinat, C, Bacci, JJ, Leete, T, Kim, J, Vanti, WB, Newman, AH, Cha, JH, Gether, U, Wang, H, Abeliovich, A. (2006) Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phenotype. Proc Natl Acad Sci U S A 103: 2874-2879.
67. Meador-Woodruff, JH, Mansour, A, Healy, DJ, Kuehn, R, Zhou, QY, Bunzow, JR, Akil, H, Civelli, O, Watson, SJ Jr. (1991) Comparison of the distributions of D1 and D2 dopamine receptor mRNAs in rat brain. Neuropsychopharmacology 5: 231-242.
68. 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.
69. Missale, C, Nash, SR, Robinson, SW, Jaber, M, Caron, MG. (1998) Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
70. Nishimura, F, Yoshikawa, M, Kanda, S, Nonaka, M, Yokota, H, Shiroi, A, Nakase, H, Hirabayaski, H, Ouji, Y, Birumachi, J, Ishizaka, S, Sakaki, T. (2003) Potential use of embryonic stem cells for the treatment of mouse parkinsonian models: improved behavior by transplantation of in vitro differentiated dopaminergic neurons from embryonic stem cells. Stem Cells 21: 171-180.
71. Olanow, CW, Goetz, CG, Kordower, JH, Stoessl, AJ, Sossi, V, Brin, MF, Shannon, KM, Nauert, GM, Perl, DP, Godbold, J, Freeman, TB. (2003) A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 54: 403-414.
72. Olanow, CW, Obeso, JA, Stocchi, F. (2006) Drug insight: Continuous dopaminergic stimulation in the treatment of Parkinson's disease. Nat Clin Pract Neurol 2: 382-392.
73. Park, CH, Minn, YK, Lee, JY, Choi, DH, Chang, MY, Shim, JW, Ko, JY, Koh, HC, Kang, MJ, Kang, JS, Rhie, DJ, Lee, YS, Son, H, Moon, SY, Kim, KS, Lee, SH. (2005) In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J Neurochem 92: 1265-1276.
74. Patapoutian, A, Reichardt, LF. (2000) Roles of Wnt proteins in neural development and maintenance. Curr Opin Neurobiol 10: 392-399.
75. Perrier, AL, Studer, L. (2003) Making and repairing the mammalian brain-in vitro production of dopaminergic neurons. Semin Cell Dev Biol 14: 181-189.
76. Perrier, AL, Tabar, V, Barberi, T, Rubio, ME, Bruses, J, Topf, N, Harrison, NL, Studer, L. (2004) Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 101: 12543-12548.
77. Perrone-Capano, C, Di Porzio, U. (2000) Genetic and epigenetic control of midbrain dopaminergic neuron development. Int J Dev Biol 44: 679-687.
78. Phinney, DG, Isakova, I. (2005) Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system. Curr Pharm Des 11: 1255-1265.
79. Phinney, DG, Gray, AJ, Hill, K, Pandey A. (2005) Murine mesenchymal and embryonic stem cells express a similar Hox gene profile. Biochem Biophys Res Commun 338: 1759-1765.
80. Potian, JA, Aviv, H, Ponzio, NM, Harrison, JS, Rameshwar, P. (2003) Vetolike activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 171: 3426-3434.
81. Prakash, N, Brodski, C, Naserke, T, Puelles, E, Gogoi, R, Hall, A, Panhuysen, M, Echevarria, D, Sussel, L, Weisenhorn, DM, Martinez, S, Arenas, E, Simeone, A, Wurst, W. (2006) A Wnt1-regulated genetic network controls the identity and fate of midbrain-dopaminergic progenitors in vivo. Development 133: 89-98.
82. Prakash, N, Wurst, W. (2006) Development of dopaminergic neurons in the mammalian brain. Cell Mol Life Sci 63: 187-206.
83. Qian, L, Saltzman, WM. (2004) Improving the expansion and neuronal differentiation of mesenchymal stem cells through culture surface modification. Biomaterials 25: 1331-1337.
84. Roussa, E, Krieglstein, K. (2004) Induction and specification of midbrain dopaminergic cells: focus on SHH, FGF8, and TGF-beta. Cell Tissue Res 318: 23-33.
85. Roussa, E, Wiehle, M, Dunker, N, Becker-Katins, S, Oehlke, O, Krieglstein, K. (2006) Transforming growth factor beta is required for differentiation of mouse mesencephalic progenitors into dopaminergic neurons in vitro and in vivo: ectopic induction in dorsal mesencephalon. Stem Cells 24: 2120-2129.
86. Sacchetti, P, Mitchell, TR, Granneman, JG, Bannon, MJ. (2001) Nurr1 enhances transcription of the human dopamine transporter gene through a novel mechanism. J Neurochem 76: 1565-1572.
87. Sakurada, K, Ohshima-Sakurada, M, Palmer, TD, Gage, FH. (1999) Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. Development 126: 4017-4026.
88. 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.
89. Saucedo-Cardenas, O, Quintana-Hau, JD, Le, WD, Smidt, MP, Cox, JJ, De Mayo, F, Burbach, JP, Conneely, OM . (1998) Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc Natl Acad Sci U S A 95: 4013-4018.
90. Schapira, AH, Olanow, CW. (2004) Neuroprotection in Parkinson disease: mysteries, myths, and misconceptions. JAMA 291: 358-364.
91. Schwarz, EJ, Alexander, GM, Prockop, DJ, Azizi, SA. (1999) Multipotent marrow stromal cells transduced to produce L-DOPA: Engraftment in a rat model of Parkinson's disease. Hum Gene Ther 10: 2539-2549.
92. Smidt, MP, van Schaick, HS, Lanctot, C, Tremblay, JJ, Cox, JJ, van der Kleij, AA, Wolterink, G, Drouin, J, Burbach, JP. (1997) A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. Proc Natl Acad Sci U S A 94: 13305-13310.
93. Smidt, MP, Smits, SM, Burbach, JP. (2003) Molecular mechanisms underlying midbrain dopamine neuron development and function. Eur J Pharmacol 480: 75-88.
94. Smidt, MP, Smits, SM, Bouwmeester, H, Hamers, FP, van der Linden, AJ, Hellemons, AJ, Graw, J, Burbach, JP. (2004) Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Development 131: 1145-1155.
95. Smidt, MP, Smits, SM, Burbach, JP. (2004) Homeobox gene Pitx3 and its role in the development of dopamine neurons of the substantia nigra. Cell Tissue Res 318: 35-43.
96. Smits, SM, Ponnio, T, Conneely, OM, Burbach, JP, Smidt, MP. (2003) Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons. Eur J Neurosci 18: 1731-1738.
97. Smits, SM, Burbach, JP, Smidt, MP. (2006) Developmental origin and fate of meso-diencephalic dopamine neurons. Prog Neurobiol 78: 1-16.
98. Snyder, BJ, Olanow, CW. (2005) Stem cell treatment for Parkinson's disease: an update for 2005. Curr Opin Neurol 18: 376-385.
99. Sonntag, KC, Simantov, R, Isacson, O. (2005) Stem cells may reshape the prospect of Parkinson's disease therapy. Brain Res Mol Brain Res 134: 34-51.
100. Studer, L, Tabar, V, McKay, RD. (1998) Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nat Neurosci 1: 290-295.
101. Suon, S, Yang, M, Iacovitti, L. (2006) Adult human bone marrow stromal spheres express neuronal traits in vitro and in a rat model of Parkinson's disease. Brain Res 1106: 46-51.
102. Takagi, Y, Takahashi, J, Saiki, H, Morizane, A, Hayashi, T, Kishi, Y, Fukuda, H, Okamoto, Y, Koyanagi, M, Ideguchi, M, Hayashi, H, Imazato, T, Kawasaki, H, Suemori, H, Omachi, S, Iida, H, Itoh, N, Nakatsuji, N, Sasai, Y, Hashimoto, N. (2005) Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115: 102-109.
103. Tatard, VM, D'Ippolito, G, Diabira, S, Valeyev, A, Hackman, J, McCarthy, M, Bouckenooghe, T, Menei, P, Montero-Menei, CN, Schiller, PC. (2006) Neurotrophin-directed differentiation of human adult marrow stromal cells to dopaminergic-like neurons. Bone 40:360-373.
104. Tatton, WG, Chalmers-Redman, R, Brown, D, Tatton, N. (2003) Apoptosis in Parkinson's disease: Signals for neuronal degradation. Ann Neurol 53(Suppl 3): S61-S70.
105. Taylor, H, Minger, SL. (2005) Regenerative medicine in Parkinson's disease: generation of mesencephalic dopaminergic cells from embryonic stem cells. Curr Opin Biotechnol 16: 487-492.
106. Thompson, LH, Andersson, E, Jensen, JB, Barraud, P, Guillemot, F, Parmar, M, Bjorklund, A. (2006) Neurogenin2 identifies a transplantable dopamine neuron precursor in the developing ventral mesencephalon. Exp Neurol 198: 183-198.
107. Ueno, M, Matsumura, M, Watanabe, K, Nakamura, T, Osakada, F, Takahashi, M, Kawasaki, H, Kinoshita, S, Sasai, Y. (2006) Neural conversion of ES cells by an inductive activity on human amniotic membrane matrix. Proc Natl Acad Sci U S A 103: 9554-9559.
108. Wagers, AJ, Weissman, IL. (2004) Plasticity of adult stem cells. Cell 116: 639-648.
109. Wagner, J, Akerud, P, Castro, DS, Holm, PC, Canals, JM, Snyder, EY, Perlmann, T, Arenas, E. (1999) Induction of midbrain dopaminergic phenotype in Nurr1-over-expressing neural stem cells by type 1 astrocytes. Nat Biotechnol 17: 653-659.
110. Wallen-Mackenzie, A, Mata de Urquiza, A, Petersson, S, Rodriguez, FJ, Friling, S, Wagner, J, Ordentlich, P, Lenggvist, J, Heymann, RA, Arenas, E, Perlmann, T. (2003) Nurr1-RXR heterodimers mediate RXR ligand-induced signaling in neuronal cells. Genes Dev 17: 3036-3047.
111. Wang, HF, Liu, FC. (2005) Regulation of multiple dopamine signal transduction molecules by retinoids in the developing striatum. Neuroscience 134: 97-105.
112. Weiss, ML, Medicetty, S, Bledsoe, AR, Rachakatla, RS, Choi, M, Merchav, S, Luo, Y, Rao, MS, Velagaleti, G, Troyer, D. (2006) Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson's disease. Stem Cells 24: 781-792.
113. Westerlund, U, Moe, MC, Varghese, M, Berg-Johnsen, J, Ohlsson, M, Langmoen, IA, Svensson, M. (2003) Stem cells from the adult human brain develop into functional neurons in culture. Exp Cell Res 289: 378-383.
114. Wislet-Gendebien, S, Hans, G, Leprince, P, Rigo, JM, Moonen, G, Rogister, B. (2005) Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23: 392-402.
115. Yan, Y, Yang, D, Zarnowska, ED, Du, Z, Werbel, B, Valliere, C, Pearce, RA, Thomson, JA, Zhang, SC. (2005) Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23: 781-790.
116. Ye, W, Shimamura, K, Rubenstein, JL, Hynes, MA, Rosenthal, A. (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93: 755-766.
117. Yue, F, Cui, L, Johkura, K, Ogiwara, N, Sasaki, K. (2006) Induction of midbrain dopaminergic neurons from primate embryonic stem cells by coculture with sertoli cells. Stem Cells 24: 1695-1706.
118. Zeng, X, Cai, J, Chen, J, Luo, Y, You, ZB, Fotter, E, Wang, Y, Harvey, B, Miura, T, Backman, C, Chen, GJ, Rao, MS, Freed, WJ. (2004) Dopaminergic differentiation of human embryonic stem cells. Stem Cells 22: 925-940.
119. Zetterstrom, RH, Solomin, L, Jansson, L, Hoffer, BJ, Olson, L, Perlmann, T. (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276: 248-250.
120. Zhao, M, Momma, S, Delfani, K, Carlen, M, Cassidy, RM, Johansson, CB, Brismar, H, Shupliakov, O, Frisen, J, Jansen, AM. (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 100: 7925-7930.