About this Journal Submit a Manuscript Table of Contents
Parkinson’s Disease
Volume 2012 (2012), Article ID 873706, 9 pages
http://dx.doi.org/10.1155/2012/873706
Review Article

Parkinson's Disease and Mesenchymal Stem Cells: Potential for Cell-Based Therapy

Department of Stem Cell Biology and Histology, Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan

Received 3 September 2011; Accepted 14 November 2011

Academic Editor: Lachlan Thompson

Copyright © 2012 Masaaki Kitada and Mari Dezawa. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. L. Zhang, Z. G. Zhang, L. Zhang, and M. Chopp, “Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia,” Neuroscience, vol. 105, no. 1, pp. 33–41, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. O. Lindvall, P. Brundin, H. Widner et al., “Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease,” Science, vol. 247, no. 4942, pp. 574–577, 1990. View at Scopus
  3. T. Deierborg, D. Soulet, L. Roybon, V. Hall, and P. Brundin, “Emerging restorative treatments for Parkinson's disease,” Progress in Neurobiology, vol. 85, no. 4, pp. 407–432, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. C. R. Freed, P. E. Greene, R. E. Breeze et al., “Transplantation of embryonic dopamine neurons for severe Parkinson's disease,” New England Journal of Medicine, vol. 344, no. 10, pp. 710–719, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. C. W. Olanow, C. G. Goetz, J. H. Kordower et al., “A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease,” Annals of Neurology, vol. 54, no. 3, pp. 403–414, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. O. Lindvall, G. Sawle, H. Widner et al., “Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson's disease,” Annals of Neurology, vol. 35, no. 2, pp. 172–180, 1994. View at Scopus
  7. C. R. Freed, R. E. Breeze, N. L. Rosenberg et al., “Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease,” New England Journal of Medicine, vol. 327, no. 22, pp. 1549–1555, 1992. View at Scopus
  8. J. H. Kordower, T. B. Freeman, B. J. Snow et al., “Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease,” New England Journal of Medicine, vol. 332, no. 17, pp. 1118–1124, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. D. J. Prockop, “Marrow stromal cells as stem cells for nonhematopoietic tissues,” Science, vol. 276, no. 5309, pp. 71–74, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Kuroda, M. Kitada, S. Wakao, and M. Dezawa, “Bone marrow mesenchymal cells: how do they contribute to tissue repair and are they really stem cells?” Archivum Immunologiae et Therapiae Experimentalis, vol. 59, no. 5, pp. 369–378, 2011. View at Publisher · View at Google Scholar · View at PubMed
  11. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Dezawa, “Insights into autotransplantation: the unexpected discovery of specific induction systems in bone marrow stromal cells,” Cellular and Molecular Life Sciences, vol. 63, no. 23, pp. 2764–2772, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. J. Tolar, K. Le Blanc, A. Keating, and B. R. Blazar, “Concise review: hitting the right spot with mesenchymal stromal cells,” Stem Cells, vol. 28, no. 8, pp. 1446–1455, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. M. Körbling and Z. Estrov, “Adult stem cells for tissue repair—a new therapeutic concept?” New England Journal of Medicine, vol. 349, no. 6, pp. 570–582, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. S. Makino, K. Fukuda, S. Miyoshi et al., “Cardiomyocytes can be generated from marrow stromal cells in vitro,” Journal of Clinical Investigation, vol. 103, no. 5, pp. 697–705, 1999. View at Scopus
  16. M. Dezawa, I. Takahashi, M. Esaki, M. Takano, and H. Sawada, “Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells,” European Journal of Neuroscience, vol. 14, no. 11, pp. 1771–1776, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Dezawa, H. Kanno, M. Hoshino et al., “Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation,” Journal of Clinical Investigation, vol. 113, no. 12, pp. 1701–1710, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Dezawa, H. Ishikawa, Y. Itokazu et al., “Developmental biology: bone marrow stromal cells generate muscle cells and repair muscle degeneration,” Science, vol. 309, no. 5732, pp. 314–317, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. S. Oyagi, M. Hirose, M. Kojima et al., “Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats,” Journal of Hepatology, vol. 44, no. 4, pp. 742–748, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. D. A. Grove, J. Xu, R. Joodi et al., “Attenuation of early airway obstruction by mesenchymal stem cells in a murine model of heterotopic tracheal transplantation,” Journal of Heart and Lung Transplantation, vol. 30, pp. 341–350, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. D. G. Phinney and D. J. Prockop, “Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views,” Stem Cells, vol. 25, no. 11, pp. 2896–2902, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. J. L. Spees, S. D. Olson, J. Ylostalo et al., “Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2397–2402, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. F. H. Gage, “Mammalian neural stem cells,” Science, vol. 287, no. 5457, pp. 1433–1438, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. I. L. Weissman and J. A. Shizuru, “The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases,” Blood, vol. 112, no. 9, pp. 3543–3553, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. Y. Kuroda, M. Kitada, S. Wakao et al., “Unique multipotent cells in adult human mesenchymal cell populations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 19, pp. 8639–8643, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. E. Mezey, K. J. Chandross, G. Harta, R. A. Maki, and S. R. McKercher, “Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow,” Science, vol. 290, no. 5497, pp. 1779–1782, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Terada, T. Hamazaki, M. Oka et al., “Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion,” Nature, vol. 416, no. 6880, pp. 542–545, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. M. Alvarez-Dolado, R. Pardal, J. M. Garcia-Verdugo et al., “Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes,” Nature, vol. 425, no. 6961, pp. 968–973, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. R. G. Harris, E. L. Herzog, E. M. Bruscia, J. E. Grove, J. S. Van Arnam, and D. S. Krause, “Lack of a fusion requirement for development of bone marrow-derived epithelia,” Science, vol. 305, no. 5680, pp. 90–93, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. E. J. Schwarz, G. M. Alexander, D. J. Prockop, and S. A. Azizi, “Multipotential marrow stromal cells transduced to produce L-DOPA: engraftment in a rat model of Parkinson disease,” Human Gene Therapy, vol. 10, no. 15, pp. 2539–2549, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. E. J. Schwarz, R. L. Reger, G. M. Alexander, R. Class, S. A. Azizi, and D. J. Prockop, “Rat marrow stromal cells rapidly transduced with a self-inactivating retrovirus synthesize L-DOPA in vitro,” Gene Therapy, vol. 8, no. 16, pp. 1214–1223, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. L. Lu, C. Zhao, Y. Liu et al., “Therapeutic benefit of TH-engineered mesenchymal stem cells for Parkinson's disease,” Brain Research Protocols, vol. 15, no. 1, pp. 46–51, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. S. Zhang, Z. Zou, X. Jiang et al., “The therapeutic effects of tyrosine hydroxylase gene transfected hematopoetic stem cells in a rat model of Parkinson's disease,” Cellular and Molecular Neurobiology, vol. 28, no. 4, pp. 529–543, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. G. Bouchez, L. Sensebé, P. Vourc'h et al., “Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease,” Neurochemistry International, vol. 52, no. 7, pp. 1332–1342, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. N. K. Venkataramana, S. K. V. Kumar, S. Balaraju et al., “Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson's disease,” Translational Research, vol. 155, no. 2, pp. 62–70, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. O. Sadan, M. Bahat-Stromza, Y. Barhum et al., “Protective effects of neurotrophic factor-secreting cells in a 6-OHDA rat model of parkinson disease,” Stem Cells and Development, vol. 18, no. 8, pp. 1179–1190, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. O. Sadan, N. Shemesh, Y. Cohen, E. Melamed, and D. Offen, “Adult neurotrophic factor-secreting stem cells: a potential novel therapy for neurodegenerative diseases,” Israel Medical Association Journal, vol. 11, no. 4, pp. 201–204, 2009. View at Scopus
  38. J. Wu, W. Yu, Y. Chen et al., “Intrastriatal transplantation of GDNF-engineered BMSCs and its neuroprotection in lactacystin-induced parkinsonian rat model,” Neurochemical Research, vol. 35, no. 3, pp. 495–502, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. T. C. Moloney, G. E. Rooney, F. P. Barry, L. Howard, and E. Dowd, “Potential of rat bone marrow-derived mesenchymal stem cells as vehicles for delivery of neurotrophins to the Parkinsonian rat brain,” Brain Research, vol. 1359, no. C, pp. 33–43, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. K. A. Trzaska, E. V. Kuzhikandathil, and P. Rameshwar, “Specification of a dopaminergic phenotype from adult human mesenchymal stem cells,” Stem Cells, vol. 25, no. 11, pp. 2797–2808, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. R. Barzilay, T. Ben-Zur, S. Bulvik, E. Melamed, and D. Offen, “Lentiviral delivery of LMX1a enhances dopaminergic phenotype in differentiated human bone marrow mesenchymal stem cells,” Stem Cells and Development, vol. 18, no. 4, pp. 591–601, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. P. Shetty, G. Ravindran, S. Sarang, A. M. Thakur, H. S. Rao, and C. Viswanathan, “Clinical grade mesenchymal stem cells transdifferentiated under xenofree conditions alleviates motor deficiencies in a rat model of Parkinson's disease,” Cell Biology International, vol. 33, no. 8, pp. 830–838, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. Y. S. Levy, M. Bahat-Stroomza, R. Barzilay et al., “Regenerative effect of neural-induced human mesenchymal stromal cells in rat models of Parkinson's disease,” Cytotherapy, vol. 10, no. 4, pp. 340–352, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. M. L. Khoo, H. Tao, A. C.B. Meedeniya, A. Mackay-Sim, and D. D.F. Ma, “Transplantation of neuronal-primed human bone marrow mesenchymal stem cells in Hemiparkinsonian rodents,” PLoS One, vol. 6, no. 5, Article ID e19025, 2011. View at Publisher · View at Google Scholar · View at PubMed
  45. T. Yasuhara, N. Matsukawa, K. Hara et al., “Notch-induced rat and human bone marrow stromal cell grafts reduce ischemic cell loss and ameliorate behavioral deficits in chronic stroke animals,” Stem Cells and Development, vol. 18, no. 10, pp. 1501–1514, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. M. Hayase, M. Kitada, S. Wakao et al., “Committed neural progenitor cells derived from genetically modified bone marrow stromal cells ameliorate deficits in a rat model of stroke,” Journal of Cerebral Blood Flow and Metabolism, vol. 29, no. 8, pp. 1409–1420, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. T. Mimura, M. Dezawa, H. Kanno, and I. Yamamoto, “Behavioral and histological evaluation of a focal cerebral infarction rat model transplanted with neurons induced from bone marrow stromal cells,” Journal of Neuropathology and Experimental Neurology, vol. 64, no. 12, pp. 1108–1117, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Nagane, M. Kitada, S. Wakao, M. Dezawa, and Y. Tabata, “Practical induction system for dopamine-producing cells from bone marrow stromal cells using spermine-pullulan-mediated reverse transfection method,” Tissue Engineering. Part A, vol. 15, no. 7, pp. 1655–1665, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. J. Lundkvist and U. Lendahl, “Notch and the birth of glial cells,” Trends in Neurosciences, vol. 24, no. 9, pp. 492–494, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. M. K. McCoy, T. N. Martinez, K. A. Ruhn et al., “Autologous transplants of Adipose-Derived Adult Stromal (ADAS) cells afford dopaminergic neuroprotection in a model of Parkinson's disease,” Experimental Neurology, vol. 210, no. 1, pp. 14–29, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. M. L. Weiss, S. Medicetty, A. R. Bledsoe et al., “Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson's disease,” Stem Cells, vol. 24, no. 3, pp. 781–792, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. N. Xiong, X. Cao, Z. Zhang et al., “Long-term efficacy and safety of human umbilical cord mesenchymal stromal cells in rotenone-induced Hemiparkinsonian rats,” Biology of Blood and Marrow Transplantation, vol. 16, no. 11, pp. 1519–1529, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. N. Xiong, Z. Zhang, J. Huang et al., “VEGF-expressing human umbilical cord mesenchymal stem cells, an improved therapy strategy for Parkinson's disease,” Gene Therapy, vol. 18, pp. 394–402, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. Y. S. Fu, Y. C. Cheng, M. Y. A. Lin et al., “Conversion of human umbilical cord mesenchymal stem cells in Wharton's Jelly to dopaminergic neurons in vitro: potential therapeutic application for Parkinsonism,” Stem Cells, vol. 24, no. 1, pp. 115–124, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. M. Li, S. Z. Zhang, Y. W. Guo et al., “Human umbilical vein-derived dopaminergic-like cell transplantation with nerve growth factor ameliorates motor dysfunction in a rat model of parkinson's disease,” Neurochemical Research, vol. 35, no. 10, pp. 1522–1529, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. I. Datta, S. Mishra, L. Mohanty, S. Pulikkot, and P. G. Joshi, “Neuronal plasticity of human Wharton's jelly mesenchymal stromal cells to the dopaminergic cell type compared with human bone marrow mesenchymal stromal cells,” Cytotherapy, vol. 13, no. 8, pp. 918–932, 2011. View at Publisher · View at Google Scholar · View at PubMed
  57. J. Wagner, P. Åkerud, D. S. Castro et al., “Induction of a midbrain dopaminergic phenotype in Nurr1-overexpressing neural stem cells by type 1 astrocytes,” Nature Biotechnology, vol. 17, no. 7, pp. 653–659, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. E. K. I. Andersson, D. K. Irvin, J. Ahlsiö, and M. Parmar, “Ngn2 and Nurr1 act in synergy to induce midbrain dopaminergic neurons from expanded neural stem and progenitor cells,” Experimental Cell Research, vol. 313, no. 6, pp. 1172–1180, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. H. J. Kim, M. Sugimori, M. Nakafuku, and C. N. Svendsen, “Control of neurogenesis and tyrosine hydroxylase expression in neural progenitor cells through bHLH proteins and Nurr1,” Experimental Neurology, vol. 203, no. 2, pp. 394–405, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998.
  61. H. Kawasaki, K. Mizuseki, S. Nishikawa et al., “Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity,” Neuron, vol. 28, no. 1, pp. 31–40, 2000. View at Scopus
  62. S. H. Lee, N. Lumelsky, L. Studer, J. M. Auerbach, and R. D. McKay, “Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells,” Nature Biotechnology, vol. 18, no. 6, pp. 675–679, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. A. L. Perrier, V. Tabar, T. Barberi et al., “Derivation of midbrain dopamine neurons from human embryonic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 34, pp. 12543–12548, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. S. Kriks, J. W. Shim, J. Piao et al., “Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease,” Nature, vol. 480, no. 7378, pp. 547–551, 2011. View at Publisher · View at Google Scholar · View at PubMed
  65. J. H. Kim, J. M. Auerbach, J. A. Rodríguez-Gómez et al., “Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease,” Nature, vol. 418, no. 6893, pp. 50–56, 2002. View at Publisher · View at Google Scholar · View at PubMed
  66. S. Arnhold, H. Klein, I. Semkova, K. Addicks, and U. Schraermeyer, “Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space,” Investigative Ophthalmology and Visual Science, vol. 45, no. 12, pp. 4251–4255, 2004. View at Publisher · View at Google Scholar · View at PubMed
  67. L. M. Bjorklund, R. Sánchez-Pernaute, S. Chung et al., “Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2344–2349, 2002. View at Publisher · View at Google Scholar · View at PubMed
  68. H. Fukuda, J. Takahashi, K. Watanabe et al., “Fluorescence-activated cell sorting-based purification of embryonic stem cell-derived neural precursors averts tumor formation after transplantation,” Stem Cells, vol. 24, no. 3, pp. 763–771, 2006. View at Publisher · View at Google Scholar · View at PubMed
  69. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at PubMed
  70. B. Y. Hu, J. P. Weick, J. Yu et al., “Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 9, pp. 4335–4340, 2010. View at Publisher · View at Google Scholar · View at PubMed
  71. M. Wernig, J. P. Zhao, J. Pruszak et al., “Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 15, pp. 5856–5861, 2008. View at Publisher · View at Google Scholar · View at PubMed
  72. R. E. Gross, R. L. Watts, R. A. Hauser et al., “Intrastriatal transplantation of microcarrier-bound human retinal pigment epithelial cells versus sham surgery in patients with advanced Parkinson's disease: a double-blind, randomised, controlled trial,” The Lancet Neurology, vol. 10, no. 6, pp. 509–519, 2011. View at Publisher · View at Google Scholar
  73. Y. Ramot, M. Steiner, V. Morad et al., “Pulmonary thrombosis in the mouse following intravenous administration of quantum dot-labeled mesenchymal cells,” Nanotoxicology, vol. 4, no. 1, pp. 98–105, 2010. View at Publisher · View at Google Scholar · View at PubMed