Table of Contents
ISRN Stem Cells
Volume 2013, Article ID 947329, 17 pages
http://dx.doi.org/10.1155/2013/947329
Review Article

Translational Research in Stem Cell Treatment of Neuromuscular Diseases

1Department of Radiology, University of Wisconsin, Madison, WI 53792, USA
2Department of Plastic and Reconstructive Surgery, Juntendo University School of Medicine, Tokyo 1138421, Japan

Received 21 August 2012; Accepted 9 September 2012

Academic Editors: A. Chapel and F. Fagioli

Copyright © 2013 Hakan Orbay and Hiroshi Mizuno. 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. O. Paciello and S. Papparella, “Histochemical and immunohistological approach to comparative neuromuscular diseases,” Folia Histochemica et Cytobiologica, vol. 47, no. 2, pp. 143–152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Mazzini, K. Mareschi, I. Ferrero et al., “Autologous mesenchymal stem cells: clinical applications in amyotrophic lateral sclerosis,” Neurological Research, vol. 28, no. 5, pp. 523–526, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. S. MacLean, W. S. Khan, A. A. Malik, S. Anand, and M. Snow, “The potential of stem cells in the treatment of skeletal muscle injury and disease,” Stem Cells International, vol. 2012, Article ID 282348, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Oka, O. Honmou, Y. Akiyama et al., “Autologous transplantation of expanded neural precursor cells into the demyelinated monkey spinal cord,” Brain Research, vol. 1030, no. 1, pp. 94–102, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. F. S. Tedesco et al., “Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy,” Science Translational Medicine, vol. 3, no. 96, p. 96ra78, 2011. View at Publisher · View at Google Scholar
  6. N. P. Hirsch, “Neuromuscular junction in health and disease,” British Journal of Anaesthesia, vol. 99, no. 1, pp. 132–138, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. J. S. Lunn, S. A. Sakowski, J. Hur, and E. L. Feldman, “Stem cell technology for neurodegenerative diseases,” Annals of Neurology, vol. 70, no. 3, pp. 353–361, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Hanley, G. Rastegarlari, and A. C. Nathwani, “An introduction to induced pluripotent stem cells,” British Journal of Haematology, vol. 151, no. 1, pp. 16–24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. H. J. Cho, C. S. Lee, Y. W. Kwon et al., “Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation,” Blood, vol. 116, no. 3, pp. 386–395, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Yakubov, G. Rechavi, S. Rozenblatt, and D. Givol, “Reprogramming of human fibroblasts to pluripotent stem cells using mRNA of four transcription factors,” Biochemical and Biophysical Research Communications, vol. 394, no. 1, pp. 189–193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. R. L. Judson, J. E. Babiarz, M. Venere, and R. Blelloch, “Embryonic stem cell-specific microRNAs promote induced pluripotency,” Nature Biotechnology, vol. 27, no. 5, pp. 459–461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J. R. Thonhoff, L. Ojeda, and P. Wu, “Stem cell-derived motor neurons: applications and challenges in amyotrophic lateral sclerosis,” Current Stem Cell Research and Therapy, vol. 4, no. 3, pp. 178–199, 2009. View at Google Scholar · View at Scopus
  14. L. Mazzini, F. Fagioli, R. Boccaletti et al., “Stem cell therapy in amyotrophic lateral sclerosis: a methodological approach in humans,” Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, vol. 4, no. 3, pp. 158–161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Mazzini, K. Mareschi, I. Ferrero et al., “Stem cell treatment in Amyotrophic Lateral Sclerosis,” Journal of the Neurological Sciences, vol. 265, no. 1-2, pp. 78–83, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Mazzini, I. Ferrero, V. Luparello et al., “Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a phase I clinical trial,” Experimental Neurology, vol. 223, no. 1, pp. 229–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Mazzini, K. Mareschi, I. Ferrero et al., “Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study,” Cytotherapy, vol. 14, no. 1, pp. 56–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Nefussy, I. Artamonov, V. Deutsch, E. Naparstek, A. Nagler, and V. E. Drory, “Recombinant human granulocyte-colony stimulating factor administration for treating amyotrophic lateral sclerosis: a pilot study,” Amyotrophic Lateral Sclerosis, vol. 11, no. 1-2, pp. 187–193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Cashman, L. Y. Tan, C. Krieger et al., “Pilot study of granulocyte colony stimulating factor (G-CSF)-mobilized peripheral blood stem cells in amyotrophic lateral sclerosis (ALS),” Muscle and Nerve, vol. 37, no. 5, pp. 620–625, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Tarella, S. Rutella, F. Gualandi et al., “Consistent bone marrow-derived cell mobilization following repeated short courses of granulocytecolony-stimulating factor in patients with amyotrophic lateral sclerosis: results from a multicenter prospective trial,” Cytotherapy, vol. 12, no. 1, pp. 50–59, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Slavin, B. G. S. Kurkalli, and D. Karussis, “The potential use of adult stem cells for the treatment of multiple sclerosis and other neurodegenerative disorders,” Clinical Neurology and Neurosurgery, vol. 110, no. 9, pp. 943–946, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Bonilla, P. Alarcón, R. Villaverde, P. Aparicio, A. Silva, and S. Martínez, “Haematopoietic progenitor cells from adult bone marrow differentiate into cells that express oligodendroglial antigens in the neonatal mouse brain,” European Journal of Neuroscience, vol. 15, no. 3, pp. 575–582, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Pluchino, A. Gritti, E. Blezer et al., “Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates,” Annals of Neurology, vol. 66, no. 3, pp. 343–354, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Czepiel, V. Balasubramaniyan, W. Schaafsma et al., “Differentiation of induced pluripotent stem cells into functional oligodendrocytes,” Glia, vol. 59, no. 6, pp. 882–892, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. K. P. Reekmans, J. Praet, N. de Vocht et al., “Clinical potential of intravenous neural stem cell delivery for treatment of neuroinflammatory disease in mice?” Cell Transplantation, vol. 20, no. 6, pp. 851–869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Yamout, R. Hourani, H. Salti et al., “Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study,” Journal of Neuroimmunology, vol. 227, no. 1-2, pp. 185–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. K. Burt, Y. Loh, B. Cohen et al., “Autologous non-myeloablative haemopoietic stem cell transplantation in relapsing-remitting multiple sclerosis: a phase I/II study,” The Lancet Neurology, vol. 8, no. 3, pp. 244–253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Saccardi, T. Kozak, C. Bocelli-Tyndall et al., “Autologous stem cell transplantation for progressive multiple sclerosis: update of the European Group for Blood and Marrow Transplantation autoimmune diseases working party database,” Multiple Sclerosis, vol. 12, no. 6, pp. 814–823, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. R. A. Nash, R. Dansey, J. Storek et al., “Epstein-Barr virus-associated posttransplantation lymphoproliferative disorder after high-dose immunosuppressive therapy and autologous CD34-selected hematopoietic stem cell transplantation for severe autoimmune diseases,” Biology of Blood and Marrow Transplantation, vol. 9, no. 9, pp. 583–591, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. J.-T. Vilquin, C. Catelain, and K. Vauchez, “Cell therapy for muscular dystrophies: advances and challenges,” Current Opinion in Organ Transplantation, vol. 16, no. 6, pp. 640–649, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Vauchez, J. P. Marolleau, M. Schmid et al., “Aldehyde dehydrogenase activity identifies a population of human skeletal muscle cells with high myogenic capacities,” Molecular Therapy, vol. 17, no. 11, pp. 1948–1958, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Ferrari, G. Cusella-De Angelis, M. Coletta et al., “Muscle regeneration by bone marrow-derived myogenic progenitors,” Science, vol. 279, no. 5356, pp. 1528–1530, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. J. F. Lafreniere, M. C. Caron, D. Skuk, M. Goulet, A. R. Cheikh, and J. P. Tremblay, “Growth factor coinjection improves the migration potential of monkey myogenic precursors without affecting cell transplantation success,” Cell Transplantation, vol. 18, no. 7, pp. 719–730, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. S.-W. Feng, F. Chen, J. Cao et al., “Restoration of muscle fibers and satellite cells after isogenic MSC transplantation with microdystrophin gene delivery,” Biochemical and Biophysical Research Communications, vol. 419, no. 1, pp. 1–6, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Xiong, Y. Xu, H. Zheng et al., “Microdystrophin delivery in dystrophin-deficient (mdx) mice by genetically-corrected syngeneic MSCs transplantation,” Transplantation Proceedings, vol. 42, no. 7, pp. 2731–2739, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Ikezawa, B. Cao, Z. Qu et al., “Dystrophin delivery in dystrophin-deficient DMDmdx skeletal muscle by isogenic muscle-derived stem cell transplantation,” Human Gene Therapy, vol. 14, no. 16, pp. 1535–1546, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Bachrach, S. Li, A. L. Perez et al., “Systemic delivery of human microdystrophin to regenerating mouse dystrophic muscle by muscle progenitor cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 10, pp. 3581–3586, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Boldrin, P. S. Zammit, F. Muntoni, and J. E. Morgan, “Mature adult dystrophic mouse muscle environment does not impede efficient engrafted satellite cell regeneration and self-renewal,” Stem Cells, vol. 27, no. 10, pp. 2478–2487, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. E. J. Gang, R. Darabi, D. Bosnakovski et al., “Engraftment of mesenchymal stem cells into dystrophin-deficient mice is not accompanied by functional recovery,” Experimental Cell Research, vol. 315, no. 15, pp. 2624–2636, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. C. S. Kuhr, M. Lupu, and R. Storb, “Hematopoietic cell transplantation directly into dystrophic muscle fails to reconstitute satellite cells and myofibers,” Biology of Blood and Marrow Transplantation, vol. 13, no. 8, pp. 886–888, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. A. M. Neumeyer, D. Cros, D. McKenna-Yasek et al., “Pilot study of myoblast transfer in the treatment of Becker muscular dystrophy,” Neurology, vol. 51, no. 2, pp. 589–592, 1998. View at Google Scholar · View at Scopus
  42. D. Skuk, M. Goulet, B. Roy et al., “Dystrophin expression in muscles of Duchenne muscular dystrophy patients after high-density injections of normal myogenic cells,” Journal of Neuropathology and Experimental Neurology, vol. 65, no. 4, pp. 371–386, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Zhang et al., “Therapy of Duchenne muscular dystrophy with umbilical cord blood stem cell transplantation,” Zhonghua Yi Xue Yi Chuan Xue Za Zhi, vol. 22, no. 4, pp. 399–405, 2005. View at Google Scholar
  44. J. Yu, C. Zheng, X. Ren et al., “Intravenous administration of bone marrow mesenchymal stem cells benefits experimental autoimmune myasthenia gravis mice through an immunomodulatory action,” Scandinavian Journal of Immunology, vol. 72, no. 3, pp. 242–249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. Z. Guo, C. Zheng, Z. Chen et al., “Fetal BM-derived mesenchymal stem cells promote the expansion of human Th17 cells, but inhibit the production of Th1 cells,” European Journal of Immunology, vol. 39, no. 10, pp. 2840–2849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. J. X. Yu et al., “Umbilical cord mesenchymal stem cell transplantation for treatment of experimental autoimmune myasthenia gravis in rats,” Zhongguo Shi Yan Xue Ye Xue Za Zhi, vol. 19, no. 3, pp. 744–748, 2011. View at Google Scholar
  47. J. R. Sheng, T. Muthusamy, B. S. Prabhakar, and M. N. Meriggioli, “GM-CSF-induced regulatory T cells selectively inhibit anti-acetylcholine receptor-specific immune responses in experimental myasthenia gravis,” Journal of Neuroimmunology, vol. 240, pp. 65–73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. N. Solomon, C. A. B. Lewis, B. Ajami, S. Y. Corbel, F. M. V. Rossi, and C. Krieger, “Origin and distribution of bone marrow-derived cells in the central nervous system in a mouse model of amyotrophic lateral sclerosis,” Glia, vol. 53, no. 7, pp. 744–753, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Corti, F. Locatelli, C. Donadoni et al., “Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues,” Brain, vol. 127, no. 11, pp. 2518–2532, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Ohnishi, H. Ito, Y. Suzuki et al., “Intra-bone marrow-bone marrow transplantation slows disease progression and prolongs survival in G93A mutant SOD1 transgenic mice, an animal model mouse for amyotrophic lateral sclerosis,” Brain Research, vol. 1296, pp. 216–224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Corti, M. Nizzardo, M. Nardini et al., “Systemic transplantation of c-kit+ cells exerts a therapeutic effect in a model of amyotrophic lateral sclerosis,” Human Molecular Genetics, vol. 19, no. 19, Article ID ddq293, pp. 3782–3796, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Morita, Y. Watanabe, M. Ishimoto et al., “A novel cell transplantation protocol and its application to an ALS mouse model,” Experimental Neurology, vol. 213, no. 2, pp. 431–438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Boucherie, S. Schäfer, P. Lavand'homme, J. M. Maloteaux, and E. Hermans, “Chimerization of astroglial population in the lumbar spinal cord after mesenchymal stem cell transplantation prolongs survival in a rat model of amyotrophic lateral sclerosis,” Journal of Neuroscience Research, vol. 87, no. 9, pp. 2034–2046, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Forostyak, P. Jendelova, M. Kapcalova, D. Arboleda, and E. Sykova, “Mesenchymal stromal cells prolong the lifespan in a rat model of amyotrophic lateral sclerosis,” Cytotherapy, vol. 13, no. 9, pp. 1036–1046, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Kim, H. Y. Kim, M. R. Choi et al., “Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice,” Neuroscience Letters, vol. 468, no. 3, pp. 190–194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. C. P. Zhao, C. Zhang, S. N. Zhou et al., “Human mesenchymal stromal cells ameliorate the phenotype of SOD1-G93A ALS mice,” Cytotherapy, vol. 9, no. 5, pp. 414–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. H. J. Habisch, M. Janowski, D. Binder et al., “Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects,” Journal of Neural Transmission, vol. 114, no. 11, pp. 1395–1406, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Vercelli, O. M. Mereuta, D. Garbossa et al., “Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis,” Neurobiology of Disease, vol. 31, no. 3, pp. 395–405, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Suzuki, J. McHugh, C. Tork et al., “Direct muscle delivery of GDNF with human mesenchymal stem cells improves motor neuron survival and function in a rat model of familial ALS,” Molecular Therapy, vol. 16, no. 12, pp. 2002–2010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Ende, F. Weinstein, R. Chen, and M. Ende, “Human umbilical cord blood effect on sod mice (amyotrophic lateral sclerosis),” Life Sciences, vol. 67, no. 1, pp. 53–59, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Chen and N. Ende, “The potential for the use of mononuclear cells from human umbilical cord blood in the treatment of amyotrophic lateral sclerosis in SOD1 mice,” Journal of Medicine, vol. 31, no. 1-2, pp. 21–30, 2000. View at Google Scholar · View at Scopus
  62. S. Garbuzova-Davis, A. E. Willing, T. Zigova et al., “Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: distribution, migration, and differentiation,” Journal of Hematotherapy and Stem Cell Research, vol. 12, no. 3, pp. 255–270, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Garbuzova-Davis, C. D. Sanberg, N. Kuzmin-Nichols et al., “Human umbilical cord blood treatment in a mouse model of ALS: Optimization of cell dose,” PLoS One, vol. 3, no. 6, Article ID e2494, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. A. A. Rizvanov, A. P. Kiyasov, I. M. Gaziziov et al., “Human umbilical cord blood cells transfected with VEGF and L1CAM do not differentiate into neurons but transform into vascular endothelial cells and secrete neuro-trophic factors to support neuro-genesis-a novel approach in stem cell therapy,” Neurochemistry International, vol. 53, no. 6-8, pp. 389–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Bigini, P. Veglianese, G. Andriolo et al., “Intracerebroventricular administration of human umbilical cord blood cells delays disease progression in two murine models of motor neuron degeneration,” Rejuvenation Research, vol. 14, no. 6, pp. 623–639, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. A. A. Rizvanov, D. S. Guseva, I. I. Salafutdinov et al., “Genetically modified human umbilical cord blood cells expressing vascular endothelial growth factor and fibroblast growth factor 2 differentiate into glial cells after transplantation into amyotrophic lateral sclerosis transgenic mice,” Experimental Biology and Medicine, vol. 236, no. 1, pp. 91–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. S. M. Klein, S. Behrstock, J. Mchugh et al., “GDNF delivery using human neural progenitor cells in a rat model of ALS,” Human Gene Therapy, vol. 16, no. 4, pp. 509–521, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Suzuki, J. McHugh, C. Tork et al., “GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS,” PLoS One, vol. 2, no. 1, article e689, 2007. View at Google Scholar · View at Scopus
  69. L. Xu, P. Shen, T. Hazel, K. Johe, and V. E. Koliatsos, “Dual transplantation of human neural stem cells into cervical and lumbar cord ameliorates motor neuron disease in SOD1 transgenic rats,” Neuroscience Letters, vol. 494, no. 3, pp. 222–226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Yan, L. Xu, A. M. Welsh et al., “Combined immunosuppressive agents or CD4 antibodies prolong survival of human neural stem cell grafts and improve disease outcomes in amyotrophic lateral sclerosis transgenic mice,” Stem Cells, vol. 24, no. 8, pp. 1976–1985, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. D. H. Hwang, H. J. Lee, I. H. Park et al., “Intrathecal transplantation of human neural stem cells overexpressing VEGF provide behavioral improvement, disease onset delay and survival extension in transgenic ALS mice,” Gene Therapy, vol. 16, no. 10, pp. 1234–1244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. N. Souayah, K. M. Coakley, R. Chen, N. Ende, and J. J. McArdle, “Defective neuromuscular transmission in the SOD1G93A transgenic mouse improves after administration of human umbilical cord blood cells,” Stem Cell Reviews and Reports, pp. 224–228, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Corti, F. Locatelli, D. Papadimitriou et al., “Neural stem cells LewisX + CXCR4 + modify disease progression in an amyotrophic lateral sclerosis model,” Brain, vol. 130, no. 5, pp. 1289–1305, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Mitrečić, C. Nicaise, S. Gajović, and R. Pochet, “Distribution, differentiation, and survival of intravenously administered neural stem cells in a rat model of amyotrophic lateral sclerosis,” Cell Transplantation, vol. 19, no. 5, pp. 537–548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. L. J. Martin and Z. Liu, “Adult olfactory bulb neural precursor cell grafts provide temporary protection from motor neuron degeneration, improve motor function, and extend survival in amyotrophic lateral sclerosis mice,” Journal of Neuropathology and Experimental Neurology, vol. 66, no. 11, pp. 1002–1018, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. R. López-González, P. Kunckles, and I. Velasco, “Transient recovery in a rat model of familial amyotrophic lateral sclerosis after transplantation of motor neurons derived from mouse embryonic stem cells,” Cell Transplantation, vol. 18, no. 10-11, pp. 1171–1181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. A. C. Lepore, J. O'Donnell, A. S. Kim et al., “Human Glial-restricted progenitor transplantation into cervical spinal cord of the SOD1G93A mouse model of ALS,” PLoS One, vol. 6, no. 10, Article ID 25968, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Deda, M. C. Inci, A. E. Kürekçi et al., “Treatment of amyotrophic lateral sclerosis patients by autologous bone marrow-derived hematopoietic stem cell transplantation: a 1-year follow-up,” Cytotherapy, vol. 11, no. 1, pp. 18–25, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. H. R. Martinez, M. T. Gonzalez-Garza, J. E. Moreno-Cuevas, E. Caro, E. Gutierrez-Jimenez, and J. J. Segura, “Stem-cell transplantation into the frontal motor cortex in amyotrophic lateral sclerosis patients,” Cytotherapy, vol. 11, no. 1, pp. 26–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Blanquer, P. M. A. Espejo, F. Iniesta et al., “Bone marrow stem cell transplantation in amyotrophic lateral sclerosis: technical aspects and preliminary results from a clinical trial,” Methods Find Exp Clin Pharmacol, vol. 32, supplement A, pp. 31–37, 2010. View at Google Scholar
  81. D. Karussis, C. Karageorgiou, A. Vaknin-Dembinsky et al., “Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis,” Archives of Neurology, vol. 67, no. 10, pp. 1187–1194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Ben-Hur, O. Einstein, R. Mizrachi-Kol et al., “Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis,” Glia, vol. 41, no. 1, pp. 73–80, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Pluchino, A. Quattrini, E. Brambilla et al., “Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis,” Nature, vol. 422, no. 6933, pp. 688–694, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. O. Einstein, Y. Friedman-Levi, N. Grigoriadis, and T. Ben-Hur, “Transplanted neural precursors enhance host brain-derived myelin regeneration,” Journal of Neuroscience, vol. 29, no. 50, pp. 15694–15702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. O. Einstein, N. Fainstein, I. Vaknin et al., “Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression,” Annals of Neurology, vol. 61, no. 3, pp. 209–218, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. L. S. Politi, M. Bacigaluppi, E. Brambilla et al., “Magnetic resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis,” Stem Cells, vol. 25, no. 10, pp. 2583–2592, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Giannakopoulou, N. Grigoriadis, E. Polyzoidoua, O. Touloumi, E. Michaloudi, and G. C. Papadopoulos, “Inflammatory changes induced by transplanted neural precursor cells in a multiple sclerosis model,” NeuroReport, vol. 22, no. 2, pp. 68–72, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. N. Muja, M. E. Cohen, J. Zhang et al., “Neural precursors exhibit distinctly different patterns of cell migration upon transplantation during either the acute or chronic phase of EAE: a serial MR imaging study,” Magnetic Resonance in Medicine, vol. 65, no. 6, pp. 1738–1749, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. M. O. Totoiu, G. I. Nistor, T. E. Lane, and H. S. Keirstead, “Remyelination, axonal sparing, and locomotor recovery following transplantation of glial-committed progenitor cells into the MHV model of multiple sclerosis,” Experimental Neurology, vol. 187, no. 2, pp. 254–265, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. J. L. Hardison, G. Nistor, R. Gonzalez, H. S. Keirstead, and T. E. Lane, “Transplantation of glial-committed progenitor cells into a viral model of multiple sclerosis induces remyelination in the absence of an attenuated inflammatory response,” Experimental Neurology, vol. 197, no. 2, pp. 420–429, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Aharonowiz, O. Einstein, N. Fainstein, H. Lassmann, B. Reubinoff, and T. Ben-Hur, “Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis,” PLoS One, vol. 3, no. 9, Article ID e3145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. B. Xu, P. Haviernik, L. A. Wolfraim, K. D. Bunting, and D. W. Scott, “Bone marrow transplantation combined with gene therapy to induce antigen-specific tolerance and ameliorate EAE,” Molecular Therapy, vol. 13, no. 1, pp. 42–48, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Cassiani-Ingoni, P. A. Muraro, T. Magnus et al., “Disease progression after bone marrow transplantation in a model of multiple sclerosis is associated with chronic microglial and glial progenitor response,” Journal of Neuropathology and Experimental Neurology, vol. 66, no. 7, pp. 637–649, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. B. Van Wijmeersch, B. Sprangers, O. Rutgeerts et al., “Allogeneic bone marrow transplantation in models of experimental autoimmune encephalomyelitis: evidence for a graft-versus-autoimmunity effect,” Biology of Blood and Marrow Transplantation, vol. 13, no. 6, pp. 627–637, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Croitoru-Lamoury, K. R. Williams, F. M. J. Lamoury et al., “Neural transplantation of human MSC and NT2 cells in the twitcher mouse model,” Cytotherapy, vol. 8, no. 5, pp. 445–458, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. K. S. Carbajal, C. Schaumburg, R. Strieter, J. Kane, and T. E. Lane, “Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viral model of multiple sclerosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 24, pp. 11068–11073, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Yang, Y. Yan, B. Ciric et al., “Evaluation of bone marrow- and brain-derived neural stem cells in therapy of central nervous system autoimmunity,” American Journal of Pathology, vol. 177, no. 4, pp. 1989–2001, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. D. Gordon, G. Pavlovska, J. B. Uney, D. C. Wraith, and N. J. Scolding, “Human mesenchymal stem cells infiltrate the spinal cord, reduce demyelination, and localize to white matter lesions in experimental autoimmune encephalomyelitis,” Journal of Neuropathology and Experimental Neurology, vol. 69, no. 11, pp. 1087–1095, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. C. Lanza, S. Morando, A. Voci et al., “Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo,” Journal of Neurochemistry, vol. 110, no. 5, pp. 1674–1684, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Rafei, E. Birman, K. Forner, and J. Galipeau, “Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis,” Molecular Therapy, vol. 17, no. 10, pp. 1799–1803, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Matysiak, M. Stasiołek, W. Orłowski et al., “Stem cells ameliorate EAE via an indoleamine 2,3-dioxygenase (IDO) mechanism,” Journal of Neuroimmunology, vol. 193, no. 1-2, pp. 12–23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. N. Grigoriadis, A. Lourbopoulos, R. Lagoudaki et al., “Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis,” Experimental Neurology, vol. 230, no. 1, pp. 78–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. L. Bai, D. P. Lennon, V. Eaton et al., “Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis,” Glia, vol. 57, no. 11, pp. 1192–1203, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Barhum, S. Gai-Castro, M. Bahat-Stromza, R. Barzilay, E. Melamed, and D. Offen, “Intracerebroventricular transplantation of human mesenchymal stem cells induced to secrete neurotrophic factors attenuates clinical symptoms in a mouse model of multiple sclerosis,” Journal of Molecular Neuroscience, vol. 41, no. 1, pp. 129–137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. K. Takahashi, M. Prinz, M. Stagi, O. Chechneva, and H. Neumann, “TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis,” PLoS Medicine, vol. 4, no. 4, article e124, pp. 675–689, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. T. K. Makar, D. Trisler, C. T. Bever et al., “Stem cell based delivery of IFN-β reduces relapses in experimental autoimmune encephalomyelitis,” Journal of Neuroimmunology, vol. 196, no. 1-2, pp. 67–81, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. T. K. Makar, C. T. Bever, I. S. Singh et al., “Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle,” Journal of Neuroimmunology, vol. 210, no. 1-2, pp. 40–51, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. G. Constantin, S. Marconi, B. Rossi et al., “Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis,” Stem Cells, vol. 27, no. 10, pp. 2624–2635, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Woodhoo, V. Sahni, J. Gilson et al., “Schwann cell precursors: a favourable cell for myelin repair in the Central Nervous System,” Brain, vol. 130, no. 8, pp. 2175–2185, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Cristofanilli, V. K. Harris, A. Zigelbaum et al., “Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice,” Stem Cells and Development, vol. 20, no. 12, pp. 2065–2076, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. Y. Wang, J. H. Piao, E. C. Larsen, Y. Kondo, and I. D. Duncan, “Migration and remyelination by oligodendrocyte progenitor cells transplanted adjacent to focal areas of spinal cord inflammation,” Journal of Neuroscience Research, vol. 89, no. 11, pp. 1737–1746, 2011. View at Publisher · View at Google Scholar · View at Scopus
  112. G. L. Mancardi, R. Saccardi, M. Filippi et al., “Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS,” Neurology, vol. 57, no. 1, pp. 62–68, 2001. View at Google Scholar · View at Scopus
  113. V. A. Rossiev, S. V. Makarov, I. Y. Alexandrova et al., “Experience with high-dose immunosuppressive therapy followed by transplantation of autologous stem hemopoietic cells in patients with multiple sclerosis,” Terapevticheskii Arkhiv, vol. 74, no. 7, pp. 35–38, 2002. View at Google Scholar · View at Scopus
  114. A. S. Fassas, J. R. Passweg, A. Anagnostopoulos et al., “Hematopoietic stem cell transplantation for multiple sclerosis: a retrospective multicenter study,” Journal of Neurology, vol. 249, no. 8, pp. 1088–1097, 2002. View at Publisher · View at Google Scholar · View at Scopus
  115. E. Carreras, A. Saiz, P. Marín et al., “CD34+ selected autologous peripheral blood stem cell transplantation for multiple sclerosis: report of toxicity and treatment results at one year of follow-up in 15 patients,” Haematologica, vol. 88, no. 3, pp. 306–314, 2003. View at Google Scholar · View at Scopus
  116. R. A. Nash, J. D. Bowen, P. A. McSweeney et al., “High-dose immunosuppressive therapy and autologous peripheral blood stem cell transplantation for severe multiple sclerosis,” Blood, vol. 102, no. 7, pp. 2364–2372, 2003. View at Publisher · View at Google Scholar · View at Scopus
  117. R. Saccardi, G. L. Mancardi, A. Solari et al., “Autologous HSCT for severe progressive multiple sclerosis in a multicenter trial: impact on disease activity and quality of life,” Blood, vol. 105, no. 6, pp. 2601–2607, 2005. View at Publisher · View at Google Scholar · View at Scopus
  118. P. A. Muraro, D. C. Douek, A. Packer et al., “Thymic output generates a new and diverse TCR repertoire after autologous stem cell transplantation in multiple sclerosis patients,” Journal of Experimental Medicine, vol. 201, no. 5, pp. 805–816, 2005. View at Publisher · View at Google Scholar · View at Scopus
  119. Y. Blanco, A. Saiz, M. Costa et al., “Evolution of brain-derived neurotrophic factor levels after autologous hematopietic stem cell transplantation in multiple sclerosis,” Neuroscience Letters, vol. 380, no. 1-2, pp. 122–126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  120. M. M. Bonab, S. Yazdanbakhsh, J. Lotfi et al., “Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study,” Iranian Journal of Immunology, vol. 4, no. 1, pp. 50–57, 2007. View at Google Scholar · View at Scopus
  121. J. Xu, B. X. Ji, L. Su et al., “Clinical outcome of autologous peripheral blood stem cell transplantation in opticospinal and conventional forms of secondary progressive multiple sclerosis in a Chinese population,” Annals of Hematology, vol. 90, no. 3, pp. 343–348, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. M. Mohajeri, A. Farazmand, M. M. Bonab, B. Nikbin, and A. Minagar, “FOXP3 gene expression in multiple sclerosis patients pre- and post mesenchymal stem cell therapy,” Iranian Journal of Allergy, Asthma and Immunology, vol. 10, no. 3, pp. 155–161, 2011. View at Google Scholar
  123. M. M. Odinak, G. N. Bisaga, and A. V. Novitskii, “Transplantation of mesenchymal stem cells in multiple sclerosis,” Zhurnal Nevrologii I Psikhiatrii Imeni S.S. Korsakova, vol. 111, no. 2 part 2, pp. 72–76, 2011. View at Google Scholar
  124. P. Connick, M. Kolappan, C. Crawley et al., “Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study,” The Lancet Neurology, vol. 11, no. 2, pp. 150–156, 2012. View at Publisher · View at Google Scholar · View at Scopus
  125. S. Walsh et al., “Myogenic reprogramming of bone marrow derived cells in a W41Dmdmdx deficient mouse model,” PLoS One, vol. 6, no. 11, Article ID e27500, 2011. View at Publisher · View at Google Scholar
  126. Z. Li, H. Y. Liu, Q. F. Lei, C. Zhang, and S. N. Li, “Improved motor function in dko mice by intravenous transplantation of bone marrow-derived mesenchymal stromal cells,” Cytotherapy, vol. 13, no. 1, pp. 69–77, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. S. W. Feng, X. L. Lu, Z. S. Liu et al., “Dynamic distribution of bone marrow-derived mesenchymal stromal cells and change of pathology after infusing into mdx mice,” Cytotherapy, vol. 10, no. 3, pp. 254–264, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. C. Zhang, Y. Zhang, S. Feng, and X. Yao, “BM stem cell transplantation rescues pathophysiologic features of aged dystrophic mdx muscle,” Cytotherapy, vol. 9, no. 1, pp. 44–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  129. C. Dell'Agnola, Z. Wang, R. Storb et al., “Hematopoietic stem cell transplantation does not restore dystrophin expression in Duchenne muscular dystrophy dogs,” Blood, vol. 104, no. 13, pp. 4311–4318, 2004. View at Publisher · View at Google Scholar · View at Scopus
  130. Y. Torrente, M. Belicchi, M. Sampaolesi et al., “Human circulating AC133+ stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle,” Journal of Clinical Investigation, vol. 114, no. 2, pp. 182–195, 2004. View at Publisher · View at Google Scholar · View at Scopus
  131. A. S. de la Garza-Rodea, I. van der Velde, H. Boersma et al., “Long-term contribution of human bone marrow mesenchymal stromal cells to skeletal muscle regeneration in mice,” Cell Transplantation, vol. 20, no. 2, pp. 217–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. 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 Scopus
  133. J. Y. Lee, Z. Qu-Petersen, B. Cao et al., “Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing,” Journal of Cell Biology, vol. 150, no. 5, pp. 1085–1100, 2000. View at Publisher · View at Google Scholar · View at Scopus
  134. Y. Torrente, J. P. Tremblay, F. Pisati et al., “Intraarterial injection of muscle-derived CD34+Sca-1+ stem cells restores dystrophin in mdx mice,” Journal of Cell Biology, vol. 152, no. 2, pp. 335–348, 2001. View at Publisher · View at Google Scholar · View at Scopus
  135. G. M. Mueller, T. O'Day, J. F. Watchko, and M. Ontell, “Effect of injecting primary myoblasts versus putative muscle-derived stem cells on mass and force generation in mdx mice,” Human Gene Therapy, vol. 13, no. 9, pp. 1081–1090, 2002. View at Publisher · View at Google Scholar · View at Scopus
  136. K. Rouger, T. Larcher, L. Dubreil et al., “Systemic delivery of allogenic muscle stem cells induces long-term muscle repair and clinical efficacy in duchenne muscular dystrophy dogs,” American Journal of Pathology, vol. 179, no. 5, pp. 2501–2518, 2011. View at Publisher · View at Google Scholar · View at Scopus
  137. S. M. Chirieleison, J. M. Feduska, R. C. Schugar, Y. Askew, and B. M. Deasy, “Human muscle-derived cell populations isolated by differential adhesion rates: phenotype and contribution to skeletal muscle regeneration in mdx/SCID mice,” Tissue Engineering. Part A, vol. 18, no. 3-4, pp. 232–241, 2012. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Meng, C. F. Adkin, S. W. Xu, F. Muntoni, and J. E. Morgan, “Contribution of human muscle-derived cells to skeletal muscle regeneration in dystrophic host mice,” PLoS One, vol. 6, no. 3, Article ID e17454, 2011. View at Publisher · View at Google Scholar · View at Scopus
  139. S. E. Berry, J. Liu, E. J. Chaney, and S. J. Kaufman, “Multipotential mesoangioblast stem cell therapy in the mdx/utrn-/- mouse model for Duchenne muscular dystrophy,” Regenerative Medicine, vol. 2, no. 3, pp. 275–288, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. C. Sciorati, B. G. Galvez, S. Brunelli et al., “Ex vivo treatment with nitric oxide increases mesoangioblast therapeutic efficacy in muscular dystrophy,” Journal of Cell Science, vol. 119, no. 24, pp. 5114–5123, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. B. G. Galvez, M. Sampaolesi, S. Brunelli et al., “Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability,” Journal of Cell Biology, vol. 174, no. 2, pp. 231–243, 2006. View at Publisher · View at Google Scholar · View at Scopus
  142. M. Sampaolesi, Y. Torrente, A. Innocenzi et al., “Cell therapy of α-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts,” Science, vol. 301, no. 5632, pp. 487–492, 2003. View at Publisher · View at Google Scholar · View at Scopus
  143. M. Sampaolesi, S. Blot, G. D'Antona et al., “Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs,” Nature, vol. 444, no. 7119, pp. 574–579, 2006. View at Publisher · View at Google Scholar · View at Scopus
  144. A. J. Beck, J. M. Vitale, Q. Zhao et al., “Differential requirement for utrophin in the induced pluripotent stem cell correction of muscle versus fat in muscular dystrophy mice,” PLoS One, vol. 6, no. 5, Article ID e20065, 2011. View at Publisher · View at Google Scholar · View at Scopus
  145. R. Darabi, W. Pan, D. Bosnakovski, J. Baik, M. Kyba, and R. C. R. Perlingeiro, “Functional myogenic engraftment from mouse iPS cells,” Stem Cell Reviews and Reports, pp. 948–957, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. Y. Mizuno, H. Chang, K. Umeda et al., “Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells,” FASEB Journal, vol. 24, no. 7, pp. 2245–2253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  147. Y. W. Eom, J. E. Lee, M. S. Yang et al., “Effective myotube formation in human adipose tissue-derived stem cells expressing dystrophin and myosin heavy chain by cellular fusion with mouse C2C12 myoblasts,” Biochemical and Biophysical Research Communications, vol. 408, no. 1, pp. 167–173, 2011. View at Publisher · View at Google Scholar · View at Scopus
  148. N. M. Vieira, E. Zucconi, C. R. Bueno et al., “Human multipotent mesenchymal stromal cells from distinct sources show different in vivo potential to differentiate into muscle cells when injected in dystrophic mice,” Stem Cell Reviews and Reports, vol. 6, no. 4, pp. 560–566, 2010. View at Publisher · View at Google Scholar · View at Scopus
  149. S. Goudenege, D. F. Pisani, B. Wdziekonski et al., “Enhancement of myogenic and muscle repair capacities of human adipose-derived stem cells with forced expression of MyoD,” Molecular Therapy, vol. 17, no. 6, pp. 1064–1072, 2009. View at Publisher · View at Google Scholar · View at Scopus
  150. N. M. Vieira, C. R. Bueno, V. Brandalise et al., “SJL dystrophic mice express a significant amount of human muscle proteins following systemic delivery of human adipose-derived stromal cells without immunosuppression,” Stem Cells, vol. 26, no. 9, pp. 2391–2398, 2008. View at Publisher · View at Google Scholar · View at Scopus
  151. Y. Liu, X. Yan, Z. Sun et al., “Flk-1+ adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx Mice,” Stem Cells and Development, vol. 16, no. 5, pp. 695–706, 2007. View at Publisher · View at Google Scholar · View at Scopus
  152. A. M. Rodriguez, D. Pisani, C. A. Dechesne et al., “Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse,” Journal of Experimental Medicine, vol. 201, no. 9, pp. 1397–1405, 2005. View at Publisher · View at Google Scholar · View at Scopus
  153. K. L. Pellegrini and M. W. Beilharz, “The survival of myoblasts after intramuscular transplantation is improved when fewer cells are injected,” Transplantation, vol. 91, no. 5, pp. 522–526, 2011. View at Publisher · View at Google Scholar · View at Scopus
  154. J. Rousseau, N. Dumont, C. Lebel et al., “Dystrophin expression following the transplantation of normal muscle precursor cells protects mdx muscle from contraction-induced damage,” Cell Transplantation, vol. 19, no. 5, pp. 589–596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  155. S. Carnio, E. Serena, C. A. Rossi, P. De Coppi, N. Elvassore, and L. Vitiello, “Three-dimensional porous scaffold allows long-term wild-type cell delivery in dystrophic muscle,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 1, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  156. A. L. Perez, E. Bachrach, B. M. W. Illigens et al., “CXCR4 enhances engraftment of muscle progenitor cells,” Muscle and Nerve, vol. 40, no. 4, pp. 562–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  157. X. Gerard, L. Vignaud, S. Charles et al., “Real-time monitoring of cell transplantation in mouse dystrophic muscles by a secreted alkaline phosphatase reporter gene,” Gene Therapy, vol. 16, no. 6, pp. 815–819, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. M. Bouchentouf, B. F. Benabdallah, P. Mills, and J. P. Tremblay, “Exercise improves the success of myoblast transplantation in mdx mice,” Neuromuscular Disorders, vol. 16, no. 8, pp. 518–529, 2006. View at Publisher · View at Google Scholar · View at Scopus
  159. E. Bachrach, A. L. Perez, Y. H. Choi et al., “Muscle engraftment of myogenic progenitor cells following intraarterial transplantation,” Muscle and Nerve, vol. 34, no. 1, pp. 44–52, 2006. View at Publisher · View at Google Scholar · View at Scopus
  160. B. F. Benabdallah, M. Bouchentouf, and J. P. Tremblay, “Improved success of myoblast transplantation in mdx mice by blocking the myostatin signal,” Transplantation, vol. 79, no. 12, pp. 1696–1702, 2005. View at Publisher · View at Google Scholar · View at Scopus
  161. T. F. Lee-Pullen, A. L. Bennett, M. W. Beilharz, M. D. Grounds, and L. M. Sammels, “Superior survival and proliferation after transplantation of myoblasts obtained from adult mice compared with neonatal mice,” Transplantation, vol. 78, no. 8, pp. 1172–1176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  162. M. Bouchentouf, B. F. Benabdallah, and J. P. Tremblay, “Myoblast survival enhancement and transplantation success improvement by heat-shock treatment in mdx mice,” Transplantation, vol. 77, no. 9, pp. 1349–1356, 2004. View at Publisher · View at Google Scholar · View at Scopus
  163. G. P. Kobinger, J. P. Louboutin, E. R. Barton, H. L. Sweeney, and J. M. Wilson, “Correction of the dystrophic phenotype by in vivo targeting of muscle progenitor cells,” Human Gene Therapy, vol. 14, no. 15, pp. 1441–1449, 2003. View at Publisher · View at Google Scholar · View at Scopus
  164. E. El Fahime, M. Bouchentouf, B. F. Benabdallah et al., “Tubulyzine, a novel tri-substituted triazine, prevents the early cell death of transplanted myogenic cells and improves transplantation success,” Biochemistry and Cell Biology, vol. 81, no. 2, pp. 81–90, 2003. View at Publisher · View at Google Scholar · View at Scopus
  165. R. J. Jankowski, B. M. Deasy, B. Cao, C. Gates, and J. Huard, “The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells,” Journal of Cell Science, vol. 115, no. 22, pp. 4361–4374, 2002. View at Publisher · View at Google Scholar · View at Scopus
  166. M. H. Parker, C. Kuhr, S. J. Tapscott, and R. Storb, “Hematopoietic cell transplantation provides an immune-tolerant platform for myoblast transplantation in dystrophic dogs,” Molecular Therapy, vol. 16, no. 7, pp. 1340–1346, 2008. View at Publisher · View at Google Scholar · View at Scopus
  167. S. Yang, T. Laumonier, and J. Menetrey, “Heat shock pretreatment enhances porcine myoblasts survival after autotransplantation in intact skeletal muscle,” Science in China, Series C, vol. 50, no. 4, pp. 438–446, 2007. View at Publisher · View at Google Scholar · View at Scopus
  168. R. Fakhfakh, A. Michaud, and J. P. Tremblay, “Blocking the myostatin signal with a dominant negative receptor improves the success of human myoblast transplantation in dystrophic mice,” Molecular Therapy, vol. 19, no. 1, pp. 204–210, 2011. View at Publisher · View at Google Scholar · View at Scopus
  169. B. F. Benabdallah, M. Bouchentouf, J. Rousseau, and J. P. Tremblay, “Overexpression of follistatin in human myoblasts increases their proliferation and differentiation, and improves the graft success in SCID mice,” Cell Transplantation, vol. 18, no. 7, pp. 709–718, 2009. View at Publisher · View at Google Scholar · View at Scopus
  170. R. Benchaouir, M. Meregalli, A. Farini et al., “Restoration of human dystrophin following transplantation of exon-skipping-engineered DMD patient stem cells into dystrophic mice,” Cell Stem Cell, vol. 1, no. 6, pp. 646–657, 2007. View at Publisher · View at Google Scholar · View at Scopus
  171. P. Mills, J. C. Dominique, J. F. Lafrenière, M. Bouchentouf, and J. P. Tremblay, “A synthetic mechano growth factor E peptide enhances myogenic precursor cell transplantation success,” American Journal of Transplantation, vol. 7, no. 10, pp. 2247–2259, 2007. View at Publisher · View at Google Scholar · View at Scopus
  172. S. P. Quenneville, P. Chapdelaine, D. Skuk et al., “Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: human cells and primate models,” Molecular Therapy, vol. 15, no. 2, pp. 431–438, 2007. View at Publisher · View at Google Scholar · View at Scopus
  173. Ç. Kocaefe, D. Balci, B. B. Hayta, and A. Can, “Reprogramming of human umbilical cord stromal mesenchymal stem cells for myogenic differentiation and muscle repair,” Stem Cell Reviews and Reports, vol. 6, no. 4, pp. 512–522, 2010. View at Publisher · View at Google Scholar · View at Scopus
  174. V. A. Nunes, N. Cavaçana, M. Canovas, B. E. Strauss, and M. Zatz, “Stem cells from umbilical cord blood differentiate into myotubes and express dystrophin in vitro only after exposure to in vivo muscle environment,” Biology of the Cell, vol. 99, no. 4, pp. 185–186, 2007. View at Publisher · View at Google Scholar · View at Scopus
  175. J. Meng, C. F. Adkin, V. Arechavala-Gomeza, L. Boldrin, F. Muntoni, and J. E. Morgan, “The contribution of human synovial stem cells to skeletal muscle regeneration,” Neuromuscular Disorders, vol. 20, no. 1, pp. 6–15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  176. C. De Bari, F. Dell'Accio, F. Vandenabeele, J. R. Vermeesch, J. M. Raymackers, and F. P. Luyten, “Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane,” Journal of Cell Biology, vol. 160, no. 6, pp. 909–918, 2003. View at Publisher · View at Google Scholar · View at Scopus
  177. E. Stillwell, J. Vitale, Q. Zhao et al., “Blastocyst injection of wild type embryonic stem cells induces global corrections in mdx mice,” PLoS One, vol. 4, no. 3, Article ID e4759, 2009. View at Publisher · View at Google Scholar · View at Scopus
  178. S. Bhagavati and W. Xu, “Generation of skeletal muscle from transplanted embryonic stem cells in dystrophic mice,” Biochemical and Biophysical Research Communications, vol. 333, no. 2, pp. 644–649, 2005. View at Publisher · View at Google Scholar · View at Scopus
  179. R. Darabi, J. Baik, M. Clee, M. Kyba, R. Tupler, and R. C. R. Perlingeiro, “Engraftment of embryonic stem cell-derived myogenic progenitors in a dominant model of muscular dystrophy,” Experimental Neurology, vol. 220, no. 1, pp. 212–216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  180. S. Corti, S. Strazzer, R. Del Bo et al., “A subpopulation of murine bone marrow cells fully differentiates along the myogenic pathway and participates in muscle repair in the mdx dystrophic mouse,” Experimental Cell Research, vol. 277, no. 1, pp. 74–85, 2002. View at Publisher · View at Google Scholar · View at Scopus
  181. H. Shao, B. Chen, and M. Tao, “Skeletal myogenesis by human primordial germ cell-derived progenitors,” Biochemical and Biophysical Research Communications, vol. 378, no. 4, pp. 750–754, 2009. View at Publisher · View at Google Scholar · View at Scopus
  182. I. Kerkis, C. E. Ambrosio, A. Kerkis et al., “Early transplantation of human immature dental pulp stem cells from baby teeth to golden retriever muscular dystrophy (GRMD) dogs: local or systemic?” Journal of Translational Medicine, vol. 6, article no. 35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  183. N. Hirt-Burri, A. S. De Buys Roessingh, C. Scaletta et al., “Human muscular fetal cells: a potential cell source for muscular therapies,” Pediatric Surgery International, vol. 24, no. 1, pp. 37–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  184. J. Chan, S. N. Waddington, K. O'Donoghue et al., “Widespread distribution and muscle differentiation of human fetal mesenchymal stem cells after intrauterine transplantation in dystrophic mdx mouse,” Stem Cells, vol. 25, no. 4, pp. 875–884, 2007. View at Publisher · View at Google Scholar · View at Scopus
  185. J. Chan, K. O'Donoghue, M. Gavina et al., “Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration,” Stem Cells, vol. 24, no. 8, pp. 1879–1891, 2006. View at Publisher · View at Google Scholar · View at Scopus
  186. R. E. Bittner, C. Schöfer, K. Weipoltshammer et al., “Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice,” Anatomy and Embryology, vol. 199, no. 5, pp. 391–396, 1999. View at Publisher · View at Google Scholar · View at Scopus
  187. Y. Torrente, M. Belicchi, C. Marchesi et al., “Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients,” Cell Transplantation, vol. 16, no. 6, pp. 563–577, 2007. View at Google Scholar · View at Scopus