Mesenchymal stem cells for the treatment of neurodegenerative disease

Regenerative Medicine

Volumn 5, Issue 6, 2010, Pages 933-946

  Joyce, Nanette ^a   Annett, Geralyn ^a   Wirthlin, Louisa ^a   Olson, Scott ^a   Bauer, Gerhard ^a   Nolta, Jan A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

amyotrophic lateral sclerosis; clinical trial; human mesenchymal stem cell; Huntington's disease; hypoxia; neurite outgrowth; neurodegenerative disease; tissue repair

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEURTURIN; RILUZOLE;

AMYOTROPHIC LATERAL SCLEROSIS; CELL SURVIVAL; CLINICAL TRIAL; DEGENERATIVE DISEASE; DISEASE DURATION; DISEASE MODEL; DISEASE SEVERITY; EXPERIMENTAL ANIMAL; HUMAN; HUNTINGTON CHOREA; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPLE SCLEROSIS; NERVE CELL GROWTH; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PATIENT MONITORING; PATIENT SAFETY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SYNAPTIC TRANSMISSION; THERAPY EFFECT; TISSUE REPAIR; UPREGULATION;

ANIMALS; CLINICAL TRIALS AS TOPIC; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEURODEGENERATIVE DISEASES; NEUROTRANSMITTER AGENTS; WOUND HEALING;

EID: 78649352832     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/rme.10.72     Document Type: Review

References (119)

1. Williams JT, Southerland SS, Souza J et al.: Cells isolated from adult human skeletal muscle capable of differentiating into multiple mesodermal phenotypes. Am. Surg. 65, 22-26 (1999).
2. Galmiche MC, Koteliansky VE, Briere J et al.: Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 82, 66-76 (1993).
3. Theise ND, Nimmakayalu M, Gardner R et al.: Liver from bone marrow in humans. Hepatology 32, 11-16 (2000).
4. Theise ND, Badve S, Saxena R et al.: Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31, 235-240 (2000).
5. Petersen BE, Bowen WC, Patrene KD et al.: Bone marrow as a potential source of hepatic oval cells. Science 284, 1168-1170 (1999).
6. Lagasse E, Connors H, Al-Dhalimy M et al.: Purifed hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 6, 1229-1234 (2000).
7. Orlic D, Kajstura J, Chimenti S et al.: Bone marrow cells regenerate infarcted myocardium. Nature 410, 701-705 (2001).
8. Wu GD, Nolta JA, Jin YS et al.: Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation 75, 679-685 (2003).
9. Jackson KA, Majka SM, Wang H et al.: Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J. Clin. Invest. 107, 1395-1402 (2001).
10. Zimmet JM, Hare JM: Emerging role for bone marrow derived mesenchymal stem cells in myocardial regenerative therapy. Basic Res. Cardiol. 100, 471-481 (2005).
11. Davidoff AM, Ng CY, Brown P et al.: Bone marrow-derived cells contribute to tumor neovasculature and, when modifed to express an angiogenesis inhibitor, can restrict tumor growth in mice. Clin. Cancer Res. 7, 2870-2879 (2001).
12. Crisa L, Cirulli V, Smith KA et al.: Human cord blood progenitors sustain thymic T-cell development and a novel form of angiogenesis. Blood 94, 3928-3940 (1999).
13. + cells identifes a population of functional endothelial precursors. Blood 95, 952-958 (2000).
14. Le Blanc K: Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 8, 559-561 (2006).
15. Lafamme MA, Murry CE: Regenerating the heart. Nat. Biotechnol. 23, 845-856 (2005).
16. Chen J, Li Y, Katakowski M et al.: Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J. Neurosci. Res. 73, 778-786 (2003).
17. Li Y, Chen J, Zhang CL et al.: Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49, 407-417 (2005).
18. Murphy JM, Fink DJ, Hunziker EB et al.: Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 48, 3464-3474 (2003).
19. Rosova I, Dao M, Capoccia B et al.: Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26(8), 2173-2182 (2008).
20. Kinnaird T, Stabile E, Burnett MS et al.: Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94, 678-685 (2004).
21. Gnecchi M, He H, Noiseux N et al.: Evidence supporting paracrine hypothesis for Akt-modifed mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J. 20, 661-669 (2006).
22. Meyerrose T, De Ugarte D, Hofing A et al.: In vivo distribution of human adipose-derived mesenchymal stem cells in novel xenotransplantation models. Stem Cells 25, 220-227 (2007).
23. Meyerrose TE, Roberts M, Ohlemiller KK et al.: Lentiviral-transduced human mesenchymal stem cells persistently express therapeutic levels of enzyme in a xenotransplantation model of human disease. Stem Cells 26, 1713-1722 (2008).
24. Bauer G, Dao MA, Case SS et al.: In vivo biosafety model to assess the risk of adverse events from retroviral and lentiviral vectors. Mol. Ther. 16, 1308-1315 (2008).
25. Dao MA, Pepper KA, Nolta JA: Long-term cytokine production from engineered primary human stromal cells infuences human hematopoiesis in an in vivo xenograft model. Stem Cells 15, 443-454(1997).
26. Nolta J: Genetic Engineering of Mesenchymal Stem Cells. Springer, Dordrecht, The Netherlands (2006).
27. Capoccia BJ, Robson DL, Levac KD et al.: Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity Blood 113, 5340-5351 (2009).
28. Danielyan L, Schafer R, von Ameln-Mayerhofer A et al.: Intranasal delivery of cells to the brain. Eur. J. Cell Biol. 88, 315-324 (2009).
29. Crigler L, Robey RC, Asawachaicharn A et al.: Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol. 198, 54-64 (2006).
30. Munoz JR, Stoutenger BR, Robinson AP et al.: Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc. Natl Acad. Sci. USA 102, 18171-18176 (2005).
31. Kassis I, Grigoriadis N, Gowda-Kurkalli B et al.: Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch. Neurol. 65, 753-761 (2008).
32. Tolar J, Nauta AJ, Osborn MJ et al.: Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25(2), 371-379 (2007).
33. Kidd S, Spaeth E, Dembinski JL et al.: Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells 27, 2614-2623 (2009).
34. Kidd S, Spaeth E, Klopp A et al.: The (in) auspicious role of mesenchymal stromal cells in cancer: be it friend or foe. Cytotherapy 10, 657-667 (2008).
35. Kim HJ, McMillan E, Han F et al.: Regionally specifed human neural progenitor cells derived from the mesencephalon and forebrain undergo increased neurogenesis following overexpression of ASCL1. Stem Cells 27, 390-398 (2009).
36. Sharp J, Keirstead HS: Stem cell-based cell replacement strategies for the central nervous system. Neurosci. Lett. 456, 107-111 (2009).
37. Hardy SA, Maltman DJ, Przyborski SA: Mesenchymal stem cells as mediators of neural differentiation. Curr. Stem Cell Res. Ther. 3, 43-52 (2008).
38. Rechavi O, Goldstein I, Kloog Y: Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett. 583, 1792-1799 (2009).
39. Spees JL, Olson SD, Whitney M J et al.: Mitochondrial transfer between cells can rescue aerobic respiration. Proc. Natl Acad. Sci. USA 103, 1283-1288 (2006).
40. Wilkins A, Kemp K, Ginty M et al.: Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. (2009) (Epub ahead of print).
41. Endo Y, Beauchamp E, Woods D et al.: Wnt-3a and Dickkopf-1 stimulate neurite outgrowth in Ewing tumor cells via a Frizzled3-and c-Jun N-terminal kinase-dependent mechanism. Mol. Cell Biol. 28, 2368-2379 (2008).
42. Etheridge SL, Spencer GJ, Heath DJ et al.: Expression profling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 22, 849-860 (2004).
43. Gregory CA, Singh H, Perry AS et al.: The Wnt signaling inhibitor dickkopf-1 is required for reentry into the cell cycle of human adult stem cells from bone marrow. J. Biol. Chem. 278, 28067-28078 (2003).
44. Allen J, Chilton JK: The specifc targeting of guidance receptors within neurons: who directs the directors? Dev. Biol. 327, 4-11 (2009).
45. Aizman I, Tate CC, McGrogan M et al.: Extracellular matrix produced by bone marrow stromal cells and by their derivative, SB623 cells, supports neural cell growth. J. Neurosci. Res. 87, 3198-3206 (2009).
46. Croft A P, Przyborski SA: Mesenchymal stem cells expressing neural antigens instruct a neurogenic cell fate on neural stem cells. Exp. Neurol. 216, 329-341 (2009).
47. Boudreau RL, McBride JL, Martins I et al.: Nonallele-specifc silencing of mutant and wild-type huntingtin demonstrates therapeutic effcacy in Huntington's disease mice. Mol. Ther. 17, 1053-1063 (2009).
48. Harper SQ, Staber PD, He X et al.: RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc. Natl Acad. Sci. USA 102, 5820-5825 (2005).
49. DiFiglia M, Sena-Esteves M, Chase K et al.: Therapeutic silencing of mutant huntingtin with siRNA attenuates striatal and cortical neuropathology and behavioral defcits. Proc. Natl Acad. Sci. USA 104, 17204-17209 (2007).
50. Wang YL, Liu W, Wada E et al.: Clinico-pathological rescue of a model mouse of Huntington's disease by siRNA. Neurosci. Res. 53, 241-249 (2005).
51. Lombardi MS, Jaspers L, Spronkmans C et al.: A majority of Huntington's disease patients may be treatable by individualized allele-specifc RNA interference. Exp. Neurol. 217, 312-319 (2009).
52. Pfster EL, Kennington L, Straubhaar J et al.: Five siRNAs targeting three SNPs may provide therapy for three-quarters of Huntington's disease patients. Curr. Biol. 19, 774-778 (2009).
53. Zhang Y, Engelman J, Friedlander RM: Allele-specifc silencing of mutant Huntington's disease gene. J. Neurochem. 108, 82-90 (2009).
54. Lescaudron L, Unni D, Dunbar GL: Autologous adult bone marrow stem cell transplantation in an animal model of Huntington's disease: behavioral and morphological outcomes. Int. J. Neurosci. 113, 945-956 (2003).
55. Bantubungi K, Blum D, Cuvelier L et al.: Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol. Cell. Neurosci. 37, 454-470 (2008).
56. Amin EM, Reza BA, Morteza BR et al.: Microanatomical evidences for potential of mesenchymal stem cells in amelioration of striatal degeneration. Neurol. Res. 30, 1086-1090 (2008).
57. Watts C, McNamara IR, Dunnett SB: Volume and differentiation of striatal grafts in rats: relationship to the number of cells implanted. Cell Transplant. 9, 65-72 (2000).
58. Delcroix GJ, Jacquart M, Lemaire L et al.: Mesenchymal and neural stem cells labeled with HEDP-coated SPIO nanoparticles: in vitro characterization and migration potential in rat brain. Brain Res. 1255, 18-31 (2009).
59. Sadan O, Shemesh N, Barzilay R et al.: Migration of neurotrophic factors-secreting mesenchymal stem cells toward a quinolinic acid lesion as viewed by magnetic resonance imaging. Stem Cells 26, 2542-2551 (2008).
60. Sadan O, Shemesh N, Cohen Y et al.: Adult neurotrophic factor-secreting stem cells: a potential novel therapy for neurodegenerative diseases. Isr. Med. Assoc. J. 11, 201-204 (2009).
61. Bachoud-Levi AC, Gaura V, Brugieres P et al.: Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long-term follow-up study. Lancet Neurol. 5, 303-309 (2006).
62. Gaura V, Bachoud-Levi AC, Ribeiro MJ et al.: Striatal neural grafting improves cortical metabolism in Huntington's disease patients. Brain 127, 65-72 (2004).
63. Canals JM, Pineda JR, Torres-Peraza JF et al.: Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease. J. Neurosci. 24, 7727-7739 (2004).
64. Her LS, Goldstein LS: Enhanced sensitivity of striatal neurons to axonal transport defects induced by mutant huntingtin. J. Neurosci. 28, 13662-13672 (2008).
65. Wu LL, Fan Y, Li S et al.: Huntingtin associated protein-1 interacts with proBDNF and mediates its transport and release. J. Biol. Chem. 285(8), 5614-5623 (2009).
66. Gharami K, Xie Y, An JJ et al.: Brain-derived neurotrophic factor over-expression in the forebrain ameliorates Huntington's disease phenotypes in mice. J. Neurochem.105, 369-379 (2008).
67. Zuccato C, Cattaneo E: Brain-derived neurotrophic factor in neurodegenerative diseases. Nature Rev. 5, 311-322 (2009).
68. Alberch J, Perez-Navarro E, Canals JM: Neurotrophic factors in Huntington's disease. Prog. Brain Res. 146, 195-229 (2004).
69. Dey ND, Bombard MC, Roland BP et al.: Genetically-engineered mesenchymal stem cells reduce behavioral defcits in the YAC 128 mouse model of Huntington's disease. Behav. Brain Res. 214(2), 193-200 (2010).
70. Nolta JA, Dao MA, Wells S et al.: Transduction of pluripotent human hematopoietic stem cells demonstrated by clonal analysis after engraftment in immune-defcient mice. Proc. Natl Acad. Sci. USA 93, 2414-2419 (1996).
71. Nolta JA, Kohn DB: Comparison of the effects of growth factors on retroviral vector-mediated gene transfer and the proliferative status of human hematopoietic progenitor cells. Hum. Gene Ther. 1, 257-268 (1990).
72. Tsark E, Dao M, Wang X et al.: IL-7 enhances the responsiveness of human T cells that develop in the bone marrow of athymic mice. J. Immunol. 166, 170-181 (2001).
73. Wang X, Ge S, McNamara G et al.: Albumin expressing hepatocyte-like cells develop in the livers of immune-defcient mice transmitted with highly purifed human hematopoietic stem cells. Blood 101(10), 4201-4208 (2003).
74. Nolta JA, Hanley MB, Kohn DB: Sustained human hematopoiesis in immunodefcient mice by cotransplantation of marrow stroma expressing human interleukin-3: analysis of gene transduction of long-lived progenitors. Blood 83, 3041-3051 (1994).
75. Meyerrose T, Rosova I, Dao M et al.: Establishment and Transduction of Primary Human Stromal/Mesenchymal Stem Cell Monolayers. Kluwer Academic Publishers, Dordrecht, The Netherlands (2006).
76. Vucic S, Kiernan MC: Pathophysiology of neurodegeneration in familial amyotrophic lateral sclerosis. Curr. Mol. Med. 9, 255-272 (2009).
77. Maxwell MM: RNAi applications in therapy development for neurodegenerative disease. Curr. Pharm. Des. 15, 3977-3991 (2009).
78. Kim SU, de Vellis J: Stem cell-based cell therapy in neurological diseases: a review. J. Neurosci. Res. 87, 2183-2200 (2009).
79. 2+ overload of motor neurons. Amyotroph. Lateral Scler. 8, 260-265 (2007).
80. Julien JP, Kriz J: Transgenic mouse models of amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1762, 1013-1024 (2006).
81. Bruijn LI, Miller TM, Cleveland DW: Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749 (2004).
82. Zhao CP, Zhang C, Zhou SN et al.: Human mesenchymal stromal cells ameliorate the phenotype of SOD1-G93A ALS mice. Cytotherapy 9, 414-426 (2007).
83. Vercelli A, Mereuta OM, Garbossa D et al.: Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinfammation in mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 31, 395-405 (2008).
84. Morita E, Watanabe Y, Ishimoto M et al.: A novel cell transplantation protocol and its application to an ALS mouse model. Exp. Neurol. 213, 431-438 (2008).
85. Fischer LR, Culver DG, Tennant P et al.: Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185, 232-240 (2004).
86. Klein SM, Behrstock S, McHugh J et al.: GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum. Gene Ther. 16, 509-521 (2005).
87. Suzuki M, McHugh J, Tork C 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 2, e689 (2007).
88. Suzuki M, McHugh J, Tork C 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. Mol. Ther. 16, 2002-2010 (2008).
89. Funakoshi H, Ohya W, Kadoyama K et al.: [ALS and neurotrophic factors-HGF as a novel neurotrophic and neuroregenerative factor]. Brain Nerve 59, 1195-1202 (2007).
90. Kadoyama K, Funakoshi H, Ohya W et al.: Hepatocyte growth factor (HGF) attenuates gliosis and motoneuronal degeneration in the brainstem motor nuclei of a transgenic mouse model of ALS. Neurosci. Res. 59, 446-456 (2007).
91. Donsante A, Miller DG, Li Y et al.: AAV vector integration sites in mouse hepatocellular carcinoma. Science 317, 477 (2007).
92. Nagano I, Ilieva H, Shiote M et al.: Therapeutic beneft of intrathecal injection of insulin-like growth factor-1 in a mouse model of amyotrophic lateral sclerosis. J. Neurol. Sci. 235, 61-68 (2005).
93. Nagano I, Shiote M, Murakami T et al.: Benefcial effects of intrathecal IGF-1 administration in patients with amyotrophic lateral sclerosis. Neurosci. Res. 27, 768-772 (2005).
94. Mazzini L, Ferrero I, Luparello V et al.: Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a Phase I clinical trial. Exp. Neurol. 223(1), 229-237 (2009).
95. Greene P: Cell-based therapies in Parkinson's disease. Curr. Neurol. Neurosci. Rep. 9, 292-297 (2009).
96. Jenner P: Functional models of Parkinson's disease: a valuable tool in the development of novel therapies. Ann. Neurol. 64(Suppl. 2), S16-S29 (2008).
97. Jin GZ, Cho SJ, Choi EG et al.: Rat mesenchymal stem cells increase tyrosine hydroxylase expression and dopamine content in ventral mesencephalic cells in vitro. Cell Biol. Int. 32, 1433-1438 (2008).
98. Bouchez G, Sensebe L, Vourc'h P et al.: Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease. Neurochem. Int. 52, 1332-1342 (2008).
99. Sadan O, Bahat-Stromza M, Barhum Y et al.: Protective effects of neurotrophic factor-secreting cells in a 6-OHDA rat model of Parkinson disease. Stem Cells Dev. 18, 1179-1190 (2009).
100. Peterson AL, Nutt JG: Treatment of Parkinson's disease with trophic factors. Neurotherapeutics 5, 270-280 (2008).
101. Manfredsson FP, Okun MS, Mandel RJ: Gene therapy for neurological disorders: challenges and future prospects for the use of growth factors for the treatment of Parkinson's disease. Curr. Gene Ther. 9, 375-388 (2009).
102. Ramaswamy S, Soderstrom KE, Kordower JH: Trophic factors therapy in Parkinson's disease. Prog. Brain Res. 175, 201-216 (2009).
103. Li JY, Englund E, Holton JL et al.: Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 14, 501-503 (2008).
104. Mazzini L, Fagioli F, Boccaletti R et al.: Stem cell therapy in amyotrophic lateral sclerosis: a methodological approach in humans. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 4, 158-161 (2003).
105. Karussis D, Kassis I, Kurkalli BG et al.: Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a proposed treatment for multiple sclerosis and other neuroimmunological/neurodegenerative diseases. J. Neurol. Sci. 265, 131-135 (2008).
106. Mancardi G, Saccardi R: Autologous haematopoietic stem-cell transplantation in multiple sclerosis. Lancet Neurol. 7, 626-636 (2008).
107. Saccardi R, Kozak T, Bocelli-Tyndall C 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. Mult. Scler. 12, 814-823 (2006).
108. Shevchenko YL, Novik AA, Kuznetsov AN et al.: High-dose immunosuppressive therapy with autologous hematopoietic stem cell transplantation as a treatment option in multiple sclerosis. Exp. Hematol. 36, 922-928 (2008).
109. Atkins H, Freedman M: Immune ablation followed by autologous hematopoietic stem cell transplantation for the treatment of poor prognosis multiple sclerosis. Methods Mol. Biol. 549, 231-246 (2009).
110. Burt RK, Loh Y, Cohen B et al.: Autologous non-myeloablative haemopoietic stem cell transplantation in relapsing-remitting multiple sclerosis: a Phase I/II study. Lancet Neurol. 8, 244-253 (2009).
111. Rogojan C, Frederiksen JL: Hematopoietic stem cell transplantation in multiple sclerosis. Acta Neurol. Scand. 120, 371-382 (2009).
112. Bonab MM, Yazdanbakhsh S, Lofti J: Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran J. Immunol. 4, 50-57 (2007).
113. Liang J, Zhang H, Hua B et al.: Allogeneic mesenchymal stem cells transplantation in treatment of multiple sclerosis. Mult. Scler. 15, 644-646 (2009).
114. Zhang ZX, Guan LX, Zhang K et al.: A combined procedure to deliver autologous mesenchymal stromal cells to patients with traumatic brain injury. Cytotherapy 10, 134-139 (2008).
115. Ting AE, Mays RW, Frey MR et al.: Therapeutic pathways of adult stem cell repair. Crit. Rev. Oncol. Hematol. 65, 81-93 (2008).
116. Mays RW, van't Hof W, Ting AE et al.: Development of adult pluripotent stem cell therapies for ischemic injury and disease. Expert Opin. Biol. Ther. 7, 173-184 (2007).
117. Hare JM, Traverse JH, Henry TD et al.: A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J. Am. Coll. Cardiol. 54, 2277-2286 (2009).
118. Newman RE, Yoo D, LeRoux MA et al.: Treatment of infammatory diseases with mesenchymal stem cells. Infamm. Allergy Drug Targets 8, 110-123 (2009).
119. Dryden GW: Overview of stem cell therapy for Crohn's disease. Expert Opin. Biol. Ther. 9, 841-847 (2009).