Human mesenchymal stem cells in the treatment of neurological diseases

Acta Neurobiologiae Experimentalis

Volumn 73, Issue 1, 2013, Pages 38-56

  Drela, Katarzyna ^a   Siedlecka, Patrycja ^a   Sarnowska, Anna ^a   Domanska Janik, Krystyna ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Cell transplantation; Mesenchymal stem cells; Neurological diseases

Indexed keywords

CELL DIFFERENTIATION; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METHODOLOGY; NEUROLOGIC DISEASE; PHYSIOLOGY; REVIEW;

CELL DIFFERENTIATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NERVOUS SYSTEM DISEASES;

EID: 84878388248     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Review

References (166)

1. Acquistapace A, Bru T, Lesault PF, Figeac F, Coudert AE, le Coz O, Christov C, Baudin X, Auber F, Yiou R, Dubois- Rande JL, Rodriguez AM (2011) Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells 29: 812-824.
2. Alessandri G, Pagano S, Bez A, Benetti A, Pozzi S, Iannolo G, Baronio M, Invernici G, Caruso A, Muneretto C, Bisleri G, Parati E (2004) Isolation and culture of human muscle- derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet 364: 1872-1883.
3. Amrani DL, Port S (2003) Cardiovascular disease: potential impact of stem cell therapy. Expert Rev Cardiovasc Ther 1: 453-461.
4. Armesilla-Diaz A, Elvira G, Silva A (2009) p53 regulates the proliferation, differentiation and spontaneous transformation of mesenchymal stem cells. Exp Cell Res 315: 3598-3610.
5. Bae KS, Park JB, Kim HS, Kim DS, Park DJ, Kang SJ. Neuron-like differentiation of bone marrow-derived mesenchymal stem cells. Yonsei Med J 52: 401-412.
6. Baek W, Kim YS, Koh SH, Lim SW, Kim HY, Yi HJ, Kim H (2012) Stem cell transplantation into the intraventricu- lar space via an Ommaya reservoir in a patient with amyotrophic lateral sclerosis. J Neurosurg Sci 56: 261-363.
7. Bang OY, Lee JS, Lee PH, Lee G (2005) Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 57: 874-882.
8. Barbosa da Fonseca LM, Gutfilen B, Rosado de Castro PH, Battistella V, Goldenberg RC, Kasai-Brunswick T, Chagas CL, Wajnberg E, Maiolino A, Salles Xavier S, Andre C, Mendez-Otero R, de Freitas GR (2010) Migration and homing of bone-marrow mononuclear cells in chronic ischemic stroke after intra-arterial injection. Exp Neurol 221: 122-128.
9. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30: 42-48.
10. Bertani N, Malatesta P, Volpi G, Sonego P, Perris R (2005) Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J Cell Sci 118: 3925-3936.
11. Bhanot Y, Rao S, Ghosh D, Balaraju S, Radhika CR, Satish Kumar KV (2011)Autologous mesenchymal stem cells in chronic spinal cord injury. Br J Neurosurg 25: 516-522.
12. Bhasin A, Srivastava MV, Kumaran SS, Mohanty S, Bhatia R, Bose S, Gaikwad S, Garg A, Airan B (2011) Autologous mesenchymal stem cells in chronic stroke. Cerebrovasc Dis Extra: 93-104.
13. Bhasin A, Padma Srivastava MV, Mohanty S, Bhatia R, Kumaran SS, Bose S (2012) Stem cell therapy: A clinical trial of stroke. Clin Neurol Neurosurg, doi: 10.1016/j. clineuro.2012.10.015. [Epub ahead of print]
14. Bitsika V, Roubelakis MG, Zagoura D, Trohatou O, Makridakis M, Pappa KI, Marini FC, Vlahou A, Anagnou NP (2012) Human amniotic fluid-derived mesenchymal stem cells as therapeutic vehicles: a novel approach for the treatment of bladder cancer. Stem Cells Dev 21: 1097-1111.
15. Brooke G, Tong H, Levesque JP, Atkinson K (2008) Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev 17: 929-940.
16. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, Tetta C, Camussi G (2009) Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol: 1053-1067.
17. Buzanska L, Machaj EK, Zablocka B, Pojda Z, Domanska- Janik K (2002) Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 115: 2131-2138.
18. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM (2001) Identification of mesenchymal stem/ progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 98: 2396-2402.
19. Canzi L, Castellaneta V, Navone S, Nava S, Dossena M, Zucca I, Mennini T, Bigini P, Parati EA (2012) Human skeletal muscle stem cell antiinflammatory activity ameliorates clinical outcome in amyotrophic lateral sclerosis models. Mol Med 18: 401-411.
20. Chao YH, Wu HP, Chan CK, Tsai C, Peng CT, Wu KH (2012) Umbilical cord-derived mesenchymal stem cells for hematopoietic stem cell transplantation. J Biomed Biotechnol 2012: 759503.
21. Chen J, Li Y, Katakowski M, Chen X, Wang L, Lu D, Lu M, Gautam SC, Chopp M (2003) Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73: 778-786.
22. Chen L, Chen D, Xi H, Wang Q, Liu Y, Zhang F, Wang H, Ren Y, Xiao J, Wang Y, Huang H (2012) Olfactory ensheathing cell neurorestorotherapy for amyotrophic lateral sclerosis patients: benefits from multiple transplantations. Cell Transplant 21: S65-77.
23. Cho YI, Choi JS, Jeong SY, Yoo HS (2010) Nerve growth factor (NGF)-conjugated electrospun nanostructures with topographical cues for neuronal differentiation of mesenchymal stem cells. Acta Biomater 6: 4725-4733.
24. Choi YJ, Li WY, Moon GJ, Lee PH, Ahn YH, Lee G, Bang OY (2010) Enhancing trophic support of mesenchymal stem cells by ex vivo treatment with trophic factors. J Neurol Sci 298: 28-34.
25. Choong PF, Mok PL, Cheong SK, Leong CF, Then KY, Generating neuron-like cells from BM-derived mesenchymal stromal cells in vitro. Cytotherapy 9: 170-183.
26. Claros S, Rodríguez-Losada N, Cruz E, Guerado E, Becerra J, Andrades JA (2012) Characterization of adult stem/ progenitor cell populations from bone marrow in a threedimensional collagen gel culture system. Cell Transplant 21: 2021-2032.
27. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Tetta C, Camussi G (2010) Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5: e11803.
28. Compston A, Coles A (2008) Multiple sclerosis. Lancet 372: 1502-1517.
29. Connick P, Kolappan M, Crawley C, Webber DJ, Patani R, Michell AW, Du MQ, Luan SL, Altmann DR, Thompson AJ, Compston A, Scott MA, Miller DH, Chandran S (2012) Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Lancet Neurol 11: 150-156.
30. Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V, Uccelli A (2006) Human mesenchymal stem cells modulate B-cell functions. Blood 107: 367-372.
31. Correa PL, Mesquita CT, Felix RM, Azevedo JC, Barbirato GB, Falcão CH, Gonzalez C, Mendonça ML, Manfrim A, de Freitas G, Oliveira CC, Silva D, Avila D, Borojevic R, Alves S, Oliveira AC Jr, Dohmann HF (2007) Assessment of intra-arterial injected autologous bone marrow mononuclear cell distribution by radioactive labeling in acute ischemic stroke. Clin Nucl Med 32: 839-841.
32. Courtney AM, Treadaway K, Remington G, Frohman E, Multiple sclerosis. Med Clin North Am 93: 451-476.
33. Crain BJ, Tran SD, Mezey E (2005) Transplanted human bone marrow cells generate new brain cells. J Neurol Sci 233: 121-123.
34. Crigler L, Robey RC, Asawachaicharn A, Gaupp D, Phinney DG (2006) Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 198: 54-64.
35. Cselenyak A, Pankotai E, Horvath EM, Kiss L, Lacza Z, Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biol 11: 29.
36. da Silva Meirelles L, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119: 2204-2213.
37. Darlington D, Deng J, Giunta B, Hou H, Sanberg CD, Kuzmin-Nichols N, Zhou HD, Mori T, Ehrhart J, Sanberg PR, Tan J (2012) Multiple low-dose infusions of human umbilical cord blood cells improve cognitive impairments and reduce amyloid-ß-associated neuropathology in Alzheimer mice. Stem Cells Dev 22: 412-421.
38. Deda H, Inci MC, Kurekci AE, Kayihan K, Ozgun E, Ustünsoy GE, Kocabay S (2008) Treatment of chronic spinal cord injured patients with autologous bone marrow-derived hematopoietic stem cell transplantation: 1-year follow-up. Cytotherapy 10: 565-574.
39. Deng J, Zou ZM, Zhou TL, Su YP, Ai GP, Wang JP, Xu H, Dong SW (2011) Bone marrow mesenchymal stem cells can be mobilized into peripheral blood by G-CSF in vivo and integrate into traumatically injured cerebral tissue. Neurol Sci 32: 641-651.
40. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC (2004) Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117: 2971-2981.
41. Djouad F, Charbonnier LM, Bouffi C, Louis-Plence P, Bony C, Apparailly F, Cantos C, Jorgensen C, Noel D (2007) Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells 25: 2025-2032.
42. Djouad F, Bouffi C, Ghannam S, Noel D, Jorgensen C, Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases. Nat Rev Rheumatol 5: 392-399.
43. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
44. Duffy MM, Ritter T, Ceredig R, Griffin MD (2011) Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther 2: 34.
45. Ende N, Chen R, Ende-Harris D (2001) Human umbilical cord blood cells ameliorate Alzheimer's disease in transgenic mice. J Med 32: 241-247.
46. Ferroni L, Gardin C, Tocco I, Epis R, Casadei A, Vindigni V, Mucci G, Zavan B (2012) Potential for neural differentiation of mesenchymal stem cells. Adv Biochem Eng Biotechnol [Epub ahead of print].
47. Filip S, Mokry J, Horacek J, English D (2008) Stem cells and the phenomena of plasticity and diversity: a limiting property of carcinogenesis. Stem Cells Dev 17: 1031-1038.
48. Fiorina P, Jurewicz M, Augello A, Vergani A, Dada S, La Rosa S, Selig M, Godwin J, Law K, Placidi C, Smith RN, Capella C, Rodig S, Adra CN, Atkinson M, Sayegh MH, Abdi R (2009) Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol 183: 993-1004.
49. Forostyak S, Jendelova P, Kapcalova M, Arboleda D, Sykova E (2011) Mesenchymal stromal cells prolong the lifespan in a rat model of amyotrophic lateral sclerosis. Cytotherapy 13: 1036-1046.
50. Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24: 150-154.
51. Friedenstein AJ, Gorskaja JF, Kulagina NN (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4: 267-274.
52. Friedrich MA, Martins MP, Araújo MD, Klamt C, Vedolin L, Garicochea B, Raupp EF, Sartori El Ammar J, Machado DC, Costa JC, Nogueira RG, Rosado-de-Castro PH, Mendez-Otero R, Freitas GR (2012) Intra-arterial infusion of autologous bone marrow mononuclear cells in patients with moderate to severe middle cerebral artery acute ischemic stroke. Cell Transplant Suppl 1: S13-S21.
53. Geffner LF, Santacruz P, Izurieta M, Flor L, Maldonado B, Auad AH, Montenegro X, Gonzalez R, Silva F (2008) Administration of autologous bone marrow stem cells into spinal cord injury patients via multiple routes is safe and improves their quality of life: comprehensive case studies. Cell Transplant 17: 1277-1293.
54. Gerdoni E, Gallo B, Casazza S, Musio S, Bonanni I, Pedemonte E, Mantegazza R, Frassoni F, Mancardi G, Pedotti R, Uccelli A (2007) Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 61: 219-227.
55. Gharami K, Xie Y, An JJ, Tonegawa S, Xu B (2008) Brain- derived neurotrophic factor overexpression in the forebrain ameliorates Huntington's disease phenotypes in mice. J Neurochem 105: 369-379.
56. Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Circ Res 100: 1249-1260.
57. Goldenberg-Cohen N, Avraham-Lubin BC, Sadikov T, Goldstein RS, Askenasy N (2012) Primitive stem cells derived from bone marrow express glial and neuronal markers and support revascularization in injured retina exposed to ischemic and mechanical damage. Stem Cells Dev 21: 1488-1500.
58. Gonzalez-Rey E, Gonzalez MA, Varela N, O'Valle F, Hernandez-Cortes P, Rico L, Büscher D, Delgado M, Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis 69: 241-248.
59. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp 183: 1797-1806.
60. Gornicka-Pawlak, Janowski M, Habich A, Jablonska A, Drela K, Kozlowska H, Lukomska B, Sypecka J, Domanska-Janik K (2011) Systemic treatment of focal brain injury in the rat by human umbilical cord blood cells being at different level of neural commitment. Acta Neurobiol Exp (Wars) 71: 46-64.
61. Grayson WL, Zhao F, Bunnell B, Ma T (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358: 948-953.
62. Grisendi G, Bussolari R, Cafarelli L, Petak I, Rasini V, Veronesi E, De Santis G, Spano C, Tagliazzucchi M, Barti-Juhasz H, Scarabelli L, Bambi F, Frassoldati A, Rossi G, Casali C, Morandi U, Horwitz EM, Paolucci P, Conte P, Dominici M (2010) Adipose-derived mesenchymal stem cells as stable source of tumor necrosis factor- related apoptosis-inducing ligand delivery for cancer therapy. Cancer Res 70: 3718-3729.
63. Habich A, Jurga M, Markiewicz I, Lukomska B, Bany- Laszewicz U, Domanska-Janik K (2006) Early appearance of neural progenitors in human cord blood mononuclear cells cultured in vitro. Exp Hematol 34: 914-925.
64. Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117: 4411-4422.
65. Honmou O, Houkin K, Matsunaga T, Niitsu Y, Ishiai S, Onodera R, Waxman SG, Kocsis JD (2011) Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain 134: 1790-1807.
66. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper- Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A (2005) International Society for Cellular Therapy: Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7: 393-399.
67. Iihoshi S, Honmou O, Houkin K, Hashi K, Kocsis JD (2004) A therapeutic window for intravenous administration of autologous bone marrow after cerebral ischemia in adult rats. Brain Res 1007: 1-9.
68. Ishii M, Arias AC, Liu L, Chen YB, Bronner ME, Maxson RE (2012) A stable cranial neural crest cell line from mouse. Stem Cells Dev 21: 3069-3080.
69. Jablonska A, Kozlowska H, Markiewicz I, Domanska-Janik K, Lukomska B (2010) Transplantation of neural stem cells derived from human cord blood to the brain of adult and neonatal rats. Acta Neurobiol Exp (Wars) 70: 337-350.
70. Jablonska A, Lukomska B (2011) Stroke induced brain changes: Implications for stem cell transplantation. Acta Neurobiol Exp (Wars) 71: 74-85.
71. Jeong JA, Gang EJ, Hong SH, Hwang SH, Kim SW, Yang IH, Ahn C, Han H, Kim H (2004) Rapid neural differentiation of human cord blood-derived mesenchymal stem cells. Neuroreport 15:1731-1734.
72. Jeong JO, Han JW, Kim JM, Cho HJ, Park C, Lee N, Kim DW, Yoon YS (2011) Malignant tumor formation after transplantation of short-term cultured bone marrow mesenchymal stem cells in experimental myocardial infarction and diabetic neuropathy. Circ Res 108: 1340-1347.
73. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41-49.
74. Jiang Y, Lv H, Huang S, Tan H, Zhang Y, Li H (2011) Bone marrow mesenchymal stem cells can improve the motor function of a Huntington's disease rat model. Neurol Res 33: 331-337.
75. Josse C, Schoemans R, Niessen NA, Delgaudine M, Hellin AC, Herens C, Delvenne P, Bours V (2010) Systematic chromosomal aberrations found in murine bone marrow-derived mesenchymal stem cells. Stem Cells Dev 19: 1167-1173.
76. Jozwiak S, Habich A, Kotulska K, Sarnowska A, Kropiwnicki T, Janowski M, Jurkiewicz E, Lukomska B, Kmiec T, Walecki J, Roszkowski M, Litwin M, Oldak T, Boruczkowski D, Domanska-Janik K (2010) Intracerebroventricular transplantation of cord blood-derived neural progenitors in a child with severe global brain ischemic injury. Cell Medicine 1: 71-80.
77. Jurga M, Lipkowski AW, Lukomska B, Buzanska L, Kurzepa K, Sobanski T, Habich A, Coecke S, Gajkowska B, Domanska-Janik K (2009) Generation of functional neural artificial tissue from human umbilical cord blood stem cells. Tissue Eng Part C Methods 15: 365-372.
78. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda- Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S (2010) Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 67: 1187-1194.
79. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, Slavin S, Abramsky O, Karussis D (2008) Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 65: 753-761.
80. Kastrinaki MC, Andreakou I, Charbord P, Papadaki HA (2008) Isolation of human bone marrow mesenchymal stem cells using different membrane markers: comparison of colony/ cloning efficiency, differentiation potential, and molecular profile. Tissue Eng Part C Methods 14: 333-339.
81. Kells AP, Fong DM, Dragunow M, During MJ, Young D, Connor B (2004) AAV-mediated gene delivery of BDNF or GDNF is neuroprotective in a model of Huntington disease. Mol Ther 9: 682-688.
82. Kim HS, Choi DY, Yun SJ, Choi SM, Kang JW, Jung JW, Hwang D, Kim KP, Kim DW (2012) Proteomic analysis of microvesicles derived from human mesenchymal stem cells. J Proteome Res 11: 839-849.
83. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ (2006) A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+) Oct-4+ stem cells identified in adult bone marrow. Leukemia 20: 857-869.
84. Kumar AA, Kumar SR, Narayanan R, Arul K, Baskaran M (2009) Autologous bone marrow derived mononuclear cell therapy for spinal cord injury: A phase I/II clinical safety and primary efficacy data. Exp Clin Transplant 7: 241-248.
85. Kurozumi K, Nakamura K, Tamiya T, Kawano Y, Kobune M, Hirai S, Uchida H, Sasaki K, Ito Y, Kato K, Honmou O, Houkin K, Date I, Hamada H (2004) BDNF gene- modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol Ther 9: 189-197.
86. Le Blanc K, Ringdén O (2007) Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 262: 509-525.
87. Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY; STARTING collaborators (2010) A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 28: 1099-1106.
88. Lee KH, Suh-Kim H, Choi JS, Jeun SS, Kim EJ, Kim SS, Yoon do H, Lee BH (2007) Human mesenchymal stem cell transplantation promotes functional recovery following acute spinal cord injury in rats. Acta Neurobiol Exp (Wars) 67: 13-22.
89. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH (2004) Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103: 1669-1675.
90. Lee PH, Kim JW, Bang OY, Ahn YH, Joo IS, Huh K (2008) Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin Pharmacol Ther 83: 723-730.
91. Lee PH, Lee JE, Kim HS, Song SK, Lee HS, Nam HS, Cheong JW, Jeong Y, Park HJ, Kim DJ, Nam CM, Lee JD, Kim HO, Sohn YH (2012) A randomized trial of mesenchymal stem cells in multiple system atrophy. Ann Neurol 72: 32-40.
92. Lescaudron L, Unni D, Dunbar GL (2003) 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.
93. Li J, Zhu H, Liu Y, Li Q, Lu S, Feng M, Xu Y, Huang L, Maan Y, Zhao RC, Wang R, Qin C (2010) Human mesenchymal stem cell transplantation protects against cerebral ischemic injury and upregulates interleukin-10 expression in Macacafascicularis. Brain Res 1334: 65-72.
94. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A, Widner H, Revesz T, Lindvall O, Brundin P (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14: 501-503.
95. Li M, Yu A, Zhang F, Dai G, Cheng H, Wang X, An Y (2012) Treatment of one case of cerebral palsy combined with posterior visual pathway injury using autologous bone marrow mesenchymal stem cells. J Transl Med 10: 100.
96. Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M (2002) Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59: 514-523.
97. Lindvall O, Kokaia Z, Martinez-Serrano A (2004) Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 10 (Suppl): S42-50.
98. Loebinger MR, Eddaoudi A, Davies D, Janes SM (2009) Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res 69: 4134-4142.
99. Locke M, Windsor J, Dunbar PR (2009) Human adipose- derived stem cells: isolation, characterization and applications in surgery. ANZ J Surg 79: 235-244.
100. Lu P, Blesch A., Tuszynski MH (2004) Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J Neurosci Res 77: 174-191.
101. Lundberg J, Södersten E, Sundström E, Le Blanc K, Andersson T, Hermanson O, Holmin S (2012) Targeted intra-arterial transplantation of stem cells to the injured CNS is more effective than intravenous administration: engraftment is dependent on cell type and adhesion mol- ecule expression. Cell Transplant 21: 333-343.
102. Markert CD, Atala A, Cann JK, Christ G, Furth M, Ambrosio F, Childers MK (2009) Mesenchymal stem cells: emerging therapy for Duchenne muscular dystrophy. PM R 1: 547-559.
103. Martinez HR, Gonzalez-Garza MT, Moreno-Cuevas JE, Caro E, Gutierrez-Jimenez E, Segura JJ (2009) Stem-cell transplantation into the frontal motor cortex in amyotrophic lateral sclerosis patients. Cytotherapy 11: 26-34.
104. Mazzini L, Mareschi K, Ferrero I, Vassallo E, Oliveri G, Nasuelli N, Oggioni GD, Testa L, Fagioli F (2008) Stem cell treatment in Amyotrophic Lateral Sclerosis. J Neurol Sci 265: 78-83.
105. Mazzini L, Ferrero I, Luparello V, Rustichelli D, Gunetti M, Mareschi K, Testa L, Stecco A, Tarletti R, Miglioretti M, Fava E, Nasuelli N, Cisari C, Massara M, Vercelli R, Oggioni GD, Carriero A, Cantello R, Monaco F, Fagioli F (2010) Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A Phase I clinical trial. Exp Neurol 223: 229-237.
106. Mazzini L, Mareschi K, Ferrero I, Miglioretti M, Stecco A, Servo S, Carriero A, Monaco F, Fagioli F (2012) Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study. Cytotherapy 14: 56-60.
107. Miller RH, Bai L, Lennon DP, Caplan AI (2010) The potential of mesenchymal stem cells for neural repair. Discov Med 9: 236-242.
108. Minguell JJ, Fierro FA, Epunan MJ, Erices AA, Sierralta WD (2005) Nonstimulated human uncommitted mesenchymal stem cells express cell markers of mesenchymal and neural lineages. Stem Cells Dev 14: 408-414.
109. Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, Seo BM, Sonoyama W, Zheng JJ, Baker CC, Chen W, Ried T, Shi S (2006) Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 24: 1095-1103.
110. Mohyeddin Bonab M, Yazdanbakhsh S, Lotfi J, Alimoghaddom K, Talebian F, Hooshmand F, Ghavamzadeh A, Nikbin B (2007) Does mesenchymal stem cell therapy help multiple sclerosis patients? Report of a pilot study. Iran J Immunol 4: 50-57.
111. Momin EN, Mohyeldin A, Zaidi HA, Vela G, Quiñones- Hinojosa A (2010) Mesenchymal stem cells: new approaches for the treatment of neurological diseases. Curr Stem Cell Res Ther 5: 326-344.
112. Moviglia GA, Varela G, Brizuela JA, Moviglia Brandolino MT, Farina P, Etchegaray G, Piccone S, Hirsch J, Martinez G, Marino S, Deffain S, Coria N, Gonzáles A, Sztanko M, Salas-Zamora P, Previgliano I, Aingel V, Farias J, Gaeta CA, Saslavsky J, Blasseti N (2009) Case report on the clinical results of a combined cellular therapy for chronic spinal cord injured patients. Spinal Cord 47: 499-503.
113. Nakamizo A, Marini F, Amano T, Khan A, Studeny M, Gumin J, Chen J, Hentschel S, Vecil G, Dembinski J, Andreeff M, Lang FF (2005) Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 65: 3307-3318.
114. Nakamura K, Ito Y, Kawano Y, Kurozumi K, Kobune M, Tsuda H, Bizen A, Honmou O, Niitsu Y, Hamada H (2004) Antitumor effect of genetically engineered mesenchymal stem cells in a rat glioma model. Gene Ther 11: 1155-1164.
115. Nakayama T, Momoki-Soga T, Inoue N (2003) Astrocyte- derived factors instruct differentiation of embryonic stem cells into neurons. Neurosci Res 46: 241-249.
116. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506.
117. Neuhuber B, Gallo G, Howard L, Kostura L, Mackay A, Fischer I (2004) Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype. J Neurosci Res 77: 192-204.
118. Newman RE, Yoo D, LeRoux MA, Danilkovitch-Miagkova A (2009) Treatment of inflammatory diseases with mesenchymal stem cells. Inflamm Allergy Drug Targets 8: 110-123.
119. Nomura T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD (2005) I.V infusion of brain-derived neu- rotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience 136: 161-169.
120. Nikolic WV, Hou H, Town T, Zhu Y, Giunta B, Sanberg CD, Zeng J, Luo D, Ehrhart J, Mori T, Sanberg PR, Tan J, Peripherally administered human umbilical cord blood cells reduce parenchymal and vascular beta-amyloid deposits in Alzheimer mice. Stem Cells Dev 17: 423-439.
121. Olson SD, Pollock K, Kambal A, Cary W, Mitchell GM, Tempkin J, Stewart H, McGee J, Bauer G, Kim HS, Tempkin T, Wheelock V, Annett G, Dunbar G, Nolta JA (2012) Genetically engineered mesenchymal stem cells as a proposed therapeutic for Huntington's disease. Mol Neurobiol 45: 87-98.
122. Onda T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD (2008) Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 28: 329-340.
123. Osanai T, Kuroda S, Sugiyama T, Kawabori M, Ito M, Shichinohe H, Kuge Y, Houkin K, Tamaki N, Iwasaki Y, Therapeutic effects of intra-arterial delivery of bone marrow stromal cells in traumatic brain injury of rats - in vivo cell tracking study by near-infrared fluorescence imaging. Neurosurgery 70: 435-444.
124. Pal R, Venkataramana NK, Bansal A, Balaraju S, Jan M, Chandra R, Dixit A, Rauthan A, Murgod U, Totey S, Ex vivo-expanded autologous bone marrow-derived mesenchymal stromal cells in human spinal cord injury/paraplegia: a pilot clinical study. Cytotherapy 11: 897-911.
125. Park JH, Kim DY, Sung IY, Choi GH, Jeon MH, Kim KK, Jeon SR (2012) Long-term results of spinal cord injury therapy using mesenchymal stem cells derived from bone marrow in humans. Neurosurgery 70: 1238-1247.
126. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M (2008) Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarct- ed myocardium. Cardiovasc Res 77: 134-142.
127. Pendharkar AV, Chua JY, Andres RH, Wang N, Gaeta X, Wang H, De A, Choi R, Chen S, Rutt BK, Gambhir SS, Guzman R (2010) Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke 41: 2064-2070.
128. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
129. Ponte AL, Marais E, Gallay N, Langonné A, Delorme B, Herault O, Charbord P, Domenech J (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25: 1737-1745.
130. Suzuki K, Sun R, Origuchi M, Kanehira M, Takahata T, Itoh J, Umezawa A, Kijima H, Fukuda S, Saijo Y (2011) Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization. Mol Med 17: 579-587.
131. Qiao L, Xu Z, Zhao T, Zhao Z, Shi M, Zhao RC, Ye L, Zhang X (2008) Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res 18: 500-507.
132. Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, Lee HY, Kim YJ, Jo JY, Yoon EJ, Choi HJ, Kwon E (2011) Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev 20: 1297-1308.
133. Sadan O, Shemesh N, Barzilay R, Dadon-Nahum M, Blumenfeld-Katzir T, Assaf Y, Yeshurun M, Djaldetti R, Cohen Y, Melamed E, Offen D (2012) Mesenchymal stem cells induced to secrete neurotrophic factors attenuate quinolinic acid toxicity: a potential therapy for Huntington's disease. Exp Neurol 234: 417-427.
134. Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR (2000) Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164: 247-256.
135. Santagati F, Rijli FM (2003) Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4: 806-818.
136. Schinkothe T, Bloch W, Schmidt A (2008) In vitro secreting profile of human mesenchymal stem cells. Stem Cells Dev 17: 199-206.
137. Schorey JS, Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9: 871-881.
138. Sheikh AM, Nagai A, Wakabayashi K, Narantuya D, Kobayashi S, Yamaguchi S, Kim SU (2011) Mesenchymal stem cell transplantation modulates neuroinflammation in focal cerebral ischemia: contribution of fractalkine and IL-5. Neurobiol Dis 41: 717-724.
139. Spaeth EL, Kidd S, Marini FC (2012) Tracking inflammation-induced mobilization of mesenchymal stem cells. Methods Mol Biol 904: 173-190.
140. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta (2008) Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood 111: 1327-1333.
141. Storch A, Schwarz J (2002) Neural stem cells and Parkinson's disease. J Neurol 249 (Suppl 3): III/30-32.
142. Sun W, Buzanska L, Domanska-Janik K, Salvi R.J, Stachowiak MK (2005) Voltage-sensitive and ligand- gated channels in differentiating neural stem-like cells derived from the nonhematopoietic fraction of human umbilical cord blood. Stem Cells 23: 931-945.
143. Suzuki K, Sun R, Origuchi M, Kanehira M, Takahata T, Itoh J, Umezawa A, Kijima H, Fukuda S, Saijo Y (2011) Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization. Mol Med 17: 579-587.
144. Sykova E, Homola A, Mazanec R, Lachmann H, Konradova SL, Kobylka P, Padr
145. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, Nishikawa S (2007) Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129: 1377-1388.
146. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW, Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 16: 542-545.
147. Tondreau T, Lagneaux L, Dejeneffe M, Massy M, Mortier Ch, Delforge A, Bron D (2004) Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 72: 319-326.
148. Toyama K, Honmou O, Harada K, Suzuki J, Houkin K, Hamada H, Kocsis JD (2009) Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp Neurol 216: 47-55.
149. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC, Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75: 389-397.
150. Uccelli A, Milanese M, Principato MC, Morando S, Bonifacino T, Vergani L, Giunti D, Voci A, Carminati E, Giribaldi F, Caponnetto C, Bonanno G (2012) Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol Med 18: 794-804.
151. Uccelli A, Benvenuto F, Laroni A, Giunti D (2011) Neuroprotective features of mesenchymal stem cells. Best Pract Res Clin Haematol 24: 59-64.
152. Venkataramana NK, Kumar SK, Balaraju S, Radhakrishnan RC, Bansal A, Dixit A, Rao DK, Das M, Jan M, Gupta PK, Totey SM (2010) Open-labeled study of unilateral autologous bone marrow-derived mesenchymal stem cell transplantation in Parkinson's disease. Transl Res 155: 62-70.
153. Wakabayashi K, Nagai A, Sheikh AM, Shiota Y, Narantuya Watanabe T, Masuda J, Kobayashi S, Kim SU, Yamaguchi S (2010) Transplantation of human mesenchymal stem cells promotes functional improvement and increased expression of neurotrophic factors in a rat focal cerebral ischemia model. J Neurosci Res 88: 1017-1025.
154. Wang Y, Deng Y, Zhou GQ (2008) SDF-1alpha/CXCR4- mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res 1195: 104-112.
155. Wen Z, Zheng S, Zhou C, Wang J, Wang T (2011) Repair mechanisms of bone marrow mesenchymal stem cells in myocardial infarction. J Cell Mol Med 15: 1032-1043.
156. Woodbury D, Schwarz EJ, Prockop DJ, Black IB (2000) Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61: 364-370.
157. Yamout B, Hourani R, Salti H, Barada W, El-Hajj T, Al-Kutoubi A, Herlopian A, Baz EK, Mahfouz R, Khalil- Hamdan R, Kreidieh NM, El-Sabban M, Bazarbachi A, Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study. J Neuroimmunol 227: 185-189
158. Yang SH, Park MJ, Yoon IH, Kim SY, Hong SH, Shin JY, Nam HY, Kim YH, Kim B, Park CG (2009) Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Exp Mol Med 41: 315-324.
159. Ying QL, Nichols J, Evans EP, Smith AG (2002) Changing potency by spontaneous fusion. Nature 416: 545-548.
160. Yoon SH, Shim YS, Park YH, Chung JK, Nam JH, Kim MO, Park HC, Park SR, Min BH, Kim EY, Choi BH, Park H, Ha Y (2007) Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage-colony stimulating factor: Phase I/II clinical trial. Stem Cells 25: 2066-2073.
161. Yu J, Li M, Qu Z, Yan D, Li D, Ruan Q (2010) SDF-1/ CXCR4-mediated migration of transplanted bone marrow stromal cells toward areas of heart myocardial infarction through activation of PI3K/Akt. J Cardiovasc Pharmacol 55: 496-505.
162. Zebardast N, Lickorish D, Davies JE (2010) Human umbilical cord perivascular cells (HUCPVC): A mesenchymal cell source for dermal wound healing. Organogenesis 6: 197-203.
163. Zeitouni S, Ford BS, Harris SM, Whitney MJ, Gregory CA, Prockop DJ (2008) Pharmaceutical induction of ApoE secretion by multipotent mesenchymal stromal cells (MSCs). BMC Biotechnol 8: 75.
164. Zhang ZX, Guan LX, Zhang K, Zhang Q, Dai LJ (2008) A combined procedure to deliver autologous mesenchymal stromal cells to patients with traumatic brain injury. Cytotherapy 10: 134-139.
165. Zolochevska O, Yu G, Gimble JM, Figueiredo ML (2012) Pigment epithelial-derived factor and melanoma differentiation associated gene-7 cytokine gene therapies delivered by adipose-derived stromal/mesenchymal stem cells are effective in reducing prostate cancer cell growth. Stem Cells Dev 21: 1112-1123.
166. Zychowicz M, Mehn D, Ruiz A, Frontczak-Baniewicz M, Rossi F, Buzanska L (2012) Patterning of human cord blood-derived stem cells on single cell posts and lines: Implications for neural commitment. Acta Neurobiol Exp (Wars) 72: 325-336.