Towards clinical application of mesenchymal stem cells for treatment of neurological diseases of the central nervous system

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 5, 2013, Pages 1062-1076

  Laroni, Alice ^a   Novi, Giovanni ^a   De Rosbo, Nicole Kerlero ^a,b   Uccelli, Antonio ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b Advanced Biotechnology Center ABC   (Italy)

Author keywords

Alzheimer's disease; Amyotrophic lateral sclerosis; Brain ischemia; Mesenchymal stem cells; Multiple sclerosis; Multiple system atrophy; Neurological diseases; Parkinson's disease; Spinal cord injury; Stroke

Indexed keywords

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROVASCULAR ACCIDENT; HUMAN; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPLE SCLEROSIS; PARKINSON DISEASE; PATIENT SAFETY; PRIORITY JOURNAL; REVIEW; SHY DRAGER SYNDROME; SPINAL CORD INJURY;

ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION;

EID: 84891373674     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-013-9456-6     Document Type: Review

References (126)

1. Akiyama Y, Radtke C, Honmou O, Kocsis JD (2002) Remyelination of the spinal cord following intravenous delivery of bone marrow cells. Glia 39(3):229-236. doi: 10.1002/glia.10102
2. Andrews EM, Tsai SY, Johnson SC, Farrer JR, Wagner JP, Kopen GC, Kartje GL (2008) Human adult bone marrow-derived somatic cell therapy results in functional recovery and axonal plasticity following stroke in the rat. Exp Neurol 211(2):588-592. doi: 10.1016/j.expneurol.2008.02.027
3. Babaei P, Soltani Tehrani B, Alizadeh A (2012) Transplanted bone marrow mesenchymal stem cells improve memory in rat models of Alzheimer's disease. Stem Cells Int 2012:369417. doi: 10.1155/2012/369417
4. Bae JS, Jin HK, Richardson JC, Carter JE (2012) Bone marrow-derived mesenchymal stem cells contribute to the reduction of amyloid-beta deposits and the improvement of synaptic transmission in a mouse model of pre-dementia Alzheimer's disease. Curr Alzheimer Res
5. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, Miller SD, Miller RH (2009) Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 57(11):1192-1203. doi: 10.1002/glia.20841
6. Bai L, Lennon DP, Caplan AI, Dechant A, Hecker J, Kranso J, Zaremba A, Miller RH (2012) Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci. doi: 10.1038/nn.3109
7. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer's disease. Lancet 377(9770):1019-1031. doi: 10.1016/S0140-6736(10) 61349-9
8. Bang OY, Lee JS, Lee PH, Lee G (2005) Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 57(6):874-882
9. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30(1):42-48
10. Barzilay R, Kan I, Ben-Zur T, Bulvik S, Melamed E, Offen D (2008) Induction of human mesenchymal stem cells into dopamine-producing cells with different differentiation protocols. Stem Cells Dev 17(3):547-554. doi: 10.1089/scd.2007.0172
11. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ (2010) Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 133(2):433-447. doi: 10.1093/brain/awp322
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 1(1):93-104. doi: 10.1159/000333381
13. Bonab MM, Sahraian MA, Aghsaie A, Karvigh SA, Hosseinian SM, Nikbin B, Lotfi J, Khorramnia S, Motamed MR, Togha M, Harirchian MH, Moghadam NB, Alikhani K, Yadegari S, Jafarian S, Gheini MR (2012) Autologous mesenchymal stem cell therapy in progressive multiple sclerosis: an open label study. Curr Stem Cell Res Ther
14. Boucherie C, Schafer S, Lavand'homme P, Maloteaux JM, Hermans E (2009) Chimerization of astroglial population in the lumbar spinal cord after mesenchymal stem cell transplantation prolongs survival in a rat model of amyotrophic lateral sclerosis. J Neurosci Res 87(9):2034-2046. doi: 10.1002/jnr.22038
15. Bouchez G, Sensebe L, Vourc'h P, Garreau L, Bodard S, Rico A, Guilloteau D, Charbord P, Besnard JC, Chalon S (2008) Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease. Neurochem Int 52(7):1332-1342. doi: 10.1016/j.neuint.2008. 02.003
16. Braak H, Del Tredici K (2008) Invited article: nervous system pathology in sporadic Parkinson disease. Neurology 70(20):1916-1925. doi: 10.1212/01.wnl.0000312279.49272.9f
17. Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98(5):1076-1084. doi: 10.1002/jcb.20886
18. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, Chopp M (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32(4):1005-1011
19. Chiesa S, Morbelli S, Morando S, Massollo M, Marini C, Bertoni A, Frassoni F, Bartolome ST, Sambuceti G, Traggiai E, Uccelli A (2011) Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci U S A 108(42):17384-17389. doi: 10.1073/pnas.1103650108
20. Connick P, Kolappan M, Patani R, Scott MA, Crawley C, He XL, Richardson K, Barber K, Webber DJ, Wheeler-Kingshott CA, Tozer DJ, Samson RS, Thomas DL, Du MQ, Luan SL, Michell AW, Altmann DR, Thompson AJ, Miller DH, Compston A, Chandran S (2011) The mesenchymal stem cells in multiple sclerosis (MSCIMS) trial protocol and baseline cohort characteristics: an open-label pre-test: post-test study with blinded outcome assessments. Trials 12:62. doi: 10.1186/1745-6215-12-62
21. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, Gini B, Bach SD, Martinello M, Bifari F, Galie M, Turano E, Budui S, Sbarbati A, Krampera M, Bonetti B (2009) Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27(10):2624-2635. doi: 10.1002/stem.194
22. de Vasconcelos dos Santos A, da Costa Reis J, Diaz Paredes B, Moraes L, Jasmin, Giraldi-Guimarães A, Mendez-Otero R (2010) Therapeutic window for treatment of cortical ischemia with bone marrow-derived cells in rats. Brain Res 1306:149-158. doi: 10.1016/j.brainres.2009.09.094
23. Dezawa M, Kanno H, Hoshino M, Cho H, Matsumoto N, Itokazu Y, Tajima N, Yamada H, Sawada H, Ishikawa H, Mimura T, Kitada M, Suzuki Y, Ide C (2004) Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J Clin Invest 113(12):1701-1710. doi: 10.1172/JCI20935
24. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99(10):3838-3843
25. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D, Jorgensen C (2003) Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102(10):3837-3844
26. Dongmei H, Jing L, Mei X, Ling Z, Hongmin Y, Zhidong W, Li D, Zikuan G, Hengxiang W (2011) Clinical analysis of the treatment of spinocerebellar ataxia and multiple system atrophy-cerebellar type with umbilical cord mesenchymal stromal cells. Cytotherapy 13(8):913-917. doi: 10.3109/14653249.2011.579958
27. Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J (2005) Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106(13):4057-4065
28. 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(9):1036-1046. doi: 10.3109/14653249.2011. 592521
29. Forslöw U, Blennow O, LeBlanc K, Ringdén O, Gustafsson B, Mattsson J, Remberger M (2012) Treatment with mesenchymal stromal cells is a risk factor for pneumonia-related death after allogeneic hematopoietic stem cell transplantation. Eur J Haematol 89(3):220-227. doi: 10.1111/j.1600-0609.2012. 01824.x
30. Fouillard L, Bensidhoum M, Bories D, Bonte H, Lopez M, Moseley AM, Smith A, Lesage S, Beaujean F, Thierry D, Gourmelon P, Najman A, Gorin NC (2003) Engraftment of allogeneic mesenchymal stem cells in the bone marrow of a patient with severe idiopathic aplastic anemia improves stroma. Leukemia 17(2):474-476. doi: 10.1038/sj.leu.2402786
31. Freedman MS, Bar-Or A, Atkins HL, Karussis D, Frassoni F, Lazarus H, Scolding N, Slavin S, Le Blanc K, Uccelli A (2010) The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: consensus report of the International MSCT Study Group. Mult Scler 16(4):503-510. doi: 10.1177/1352458509359727
32. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV (1974) Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17(4):331-340
33. Gandhi R, Laroni A, Weiner HL (2010) Role of the innate immune system in the pathogenesis of multiple sclerosis. J Neuroimmunol 221(1-2):7-14. doi: 10.1016/j.jneuroim.2009.10.015
34. 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(3):219-227
35. Glavaski-Joksimovic A, Virag T, Mangatu TA, McGrogan M, Wang XS, Bohn MC (2010) Glial cell line-derived neurotrophic factor-secreting genetically modified human bone marrow-derived mesenchymal stem cells promote recovery in a rat model of Parkinson's disease. J Neurosci Res 88(12):2669-2681. doi: 10.1002/jnr.22435
36. Gordon D, Pavlovska G, Glover CP, Uney JB, Wraith D, Scolding NJ (2008) Human mesenchymal stem cells abrogate experimental allergic encephalomyelitis after intraperitoneal injection, and with sparse CNS infiltration. Neurosci Lett 448(1):71-73. doi: 10.1016/j.neulet.2008.10.040
37. Grigoriadis N, Lourbopoulos A, Lagoudaki R, Frischer JM, Polyzoidou E, Touloumi O, Simeonidou C, Deretzi G, Kountouras J, Spandou E, Kotta K, Karkavelas G, Tascos N, Lassmann H (2011) Variable behavior and complications of autologous bone marrow mesenchymal stem cells transplanted in experimental autoimmune encephalomyelitis. Exp Neurol 230(1):78-89. doi: 10.1016/j.expneurol. 2011.02.021
38. Gutiérrez-Fernández M, Rodríguez-Frutos B, Álvarez-Grech J, Vallejo-Cremades MT, Expósito-Alcaide M, Merino J, Roda JM, Díez-Tejedor E (2011) Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience 175:394-405. doi: 10.1016/j.neuroscience.2010.11.054
39. Hawryluk GW, Mothe A, Wang J, Wang S, Tator C, Fehlings MG (2012) An in vivo characterization of trophic factor production following neural precursor cell or bone marrow stromal cell transplantation for spinal cord injury. Stem Cells Dev 21(12):2222-2238. doi: 10.1089/scd.2011.0596
40. Hayashi T, Wakao S, Kitada M, Ose T, Watabe H, Kuroda Y, Mitsunaga K, Matsuse D, Shigemoto T, Ito A, Ikeda H, Fukuyama H, Onoe H, Tabata Y, Dezawa M (2013) Autologous mesenchymal stem cell-derived dopaminergic neurons function in parkinsonian macaques. J Clin Investig 123(1):272-284. doi: 10.1172/jci62516
41. 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(6):1790-1807. doi: 10.1093/brain/awr063
42. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5(3):309-313
43. Hughes V (2011) A raw nerve. Nat Med 17(11):1333-1335. doi: 10.1038/nm1111-1333
44. Inoue M, Honmou O, Oka S, Houkin K, Hashi K, Kocsis JD (2003) Comparative analysis of remyelinating potential of focal and intravenous administration of autologous bone marrow cells into the rat demyelinated spinal cord. Glia 44(2):111-118. doi: 10.1002/glia.10285
45. Jeong SR, Park JH, Lee JH, Kim DY, Kim HS, Sung GIY, Jeon MH, Gook G (2010) Treatment of spinal cord injury with bone marrow-derived, cultured autologous mesenchymal stem cells. Tissue Eng Regen Med 7(3):316-322. doi: 10.3345/kjp.2010.7.3.316
46. Jin HK, Bae JS, Furuya S, Carter JE (2009) Amyloid beta-derived neuroplasticity in bone marrow-derived mesenchymal stem cells is mediated by NPY and 5-HT2B receptors via ERK1/2 signalling pathways. Cell Prolif 42(5):571-586. doi: 10.1111/j.1365-2184.2009.00625.x
47. Kang SK, Lee DH, Bae YC, Kim HK, Baik SY, Jung JS (2003) Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol 183(2):355-366. doi: 10.1016/S0014-4886(03)00089-X
48. 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(10):1187-1194. doi: 10.1001/archneurol.2010.248
49. 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(6):753-761. doi: 10.1001/archneur.65.6.753
50. Kim YJ, Park HJ, Lee G, Bang OY, Ahn YH, Joe E, Kim HO, Lee PH (2009) Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action. Glia 57(1):13-23. doi: 10.1002/glia.20731
51. Kim H, Kim HY, Choi MR, Hwang S, Nam KH, Kim HC, Han JS, Kim KS, Yoon HS, Kim SH (2010) Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice. Neurosci Lett 468(3):190-194. doi: 10.1016/j.neulet.2009.10.074
52. Kim JY, Kim DH, Kim JH, Lee D, Jeon HB, Kwon SJ, Kim SM, Yoo YJ, Lee EH, Choi SJ, Seo SW, Lee JI, Na DL, Yang YS, Oh W, Chang JW (2012) Soluble intracellular adhesion molecule-1 secreted by human umbilical cord blood-derived mesenchymal stem cell reduces amyloid-beta plaques. Cell Death Differ 19(4):680-691. doi: 10.1038/cdd.2011.140
53. Koc ON, Gerson SL, Cooper BW, Dyhouse SM, Haynesworth SE, Caplan AI, Lazarus HM (2000) Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol 18(2):307-316
54. Koc ON, Day J, Nieder M, Gerson SL, Lazarus HM, Krivit W (2002) Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant 30(4):215-222
55. Komatsu K, Honmou O, Suzuki J, Houkin K, Hamada H, Kocsis JD (2010) Therapeutic time window of mesenchymal stem cells derived from bone marrow after cerebral ischemia. Brain Res 1334:84-92. doi: 10.1016/j.brainres.2010.04.006
56. Lanz TV, Opitz CA, Ho PP, Agrawal A, Lutz C, Weller M, Mellor AL, Steinman L, Wick W, Platten M (2010) Mouse mesenchymal stem cells suppress antigen-specific TH cell immunity independent of indoleamine 2,3-dioxygenase 1 (IDO1). Stem Cells Dev 19(5):657-668. doi: 10.1089/scd.2009.0385
57. Lanza C, Morando S, Voci A, Canesi L, Principato MC, Serpero LD, Mancardi G, Uccelli A, Vergani L (2009) Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo. J Neurochem 110(5):1674-1684. doi: 10.1111/j.1471-4159.2009.06268.x
58. Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI (1995) Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant 16(4):557-564
59. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W, Ringden O (2008) Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371(9624):1579-1586
60. Lee ST, Jang JH, Cheong JW, Kim JS, Maemg HY, Hahn JS, Ko YW, Min YH (2002) Treatment of high-risk acute myelogenous leukaemia by myeloablative chemoradiotherapy followed by co-infusion of T cell-depleted haematopoietic stem cells and culture-expanded marrow mesenchymal stem cells from a related donor with one fully mismatched human leucocyte antigen haplotype. Br J Haematol 118(4):1128-1131
61. 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(5):723-730. doi: 10.1038/sj.clpt.6100386
62. Lee ES, Chan J, Shuter B, Tan LG, Chong MS, Ramachandra DL, Dawe GS, Ding J, Teoh SH, Beuf O, Briguet A, Tam KC, Choolani M, Wang SC (2009a) Microgel iron oxide nanoparticles for tracking human fetal mesenchymal stem cells through magnetic resonance imaging. Stem Cells 27(8):1921-1931. doi: 10.1002/stem.112
63. Lee JK, Jin HK, Bae JS (2009b) Bone marrow-derived mesenchymal stem cells reduce brain amyloid-beta deposition and accelerate the activation of microglia in an acutely induced Alzheimer's disease mouse model. Neurosci Lett 450(2):136-141. doi: 10.1016/j.neulet.2008.11.059
64. Lee HJ, Lee JK, Lee H, Shin JW, Carter JE, Sakamoto T, Jin HK, Bae JS (2010a) The therapeutic potential of human umbilical cord blood-derived mesenchymal stem cells in Alzheimer's disease. Neurosci Lett 481(1):30-35. doi: 10.1016/j.neulet.2010.06.045
65. Lee JK, Jin HK, Endo S, Schuchman EH, Carter JE, Bae JS (2010b) Intracerebral transplantation of bone marrow-derived mesenchymal stem cells reduces amyloid-beta deposition and rescues memory deficits in Alzheimer's disease mice by modulation of immune responses. Stem Cells 28(2):329-343. doi: 10.1002/stem.277
66. Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY (2010c) A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 28(6):1099-1106. doi: 10.1002/stem.430
67. Lee HJ, Lee JK, Lee H, Carter JE, Chang JW, Oh W, Yang YS, Suh JG, Lee BH, Jin HK, Bae JS (2012a) Human umbilical cord blood-derived mesenchymal stem cells improve neuropathology and cognitive impairment in an Alzheimer's disease mouse model through modulation of neuroinflammation. Neurobiol Aging 33(3):588-602. doi: 10.1016/j.neurobiolaging.2010.03.024
68. Lee JK, Schuchman EH, Jin HK, Bae J-S (2012b) Soluble CCL5 derived from bone marrow-derived mesenchymal stem cells and activated by amyloid β ameliorates Alzheimer's disease in mice by recruiting bone marrow-induced microglia immune responses. Stem Cells 30(7):1544-1555. doi: 10.1002/stem.1125
69. 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 (2012c) A randomized trial of mesenchymal stem cells in multiple system atrophy. Ann Neurol 72(1):32-40. doi: 10.1002/ana.23612
70. Levy YS, Bahat-Stroomza M, Barzilay R, Burshtein A, Bulvik S, Barhum Y, Panet H, Melamed E, Offen D (2008) Regenerative effect of neural-induced human mesenchymal stromal cells in rat models of Parkinson's disease. Cytotherapy 10(4):340-352. doi: 10.1080/14653240802021330
71. Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX, Zhang Z (2000) Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 20(9):1311-1319. doi: 10.1097/00004647-200009000-00006
72. Li Y, Chen J, Wang L, Lu M, Chopp M (2001) Treatment of stroke in rat with intracarotid administration of marrow stromal cells. Neurology 56(12):1666-1672
73. 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(4):514-523
74. Lu L, Zhao C, Liu Y, Sun X, Duan C, Ji M, Zhao H, Xu Q, Yang H (2005) Therapeutic benefit of TH-engineered mesenchymal stem cells for Parkinson's disease. Brain Res Brain Res Protocol 15(1):46-51. doi: 10.1016/j.brainresprot. 2005.03.002
75. Lucchini G, Dander E, Pavan F, Di Ceglie I, Balduzzi A, Perseghin P, Gaipa G, Algarotti A, Introna M, Rambaldi A, Rovelli A, Biondi A, Biagi E, D'Amico G (2012) Mesenchymal stromal cells do not increase the risk of viral reactivation nor the severity of viral events in recipients of allogeneic stem cell transplantation. Stem Cells Int 2012:690236. doi: 10.1155/2012/690236
76. 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(1-2):78-83. doi: 10.1016/j.jns.2007.05.016
77. 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(1):229-237. doi: 10.1016/j.expneurol. 2009.08.007
78. 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(1):56-60. doi: 10.3109/14653249.2011.613929
79. Meirelles LDS, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119(11):2204-2213
80. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829-834. doi: 10.1038/nature09262
81. 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(1):50-57
82. Moloney TC, Rooney GE, Barry FP, Howard L, Dowd E (2010) Potential of rat bone marrow-derived mesenchymal stem cells as vehicles for delivery of neurotrophins to the Parkinsonian rat brain. Brain Res 1359:33-43. doi: 10.1016/j.brainres.2010.08.040
83. Morando S, Vigo T, Esposito M, Casazza S, Novi G, Principato MC, Furlan R, Uccelli A (2012) The therapeutic effect of mesenchymal stem cell transplantation in experimental autoimmune encephalomyelitis is mediated by peripheral and central mechanisms. Stem Cell Res Ther 3(1):3. doi: 10.1186/scrt94
84. Morita E, Watanabe Y, Ishimoto M, Nakano T, Kitayama M, Yasui K, Fukada Y, Doi K, Karunaratne A, Murrell WG, Sutharsan R, Mackay-Sim A, Hata Y, Nakashima K (2008) A novel cell transplantation protocol and its application to an ALS mouse model. Exp Neurol 213(2):431-438. doi: 10.1016/j.expneurol.2008.07. 011
85. Mottaghi S, Larijani B, Sharifi AM (2013) Atorvastatin: an efficient step forward in mesenchymal stem cell therapy of diabetic retinopathy. Cytotherapy 15(3):263-266. doi: 10.1016/j.jcyt.2012.11.002
86. Offen D, Barhum Y, Levy YS, Burshtein A, Panet H, Cherlow T, Melamed E (2007) Intrastriatal transplantation of mouse bone marrow-derived stem cells improves motor behavior in a mouse model of Parkinson's disease. J Neural Transm Suppl 72:133-143
87. Pal R, Venkataramana NK, Bansal A, Balaraju S, Jan M, Chandra R, Dixit A, Rauthan A, Murgod U, Totey S (2009) Ex vivo-expanded autologous bone marrow-derived mesenchymal stromal cells in human spinal cord injury/paraplegia: a pilot clinical study. Cytotherapy 11(7):897-911. doi: 10.3109/ 14653240903253857
88. Park HJ, Lee PH, Bang OY, Lee G, Ahn YH (2008) Mesenchymal stem cells therapy exerts neuroprotection in a progressive animal model of Parkinson's disease. J Neurochem 107(1):141-151. doi: 10.1111/j.1471-4159.2008.05589.x
89. Park H-W, Lim M-J, Jung H, Lee S-P, Paik K-S, Chang M-S (2010) Human mesenchymal stem cell-derived Schwann cell-like cells exhibit neurotrophic effects, via distinct growth factor production, in a model of spinal cord injury. Glia 58(9):1118-1132. doi: 10.1002/glia.20992
90. Park HJ, Bang G, Lee BR, Kim HO, Lee PH (2011) Neuroprotective effect of human mesenchymal stem cells in an animal model of double toxin-induced multiple system atrophy parkinsonism. Cell Transplant 20(6):827-835. doi: 10.3727/096368910X540630
91. Pastor D, Viso-Leon MC, Jones J, Jaramillo-Merchan J, Toledo-Aral JJ, Moraleda JM, Martinez S (2011) Comparative effects between bone marrow and mesenchymal stem cell transplantation in GDNF expression and motor function recovery in a motorneuron degenerative mouse model. Stem Cell Rev. doi: 10.1007/s12015-011-9295-x
92. Paul C, Samdani AF, Betz RR, Fischer I, Neuhuber B (2009) Grafting of human bone marrow stromal cells into spinal cord injury: a comparison of delivery methods. Spine (Phila Pa 1976) 34(4):328-334. doi: 10.1097/BRS. 0b013e31819403ce
93. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309):71-74
94. Quertainmont R, Cantinieaux D, Botman O, Sid S, Schoenen J, Franzen R (2012) Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PLoS One 7(6):e39500
95. 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. doi: 10.1089/scd.2010.0466
96. Rafei M, Campeau PM, Aguilar-Mahecha A, Buchanan M, Williams P, Birman E, Yuan S, Young YK, Boivin MN, Forner K, Basik M, Galipeau J (2009) Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. J Immunol 182(10):5994-6002. doi: 10.4049/jimmunol.0803962
97. Saito F, Nakatani T, Iwase M, Maeda Y, Hirakawa A, Murao Y, Suzuki Y, Onodera R, Fukushima M, Ide C (2008) Spinal cord injury treatment with intrathecal autologous bone marrow stromal cell transplantation: the first clinical trial case report. J Trauma 64(1):53-59. doi: 10.1097/TA. 0b013e31815b847d
98. Saito F, Nakatani T, Iwase M, Maeda Y, Murao Y, Suzuki Y, Fukushima M, Ide C (2012) Administration of cultured autologous bone marrow stromal cells into cerebrospinal fluid in spinal injury patients: a pilot study. Restor Neurol Neurosci 30(2):127-136. doi: 10.3233/RNN-2011-0629
99. Sensebé L, Tarte K, Galipeau J, Krampera M, Martin I, Phinney Donald G, Shi Y (2012) Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Cell Stem Cell 10(1):9-10. doi: 10.1016/j.stem.2011.12.005
100. Shi D, Chen G, Lv L, Li L, Wei D, Gu P, Gao J, Miao Y, Hu W (2011) The effect of lentivirus-mediated TH and GDNF genetic engineering mesenchymal stem cells on Parkinson's disease rat model. Neurol Sci 32(1):41-51. doi: 10.1007/s10072-010-0385-3
101. Shintani A, Nakao N, Kakishita K, Itakura T (2007) Protection of dopamine neurons by bone marrow stromal cells. Brain Res 1186:48-55. doi: 10.1016/j.brainres.2007.09.086
102. Sospedra M, Martin R (2005) Immunology of multiple sclerosis. Annu Rev Immunol 23:683-747. doi: 10.1146/annurev.immunol.23.021704.115707
103. Stemberger S, Jamnig A, Stefanova N, Lepperdinger G, Reindl M, Wenning GK (2011) Mesenchymal stem cells in a transgenic mouse model of multiple system atrophy: immunomodulation and neuroprotection. PLoS One 6(5):e19808. doi: 10.1371/journal.pone.0019808
104. Suzuki M, McHugh J, Tork C, Shelley B, Hayes A, Bellantuono I, Aebischer P, Svendsen CN (2008) 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(12):2002-2010. doi: 10.1038/mt.2008.197
105. Thomas MG, Stone L, Evill L, Ong S, Ziman M, Hool L (2011) Bone marrow stromal cells as replacement cells for Parkinson's disease: generation of an anatomical but not functional neuronal phenotype. Transl Res 157(2):56-63. doi: 10.1016/j.trsl.2010.11.001
106. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, Xia L, Zhou N, Riddle M, Schroeder TM, Westendorf JJ, McIvor RS, Hogendoom PC, Szuhai K, Oseth L, Hirsch B, Yant SR, Kay MA, Peister A, Prockop DJ, Fibbe WE, Blazar BR (2006) Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25:371-379
107. Trzaska KA, Kuzhikandathil EV, Rameshwar P (2007) Specification of a dopaminergic phenotype from adult human mesenchymal stem cells. Stem Cells 25(11):2797-2808. doi: 10.1634/stemcells.2007-0212
108. Ubhi K, Low P, Masliah E (2011) Multiple system atrophy: a clinical and neuropathological perspective. Trends Neurosci 34(11):581-590. doi: 10.1016/j.tins.2011.08.003
109. Uccelli A, Prockop DJ (2010) Why should mesenchymal stem cells (MSCs) cure autoimmune diseases? Curr Opin Immunol 22(6):768-774. doi: 10.1016/j.coi.2010.10.012
110. Uccelli A, Moretta L, Pistoia V (2008) Mesenchymal stem cells in health and disease. Nat Rev Immunol 8(9):726-736
111. Uccelli A, Laroni A, Freedman MS (2011) Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol 10(7):649-656. doi: 10.1016/S1474-4422(11)70121-1
112. Uccelli A, Laroni A, Freedman MS (2012a) Mesenchymal stem cells as treatment for MS - progress to date. Mult Scler. doi: 10.1177/1352458512464686
113. Uccelli A, Milanese M, Principato MC, Morando S, Bonifacino T, Vergani L, Giunti D, Voci A, Carminati E, Giribaldi F, Caponnetto C, Bonanno G (2012b) Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol Med. doi: 10.2119/molmed.2011. 00498
114. van Velthoven CTJ, van de Looij Y, Kavelaars A, Zijlstra J, van Bel F, Huppi PS, Sizonenko S, Heijnen CJ (2012) Mesenchymal stem cells restore cortical rewiring after neonatal ischemia in mice. Ann Neurol 71(6):785-796. doi: 10.1002/ana.23543
115. 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(2):62-70. doi: 10.1016/j.trsl.2009.07.006
116. Vercelli A, Mereuta OM, Garbossa D, Muraca G, Mareschi K, Rustichelli D, Ferrero I, Mazzini L, Madon E, Fagioli F (2008) Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 31(3):395-405
117. Vilalta M, Degano IR, Bago J, Gould D, Santos M, Garcia-Arranz M, Ayats R, Fuster C, Chernajovsky Y, Garcia-Olmo D, Rubio N, Blanco J (2008) Biodistribution, long-term survival, and safety of human adipose tissue-derived mesenchymal stem cells transplanted in nude mice by high sensitivity non-invasive bioluminescence imaging. Stem Cells Dev 17(5):993-1003. doi: 10.1089/scd.2007.0201
118. Voulgari-Kokota A, Fairless R, Karamita M, Kyrargyri V, Tseveleki V, Evangelidou M, Delorme B, Charbord P, Diem R, Probert L (2012) Mesenchymal stem cells protect CNS neurons against glutamate excitotoxicity by inhibiting glutamate receptor expression and function. Exp Neurol 236(1):161-170. doi: 10.1016/j.expneurol.2012.04.011
119. Wright KT, El Masri W, Osman A, Chowdhury J, Johnson WE (2011) Concise review: bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 29(2):169-178. doi: 10.1002/stem.570
120. Yamout B, Hourani R, Salti H, Barada W, El-Hajj T, Al-Kutoubi A, Herlopian A, Baz EK, Mahfouz R, Khalil-Hamdan R, Kreidieh NMA, El-Sabban M, Bazarbachi A (2010) Bone marrow mesenchymal stem cell transplantation in patients with multiple sclerosis: a pilot study. J Neuroimmunol 227(1):185-189
121. Yoo SW, Kim SS, Lee SY, Lee HS, Kim HS, Lee YD, Suh-Kim H (2008) Mesenchymal stem cells promote proliferation of endogenous neural stem cells and survival of newborn cells in a rat stroke model. Exp Mol Med 40(4):387-397
122. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A (2005) Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T cell anergy. Blood 106(5):1755-1761
123. Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M (2005) Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 195(1):16-26
124. Zhang J, Li Y, Lu M, Cui Y, Chen J, Noffsinger L, Elias SB, Chopp M (2006) Bone marrow stromal cells reduce axonal loss in experimental autoimmune encephalomyelitis mice. J Neurosci Res 84(3):587-595
125. Zhao CP, Zhang C, Zhou SN, Xie YM, Wang YH, Huang H, Shang YC, Li WY, Zhou C, Yu MJ, Feng SW (2007) Human mesenchymal stromal cells ameliorate the phenotype of SOD1-G93A ALS mice. Cytotherapy 9(5):414-426. doi: 10.1080/14653240701376413
126. Zhao X, Liu L, Liu D, Fan H, Wang Y, Hu Y, Hou Y (2012) Progesterone enhances immunoregulatory activity of human mesenchymal stem cells via PGE2 and IL-6. Am J Reprod Immunol 68(4):290-300. doi: 10.1111/j.1600-0897.2012.01163.x