Stem cells therapy for ALS

Expert Opinion on Biological Therapy

Volumn 16, Issue 2, 2016, Pages 187-199

  Mazzini, Letizia ^a   Vescovi, Angelo ^b,c   Cantello, Roberto ^d   Gelati, Maurizio ^b,c   Vercelli, Alessandro ^e  

^a University Hospital Maggiore della Carita   (Italy)

^b CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^c Cell Factory e Biobanca   (Italy)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Neuroinflammation; Neuroprotection; Stem cell

Indexed keywords

NEUROTROPHIC FACTOR; AUTACOID;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CLINICAL TRIAL (TOPIC); HUMAN; META ANALYSIS (TOPIC); NONHUMAN; PERIPHERAL BLOOD STEM CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); STEM CELL TRANSPLANTATION; TRANSLATIONAL RESEARCH; ANIMAL; ANTAGONISTS AND INHIBITORS; GENE THERAPY; METABOLISM; NEURAL STEM CELL; PROCEDURES; QUALITY OF LIFE; TRANSPLANTATION; TRENDS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CLINICAL TRIALS AS TOPIC; GENETIC THERAPY; HUMANS; INFLAMMATION MEDIATORS; NEURAL STEM CELLS; QUALITY OF LIFE; STEM CELL TRANSPLANTATION;

EID: 84957949225     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2016.1116516     Document Type: Article

References (89)

1. Chiò A, Mora G, Calvo A, et al. On behalf of the PARALS epidemiology of ALS in Italy: a 10-year prospective population-based study. Neurology. 2009;72(8):725-731.
2. Marangi G, Traynor BJ. Genetic causes of amyotrophic lateral sclerosis: new genetic analysis methodologies entailing new opportunities and challenges. Brain Res. 2015;1607:75-93.
3. Turner MR, Bowser R, Bruijn L, et al. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:19-32.
4. Kang SH, Li Y, Fukaya M, et al. Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis. Nat Neurosci. 2013;16:571-579.
5. Boillée S, Koji Y, Lobsiger CS, et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006;312(5778):1389-1392.
6. Clement AM, Nguyen MD, Roberts EA, et al. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science. 2003;302(642):113-117.
7. Anneser JM, Chahli C, Ince PC, et al. Glial proliferation and metabotropic glutamate receptor expression in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 2004;63:831-840.
8. Weydt P, Yuen EC, Ransom BR, et al. Increased cytotoxic potential of microglia from ALS-transgenic mice. Glia. 2004;48:179-182.
9. Zhao W, Beers DR, Appel SH. Immune-mediated mechanisms in the pathoprogression of amyotrophic lateral sclerosis. J Neuroimmune Pharmacol. 2013;8(4):888-899.
10. Rodrigues MC, Sanberg PR, Cruz LE, et al. The innate and adaptive immunological aspects in neurodegenerative diseases. J Neuroimmunol. 2014;269(1-2):1-8.
11. Henkel JS, Engelhardt JI, Siklós L, et al. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol. 2004;55(2):221-235.
12. Bensimon G, Lacomblez L, Meininger V., the ALS/Riluzole Study Group. A controlled trial of riluzole in amyotrophic lateral sclerosis. N Engl J Med. 1994;330(9):585-591.
13. Goyal NA, Mozaffar T. Experimental trials in amyotrophic lateral sclerosis: a review of recently completed, ongoing and planned trials using existing and novel drugs. Expert Opin Investig Drugs. 2014;23(11):1541-1551.
14. Lindvall O, Kokaia Z. Stem cells in human neurodegenerative disorders-time for clinical translation? J Clin Invest. 2010;120(1):29-40.
15. Lee H, Shamy GA, Elkabetz Y, et al. Directed differentiation and transplantation of human embryonic stem cell derived motoneurons. Stem Cells. 2007;25:1931-1939.
16. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008;321:1218-122.
17. Ilieva H, Polymenidou M, Cleveland DW. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol. 2009;187(6):761-772.
18. Salminen A, Ojala J, Kaarniranta K, et al. Astrocytes in the aging brain express characteristics of senescence-associated secretory phenotype. Eur J Neurosci. 2011;34:3-11.
19. Chinta SJ, Lieu CA, Demaria M, et al. Environmental stress, ageing and glial cell senescence: a novel mechanistic link to Parkinson's disease? J Intern Med. 2013;273:429-436.
20. Dass MM, Svendsen CN. Astrocytes show reduced support of motor neurons with aging that is accelerated in a rodent model of ALS. Neurobiol Aging. 2015;36(2):1130-1139.
21. Lepore AC, Rauck B, Dejea C, et al. Focal transplantationbased astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci. 2008;11 (1):1294-1301.
22. Lepore AC. Human glial-restricted progenitor transplantation into cervical spinal cord of the SOD1G93A mouse model of ALS. PLoS One. 2011;6(10):1-17.
23. Nicaise C, Mitrecic D, Falnikar A, et al. Transplantation of stem cell-derived astrocytes for the treatment of amyotrophic lateral sclerosis and spinal cord injury. World J Stem Cells. 2015;7(2):380-398.
24. Beers DR, Henkel JS, Xiao Q, et al. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA. 2006;103(43):16021-16026.
25. Henriques A, Pitzer C, Schneider A. Neurotrophic growth factors for the treatment of amyotrophic lateral sclerosis: where do we stand? Front Neurosci. 2010;4:32.
26. Caplan AI. Why are MSCs therapeutic? New data: new insight. J Pathol. 2009;217(2):318-324.
27. 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. 2008;6(10):2542-2551.
28. Lunn JS, Sakowski SA, Federici T, et al. Stem cell technology for the study and treatment of motor neuron diseases. Regen Med. 2011 Mar;6(2):201-213.
29. Gowing G, Shelley B, Staggenborg K, et al. Glial cell linederived neurotrophic factor-secreting human neural progenitors show long-term survival, maturation into astrocytes, and no tumor formation following transplantation into the spinal cord of immunocompromised rats. Neuroreport. 2014;25(6):367-372.
30. The BDNF Study Group (Phase III). A controlled trial of recombinant methionyl human BDNF in ALS. Neurology. 1999;52(7):1427-1433.
31. Bongioanni P, Reali C, Sogos V. Ciliary neurotrophic factor (CNTF) for amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst Rev. 2004;3:CD004302.
32. Sorenson EJ, Windbank AJ, Mandrekar JN, et al. Subcutaneous IGF-1 is not beneficial in 2-year ALS trial. Neurology. 2008;71(22):1770-1775.
33. Klein SM, Behrstock S, McHugh J, et al. GDNF delivery using human neural progenitor cells in a rat model of ALS. Human Gene Therapy. 2005;16(4):509-521.
34. Ericson C, Georgievska B, Lundberg C. Ex vivo gene delivery of GDNF using primary astrocytes transduced with a lentiviral vector provides neuroprotection in a rat model of Parkinson's disease. Eur J Neurosci. 2005;22(11):2755-2764.
35. Kim SU, Hwang DH, Kim BG, et al. Human neural stem cells over-expressing VEGF provide behavioral improvement, disease onset delay and survival extension in transgenic ALS mice. Mol Ther. 2008;16(Suppl 1):S32.
36. Martino G, Pluchino S. The therapeutic potential of neural stem cells. Nat Rev Neurosci. 2006;7(5):395-396.
37. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8(9):726-736.
38. Vercelli A, Mereuta OM, Garbossa D, et al. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis. 2008;31(3):395-405.
39. Boido M, Piras A, Valsecchi V. Human mesenchymal stromal cell transplantation modulates neuroinflammatory milieu in a mouse model of amyotrophic lateral sclerosis. Cytotherapy. 2014;16(8):1059-1072.
40. Uccelli A, Laroni A, Freedman MS. Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol. 2011;10(7):649-656.
41. Wang Y, Chen X, Cao W, et al. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat Immunol. 2014;15(11):1009-1016.
42. Thomsen GM, Gowing G, Svendsen S, et al. The past, present and future of stem cell clinical trials for ALS. Exp Neurol. 2014;262:127-137.
43. Chen Y, Shao JZ, Xiang LX, et al. Mesenchymal stem cells: a promising candidate in regenerative medicine. Int J Biochem Cell Biol. 2008;40(5):815-820.
44. Garbuzova-Davis S, Willing AE, Saporta S, et al. Novel cell therapy approaches for brain repair. Prog Brain Res. 2006;157:207-222.
45. Kim J, Kang JW, Park JH, et al. Biological characterization of long-term cultured human mesenchymal stem cells. Arch Pharm Res. 2009;32(1):117-126.
46. 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. 2003;4(3):158-161.
47. Mazzini L, Mareschi K, Ferrero I, et al. Autologous mesenchymal stem cells: clinical applications in amyotrophic lateral sclerosis. Neurol Res. 2006;28(5):523-526.
48. Mazzini L, Mareschi K, Ferrero I, et al. Stem cell treatment in amyotrophic lateral sclerosis. J Neurol Sci. 2008;265(1-2):78-83.
49. Mazzini L, Mareschi K, Ferrero I, et al. Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study. Cytotherapy. 2012;14(1):56-60.
50. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol. 2010;67 (10):1187-1194.
51. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992;255(5052):1707-1710.
52. Vescovi AL, Parati EA, Gritti A, et al. Isolation and cloning of multipotent stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp Neurol. 1999;156(1):71-83.
53. De Feo D, Merlini A, Laterza C, et al. Neural stem cell transplantation in central nervous system disorders: from cell replacement to neuroprotection. Curr Opin Neurol. 2012;25(3):322-333.
54. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell. 2007;1:39-49.
55. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can generate motor neurons. Science. 2008;321:1218-1221.
56. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663-676.
57. Woltjen K, Michael IP, Mohseni P, et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature. 2009;458:7662770.
58. Federation AJ, Bradner JE, Meissner A. The use of small molecules in somatic-cell reprogramming. Trends Cell Biol. 2014;24:179-187.
59. Vercelli A, Boido M, Spigolon G, et al. Motor behavior tests to detect the early symptoms in a mouse ALS model. San Diego (CA): SFN; 2010. SFN 2010 abstracts.
60. Ludolph AC, Bendotti C, Blaugrund E, et al. Guidelines for preclinical animal research in ALS/MND: a consensus meeting. Amyotroph Lateral Scler. 2010;11(1-2):38-45.
61. Bruijn L, Cudkowicz M, ALS Clinical Trials Working Group. Opportunities for improving therapy development in ALS. Amyotroph Lateral Scler Frontotemporal Degener. 2014;15(3-4):169-173.
62. Mazzini L, Ferrero I, Luparello V, et al. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: a phase I clinical trial. Exp Neurol. 2010;223(1):229-237.
63. Blanquer M, Pérez-Espejo MA, Martínez-Lage JF, et al. A surgical technique of spinal cord cell transplantation in amyotrophic lateral sclerosis. J Neurosci Methods. 2010;191(2):255-257.
64. Blanquer M, Moraleda JM, Iniesta F, et al. Neurotrophic bone marrow cellular nests prevent spinal motoneuron degeneration in amyotrophic lateral sclerosis patients: a pilot safety study. Stem Cells. 2012;30(6):1277-1285.
65. Huang H, Chen L, Xi H, et al. Fetal olfactory ensheathing cells transplantation in amyotrophic lateral sclerosis patients: a controlled pilot study. Clin Transplant. 2008;22(7):10-718.
66. Appel SH, Engelhardt JI, Henkel JS. Hematopoietic stem cell transplantation in patients with sporadic amyotrophic lateral sclerosis. Neurology. 2008;71(21):1326-1334.
67. Deda H, Inci MC, Kürekçi AE, et al. Treatment of amyotrophic lateral sclerosis patients by autologous bone marrow-derived hematopoietic stem cell transplantation: a 1-year follow-up. Cytotherapy. 2009;11 (1):18-25.
68. Prabhakar S, Marwaha N, Lal V, et al. Autologous bone marrow-derived stem cells in amyotrophic lateral sclerosis: a pilot study. Neurol India. 2012;60:465-469.
69. Martinez HR, Gonzalez-Garza MT, Moreno-Cuevas JE, et al. Stem cell transplantation into the frontal motor cortex in amyotrophic lateral sclerosis patients. Cytotherapy. 2009;11(1):26-34.
70. Martinez HR, Molina-Lopez JF, Alez-Garza MT, et al. Stem cell transplantation in amyotrophic lateral sclerosis patients. Methodological approach, safety, and feasibility. Cell Transplant. 2012;21:1899-1907.
71. Baek W, Kim YS, Koh SH, et al. Stem cell transplantation into the intraventricular space via an Ommaya reservoir in a patient with amyotrophic lateral sclerosis. J Neurosurg Sci. 2012;56:261-263.
72. Cashman N, Tan LY, Krieger C, et al. Pilot study of granulocyte colony stimulating factor (G-CSF)-mobilized peripheral blood stem cells in amyotrophic lateral sclerosis (ALS). Muscle Nerve. 2008;37:620-625.
73. Chio A, Mora G, La Bella V, et al. Repeated courses of granulocyte colony stimulating factor in amyotrophic lateral sclerosis: clinical and biological results from a prospective multicenter study. Muscle Nerve. 2011;43:189-195.
74. Nefussy B, Artamonov I, Deutsch V, et al. Recombinant human granulocyte-colony stimulating factor administration for treating amyotrophic lateral sclerosis: a pilot study. Amyotroph Lateral Scler. 2010;11:187-193.
75. Riley J, Glass J, Feldman EL, et al. Intraspinal stem cell transplantation in ALS: a phase I trial, cervical microinjection and final surgical safety outcomes. Neurosurgery. 2014;74:77-87.
76. Glass JD, Boulis NM, Johe K, et al. Lumbar intraspinal injection of neural stem cells in patients with ALS: results of a phase I trial in 12 patients. Stem Cells. 2012;30 (6):1144-1151.
77. Feldman EL, Boulis NM, Hur J, et al. Intraspinal neural stem cell transplantation in amyotrophic lateral sclerosis: phase 1 trial outcomes. Ann Neurol. 2014;75(3):363-373.
78. Mazzini L, Gelati M, Profico DC. Human neural stem cell transplantation in ALS: initial results from a phase I trial. J Transl Med. 2015;13(1):17.
79. Ravits J. Focality, stochasticity and neuroanatomic propagation in ALS pathogenesis. Exp Neurol. 2014;262:121-126.
80. Kaplan LM, Hollander D. Respiratory dysfunction in amyotrophic lateral sclerosis. Clin Chest Med. 1994;15 (4):675-681.
81. Teng YD, Benn SC, Kalkanis SN. Multimodal actions of neural stem cells in a mouse model of ALS: a metaanalysis. Sci Transl Med. 2012;4(165):165ra164.
82. Nichols NL, Gowing G, Satriotomo I. Intermittent hypoxia and stem cell implants preserve breathing capacity in a rodent model of amyotrophic lateral sclerosis. Am J Respir Crit Care Med. 2013;187(5):535-542.
83. Riley JP, Raore B, Taub JS, et al. Platform and cannula design improvements for spinal cord therapeutics delivery. Neurosurgery. 2011;69(2):147-155.
84. Riley J, Federici T, Polak M, et al. Intraspinal stem cell transplantation in amyotrophic lateral sclerosis: a phase I safety trial, technical note, and lumbar safety outcomes. Neurosurgery. 2012;71:405-416.
85. Xu L, Shen P, Hazel T, et al. Dual transplantation of human neural stem cells into cervical and lumbar cord ameliorates motor neuron disease in SOD1 transgenic rats. Neurosci Lett. 2011;494(3):222-226.
86. García Santos JM, Blanquer M, Torres del Río S, et al. Acute and chronic MRI changes in the spine and spinal cord after surgical stem cell grafting in patients with definite amyotrophic lateral sclerosis: post-infusion injuries are unrelated with clinical impairment. Magn Reson Imaging. 2013;1(8):1298-1308.
87. Bernau K, Lewis CM, Petelinsek AM, et al. In vivo tracking of human neural progenitor cells in the rat brain using magnetic resonance imaging is not enhanced by ferritin expression. Cell Transplant. 2015 Jul 8 [Epub ahead of print].
88. Tadesse T, Gearing M, Senitzer D, et al. Analysis of graft survival in a trial of stem cell transplant in ALS. Ann Clin Transl Neurol. 2014;1(11):900-908.
89. Hyun I, Lindvall O, Ahrlund-Richter L, et al. New ISSCR guidelines underscore major principles for responsible translational stem cell research. Cell Stem Cell. 2008;3(6):607-609.