Comparative study on the therapeutic potential of neurally differentiated stem cells in a mouse model of multiple sclerosis

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Payne, Natalie L ^a   Sun, Guizhi ^a   Herszfeld, Daniella ^a   Tat Goh, Pollyanna A ^a   Verma, Paul J ^a   Parkington, Helena C ^a   Coleman, Harold A ^a   Tonta, Mary A ^a   Siatskas, Christopher ^a   Bernard, Claude C A ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; BETA3 TUBULIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 6; MICROTUBULE ASSOCIATED PROTEIN 2; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; MYOSIN HEAVY CHAIN; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRACHYURY; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX5; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; MYELIN PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURFACE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; DISEASE MODEL; EMBRYONIC STEM CELL; FEMALE; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOID TISSUE; MOUSE; MULTIPLE SCLEROSIS; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SPLEEN CELL; SUBVENTRICULAR ZONE; TREATMENT OUTCOME; ANIMAL; CHEMICALLY INDUCED DISORDER; CYTOLOGY; PHYSIOLOGY; TRANSPLANTATION;

MUS;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MULTIPLE SCLEROSIS; MYELIN PROTEINS; NEURAL STEM CELLS;

EID: 84859732266     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035093     Document Type: Article

References (69)

1. Payne N, Siatskas C, Barnard A, Bernard CC, (2011) The prospect of stem cells as multi-faceted purveyors of immune modulation, repair and regeneration in multiple sclerosis. Curr Stem Cell Res Ther 6: 50-62.
2. Einstein O, Karussis D, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, et al. (2003) Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 24: 1074-1082.
3. Einstein O, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, Polyzoidou E, et al. (2006) Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp Neurol 198: 275-284.
4. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, et al. (2003) Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422: 688-694.
5. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, et al. (2005) Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436: 266-271.
6. Pluchino S, Gritti A, Blezer E, Amadio S, Brambilla E, et al. (2009) Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates. Ann Neurol 66: 343-354.
7. Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, et al. (2007) Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61: 209-218.
8. Martino G, Pluchino S, (2006) The therapeutic potential of neural stem cells. Nat Rev Neurosci 7: 395-406.
9. Schwarz SC, Schwarz J, (2010) Translation of stem cell therapy for neurological diseases. Transl Res 156: 155-160.
10. Parsons XH, Teng YD, Snyder EY, (2009) Important precautions when deriving patient-specific neural elements from pluripotent cells. Cytotherapy 11: 815-824.
11. Reynolds BA, Tetzlaff W, Weiss S, (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12: 4565-4574.
12. Ying QL, Stavridis M, Griffiths D, Li M, Smith A, (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21: 183-186.
13. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, et al. (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3: e283.
14. Glaser T, Pollard SM, Smith A, Brustle O, (2007) Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS One 2: e298.
15. Brustle O, Spiro AC, Karram K, Choudhary K, Okabe S, et al. (1997) In vitro-generated neural precursors participate in mammalian brain development. PNAS 94: 14809-14814.
16. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA, (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
17. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, et al. (2001) Neural progenitors from human embryonic stem cells. Nat Biotechnol 19: 1134-1140.
18. Perez-Alvarez MJ, Isiegas C, Santano C, Salazar JJ, Ramirez AI, et al. (2008) Vimentin isoform expression in the human retina characterized with the monoclonal antibody 3CB2. J Neurosci Res 86: 1871-1883.
19. Ng ES, Davis RP, Azzola L, Stanley EG, Elefanty AG, (2005) Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106: 1601-1603.
20. Sprinkle TJ, (1989) 2′,3′-cyclic nucleotide 3′-phosphodiesterase, an oligodendrocyte-Schwann cell and myelin-associated enzyme of the nervous system. Crit Rev Neurobiol 4: 235-301.
21. Aharonowiz M, Einstein O, Fainstein N, Lassmann H, Reubinoff B, et al. (2008) Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS ONE 3: e3145.
22. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, et al. (2003) Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med 197: 1073-1081.
23. Codarri L, Fontana A, Becher B, (2010) Cytokine networks in multiple sclerosis: lost in translation. Curr Opin Neurol 23: 205-211.
24. Weber MS, Prod'homme T, Patarroyo JC, Molnarfi N, Karnezis T, et al. (2010) B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann Neurol 68: 369-383.
25. Bettadapura J, Menon KK, Moritz S, Liu J, Bernard CC, (1998) Expression, purification, and encephalitogenicity of recombinant human myelin oligodendrocyte glycoprotein. J Neurochem 70: 1593-1599.
26. Reekmans KP, Praet J, de Vocht N, Tambuyzer BR, Bergwerf I, et al. (2011) Clinical potential of intravenous neural stem cell delivery for treatment of neuro-inflammatory disease in mice? Cell Transplant 20: 851-869.
27. Krumbholz M, Theil D, Cepok S, Hemmer B, Kivisakk P, et al. (2006) Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain 129: 200-211.
28. Liu KK, Dorovini-Zis K, (2009) Regulation of CXCL12 and CXCR4 expression by human brain endothelial cells and their role in CD4+ and CD8+ T cell adhesion and transendothelial migration. J Neuroimmunol 215: 49-64.
29. Gordon D, Pavlovska G, Glover CP, Uney JB, Wraith D, et al. (2008) Human mesenchymal stem cells abrogate experimental allergic encephalomyelitis after intraperitoneal injection, and with sparse CNS infiltration. Neurosci Lett 448: 71-73.
30. Rafei M, Hsieh J, Fortier S, Li M, Yuan S, et al. (2008) Mesenchymal stromal cell-derived CCL2 suppresses plasma cell immunoglobulin production via STAT3 inactivation and PAX5 induction. Blood 112: 4991-4998.
31. Rafei M, Birman E, Forner K, Galipeau J, (2009) Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther 17: 1799-1803.
32. Pluchino S, Zanotti L, Brambilla E, Rovere-Querini P, Capobianco A, et al. (2009) Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One 4: e5959.
33. Pluchino S, Martino G, (2008) The therapeutic plasticity of neural stem/precursor cells in multiple sclerosis. J Neurol Sci 265: 105-110.
34. Payne N, Siatskas C, Bernard CC, (2008) The promise of stem cell and regenerative therapies for multiple sclerosis. J Autoimmun 31: 288-294.
35. Pera MF, Tam PP, (2010) Extrinsic regulation of pluripotent stem cells. Nature 465: 713-720.
36. Campos LS, (2004) Neurospheres: insights into neural stem cell biology. J Neurosci Res 78: 761-769.
37. Reid CA, Coleman HA, Finkelstein DI, Horne MK, Drago J, (2006) Null mutation of the alpha4 nicotinic receptor subunit increases the propensity of muscarinic-mediated neuronal bursting in mouse hippocampal slices. Neuropharmacology 51: 587-596.
38. Gu XQ, Xue J, Haddad GG, (2004) Effect of chronically elevated CO2 on CA1 neuronal excitability. Am J Physiol Cell Physiol 287: C691-697.
39. Johnson MA, Weick JP, Pearce RA, Zhang SC, (2007) Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci 27: 3069-3077.
40. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, et al. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
41. Fields RD, Stevens-Graham B, (2002) New insights into neuron-glia communication. Science 298: 556-562.
42. Kim SY, Cho HS, Yang SH, Shin JY, Kim JS, et al. (2009) Soluble mediators from human neural stem cells play a critical role in suppression of T-cell activation and proliferation. J Neurosci Res 87: 2264-2272.
43. Akesson E, Wolmer-Solberg N, Cederarv M, Falci S, Odeberg J, (2009) Human neural stem cells and astrocytes, but not neurons, suppress an allogeneic lymphocyte response. Stem Cell Res 2: 56-67.
44. Conti L, Cattaneo E, (2010) Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci 11: 176-187.
45. Imitola J, Chitnis T, Khoury SJ, (2005) Cytokines in multiple sclerosis: from bench to bedside. Pharmacol Ther 106: 163-177.
46. Yang J, Yan Y, Ciric B, Yu S, Guan Y, et al. (2010) Evaluation of bone marrow- and brain-derived neural stem cells in therapy of central nervous system autoimmunity. Am J Pathol 177: 1989-2001.
47. Politi LS, Bacigaluppi M, Brambilla E, Cadioli M, Falini A, et al. (2007) Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells 25: 2583-2592.
48. Bacigaluppi M, Pluchino S, Peruzzotti-Jametti L, Kilic E, Kilic U, et al. (2009) Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132: 2239-2251.
49. Lee ST, Chu K, Park JE, Lee K, Kang L, et al. (2005) Intravenous administration of human neural stem cells induces functional recovery in Huntington's disease rat model. Neurosci Res 52: 243-249.
50. Tsuji O, Miura K, Okada Y, Fujiyoshi K, Mukaino M, et al. (2010) Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proc Natl Acad Sci U S A 107: 12704-12709.
51. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, et al. (1999) Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5: 1410-1412.
52. Liu S, Qu Y, Stewart TJ, Howard MJ, Chakrabortty S, et al. (2000) Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci U S A 97: 6126-6131.
53. Pendharkar AV, Chua JY, Andres RH, Wang N, Gaeta X, et al. (2010) Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke 41: 2064-2070.
54. Crocker SJ, Bajpai R, Moore CS, Frausto RF, Brown GD, et al. (2011) Intravenous Administration of Human ES-derived Neural Precursor Cells Attenuates Cuprizone-induced CNS Demyelination. Neuropathol Appl Neurobiol 37: 643-653.
55. Bakshi A, Keck CA, Koshkin VS, LeBold DS, Siman R, et al. (2005) Caspase-mediated cell death predominates following engraftment of neural progenitor cells into traumatically injured rat brain. Brain Res 1056: 8-19.
56. Robey TE, Saiget ML, Reinecke H, Murray CE, (2008) Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 45: 567-581.
57. Rossi B, Angiari S, Zenaro E, Budui SL, Constantin G, (2011) Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyte-endothelial interactions. J Leukoc Biol 89: 539-556.
58. Brocke S, Piercy C, Steinman L, Weissman IL, Veromaa T, (1999) Antibodies to CD44 and integrin alpha4, but not L-selectin, prevent central nervous system inflammation and experimental encephalomyelitis by blocking secondary leukocyte recruitment. Proc Natl Acad Sci U S A 96: 6896-6901.
59. Rampon C, Weiss N, Deboux C, Chaverot N, Miller F, et al. (2008) Molecular mechanism of systemic delivery of neural precursor cells to the brain: assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells 26: 1673-1682.
60. Tran PB, Miller RJ, (2003) Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci 4: 444-455.
61. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, et al. (2004) Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101: 18117-18122.
62. Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, et al. (2006) Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 24: 1030-1041.
63. Shin S, Sun Y, Liu Y, Khaner H, Svant S, et al. (2007) Whole genome analysis of human neural stem cells derived from embryonic stem cells and stem and progenitor cells isolated from fetal tissue. Stem Cells 25: 1298-1306.
64. Prowse AB, Chong F, Gray PP, Munro TP, (2011) Stem cell integrins: implications for ex-vivo culture and cellular therapies. Stem Cell Res 6: 1-12.
65. Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, et al. (2008) Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14: 181-187.
66. Szabo P, Mann JR, (1994) Expression and methylation of imprinted genes during in vitro differentiation of mouse parthenogenetic and androgenetic embryonic stem cell lines. Development 120: 1651-1660.
67. Tat PA, Sumer H, Jones KL, Upton K, Verma PJ, (2010) The efficient generation of induced pluripotent stem (iPS) cells from adult mouse adipose tissue-derived and neural stem cells. Cell Transplant 19: 525-536.
68. McQualter JL, Darwiche R, Ewing C, Onuki M, Kay TW, et al. (2001) Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J Exp Med 194: 873-882.
69. Linnington C, Webb M, Woodhams PL, (1984) A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J Neuroimmunol 6: 387-396.