Effects of Olig2-Overexpressing Neural Stem Cells and Myelin Basic Protein-Activated T Cells on Recovery from Spinal Cord Injury

Neurotherapeutics

Volumn 9, Issue 2, 2012, Pages 422-445

  Hu, Jian Guo ^a   Shen, Lin ^a   Wang, Rui ^a   Wang, Qi Yi ^a   Zhang, Chen ^a   Xi, Jin ^a   Ma, Shan Feng ^a   Zhou, Jian Sheng ^a   Lü, He Zuo ^a  

^a BENGBU MEDICAL COLLEGE   (China)

Author keywords

Neural stem cells; Olig2; Passive immunization; Spinal cord injury; Transplantation

Indexed keywords

ARGINASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; MYELIN; MYELIN BASIC PROTEIN; NERVE GROWTH FACTOR; NESTIN; NEUROTROPHIN 3; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BLOOD BRAIN BARRIER; CELL DIFFERENTIATION; CELL INFILTRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LENTIVIRINAE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MICROENVIRONMENT; MICROGLIA; MONOCYTE; MOTONEURON; MYELINATION; NERVE FIBER; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY; T LYMPHOCYTE ACTIVATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; LYMPHOCYTE ACTIVATION; MYELIN BASIC PROTEIN; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; T-LYMPHOCYTES;

EID: 84859698907     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-011-0090-9     Document Type: Article

References (88)

1. Nandoe Tewarie RS, Hurtado A, Bartels RH, Grotenhuis A, Oudega M. Stem cell-based therapies for spinal cord injury. J Spinal Cord Med 2009; 32: 105-114.
2. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 2006; 26: 3377-3389.
3. Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006; 7: 628-643.
4. Xu XM, Onifer SM. Transplantation-mediated strategies to promote axonal regeneration following spinal cord injury. Respir Physiol Neurobiol 2009; 169: 171-182.
5. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 2001; 167: 48-58.
6. Ricci-Vitiani L, Casalbore P, Petrucci G, et al. Influence of local environment on the differentiation of neural stem cells engrafted onto the injured spinal cord. Neurol Res 2006; 28: 488-492.
7. Blakemore WF, Gilson JM, Crang AJ. The presence of astrocytes in areas of demyelination influences remyelination following transplantation of oligodendrocyte progenitors. Exp Neurol 2003; 184: 955-963.
8. Butovsky O, Hauben E, Schwartz M. Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7-2 (CD86) and prevention of cyst formation. Faseb J 2001; 15: 1065-1067.
9. Kipnis J, Mizrahi T, Hauben E, Shaked I, Shevach E, Schwartz M. Neuroprotective autoimmunity: naturally occurring CD4 + CD25+ regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci U S A 2002; 99: 15620-15625.
10. Schwartz M. Harnessing the immune system for neuroprotection: therapeutic vaccines for acute and chronic neurodegenerative disorders. Cell Mol Neurobiol 2001; 21: 617-627.
11. Schwartz M. Protective autoimmunity as a T-cell response to central nervous system trauma: prospects for therapeutic vaccines. Prog Neurobiol 2001; 65: 489-496.
12. Schwartz M, Kipnis J. Protective autoimmunity: regulation and prospects for vaccination after brain and spinal cord injuries. Trends Mol Med 2001; 7: 252-258.
13. Yoles E, Hauben E, Palgi O, et al. Protective autoimmunity is a physiological response to CNS trauma. J Neurosci 2001; 21: 3740-3748.
14. Lu HZ, Xu L, Zou J, et al. Effects of autoimmunity on recovery of function in adult rats following spinal cord injury. Brain Behav Immun 2008; 22: 1217-1230.
15. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M. Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci U S A 2006; 103: 13174-13179.
16. Cooke MJ, Zahir T, Phillips SR, et al. Neural differentiation regulated by biomimetic surfaces presenting motifs of extracellular matrix proteins. J Biomed Mater Res A 2010; 93: 824-832.
17. Lu HZ, Wang YX, Li Y, Fu SL, Hang Q, Lu PH. Proliferation and differentiation of oligodendrocyte progenitor cells induced from rat embryonic neural precursor cells followed by flow cytometry. Cytometry A 2008; 73: 754-760.
18. Lu HZ, Wang YX, Zou J, et al. Differentiation of neural precursor cell-derived oligodendrocyte progenitor cells following transplantation into normal and injured spinal cords. Differentiation 2010; 80: 228-240.
19. Mitsuhashi T, Takahashi T. Genetic regulation of proliferation/differentiation characteristics of neural progenitor cells in the developing neocortex. Brain Dev 2009; 31: 553-557.
20. Kwon BK, Tetzlaff W, Grauer JN, Beiner J, Vaccaro AR. Pathophysiology and pharmacologic treatment of acute spinal cord injury. Spine J 2004; 4: 451-464.
21. Rowland JW, Hawryluk GW, Kwon B, Fehlings MG. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus 2008; 25: E2.
22. Sheerin F. Spinal cord injury: causation and pathophysiology. Emerg Nurse 2005; 12: 29-38.
23. Cheng X, Wang Y, He Q, Qiu M, Whittemore SR, Cao Q. Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 2007; 25: 3204-3214.
24. Takebayashi H, Nabeshima Y, Yoshida S, Chisaka O, Ikenaka K, Nabeshima Y. The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol 2002; 12: 1157-1163.
25. Zhou Q, Anderson DJ. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002; 109: 61-73.
26. Balasubramaniyan V, Timmer N, Kust B, Boddeke E, Copray S. Transient expression of Olig1 initiates the differentiation of neural stem cells into oligodendrocyte progenitor cells. Stem Cells 2004; 22: 878-882.
27. Copray S, Balasubramaniyan V, Levenga J, de Bruijn J, Liem R, Boddeke E. Olig2 overexpression induces the in vitro differentiation of neural stem cells into mature oligodendrocytes. Stem Cells 2006; 24: 1001-1010.
28. Hwang DH, Kim BG, Kim EJ, et al. Transplantation of human neural stem cells transduced with Olig2 transcription factor improves locomotor recovery and enhances myelination in the white matter of rat spinal cord following contusive injury. BMC Neurosci 2009; 10: 117.
29. Fu SL, Ma ZW, Yin L, Iannotti C, Lu PH, Xu XM. Region-specific growth properties and trophic requirements of brain- and spinal cord-derived rat embryonic neural precursor cells. Neuroscience 2005; 135: 851-862.
30. He Y, Zhang J, Mi Z, Robbins P, Falo LD Jr. Immunization with lentiviral vector-transduced dendritic cells induces strong and long-lasting T cell responses and therapeutic immunity. J Immunol 2005; 174: 3808-3817.
31. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M. Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 1999; 5: 49-55.
32. Gu WL, Fu SL, Wang YX, et al. Expression and regulation of versican in neural precursor cells and their lineages. Acta Pharmacol Sin 2007; 28: 1519-1530.
33. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.
34. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 2010; 133: 433-447.
35. Cao Q, Xu XM, Devries WH et al. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J Neurosci 2005; 25: 6947-6957.
36. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995; 12: 1-21.
37. Basso DM, Beattie MS, Bresnahan JC, et al. MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 1996; 13: 343-359.
38. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990; 60: 585-595.
39. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 2009; 29: 13435-13444.
40. Cao Q, He Q, Wang Y, et al. Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 2010; 30: 2989-3001.
41. Gilson JM, Blakemore WF. Schwann cell remyelination is not replaced by oligodendrocyte remyelination following ethidium bromide induced demyelination. Neuroreport 2002; 13: 1205-1208.
42. Hildebrand C, Hahn R. Relation between myelin sheath thickness and axon size in spinal cord white matter of some vertebrate species. J Neurol Sci 1978; 38: 421-434.
43. McDonald JW. Repairing the damaged spinal cord. Sci Am 1999; 281: 64-73.
44. McDonald JW. Repairing the damaged spinal cord: from stem cells to activity-based restoration therapies. Clin Neurosurg 2004; 51: 207-227.
45. McDonald JW, Howard MJ. Repairing the damaged spinal cord: a summary of our early success with embryonic stem cell transplantation and remyelination. Prog Brain Res 2002; 137: 299-309.
46. Coutts M, Keirstead HS. Stem cells for the treatment of spinal cord injury. Exp Neurol 2008; 209: 368-377.
47. Enzmann GU, Benton RL, Talbott JF, Cao Q, Whittemore SR. Functional considerations of stem cell transplantation therapy for spinal cord repair. J Neurotrauma 2006; 23: 479-495.
48. Kulbatski I, Mothe AJ, Parr AM, et al. Glial precursor cell transplantation therapy for neurotrauma and multiple sclerosis. Prog Histochem Cytochem 2008; 43: 123-176.
49. Louro J, Pearse DD. Stem and progenitor cell therapies: recent progress for spinal cord injury repair. Neurol Res 2008; 30: 5-16.
50. Chow SY, Moul J, Tobias CA, et al. Characterization and intraspinal grafting of EGF/bFGF-dependent neurospheres derived from embryonic rat spinal cord. Brain Res 2000; 874: 87-106.
51. Hofstetter CP, Holmstrom NA, Lilja JA, et al. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 2005; 8: 346-353.
52. Shihabuddin LS, Horner PJ, Ray J, Gage FH. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 2000; 20: 8727-8735.
53. Wu S, Suzuki Y, Noda T, et al. Immunohistochemical and electron microscopic study of invasion and differentiation in spinal cord lesion of neural stem cells grafted through cerebrospinal fluid in rat. J Neurosci Res 2002; 69: 940-945.
54. Ahn SM, Byun K, Kim D et al. Olig2-induced neural stem cell differentiation involves downregulation of Wnt signaling and induction of Dickkopf-1 expression. PLoS One 2008; 3: e3917.
55. Islam MS, Tatsumi K, Okuda H, Shiosaka S, Wanaka A. Olig2-expressing progenitor cells preferentially differentiate into oligodendrocytes in cuprizone-induced demyelinated lesions. Neurochem Int 2009; 54: 192-198.
56. Liu Z, Hu X, Cai J, et al. Induction of oligodendrocyte differentiation by Olig2 and Sox10: evidence for reciprocal interactions and dosage-dependent mechanisms. Dev Biol 2007; 302: 683-693.
57. Ankeny DP, Popovich PG. Central nervous system and non-central nervous system antigen vaccines exacerbate neuropathology caused by nerve injury. Eur J Neurosci 2007; 25: 2053-2064.
58. Jones TB, Ankeny DP, Guan Z, et al. Passive or active immunization with myelin basic protein impairs neurological function and exacerbates neuropathology after spinal cord injury in rats. J Neurosci 2004; 24: 3752-3761.
59. Jones TB, Basso DM, Sodhi A, et al. Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J Neurosci 2002; 22: 2690-2700.
60. Popovich PG, Jones TB. Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics. Trends Pharmacol Sci 2003; 24: 13-17.
61. Hauben E, Butovsky O, Nevo U, et al. Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 2000; 20: 6421-6430.
62. Kipnis J, Yoles E, Schori H, Hauben E, Shaked I, Schwartz M. Neuronal survival after CNS insult is determined by a genetically encoded autoimmune response. J Neurosci 2001; 21: 4564-4571.
63. Barouch R, Schwartz M. Autoreactive T cells induce neurotrophin production by immune and neural cells in injured rat optic nerve: implications for protective autoimmunity. Faseb J 2002; 16: 1304-1306.
64. Moalem G, Gdalyahu A, Shani Y, et al. Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J Autoimmun 2000; 15: 331-345.
65. Avidan H, Kipnis J, Butovsky O, Caspi RR, Schwartz M. Vaccination with autoantigen protects against aggregated beta-amyloid and glutamate toxicity by controlling microglia: effect of CD4 + CD25+ T cells. Eur J Immunol 2004; 34: 3434-3445.
66. Butovsky O, Bukshpan S, Kunis G, Jung S, Schwartz M. Microglia can be induced by IFN-gamma or IL-4 to express neural or dendritic-like markers. Mol Cell Neurosci 2007; 35: 490-500.
67. Schori H, Robenshtok E, Schwartz M, Hourvitz A. Post-intoxication vaccination for protection of neurons against the toxicity of nerve agents. Toxicol Sci 2005; 87: 163-168.
68. Schwartz M. Macrophages and microglia in central nervous system injury: are they helpful or harmful? J Cereb Blood Flow Metab 2003; 23: 385-394.
69. Shaked I, Tchoresh D, Gersner R, et al. Protective autoimmunity: interferon-gamma enables microglia to remove glutamate without evoking inflammatory mediators. J Neurochem 2005; 92: 997-1009.
70. Hickey WF, Hsu BL, Kimura H. T-lymphocyte entry into the central nervous system. J Neurosci Res 1991; 28: 254-260.
71. Jones TB, Hart RP, Popovich PG. Molecular control of physiological and pathological T-cell recruitment after mouse spinal cord injury. J Neurosci 2005; 25: 6576-6583.
72. Bartholdi D, Schwab ME. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci 1997; 9: 1422-1438.
73. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 2003; 184: 313-325.
74. Wu KL, Chan SH, Chao YM, Chan JY. Expression of pro-inflammatory cytokine and caspase genes promotes neuronal apoptosis in pontine reticular formation after spinal cord transection. Neurobiol Dis 2003; 14: 19-31.
75. Yang L, Jones NR, Blumbergs PC, et al. Severity-dependent expression of pro-inflammatory cytokines in traumatic spinal cord injury in the rat. J Clin Neurosci 2005; 12: 276-284.
76. Chu TH, Wu W. Neurotrophic factor treatment after spinal root avulsion injury. Cent Nerv Syst Agents Med Chem 2009; 9: 40-55.
77. Mocchetti I, Wrathall JR. Neurotrophic factors in central nervous system trauma. J Neurotrauma 1995; 12: 853-870.
78. Sharma HS. Neurotrophic factors in combination: a possible new therapeutic strategy to influence pathophysiology of spinal cord injury and repair mechanisms. Curr Pharm Des 2007; 13: 1841-1874.
79. Bethea JR. Spinal cord injury-induced inflammation: a dual-edged sword. Prog Brain Res 2000; 128: 33-42.
80. Offner H, Subramanian S, Wang C, et al. Treatment of passive experimental autoimmune encephalomyelitis in SJL mice with a recombinant TCR ligand induces IL-13 and prevents axonal injury. J Immunol 2005; 175: 4103-4111.
81. Schroeter M, Jander S. T-cell cytokines in injury-induced neural damage and repair. Neuromolecular Med 2005; 7: 183-195.
82. Stoll G, Jander S, Schroeter M. Cytokines in CNS disorders: neurotoxicity versus neuroprotection. J Neural Transm Suppl 2000; 59: 81-89.
83. Goerdt S, Orfanos CE. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 1999; 10: 137-142.
84. Mikita J, Dubourdieu-Cassagno N, Deloire MS, et al. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration. Mult Scler xxxx; 17: 2-15.
85. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8: 958-969.
86. Bethea JR, Nagashima H, Acosta MC, et al. Systemically administered interleukin-10 reduces tumor necrosis factor-alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats. J Neurotrauma 1999; 16: 851-863.
87. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13: 453-461.
88. Sica A, Schioppa T, Mantovani A, Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 2006; 42: 717-727.