The reactions and role of NG2 glia in spinal cord injury

Brain Research

Volumn 1638, Issue , 2016, Pages 199-208

  Levine, Joel ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Inflammation; NG2; Oligodendrocyte precursor cell; Regeneration; Remyelination; Spinal cord injury

Indexed keywords

CELL FUNCTION; CELL PLASTICITY; CELL POPULATION; CELL PROLIFERATION; DEGENERATIVE DISEASE; HUMAN; IN VIVO STUDY; INFLAMMATION; NERVE FIBER REGENERATION; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; REGULATORY MECHANISM; REMYELINIZATION; REVIEW; SPINAL CORD INJURY; ANIMAL; METABOLISM; OLIGODENDROGLIA; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL;

ANTIGEN; CHONDROITIN SULFATE PROTEOGLYCAN 4; PROTEOGLYCAN;

ANIMALS; ANTIGENS; HUMANS; OLIGODENDROGLIA; PROTEOGLYCANS; SPINAL CORD; SPINAL CORD INJURIES; STEM CELLS;

EID: 84939839080     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.07.026     Document Type: Review

References (131)

1. Afshari, F.T., Kwok, J.C., White, L., et al. Schwann cell migration is integrin-dependent and inhibited by astrocyte-produced aggrecan. Glia, 58, 2010, 857–869.
2. Allan, S.M., Tyrrell, P.J., Rothwell, N.J., Interleukin-1 and neuronal injury. Nat. Rev. Immunol. 5 (2005), 629–640.
3. Almad, A., Sahinkaya, F.R., McTigue, D.M., Oligodendrocyte fate after spinal cord injury. Neurotherapeutics 8 (2011), 262–273.
4. Amankulor, N.M., Hambardzumyan, D., Pyonteck, S.M., et al. Sonic hedgehog pathway activation is induced by acute brain injury and regulated by injury-related inflammation. J. Neurosci. 29 (2009), 10299–102308.
5. Aquirre, A., Gallo, V., Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J. Neurosci. 24 (2004), 10530–10541.
6. Arnett, H.A., Mason, J., Marino, M., TNFα promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4 (2001), 1116–1122.
7. Arvanian, V.L., Schnell, L., Lou, L., et al. Chronic spinal hemisection in rats induces a progressive decline in transmission in uninjured fibers to motoneurons. Exp. Neurol. 216 (2009), 471–480.
8. Bartholdi, D., Schwab, M.E., Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur. J. Neurosci. 9 (1997), 1422–1438.
9. Barres, B.A., Raff, M.C., Gaese, F., et al. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367 (1994), 371–375.
10. Bastien, D., Lacriox, S., Cytokine pathways regulating glial and leukocyte function after spinal cord and peripheral nerve injury. Exp. Neurol 258 (2014), 62–77.
11. Bennett, M.R., Rizvi, T.A., Karyala, S., et al. Aberrant growth and differentiation of oligodendrocyte progenitors in neurofibromatosis type 1 mutant. J, Neurosci. 23 (2003), 7207–7217.
12. Boyce, V.S., Mendell, L.M., Neurotrophic factors in spinal cord injury, 220, 2014, Handbook of Experimental Pharmacology, 443–460.
13. Bradke, F., Fawcett, J.W., Spira, M.E., Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 13 (2012), 183–193.
14. Brannan, C.I., Perkins, A.S., Vogel, K.S., et al. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev. 8 (1994), 1019–1029.
15. Bu, J., Akhtar, N., Nishiyama, A., Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 34 (2001), 296–310.
16. Buffo, A., Vosko, M.R., Erturk, D., et al. Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 18183–18188.
17. Buffo, A., Rite, I., Tripathi, P., et al. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl. Acad. Sci. U.S.A. 105:9 (2008), 3581–3586.
18. Busch, S.A., Horn, K.P., Cuascut, F.X., et al. NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J. Neurosci. 30 (2010), 255–265.
19. Bush, T.G., Puvanachandra, N., Horner, C.H., et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 23 (1999), 297–308.
20. Buss, A., Pech, K., Kakulas, B.A., et al. NG2 and phosphacan are present in the astroglial scar after human traumatic spinal cord injury. BMC Neurol, 9, 2009, 32.
21. Butt, A.M., Duncan, A., Hornby, M.F., et al. Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26 (1999), 92–96.
22. Cameron, S., Rao, Y., Molecular mechanisms of tiling and self-avoidance in neural development. Mol. Brain 3 (2010), 28–35.
23. Chen, K.B., Uchida, K., Nakajima, H., et al. Tumor necrosis factor-alpha antagonist reduces apoptosis of neurons and oligodendroglia in rat spinal cord injury. Spine (Phila Pa 1976) 36 (2011), 1350–1358.
24. Crowe, M.J., Bresnahan, J.C., Shuman, S.L., et al. Apoptosis anddelayed degeneration after spinal cord injury in rats and monkeys. Nat. Med 3 (1997), 73–76.
25. Curtis, R., Cohen, J., Fok-Seang, J., et al. Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J. Neurocytol. 17 (1988), 43–54.
26. David, S., Kroner, A., Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 12 (2011), 388–399.
27. Dawson, M.R., Levine, J.M., Reynolds, R., NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors?. J. Neurosci. Res 61 (2000), 471–479.
28. Dawson, M.L., Polito, A., Levine, J.M., et al. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 24 (2003), 787–802.
29. deCastro, R., Tajrishi, R., Claros, J., et al. Differential responses of spinal axons to transection: influence of the NG2 proteoglycan. Exp. Neurol. 192 (2005), 299–309.
30. Dimou, L., Simon, C., Kirchholl, et al. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28 (2008), 10434–10442.
31. Dou, C., Levine, J.M., Inhibition of neurite growth by the NG2 chondroitin-sulfate proteoglycan. J. Neurosci. 14 (1994), 7616–7628.
32. Dou, C., Levine, J.M., Identification of neuronal cell surface receptor for a growth inhibitory chondroitin sulfate proteoglycan (NG2). J. Neurochem. 68 (1997), 1021–1030.
33. Faulkner, J.R., Herrmann, J.E., Woo, M.J., et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci 24 (2004), 2143–2155.
34. Fernandez-Martos, C.M., Gonzalez-Fernandez, C., Gonzalez, P., et al. Differential expression of Wnts after spinal cord contusion injury in adult rats. PLoS One, 6, 2011, e27000.
35. Fidler, P.S., Schuette, K., Powell, E.M., et al. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J. Neurosci. 19 (1999), 8778–8788.
36. Filous, A.R., Tran, A., Howell, J.C., et al. Entrapment via synaptic-like connections between NG2 proteoglycan+ cells and dystrophic axons in the lesion plays a role in regeneration failure after spinal cord injury. J. Neurosci. 34 (2014), 16369–16784.
37. Gonzalez, P., Fernandez-Martos, C.M., Gonzalez-Fernandez, C., et al. Spatio-temporal expression pattern of frizzled receptors after contusive spinal cord injury in adult rats. PLoS One, 7, 2012, e50793.
38. Göritz, C., Dias, D.O., Tomilin, N., et al. A pericyte origin of spinal cord scar tissue. Science 333 (2011), 238–242.
39. Guest, J.D., Hiester, E.D., Bunge, R.P., Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 192 (2005), 384–393.
40. Guo, Z., Zhang, L., Wu, Z., et al. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and Alzheimer;s disease model. Cell Stem Cell. 14 (2014), 188–202.
41. Hampton, D.W., Rhodes, K.E., Zhao, C., et al. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a corticasl stab injury, in the brain. Neuroscience 127 (2004), 813–820.
42. Haroutunian, V., Katsel, P., Rousses, P., et al. Myelination, oligodendrocyhtes and serious mental illness. Glia 62 (2014), 1856–1877.
43. Hawryluk, G.W.J., Mothe, A., Wang, J., et al. An in vivo characterization of trophic factor production following neural precursor cell or bone marrow stromal cell transplantation following spinal cord injury. Stem Cell Dev. 21 (2012), 2222–2239.
44. Harvey, A.R., Lovett, S.J., Majda, B.T., Neurotrophic factors for spinal cord repair: Which, where, how and when to apply, and for what period of time. Brain Res., S0006, 2014 Epub.
45. Heinrich, C., Bergami, M., Gascon, S., et al. Sox-2 mediated conversion of NG2 glia into induced neurons in the injured adult cerebral cortex. Stem Cell Reports 3 (2014), 100–1014.
46. Hesp, Z.C., Goldstein, E.Z., Miranda, C.J., et al. Chronic oligodendrogenesis and remyelination after spinal cord injury in mice and rats. J. Neurosci. 35 (2015), 1274–1290.
47. Hill, C.E., Hurtado, A., Blits, B., et al. Early necrosis and apoptosis of Schwann cells transplanted into the injured rat spinal cord. Eur. J. Neurosci. 26 (2007), 1433–1445.
48. Hossain-Ibrahim, M.K., Rezajooi, K., Stallcup, W.B., et al. Analysis of axonal regeneration in the central and peripheral nervous systems of the NG2-deficient mouse. BMC Neurosci 8 (2007), 80–92.
49. Horky, L.L., Galimi, F., Gage, F.H., et al. Fate of endogenous stem/progenitor cells following spinal cord injury. J. Comp. Neurol 498 (2006), 525–538.
50. Hsu, J.Y., Bourguignon, L.Y., Adams, C.M., et al. Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord. J. Neurosci. 28 (2008), 13467–13477.
51. Hughes, E.G., Kang, S.H., Fukaya, M., et al. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16 (2013), 668–676.
52. Hunanyan, A., Garcia-Alias, G., Levine, J.M., et al. Role of chondroitin sulfate proteoglycan in axonal conduction in mammalian spinal cord. J. Neurosci. 30 (2010), 7761–7769.
53. Ip, N.Y., Wiegand, S.J., Morse, J., Rudge, J.S., Injury-induced regulation of ciliary neurotrophic factor mRNA in the adult rat brain. Eur. J. Neurosci. 5 (1993), 25–33.
54. Jones, L.L., Yamaguchi, Y., Stallcup, W.B., et al. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22 (2002), 2792–2803.
55. Kadota, R., Koda, M., Kawabe, J., et al. Granulocyte-colony-stimulating factor (G-CSF) protects oligodendrocyte and promotes hindlimb functional recovery after spinal cord injury in rats. PLoS One, 7, 2012, e50391.
56. Kang, S.H., Fukaya, M., Yang, J.K., et al. NG2+CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68 (2010), 668–681.
57. Kang, S.H., Li, Y., Fukaya, M., et al. Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis. Nat. Neurosci. 16 (2013), 571–581.
58. Kang, Z., Wang, C., Zepp, J., et al. Act1 mediates IL-17-induced EAE pathogenesis selectively in NG2+ glial cells. Nat. Neurosci., 2013, 1401–1408.
59. Karimi-Abdolrezaee, S., Billakanti, R., Reactive astrogliosis after spinal cord injury-beneficial and detrimental effects. Mol. Neurobiol. 46 (2012), 251–264.
60. Karimi-Abdolrezaee, S., Schut, D., Wang, J., et al. Chondroitinase and growth factors enhance activation and oligodendrocyte differentiation of endogenous neural precursor cells after spinal cord injury. PLoS One, 7, 2012, e37589.
61. Kim, S., Steelman, A.J., Koito, H., et al. Astrocytes promote TBF-mediated toxicity to oligodendrocyte precursors. J. Neurochem. 116 (2011), 53–66.
62. Komitova, M., Serwanski, D.R., Lu, Q.R., et al. NG2 cells are not a major source of reactive astrocytes after neocortical stab wound injury. Glia 59 (2011), 800–809.
63. Knerlich-Lukoschus, F., von der Ropp-Brenner, B., Lucius, R., et al. Chemokine expression in the white matter spinal cord precursor niche after force-defined spinal cord contusion injuries in adult rats. Glia 58 (2010), 916–931.
64. Kucharova, K., Chang, Y., Boor, A., et al. Reduced inflammation accompanies diminished myelin damage and repair in the ng2 null mouse spinal cord. J. Neuroinflamm., 13, 2011, 158.
65. Larsen, P.H., Wells, J.E., Stallcup, W.B., et al. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 23 (2003), 11127–11135.
66. Lasiene, J., Shupe, L., Perlmutter, S., et al. No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J. Neurosci. 28 (2008), 3887–3896.
67. Lee, M.Y., Kim, C.J., Shin, S.L., Moon, S.H., Chun, M.H., Increased ciliary neurotrophic factor expression in reactive astrocytes following spinal cord injury in the rat. Neurosci. Lett. 255 (1998), 79–82.
68. Lee, B.L., Yune, T.Y., Baik, S.Y., et al. Role of tumor necrosis factor-α in neuronal and glial apoptosis after spinal cord injury. Expl Neurol 166 (2000), 190–195.
69. Lee, S., Zhang, W., Ravi, M., et al. Atypical protein kinase C and par3 are required for proteoglycan-induced axon growth inhibition. J. Neurosci. 33 (2013), 2541–2554.
70. Levine, J., Stallcup, W.B., Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J. Neurosci. 7 (1987), 2721–2731.
71. Levine, J.M., Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci 14 (1994), 4716–4730.
72. Levine, J.M., Stincone, F., Lee, Y.S., Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7 (1993), 307–321.
73. Ligon, K.L., Kesari, S., Kitada, M., et al. Development of NG2 neural progenitor cells requires Olig gene function. Proc. Natl. Acad. Sci. U.S.A. 103 (2006), 7853–7858.
74. Lu, Q.R., Sun, T., Zhu, Z., et al. Common developmental requirement for Olig function indicates a motor neuron/ oligodendrocyte connection. Cell 109 (2002), 75–86.
75. Lytle, J.M., Vicini, S., Wrathall, J.R., Phenotypic changes in NG2+ cells after spinal cord injury. J. Neurotrauma 23 (2006), 1726–1738.
76. Lytle, J.M., Chittajallu, R., Wrathall, J.R., et al. NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 57 (2009), 270–285.
77. Maier, O., Fischer, R., Agresti, C., et al. TNF receptor 2 protects oligodendrocyte progenitor cells against oxidative stress. BBRC 440 (2013), 336–341.
78. Martin, S., Levine, A.K., Chen, Z.J., et al. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J. Neurosci. 21 (2001), 8119–8128.
79. Mason, J.L., Suzuki, K., Chaplin, D.D., et al. Interleukin-1beta promotes repair of the CNS. J. Neurosci. 21 (2001), 7046–7052.
80. Matsumoto, H., Kumon, Y., Watanabe, H., et al. Accumulation of macrophage-like cells expressing NG2 proteoglycan and Iba1 in ischemic core of rat brain after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 28 (2008), 149–163.
81. McKensie, I.A., Obayon, D., Li, H., Motor skill learning requires active central myelination. Science 346 (2014), 318–322.
82. McCoy, M.K., Tansey, M.G., TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflamm. 5 (2008), 45–58.
83. McTigue, D.M., Wei, P., Stokes, B.T., Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci 21 (2001), 3392–3400.
84. McTigue, D.M., Tripathi, R.B., Wei, P., NG2 co-localizes with axons and is expressed by a mixed cell population in spinal cord lesions. J. Neuropathol. Exp. Neurol 65 (2006), 406–420.
85. Nave, K., Myelination and support of axonal integrity by glia. Nature 468 (2010), 244–252.
86. Neilsen, H.M., Ek, D., Avdic, U., et al. NG2 cells, a new trail for Alzheimer's disease mechanisms?. Act Neuropath. Comm 1 (2013), 7–20.
87. Nishiyama, A., Komitova, M., Suzuki, R., et al. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10 (2009), 9–22.
88. Noble L.J., Donovan F., Igarashi T., et al., (2002) Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22, 7526–7535.
89. Ozerdem, U., Grako, K.A., Dahlin-Huppe, K., et al. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev. Dyn. 222 (2001), 218–227.
90. Patel J.R., McCandless E.E., Dorsey D., et al., (2010) CXCR4 promotes differentiation of oligodendrocyte progenitors and remyelination.Proc. Natl. Acad. Sci. U.S.A.;107:11062–11067.
91. Pendleton, J.C., Shamblot, M.J., Gary, D.S., et al. Chondriotin sulfate proteoglycans inhibit oligodendrocyte myelination through PTPσ. Exp. Neurol. 247 (2013), 113–121.
92. Peters, A., Sethares, C., Oligodendrocytes, their progenitors and other neuroglial cells in the aging primate cerebral cortex. Cereb. Cortex 14 (2004), 995–1007.
93. Petrosyan, H.A., Hunanyan, A.S., Alessi, V., et al. Neutralization of inhibitory molecule NG2 improves synaptic transmission, retrograde transport and locomotor function after spinal cord injury in adults rats. J. Neurosci. 33 (2013), 4032–4043.
94. Plemel, J.R., Keough, M.B., Duncan, G.J., Remyelination after spinal cord injury: is it a target for repair?. Prog. Neurobiol 117 (2014), 54–72.
95. Pringle, N.P., Mudhar, H.S., Collarini, E.J., et al. PDGF receptors in the rat CNS: during late neurogenesis PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115 (1992), 535–551.
96. Psachoulia, K., Jamen, F., Young, K.M., et al. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol 5 (2009), 57–67.
97. Rabchevsky, A.G., Sullivan, P.G., Scheff, S.W., Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55 (2007), 831–843.
98. Rhodes, K.E., Raivich, G., Fawcett, J.W., The injury response of oligodendrocyte precursor cells is induced by platelets, macrophages and inflammation-associated cytokines. Neuroscience 140 (2006), 87–100.
99. Rice, T., Larsen, J., Rivest, S., et al. Characterization of the early neuroinflammation after spinal cord injury in mice. J. Neuropathol. Exp. Neurol. 66 (2007), 184–195.
100. Richardson, W.D., Young, K.M., Tripathi, R.B., et al. NG2 glia as multipotent neural stem cells:fact or fantasy?. Neuron 70 (2011), 661–673.
101. Rivers, L.E., Young, K.M., Rizzi, M., et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci 11 (2008), 1392–1401.
102. Rodriguez, J.P., Coulter, M., Miotke, J., et al. Abrogation of β-catenin signaling in oligodendrocyte precursor cells reduces glial scarring and promotes axon regeneration after CNS injury. J. Neurosci. 34 (2014), 10285–10297.
103. Rolls, A., Shechter, R., London, A., Segev, Y., et al. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role inmicroglia/macrophage activation. PLoS Med, 5, 2008, e171.
104. Rosenberg, L.J., Zai, L.J., Wrathall, J.R., Chronic alterations in the cellular composition of spinal cord white matter following contusion injury. Glia 49 (2005), 107–120.
105. Sakry, D., Neitz, A., Singh, J., et al. Oligodendrocyte precursor cells modulate the neuronal network by activity-dependent ectodomain cleavage of glial NG2. PLoS Biol, 12, 2014, e10010993.
106. Seo, J.H., Miyamoto, N., Hayakawa, K., et al. Oligodendrocyte precursors induce early blood–brain barrier opening after white matter injury. J. Clin. Invest. 123 (2013), 782–786.
107. Shechter, R., Raposo, C., London, A., et al. The glial scar–monocyte interplay: a pivotal resolution phase in spinal cord repair. PLoS One, 6, 2011, e27969.
108. Simon, C., Gotz, M., Dimou, L., Progenitors in the adult cerebral cortex:cell cycle properties and regulation by physiological stimuli and injury. Glia 59 (2011), 869–881.
109. Stallcup, W.B., Beasley, L., Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J. Neurosci. 7 (1989), 2737–2744.
110. Su, Z., Yuan, Y., Chen, J., Reactive astrocytes inhibit the survival and differentiation of oligodendrocyte precursor cells by secreted TNF-α. J. Neurotrauma 28 (2011), 1089–1100.
111. Tan, A.M., Colletti, M., Rorai, A.T., et al. Antibodies against the NG2 proteoglycan promote the regeneration of sensory axons within the dorsal columns of the spinal cord. J. Neurosci. 26 (2006), 4729–4739.
112. Takahishi, N., Sakuri, T., Role of glial cells in schizophrenia: possible targets for therapeutic approaches. Neurobiol. Dis. 53 (2013), 49–60.
113. Tatsumi, K., Takebayashi, H., Manabe, T., et al. Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes. J. Neurosci. Res. 86 (2008), 3494–3502.
114. Taylor, D.L., Pirianov, G., Holland, S., et al. Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J. Neurosci. Res. 88 (2010), 1632–1644.
115. Tetzlaff, W., Okon, E.B., Karimi-Abdolrezaee, S., et al. A systematic review of cellular transplantation therapies for spinal cord injury. J. Neurotrauma 28 (2011), 1611–1682.
116. Thomas, A.M., Seidlits, S.K., Goodman, A.G., et al. Sonic hedgehog and neurotrophin-3 increase oligodendrocyte numbers and myelination after spinal cord injury. Integr. Biol. (Cambridge) 6 (2014), 694–705.
117. Totoiu, M.O., Keirstead, H.S., Spinal cord injury is accompanied by chronic progressive demyelination. J. Comp. Neurol 86 (2005), 373–383.
118. Tripathi, R., McTigue, D.M., Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia 55 (2007), 698–711.
119. Tripathi, R., McTigue, D., Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J. Comp. Neurol. 510 (2008), 129–144.
120. Uhgrin, Y., Chen, Z.J., Levine, J.M., Multiple domains of the NG2 proteoglycan mediate axon growth inhibition. J. Neurosci. 23 (2003), 175–186.
121. Wennstrom, M., Janelidze, S., Bay-Richter, C., et al. Pro-inflammatory cytokines reduce the proliferation of NG2 cells and increase shedding of NG2 in vivo and in vitro. PLoS ONE, 9, 2014, e109387.
122. Wilson, H.C., Scolding, N.J., Raine, C.S., Co-expression of PDGF α receptor and NG2 by oligodendrocyte precursors in human CNS and multiple sclerosis lesions. J. Neuroimmunol. 176 (2006), 162–173.
123. Yang, Z., Suzuki, R., Daniles, S.B., et al. NG2 glial cells provide a favorable substrate for growing axons. J. Neurosci., 26, 2006 3829-3829.
124. Yiu, G., He, Z., Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7 (2006), 617–627.
125. Zhang, H., Miller, R.H., Density-dependent feedback inhibition of oligodendrocyte precursor expansion. J. Neurosci. 16 (1996), 6886–6895.
126. Zai, L.J., Wrathall, J.R., Cell proliferation and replacement following contusive spinal cord injury. Glia 50 (2005), 247–257.
127. Zai, L.J., Yoo, S., Wrathall, J.R., Increased growth factor expression and cell proliferation after contusive spinal cord injury. Brain Res. 1052 (2005), 147–155.
128. Zawadzka, M., Rivers, L.E., Fancy, S.P., CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6 (2010), 578–590.
129. Zhou, Q., Anderson, D.J., The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109(61–73), 2002, 2002.
130. Zhu, X., Bergles, D.E., Nishiyama, A., NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135 (2008), 145–157.
131. Zhu, X., Hill, R.A., Dietrich, D., et al. Age-dependent fate and lineage restriction of single NG2 cells. Development, 138(745–753), 2011, 2011.