Chronic oligodendrogenesis and remyelination after spinal cord injury in mice and rats

Journal of Neuroscience

Volumn 35, Issue 3, 2015, Pages 1274-1290

  Hesp, Zoe C ^a   Goldstein, Evan A ^a   Miranda, Carlos J ^b   Kaspar, Brain K ^a,b   McTigue, Dana M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

Demyelination; Glial scar; Growth factor; NG2 cell; Stem cell; Transplant

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CILIARY NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; INHIBITOR OF DIFFERENTIATION 2; JANUS KINASE; MYELIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STAT PROTEIN; TAMOXIFEN; TRANSCRIPTION FACTOR HES 5; TRANSCRIPTION FACTOR SOX11;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CHRONIC OLIGODENDROGENESIS; CONTROLLED STUDY; FEMALE; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; REGENERATION; REMYELINIZATION; SPINAL CORD INJURY; STEM CELL; ANIMAL; CELL DIFFERENTIATION; CONVALESCENCE; CYTOLOGY; DEMYELINATING DISEASE; NERVE REGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL DIFFERENTIATION; DEMYELINATING DISEASES; FEMALE; MALE; MICE; NERVE REGENERATION; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84921465792     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2568-14.2015     Document Type: Article

References (57)

1. Barnabé-Heider F, Göritz C, Sabelström H, Takebayashi H, Pfrieger FW, Meletis K, Frisén J (2010) Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7:470-482. CrossRef Medline
2. Baron W, Metz B, Bansal R, Hoekstra D, de Vries H (2000) PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 15:314-329. CrossRef Medline
3. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295. Medline
4. Barres BA, Burne JF, Holtmann B, Thoenen H, Sendtner M, Raff MC (1996) Ciliary neurotrophic factor enhances the rate of oligodendrocyte generation. Mol Cell Neurosci 8:146-156. CrossRef Medline
5. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, Kim DH, Whittemore SR (2010) Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 30:2989-3001. CrossRef Medline
6. Cheng X, Wang Y, He Q, Qiu M, Whittemore SR, Cao Q (2007) Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 25:3204-3214. CrossRef Medline
7. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76. CrossRef Medline
8. Daneman R, Zhou L, Kebede AA, Barres BA (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468:562-566. CrossRef Medline
9. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24:476-788. CrossRef Medline
10. Dell'Albani P, Kahn MA, Cole R, Condorelli DF, Giuffrida-Stella AM, de Vellis J (1998) Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J Neurosci Res 54:191-205. CrossRef Medline
11. Gledhill RF, Harrison BM, McDonald WI (1973) Demyelination and remyelination after acute spinal cord compression. Exp Neurol 38:472-487. CrossRef Medline
12. Grossman SD, Rosenberg LJ, Wrathall JR (2001) Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 168:273-282. CrossRef Medline
13. Harrison BM, Gledhill RF, McDonald WJ (1975) Remyelination after transient compression of the spinal cord. Proc Aust Assoc Neurol 12:117-122. Medline
14. Horky LL, Galimi F, Gage FH, Horner PJ (2006) Fate of endogenous stem/ progenitor cells following spinal cord injury. J Comp Neurol 498:525-538. CrossRef Medline
15. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:2218-2228. Medline
16. Horner PJ, Thallmair M, Gage FH (2002) Defining the NG2-expressing cell of the adult CNS. J Neurocytol 31:469-480. CrossRef Medline
17. + CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:668-681. CrossRef Medline
18. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG (2006) Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26:3377-3389. CrossRef Medline
19. Keirstead HS, Blakemore WF (1997) Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J Neuropathol Exp Neurol 56:1191-1201. CrossRef Medline
20. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705. CrossRef Medline
21. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG (2007) Tolllike receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 102:37-50. CrossRef Medline
22. Lasiene J, Shupe L, Perlmutter S, Horner P (2008) No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 28:3887-3896. CrossRef Medline
23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(Delta Delta C(T)) Method. Methods 25:402-408. CrossRef Medline
24. Lytle JM, Wrathall JR (2007) Glial cell loss, proliferation and replacement in the contused murine spinal cord. Eur J Neurosci 25:1711-1724. CrossRef Medline
25. + cells after spinal cord injury. J Neurotrauma 23:1726-1738. CrossRef Medline
26. Lytle JM, Chittajallu R, Wrathall JR, Gallo V (2009) NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 57:270-285. CrossRef Medline
27. Mayer M, Bhakoo K, Noble M (1994) Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development 120:143-153. Medline
28. McTigue DM, Tripathi RB (2008) The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem 107:1-19. CrossRef Medline
29. McTigue DM, Wei P, Stokes BT (2001) Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 21:3392-3400. Medline
30. Mekhail M, Almazan G, Tabrizian M (2012) Oligodendrocyte-protection and remyelination post-spinal cord injuries: a review. Prog Neurobiol 96:322-339. CrossRef Medline
31. Meletis K, Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, Frisén J (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6:e182. CrossRef Medline
32. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluroescent Cre reporter mouse. Genesis 45:593-605. CrossRef Medline
33. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Colocalization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314. CrossRef Medline
34. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22. CrossRef Medline
35. Plemel JR, Chojnacki A, Sparling JS, Liu J, Plunet W, Duncan GJ, Park SE, Weiss S, Tetzlaff W (2011) Platelet-derived growth factor-responsive neural precursors give rise to myelinating oligodendrocytes after transplantation into the spinal cords of contused rats and dysmyelinated mice. Glia 59:1891-1910. CrossRef Medline
36. Plemel JR, Keough MB, Duncan GJ, Sparling JS, Yong VW, Stys PK, Tetzlaff W (2014) Remyelination after spinal cord injury: is it a target for repair? Prog Neurobiol 117:54-72. CrossRef Medline
37. Porlan E, Morante-Redolat JM, Marqués-Torrejón MÁ, Andreu-AgullóC, Carneiro C, Gómez-Ibarlucea E, Soto A, Vidal A, Ferrón SR, Fariñas I (2013) Transcriptional repression of Bmp2 by p21Waf1/Cip1 links quiescence to neural stem cell maintenance. Nat Neurosci 16:1567-1575. CrossRef Medline
38. Powers BE, Sellers DL, Lovelett EA, Cheung W, Aalami SP, Zapertov N, Maris DO, Horner PJ (2013) Remyelination reporter reveals prolonged refinement of spontaneously regenerated myelin. Proc Natl Acad Sci U S A 110:4075-4080. CrossRef Medline
39. Psachoulia K, Jamen F, Young KM, Richardson WD (2009) Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biology 5:57-67. CrossRef Medline
40. Rabchevsky AG, Sullivan PG, Scheff SW (2007) Temporal-spatial dynamics of oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55:831-843. CrossRef Medline
41. Richardson WD, Young KM, Tripathi RB, McKenzie I (2011) NG2-glia as multipotent neural stem cells-fact or fantasy? Neuron 70:661-673. CrossRef Medline
42. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392-1401. CrossRef Medline
43. Rosenberg LJ, Zai LJ, Wrathall JR (2005) Chronic alternations in the cellular composition of spinal cord white matter following contusion injury. Glia 49:107-120. CrossRef Medline
44. Salehi Z, Hadiyan SP, Navidi R (2013) Ciliary neurotrophic factor role in myelin oligodendrocyte glycoprotein expression in Cuprizone-induced multiple sclerosis mice. Cell Mol Neurobiol 33:531-535. CrossRef Medline
45. Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131:4131-4142. CrossRef Medline
46. See J, Zhang X, Eraydin N, Mun SB, Mamontov P, Golden JA, Grinspan JB (2004) Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol Cell Neurosci 26:481-492. CrossRef Medline
47. Sellers DL, Maris DO, Horner PJ (2009) Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. J Neurosci 29(20)6722-6733. CrossRef
48. Sun Y, Xu CC, Li J, Guan XY, Gao L, Ma LX, Li RX, Peng YW, Zhu GP (2013) Transplantation of oligodendrocyte precursor cells improves locomotor deficits in rats with spinal cord irradiation injury. PLoS ONE 8:e57534. CrossRef Medline
49. Swiss VA, Nguyen T, Dugas J, Ibrahim A, Barres B, Androulakis IP, Casaccia P (2011) Identification of a gene regulatory network necessary for the initiation of oligodendrocyte differentiation. PLoS ONE 6:e18088. CrossRef Medline
50. Tashiro A, Zhao C, Gage FH (2006) Retrovirus-mediated single-cell gene knockout technique in adult newborn neurons in vivo. Nat Protoc 1:3049-3055. CrossRef Medline
51. Tripathi R, McTigue DM (2007) Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia 55:698-711. CrossRef Medline
52. Tripathi RB, McTigue DM (2008) Chronically increase ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J Comp Neurol 510:129-144. CrossRef Medline
53. Tripathi RB, Rivers LE, Young KM, Jamen F, Richardson WD (2010) NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J Neurosci 30:16383-16390. CrossRef Medline
54. Vernerey J, Macchi M, Magalon K, Cayre M, Durbec P (2013) Ciliary neurotrophic factor controls progenitor migration during remyelination in the adult rodent brain. J Neurosci 33:3240-3250. CrossRef Medline
55. Watanabe M, Toyama Y, Nishiyama A (2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69:826-836. CrossRef Medline
56. Yokogami K, Wakisaka S, Avruch J, Reeves SA (2000) Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol 10:47-50. CrossRef Medline
57. Zai LJ, Wrathall JR (2005) Cell proliferation and replacement following contusive spinal cord injury. Glia 50:247-257. CrossRef Medline