Central canal ependymal cells proliferate extensively in response to traumatic spinal cord injury but not demyelinating lesions

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lacroix, Steve ^b   Hamilton, Laura K ^a   Vaugeois, Alexandre ^a   Beaudoin, Stéfanny ^a   Breault Dugas, Christian ^a   Pineau, Isabelle ^b   Lévesque, Sébastien A ^b   Grégoire, Catherine Alexandra ^a   Fernandes, Karl J L ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CENTRAL CANAL; CONTROLLED STUDY; DEMYELINATION; EPENDYMA CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; LOCOMOTION; NONHUMAN; REMYELINIZATION; SPINAL CORD; SPINAL CORD INJURY; SPINAL CORD REGENERATION;

ADULT; ANALYSIS OF VARIANCE; ANIMALS; CELL PROLIFERATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPENDYMA; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LAMINECTOMY; LYSOPHOSPHATIDYLCHOLINES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NEURAL STEM CELLS; SPINAL CANAL; SPINAL CORD INJURIES;

EID: 84899949840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085916     Document Type: Article

References (40)

1. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, et al. (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6: e182.
2. Hamilton LK, Truong MK, Bednarczyk MR, Aumont A, Fernandes KJ (2009) Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience 164: 1044-1056.
3. Bruni JE, Reddy K (1987) Ependyma of the central canal of the rat spinal cord: a light and transmission electron microscopic study. J Anat 152: 55-70. (Pubitemid 17121524)
4. Bruni JE (1998) Ependymal development, proliferation, and functions: a review. Microsc Res Tech 41: 2-13.
5. Rafols JA, Goshgarian HG (1985) Spinal tanycytes in the adult rat: a correlative Golgi gold-toning study. Anat Rec 211: 75-86. (Pubitemid 15174477)
6. Yu K, McGlynn S, Matise MP (2013) Floor plate-derived sonic hedgehog regulates glial and ependymal cell fates in the developing spinal cord. Development 140: 1594-1604.
7. Fu H, Qi Y, Tan M, Cai J, Hu X, et al. (2003) Molecular mapping of the origin of postnatal spinal cord ependymal cells: evidence that adult ependymal cells are derived from Nkx6.1+ ventral neural progenitor cells. J Comp Neurol 456: 237-244. (Pubitemid 36110246)
8. Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, et al. (2006) Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 293: 358-369.
9. Ferretti P, Zhang F, O'Neill P (2003) Changes in spinal cord regenerative ability through phylogenesis and development: lessons to be learnt. Dev Dyn 226: 245-256. (Pubitemid 36158169)
10. McHedlishvili L, Mazurov V, Grassme KS, Goehler K, Robl B, et al. (2012) Reconstitution of the central and peripheral nervous system during salamander tail regeneration. Proc Natl Acad Sci U S A 109: E2258-2266.
11. Tanaka EM, Ferretti P (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10: 713-723.
12. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, et al. (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34. (Pubitemid 29044150)
13. Alfaro-Cervello C, Soriano-Navarro M, Mirzadeh Z, Alvarez-Buylla A, Garcia-Verdugo JM (2012) Biciliated ependymal cell proliferation contributes to spinal cord growth. J Comp Neurol 520: 3528-3552.
14. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, et al. (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20: 2218-2228. (Pubitemid 30230075)
15. David S, Lacroix S (2003) Molecular approaches to spinal cord repair. Annu Rev Neurosci 26: 411-440. (Pubitemid 37064940)
16. Rossignol S, Frigon A (2011) Recovery of locomotion after spinal cord injury: some facts and mechanisms. Annu Rev Neurosci 34: 413-440.
17. Barnabe-Heider F, Goritz C, Sabelstrom H, Takebayashi H, Pfrieger FW, et al. (2010) Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7: 470-482.
18. Sabelstrom H, Stenudd M, Reu P, Dias DO, Elfineh M, et al. (2013) Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 342: 637-640.
19. Namiki J, Tator CH (1999) Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 58: 489-498. (Pubitemid 29220742)
20. Mothe AJ, Tator CH (2005) Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 131: 177-187. (Pubitemid 40170498)
21. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U (1995) Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131: 453-464.
22. Sabelstrom H, Stenudd M, Frisen J (2013) Neural stem cells in the adult spinal cord. Exp Neurol.
23. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE, Jr. (2003) Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 20: 179-193. (Pubitemid 36292827)
24. Ghasemlou N, Jeong SY, Lacroix S, David S (2007) T cells contribute to lysophosphatidylcholine-induced macrophage activation and demyelination in the CNS. Glia 55: 294-302. (Pubitemid 46225961)
25. Stromnes IM, Goverman JM (2006) Active induction of experimental allergic encephalomyelitis. Nat Protoc 1: 1810-1819. (Pubitemid 46773300)
26. Pineau I, Lacroix S (2007) Proinflammatory cytokine synthesis in the injured mouse spinal cord: multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 500: 267-285. (Pubitemid 44937122)
27. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, et al. (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23: 635-659. (Pubitemid 43728052)
28. Nishi RA, Liu H, Chu Y, Hamamura M, Su MY, et al. (2007) Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J Neurotrauma 24: 674-689. (Pubitemid 46996027)
29. Ousman SS, David S (2000) Lysophosphatidylcholine induces rapid recruitment and activation of macrophages in the adult mouse spinal cord. Glia 30: 92-104. (Pubitemid 30172156)
30. Blakemore WF, Franklin RJ (2008) Remyelination in experimental models of toxin-induced demyelination. Curr Top Microbiol Immunol 318: 193-212.
31. Ghasemlou N, Kerr BJ, David S (2005) Tissue displacement and impact force are important contributors to outcome after spinal cord contusion injury. Exp Neurol 196: 9-17. (Pubitemid 41416645)
32. Lee JY, Kim HS, Choi HY, Oh TH, Yune TY (2012) Fluoxetine inhibits matrix metalloprotease activation and prevents disruption of blood-spinal cord barrier after spinal cord injury. Brain 135: 2375-2389.
33. Lu P, Wang Y, Graham L, McHale K, Gao M, et al. (2012) Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150: 1264-1273.
34. Hofstetter CP, Holmstrom NA, Lilja JA, Schweinhardt P, Hao J, et al. (2005) Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8: 346-353. (Pubitemid 40300192)
35. Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, et al. (2002) Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A 99: 13211-13216.
36. Aharoni R, Herschkovitz A, Eilam R, Blumberg-Hazan M, Sela M, et al. (2008) Demyelination arrest and remyelination induced by glatiramer acetate treatment of experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 105: 11358-11363.
37. Girolamo F, Ferrara G, Strippoli M, Rizzi M, Errede M, et al. (2011) Cerebral cortex demyelination and oligodendrocyte precursor response to experimental autoimmune encephalomyelitis. Neurobiol Dis 43: 678-689.
38. Guo F, Maeda Y, Ma J, Delgado M, Sohn J, et al. (2011) Macroglial plasticity and the origins of reactive astroglia in experimental autoimmune encephalomyelitis. J Neurosci 31: 11914-11928.
39. Chi L, Ke Y, Luo C, Li B, Gozal D, et al. (2006) Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24: 34-43.
40. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, et al. (2009) Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 29: 11511-11522.