Interaction of NG2+ glial progenitors and microglia/macrophages from the injured spinal cord

GLIA

Volumn 58, Issue 4, 2010, Pages 410-422

  Wu, Junfang ^a   Yoo, Soonmoon ^a,c   Wilcock, Donna ^b   Lytle, Judith M ^a   Leung, Philberta Y ^a   Colton, Carol A ^b   Wrathall, Jean R ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

Author keywords

Cell culture; Glial progenitors; Macrophage; MACS; NG2; Proliferation; Spinal cord injury

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GELATINASE B; THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL CULTURE; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; IBA1 GENE; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; MACROPHAGE; MARKER GENE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SPINAL CORD INJURY; STATISTICAL ANALYSIS;

ANIMALS; ANTIGENS; ASTROCYTES; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; FEMALE; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICROGLIA; NEUROGLIA; PROTEOGLYCANS; RATS; SPINAL CORD INJURIES; STEM CELLS; THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 76549094517     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20932     Document Type: Article

References (43)

1. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W. 1997. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463.
2. Butt AM, Kiff J, Hubbard P, Berry M. 2002. Synantocytes: New functions for novel NG2 expressing glia. J Neurocytol 31:551-565.
3. Cao Q, Xu XM, Devries WH, Enzmann GU, Ping P, Tsoulfas P, Wood PM, Bunge MB, Whittemore SR. 2005. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J Neurosci 25:6947-6957.
4. Colton CA, Mott RT, Sharpe H, Xu Q, Van Nostrand WE, Vitek MP. 2006. Expression profiles for macrophage alternative activation genes in AD, in mouse models of AD. J Neuroinflammation 3:27.
5. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, Gage FH, Anderson AJ. 2005. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci USA 102:14069-14074.
6. Franklin RJ, Kotter MR. 2008. The biology of CNS remyelination: The key to therapeutic advances. J Neurol 255 (Suppl 1):19-25.
7. Frost EE, Nielsen JA, Le TQ, Armstrong RC. 2003. PDGF and FGF2 regulate oligodendrocyte progenitor responses to demyelination. J Neurobiol 54:457-472.
8. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3:23-35.
9. 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.
10. Hagg T, Oudega M. 2006. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23:264-280.
11. Hamanoue M, Yoshioka A, Ohashi T, Eto Y, Takamatsu K. 2004. NF-kappaB prevents TNF-alpha-induced apoptosis in an oligodendrocyte cell line. Neurochem Res 29:1571-1576.
12. 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.
13. 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.
14. Jakovcevski I, Wu J, Karl N, Leshchyns'ka I, Sytnyk V, Chen J, Irintchev A, Schachner M. 2007. Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 27:7222-7233.
15. Larsen PH, Wells JE, Stallcup WB, Opdenakker G, Yong VW. 2003. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J Neurosci 23:11127-11135.
16. Liu Y, Ford BD, Mann MA, Fischbach GD. 2005. Neuregulin-1 increases the proliferation of neuronal progenitors from embryonic neural stem cells. Dev Biol 283:437-445.
17. Lu FG, Wong CS. 2007. Time-dependent neurosphere-forming ability of adult rat spinal cord after irradiation. Radiat Res 168:453-461.
18. 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.
19. Lytle JM, Wrathall JR. 2007. Glial cell loss, proliferation and replacement in the contused murine spinal cord. Eur J Neurosci 25:1711-1724.
20. Margosio B, Marchetti D, Vergani V, Giavazzi R, Rusnati M, Presta M, Taraboletti G. 2003. Thrombospondin 1 as a scavenger for matrix-associated fibroblast growth factor 2. Blood 102:4399-4406.
21. Martinez FO, Sica A, Mantovani A, Locati M. 2008. Macrophage activation and polarization. Front Biosci 13:453-461.
22. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW. 1999. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5:1410-1412.
23. McTigue DM, Tripathi R, Wei P. 2006. NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions. J Neuropathol Exp Neurol 65:406-420.
24. 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.
25. Mocchetti I, Rabin SJ, Colangelo AM, Whittemore SR, Wrathall JR. 1996. Increased basic fibroblast growth factor expression following contusive spinal cord injury. Exp Neurol 141:154-164.
26. Nishiyama A. 2007. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13:62-76.
27. Noble LJ, Donovan F, Igarashi T, Goussev S, Werb Z. 2002. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci 22:7526-7535.
28. Oh LY, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW. 1999. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 19:8464-8475.
29. Ostenfeld T, Svendsen CN. 2004. Requirement for neurogenesis to proceed through the division of neuronal progenitors following differentiation of epidermal growth factor and fibroblast growth factor-2-responsive human neural stem cells. Stem Cells 22:798-811.
30. Popovich PG, Wei P, Stokes BT. 1997. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 377:443-464.
31. Rabchevsky AG, Sullivan PG, Scheff SW. 2007. Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55:831-843.
32. Rosenberg LJ, Teng YD, Wrathall JR. 1999. 2,3-Dihydroxy-6-nitro-7- sulfamoyl-benzo(f)quinoxaline reduces glial loss and acute white matter pathology after experimental spinal cord contusion. J Neurosci 19:464-475.
33. Rosenberg LJ, Wrathall JR. 1997. Quantitative analysis of acute axonal pathology in experimental spinal cord contusion. J Neurotrauma 14:823-838.
34. Rosenberg LJ, Zai LJ, Wrathall JR. 2005. Chronic alterations in the cellular composition of spinal cord white matter following contusion injury. Glia 49:107-120.
35. Schonberg DL, Popovich PG, McTigue DM. 2007. Oligodendrocyte generation is differentially influenced by toll-like receptor (TLR) 2 and TLR4-mediated intraspinal macrophage activation. J Neuropathol Exp Neurol 66:1124-1135.
36. Shihabuddin LS, Ray J, Gage FH. 1997. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148:577-586.
37. Uhm JH, Dooley NP, Oh LY, Yong VW. 1998. Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 22:53-63.
38. Wrathall JR, Li W, Hudson LD. 1998. Myelin gene expression after experimental contusive spinal cord injury. J Neurosci 18:8780-8793. Wrathall JR, Pettegrew RK, Harvey F. 1985. Spinal cord contusion in the rat: Production of graded, reproducible, injury groups. Exp Neurol 88:108-122.
39. Ye P, D'Ercole AJ. 1999. Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-alpha-induced injury. Endocrinology 140:3063-3072.
40. Yoo S, Wrathall JR. 2007. Mixed primary culture and clonal analysis provide evidence that NG2 proteoglycan-expressing cells after spinal cord injury are glial progenitors. Dev Neurobiol 67:860-874.
41. Yuan X, Chittajallu R, Belachew S, Anderson S, McBain CJ, Gallo V. 2002. Expression of the green fluorescent protein in the oligodendrocyte lineage: A transgenic mouse for developmental and physiological studies. J Neurosci Res 70:529-545.
42. Yune TY, Lee JY, Jung GY, Kim SJ, Jiang MH, Kim YC, Oh YJ, Markelonis GJ, Oh TH. 2007. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci 27:7751-7761.
43. Zai LJ, Wrathall JR. 2005. Cell proliferation and replacement following contusive spinal cord injury. Glia 50:247-257.