The ameboid phenotype of NG2 (+) cells in the region of apoptotic dentate granule neurons in trimethyltin intoxicated mice shares antigen properties with microglia/macrophages

GLIA

Volumn 56, Issue 2, 2008, Pages 209-222

  Fiedorowicz, Anna ^a   Figiel, Izabela ^a   Zaremba, Małgorzata ^a   Dzwonek, Karolina ^a   Oderfeld Nowak, Barbara ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Hippocampus; Microglia; Neurodegeneration; Neurotoxicity; NG2+ cells

Indexed keywords

ANTIBODY; ANTIGEN; NESTIN; O4 ANTIBODY; OX42 ANTIGEN; TRIMETHYLTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; COLON POLYPOSIS; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GRANULE CELL; IMMUNOCYTOCHEMISTRY; INTOXICATION; MACROPHAGE; MICROGLIA; MOUSE; MOUSE STRAIN; NERVE DEGENERATION; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STELLATE CELL;

ANIMALS; ANTIGENS; ANTIGENS, CD11B; APOPTOSIS; DENTATE GYRUS; DNA FRAGMENTATION; ECTODYSPLASINS; FEMALE; GENE EXPRESSION; IN SITU NICK-END LABELING; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, INBRED BALB C; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; NEUROTOXINS; O ANTIGENS; PROTEOGLYCANS; TIME FACTORS; TRIMETHYLTIN COMPOUNDS;

EID: 37349108615     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20605     Document Type: Article

References (58)

1. Aguirre A, Chittajallu R, Belachew S, Gallo V. 2004. NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J Cell Biol 165:575-589,
2. Aguirre A, Gallo V. 2004. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci 24:10530-10541.
3. Alonso G. 2005. NG2 proteoglycan-expressing cells of the adult rat brain: Possible involvement in the formation of glial scar astrocytes following stab wound. Glia 49:318-338.
4. Barral-Moran MJ, Calaora V, Vutskits L, Wang C, Zhang H, Durbec P, Rougon G, Kiss JZ. 2003. Oligodendrocyte progenitor migration in response to injury of glial monolayers requires the polysialic neural cell-adhesion molecule. J Neurosci Res 72:679-690.
5. Berry M, Hubbard P, Butt AM. 2002. Cytology and lineage of NG2-positive glia. J Neurocytol 31:457-467.
6. Bruccoleri A, Brown H, Harry GJ. 1998. Cellular localization and temporal elevation of tumor necrosis factor-α, interleukin-1 α, and transforming growth factor-β 1 mRNA in hippocampal injury response induced by trimethyltin. J Neurochem 71:1577-1587.
7. Bu J, Akhtar N, Nishiyama A. 2001. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 34:296-310.
8. Butt AM, Kiff J, Hubbard P, Berry M. 2002. Synantocytes: New functions for novel NG2 expressing glia. J Neurocytol 31:551-565.
9. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M. 2005. Synantocytes: The fifth element. J Anat 207:695-706.
10. Casella GT, Bunge MB, Wood PM. 2004. Improved immunocytochemical identification of neural, endothelial, and inflammatory cell types in paraffin-embedded injured adult rat spinal cord. J Neurosci Methods 139:1-11.
11. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. 2000. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20:6404-6412.
12. Chari DM, Blakemore WF. 2002. Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 37:307-313.
13. Dawson MR, Levine JM, Reynolds R. 2000. NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors? J Neurosci Res 61:471-479.
14. Dehn D, Burbach GJ, Schafer R, Deller T. 2006. NG2 upregulation in the denervated rat fascia dentata following unilateral entorhinal cortex lesion. Glia 53:491-500.
15. Di Bello IC, Dawson MR, Levine JM, Reynolds R. 1999. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J Neurocytol 28:365-381.
16. Diers-Fenger M, Kirchhoff F, Kettenmann H, Levine JM, Trotter J. 2001. AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: Isolation, differentiation, and association with radial glia. Glia 34:213-228.
17. Eglitis MA, Mezey E. 1997. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA 94:4080-4085.
18. Fedoroff S, Zhai R, Novak JP. 1997. Microglia and astroglia have a common progenitor cell. J Neurosci Res 50:477-486.
19. Fiedorowicz A, Figiel I, Kaminska B, Zaremba M, Wilk S, Oderfeld-Nowak B. 2001. Dentate granule neuron apoptosis and glia activation in murine hippocampus induced by trimethyltin exposure. Brain Res 912:116-127.
20. Frisen J. 2002. Stem cell plasticity? Neuron 35:415-418.
21. Greenwood K, Butt AM. 2003. Evidence that perinatal and adult NG2-glia are not conventional oligodendrocyte progenitors and do not depend on axons for their survival. Mol Cell Neurosci 23:544-558.
22. Hampton DW, Rhodes KE, Zhao C, Franklin RJ, Fawcett JW. 2004. The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127: 813-820.
23. Hao C, Richardson A, Fedoroff S. 1991. Macrophage-like cells originate from neuroepithelium in culture: Characterization and properties of the macrophage-like cells. Int J Dev Neurosci 9:1-14.
24. Hickey WF. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36:118-124.
25. Hirata K, Kawabuchi M. 2002. Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microsc Res Tech 57:541-547.
26. Horner PJ, Thallmair M, Gage FH. 2002. Defining the NG2-expressing cell of the adult CNS. J Neurocytol 31:469-480.
27. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. 2002. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22:2792-2803.
28. Koczyk D, Oderfeld-Nowak B. 2000. Long-term microglial and astroglial activation in the hippocampus of trimethyltin-intoxicated rat: Stimulation of NGF and TrkA immunoreactivities in astroglia but not in microglia. Int J Dev Neurosci 18:591-606.
29. Kronenberg G, Wang LP, Synowitz M, Gertz K, Katchanov J, Glass R, Harms C, Kempermann G, Kettenmann H, Endres M. 2005. Nestin-expresing cells divide and adopt a complex electrophysiologic phenotype after transient brain ischemia. J Cereb Blood Flow Metab 25: 1613-1624.
30. Ladeby R, Wirenfeldt M, Dalmau I, Gregersen R, Garcia-Ovejero D, Babcock A, Owens T, Finsen B. 2005. Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury. Glia 50:121-131.
31. Levine JM, Enquist L, Card JP. 1998. Reactions of oligodendrocyte precursor cells to α herpesvirus infection of the central nervous system. Glia 23:316-328.
32. Levine JM, Reynolds R, Fawcett JW. 2001. The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24:39-47.
33. Li G, Crang AJ, Rundle JL, Blakemore WF. 2002. Oligodendrocyte progenitor cells in the adult rat CNS express myelin oligodendrocyte glycoprotein (MOG). Brain Pathol 12:463-471.
34. Little AR, Benkovic SA, Miller DB, O'Callaghan JP. 2002. Chemically induced neuronal damage and gliosis: Enhanced expression of the proinflammatory chemokine, monocyte chemoattractant protein (MCP)-1, without a corresponding increase in proinflammatory cytokines. Neuroscience 115:307-320.
35. Matsumoto H, Kumon Y, Watanabe H, Ohnishi T, Shudou M, Chuai M, Imai Y, Takahashi H, Tanaka J. 2007. 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 1-15; Epub ahead print.
36. 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.
37. Nielsen HH, Ladeby R, Drojdahl N, Peterson AC, Finsen B. 2006. Axonal degeneration stimulates the formation of NG2+ cells and oligodendrocytes in the mouse. Glia 54:105-115.
38. Nishiyama A. 2007. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13:62-75.
39. Nishiyama A, Chang A, Trapp BD. 1999. NG2+ glial cells: A novel glial cell population in the adult brain. J Neuropathol Exp Neurol 58:1113-1124.
40. Nishiyama A, Yu M, Drazba JA, Tuohy VK. 1997. Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. J Neurosci Res 48:299-312.
41. Nishiyama A, Watanabe M, Yang Z, Bu J. 2002. Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. J Neurocytol 31:437-455.
42. Ogita K, Nitta Y, Watanabe M, Nakatani Y, Nishiyama N, Sugiyama C, Yoneda Y. 2004. In vivo activation of c-Jun N-terminal kinase signaling cascade prior to granule cell death induced by trimethyltin in the dentate gyrus of mice. Neuropharmacology 47:619-630.
43. Ogita K, Nishiyama N, Sugiyama C, Higuchi K, Yoneyama M, Yoneda Y. 2005. Regeneration of granule neurons after lesioning of hippocampal dentate gyrus: Evaluation using adult mice treated with trimethyltin chloride as a model. J Neurosci Res 82:609-621.
44. Ong WY, Levine JM. 1999. A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience 92:83-95.
45. Peters A. 2004. A fourth type of neuroglial cell in the adult central nervous system. J Neurocytol 33:345-357.
46. Polito A, Reynolds R. 2005. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707-716.
47. Pouly S, Becher B, Blain M, Antel JP. 1999. Expression of a homologue of rat NG2 on human microglia. Glia 27:259-268.
48. Rakic S, Zecevic N. 2003. Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 41:117-127.
49. Reynolds R, Hardy R. 1997. Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 47:455-470.
50. Rezajooi K, Pavlides M, Winterbottom J, Stallcup WB, Hamlyn PJ, Lieberman AR, Anderson PN. 2004. NG2 proteoglycan expression in the peripheral nervous system: Upregulation following injury and comparison with CNS lesions. Mol Cell Neurosci 25:572-584.
51. Schilling M, Besselmann M, Leonhard C, Mueller M, Ringelstein EB, Kiefer R. 2003. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: A study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 183:25-33.
52. Schilling M, Besselmann M, Muller M, Strecker JK, Ringelstein EB, Kiefer R. 2005. Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: An investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 196:290-297.
53. Sellers DL, Horner P. 2005. Instructive niches: Environmental instructions that confound NG2 proteoglycan expression and the fate-restriction of CNS progenitore. J Anat 207:727-734.
54. Tanaka K, Nogawa S, Ito D, Suzuki S, Dembo T, Kosakai A, Fukuuchi Y. 2001. Activation of NG2-positive oligodendrocyte progenitor cells during post-ischemic reperfusion in the rat brain. Neuroreport 12:2169-2174.
55. Tatsumi K, Haga S, Matsuyoshi H, Inoue M, Manabe T, Makinodan M, Wanaka A. 2005. Characterization of cells with proliferative activity after a brain injury. Neurochem Int 46:381-389.
56. Yokoyama A, Sakamoto A, Kameda K, Imai Y, Tanaka J. 2006. NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathological brains. Glia 53:754-768.
57. Yokoyama A, Yang L, Itoh S, Mori K, Tanaka J. 2004. Microglia, a potential source of neurons, astrocytes and oligodendrocytes. Glia 45:96-104.
58. Zhang Y, Tohyama K, Winterbottom JK, Hague NS, Schachner M, Lieberman AR, Anderson PN. 2001. Correlation between putative inhibitory molecules at the dorsal root entry zone and failure of dorsal root axonal regeneration. Mol Cell Neurosci 17:444-459.