The 6-hydroxydopamine-induced nigrostriatal neurodegeneration produces microglia-like NG2 glial cells in the rat substantia nigra

GLIA

Volumn 58, Issue 14, 2010, Pages 1686-1700

  Kitamura, Yoshihisa ^a   Inden, Masatoshi ^a,b   Minamino, Hideaki ^a   Abe, Mari ^a   Takata, Kazuyuki ^a   Taniguchi, Takashi ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

Dopamine neurons; Microglia; Neuron glial 2; Neuroprotection; Parkinson's disease

Indexed keywords

CELL MARKER; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL SURVIVAL; GLIA CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INJECTION; MESENCEPHALON; MICROGLIA; NERVE DEGENERATION; NEURON GLIAL 2; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; PERIKARYON; PRIORITY JOURNAL; RAT; STEM CELL; STEREOMETRY; SUBSTANTIA NIGRA; WISTAR RAT;

ANIMALS; ANTIGENS; BIOLOGICAL MARKERS; CORPUS STRIATUM; CYTOPROTECTION; DISEASE MODELS, ANIMAL; MICROGLIA; NEURAL PATHWAYS; OXIDOPAMINE; PARKINSONIAN DISORDERS; PROTEOGLYCANS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA;

EID: 78349253758     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21040     Document Type: Article

References (49)

1. Banati RB, Daniel SE, Blunt SB. 1998. Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinson's disease. Mov Disord 13: 221-227.
2. Batchelor PE, Liberatore GT, Wong JYF, Porritt MJ, Frerichs F, Donnan GA, Howells DW. 1999. Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J Neurosci 19: 1708-1716.
3. Bergles DE, Roberts JD, Somogyi P, Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405: 187-191.
4. Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nat Rev Neurosci 8: 57-69.
5. 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.
6. Butt AM, Duncan A, Berry M. 1999. Astrocyte associations with nodes of Ranvier: Ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve. J Neurocytol 23: 486-499.
7. Butt AM, Kiff J, Hubbard P, Berry M. 2002. Synatocytes: New functions for novel NG2 expressing glia. J Neurocytol 31: 551-565.
8. Cassarino DS, Fall CP, Swerdlow RH, Smith TS, Halvorsen EM, Miller SW, Parks JP, Parker WDJr, Bennnett JPJr. 1997. Elevated reactive oxygen species and antioxidant enzyme activities in animal and cellular models of Parkinson's disease. Biochim Biophys Acta 1362: 77-86.
9. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK. 1992. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149: 2736-2741.
10. Cicchetti F, Brownell AL, Williams K, Chen YI, Livni E, Isacson O. 2002. Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 15: 991-998.
11. Depino AM, Earl C, Kaczmarczyk E, Ferrari C, Besedovsky H, del Rey A, Pitossi FJ, Oertel WH. 2003. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur J Neurosci 18: 2731-2742.
12. Esposito E, Di Matteo V, Benigno A, Pierucci M, Crescimanno G, Di Giovanni G. 2007. Non-steroidal anti-inflammatory drugs in Parkinson's disease. Exp Neurol 205: 295-312.
13. Fiedorowicz A, Figiel I, Zaremba M, Dzwonek K, Oderfeld-Nowak B. 2008. 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 56: 209-222.
14. 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.
15. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
16. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. 1996. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224: 855-862.
17. Inden M, Taira T, Kitamura Y, Yanagida T, Tsuchiya T, Takata K, Yanagisawa D, Nishimura K, Taniguchi T, Kiso Y, Yoshimoto K, Agatsuma T, Koide-Yoshida S, Iguchi-Ariga SM, Shimohama S, Ariga H. 2006. PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson's disease rat model. Neurobiol Dis 24: 144-158.
18. 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.
19. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. 2000. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: Role of microglia. J Neurosci 20: 6309-6316.
20. Kitamura Y, Nomura Y. 2003. Stress proteins and glial functions: Possible therapeutic targets for neurodegenerative disorders. Pharmacol Ther 97: 35-53.
21. Kitamura Y, Yanagisawa D, Takata K, Taniguchi T. 2009. Neuroprotective function in brain microglia. Curr Anaesth Crit Care 20: 142-147.
22. Kreutzberg GW. 1996. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
23. 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 the response to acute neural injury. Glia 50: 121-131.
24. Lin SC, Huck JH, Roberts JD, Macklin WB, Somogyi P, Bergles DE. 2005. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46: 773-785.
25. Liu J, Marino MW, Wong G, Grail D, Dunn A, Bettadapura J, Slavin AJ, Old L, Bernard CC. 1998. TFN is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat Med 4: 78-83.
26. Matsumoto H, Kumon Y, Watanabe H, Ohnishi T, Shudou M, Chuai M, Imai Y, Takahashi H, Tanaka J. 2008. 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: 149-163.
27. McGeer PL, Itagaki S, Boyes BE, McGeer EG. 1988. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38: 1285-1291.
28. Miwa T, Furukawa S, Nakajima K, Furukawa Y, Kohsaka S. 1997. Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia. J Neurosci Res 50: 1023-1029.
29. Nakajima K, Honda S, Tohyama Y, Imai Y, Kohsaka S, Kurihara T. 2001. Neurotrophin secretion from cultured microglia. J Neurosci Res 65: 322-331.
30. Nishiyama A. 2001. NG2 cells in the brain: A novel glial cell population. Hum Cell 14: 77-82.
31. Nishiyama A. 2007. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13: 62-76.
32. Pascual A, Hidalgo-Figuroa M, Piruat JI, Pintado CO, Gómez-Díaz R, LóPez-Barneo J. 2008. Absolute requirement of GDNF for adult catecholaminergic neurons survival. Nat Neurosci 11: 755-761.
33. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates, 2nd ed. North Ryde, Australia: Academic Press.
34. Peters A. 2004. A fourth type of neuroglial cell in the adult central nervous system. J Neurocytol 33: 345-357.
35. Priller J, Flügel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernández-Klett F, Prass K, Bechmann I, de Boer BA, Frotscher M, Kreutzberg GW, Persons DA, Dirnagl U. 2001. Targeting gene-modified hematopoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat Med 7: 1356-1361.
36. Raff MC, Miller RH, Noble M. 1983. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303: 390-396.
37. 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.
38. Rousselet E, Callebert J, Parain K, Joubert C, Hunot S, Hartmann A, Jacque C, Perez-Diaz F, Cohen-Salmon C, Launay JM, Hirsch EC. 2002. Role of TNF-α receptors in mice intoxicated with the parkinsonian toxin MPTP. Exp Neurol 177: 183-192.
39. Sawada H, Hishida R, Hirata Y, Ono K, Suzuki H, Muramatsu S, Nakano I, Nagastu T, Sawada M. 2007. Activated microglia affect the nigro-striatal dopamine neurons differently in neonatal and aged mice treated with 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine. J Neurosci Res 85: 1752-1761.
40. Shimohama S, Sawada H, Kitamura Y, Taniguchi T. 2003. Disease model: Parkinson's disease. Trends Mol Med 9: 360-365.
41. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. 2006. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49: 489-502.
42. + macrophage-like cells expressing a variety of neuroprotective factors ameliorate ischemic damage of the brain. J Cereb Blood Flow Metab 30: 603-615.
43. Stallcup WB. 2002. The NG2 proteoglycan: Past insights and future prospects. J Neurocytol 31: 423-435.
44. Suzuki T, Hide I, Ido K, Kohsaka S, Inoue K, Nakata Y. 2004. Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J Neurosci 24: 1-7.
45. Tanaka R, Komine-Kobayashi M, Mochizuki H, Yamada M, Furuya T, Migita M, Shimada T, Mizuno Y, Urabe T. 2003. Migration of enhanced green fluorescent protein expressing bone marrow-derived microglia/macrophage into the mouse brain following permanent focal ischemia. Neuroscience 117: 531-539.
46. Wigley R, Hamilton N, Nishiyama A, Kirchhoff F, Butt AM. 2007. Morphological and physiological interactions of NG2-glia with astrocytes and neurons. J Anat 210: 661-670.
47. Yokoyama A, Sakamoto A, Kameda K, Imai Y, Tanaka J. 2006. NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia 53: 754-768.
48. Zhang Y, Tohyama K, Winterbottom JK, Haque 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.
49. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE. 2007. Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10: 321-330.