Effect of 6-hydroxydopamine (6-OHDA) on proliferation of glial cells in the rat cortex and striatum: Evidence for de-differentiation of resident astrocytes

Cell and Tissue Research

Volumn 342, Issue 2, 2010, Pages 147-160

  Wachter, Britta ^a   Schürger, Sonja ^b,c   Rolinger, Jens ^b,c   Von Ameln Mayerhofer, Andreas ^b   Berg, Daniela ^c   Wagner, Hans Jochen ^a   Kueppers, Eva ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Department of Neuropharmacology   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cortex; Nestin; Proliferation; Rat (adult, Sprague Dawley); Reactive astrocytes

Indexed keywords

CELL MARKER; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; OXIDOPAMINE; PROTEIN NG2; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL DEDIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; GLIA CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; STEM CELL;

ADRENERGIC AGENTS; ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; CELL DEDIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CEREBRAL CORTEX; CORPUS STRIATUM; GLIAL FIBRILLARY ACIDIC PROTEIN; INJECTIONS, INTRAVENTRICULAR; KI-67 ANTIGEN; NEUROGLIA; OXIDOPAMINE; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 78649323061     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-010-1061-x     Document Type: Article

References (72)

1. A Alvarez-Buylla B Seri F Doetsch 2002 Identification of neural stem cells in the adult vertebrate brain Glia 16 368 382
2. JA Amat H Ishiguro K Nakamura WT Norton 1996 Phenotypic diversity and kinetics of proliferating microglia and astrocytes following cortical stab wounds Glia 16 368 382 1:STN:280:DyaK283ot1aqsw%3D%3D 10.1002/(SICI)1098- 1136(199604)16:4<368::AID-GLIA9>3.0.CO;2-W 8721677 (Pubitemid 26309460)
3. PM Aponso RLM Faull B Connor 2008 Increased progenitor cell proliferation and astrogenesis in the partial progressive 6-hydroxydopamine model of Parkinson's disease Neuroscience 151 1142 1153 1:CAS:528:DC%2BD1cXitVKgtLk%3D 10.1016/j.neuroscience.2007.11.036 18201835
4. J Badaut JF Brunet JM Petit CF Guerin PJ Magistretti L Regli 2008 Induction of brain aquaporin 9 (AQP9) in catecholaminergic neurons in diabetic rats Brain Res 1188 17 24 1:CAS:528:DC%2BD2sXhsVOktrvN 10.1016/j.brainres.2007. 10.087 18053968 (Pubitemid 350296067)
5. SA Baker KA Baker T Hagg 2004 Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone Eur J Neurosci 20 575 579 10.1111/j.1460-9568.2004.03486.x 15233767 (Pubitemid 38969643)
6. B Berninger MA Hack M Götz 2006 Neural stem cells: on where they hide, in which disguise, and how we may lure them out Handb Exp Pharmacol 174 319 360 10.1007/978-3-540-77855-4-14 16370334
7. B Berninger MR Costa U Koch T Schroeder B Sutor B Grothe M Götz 2007 Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia J Neurosci 27 8654 8664 1:CAS:528:DC%2BD2sXptlSnsLg%3D 10.1523/JNEUROSCI.1615-07.2007 17687043 (Pubitemid 47254260)
8. JP Brown S Couillard-Després CM Cooper-Kuhn J Winkler L Aigner HG Kuhn 2003 Transient expression of doublecortin during adult neurogenesis J Comp Neurol 467 1 10 1:CAS:528:DC%2BD3sXpsFCgs70%3D 10.1002/cne.10874 14574675 (Pubitemid 37339753)
9. A Buffo I Rite P Tripathi A Lepier D Colak AP Horn T Mori M Götz 2008 Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain Proc Natl Acad Sci USA 105 3581 3586 1:CAS:528: DC%2BD1cXjtlars7k%3D 10.1073/pnas.0709002105 18299565 (Pubitemid 351723595)
10. A Buffo C Rolando S Ceruti 2010 Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential Biochem Pharmacol 79 77 89 1:CAS:528:DC%2BD1MXhsVWqtbfJ 10.1016/j.bcp.2009.09.014 19765548
11. KA Burns B Murphy SC Danzer C-Y Kuan 2009 Developmental and post-injury cortical gliogenesis: a genetic fate-mapping study with Nestin-CreER mice Glia 57 1115 1129 10.1002/glia.20835 19115384
12. LA Buttitta BA Edgar 2007 Mechanisms controlling cell cycle exit upon terminal differentiation Curr Opin Cell Biol 19 697 704 1:CAS:528: DC%2BD2sXhsVWisLjF 10.1016/j.ceb.2007.10.004 18035529 (Pubitemid 350216428)
13. G Chadi VC Gomide 2004 FGF-2 and S100[beta] immunoreactivities increase in reactive astrocytes, but not in microglia, in ascending dopamine pathways following a striatal 6-OHDA-induced partial lesion of the nigrostriatal system Cell Biol Int 28 849 861 1:CAS:528:DC%2BD2cXhtVWit7rJ 10.1016/j.cellbi.2004.08. 005 15566955 (Pubitemid 39573512)
14. LW Chen LC Wei Y Qiu HL Liu ZR Rao G Ju YS Chan 2002 Significant up-regulation of nestin protein in the neostriatum of MPTP-treated mice. Are the striatal astrocytes regionally activated after systemic MPTP administration? Brain Res 925 9 17 1:CAS:528:DC%2BD38XitVKr 10.1016/S0006-8993(01)03253-X 11755896 (Pubitemid 34075357)
15. LW Chen HJ Hu HL Liu KK Yung YS Chan 2004 Identification of brain-derived neurotrophic factor in nestin-expressing astroglial cells in the neostriatum of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated mice Neuroscience 126 941 953 1:CAS:528:DC%2BD2cXltVCjtbs%3D 10.1016/j.neuroscience.2004.04.020 15207328 (Pubitemid 38780898)
16. AK Chojnacki GK Mak S Weiss 2009 Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci 10 153 163 1:CAS:528:DC%2BD1MXntFGnsA%3D%3D 10.1038/nrn2571 19153578
17. EK Chung LW Chen YS Chan KK Yung 2008 Downregulation of glial glutamate transporters after dopamine denervation in the striatum of 6-hydroxydopamine- lesioned rats J Comp Neurol 511 421 437 1:CAS:528:DC%2BD1cXhsFWgsrfF 10.1002/cne.21852 18831527
18. MR Costa M Götz B Berninger 2010 What determines neurogenic competence in glia? Brain Res Rev 63 47 59 1:CAS:528:DC%2BC3cXlsFahsbY%3D 10.1016/j.brainresrev.2010.01.002 20096728
19. J Dahlstrand M Lardelli U Lendahl 1995 Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system Brain Res Dev Brain Res 84 109 129 1:CAS:528:DyaK2MXivVKlsro%3D 10.1016/0165-3806(94)00162-S 7720210
20. L Dimou C Simon F Kirchhoff H Takebayashi M Götz 2008 Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex J Neurosci 28 10434 10442 1:CAS:528:DC%2BD1cXht1Gksb7M 10.1523/JNEUROSCI.2831-08.2008 18842903
21. F Doetsch 2003 The glial identity of neural stem cells Nat Neurosci 6 1127 1134 1:CAS:528:DC%2BD3sXosVOiu7g%3D 10.1038/nn1144 14583753 (Pubitemid 37346029)
22. F Doetsch 2003 A niche for adult neural stem cells Curr Opin Genet Dev 13 543 550 1:CAS:528:DC%2BD3sXnvVOlsrw%3D 10.1016/j.gde.2003.08.012 14550422 (Pubitemid 37204933)
23. M Eddleston L Mucke 1993 Molecular profile of reactive astrocytes-implications for their role in neurologic disease Neuroscience 54 15 36 1:CAS:528:DyaK3sXltFCnsbo%3D 10.1016/0306-4522(93)90380-X 8515840 (Pubitemid 23147085)
24. LJ Freedman MT Maddox 2001 A comparison of anti-biotin and biotinylated anti-avidin double-bridge and biotinylated tyramide immunohistochemical amplification J Neurosci Methods 112 43 49 1:CAS:528:DC%2BD3MXnsF2gtL4%3D 10.1016/S0165-0270(01)00454-X 11640956 (Pubitemid 32964711)
25. J Frisen CB Johansson C Torok M Risling U Lendahl 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 1:CAS:528:DyaK2MXosFygtb4%3D 10.1083/jcb.131.2.453 7593171
26. GA Garden T Moller 2006 Microglia biology in health and disease J Neuroimmune Pharmacol 1 127 137 10.1007/s11481-006-9015-5 18040779 (Pubitemid 44257488)
27. J Gerdes H Lemke H Baisch H Wacker U Schwab H Stein 1984 Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67 J Immunol 133 1710 1715 1:STN:280: DyaL2c3ptVKgtA%3D%3D 6206131
28. AV Gilyarov 2008 Nestin in central nervous system cells Neurosci Behav Physiol 38 165 169 1:STN:280:DC%2BD1c%2FksVSmtw%3D%3D 10.1007/s11055-008-0025-z 18197384
29. VC Gomide GA Silveira G Chadi 2005 Transient and widespread astroglial activation in the brain after a striatal 6-OHDA-induced partial lesion of the nigrostriatal system Int J Neurosci 115 99 117 1:CAS:528:DC%2BD2MXhtVehtL4%3D 10.1080/00207450490512696 15768855 (Pubitemid 40065762)
30. MN Gordon WA Schreier X Ou LA Holcomb DG Morgan 1997 Exaggerated astrocyte reactivity after nigrostriatal deafferentation in the aged rat J Comp Neurol 388 106 119 1:STN:280:DyaK1c%2FjtVyitA%3D%3D 10.1002/(SICI)1096- 9861(19971110)388:1<106::AID-CNE7>3.0.CO;2-5 9364241 (Pubitemid 27485635)
31. M Götz A Stoykova P Gruss 1998 Pax6 controls radial glia differentiation in the cerebral cortex Neuron 21 1031 1044 10.1016/S0896- 6273(00)80621-2 9856459 (Pubitemid 29018073)
32. E Gould 2007 How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8 481 488 1:CAS:528:DC%2BD2sXlsVSktb8%3D 10.1038/nrn2147 17514200 (Pubitemid 46789229)
33. C Heinrich R Blum S Gascón G Masserdotti P Tripathi R Sánchez S Tiedt T Schroeder M Götz B Berninger 2010 Directing astroglia from the cerebral cortex into subtype specific functional neurons PLoS Biol 8 e1000373 10.1371/journal.pbio.1000373 20502524
34. N Heins P Malatesta F Cecconi M Nakafuku KL Tucker MA Hack P Chapouton YA Barde M Götz 2002 Glial cells generate neurons: the role of the transcription factor Pax6 Nat Neurosci 5 308 315 1:CAS:528:DC%2BD38Xis1Kis7s%3D 10.1038/nn828 11896398 Erratum in: Nat Neurosci 5:500 (Pubitemid 34279810)
35. J Henning U Strauss A Wree J Gimsa A Rolfs R Benecke U Gimsa 2008 Differential astroglial activation in 6-hydroxydopamine models of Parkinson's disease Neurosci Res 62 246 253 1:CAS:528:DC%2BD1cXhtlyhsL7P 10.1016/j.neures.2008.09.001 18824050
36. V Henry V Paille F Lelan P Brachet P Damier 2009 Kinetics of microglial activation and degeneration of dopamine-containing neurons in a rat model of Parkinson disease induced by 6-hydroxydopamine J Neuropathol Exp Neurol 68 1092 1102 1:CAS:528:DC%2BD1MXhtFyntrfP 10.1097/NEN.0b013e3181b767b4 19918121
37. GU Hoglinger P Rizk MP Muriel C Duyckaerts WH Oertel I Caille EC Hirsch 2004 Dopamine depletion impairs precursor cell proliferation in Parkinson disease Nat Neurosci 7 726 735 10.1038/nn1265 15195095 (Pubitemid 38859057)
38. XT Hu SR Wachtel MP Galloway FJ White 1990 Lesions of the nigrostriatal dopamine projection increase the inhibitory effects of D1 and D2 dopamine agonists on caudate-putamen neurons and relieve D2 receptors from the necessity of D1 receptor stimulation J Neurosci 10 2318 2329 1:CAS:528:DyaK3cXlsVGktL0%3D 1973947
39. D Ito Y Imai K Ohsawa K Nakajima Y Fukuuchi S Kohsaka 1998 Microglia-specific localisation of a novel calcium binding protein, Iba1 Mol Brain Res 57 1 9 1:CAS:528:DyaK1cXjs1alsrs%3D 10.1016/S0169-328X(98)00040-0 9630473 (Pubitemid 28279554)
40. S Karakaya M Kipp C Beyer 2007 Oestrogen regulates the expression and function of dopamine transporters in astrocytes of the nigrostriatal system J Neuroendocrinol 19 682 690 1:CAS:528:DC%2BD2sXhtVSnsrfO 10.1111/j.1365-2826. 2007.01575.x 17680883 (Pubitemid 47386542)
41. MO Karl S Hayes BR Nelson K Tan B Buckingham TA Reh 2008 Stimulation of neural regeneration in the mouse retina Proc Natl Acad Sci USA 105 19508 19513 1:CAS:528:DC%2BD1cXhsFanurnK 10.1073/pnas.0807453105 19033471
42. JN Kay M Blum 2000 Differential response of ventral midbrain and striatal progenitor cells to lesions of the nigrostriatal dopaminergic projection Dev Neurosci 22 56 67 1:CAS:528:DC%2BD3cXhvValu70%3D 10.1159/000017427 10657698
43. SW Levison JE Goldman 1993 Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain Neuron 10 201 212 1:STN:280:DyaK3s7ns1Cjuw%3D%3D 10.1016/0896-6273(93)90311-E 8439409 (Pubitemid 23079542)
44. RC Lin DF Matesic M Marvin RD McKay O Brustle 1995 Re-expression of the intermediate filament nestin in reactive astrocytes Neurobiol Dis 2 79 85 1:CAS:528:DyaK2MXptlShsrs%3D 10.1006/nbdi.1995.0008 8980011
45. L Mao Y-S Lau E Petroske JQ Wang 2001 Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration Dev Brain Res 131 57 65 1:CAS:528:DC%2BD3MXosFKrtLs%3D 10.1016/S0165-3806(01)00260-7 (Pubitemid 33079218)
46. AJ Mathewson M Berry 1985 Observations on the astrocyte response to a cerebral stab wound in adult rats Brain Res 327 61 69 1:STN:280: DyaL2M7nsF2ktA%3D%3D 10.1016/0006-8993(85)91499-4 3986520 (Pubitemid 15167294)
47. RH Miller 2002 Regulation of oligodendrocyte development in the vertebrate CNS Prog Neurobiol 67 451 467 1:CAS:528:DC%2BD38XnvVKjsr0%3D 10.1016/S0301-0082(02)00058-8 12385864 (Pubitemid 35232446)
48. T Mori T Wakabayashi Y Takamori K Kitaya H Yamada 2009 Phenotype analysis and quantification of proliferating cells in the cortical gray matter of the adult rat Acta Histochem Cytochem 42 1 8 1:CAS:528:DC%2BD1MXlslamtrs%3D 10.1267/ahc.08037 19293989
49. A Nishiyama M Komitova R Suzuki X Zhu 2009 Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity Nat Rev Neurosci 10 9 22 1:CAS:528:DC%2BD1MXpt12m 10.1038/nrn2495 19096367
50. WT Norton 1999 Cell reactions following acute brain injury: a review Neurochem Res 24 213 218 1:STN:280:DyaK1M7jslWmsA%3D%3D 10.1023/A:1022505903312 9972867 (Pubitemid 29067962)
51. N Osumi 2001 The role of Pax6 in brain patterning Tohoku J Exp Med 193 163 174 1:CAS:528:DC%2BD3MXjslemu7s%3D 10.1620/tjem.193.163 11315763 (Pubitemid 33617018)
52. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates (2nd edn). Academic Press, San Diego
53. L Pinto M Götz 2007 Radial glial cell heterogeneity-the source of diverse progeny in the CNS Prog Neurobiol 83 2 23 1:CAS:528:DC%2BD2sXpt1Skur8%3D 10.1016/j.pneurobio.2007.02.010 17580100 (Pubitemid 47241312)
54. J Prosser V van Heyningen 1998 PAX6 mutations reviewed Hum Mutat 11 93 108 1:CAS:528:DyaK1cXhtVGjtbw%3D 10.1002/(SICI)1098-1004(1998)11:2<93::AID- HUMU1>3.0.CO;2-M 9482572 (Pubitemid 28074262)
55. N Raicevic A Mladenovi M Perovi D Miljkovi V Trajkovi 2005 The Mechanisms of 6-Hydroxydopamine-Induced Astrocyte Death Annals of the New York Academy of Sciences 1048 400 405 1:CAS:528:DC%2BD2MXhtFakt7rK 10.1196/annals.1342.049 16154962 (Pubitemid 41335396)
56. Rasband WS (1997-2009) ImageJ. National Institutes of Health, Bethesda, Md., USA
57. M Rodriguez P Barroso-Chinea P Abdala J Obeso T Gonzalez-Hernandez 2001 Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in Parkinson's disease Exp Neurol 169 163 181 1:CAS:528:DC%2BD3MXivVeiurw%3D 10.1006/exnr.2000.7624 11312569 (Pubitemid 32424333)
58. K Sakurai N Osumi 2008 The neurogenesis-controlling factor, Pax6, inhibits proliferation and promotes maturation in murine astrocytes J Neurosci 28 4604 4612 1:CAS:528:DC%2BD1cXlvFWhtLw%3D 10.1523/JNEUROSCI.5074-07.2008 18448636
59. T Scholzen J Gerdes 2000 The Ki-67 protein: from the known and the unknown J Cell Physiol 182 311 322 1:CAS:528:DC%2BD3cXot1Ggsg%3D%3D 10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9 10653597 (Pubitemid 30054364)
60. JG Sheng S Shirabe N Nishiyama JP Schwartz 1993 Alterations in striatal glial fibrillary acidic protein expression in response to 6-hydroxydopamine- induced denervation Exp Brain Res 95 450 456 1:CAS:528:DyaK2cXht1Oht7k%3D 10.1007/BF00227138 8224071
61. TI Simpson DJ Price 2002 Pax6; a pleiotropic player in development Bioessays 24 1041 1051 1:CAS:528:DC%2BD38XovFKlt7o%3D 10.1002/bies.10174 12386935 (Pubitemid 35326162)
62. MV Sofroniew 2005 Reactive astrocytes in neural repair and protection Neuroscientist 11 400 407 1:CAS:528:DC%2BD2MXhtFegtb3M 10.1177/1073858405278321 16151042 (Pubitemid 41339226)
63. MV Sofroniew 2009 Molecular dissection of reactive astrogliosis and glial scar formation Trends Neurosci 32 638 647 1:CAS:528:DC%2BD1MXhsVKgs7bP 10.1016/j.tins.2009.08.002 19782411
64. I Stromberg H Bjorklund D Dahl G Jonsson E Sundstrom L Olson 1986 Astrocyte responses to dopaminergic denervations by 6-hydroxydopamine and 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine as evidenced by glial fibrillary acidic protein immunohistochemistry Brain Res Bull 17 225 236 1:STN:280:DyaL2s%2FislGktw%3D%3D 10.1016/0361-9230(86)90119-X 3094835 (Pubitemid 16015777)
65. K Tatsumi H Takebayashi T Manabe KF Tanaka M Makinodan T Yamauchi E Makinodan H Matsuyoshi H Okuda K Ikenaka A Wanaka 2008 Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes J Neurosci Res 86 3494 3502 1:CAS:528: DC%2BD1cXhsFaksL%2FM 10.1002/jnr.21862 18816798
66. A Wang BP He 2009 Characteristics and functions of NG2 cells in normal brain and neuropathology Neurol Res 31 144 150 10.1179/174313209X393555 19298754
67. Y-P Yan BT Lang R Vemuganti RJ Dempsey 2009 Persistent migration of neuroblasts from the subventricular zone to the injured striatum mediated by osteopontin following intracerebral hemorrhage J Neurochem 109 1624 1635 1:CAS:528:DC%2BD1MXnvVekurs%3D 10.1111/j.1471-4159.2009.06059.x 19457159
68. H Yang XP Cheng JW Li Q Yao G Ju 2009 De-differentiation response of cultured astrocytes to injury induced by scratch or conditioned culture medium of scratch-insulted astrocytes Cell Mol Neurobiol 29 455 473 10.1007/s10571-008-9337-3 19130217
69. YM Yoo U Lee YJ Kim 2005 Apoptosis and nestin expression in the cortex and cultured astrocytes following 6-OHDA administration Neurosci Lett 382 88 92 1:CAS:528:DC%2BD2MXks1Ggu7s%3D 10.1016/j.neulet.2005.02.070 15911127 (Pubitemid 40725871)
70. T Yu G Cao L Feng 2006 Low temperature induced de-differentiation of astrocytes J Cell Biochem 99 1096 1107 1:CAS:528:DC%2BD28XhtFygtLrL 10.1002/jcb.20979 16767696 (Pubitemid 44673967)
71. J-W Zhao R Raha-Chowdhury JW Fawcett C Watts 2009 Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice Eur J Neurosci 29 1853 1869 10.1111/j.1460-9568.2009.06736.x 19473238
72. MJ Zigmond EM Stricker 1972 Deficits in feeding behavior after intraventricular injection of 6-hydroxydopamine in rats Science 177 1211 1214 1:CAS:528:DyaE3sXivVw%3D 10.1126/science.177.4055.1211 5057630