Evidence for oxidative stress in the developing cerebellum of the rat after chronic mild carbon monoxide exposure (0.0025% in air)

BMC Neuroscience

Volumn 10, Issue , 2009, Pages

  Lopez, Ivan A ^a   Acuna, Dora ^a   Beltran Parrazal, Luis ^a   Lopez, Ivan E ^a   Amarnani, Abhimanyu ^a   Cortes, Max ^a   Edmond, John ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CALBINDIN; CARBON MONOXIDE; COPPER ZINC SUPEROXIDE DISMUTASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FERRITIN; FERRITIN H; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; NEUROFILAMENT PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; PARVALBUMIN; SYNAPSIN I; UNCLASSIFIED DRUG; 3-NITROTYROSINE; APOFERRITIN; DRUG DERIVATIVE; NERVE PROTEIN; SUPEROXIDE DISMUTASE; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN HYPOXIA; CELLULAR STRESS RESPONSE; CEREBELLUM CORTEX; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; LONG TERM EXPOSURE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PERINATAL PERIOD; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; PURKINJE CELL; RAT; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; ANIMAL EMBRYO; CARBON MONOXIDE INTOXICATION; CEREBELLUM; DISEASE MODEL; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; NERVE CELL; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY;

ANIMALS; ANIMALS, NEWBORN; APOFERRITINS; CARBON MONOXIDE POISONING; CEREBELLUM; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; FEMALE; HEME OXYGENASE-1; MALE; NERVE TISSUE PROTEINS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RNA, MESSENGER; SUPEROXIDE DISMUTASE; TYROSINE;

EID: 67649421629     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-10-53     Document Type: Article

References (103)

1. Raub JA Benignus VA Carbon monoxide and the nervous system Neurosci and Biobehab Reviews 2002, 26:925-940. 10.1016/S0149-7634(03)00002-2
2. Piantadosi CA Biological chemistry of carbon monoxide Antioxidant Redox Signal 2002, 4:259-270. 10.1089/152308602753666316
3. Piantadosi CA Carbon monoxide poisoning N Engl J Med 2002, 347:1054-1055. 10.1056/NEJMp020104 12362005
4. Ryter SW Otterbein LE Carbon monoxide in biology and medicine Bioessays 2004, 26:270-280. 10.1002/bies.20005 14988928
5. Piantadosi CA Carraway MS Suliman HB Carbon monoxide, oxidative stress, and mitochondrial permeability pore transition Free Radic Biol Med 2006, 40:1332-1339. 10.1016/j.freeradbiomed.2005.11.020 16631523
6. Kanu A Whitfields J Leffler CW Carbon monoxide contributes to hypotension-induced cerebrovascular vasodilation in piglets Am J Physiol Hearth Circ Physiol 2006, 291:2409-14. 10.1152/ajpheart.01368.2005
7. Mendelman A Zarchin N Rifkind J Mayevsky A Brain multiparametric responses to carbon monoxide in the aging rat Brain Res 2000, 867:217-22. 10.1016/S0006-8993(00)02326-X 10837816
8. Raub JA Mathieu-Nolf Hampson NB Thom SR Carbon monoxide poisoning- a public heath perspective Toxicology 2000, 145:1-14. 10.1016/ S0300-483X(99)00217-6 10771127
9. Resch H Zawinka C Weiger Gm Schmetter L Garhofer G Inhaled carbon monoxide increases retinal and choroidal blood flow in healthy humans Invest Ophthalmol and Vis Sci 2005, 46:4275-4280. 10.1167/iovs.05-0417
10. Sorhaug S Steinshamn S Nilsen OG Waldum HL Chronic inhalation of carbon monoxide: Effects on the respiratory and cardiovascular system at doses corresponding to tobacco smoking Toxicology 2006, 228:280-290. 10.1016/ j.tox.2006.09.008 17056171
11. McGregor HP Westcott K Walker DW The effect of prenatal exposure to carbon monoxide on breathing and growth of the newborn guinea pig Int Pediatrics Research Found 1998, 43:126-131.
12. Mereu G Cammalleri M Fa M Francesconi W Saba P Tattoli M Trabace L Vaccari A Cuomo V Prenatal exposure to a low concentration of carbon monoxide disrupts hippocampal long-term potentiation in rat offspring J Pharmacol Exp Ther 2000, 294:728-734. 10900254
13. Montagnani M Serio M Potenza MA Mansi G De Salvia MA Caginao R Cuomo V Mitolo Chieppa D Prenatal exposure to carbon monoxide and vascular responsiveness of rat resistance vessels Life Sci 1996, 59:1553-1561. 10.1016/0024-3205(96)00486-9 8890936
14. Neuberger M Endler M Resch W Carbon monoxide in mother and newborn infant from smoking during pregnancy Zentralbl Bakteriol Mikrobiol Hyg (B) 1982, 176:349-353. 7148208
15. Lavezzi AM Ottaviani G Matturi L Adverse effects of prenatal tobacco smoke exposure on biological parameters of the developing brainstem Neurobiology of Disease 2005, 20:601-607. 10.1016/j.nbd.2005.04.015 15925516
16. Longo LD The biological effects of carbon monoxide on the pregnant woman, fetus and newborn infant Am J Obstetric Gynecol 1977, 129:69-103.
17. Di Giovanni V Cagiano R De Silva MA Giustino A Lacomba C Renna G Cuomo V Neurobehavioral changes produced in rats by prenatal exposure to carbon monoxide Brain Res 1993, 616:126-131. 10.1016/0006-8993(93)90200-7 8358603
18. Mactutus M Fechter LD Prenatal carbon monoxide exposure: Learning and memory deficits Science 1984, 23:409-411. 10.1126/science.6691152
19. Cagiano R Ancona D Cassano T Tattoli M Trabace L Cuomo V Effects of prenatal exposure to low concentrations of carbon monoxide on sexual behavior and mesolimbic dopaminergic function in rat offspring Br J Pharmacol 1998, 125:909-915. 1571044 9831932 10.1038/sj.bjp.0702143
20. De Luca A Pierno S Tricarico D Carratu MR Cagiano R Cuomo V Conte CD Developmental changes of membrane electrical properties of rat skeletal muscle fibers produced by neonatal exposure to carbon monoxide Environ Toxicol Pharmacol 1996, 2:213-221. 10.1016/S1382-6689(96)00058-0
21. De Silva MA Cagiano R Carratu MR Di Giovanni V Trabace L Cuomo V Irreversible impairment of active avoidance behavior in rats prenatally exposed to mild concentration of carbon monoxide Psychopharmacol 1995, 122:66-71. 10.1007/BF02246443
22. Benagiano V Lorusso L Coluccia A Tarullo A Flace P Girolamo F Bosco L Cagiano R Ambrosi G Glutamic acid decarboxylase and GABA immunoreactivities in the cerebellar cortex of adult rat after prenatal exposure to a low concentration of carbon monoxide Neuroscience 2005, 135:897-905. 10.1016/j.neuroscience.2005.06.058 16112480
23. Benagiano V Lorusso L Flace P Girolamo F Rizzi A Sabatini R Auteri P Bosco L Cagiano R Ambrosi G Effects of prenatal exposure to the CB-1 receptor agonist win 55212-2 or CO on the GABAergic neuronal systems of rat cerebellar cortex Neuroscience 2007, 149:592-601. 10.1016/ j.neuroscience.2007.07.050 17916407
24. Annau Z Fechter LD The effect of prenatal exposure to carbon monoxide In prenatal exposure to toxicant Baltimore; Johns Hopkins. University Press Needleman HL, Bellinger D 1994:249-267.
25. Carratù MR Ancona D Cagiano R Trabace L Schiavulli N Cuomo V Functional sequelae of developmental exposure to mild concentrations of carbon monoxide in rats Dev Brain Dysfunc 1997, 10:438-444.
26. Fechter LD Annau Z Toxicity of mild prenatal carbon monoxide exposure Science 1977, 197:680-682. 10.1126/science.877585 877585
27. Giustino A Cagiano R Carratu MR Cassano T Tattoli M Cuomo V Prenatal exposure to low concentrations of carbon monoxide alters habituation and non-spatial working memory in rat offspring Brain Res 1999, 844:201-205. 10.1016/S0006-8993(99)01832-6 10536278
28. Storm JE Fechter LD Alteration in the postnatal ontogeny of cerebellar norepinephrine content following chronic prenatal carbon monoxide J Neurochem 1985, 45:965-969. 10.1111/j.1471-4159.1985.tb04088.x 4031872
29. Storm JE Valdes JJ Fechter LD Postnatal alterations in cerebellar GABA content, GABA uptake and morphology following exposure to carbon monoxide early in development Dev Neurosci 1986, 8:251-261. 10.1159/ 000112259 2881771
30. Tolcos M McGregor H Walker D Rees S Chronic prenatal exposure to carbon monoxide results in a reduction in tyrosine hydroxylase-immunoreactivity and an increase in choline acetyltransferase-immunoreactivity in the fetal medulla: Implications for sudden infant death syndrome J Neuropathol Exp Neuro 2000, 59:218-228.
31. Altman J Autoradiographic and histological studies of postnatal neurogenesis III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats J Comp Neurol 1969, 136:269-294. 10.1002/cne.901360303 5788129
32. Altman J Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer J Comp Neurol 1972, 145:353-397. 10.1002/cne.901450305 4113154
33. Altman J Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer J Comp Neurol 1972, 145:399-463. 10.1002/cne.901450402 5044254
34. Altman J Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer J Comp Neurol 1972, 145:465-513. 10.1002/cne.901450403 4114591
35. Bouet V Dijk F Ijkema-Paassen J Wubbles RJ Want van der JJ Gramsbergen A Early hypergravity exposure effects calbindin-D28K and inosito-3-phosphate expression in Purkinje cells Neurosci Letters 2005, 382:10-15. 10.1016/j.neulet.2005.02.051
36. Wang VY Zoghbi HY Genetic regulation of cerebellar development Nature Rev 2001, 2:484-491. 10.1038/35081558
37. Kern JK Jones AM Evidence of toxicity, oxidative stress, and neuronal insult in autism J Toxicol Environ Health B Crit Rev 2006, 9:485-99. 10.1080/10937400600882079 17090484
38. Lopez I Acuna D Webber DS Korsak RA Edmond J Mild carbon monoxide exposure diminishes selectively the integrity of the cochlea of the developing rat J Neurosci Res 2003, 74:666-675. 10.1002/jnr.10813 14635218
39. Stockard-Sullivan JE Korsak RA Webber DS Edmond J Mild carbon monoxide exposure and auditory function in the developing rat J Neurosci Res 2003, 74:644-654. 10.1002/jnr.10808 14635216
40. Webber DS Korsak RA Sininger LK Sampogna SL Edmond J Mild carbon monoxide exposure impairs the developing auditory system of the rat J Neurosci Res 2003, 74:655-665. 10.1002/jnr.10809 14635217
41. Webber DS Lopez IA Korsak RA Hirota S Acuna D Edmond J Limiting iron availability confers neuroprotection from chronic mild carbon monoxide exposure in the developing auditory system of the rat J Neurosci Research 2005, 80:620-633. 10.1002/jnr.20495
42. Lopez IA Acuna D Beltran-Parrazal L Espinosa-Jeffrey A Edmond J Oxidative stress and the deleterious consequences to the rat cochlea after prenatal chronic mild exposure to carbon monoxide in air Neurosci 2008, 152:854-867. 10.1016/j.neuroscience.2007.10.053
43. Acuna D Lopez I Webber DS Espinosa-Jeffrey A Edmond J Chronic carbon monoxide exposure (0.0025% in air) promotes oxidative stress and results in cellular deficits in the cerebellum of developing rats Nitric Oxide 2006 ,14:A26. P026. 10.1016/j.niox.2006.04.086
44. Edmond J Acuna D Beltran-Parrazal L Kawakami K Lopez IA Evidence for oxidative stress in the developing cerebellum of the rat after chronic mild carbon monoxide exposure (0.0025%) in air J Neurochem 2008, 104(Suppl. 1):ABst # PTW06-20. 18254785
45. Paxinos G Watson C The rat brain in stereotaxic coordinates Academic Press, Harcourt brace Jovanovich Publishers, San Diego, NY, Berkeley, Boston, London, Sydney, Tokyo, Toronto 2 1986.
46. Carmona R Macias D Guadix JA Portillo V Perez-Pomares JM Munos-chapulli R A simple technique of image analysis for specific nuclear immunolocalization of proteins J Microscopy 2007, 225:96-99. 10.1111/ j.1365-2818.2007.01719.x
47. Konsti J Jumppanen M Lundin M Isola J A public-domain image processing tool for automated quantification of fluorescence in situ hybridization signals J Clin Pathol 2008, 61:278-282. 10.1136/jcp.2007.048991 17693574
48. Papadopulus F Spinelli M Valente S Foroni L Orrico C Alviano F Pasquinelli G Common tasks in microscopy and ultrastrucutural image analysis using Imagej Ultrastructural Pathology 2007, 31:401-407. 10.1080/01913120701719189 18098058
49. Beltran-Parrazal L Dora Acuna D Edmond J López IA Cytoglobin and neuroglobin expression in the rat cerebellar cortex after prenatal and postnatal chronic mild carbon monoxide exposure 37th Society for Neuroscience meeting 2007:P903 13.
50. Korres S Riga M Balatsouras D Papadakis C Kanellos P Ferekidis E Influence of smoking on developing cochlea. Does smoking during pregnancy affect the amplitudes of transient evoked otoacustic emissions in newborns? Int J Pediatr Otorhinolaryngol 2007, 71:781-786. 10.1016/ j.ijporl.2007.01.015 17343925
51. Kregel KC Zhang HJ An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations Am J Physiol Regul Integr Comp Physiol 2007, 292:18-36.
52. Jones DP Radical-free biology of oxidative stress Am J Physiol Cell Physiol 2008, 295:849-868. 10.1152/ajpcell.00283.2008
53. Blumberg J Use of biomarkers of oxidative stress in research studies J Nutr 2004, 134:3188-3189.
54. Piantadosi CA Carbon monoxide, reactive oxygen signaling, and oxidative stress Free Radical Biol & Med 2008, 45:562-569. 10.1016/ j.freeradbiomed.2008.05.013
55. Calabrese V Butterfield DA Scapagnini G Stella AMG Maines MD Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: Relevance to brain aging, neurodegenerative disorders, and longevity Antioxidants & Redox Signaling 2006, 8:444-477. 10.1089/ars.2006.8.1975 16677090
56. Zelco IN Mariani TJ Folz RJ Superoxide dismutase multigene family: A comparison of the CuZN-SOD(SOD1), Mn-SOD(SDO2), and EC-SOD(SOD3) gene structures, evolution, and expression Free Radical Biol & Med 2002, 33:337-349. 10.1016/S0891-5849(02)00905-X
57. Colombrita C Calabrese V Stella AMG Mattei F Alkon DL Scapagnini G Regional rat brain distribution of heme oxygenase and manganese superoxide dismutase mRNA: Relevance of redox homeostasis in the aging processes Exp Biol Med 2003, 228:517-524.
58. Melov S Coskun P Patel M Tuinstra R Cottrell B Jun AS Zastawny TH Dizdaroglu M Goodman SI Huang TT Miziorko H Epstein CJ Wallace DC Mitochondrial disease in superoxide dismutase 2 mutant mice PNAS 1999, 96:846-851. 15313 9927656 10.1073/pnas.96.3.846
59. Landis GN Tower J Superoxide dismutase evolution and life span regulation Mech Ageing & Dev 2005, 126:365-379. 10.1016/ j.mad.2004.08.012 15664623
60. Faraci FM Didion SP Vascular protection: Superoxide dismutase isoforms in the vessel wall Arterioscler Thromb Vasc Biol 2004, 24:1367-1373. 10.1161/01.ATV.0000133604.20182.cf 15166009
61. Ewing JF Maines MD Regulation and expression of heme oxygenase enzymes in aged-rat brain: Age related depression in HO-1 and HO-2 expression and altered stress-response J Neural Trans 2006, 113:439-454. 10.1007/ s00702-005-0408-z
62. Bergeron M Ferreiro DM Sharp FR Developmental expression of heme oxygenase-1 (HSP32) in rat brain: An immunohistochemical study Dev Brain Res 1998, 105:181-194. 10.1016/S0165-3806(97)00169-7
63. Morse D Choi AMK Heme oxygenase-1 from bench to bedside Am J Respir Crit Care Med 2005, 172:660-670. 10.1164/rccm.200404-465SO 15901614
64. Chang EF Claus CP Vreman HJ Wong RJ Noble-Haeusslein LJ Heme regulation in traumatic brain injury: Relevance to the adult and developing brain J Cereb Blood Flow & Metabolism 2005, 25:1401-1417. 10.1038/ sj.jcbfm.9600147
65. Ewing JF Maines MD Glutathione depletion induces heme oxygenase-1 (HSP-32) mRNA and protein in rat brain J Neurochem 1993, 60:1512-1519. 10.1111/j.1471-4159.1993.tb03315.x 8455037
66. Fairfield DA Kanicki AC Lomax MI Altschuler RA Induction of heat shock protein 32 (Hsp32) in the rat cochlea following hyperthermia Hearing Res 2004, 188:1-11. 10.1016/S0378-5955(03)00369-1
67. Liu JSH Zhao ML Brosnan C Lee SC Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions American J Pathology 2001, 158:2057-2066.
68. Beckman JS Koppenol WH Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly Am J Physiol 1996, 271:1424-1437.
69. Cross AH Manning PT Keeling RM Schmidt RE Misko TP Peroxynitrite formation within the central nervous system in active multiple sclerosis J Neuroimmunol 1998, 88:45-56. 10.1016/S0165-5728(98)00078-2 9688323
70. Veen Van der RC Hinton DR Incardonna F Hofman FM Extensive peroxynitrite activity during progressive stages of central nervous system inflammation J Neuroimmunol 1997, 77:1-7. 10.1016/S0165-5728(97)00013-1 9209262
71. Cirino G Fiorucci S Sessa WC Endothelial nitric oxide synthase: The Cinderella of inflammation Trends in Pharmacol Sci 2003, 24:91-95. 10.1016/S0165-6147(02)00049-4
72. Fessenden JD Altschuler RA Seasholtz AF Schacht J Nitric oxide/cyclic guanoside monophosphate pathway in the peripheral and central auditory system of the rat J Comp Neurol 1999, 404:52-63. 10.1002/ (SICI)1096-9861(19990201)404:1<52::AID-CNE4>3.0.CO;2-W 9886024
73. Hernandez-Viadel M Castoldi AF Coccini T Manzo L Erceg S Felipo V In vivo exposure to carbon monoxide causes delayed impairment of activation of soluble guanylate cyclase by nitric oxide in rat brain cortex and cerebellum J Neurochem 2004, 89:1157-1165. 10.1111/ j.1471-4159.2004.02424.x 15147508
74. Morse D Sethi J Choi AMK Carbon Monoxide-dependent signaling Crit Care Med 2002, 30:12-17. 10.1097/00003246-200201001-00002
75. Sharma VS Magde D Activation of soluble guanylate cyclase by carbon monoxide and nitric oxide: A mechanistic model Methods 1999, 19:494-505. 10.1006/meth.1999.0892 10581149
76. Vaccari A Ruiu P Saba P Fa M Cagiano R Coluccia A Merei G Steardo L Tattoli M Trabace L Cuomo V Prenatal low-level exposure to CO alters postnatal development of hippocampal nitric oxide synthase and haem-oxygenase activities in rats Int J Neuropsychopharmacol 2001, 4:219-222. 10.1017/S1461145701002450 11602027
77. Beal MF Oxidatively modified proteins in aging and disease Free Radical Biol & Med 2002, 32:797-803. 10.1016/S0891-5849(02)00780-3
78. Lavezzi AM Ottaviani G Matturri L Adverse effects of prenatal tobacco smoke exposure on biological parameters of the developing brain stem Neurobiology of disease 2005, 109:601-607. 10.1016/j.nbd.2005.04.015
79. Matturri L Ottaviani G Lavezzi AM Maternal smoking and sudden infant death syndrome: Epidemiological study related to pathology Virchows Arch 2006, 449:697-706. 10.1007/s00428-006-0308-0 17091255
80. Gess B Wolf K Pfeifer M Riegger GAJ Pflugers A Kurtz In vivo carbon monoxide exposure and hypoxic hypoxia stimulate immediate early gene expression Arch-Eur J Physiol 1997, 434:568-574. 10.1007/s004240050437
81. Castejon OJ Fuller L Dailey ME Localization of synapsin-I and PSD-95 in developing postnatal rat cerebellar cortex Developmental Brain Res 2004, 151:25-32. 10.1016/j.devbrainres.2004.03.019
82. Hilfiker S Benfenati F Doussau F Nairin AC Czernik AJ Augustine GJ Greengard P Structural domains involved in the regulation of transmitter release by synapsins J Neuroscience 2005, 25:2658-2669. 10.1523/ JNEUROSCI.4278-04.2005
83. Bastianelli E Distribution of calcium-binding proteins in the cerebellum Cerebellum 2003, 2:242-262. 10.1080/14734220310022289 14964684
84. Kang TC Park SK Hwang IK An SJ Bahn JH Choi Sym Kim JS Won MH The decreases in calcium binding proteins and neurofilament immunoreactivities in the Purkinje cell of the seizure sensitive gerbils Neurochem Int 2002, 40:115-122. 10.1016/S0197-0186(01)00085-7 11738477
85. Baurle J Vogten H Grusser-Cornehls U Course and targets of the calbindin D-28k subpopulation of primary vestibular afferents J Comp Neurol 1998, 402:111-128. 10.1002/ (SICI)1096-9861(19981207)402:1<111::AID-CNE8>3.0.CO;2-1 9831049
86. Schmidt-Kastner R Meller D Eysel UT Immunohistochemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentation in the rat visual system Exp Neurol 1992, 117:230-246. 10.1016/0014-4886(92)90132-A 1397159
87. Takayama C Inoue Y GABAergic signaling in the developing cerebellum Anat Sci Int 2004, 79:124-136. 10.1111/j.1447-073x.2004.00081.x 15453613
88. Di Giovani V Cagiano R De Salvia MA Giustino A Lacomba C Renna G Cuomo V Neurobehavioral changes produced in rats by prenatal exposure to carbon monoxide Brain Res 1993, 616:126-131. 10.1016/0006-8993(93)90200-7 8358603
89. Yamada K Fukaya M Shibata T Kurihara H Tanaka K Inoue Y Watanabe M Dynamic transformation of Bergman glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells J Comp Neurol 2000, 418:106-120. 10.1002/ (SICI)1096-9861(20000228)418:1<106::AID-CNE8>3.0.CO;2-N 10701759
90. Yamada K Watanabe M Cytodifferentiation of Bergmann glia and its relationship with Purkinje cells Anat Sci Int 2002, 77:94-108. 10.1046/ j.0022-7722.2002.00021.x 12418089
91. Horvat A Schwaigner FW Hager G Brocker F Streif R Knyazev PG Ullrich A Kreutzberg GW A novel role of protein tyrosine phosphatase SHP1 in controlling glial activation in the normal and injured nervous system J Neurosci 2001, 21:665-674.
92. Thom SR Bhopale VM Fisher D Gimotty P Delayed neuropathology after carbon monoxide poisoning is immune mediated PNAS 2004, 101:13660-13665. 518809 15342916 10.1073/pnas.0405642101
93. Ekdahl CT Claasen JH Bonde S Kokaia Z Lindvall O Inflammation is detrimental for neurogenesis in adult brain PNAS, USA 2003, 100:13632-13637. 10.1073/pnas.2234031100
94. Wu DC Jackson-Lewis V Vila M Teismann P Vadseth C Choi D.-K Ischiropoulos H Przedborski S Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease J Neurosci 2002, 22:1763-1771. 11880505
95. Gorter JA Mesquita ARM van Vliet EA Lopez da Silva FH Aronica E Increased expression of ferritin, an iron-storage protein, in specific regions of the parahippocampal cortex of epileptic rats Epilepsia 2005, 46:1371-1379. 10.1111/j.1528-1167.2005.11505.x 16146431
96. Koorts AM Viljoen M Ferritin and ferritin isoforms II: Protection against uncontrolled cellular proliferation, oxidative damage and inflammatory processes Arch Physiol Biochem 2007, 113:55-64. 10.1080/ 13813450701422575 17558604
97. Zecca L Youdim MBH Riederer P Connor JR Crichton RR Iron, brain ageing and neurodegenerative disorders Nature Reviews Neuroscience 2004, 5:863-873. 10.1038/nrn1537 15496864
98. Lopes KO Sparks DL Streit WJ Microgial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity Glia 2008, 56:1048-1060. 10.1002/glia.20678 18442088
99. Calabrese V Butterfield DA Scapagnini G Stella AMG Maines MD Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: Relevance to brain aging, neurodegenerative disorders, and longevity Antioxidants & Redox Signaling 2006, 8:444-477. 10.1089/ars.2006.8.1975 16677090
100. Ferriero DM Oxidant mechanisms in neonatal hypoxia-ischemia Dev Neurosci 2001, 23:198-202. 10.1159/000046143 11598320
101. Berry M McConnell P Sievers J Price S Anwar A Factors influencing the growth of cerebellar neural networks Bibl Anat 1981, 19:1-51. 7225059
102. Calabrese V Mancuso C Ravagna A Perlugi M Cini C De Marco C Butterfield DA Stella AM In vivo induction of heat shock proteins in the substantia nigra following L-DOPA administration is associated with increased activity of mitochondrial complex I and nitrosative stress in rats: regulation by glutathione redox state J Neurochem 2007, 101:709-717. 10.1111/j.1471-4159.2006.04367.x 17241115
103. Calabrese V Mancuso C Calvani M Rizzarelli E Butterfield DA Stella AM Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity Nat Rev Neurosci 2007, 10:766-775. 10.1038/nrn2214