Heme regulation in traumatic brain injury: Relevance to the adult and developing brain

Journal of Cerebral Blood Flow and Metabolism

Volumn 25, Issue 11, 2005, Pages 1401-1417

  Chang, Edward F ^a   Claus, Catherine P ^a   Vreman, Hendrik J ^b   Wong, Ronald J ^b   Noble Haeusslein, Linda J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bilirubin; Developing brain; Heme metabolism; Heme oxygenase; Iron; Oxidative stress; Traumatic brain injury

Indexed keywords

ANTIOXIDANT; BILIRUBIN; CARBON MONOXIDE; CATALASE; FERRITIN; GLUTATHIONE PEROXIDASE; HEME; HEME OXYGENASE 1; HEME OXYGENASE 2; HEME OXYGENASE INHIBITOR; IRON; PROTOPORPHYRIN TIN; SUPEROXIDE DISMUTASE; TRANSFERRIN;

ALZHEIMER DISEASE; BASAL GANGLION; BIOLUMINESCENCE; BLEEDING; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN EDEMA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN STEM; CAUSE OF DEATH; CELL CULTURE; CEREBELLUM; ENZYME ACTIVITY; GENE DELETION; GENE TRANSFER; GENETIC TRANSCRIPTION; HEMOLYTIC ANEMIA; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; IMMUNOLOCALIZATION; MESENCEPHALON; MYELINATION; NEUROTOXICITY; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; THALAMUS;

ANIMALS; BILIRUBIN; BRAIN; CARBON MONOXIDE; HEME; HUMANS; IRON; MICE; OXIDATIVE STRESS; PROGNOSIS; RATS; SUBARACHNOID HEMORRHAGE, TRAUMATIC;

EID: 27544492193     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600147     Document Type: Review

References (181)

1. Acarin L, Paris J, Gonzalez B, Castellano B (2002) Glial expression of small heat shock proteins following an excitotoxic lesion in the immature rat brain. Glia 38:1-14
2. Adelson PD, Kochanek PM (1998) Head injury in children. J Child Neurol 13:2-15
3. Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915-22
4. Appleton SD, Chretien ML, McLaughlin BE, Vreman HJ, Stevenson DK, Brien JF, Nakatsu K, Maurice DH, Marks GS (1999) Selective inhibition of heme oxygenase, without inhibition of nitric oxide synthase or soluble guanylyl cyclase, by metalloporphyrins at low concentrations. Drug Metab Dispos 27:1214-9
5. Banks WA, Kastin AJ, Fasold MB, Barrera CM, Augereau G (1988) Studies of the slow bidirectional transport of iron and transferrin across the blood-brainbarrier. Brain Res Bull 21:881-5
6. Baranano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci USA 99:16093-8
7. Baranano DE, Snyder SH (2001) Neural roles for heme oxygenase: contrasts to nitric oxide synthase. Proc Natl Acad Sci USA 98:10996-1002
8. Bayir H, Clark RS, Kochanek PM (2003a) Promising strategies to minimize secondary brain injury after head trauma. Crit Care Med 31:S112-117
9. Bayir H, Kagan VE, Tyurina YY, Tyurin V, Ruppel RA, Adelson PD, Graham SH, Janesko K, Clark RS, Kochanek PM (2002) Assessment of antioxidant reserves and oxidative stress in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatr Res 51:571-8
10. Bayir H, Kochanek PM, Clark RS (2003b) Traumatic brain injury in infants and children: mechanisms of secondary damage and treatment in the intensive care unit. Crit Care Clin 19:529-49
11. Bergeron M, Ferriero DM, Sharp FR (1998) Developmental expression of heme oxygenase-1 (HSP32) in rat brain: an immunocytochemical study. Brain Res Dev Brain Bes 105:181-94
12. Bergeron M, Ferriero DM, Vreman HJ, Stevenson DK, Sharp FR (1997) Hypoxia-ischemia, but not hypoxia alone, induces the expression of heme oxygenase-1 (HSP32) in newborn rat brain. J Cereb Blood Flow Metab 17:647-58
13. Berk PD, Rodkey FL, Blaschke TF, Collison HA, Waggoner JG (1974) Comparison of plasma bilirubin turnover and carbon monoxide production in man. J Lab Clin Med 83:29-37
14. Beschorner R, Adjodah D, Schwab JM, Mittelbronn M, Pedal I, Mattern R, Schluesener HJ, Meyermann R (2000) Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol (Berlin) 100:377-84
15. Bhasin RR, Xi G, Hua Y, Keep RF, Hoff JT (2002) Experimental intracerebral hemorrhage: effect of lysed erythrocytes on brain edema and blood-brainbarrier permeability. Acta Neurochir Suppl 81:249-51
16. Buard A, Clement M, Bourre JM (1992) Developmental changes in enzymatic systems involved in protection against peroxidation in isolated rat brain microvessels. Neurosci Lett 141:72-4
17. Burdo JR, Martin J, Menzies SL, Dolan KG, Romano MA, Fletcher RJ, Garrick MD, Garrick LM, Connor JR (1999) Cellular distribution of iron in the brain of the Belgrade rat. Neuroscience 93:1189-96
18. Ceballos-Picot I, Nicole A, Clement M, Bourre JM, Sinet PM (1992) Age-related changes in antioxidant enzymes and lipid peroxidation in brains of control and transgenic mice overexpressing copper-zinc superoxide dismutase. Mutat Res 275:281-93
19. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, Epstein CJ (1998) Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18:8292-9
20. Chang EF, Wong RJ, Vreman HJ, Igarashi T, Galo E, Sharp FR, Stevenson DK, Noble-Haeusslein LJ (2003) Heme oxygenase-2 protects against lipid peroxidation-mediated cell loss and impaired motor recovery after traumatic brain injury. J Neurosci 23:3689-96
21. Cheepsunthorn P, Palmer C, Connor JR (1998) Cellular distribution of ferritin subunits in postnatal rat brain. J Comp Neurol 400:73-86
22. Cheepsunthorn P, Palmer C, Menzies S, Roberts RL, Connor JR (2001) Hypoxic/ischemic insult alters ferritin expression and myelination in neonatal rat brains. J Comp Neurol 431:382-96
23. Chen J, Regan RF (2004) Heme oxygenase-2 gene deletion increases astrocyte vulnerability to hemin. Biochem Biophys Res Commun 318:88-94
24. Chen J, Tu Y, Moon C, Nagata E, Ronnett GV (2003) Heme oxygenase-1 and heme oxygenase-2 have distinct roles in the proliferation and survival of olfactory receptor neurons mediated by cGMP and bilirubin, respectively. J Neurochem 85:1247-61
25. Clark JE, Foresti R, Green CJ, Motterlini R (2000) Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress. Biochem J 348(Part 3):615-9
26. Connor JR, Boeshore KL, Benkovic SA, Menzies SL (1994) Isoforms of ferritin have a specific cellular distribution in the brain. J Neurosci Res 37:461-5
27. Connor JR, Menzies SL (1996) Relationship of iron to oligodendrocytes and myelination. Glia 17:83-93
28. Connor JR, Menzies SL, Burdo JR, Boyer PJ (2001) Iron and iron management proteins in neurobiology. Pediatr Neurol 25:118-29
29. Connor JR, Pavlick G, Karli D, Menzies SL, Palmer C (1995a) A histochemical study of iron-positive cells in the developing rat brain. J Comp Neurol 355:111-23
30. Connor JR, Snyder BS, Arosio P, Loeffler DA, LeWitt P (1995b) A quantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer's diseased brains. J Neurochem 65:717-24
31. Crowe A, Morgan EH (1992) Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res 592:8-16
32. Cruse I, Maines MD (1988) Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 263:3348-53
33. de Haan JB, Tymms MJ, Cristiano F, Kola I (1994) Expression of copper/zinc superoxide dismutase and glutathione peroxidase in organs of developing mouse embryos, fetuses, and neonates. Pediatr Res 35:188-96
34. Dennery PA (2000) Regulation and role of heme oxygenase in oxidative injury. Curr Top Cell Regul 36:181-99
35. Dennery PA, Visner G, Weng YH, Nguyen X, Lu F, Zander D, Yang G (2003) Resistance to hyperoxia with heme oxygenase-1 disruption: role of iron. Free Radic Biol Med 34:124-33
36. DeWitt DS, Prough DS (2003) Traumatic cerebral vascular injury: the effects of concussive brain injury on the cerebral vasculature. J Neurotrauma 20:795-825
37. Dietrich RB, Bradley WG, Jr (1988) Iron accumulation in the basal ganglia following severe ischemic-anoxic insults in children. Radiology 168:203-6
38. Ditelberg JS, Sheldon RA, Epstein CJ, Ferriero DM (1996) Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatr Res 39:204-8
39. Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83
40. Dore S, Goto S, Sampei K, Blackshaw S, Hester LD, Ingi T, Sawa A, Traystman RJ, Koehler RC, Snyder SH (2000) Heme oxygenase-2 acts to prevent neuronal death in brain cultures and following transient cerebral ischemia. Neuroscience 99:587-92
41. Dore S, Sampei K, Goto S, Alkayed NJ, Guastella D, Blackshaw S, Gallagher M, Traystman RJ, Hurn PD, Koehler RC, Snyder SH (1999a) Heme oxygenase-2 is neuroprotective in cerebral ischemia. Mol Med 5:656-63
42. Dore S, Snyder SH (1999) Neuroprotective action of bilirubin against oxidative stress in primary hippocampal cultures. Ann NY Acad Sci 890:167-72
43. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH (1999b) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96:2445-50
44. Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649-71
45. Dringen R, Gutterer JM, Hirrlinger J (2000) Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur J Biochem 267:4912-6
46. Drysdale JW (1988) Human ferritin gene expression. Prog Nucleic Acid Res Mol Biol 35:127-72
47. Durkin MS, Olsen S, Barlow B, Virella A, Connolly ES, Jr (1998) The epidemiology of urban pediatric neurological trauma: evaluation of, and implications for, injury prevention programs. Neurosurgery 42:300-10
48. Dwork AJ (1995) Effects of diet and development upon the uptake and distribution of cerebral iron. J Neurol Sci 134(Suppl):45-51
49. Dwyer BE, Nishimura RN, Lu SY (1995) Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Brain Res Mol Brain Res 30:37-47
50. Elbirt KK, Bonkovsky HL (1999) Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 111:438-47
51. Ewing JF, Haber SN, Maines MD (1992) Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J Neurochem 58:1140-9
52. Ewing JF, Maines MD (1993) Glutathione depletion induces heme oxygenase-1 (HSP32) mRNA and protein in rat brain. J Neurochem 60:1512-9
53. Ewing JF, Maines MD (1997) Histochemical localization of heme oxygenase-2 protein and mRNA expression in rat brain. Brain Res Brain Bes Protoc 1:165-74
54. Ewing-Cobbs L, Miner ME, Fletcher JM, Levin HS (1989) Intellectual, motor, and language sequelae following closed head injury in infants and preschoolers. J Pediatr Psychol 14:531-47
55. Fan P, Yamauchi T, Noble LJ, Ferriero DM (2003) Age-dependent differences in glutathione peroxidase activity after traumatic brain injury. J Neurotrauma 20:437-45
56. Ferriero DM (2001) Oxidant mechanisms in neonatal hypoxia-ischemia. Dev Neurosci 23:198-202
57. Ferris CD, Jaffrey SR, Sawa A, Takahashi M, Brady SD, Barrow RK, Tysoe SA, Wolosker H, Baranano DE, Dore S, Poss KD, Snyder SH (1999) Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat Cell Biol 1:152-7
58. Focht SJ, Snyder BS, Beard JL, Van Gelder W, Williams LR, Connor JR (1997) Regional distribution of iron, transferrin, ferritin, and oxidatively-modified proteins in young and aged Fischer 344 rat brains. Neuroscience 79:255-61
59. Fredriksson A, Schroder N, Eriksson P, Izquierdo I, Archer T (1999) Neonatal iron exposure induces neurobehavioural dysfunctions in adult mice. Toxicol Appl Pharmacol 159:25-30
60. Fukuda K, Panter SS, Sharp FR, Noble LJ (1995) Induction of heme oxygenase-1 (HO-1) after traumatic brain injury in the rat. Neurosci Lett 199:127-30
61. Fukuda K, Richmon JD, Sato M, Sharp FR, Panter SS, Noble LJ (1996) Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury. Brain Res 736:68-75
62. Fullerton HJ, Ditelberg JS, Chen SF, Sarco DP, Chan PH, Epstein CJ, Ferriero DM (1998) Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann Neurol 44:357-64
63. Geddes JW, Pettigrew LC, Holtz ML, Craddock SD, Maines MD (1996) Permanent focal and transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci Lett 210:205-8
64. Goldstein L, Teng ZP, Zeserson E, Patel M, Regan RF (2003) Hemin induces an iron-dependent, oxidative injury to human neuron-like cells. J Neurosci Res 73:113-21
65. Gopinathan V, Miller NJ, Milner AD, Rice-Evans CA (1994) Bilirubin and ascorbate antioxidant activity in neonatal plasma. FEBS Lett 349:197-200
66. Goss JR, Taffe KM, Kochanek PM, DeKosky ST (1997) The antioxidant enzymes glutathione peroxidase and catalase increase following traumatic brain injury in the rat. Exp Neurol 146:291-4
67. Grundemar L, Ny L (1997) Pitfalls using metalloporphyrins in carbon monoxide research. Trends Pharmacol Sci 18:193-5
68. Halliwell B (1992) Reactive oxygen species and the central nervous system. J Neurochem 59:1609-23
69. Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M (2004) Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 336:241-50
70. Hoff JT, Xi G (2003) Brain edema from intracerebral hemorrhage. Acta Neurochir Suppl 86:11-5
71. Hua Y, Xi G, Keep RF, Hoff JT (2000) Complement activation in the brain after experimental intracerebral hemorrhage. J Neurosurg 92:1016-22
72. Huang FP, Xi G, Keep RF, Hua Y, Nemoianu A, Hoff JT (2002) Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J Neurosurg 96:287-93
73. Hulet SW, Powers S, Connor JR (1999) Distribution of transferrin and ferritin binding in normal and multiple sclerotic human brains. J Neurol Sci 165:48-55
74. Imai K, Aimoto T, Sato M, Kimura R (1990) Antioxidative effect of several porphyrins on lipid peroxidation in rat liver homogenates. Chem Pharm Bull (Tokyo) 38:258-60
75. Jefferies WA, Brandon MR, Hunt SV, Williams AF, Gatter KC, Mason DY (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312:162-3
76. Kadoya C, Domino EF, Yang GY, Stern JD, Betz AL (1995) Preischemic but not postischemic zinc protoporphyrin treatment reduces infarct size and edema accumulation after temporary focal cerebral ischemia in rats. Stroke 26:1035-8
77. Kawashima A, Oda Y, Yachie A, Koizumi S, Nakanishi I (2002) Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol 33:125-30
78. Koehler RC, Traystman RJ (2002) Cerebrovascular effects of carbon monoxide. Antioxid Redox Signal 4:279-90
79. Kondo Y, Ogawa N, Asanuma M, Ota Z, Mori A (1995) Regional differences in late-onset iron deposition, ferritin, transferrin, astrocyte proliferation, and microglial activation after transient forebrain ischemia in rat brain. J Cereb Blood Flow Metab 15:216-26
80. Koskiniemi M, Kyykka T, Nybo T, Jarho L (1995) Long-term outcome after severe brain injury in preschoolers is worse than expected. Arch Pediatr Adolesc Med 149:249-54
81. Kreiser D, Kelly DK, Seidman DS, Stevenson DK, Baum M, Dennery PA (2003) Gestational pattern of heme oxygenase expression in the rat. Pediatr Res 54:172-8
82. Kutty RK, Kutty G, Rodriguez IR, Chader GJ, Wiggert B (1994) Chromosomal localization of the human heme oxygenase genes: heme oxygenase-1 (HMOX1) maps to chromosome 22q12 and heme oxygenase-2 (HMOX2) maps to chromosome 16p13.3. Genomics 20:513-6
83. Kuwano A, Ikeda H, Takeda K, Nakai H, Kondo I, Shibahara S (1994) Mapping of the human gene for inducible heme oxygenase to chromosome 22q12. Tohoku J Exp Med 172:389-92
84. Landaw SA (1988) Factors that accelerate or retard red blood cell senescence. Blood Cells 14:47-67
85. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG (1994) Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 91:5987-91
86. Lazo O, Singh AK, Singh I (1991) Postnatal development and isolation of peroxisomes from brain. J Neurochem 56:1343-53
87. Levi S, Yewdall SJ, Harrison PM, Santambrogio P, Cozzi A, Rovida E, Albertini A, Arosio P (1992) Evidence of H- and L-chains have co-operative roles in the iron-uptake mechanism of human ferritin. Biochem J 288(Part 2):591-6
88. Liem HH, Tavassoli M, Muller-Eberhard U (1975) Cellular and subcellular localization of heme and hemopexin in the rabbit. Acta Haematol 53:219-25
89. Liu Y, Zhu B, Wang X, Luo L, Li P, Paty DW, Cynader MS (2003) Bilirubin as a potent antioxidant suppresses experimental autoimmune encephalomyelitis: implications for the role of oxidative stress in the development of multiple sclerosis. J Neuroimmunol 139:27-35
90. Long DA, Ghosh K, Moore AN, Dixon CE, Dash PK (1996) Deferoxamine improves spatial memory performance following experimental brain injury in rats. Brain Res 717:109-17
91. Luerssen TG, Klauber MR, Marshall LF (1988) Outcome from head injury related to patient's age. A longitudinal prospective study of adult and pediatric head injury. J Neurosurg 68:409-16
92. Luo D, Vincent SR (1994) Metalloporphyrins inhibit nitric oxide-dependent cGMP formation in vivo. Eur J Pharmacol 267:263-7
93. Macdonald RL, Weir BK (1991) A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 22:971-82
94. Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2:2557-68
95. Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517-54
96. Maines MD (2000) The heme oxygenase system and its functions in the brain. Cell Mol Biol (Noisy-le-grand) 46:573-85
97. Maines MD, Eke BC, Zhao X (1996) Corticosterone promotes increased heme oxygenase-2 protein and transcript expression in the newborn rat brain. Brain Res 722:83-94
98. Maines MD, Trakshel GM (1993) Purification and characterization of human biliverdin reductase. Arch Biochem Biophys 300:320-6
99. Mancuso C (2004) Heme oxygenase and its products in the nervous system. Antioxid Redox Signal 6:878-87
100. Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, Luerssen TG, Marmarou A, Foulkes MA (1992) The diagnosis of head injury requires a classification based on computed axial tomography. J Neurotrauma 9(Suppl 1):S287-92
101. Matz P, Turner C, Weinstein PR, Massa SM, Panter SS, Sharp FR (1996) Heme-oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. Brain Res 713:211-22
102. McCoubrey WK, Jr, Maines MD (1994) The structure, organization and differential expression of the gene encoding rat heme oxygenase-2. Gene 139:155-61
103. McDonald JW, Johnston MV (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Brain Res Rev 15:41-70
104. McDonald JW, Shapiro SM, Silverstein FS, Johnston MV (1998) Role of glutamate receptor-mediated excitotoxicity in bilirubin-induced brain injury in the Gunn rat model. Exp Neurol 150:21-9
105. Meffert MK, Haley JE, Schuman EM, Schulman H, Madison DV (1994) Inhibition of hippocampal heme oxygenase, nitric oxide synthase, and long-term potentiation by metalloporphyrins. Neuron 13:1225-33
106. Mikawa S, Kinouchi H, Kamii H, Gobbel GT, Chen SF, Carlson E, Epstein CJ, Chan PH (1996) Attenuation of acute and chronic damage following traumatic brain injury in copper, zinc-superoxide dismutase transgenic mice. J Neurosurg 85:885-91
107. Moos T, Morgan EH (2001) Restricted transport of antitransferrin receptor antibody (OX26) through the blood-brainbarrier in the rat. J Neurochem 79:119-29
108. Moos T, Oates PS, Morgan EH (1998) Expression of the neuronal transferrin receptor is age dependent and susceptible to iron deficiency. J Comp Neurol 398:420-30
109. Muller RM, Taguchi H, Shibahara S (1987) Nucleotide sequence and organization of the rat heme oxygenase gene. J Biol Chem 262:6795-802
110. Murray M (1997) Drug-mediated inactivation of cytochrome P450. Clin Exp Pharmacol Physiol 24:465-70
111. Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100:672-8
112. O'Brien PJ, Little C (1969) Intracellular mechanisms for the decomposition of a lipid peroxide. II. Decomposition of a lipid peroxide by subcellular fractions. Can J Biochem 47:493-9
113. Ogihara K, Zubkov AY, Bernanke DH, Lewis AI, Parent AD, Zhang JH (1999) Oxyhemoglobin-induced apoptosis in cultured endothelial cells. J Neurosurg 91:459-65
114. Ostrow JD, Pascolo L, Brites D, Tiribelli C (2004) Molecular basis of bilirubin-induced neurotoxicity. Trends Mol Med 10:65-70
115. Ostrow JD, Pascolo L, Shapiro SM, Tiribelli C (2003) New concepts in bilirubin encephalopathy. Eur J Clin Invest 33:988-97
116. Ostrow JD, Pascolo L, Tiribelli C (2002) Mechanisms of bilirubin neurotoxicity. Hepatology 35:1277-80
117. Ostrow JD, Tiribelli C (2001) New concepts in bilirubin neurotoxicity and the need for studies at clinically relevant bilirubin concentrations. J Hepatol 34:467-70
118. Palmer C, Menzies SL, Roberts RL, Pavlick G, Connor JR (1999) Changes in iron histochemistry after hypoxicischemic brain injury in the neonatal rat. J Neurosci Res 56:60-71
119. Palmer C, Roberts RL, Bero C (1994) Deferoxamine posttreatment reduces ischemic brain injury in neonatal rats. Stroke 25:1039-45
120. Panizzon KL, Dwyer BE, Nishimura RN, Wallis RA (1996) Neuroprotection against CAl injury with metalloporphyrins. Neuroreport 7:662-6
121. Panter SS, Braughler JM, Hall ED (1992) Dextran-coupled deferoxamine improves outcome in a murine model of head injury. J Neurotrauma 9:47-53
122. Patel BN, Dunn RJ, Jeong SY, Zhu Q, Julien JP, David S (2002) Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury. J Neurosci 22:6578-86
123. Paxinos G (ed) (1995) The rat nervous system. Sydney: Academic Press
124. Percy ME, Wong S, Bauer S, Liaghati-Nasseri N, Perry MD, Chauthaiwale VM, Dhar M, Joshi JG (1998) Iron metabolism and human ferritin heavy chain cDNA from adult brain with an elongated untranslated region: new findings and insights. Analyst 123:41-50
125. Platt JL, Nath KA (1998) Heme oxygenase: protective gene or Trojan horse. Nat Med 4:1364-5
126. Ponka P (1999) Cell biology of heme. Am J Med Sci 318:241-56
127. Poss KD, Thomas MJ, Ebralidze AK, O'Dell TJ, Tonegawa S (1995) Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron 15:867-73
128. Poss KD, Tonegawa S (1997) Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA 94:10919-24
129. Prestera T, Talalay P, Alam J, Ahn YI, Lee PJ, Choi AM (1995) Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE). Mol Med 1:827-37
130. Raju VS, McCoubrey WK, Jr, Maines MD (1997) Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta 1351:89-104
131. Regan R, Kumar N, Gao F, Guo Y (2002) Ferritin induction protects cortical astrocytes from heme-mediated oxidative injury. Neuroscience 113:985
132. Regan RF, Chen J, Benvenisti-Zarom L (2004) Heme oxygenase-2 gene deletion attenuates oxidative stress in neurons exposed to extracellular hemin. BMC Neurosci 5:34
133. Regan RF, Guo Y, Kumar N (2000) Heme oxygenase-1 induction protects murine cortical astrocytes from hemoglobin toxicity. Neurosci Lett 282:1-4
134. Regan RF, Panter SS (1996) Hemoglobin potentiates excitotoxic injury in cortical cell culture. J Neurotrauma 13:223-31
135. Regan RF, Rogers B (2003) Delayed treatment of hemoglobin neurotoxicity. J Neurotrauma 20:111-20
136. Ribas GC, Jane JA (1992) Traumatic contusions and intracerebral hematomas. J Neurotrauma 9(Suppl 1):S265-78
137. Robertson PL, Du Bois M, Bowman PD, Goldstein GW (1985) Angiogenesis in developing rat brain: an in vivo and in vitro study. Brain Res 355:219-23
138. Rogers B, Yakopson V, Teng ZP, Guo Y, Regan RF (2003) Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Radic Biol Med 35:872-81
139. Roskams AJ, Connor JR (1994) Iron, transferrin, and ferritin in the rat brain during development and aging. J Neurochem 63:709-16
140. Rotenberg MO, Maines MD (1990) Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J Biol Chem 265:7501-6
141. Rotenberg MO, Maines MD (1991) Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: possible heme-binding site? Arch Biochem Biophys 290:336-44
142. Rouault TA (2001) Systemic iron metabolism: a review and implications for brain iron metabolism. Pediatr Neurol 25:130-7
143. Ruppel RA, Clark RS, Bayir H, Satchell MA, Kochanek PM (2002) Critical mechanisms of secondary damage after inflicted head injury in infants and children. Neurosurg Clin N Am 13:169-82, v
144. Ryter SW, Tyrrell RM (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 28:289-309
145. Saikawa Y, Kaneda H, Yue L, Shimura S, Toma T, Kasahara Y, Yachie A, Koizumi S (2000) Structural evidence of genomic exon-deletion mediated by Alu-Alu recombination in a human case with heme oxygenase-1 deficiency. Hum Mutat 16:178-9
146. Sarco DP, Becker J, Palmer C, Sheldon RA, Ferriero DM (2000) The neuroprotective effect of deferoxamine in the hypoxic-ischemic immature mouse brain. Neurosci Lett 282:113-6
147. Schipper HM (1999) Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases. Neurotox Res 1:57-70
148. Schipper HM (2004) Heme oxygenase expression in human central nervous system disorders. Free Radic Biol Med 37:1995-2011
149. Seligman PAKRD, Huebers HA (1987) Molecular mechanisms of iron metabolism. In: The molecular basis of blood diseases (Stamatoyannopolous GNA, Leder P, Majerus PW, eds), Philadelphia: W.B. Saunders, pp 219-44
150. Shaklai N, Shviro Y, Rabizadeh E, Kirschner-Zilber I (1985) Accumulation and drainage of hemin in the red cell membrane. Biochim Biophys Acta 821:355-66
151. Shapiro SM (2003) Bilirubin toxicity in the developing nervous system. Pediatr Neurol 29:410-21
152. Shapiro SM (2005) Definition of the clinical spectrum of kernicterus and bilirubin-induced neurologic dysfunction (BIND). J Perinatol 25:54-9
153. Sharp FR, Massa SM, Swanson RA (1999) Heat-shock protein protection. Trends Neurosci 22:97-9
154. Shibahara S, Muller R, Taguchi H, Yoshida T (1985) Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci USA 82:7865-9
155. Shohami E, Beit-Yannai E, Horowitz M, Kohen R (1997) Oxidative stress in closed-head injury: brain antioxidant capacity as an indicator of functional outcome. J Cereb Blood Flow Metab 17:1007-19
156. Stocker R, Glazer AN, Ames BN (1987a) Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci USA 84:5918-22
157. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN (1987b) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043-6
158. Sun Y, Rotenberg MO, Maines MD (1990) Developmental expression of heme oxygenase isozymes in rat brain. Two HO-2 mRNAs are detected. J Biol Chem 265:8212-7
159. Suttner DM, Dennery PA (1999) Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 13:1800-9
160. Suzuki H, Kanamaru K, Tsunoda H, Inada H, Kuroki M, Sun H, Waga S, Tanaka T (1999) Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats. J Clin Invest 104:59-66
161. Takahashi M, Dore S, Ferris CD, Tomita T, Sawa A, Wolosker H, Borchelt DR, Iwatsubo T, Kim SH, Thinakaran G, Sisodia SS, Snyder SH (2000) Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease. Neuron 28:461-73
162. Tanaka T, Nishimura Y, Tsunoda H, Naka M (2000) Pharmacogenomics and therapeutic target validation in cerebral vasospasm. J Cardiovasc Pharmacol 36(Suppl 2):S1-4
163. Taylor EM, Crowe A, Morgan EH (1991) Transferrin and iron uptake by the brain: effects of altered iron status. J Neurochem 57:1584-92
164. Taylor EM, Morgan EH (1990) Developmental changes in transferrin and iron uptake by the brain in the rat. Brain Res Dev Brain Res 55:35-42
165. Turner CP, Bergeron M, Matz P, Zegna A, Noble LJ, Panter SS, Sharp FR (1998) Heme oxygenase-1 is induced in glia throughout brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab 18:257-73
166. Turner CP, Panter SS, Sharp FR (1999) Anti-oxidants prevent focal rat brain injury as assessed by induction of heat shock proteins (HSP70, HO-1/HSP32, HSP47) following subarachnoid injections of lysed blood. Brain Res Mol Brain Res 65:87-102
167. Vreman HJ, Wong RJ, Stevenson DK, Route RK, Reader SD, Fejer MM, Gale R, Seidman DS (1998) Light-emitting diodes: a novel light source for phototherapy. Pediatr Res 44:804-9
168. Wagner KR, Hua Y, de Courten-Myers GM, Broderick JP, Nishimura RN, Lu SY, Dwyer BE (2000) Tin-mesoporphyrin, a potent heme oxygenase inhibitor, for treatment of intracerebral hemorrhage: in vivo and in vitro studies. Cell Mol Biol (Noisy-le-grand) 46:597-608
169. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF (2003) Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab 23:629-52
170. Wagner KR, Xi G, Hua Y, Kleinholz M, de Courten-Myers GM, Myers RE, Broderick JP, Brott TG (1996) Lobar intracerebral hemorrhage model in pigs: rapid edema development in perihematomal white matter. Stroke 27:490-7
171. Watson BD (1993) Evaluation of the concomitance of lipid peroxidation in experimental models of cerebral ischemia and stroke. Prog Brain Res 96:69-95
172. Weber CM, Eke BC, Maines MD (1994) Corticosterone regulates heme oxygenase-2 and NO synthase transcription and protein expression in rat brain. J Neurochem 63:953-62
173. Wong RJ, Vreman HJ, Stevenson DK (2000) Effects of (metallo)Porphyrin inhibitors of heme oxygenase on lipid peroxidation. Acta Hematol 103:78
174. Wong RJN, X N, Zhao H, Vreman HJ, Contag CH, Stevenson DK (2002) Developmentally regulated pattern of heme oxygenase-1 expression in the mouse brain. Pediatri Res 51:328A
175. Wu J, Hua Y, Keep RF, Nakamura T, Hoff JT, Xi G (2003) Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke 34:2964-9
176. Wu J, Hua Y, Keep RF, Schallert T, Hoff JT, Xi G (2002) Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Res 953:45-52
177. Xi G, Hua Y, Bhasin RR, Ennis SR, Keep RF, Hoff JT (2001) Mechanisms of edema formation after intracerebral hemorrhage: effects of extravasated red blood cells on blood flow and blood-brainbarrier integrity. Stroke 32:2932-8
178. Xi G, Keep RF, Hoff JT (1998) Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg 89:991-6
179. Xia ZW, Cui WJ, Zhang XH, Shen QX, Wang J, Li YZ, Chen SN, Yu SC (2002) Analysis of heme oxygenase isomers in rat. World J Gastroenterol 8:1123-8
180. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103:129-35
181. Zhang W, Feng JQ, Harris SE, Contag PR, Stevenson DK, Contag CH (2001) Rapid in vivo functional analysis of transgenes in mice using whole body imaging of luciferase expression. Transgenic Res 10:423-34