Nrf2 to Pre-condition the Brain Against Injury Caused by Products of Hemolysis After ICH

Translational Stroke Research

Volumn 4, Issue 1, 2013, Pages 71-75

  Zhao, Xiurong ^a   Aronowski, Jaroslaw ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Cytoprotection; Intracerebral hemorrhage; Nrf2; Oxidative stress

Indexed keywords

CATALASE; FERRITIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HAPTOGLOBIN; HEME OXYGENASE 1; HEMOGLOBIN; HEMOPEXIN; PEROXIREDOXIN; SUPEROXIDE DISMUTASE; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR NRF2;

ALKYLATION; ARTICLE; BRAIN HEMORRHAGE; BRAIN INJURY; DETOXIFICATION; ERYTHROCYTE; HEMOLYSIS; HUMAN; OXIDATION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UBIQUITINATION;

CEREBRAL HEMORRHAGE; HEMOLYSIS; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS;

EID: 84872667758     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-012-0245-y     Document Type: Article

References (69)

1. Keep RF, Hua Y, Xi G. Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol. 2012; 11(8): 720-31.
2. Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet. 2009; 373(9675): 1632-44.
3. Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke. 2011; 42(6): 1781-6.
4. Xi G, Fewel ME, Hua Y, Thompson Jr BG, Hoff JT, Keep RF. Intracerebral hemorrhage: pathophysiology and therapy. Neurocrit Care. 2004; 1(1): 5-18.
5. Wagner KR, Dwyer BE. Hematoma removal, heme, and heme oxygenase following hemorrhagic stroke. Ann N Y Acad Sci. 2004; 1012: 237-51.
6. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF. Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab. 2003; 23(6): 629-52.
7. Aronowski J, Hall CE. New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res. 2005; 27(3): 268-79.
8. Huang FP, Xi G, Keep RF, Hua Y, Nemoianu A, Hoff JT. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J Neurosurg. 2002; 96(2): 287-93.
9. Wu J, Hua Y, Keep RF, Schallert T, Hoff JT, Xi G. Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Res. 2002; 953(1-2): 45-52.
10. Ascenzi P, Bocedi A, Visca P, Altruda F, Tolosano E, Beringhelli T, et al. Hemoglobin and heme scavenging. IUBMB Life. 2005; 57(11): 749-59.
11. Schaer DJ, Alayash AI, Buehler PW. Gating the radical hemoglobin to macrophages: the anti-inflammatory role of CD163, a scavenger receptor. Antioxid Redox Signal. 2007; 9(7): 991-9.
12. Tolosano E, Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol. 2002; 21(4): 297-306.
13. Muller-Eberhard U. Hemopexin. N Engl J Med. 1970; 283(20): 1090-4.
14. Hvidberg V, Maniecki MB, Jacobsen C, Hojrup P, Moller HJ, Moestrup SK. Identification of the receptor scavenging hemopexin-heme complexes. Blood. 2005; 106(7): 2572-9.
15. Kirkby KA, Adin CA. Products of heme oxygenase and their potential therapeutic applications. Am J Physiol. 2006; 290(3): F563-71.
16. Roskams AJ, Connor JR. Iron, transferrin, and ferritin in the rat brain during development and aging. J Neurochem. 1994; 63(2): 709-16.
17. Rogers J, Munro H. Translation of ferritin light and heavy subunit mRNAs is regulated by intracellular chelatable iron levels in rat hepatoma cells. Proc Natl Acad Sci U S A. 1987; 84(8): 2277-81.
18. van Muiswinkel FL, Kuiperij HB. The Nrf2-ARE signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders. Curr Drug Targets CNS Neurol Disord. 2005; 4(3): 267-81.
19. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47: 89-116.
20. Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB. Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J Biol Chem. 2005; 280(37): 32485-92.
21. Zhao X, Sun G, Zhang J, Strong R, Dash PK, Kan YW, et al. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke. 2007; 38(12): 3280-6.
22. Wang J, Fields J, Zhao C, Langer J, Thimmulappa RK, Kensler TW, et al. Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med. 2007; 43(3): 408-14.
23. Lee JM, Shih AY, Murphy TH, Johnson JA. NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J Biol Chem. 2003; 278(39): 37948-56.
24. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem. 2003; 278(14): 12029-38.
25. Johnson DA, Amirahmadi S, Ward C, Fabry Z, Johnson JA. The absence of the pro-antioxidant transcription factor Nrf2 exacerbates experimental autoimmune encephalomyelitis. Toxicol Sci. 2010; 114(2): 237-46.
26. Wada T, Oara H, Watanabe K, Kinoshita H, Yachi A. Autoradiographic study on the site of uptake of the haptoglobin-hemoglobin complex. J Reticuloendothel Soc. 1970; 8(2): 185-93.
27. Xi G, Keep RF, Hoff JT. Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg. 1998; 89(6): 991-6.
28. Wang X, Mori T, Sumii T, Lo EH. Hemoglobin-induced cytotoxicity in rat cerebral cortical neurons: caspase activation and oxidative stress. Stroke. 2002; 33(7): 1882-8.
29. Sadrzadeh SM, Graf E, Panter SS, Hallaway PE, Eaton JW. Hemoglobin. A biologic fenton reagent. J Biol Chem. 1984; 259(23): 14354-6.
30. Lee MY, Kim SY, Choi JS, Lee IH, Choi YS, Jin JY, et al. Upregulation of haptoglobin in reactive astrocytes after transient forebrain ischemia in rats. J Cereb Blood Flow Metab. 2002; 22(10): 1176-80.
31. Cid MC, Grant DS, Hoffman GS, Auerbach R, Fauci AS, Kleinman HK. Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis. J Clin Invest. 1993; 91(3): 977-85.
32. Yang F, Haile DJ, Berger FG, Herbert DC, van Beveren E, Ghio AJ. Haptoglobin reduces lung injury associated with exposure to blood. Am J Physiol Lung Cell Mol Physiol. 2003; 284(2): L402-9.
33. Chen W, Lu H, Dutt K, Smith A, Hunt DM, Hunt RC. Expression of the protective proteins hemopexin and haptoglobin by cells of the neural retina. Exp Eye Res. 1998; 67(1): 83-93.
34. Zhao X, Song S, Sun G, Strong R, Zhang J, Grotta JC, et al. Neuroprotective role of haptoglobin after intracerebral hemorrhage. J Neurosci. 2009; 29(50): 15819-27.
35. Panter SS, Sadrzadeh SM, Hallaway PE, Haines J, Anderson VE, Eaton JW. Hypohaptoglobinemia: a possible predisposition to epilepsy. Trans Assoc Am Physicians. 1984; 97: 56-62.
36. Miller YI, Altamentova SM, Shaklai N. Oxidation of low-density lipoprotein by hemoglobin stems from a heme-initiated globin radical: antioxidant role of haptoglobin. Biochemistry. 1997; 36(40): 12189-98.
37. Goldstein L, Teng ZP, Zeserson E, Patel M, Regan RF. Hemin induces an iron-dependent, oxidative injury to human neuron-like cells. J Neurosci Res. 2003; 73(1): 113-21.
38. Camejo G, Halberg C, Manschik-Lundin A, Hurt-Camejo E, Rosengren B, Olsson H, et al. Hemin binding and oxidation of lipoproteins in serum: mechanisms and effect on the interaction of LDL with human macrophages. J Lipid Res. 1998; 39(4): 755-66.
39. Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Eaton JW, et al. Heme, heme oxygenase and ferritin in vascular endothelial cell injury. Mol Nutr Food Res. 2005; 49(11): 1030-43.
40. Nikkila H, Gitlin JD, Muller-Eberhard U. Rat hemopexin. Molecular cloning, primary structural characterization, and analysis of gene expression. Biochemistry. 1991; 30(3): 823-9.
41. Grinberg LN, O'Brien PJ, Hrkal Z. The effects of heme-binding proteins on the peroxidative and catalatic activities of hemin. Free Radic Biol Med. 1999; 27(1-2): 214-9.
42. Hunt RC, Hunt DM, Gaur N, Smith A. Hemopexin in the human retina: protection of the retina against heme-mediated toxicity. J Cell Physiol. 1996; 168(1): 71-80.
43. Tolosano E, Cutufia MA, Hirsch E, Silengo L, Altruda F. Specific expression in brain and liver driven by the hemopexin promoter in transgenic mice. Biochem Biophys Res Commun. 1996; 218(3): 694-703.
44. Delanghe JR, Langlois MR. Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin Chim Acta. 2001; 312(1-2): 13-23.
45. Tolosano E, Fagoonee S, Hirsch E, Berger FG, Baumann H, Silengo L, et al. Enhanced splenomegaly and severe liver inflammation in haptoglobin/hemopexin double-null mice after acute hemolysis. Blood. 2002; 100(12): 4201-8.
46. Kristiansson MH, Bhat VB, Babu IR, Wishnok JS, Tannenbaum SR. Comparative time-dependent analysis of potential inflammation biomarkers in lymphoma-bearing SJL mice. J Proteome Res. 2007; 6(5): 1735-44.
47. Shen G, Xu C, Hu R, Jain MR, Gopalkrishnan A, Nair S, et al. Modulation of nuclear factor E2-related factor 2-mediated gene expression in mice liver and small intestine by cancer chemopreventive agent curcumin. Mol Cancer Ther. 2006; 5(1): 39-51.
48. Li N, Venkatesan MI, Miguel A, Kaplan R, Gujuluva C, Alam J, et al. Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol. 2000; 165(6): 3393-401.
49. Turner CP, Bergeron M, Matz P, Zegna A, Noble LJ, Panter SS, et al. Heme oxygenase-1 is induced in glia throughout brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab. 1998; 18(3): 257-73.
50. Ewing JF, Haber SN, Maines MD. 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. 1992; 58(3): 1140-9.
51. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006; 86(2): 583-650.
52. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997; 37: 517-54.
53. Lin Y, Vreman HJ, Wong RJ, Tjoa T, Yamauchi T, Noble-Haeusslein LJ. Heme oxygenase-1 stabilizes the blood-spinal cord barrier and limits oxidative stress and white matter damage in the acutely injured murine spinal cord. J Cereb Blood Flow Metab. 2007; 27(5): 1010-21.
54. Parfenova H, Basuroy S, Bhattacharya S, Tcheranova D, Qu Y, Regan RF, et al. Glutamate induces oxidative stress and apoptosis in cerebral vascular endothelial cells: contributions of HO-1 and HO-2 to cytoprotection. Am J Physiol Cell Physiol. 2006; 290(5): C1399-410.
55. Ahmad AS, Zhuang H, Dore S. Heme oxygenase-1 protects brain from acute excitotoxicity. Neuroscience. 2006; 141(4): 1703-8.
56. Panahian N, Yoshiura M, Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem. 1999; 72(3): 1187-203.
57. Wagener FA, van Beurden HE, von den Hoff JW, Adema GJ, Figdor CG. The heme-heme oxygenase system: a molecular switch in wound healing. Blood. 2003; 102(2): 521-8.
58. Gong Y, Tian H, Xi G, Keep RF, Hoff JT, Hua Y. Systemic zinc protoporphyrin administration reduces intracerebral hemorrhage-induced brain injury. Acta Neurochir Suppl. 2006; 96: 232-6.
59. Wagner KR, Hua Y, de Courten-Myers GM, Broderick JP, Nishimura RN, Lu SY, et al. Tin-mesoporphyrin, a potent heme oxygenase inhibitor, for treatment of intracerebral hemorrhage: in vivo and in vitro studies. Cell Mol Biol (Noisy-le-Grand). 2000; 46(3): 597-608.
60. Koeppen AH, Dickson AC, Smith J. Heme oxygenase in experimental intracerebral hemorrhage: the benefit of tin-mesoporphyrin. J Neuropathol Exp Neurol. 2004; 63(6): 587-97.
61. Gerlach M, Ben-Shachar D, Riederer P, Youdim MB. Altered brain metabolism of iron as a cause of neurodegenerative diseases? J Neurochem. 1994; 63(3): 793-807.
62. Chi SI, Wang CK, Chen JJ, Chau LY, Lin TN. Differential regulation of H- and L-ferritin messenger RNA subunits, ferritin protein and iron following focal cerebral ischemia-reperfusion. Neuroscience. 2000; 100(3): 475-84.
63. Yanagawa T, Itoh K, Uwayama J, Shibata Y, Yamaguchi A, Sano T, et al. Nrf2 deficiency causes tooth decolourization due to iron transport disorder in enamel organ. Genes Cells. 2004; 9(7): 641-51.
64. Pietsch EC, Chan JY, Torti FM, Torti SV. Nrf2 mediates the induction of ferritin H in response to xenobiotics and cancer chemopreventive dithiolethiones. J Biol Chem. 2003; 278(4): 2361-9.
65. Hua Y, Nakamura T, Keep RF, Wu J, Schallert T, Hoff JT, et al. Long-term effects of experimental intracerebral hemorrhage: the role of iron. J Neurosurg. 2006; 104(2): 305-12.
66. Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G. Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg. 2004; 100(4): 672-8.
67. Wan S, Hua Y, Keep RF, Hoff JT, Xi G. Deferoxamine reduces CSF free iron levels following intracerebral hemorrhage. Acta Neurochir Suppl. 2006; 96: 199-202.
68. Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, et al. Identification of the haemoglobin scavenger receptor. Nature. 2001; 409(6817): 198-201.
69. Hu R, Hebbar V, Kim BR, Chen C, Winnik B, Buckley B, et al. In vivo pharmacokinetics and regulation of gene expression profiles by isothiocyanate sulforaphane in the rat. J Pharmacol Exp Ther. 2004; 310(1): 263-71.