Redox regulation in neurodegeneration and longevity: Role of the heme oxygenase and HSP70 systems in brain stress tolerance

Antioxidants and Redox Signaling

Volumn 6, Issue 5, 2004, Pages 895-913

  Calabrese, Vittorio ^a   Giuffrida Stella, A M ^a   Butterfield, D Allan ^b   Scapagnini, Giovanni ^a  

^a UNIVERSITY OF CATANIA   (Italy)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; ANTIOXIDANT; BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; DNA; GLUTATHIONE; HEAT SHOCK PROTEIN 70; HEME OXYGENASE; NITRIC OXIDE; RNA; THIOL; VASOACTIVE AGENT;

AGING; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; BRAIN; BRAIN DYSFUNCTION; BRAIN FUNCTION; BRAIN ISCHEMIA; CANCER; CATALYSIS; CELL PROTECTION; CELL REGENERATION; DEFENSE MECHANISM; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME INDUCTION; EXON; GENE; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENETIC CONSERVATION; HUMAN; INFLAMMATION; INTRON; LIFESPAN; LONGEVITY; MACROMOLECULE; METABOLIC DISORDER; MOLECULE; NERVE DEGENERATION; NEUROPROTECTION; NITROSATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; QUALITY OF LIFE; REPERFUSION INJURY; REVIEW; STRESS; SURVIVAL; TISSUE INJURY;

AGING; ANTIOXIDANTS; BRAIN; CARBON MONOXIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE (DECYCLIZING); HSP70 HEAT-SHOCK PROTEINS; HUMANS; ISOENZYMES; LONGEVITY; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 4544327666     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2004.6.895     Document Type: Review

References (162)

1. Alam J. Heme oxygenase-1: past, present, and future. Antioxid Redox Signal 4: 559-562, 2002.
2. Alam J and Cook JL. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9: 2499-2511, 2003.
3. Aquino DA, Capello E, Weisstein J, Sanders V, Lopez C, Tourtellotte WW, Brosnan CF, Raine CS, and Norton WT. Multiple sclerosis: altered expression of 70- and 27-kDa heat shock proteins in lesions and mielin. J Neuropathol Exp Neurol 56: 664-672, 1977.
4. Bagasra O, Michaels FH, Zheng YM, Bobroski LE, Spitsin SV, Fu ZF, Tawadros R, and Koprowski H. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc Natl Acad Sci USA 92: 12041-12045, 1995.
5. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, Alam J, and Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 371: 887-895, 2003.
6. Beal MF. Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann Neurol 44: S110-S114, 1998.
7. Beal MF. Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Ann N Y Acad Sci 991: 120-131, 2003.
8. Bechtold DA and Brown IR. Induction of Hsp27 and Hsp32 stress proteins and vimentin in glial cells of the rat hippocampus following hyperthermia. Neurochem Res 28: 1163-1173, 2003.
9. Beschorner R, Adjodah D, Schwab JM, Mittelbronn M, Pedal I, Mattern R, Schluesener HJ, and Meyermann R. Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans. Acta Neuropathol 100: 377-384, 2000.
10. Borger DR and Essig DA. Induction of HSP32 gene in hypoxic cardiomyocytes is attenuated by treatment with N-acetyl-L-cysteine. Am J Physiol 274: H965-H973, 1998.
11. Bouton C and Demple B, Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J Biol Chem 275: 32688-32693, 2000.
12. Bredt DS. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31: 577-596, 1999.
13. Butterfield DA. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic Res 36: 1307-1313, 2002.
14. Butterfield DA. Oxidative stress in animal model of accelerated aging, Alzheimer's disease and Huntington's disease. In: Frontiers of Medicinal Chemistry, edited by Reitz AB, Kordki CP, Choudhary MI, and Rahman AU. New York: Bentham Science Publishers, 2004, pp. 385-397.
15. Butterfield DA and Kanski J. Methionine residue 35 is critical for the oxidative stress and neurotoxic properties of Alzheimer's amyloid-peptide 1-42. Review. Peptides 23: 1299-1309, 2002.
16. Butterfield DA, Castegna A, Drake J, Scapagnini G, and Calabrese V Vitamin E and neurodegenerative disorders associated with oxidative stress. Nutr Neurosci 5: 229-239, 2002.
17. Butterfield DA, Castegna A, Pocernich CB, Drake J, Scapagnini G, and Calabrese V. Nutritional approaches to combat oxidative stress in Alzheimer's disease. J Nutr Biochem 13: 444-461, 2002.
18. Butterfield DA, Pocernich CB, and Drake J. Elevated glutathione as a therapeutic strategy in Alzheimer's disease, Drug Discov Res 56: 428-437, 2002.
19. Butterfield DA, Boyd-Kimball D, and Castegna A. Proteomics in Alzheimer's disease: insights into mechanisms of neurodegeneration. J Neurochem 86: 1313-1327, 2003.
20. Calabrese V, Raffaele R, Cosentino E, and Rizza V. Changes in cerebrospinal fluid levels of malonaldehyde and glutathione reductase activity in multiple sclerosis. J Clin Pharmacol Res 4: 119-123, 1994.
21. Calabrese V, Bella R, Testa D, Spadaro F, Scrofani A, Rizza V, and Pennisi G. Increased cerebrospinal fluid and plasma levels of ultraweak chemiluminescence are associated with changes in the thiol pool and lipid-soluble fluorescence in multiple sclerosis: the pathogenic role of oxidative stress. Drugs Exp Clin Res 24: 125-131, 1998.
22. Calabrese V, Copani A, Testa D, Ravagna A, Spadaro F, Tendi E, Nicoletti VG, and Giuffrida Stella AM. Nitric oxide synthase induction in astroglial cell cultures: effect on heat shock protein 70 synthesis and oxidant/antioxidant balance. J Neurosci Res 60: 613-622, 2000.
23. Calabrese V, Bates TE, and Giuffrida Stella AM. NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem Res 65: 1315-1341, 2000.
24. Calabrese V, Testa D, Ravagna A, Bates TE, and Giuffrida Stella AM. Hsp70 induction in the brain following ethanol administration in the rat: regulation by glutathione redox state. Biochem Biophys Res Commun 269: 397-400, 2000.
25. Calabrese V, Scapagnini G, Giuffrida Stella AM, Bates TE, and Clark JB. Mitocondrial involvement in brain function and dysfunction: relevance to aging, neurodegenerative disorders and longevity. Neurochem Res 26: 739-764, 2001.
26. Calabrese V, Scapagnini G, Ravagna A, Fariello RG, Giuffrida Stella AM, and Abraham NG. Regional distribution of heme oxygenase, HSP70, and glutathione in brain: relevance for endogenous oxidant/antioxidant balance and stress tolerance. J Neurosci Res 68: 65-75, 2002.
27. Calabrese V, Scapagnini G, Ravagna A, Bella R, Foresti R, Bates TE, Giuffrida Stella AM, and Pennisi G. Nitric oxide synthase is present in the cerebrospinal fluid of patients with active multiple sclerosis and is associated with increases in cerebrospinal fluid protein nitrotyrosine, S-nitrosothiols and with changes in glutathione levels. J Neurosci Res 70: 580-587, 2002.
28. Calabrese V, Scapagnini G, Ravagna A, Giuffrida Stella AM, and Butterfield DA, Molecular chaperones and their roles in neural cell differentiation. Dev Neurosci 24: 1-13, 2002.
29. Calabrese V, Scapagnini G, Colombrita C, Ravagna A, Pennisi G, Giuffrida Stella AM, Galli F, and Butterfield DA. Redox regulation of heat shock protein expression in aging and neurodegenerative disorders associated with oxidative stress: a nutritional approach. Amino Acids 25: 437-444, 2003.
30. Calabrese V, Scapagnini G, Ravagna A, Bella R, Butterfield DA, Calvani M. Pennisi G, and Giuffrida Stella AM. Disruption of thiol homeostasis and nitrosative stress in the cerebrospinal fluid of patients with active multiple sclerosis: evidence for a protective role of acetylcarnitine. Neurochem Res 28: 1321-1328, 2003.
31. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, and Giuffrida Stella AM. Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech Ageing Dev 125: 325-335, 2004.
32. Catania MV, Giuffrida R, Seminara G, Barbagallo G, Aronica E, Gorter JA, Dell' Albani P, Ravagna A, Calabrese V, and Giuffrida Stella AM. Upregulation of neuronal nitric oxide synthase in in vitro stellate astrocytes and in vivo reactive astrocytes after electrically induced status epilepticus. Neurochem Res 28: 607-615, 2003.
33. Chakrabarty A, Emerson MR, and LeVine SM. Heme oxygenase-1 in SJL mice with experimental allergic encephalomyelitis. Mult Scler 9: 372-381, 2003.
34. Chen K and Maines MD. Nitric oxide induces heme oxygenase-1 via mitogen-activated protein kinases ERK and p38. Cell Mol Biol 46: 609-617, 2000.
35. Chen K, Gunter K, and Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 75: 304-312, 2000.
36. Christman MF, Morgan RW, Jacobson FS, and Ames BN. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753-762, 1985.
37. Clark JE, Foresti R, Green CJ, and Motterlini R. Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress. Biochem J 348: 615-619, 2000.
38. Coceani F, Kelsey L, Seidlitz E, Marks GS, McLaughlin BE, Vreman HJ, Stevenson DK, Rabinovitch M, and Ackerley C. Carbon monoxide formation in the ductus arteriosus in the lamb: implications for the regulation of muscle tone. Br J Pharmacol 120: 599-608, 1997.
39. Colombrita C, Calabrese V, Giuffrida Stella AM, Mattei F, Alkon DL, and Scapagnini G. Regional rat brain distribution of heme oxygenase-1 and manganese superoxide dismutase mRNA: relevance of redox homeostasis in the aging processes. Exp Biol Med 228: 517-524, 2003.
40. Dawson TM and Dawson VL. Neuroprotective and neurorestorative strategies for Parkinson's disease. Nat Neurosci 5: 1058-1061, 2002.
41. Dawson VL and Dawson TM. Physiological and toxicological actions of nitric oxide in the central nervous system. Adv Pharmacol 34: 323-342, 1995.
42. Dore S. Decreased activity of the antioxidant heme oxygenase enzyme: implications in ischemia and in Alzheimer's disease. Free Radic Biol Med 12: 1276-1282, 2002.
43. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, and Snyder SH. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450, 1999.
44. Dore S, Goto S, Sampei K, Blackshaw S, Hester LD, Ingi T, Sawa A, Traystman RJ, Koehler RC, and Snyder SH. Heme oxygenase-2 acts to prevent neuronal death in brain cultures and following transient cerebral ischemia. Neuroscience 99: 587-592, 2000.
45. Dringen R and Hirrlinger J. Glutathione pathways in the brain. Biol Chem 384: 505-516, 2003.
46. Ewing JF and Maines MD. Rapid induction of heme oxygenase 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc Natl Acad Sci USA 88: 5364-5368, 1991.
47. Ewing JF and Maines MD. In situ hybridization and immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: differential distribution of isozyme 1 and 2. Mol Cell Neurosci 3: 559-570, 1992.
48. Fink SL, Chang LK, Ho DY, and Sapolsky RM. Defective herpes simplex virus vectors expressing the rat brain stress-inducible heat shock protein 72 protect cultured neurons from severe heat shock. J Neurochem 68: 961-969, 1997.
49. Fogg S, Agarwal A, Nick HS, and Visne GA. Iron regulates hyperoxia dependent human heme oxygenase 1 gene expression in pulmonary endothelial cells. Am J Respir Cell Mol Biol 20: 797-804, 1999.
50. Foresti R and Motterlini R. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res 31: 459-475, 1999.
51. Foresti R, Clark JE, Green CJ, and Motterlini R. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. J Biol Chem 111: 18411-18417, 1997.
52. Foresti R, Goatly H, Green CJ, and Motterlini R. Role of heme oxygenase-1 in hypoxia-reoxygenation: requirement of substrate heme to promote cardioprotection. Am J Physiol Heart Circ Physiol 281: H1976-H1984, 2001.
53. Gegg ME, Beltran B, Salas-Pino S, Bolanos JP, Clark JB, Moncada S, and Heales SJ. Differential effect of nitric oxide on glutathione metabolism and mitochondrial function in astrocytes and neurones: implications for neuroprotection/neurodegeneration? J Neurochem 86: 228-237, 2003.
54. Glaum SR and Miller RJ. Zinc protoporphyrin-IX blocks the effects of metabotropic glutamate receptor activation in the rat nucleus tractus solitarii. Mol Pharmacol 43: 965-969, 1993.
55. Gong P, Stewart D, Hu B, Vinson C, and Alam J. Multiple basic-leucine zipper proteins regulate induction of the mouse heme oxygenase-1 gene by arsenite. Arch Biochem Biophys 405: 265-274, 2002.
56. Gorbunov NV, Yalowich JC, Gaddam A, Thampatty P, Ritov VB, Kisin ER, Elsayed NM, and Kagan VE. Nitric oxide prevents oxidative damage produced by tert-butyl hydroperoxide in erythroleukemia cells via nitrosylation of heme and non-heme iron. Electron paramagnetic resonance evidence. J Biol Chem 272: 12328-12341, 1997.
57. Graser T, Vedernikov YP, and Li DS. Study on the mechanism of carbon monoxide induced endothelium-independent relaxation in porcine coronary artery and vein. Biomed Biochim Acta 49: 293-296, 1990.
58. Greenberg JT, Monach P, Chou JH, Josephy PD, and Demple B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci USA 87: 6181-6185, 1990.
59. Gréhant N. Le gas du sang. Paris: 1894.
60. Halliwell B. Hypothesis: proteasomal dysfunction: a primary event in neurogeneration that leads to nitrative and oxidative stress and subsequent cell death. Ann N Y Acad Sci 962: 182-194, 2002.
61. Harman DA. A theory based on free radical and radiation chemistry. J Gerontol 11: 298-300, 1956.
62. Hartsfield CL, Alam J, Cook JL, and Choi AMK. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 273: L980-L988, 1997.
63. Hausladen A, Privalle CT, Keng T, DeAngelo J, and Stamler JS. Nitrosative stress: activation of the transcription factor OxyR. Cell 86: 719-729, 1996.
64. Heales SJR, Bolanos JP, Stewart VC, Brookes PS, Land JM, and Clark JB. Nitric oxide, mitochondria and neurological disease. Biochim Biophys Acta 1410: 215-228, 1999.
65. Hill-Kapturczak N, Sikorski EM, Voakes C, Garcia J, Nick HS, and Agarwal A. An internal enhancer regulates heme and cadmium-mediated induction of human heme oxygenase-1. Am J Physiol Renal Physiol 285: F515-F523, 2003.
66. Hon T, Hach A, Lee HC, Cheng T, and Zhang L. Functional analysis of heme regulatory elements of the transcriptional activator Hap1. Biochem Biophys Res Commun 273: 584-591, 2000.
67. Hyun DH, Lee M, Halliwell B, and Jenner P. Proteasomal inhibition causes the formation of protein aggregates containing a wide range of proteins, including nitrated proteins. J Neurochem 86: 363-373, 2003.
68. Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 53: 503-514, 2002.
69. Immenschuh S and Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem Pharmacol 60: 1121-1128, 2000.
70. Izaki K, Kinouchi H, Watanabe K, Owada Y, Okubo A, Itoh H, Kondo H, Tashima Y, Tamura S, Yoshimoto T, and Mizoi K. Induction of mitochondrial heat shock protein 60 and 10 mRNAs following transient focal cerebral ischemia in the rat. Brain Res Mol Brain Res 31: 14-25, 2001.
71. Jourd'heuil D, Hallen K, Feelisch M, and Grisham MB. Dynamic state of S-nitrosothiols in human plasma and whole blood. Free Radic Biol Med 28: 409-417, 2000.
72. Kanakiriya SK, Croatt AJ, Haggard JJ, Ingelfinger JR, Tang SS, Alam J, and Nath KA. Heme: a novel inducer of MCP-1 through HO-dependent and HO-independent mechanisms. Am J Physiol Renal Physiol 284: F546-F554, 2003.
73. Katory M, Busuttil RW, and Kupiec-Weglinski JW. Heme oxygenase-1 system in organ transplantation. Transplantation 74: 905-912, 2002.
74. Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, and Motterlini R. Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543: 113-119, 2003.
75. Kazazian HH Jr. Genetics. L1 retrotransposons shape the mammalian genome. Science 289: 1152-1153, 2000.
76. Kelly S and Yenari MA. Neuroprotection: heat shock proteins. Curr Med Res Opin 18: 55-60, 2002.
77. Kelly S, Zhang ZJ, Zhao H, Xu L, Giffard RG, Sapolsky RM, Yenari MA, and Steinberg GK. Gene transfer of HSP72 protects cornu ammonis 1 region of the hippocampus neurons from global ischemia: influence of Bcl-2. Ann Neurol 52: 160-167, 2002.
78. Keyse SM and Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide and sodium arsenite. Proc Natl Acad Sci USA 86: 99-103, 1989.
79. Kimpara T, Takeda A, Yamaguchi T, Arai H, Okita N, Takase S, Sasaki H, and Itoyama Y. Increased bilirubins and their derivatives in cerebrospinal fluid in Alzheimer's disease. Neurobiol Aging 21: 551-554, 2000.
80. Kirkwood TB. Evolution of ageing. Nature 270: 301-304, 1977.
81. Kullik I, Toledano MB, Tartaglia LA, and Storz G. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177: 1275-1284, 1995.
82. Le WD, Xie WJ, and Appel SH. Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury. J Neurosci Res 56: 652-658, 1999.
83. Lee TS and Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8: 240-248, 2002.
84. 2. J Biol Chem 278: 19325-19330, 2003.
85. Lindsey JW, Kerman RH, and Wolinsky JS. T cell-T cell activation in multiple sclerosis. Mult Scler 3: 238-242, 1997.
86. Liu N, Wang X, McCoubrey WK, and Maines MD. Developmentally regulated expression of two transcripts for heme oxygenase-2 with a first exon unique to rat testis: control by corticosterone of the oxygenase protein expression. Gene 241: 175-183, 2000.
87. Liu Y, Zhu B, Luo L, Li P, Paty DW, and Cynader MS. Heme oxygenase-1 plays an important protective role in experimental autoimmune encephalomyelitis. Neuroreport 12: 1841-1845, 2001.
88. Maines MD. The heme oxygenase system; a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517-554, 1997.
89. Maines MD. The heme oxygenase system and its functions in the brain. Cell Mol Biol 46: 573-585, 2000.
90. Mancuso C, Bonsignore A, Di Stasio E, Mordente A, and Motterlini R. Bilirubin and S-nitrosothiols interaction: evidence for a possible role of bilirubin as a scavenger of nitric oxide. Biochem Pharmacol 66: 2355-2366, 2003.
91. Marshall HE, Merchant K, and Stamler JS. Nitrosation and oxidation in the regulation of gene expression. FASEB J 14: 1889-1900, 2000.
92. Mattson MP, Duan W, Chan SL, Cheng A, Haughey N, Gary DS, Guo Z, Lee J, and Furukawa K. Neuroprotective and neurorestorative signal transduction mechanisms in brain aging: modification by genes, diet and behavior. Neurobiol Aging 23: 695-705, 2002.
93. Mautes AE, Bergeron M, Sharp FR, Panter SS, Weinzierl M, Guenther K, and Noble LJ. Sustained induction of heme oxygenase-1 in the traumatized spinal cord. Exp Neurol 166: 254-265, 2000.
94. Mayer RJ. From neurodegeneration to neurohomeostasis: the role of ubiquitin. Drug News Perspect 16: 103-108, 2003.
95. McCann SM, Licinio J, Wong ML, Yu WH, Karanth S, and Rettorri V. The nitric oxide hypothesis of aging. Exp Gerontol 33: 813-826, 1998.
96. McCoubrey WK, Huang TJ, and Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 272: 12568-12574, 1997.
97. McLaughlin B, Hartnett KA, Erhardt JA, Legos JJ, White RF, Barone FC, and Aizenman E. Caspase 3 activation is essential for neuroprotection in preconditioning. Proc Natl Acad Sci USA 100: 715-720, 2003.
98. McNaught KS, Olanow CW, Halliwell B, Isacson O, and Jenner P. Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat Rev Neurosci 2: 589-594, 2001.
99. Misseri R, Shaw MB, Gearhart JP, and Meldrum DR. Liposomal delivery of heat shock protein 72 into renal tubular cells blocks nuclear factor-kappaB activation, tumor necrosis factor-alpha production, and subsequent ischemia-induced apoptosis. Circ Res 92: 293-299, 2003.
100. Mohr S, Hallak H, de Boitte A, Lapetina EG, and Brune B. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274: 9427-9430, 1999.
101. Moore DJ, Dawson VL, and Dawson TM. Role for the ubiquitin-proteasome system in Parkinson's disease and other neurodegenerative brain amyloidoses. Neuromolecular Med 4: 95-108, 2003.
102. Mosser DD, Caron AW, Bourget L, and Denis-Larose D. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 17: 5317-5327, 1977.
103. Motterlini R, Foresti R, Bassi R, Calabrese V, Clark JE, and Green CJ. Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J Biol Chem 275: 13613-13620, 2000.
104. Motterlini R, Foresti R, Bassi R, and Green CJ. Curcumin, an antioxidant and antiinflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic Biol Med 28: 1303-1312, 2000.
105. Motterlini R, Green CJ, and Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal 4: 615-624, 2002.
106. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, ad Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 92: 17-24, 2002.
107. Motterlini R, Mann BE, Johnson TR, Clark JE, Foresti R, and Green CJ. Bioactivity and pharmacological actions of carbon monoxide-releasing molecules. Curr Pharm Des 9: 2525-2539, 2003.
108. Narasimhan P, Swanson RA, Sagar SM, and Sharp FR. Astrocyte survival and HSP70 heat shock protein induction following heat shock and acidosis. Glia 17: 147-159, 1996.
109. Nikitovic D, Holmgren A. and Spyrou G. Inhibition of AP-1 DNA binding by nitric oxide involving conserved cyteine residues in Jun and Fos. Biochem Biophys Res Commun 242: 109-112, 1998.
110. Otterbein LE. Carbon monoxide: innovative anti-inflammatory properties of an age-old gas molecule. Antioxid Redox Signal 4: 309-319, 2002.
111. Otterbein LE, Scares MP, Yamashita K, and Bach F. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24: 449-466, 2003.
112. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, Tyagi S, Akamatsu Y, Flavell RJ, Billiar TR, Tzeng E, Bach FH, Choi AM, and Soares MP. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 9: 183-190, 2003.
113. Perry G, Taddeo MA, Petersen RB, Castellani RJ, Harris PL, Siedlak SL, Cash AD, Liu Q, Nunomura A, Atwood CS, and Smith MA. Adventiously-bound redox active iron and copper are at the center of oxidative damage in Alzheimer disease. Biometals 16: 77-81, 2003.
114. Piantadosi CA, Zhang J, Levin ED, Folz RJ, and Schmechel DE. Apoptosis and delayed neuronal damage after carbon monoxide poisoning in the rat. Exp Neurol 147: 103-114, 1997.
115. Pieper GM, Halligan NL, Hilton G, Konorev EA, Felix CC, Roza AM, Adams MB, and Griffith OW. Non-heme iron protein: a potential target of nitric oxide in acute cardiac allograft rejection. Proc Natl Acad Sci USA 100: 3125-3130, 2003.
116. Poon F, Calabrese V, Scapagnini G, and Butterfield DA. Free radicals: key to brain aging and heme oxygenase as a cellular response to oxidative stress. J Gerontol 59: 478-493, 2004.
117. Poss KD and Tonegawa S. Reduced stress defense in heme oxygenase-deficient cells. Proc Natl Acad Sci U S A 94: 10925-10930, 1997.
118. Premkumar DR, Smith MA, Richey PL, Petersen RB, Castellani R, Kutty RK, Wiggert B, Perry G, and Kalaria RN. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J Neurochem 65: 1399-1402, 1995.
119. Raju VS, McCoubrey WK, and Maines MD. Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta 1351: 89-104, 1997.
120. Risch N and Merikangas K. The future of genetic studies of complex human diseases. Science 273: 1516-1517, 1996.
121. Rizzardini M, Carelli M, Cabello Porras MR, and Cantoni L. Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochem J 304: 477-483, 1994.
122. Rosenberg PA, Li Y, Ali S, Altiok N, Back SA, and Volpe JJ. Intracellular redox state determines whether nitric oxide is toxic or protective to rat oligodendrocytes in culture. J Neurochem 73: 476-484, 1999.
123. Roses AD. Apolipoprotein E alleles as risk factors in Alzheimer's disease. Annu Rev Med 47: 387-400, 1996.
124. Rossig L, Fichtlscherer B, Breitschopf K, Haendeler J, Zeiher AM, Mulsch A, and Dimmeler S. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 274: 6823-6826, 1999.
125. Rothschild H and Jazwinski S. Human longevity determinant genes. J La State Med Soc 150: 272-274, 1998.
126. Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, and Smith MA. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: a central role for bound transition metals. J Neurochem 74: 270-279, 2000.
127. Scapagnini G, Giuffrida Stella AM, Abraham NG, Alkon D, and Calabrese V. Differential expression of heme oxygenase-1 in rat brain by endotoxin (LPS). In: Heme Oxygenase in Biology and Medicine, Vol. 10, edited by Abraham NG, Alam J, and Nath KA. New York: Kluwer Academic/Plenum Publisher, 2002, pp. 121-134.
128. Scapagnini G, D'Agata V, Calabrese V, Pascal A, Colombrita C, Alkon D, and Cavallaro S. Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res 954: 51-59, 2002.
129. Scapagnini G, Foresti R, Calabrese V, Giuffrida Stella AM, Green CJ, and Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol Pharmacol 61: 554-561, 2002.
130. Scapagnini G, Ravagna A, Bella R, Colombrita C, Pennisi G, Calvani M, Alkon D, and Calabrese V. Long-term ethanol administration enhances age-dependent modulation of redox state in brain and peripheral organs of rat: protection by acetyl carnitine. Int J Tissue React 24: 89-96, 2002.
131. Schipper HM. Heme oxygenase-1: role in brain aging and neurodegeneration. Exp Gerontol 35: 821-830, 2000.
132. Schipper HM, Liberman A, and Stopa EG. Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp Neurol 150: 60-68, 1998.
133. Schipper HM, Chertkow H, Mehindate K, Frankel D, Melmed C, and Bergman H. Evaluation of heme oxygenase-1 as a systemic biological marker of sporadic AD. Neurology 54: 1297-1304, 2000.
134. Sergent O, Griffon B, Morel I, Chevanne M, Dubos MP, Cillard P, and Cillard J. Effect of nitric oxide on iron-mediated oxidative stress in primary rat hepatocyte culture. Hepatology 25: 122-127, 1997.
135. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, and Murphy TH. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 23: 3394-3406, 2003.
136. Sjorstrand T. Endogenous formation of carbon monoxide in man under normal and pathological conditions. Scand J Clin Lab Invest 1: 201-214, 1949.
137. Soti C and Csermely P. Chaperones and aging: role in neurodegeneration and in other civilizational diseases. Neurochem Int 41: 383-389, 2002.
138. Stamler JS and Hausladen A. Oxidative modifications in nitrosative stress. Cell 78: 931-936, 1998.
139. Stamler JS, Singel DI, and Loscalzo J. Biochemistry of nitric oxide and its redox activated forms. Science 258: 1898-1902, 1992.
140. Stewart D, Killeen E, Naquin R, Alam S, and Alam J. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem 278: 2396-2402, 2003.
141. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, and Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046, 1987.
142. Storz G, Tartaglia LA, and Ames BN. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248: 189-194, 1990.
143. Sun J, Hoshino O, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo M, Yamamoto M, and Igarashi K. Hemoprotein Bach 1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 21: 5216-5224, 2002.
144. Szabo G, Mandrekar P, and Catalane D. Inhibition of superantigen-induced T cell proliferation and moncyte IL-β, TNFα, and IL-6 production by acute ethanol treatment. J Leukoc Biol 58: 342-351, 1995.
145. Szilard L. On the nature of the aging process. Proc Natl Acad Sci USA 45: 35-45, 1959.
146. Takahashi M, Dore S, Ferris CD, Tomita T, Sawa A, Wolosker H, Borchelt DR, Iwatsubo T, Kim SH, Thinakaran G, Sisodia SS, and Snyder SH. Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease. Neuron 28: 461-473, 2002.
147. Takeda A, Perry G, Abraham NG, Dwyer BE, Kutty RK, Laitinen JT, Petersen RB, and Smith RB. Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau. J Biol Chem 275: 5395-5399, 2000.
148. Tenhunen R, Marver HS, and Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem 244: 6388-6394, 1969.
149. Tran EH, Hardin PH, Verge G, and Owens T. Astrocytes and microglia express inducible nitric oxide synthase in mice with experimental allergic encephalomyelitis. J Neuroimmunol 74: 121-129, 1997.
150. Turcanu V, Dhouib M, and Poindron P. Nitric oxide synthase inhibition by haem oxygenase decreases macrophage nitric-oxide-dependent cytotoxicity: a negative feedback mechanism for the regulation of nitric oxide production. Res Immunol 149: 741-744, 1998.
151. Turner CP, Panter SS, and Sharp FR. 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, 1999.
152. Tyrrell R. Redox regulation and oxidant activation of heme oxygenase-1. Free Radic Res 31: 335-340, 1999.
153. Valentim LM, Rodnight R, Geyer AB, Horn AP, Tavares A, Cimarosti H, Netto CA, and Salbego CG. Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience 118: 379-386, 2003.
154. van Noort JM, van Sechel AC, van Stipdonk MJ, and Bajramovic JJ. The small heat shock protein alpha B-crystallin as key autoantigen in multiple sclerosis. Prog Brain Res 117: 435-452, 1998.
155. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, and Snyder SH. Carbon monoxide: a putative neural messenger. Science 259: 381-384, 1993.
156. Visner GA, Lu F, Zhou H, Liu J, Kazemfar K, and Agarwal A. Rapamycin induces heme oxygenase-1 in human pulmonary vascular cells: implications in the antiproliferative response to rapamycin. Circulation 107: 911-916, 2003.
157. Wang R and Wu L. Interaction of selective amino acid residues of K(Ca) channels with carbon monoxide. Exp Biol Med 228: 474-480, 2003.
158. Weng YH, Yang G, Weiss S, and Dennery PA. Interaction between heme oxygenase-1 and -2 proteins. J Biol Chem 278: 50999-51005, 2003.
159. Wheeler DS, Dunsmore KE, and Wong HR. Intracellular delivery of HSP70 using HIV-1 Tat protein transduction domain. Biochem Biophys Res Commun 301: 54-59, 2003.
160. Yenari MA. Heat shock proteins and neuroprotection. Adv Exp Med Biol 513: 281-299, 2002.
161. Yoo MS, Chun HS, Son JJ, DeGiorgio LA, Kim DJ, Peng C, and Son JH. Oxidative stress regulated genes in nigral dopaminergic neuronal cells: correlation with the known pathology in Parkinson's disease. Brain Res Mol Brain Res 110: 76-84, 2003.
162. Zheng M, Aslund F, and Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721, 1998.