The Janus face of the heme oxygenase/biliverdin reductase system in Alzheimer disease: It's time for reconciliation

Neurobiology of Disease

Volumn 62, Issue , 2014, Pages 144-159

  Barone, Eugenio ^a,d   Di Domenico, Fabio ^b   Mancuso, Cesare ^c   Butterfield, D Allan ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d EPFL   (Switzerland)

Author keywords

Aging; Alzheimer disease; Biliverdin reductase; Heme oxygenase; Mild cognitive impairment; Oxidative stress

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; BILIVERDIN; BILIVERDIN REDUCTASE; CARBON MONOXIDE; FERROUS ION; HEME; HEME OXYGENASE 1; HEME OXYGENASE 2; JANUS KINASE; OXIDOREDUCTASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; BRAIN DEGENERATION; CELLULAR STRESS RESPONSE; CLINICAL FEATURE; DIET THERAPY; DISEASE ACTIVITY; DISEASE COURSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; MEMORY DISORDER; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NEUROTOXICITY; NITROSATIVE STRESS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; UPREGULATION;

3-NITROTYROSINE; 3-NT; 4-HYDROXY-2-NONENAL; AGING; ALZHEIMER DISEASE; ANTIOXIDANT RESPONSIVE ELEMENTS; ARE; BILIVERDIN REDUCTASE; BILIVERDIN REDUCTASE ISOFORM A; BVR-A; HEME OXYGENASE; HEME OXYGENASE ISOFORM 1 OR 2; HNE; HO-1/2; MILD COGNITIVE IMPAIRMENT; OXIDATIVE STRESS; PC; PROTEIN CARBONYLS;

ALZHEIMER DISEASE; ANIMALS; BRAIN; HEME OXYGENASE (DECYCLIZING); HUMANS; MODELS, NEUROLOGICAL; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS;

EID: 84886872345     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.09.018     Document Type: Article

References (223)

1. Akama K.T., et al. Amyloid beta-peptide stimulates nitric oxide production in astrocytes through an NFkappaB-dependent mechanism. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5795-5800.
2. Aksenov M., et al. Enhancement of beta-amyloid peptide A beta(1-40)-mediated neurotoxicity by glutamine synthetase. J. Neurochem. 1995, 65:1899-1902.
3. Akter K., et al. Diabetes mellitus and Alzheimer's disease: shared pathology and treatment?. Br. J. Clin. Pharmacol. 2011, 71:365-376.
4. Alam J., Cook J.L. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr. Pharm. Des. 2003, 9:2499-2511.
5. Axelsen P.H., et al. Oxidative stress and cell membranes in the pathogenesis of Alzheimer's disease. Physiology (Bethesda) 2011, 26:54-69.
6. Badia M.C., et al. Reductive stress in young healthy individuals at risk of Alzheimer disease. Free Radic. Biol. Med. 2013, 63C:274-279.
7. Balogun E., et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J. 2003, 371:887-895.
8. Barone E., et al. Characterization of the S-denitrosylating activity of bilirubin. J. Cell. Mol. Med. 2009, 13:2365-2375.
9. Barone E., et al. Biliverdin reductase-a protein levels and activity in the brains of subjects with Alzheimer disease and mild cognitive impairment. Biochim. Biophys. Acta 2011, 1812:480-487.
10. Barone E., et al. Oxidative and nitrosative modifications of biliverdin reductase-A in the brain of subjects with Alzheimer's disease and amnestic mild cognitive impairment. J. Alzheimers Dis. 2011, 25:623-633.
11. Barone E., et al. Heme oxygenase-1 posttranslational modifications in the brain of subjects with Alzheimer disease and mild cognitive impairment. Free Radic. Biol. Med. 2012, 52:2292-2301.
12. Barone E., et al. Biliverdin reductase-A: a novel drug target for atorvastatin in a dog pre-clinical model of Alzheimer disease. J. Neurochem. 2012, 120:135-146.
13. Behl C. Brain aging and late-onset Alzheimer's disease: many open questions. Int. Psychogeriatr. 2012, 24(Suppl. 1):S3-S9.
14. Boehning D., et al. Carbon monoxide neurotransmission activated by CK2 phosphorylation of heme oxygenase-2. Neuron 2003, 40:129-137.
15. Boehning D., et al. Heme oxygenase-2 is activated by calcium-calmodulin. J. Biol. Chem. 2004, 279:30927-30930.
16. Bonda D.J., et al. Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 2010, 59:290-294.
17. Braughler J.M., et al. The involvement of iron in lipid peroxidation. Importance of ferric to ferrous ratios in initiation. J. Biol. Chem. 1986, 261:10282-10289.
18. Brito M.A., et al. A link between hyperbilirubinemia, oxidative stress and injury to neocortical synaptosomes. Brain Res. 2004, 1026:33-43.
19. Brydun A., et al. Reduced expression of heme oxygenase-1 in patients with coronary atherosclerosis. Hypertens. Res. 2007, 30:341-348.
20. Bucher J.R., et al. Redox cycling and lipid peroxidation: the central role of iron chelates. Fundam. Appl. Toxicol. 1983, 3:222-226.
21. Butterfield D.A. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic. Res. 2002, 36:1307-1313.
22. Butterfield D.A. Oxidative stress in neurodegenerative disorders. Antioxid. Redox Signal. 2006, 8:1971-1973.
23. Butterfield D.A., Boyd-Kimball D. Amyloid beta-peptide(1-42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol. 2004, 14:426-432.
24. Butterfield D.A., Lauderback C.M. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic. Biol. Med. 2002, 32:1050-1060.
25. Butterfield D.A., Stadman E.R. Protein oxidation processes in aging brain. Advances in Cell Aging and Gerontology 1997, 161-191. S.T. Paula, E.E. Bittar (Eds.).
26. Butterfield D.A., Stadtman E.R. Protein Oxidation Processes in Aging Brain 1997.
27. Butterfield D.A., et al. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 2001, 7:548-554.
28. Butterfield D., et al. Nutritional approaches to combat oxidative stress in Alzheimer's disease. J. Nutr. Biochem. 2002, 13:444.
29. Butterfield D.A., et al. Vitamin E and neurodegenerative disorders associated with oxidative stress. Nutr. Neurosci. 2002, 5:229-239.
30. Butterfield D.A., et al. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol. Dis. 2006, 22:223-232.
31. Butterfield D.A., et al. Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic. Biol. Med. 2007, 43:658-677.
32. Butterfield D.A., et al. In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid beta-peptide of APP. Free Radic. Biol. Med. 2010, 48:136-144.
33. Butterfield D.A., et al. Atorvastatin treatment in a dog preclinical model of Alzheimer's disease leads to up-regulation of haem oxygenase-1 and is associated with reduced oxidative stress in brain. Int. J. Neuropsychopharmacol. 2012, 15:981-987.
34. Butterfield D.A., et al. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid. Redox Signal. 2012, 17:1610-1655.
35. Butterfield D.A., et al. Amyloid beta-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid. Redox Signal. 2013, 19(8):823-835.
36. Cai Z., et al. Oxidative stress and beta-amyloid protein in Alzheimer's disease. Neuromolecular Med. 2011, 13:223-250.
37. Calabrese V., et al. Redox regulation of heat shock protein expression in aging and neurodegenerative disorders associated with oxidative stress: a nutritional approach. Amino Acids 2003, 25:437-444.
38. Calabrese V., et al. Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer's disease. Antioxid. Redox Signal. 2006, 8:1975-1986.
39. Calabrese V., et al. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 2007, 8:766-775.
40. Calabrese V., et al. Oxidative stress and cellular stress response in diabetic nephropathy. Cell Stress Chaperones 2007, 12:299-306.
41. Calabrese V., et al. Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem. Res. 2008, 33:2444-2471.
42. Castegna A., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic. Biol. Med. 2002, 33:562-571.
43. Castegna A., et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J. Neurochem. 2002, 82:1524-1532.
44. Chen Z., Zhong C. Decoding Alzheimer's disease from perturbed cerebral glucose metabolism: implications for diagnostic and therapeutic strategies. Prog. Neurobiol. 2013, 108:21-43.
45. Chiang H.C., et al. PI3 kinase signaling is involved in Abeta-induced memory loss in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7060-7065.
46. Chiueh C.C. Iron overload, oxidative stress, and axonal dystrophy in brain disorders. Pediatr. Neurol. 2001, 25:138-147.
47. Clark T.A., et al. Oxidative stress and its implications for future treatments and management of Alzheimer disease. Int. J. Biomed. Sci. 2010, 6:225-227.
48. Cotman C.W., Head E. The canine (dog) model of human aging and disease: dietary, environmental and immunotherapy approaches. J. Alzheimers Dis. 2008, 15:685-707.
49. Cunningham O., et al. Initial-rate kinetics of the flavin reductase reaction catalysed by human biliverdin-IXbeta reductase (BVR-B). Biochem. J. 2000, 345(Pt 2):393-399.
50. Deane R., et al. RAGE (yin) versus LRP (yang) balance regulates Alzheimer amyloid beta-peptide clearance through transport across the blood-brain barrier. Stroke 2004, 35:2628-2631.
51. Dhakshinamoorthy S., et al. Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J. Biol. Chem. 2005, 280:16891-16900.
52. Di Domenico F., et al. Protein levels of heat shock proteins 27, 32, 60, 70, 90 and thioredoxin-1 in amnestic mild cognitive impairment: an investigation on the role of cellular stress response in the progression of Alzheimer disease. Brain Res. 2010, 1333:72-81.
53. Di Domenico F., et al. Circulating biomarkers of protein oxidation for Alzheimer disease: expectations within limits. Biochim. Biophys. Acta 2011, 1814:1785-1795.
54. Di Domenico F., et al. HO-1/BVR-a system analysis in plasma from probable Alzheimer's disease and mild cognitive impairment subjects: a potential biochemical marker for the prediction of the disease. J. Alzheimers Dis. 2012, 32:277-289.
55. Di Domenico F., et al. Impairment of proteostasis network in Down syndrome prior to the development of Alzheimer's disease neuropathology: redox proteomics analysis of human brain. Biochim. Biophys. Acta 2013, 1832:1249-1259.
56. Di Domenico F., et al. Biliverdin reductase-A correlates with iNOS in atorvastatin treated aged canine brain. Neural. Reg. Res. 2013, 8:1925-1937.
57. Dildar K., et al. Serum nitrosative stress levels are increased in Alzheimer disease but not in vascular dementia. Alzheimer Dis. Assoc. Disord. 2010, 24:194-197.
58. Dore S., et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2445-2450.
59. Dufouil C., et al. APOE genotype, cholesterol level, lipid-lowering treatment, and dementia: the Three-City Study. Neurology 2005, 64:1531-1538.
60. Dwyer B.E., et al. 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. 1995, 30:37-47.
61. Errico S., et al. Heme oxygenase-derived carbon monoxide modulates gonadotropin-releasing hormone release in immortalized hypothalamic neurons. Neurosci. Lett. 2010, 471:175-178.
62. Ewing J.F., et al. Biliverdin reductase is heat resistant and coexpressed with constitutive and heat shock forms of heme oxygenase in brain. J. Neurochem. 1993, 61:1015-1023.
63. Fagan A.M., Perrin R.J. Upcoming candidate cerebrospinal fluid biomarkers of Alzheimer's disease. Biomark. Med 2012, 6:455-476.
64. Fakhrai H., Maines M.D. Expression and characterization of a cDNA for rat kidney biliverdin reductase. Evidence suggesting the liver and kidney enzymes are the same transcript product. J. Biol. Chem. 1992, 267:4023-4029.
65. Feng Y., Wang X. Antioxidant therapies for Alzheimer's disease. Oxid. Med. Cell. Longev. 2012, 2012:472932.
66. Frankel D., et al. Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively-challenged astroglia. J. Cell. Physiol. 2000, 185:80-86.
67. Fujita T., et al. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 2001, 7:598-604.
68. Galasko D., Montine T.J. Biomarkers of oxidative damage and inflammation in Alzheimer's disease. Biomark. Med 2010, 4:27-36.
69. Gibbs P.E., Maines M.D. Biliverdin inhibits activation of NF-kappaB: reversal of inhibition by human biliverdin reductase. Int. J. Cancer 2007, 121:2567-2574.
70. Gibbs P.E., et al. Formation of ternary complex of human biliverdin reductase-protein kinase Cdelta-ERK2 protein is essential for ERK2-mediated activation of Elk1 protein, nuclear factor-kappaB, and inducible nitric-oxidase synthase (iNOS). J. Biol. Chem. 2012, 287:1066-1079.
71. Gibbs P.E., et al. Biliverdin reductase: more than a namesake - the reductase, its peptide fragments, and biliverdin regulate activity of the three classes of protein kinase C. Front. Pharmacol. 2012, 3:31.
72. Gozzelino R., et al. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 2010, 50:323-354.
73. Grossman M., et al. Cerebrospinal fluid profile in frontotemporal dementia and Alzheimer's disease. Ann. Neurol. 2005, 57:721-729.
74. Gustaw-Rothenberg K., et al. Biomarkers in Alzheimer's disease: past, present and future. Biomark. Med 2010, 4:15-26.
75. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
76. Hajjar I., et al. The impact of the use of statins on the prevalence of dementia and the progression of cognitive impairment. J. Gerontol. A Biol. Sci. Med. Sci. 2002, 57:M414-M418.
77. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 2006, 97:1634-1658.
78. Hascalovici J.R., et al. Brain sterol dysregulation in sporadic AD and MCI: relationship to heme oxygenase-1. J. Neurochem. 2009, 110:1241-1253.
79. Hayashi S., et al. Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 2004, 336:241-250.
80. He X., et al. Protection against chromium (VI)-induced oxidative stress and apoptosis by Nrf2. Recruiting Nrf2 into the nucleus and disrupting the nuclear Nrf2/Keap1 association. Toxicol. Sci. 2007, 98:298-309.
81. Head E., et al. Oxidative stress, aging, and central nervous system disease in the canine model of human brain aging. Vet. Clin. North Am. Small Anim. Pract. 2008, 38:167-178. (vi).
82. Hensley K., et al. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J. Neurochem. 1995, 65:2146-2156.
83. Horwood J.M., et al. Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur. J. Neurosci. 2006, 23:3375-3384.
84. Hui Y., et al. Long-term overexpression of heme oxygenase 1 promotes tau aggregation in mouse brain by inducing tau phosphorylation. J. Alzheimers Dis. 2011, 26:299-313.
85. Hyman B.T., Hyman B.T., et al. Extracellular signal regulated kinases. Localization of protein and mRNA in the human hippocampal formation in Alzheimer's disease. Am. J. Pathol. 1994, 144:565-572.
86. Irizarry M.C., et al. Plasma F2A isoprostane levels in Alzheimer's and Parkinson's disease. Neurodegener. Dis. 2007, 4:403-405.
87. Ishizuka K., et al. Possible assessment for antioxidant capacity in Alzheimer's disease by measuring lymphocyte heme oxygenase-1 expression with real-time RT-PCR. Ann. N. Y. Acad. Sci. 2002, 977:173-178.
88. Jack C.R., et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010, 9:119-128.
89. Jick H., et al. Statins and the risk of dementia. Lancet 2000, 356:1627-1631.
90. Johnstone E.M., et al. Conservation of the sequence of the Alzheimer's disease amyloid peptide in dog, polar bear and five other mammals by cross-species polymerase chain reaction analysis. Brain Res. Mol. Brain Res. 1991, 10:299-305.
91. Joshi G., et al. Glutathione elevation by gamma-glutamyl cysteine ethyl ester as a potential therapeutic strategy for preventing oxidative stress in brain mediated by in vivo administration of adriamycin: implication for chemobrain. J. Neurosci. Res. 2007, 85:497-503.
92. Kaide J.I., et al. Carbon monoxide of vascular origin attenuates the sensitivity of renal arterial vessels to vasoconstrictors. J. Clin. Invest. 2001, 107:1163-1171.
93. Kanninen K., et al. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16505-16510.
94. Kapitulnik J. Bilirubin: an endogenous product of heme degradation with both cytotoxic and cytoprotective properties. Mol. Pharmacol. 2004, 66:773-779.
95. Kapitulnik J., Maines M.D. Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol. Sci. 2009, 30:129-137.
96. Keller J.N., et al. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 2005, 64:1152-1156.
97. Kim T.S., et al. Decreased plasma antioxidants in patients with Alzheimer's disease. Int. J. Geriatr. Psychiatry 2006, 21:344-348.
98. Kimpara T., et al. Increased bilirubins and their derivatives in cerebrospinal fluid in Alzheimer's disease. Neurobiol. Aging 2000, 21:551-554.
99. Kitamuro T., et al. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J. Biol. Chem. 2003, 278:9125-9133.
100. Kooli A., et al. trans-Arachidonic acids induce a heme oxygenase-dependent vasorelaxation of cerebral microvasculature. Free Radic. Biol. Med. 2008, 44:815-825.
101. Kosaka J., et al. Effects of biliverdin administration on acute lung injury induced by hemorrhagic shock and resuscitation in rats. PLoS One 2013, 8:e63606.
102. Lauderback C.M., et al. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42. J. Neurochem. 2001, 78:413-416.
103. Leffler C.W., et al. Mechanism of glutamate stimulation of CO production in cerebral microvessels. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H74-H80.
104. Leffler C.W., et al. Regulation of CO production in cerebral microvessels of newborn pigs. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H292-H297.
105. Lerner-Marmarosh N., et al. Human biliverdin reductase: a member of the insulin receptor substrate family with serine/threonine/tyrosine kinase activity. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7109-7114.
106. Lerner-Marmarosh N., et al. Regulation of TNF-alpha-activated PKC-zeta signaling by the human biliverdin reductase: identification of activating and inhibitory domains of the reductase. FASEB J. 2007, 21:3949-3962.
107. Lerner-Marmarosh N., et al. Human biliverdin reductase is an ERK activator; hBVR is an ERK nuclear transporter and is required for MAPK signaling. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6870-6875.
108. Liu N., et al. 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 2000, 241:175-183.
109. Liu X.M., et al. Antiapoptotic action of carbon monoxide on cultured vascular smooth muscle cells. Exp. Biol. Med. (Maywood) 2003, 228:572-575.
110. Lovell M.A., et al. Acrolein is increased in Alzheimer's disease brain and is toxic to primary hippocampal cultures. Neurobiol. Aging 2001, 22:187-194.
111. Maes O.C., et al. Characterization of alpha1-antitrypsin as a heme oxygenase-1 suppressor in Alzheimer plasma. Neurobiol. Dis. 2006, 24:89-100.
112. Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 1997, 37:517-554.
113. Maines M.D. The heme oxygenase system and its functions in the brain. Cell. Mol. Biol. (Noisy-le-grand) 2000, 46:573-585.
114. Maines M.D. The heme oxygenase system: update 2005. Antioxid. Redox Signal. 2005, 7:1761-1766.
115. Maines M.D. New insights into biliverdin reductase functions: linking heme metabolism to cell signaling. Physiology (Bethesda) 2005, 20:382-389.
116. Maines M.D. Biliverdin reductase: PKC interaction at the cross-talk of MAPK and PI3K signaling pathways. Antioxid. Redox Signal. 2007, 9:2187-2195.
117. Maines M.D., Panahian N. The heme oxygenase system and cellular defense mechanisms. Do HO-1 and HO-2 have different functions?. Adv. Exp. Med. Biol. 2001, 502:249-272.
118. Maines M.D., Trakshel G.M. Purification and characterization of human biliverdin reductase. Arch. Biochem. Biophys. 1993, 300:320-326.
119. Maines M.D., et al. Human biliverdin IXalpha reductase is a zinc-metalloprotein. Characterization of purified and Escherichia coli expressed enzymes. Eur. J. Biochem. 1996, 235:372-381.
120. Maines M.D., et al. Nuclear localization of biliverdin reductase in the rat kidney: response to nephrotoxins that induce heme oxygenase-1. J. Pharmacol. Exp. Ther. 2001, 296:1091-1097.
121. Maines M.D., et al. Human biliverdin reductase, a previously unknown activator of protein kinase C betaII. J. Biol. Chem. 2007, 282:8110-8122.
122. Mancuso C., Barone E. The heme oxygenase/biliverdin reductase pathway in drug research and development. Curr. Drug Metab. 2009, 10:579-594.
123. Mancuso C., et al. Activation of heme oxygenase and consequent carbon monoxide formation inhibits the release of arginine vasopressin from rat hypothalamic explants. Molecular linkage between heme catabolism and neuroendocrine function. Brain Res. Mol. Brain Res. 1997, 50:267-276.
124. Mancuso C., et al. The generation of nitric oxide and carbon monoxide produces opposite effects on the release of immunoreactive interleukin-1beta from the rat hypothalamus in vitro: evidence for the involvement of different signaling pathways. Endocrinology 1998, 139:1031-1037.
125. Mancuso C., et al. Inhibition of heme oxygenase in the central nervous system potentiates endotoxin-induced vasopressin release in the rat. J. Neuroimmunol. 1999, 99:189-194.
126. Mancuso C., et al. Bilirubin and S-nitrosothiols interaction: evidence for a possible role of bilirubin as a scavenger of nitric oxide. Biochem. Pharmacol. 2003, 66:2355-2363.
127. Mancuso C., et al. Bilirubin as an endogenous modulator of neurotrophin redox signaling. J. Neurosci. Res. 2008, 86:2235-2249.
128. Mancuso C., et al. Roles of nitric oxide, carbon monoxide, and hydrogen sulfide in the regulation of the hypothalamic-pituitary-adrenal axis. J. Neurochem. 2010, 113:563-575.
129. Mancuso C., et al. Inhibition of lipid peroxidation and protein oxidation by endogenous and exogenous antioxidants in rat brain microsomes in vitro. Neurosci. Lett. 2012, 518:101-105.
130. Mancuso C., Siciliano R., Barone E., Preziosi P. Natural substances and Alzheimer's disease: from preclinical studies to evidence based medicine. Biochim. Biophys. Acta 2012, 1822:616-624.
131. Mark R.J., et al. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J. Neurochem. 1997, 68:255-264.
132. Markesbery W.R. Oxidative stress hypothesis in Alzheimer's disease. Free Radic. Biol. Med. 1997, 23:134-147.
133. Markesbery W.R. The role of oxidative stress in Alzheimer disease. Arch. Neurol. 1999, 56:1449-1452.
134. Markesbery W.R. Neuropathologic alterations in mild cognitive impairment: a review. J. Alzheimers Dis. 2010, 19(1):221-228.
135. Markesbery W.R., Lovell M.A. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 1998, 19:33-36.
136. Mateo I., et al. Serum heme oxygenase-1 levels are increased in Parkinson's disease but not in Alzheimer's disease. Acta Neurol. Scand. 2010, 121:136-138.
137. McCoubrey W.K., et al. The structure, organization and differential expression of the rat gene encoding biliverdin reductase. Gene 1995, 160:235-240.
138. McCoubrey W.K., et al. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 1997, 247:725-732.
139. Mecocci P., et al. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 1994, 36:747-751.
140. Minotti G., Aust S.D. The role of iron in oxygen radical mediated lipid peroxidation. Chem. Biol. Interact. 1989, 71:1-19.
141. Miyazaki T., et al. Serum HO-1 is useful to make differential diagnosis of secondary hemophagocytic syndrome from other similar hematological conditions. Int. J. Hematol. 2010, 91:229-237.
142. Morris J.C., Cummings J. Mild cognitive impairment (MCI) represents early-stage Alzheimer's disease. J. Alzheimers Dis. 2005, 7:235-239. (discussion 255-62).
143. Mueller C., et al. The heme degradation pathway is a promising serum biomarker source for the early detection of Alzheimer's disease. J. Alzheimers Dis. 2010, 19:1081-1091.
144. Mulder C., et al. Amyloid-beta(1-42), total tau, and phosphorylated tau as cerebrospinal fluid biomarkers for the diagnosis of Alzheimer disease. Clin. Chem. 2010, 56:248-253.
145. Nuhn P., et al. Heme oxygenase 1-generated carbon monoxide and biliverdin attenuate the course of experimental necrotizing pancreatitis. Pancreas 2013, 42:265-271.
146. Nunomura A., et al. Oxidative damage to RNA in aging and neurodegenerative disorders. Neurotox. Res. 2012, 22:231-248.
147. Ogawa K., et al. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J. 2001, 20:2835-2843.
148. Opii W.O., et al. Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer's disease. Neurobiol. Aging 2008, 29:51-70.
149. Owen J.B., et al. Oxidative modification to LDL receptor-related protein 1 in hippocampus from subjects with Alzheimer disease: implications for Abeta accumulation in AD brain. Free Radic. Biol. Med. 2010, 49:1798-1803.
150. Padurariu M., et al. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer's disease. Neurosci. Lett. 2010, 469:6-10.
151. Palozza P., et al. beta-Carotene and cigarette smoke condensate regulate heme oxygenase-1 and its repressor factor Bach1: relationship with cell growth. Antioxid. Redox Signal. 2006, 8:1069-1080.
152. Pereira P.J., et al. Structure of human biliverdin IXbeta reductase, an early fetal bilirubin IXbeta producing enzyme. Nat. Struct. Biol. 2001, 8:215-220.
153. Perluigi M., Butterfield D.A. Oxidative stress and Down syndrome: A route toward Alzheimer-like dementia. Curr. Gerontol. Geriatr. Res. 2012, 2012:724904.
154. Perluigi M., et al. In vivo protective effects of ferulic acid ethyl ester against amyloid-beta peptide 1-42-induced oxidative stress. J. Neurosci. Res. 2006, 84:418-426.
155. Perluigi M., et al. Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis. Proteomics Clin. Appl. 2009, 3:682-693.
156. Petersen R.C., et al. Alzheimer's Disease Neuroimaging Initiative (ADNI): clinical characterization. Neurology 2010, 74:201-209.
157. Piantadosi C.A. Carbon monoxide, reactive oxygen signaling, and oxidative stress. Free Radic. Biol. Med. 2008, 45:562-569.
158. Pink R.C., et al. Pseudogenes: pseudo-functional or key regulators in health and disease?. RNA 2011, 17:792-798.
159. Poon H.F., et al. Free radicals: key to brain aging and heme oxygenase as a cellular response to oxidative stress. J. Gerontol. A Biol. Sci. Med. Sci. 2004, 59:478-493.
160. Pozzoli G., et al. Carbon monoxide as a novel neuroendocrine modulator: inhibition of stimulated corticotropin-releasing hormone release from acute rat hypothalamic explants. Endocrinology 1994, 135:2314-2317.
161. Pratico D., et al. Increased F2-isoprostanes in Alzheimer's disease: evidence for enhanced lipid peroxidation in vivo. FASEB J. 1998, 12:1777-1783.
162. Pratico D., et al. Increased 8,12-iso-iPF2alpha-VI in Alzheimer's disease: correlation of a noninvasive index of lipid peroxidation with disease severity. Ann. Neurol. 2000, 48:809-812.
163. Premkumar D.R., et al. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem. 1995, 65:1399-1402.
164. Price J.L., Morris J.C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann. Neurol. 1999, 45:358-368.
165. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
166. Ravanelli M.I., et al. Role of the locus coeruleus carbon monoxide pathway in endotoxin fever in rats. Pflugers Arch. 2007, 453:471-476.
167. Reed T.T., et al. Proteomic identification of HNE-bound proteins in early Alzheimer disease: insights into the role of lipid peroxidation in the progression of AD. Brain Res. 2009, 1274:66-76.
168. Rockwood K., et al. Use of lipid-lowering agents, indication bias, and the risk of dementia in community-dwelling elderly people. Arch. Neurol. 2002, 59:223-227.
169. Rodriguez E.G., et al. Use of lipid-lowering drugs in older adults with and without dementia: a community-based epidemiological study. J. Am. Geriatr. Soc. 2002, 50:1852-1856.
170. Rodriguez F., et al. Effects of exogenous heme on renal function: role of heme oxygenase and cyclooxygenase. Hypertension 2003, 42:680-684.
171. Sacktor T.C. How does PKMzeta maintain long-term memory?. Nat. Rev. Neurosci. 2011, 12:9-15.
172. Saint-Aubert L., et al. Cortical florbetapir-PET amyloid load in prodromal Alzheimer's disease patients. EJNMMI Res. 2013, 3:43.
173. Salinas M., et al. Protein kinase Akt/PKB phosphorylates heme oxygenase-1 in vitro and in vivo. FEBS Lett. 2004, 578:90-94.
174. Scapagnini G., et al. Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress. Antioxid. Redox Signal. 2004, 6:811-818.
175. Schipper H.M. Biomarker potential of heme oxygenase-1 in Alzheimer's disease and mild cognitive impairment. Biomark. Med 2007, 1:375-385.
176. Schipper H.M. Heme oxygenase-1 in Alzheimer disease: a tribute to Moussa Youdim. J. Neural Transm. 2011, 118:381-387.
177. Schipper H.M., et al. Evaluation of heme oxygenase-1 as a systemic biological marker of sporadic AD. Neurology 2000, 54:1297-1304.
178. Schipper H.M., et al. Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment. Neurobiol. Aging 2006, 27:252-261.
179. Schipper H.M., et al. Suppression of glial HO-1 activity as a potential neurotherapeutic intervention in AD. Curr. Alzheimer Res. 2009, 6:424-430.
180. Shibahara S., et al. Repression of heme oxygenase-1 expression as a defense strategy in humans. Exp. Biol. Med. (Maywood) 2003, 228:472-473.
181. 18F-FDG PET. J. Nucl. Med. 2013, 54(9):1564-1569.
182. Smith M.A., et al. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am. J. Pathol. 1994, 145:42-47.
183. Smith M.A., et al. Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann. N. Y. Acad. Sci. 1994, 738:447-454.
184. Smith M.A., et al. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9866-9868.
185. Song R., et al. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am. J. Pathol. 2003, 163:231-242.
186. Song W., et al. Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. J. Cell. Physiol. 2006, 206:655-663.
187. Song F., et al. Plasma biomarkers for mild cognitive impairment and Alzheimer's disease. Brain Res. Rev. 2009, 61:69-80.
188. Srikanth V., et al. Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging 2011, 32:763-777.
189. Steiner A.A., Branco L.G. Central CO-heme oxygenase pathway raises body temperature by a prostaglandin-independent way. J. Appl. Physiol. 2000, 88:1607-1613.
190. Steiner A.A., Branco L.G. Carbon monoxide is the heme oxygenase product with a pyretic action: evidence for a cGMP signaling pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R448-R457.
191. Steiner A.A., et al. Carbon monoxide as a novel mediator of the febrile response in the central nervous system. Am. J. Physiol. 1999, 277:R499-R507.
192. Steiner A.A., et al. Role of the brain heme oxygenase-carbon monoxide pathway in stress fever in rats. Neurosci. Lett. 2003, 341:193-196.
193. Stewart D., et al. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 2003, 278:2396-2402.
194. Stocker R. Antioxidant activities of bile pigments. Antioxid. Redox Signal. 2004, 6:841-849.
195. Stocker R., et al. Antioxidant activity of albumin-bound bilirubin. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:5918-5922.
196. Stocker R., et al. Bilirubin is an antioxidant of possible physiological importance. Science 1987, 235:1043-1046.
197. Subramaniam R., et al. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. J. Neurochem. 1997, 69:1161-1169.
198. Sultana R., Butterfield D.A. Role of oxidative stress in the progression of Alzheimer's disease. J. Alzheimers Dis. 2010, 19:341-353.
199. Sultana R., et al. Ferulic acid ethyl ester protects neurons against amyloid beta- peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity. J. Neurochem. 2005, 92:749-758.
200. Sultana R., et al. Protein oxidation and lipid peroxidation in brain of subjects with Alzheimer's disease: insights into mechanism of neurodegeneration from redox proteomics. Antioxid. Redox Signal. 2006, 8:2021-2037.
201. Sultana R., et al. Oxidatively modified proteins in Alzheimer's disease (AD), mild cognitive impairment and animal models of AD: role of Abeta in pathogenesis. Acta Neuropathol. 2009, 118:131-150.
202. Sultana R., et al. Do proteomics analyses provide insights into reduced oxidative stress in the brain of an Alzheimer disease transgenic mouse model with an M631L amyloid precursor protein substitution and thereby the importance of amyloid-beta-resident methionine 35 in Alzheimer disease pathogenesis?. Antioxid. Redox Signal. 2012, 17:1507-1514.
203. Sun J., et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 2002, 21:5216-5224.
204. Sun J., et al. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1461-1466.
205. Suzuki A., et al. Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J. Neurosci. 2011, 31:8786-8802.
206. Takahashi M., et al. Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease. Neuron 2000, 28:461-473.
207. Takeda A., et al. Heme catabolism and heme oxygenase in neurodegenerative disease. Antioxid. Redox Signal. 2004, 6:888-894.
208. Torp R., Head E., Cotman C.W. Ultrastructural analyses of beta-amyloid in the aged dog brain: neuronal beta-amyloid is localized to the plasma membrane. Prog. Neuropsychopharmacol. Biol. Psychiatry 2000, 24:801-810.
209. Torp R., Head E., Milgram N.W., Hahn F., Ottersen O.P., Cotman C.W. Ultrastructural evidence of fibrillar β-amyloid associated with neuronal membranes in behaviorally characterized aged dog brains. Neuroscience 2000, 93:495-506.
210. Torp R., et al. Identification of neuronal plasma membrane microdomains that colocalize beta-amyloid and presenilin: implications for beta-amyloid precursor protein processing. Neuroscience 2003, 120:291-300.
211. Tudor C., et al. Biliverdin reductase is a transporter of haem into the nucleus and is essential for regulation of HO-1 gene expression by haematin. Biochem. J. 2008, 413:405-416.
212. Vaya J., et al. Effects of heme oxygenase-1 expression on sterol homeostasis in rat astroglia. Free Radic. Biol. Med. 2007, 42:864-871.
213. Vitek L. The role of bilirubin in diabetes, metabolic syndrome, and cardiovascular diseases. Front. Pharmacol. 2012, 3:55.
214. Walsh D.M., et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
215. Wolozin B., et al. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 2000, 57:1439-1443.
216. Wolozin B., et al. Simvastatin is associated with a reduced incidence of dementia and Parkinson's disease. BMC Med. 2007, 5:20.
217. Wu L., Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol. Rev. 2005, 57:585-630.
218. Yamashita K., et al. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J. 2004, 18:765-767.
219. Zafrilla P., et al. Oxidative stress in Alzheimer patients in different stages of the disease. Curr. Med. Chem. 2006, 13:1075-1083.
220. Zamrini E., et al. Association between statin use and Alzheimer's disease. Neuroepidemiology 2004, 23:94-98.
221. Zenke-Kawasaki Y., et al. Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol. Cell. Biol. 2007, 27:6962-6971.
222. Zhang F., et al. Carbon monoxide produced by isolated arterioles attenuates pressure-induced vasoconstriction. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H350-H358.
223. Zhang F., et al. CO modulates pulmonary vascular response to acute hypoxia: relation to endothelin. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H137-H144.