The sinister face of heme oxygenase-1 in brain aging and disease

Progress in Neurobiology - Tập 172 - Trang 40-70 - 2019
Hyman M. Schipper1,2,3, Wei Song1, Ayda Tavitian1,2, Marisa Cressatti1,2
1Lady Davis Institute for Medical Research, Jewish General Hospital, Montreal, Quebec, Canada
2Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada
3Department of Medicine, McGill University, Montreal, Quebec, Canada

Tài liệu tham khảo

Ahmad, 2006, Heme oxygenase-1 protects brain from acute excitotoxicity, Neuroscience, 141, 1703, 10.1016/j.neuroscience.2006.05.035 Alaoui-Jamali, 2009, A novel experimental heme oxygenase-1-targeted therapy for hormone-refractory prostate cancer, Cancer Res., 69, 8017, 10.1158/0008-5472.CAN-09-0419 Ali, 1993, Age-related susceptibility to MPTP-induced neurotoxicity in mice, Neurotoxicology, 14, 29 Anthony, 2003, Stress protein expression in the Alzheimer-diseased choroid plexus, J. Alzheimers Dis., 5, 171, 10.3233/JAD-2003-5301 Arkadir, 2014, Redundant dopaminergic activity may enable compensatory axonal sprouting in Parkinson disease, Neurology, 82, 1093, 10.1212/WNL.0000000000000243 Aschner, 2000, Neuron-astrocyte interactions: implications for cellular energetics and antioxidant levels, Neurotoxicology, 21, 1101 Auge, 2017, New perspectives on corpora amylacea in the human brain, Sci. Rep., 7, 41807, 10.1038/srep41807 Ayuso, 2014, An association study between Heme oxygenase-1 genetic variants and Parkinson’s disease, Front. Cell. Neurosci., 8, 298, 10.3389/fncel.2014.00298 Bach, 2010, Elevated bilirubin in acute and transient psychotic disorder, Pharmacopsychiatry, 43, 12, 10.1055/s-0029-1237376 Bakhshi, 2015, The neuropathology of schizophrenia: a selective review of past studies and emerging themes in brain structure and cytoarchitecture, Neuroscience, 303, 82, 10.1016/j.neuroscience.2015.06.028 Bansal, 2014, Mitochondria-targeted heme oxygenase-1 induces oxidative stress and mitochondrial dysfunction in macrophages, kidney fibroblasts and in chronic alcohol hepatotoxicity, Redox Biol., 2, 273, 10.1016/j.redox.2013.07.004 Baranano, 2001, Neural roles for heme oxygenase: contrasts to nitric oxide synthase, Proc. Natl. Acad. Sci U. S. A., 98, 10996, 10.1073/pnas.191351298 Barone, 2012, Heme oxygenase-1 posttranslational modifications in the brain of subjects with Alzheimer disease and mild cognitive impairment, Free Radic. Biol. Med., 52, 2292, 10.1016/j.freeradbiomed.2012.03.020 Beal, 1995 Beal, 1996, Mitochondria, free radicals, and neurodegeneration, Curr. Opin. Neurobiol., 6, 661, 10.1016/S0959-4388(96)80100-0 Bergeron, 1998, Developmental expression of heme oxygenase-1 (HSP32) in rat brain: an immunocytochemical study, Brain Res. Dev. Brain Res., 105, 181, 10.1016/S0165-3806(97)00169-7 Bernardi, 1996, The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death, Biochim. Biophys. Acta, 1275, 5, 10.1016/0005-2728(96)00041-2 Bertram, 2007, Systematic meta-analyses of Alzheimer disease genetic association studies: the AlzGene database, Nat. Genet., 39, 17, 10.1038/ng1934 Beschorner, 2000, Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans, Acta Neuropathol. (Berl.), 100, 377, 10.1007/s004010000202 Bilbul, 2011, Risk profiles of Alzheimer disease, Can. J. Neurol. Sci., 38, 580, 10.1017/S0317167100012129 Biswas, 2014, Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses, J. Biol. Chem., 289, 26882, 10.1074/jbc.M114.567685 Bjorkhem, 2009, Oxysterols and neurodegenerative diseases, Mol. Asp. Med., 30, 171, 10.1016/j.mam.2009.02.001 Boddaert, 2007, Selective iron chelation in Friedreich ataxia: biologic and clinical implications, Blood, 110, 401, 10.1182/blood-2006-12-065433 Bolisetty, 2010, Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury, J. Am. Soc. Nephrol., 21, 1702, 10.1681/ASN.2010030238 Bonilla, 1999, Mitochondrial involvement in Alzheimer’s disease, Biochim. Biophys. Acta, 1410, 171, 10.1016/S0005-2728(98)00165-0 Borten, 2004, Effects of dietary restriction and metal supplementation on the accumulation of iron-laden glial inclusions in the aging rat hippocampus, Biogerontology, 83, 81, 10.1023/B:BGEN.0000025071.78517.3a Botella-Lopez, 2006, Reelin expression and glycosylation patterns are altered in Alzheimer’s disease, Proc. Natl. Acad. Sci. U. S. A., 103, 5573, 10.1073/pnas.0601279103 Bowen, 1995, Proton MR spectroscopy of the brain in 14 patients with Parkinson disease, AJNR Am. J. Neuroradiol., 16, 61 Bracha, 1987, Asymmetric rotational (circling) behavior, a dopamine-related asymmetry: preliminary findings in unmedicated and never-medicated schizophrenic patients, Biol. Psychiatry, 22, 995, 10.1016/0006-3223(87)90009-6 Bracha, 1987, Spontaneous asymmetric circling behavior in hemi-Parkinsonism; a human equivalent of the lesioned-circling rodent behavior, Life Sci., 40, 1127, 10.1016/0024-3205(87)90576-5 Brawer, 1975, Cytopathological effects of estradiol on the arcuate nucleus of the female rat. A possible mechanism for pituitary tumorigenesis, Am. J. Anat., 144, 57, 10.1002/aja.1001440105 Brawer, 1978, Effects of a single injection of estradiol valerate on the hypothalamic arcuate nucleus and on reproductive function in the female rat, Endocrinology, 103, 501, 10.1210/endo-103-2-501 Brawer, 1983, Effects of long term androgen and estradiol exposure on the hypothalamus, Endocrinology, 112, 194, 10.1210/endo-112-1-194 Brawer, 1993, Pathologic effect of estradiol on the hypothalamus, Biol. Reprod., 49, 647, 10.1095/biolreprod49.4.647 Brawer, 1994, The origin and composition of peroxidase-positive granules in cysteamine-treated astrocytes in culture, Brain Res., 633, 9, 10.1016/0006-8993(94)91516-4 Brawer, 1994, Composition of Gomori-positive inclusions in astrocytes of the hypothalamic arcuate nucleus, Anat. Rec., 240, 407, 10.1002/ar.1092400313 Brawer, 1995, Uptake and subcellular distribution of 51Cr in Gomori-positive astrocytes in primary culture, Neurotoxicology, 16, 327 Brewer, 2003, Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia, Am. J. Psychiatry, 160, 1790, 10.1176/appi.ajp.160.10.1790 Brown, 2011, Exposure to prenatal infection and risk of schizophrenia, Front. Psychiatry, 2, 63, 10.3389/fpsyt.2011.00063 Brunetti, 2004, Aging increases amyloid beta-peptide-induced 8-iso-prostaglandin F(2alpha) release from rat brain, Neurobiol. Aging, 25, 125, 10.1016/S0197-4580(03)00038-1 Businaro, 2002, Myelin basic protein induces heme oxygenase-1 in human astroglial cells, Glia, 37, 83, 10.1002/glia.10018 Butcher, 2013, Association between early-onset Parkinson disease and 22q11.2 deletion syndrome: identification of a novel genetic form of Parkinson disease and its clinical implications, JAMA Neurol., 70, 1359, 10.1001/jamaneurol.2013.3646 Butterfield, 2018, Oxidative stress, amyloid-beta peptide, and altered key molecular pathways in the pathogenesis and progression of Alzheimer’s disease, J. Alzheimers Dis., 62, 1345, 10.3233/JAD-170543 Butterfield, 2002, Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer’s disease brain contribute to neuronal death, Neurobiol. Aging, 23, 655, 10.1016/S0197-4580(01)00340-2 Calabrese, 2006, Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer’s disease, Antioxid. Redox Signal., 8, 1975, 10.1089/ars.2006.8.1975 Calabrese, 2017, Hormesis, cellular stress response and neuroinflammation in schizophrenia: early onset versus late onset state, J. Neurosci. Res., 95, 1182, 10.1002/jnr.23967 Caligiuri, 1993, Parkinsonism in neuroleptic-naive schizophrenic patients, Am. J. Psychiatry, 150, 1343, 10.1176/ajp.150.9.1343 Canning, 2015, Structural basis of Keap1 interactions with Nrf2, Free Radic. Biol. Med., 88, 101, 10.1016/j.freeradbiomed.2015.05.034 Cantuti-Castelvetri, 2003, Dopamine neurotoxicity: age-dependent behavioral and histological effects, Neurobiol. Aging, 24, 697, 10.1016/S0197-4580(02)00186-0 Carboni, 2017, Deferiprone rescues behavioral deficits induced by mild Iron exposure in a mouse model of alpha-synuclein aggregation, Neuromol. Med., 19, 309, 10.1007/s12017-017-8447-9 Carchman, 2011, Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice, Hepatology, 53, 2053, 10.1002/hep.24324 Castellani, 1995, Evidence for oxidative stress in pick disease and corticobasal degeneration, Brain Res., 696, 268, 10.1016/0006-8993(95)00535-X Castellani, 1996, Glycoxidation and oxidative stress in Parkinson disease and diffuse Lewy body disease, Brain Res., 737, 195, 10.1016/0006-8993(96)00729-9 Cavanagh, 1999, Corpora-amylacea and the family of polyglucosan diseases, Brain Res. Brain Res. Rev., 29, 265, 10.1016/S0165-0173(99)00003-X Chakrabarty, 2003, Heme oxygenase-1 in SJL mice with experimental allergic encephalomyelitis, Mult. Scler., 9, 372, 10.1191/1352458503ms928oa Chang, 1998, Neurotoxicity of cholesterol oxides on cultured cerebellar granule cells, Neurochem. Int., 32, 317, 10.1016/S0197-0186(97)00103-4 Chang, 1995, Neuronal ultrastructural abnormalities in a patient with frontotemporal dementia and motor neuron disease, Dementia, 6, 1 Chen, 2000, Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death, J. Neurochem., 75, 304, 10.1046/j.1471-4159.2000.0750304.x Chen, 2013, Regulation of SIRT1 by oxidative stress-responsive miRNAs and a systematic approach to identify its role in the endothelium, Antioxid. Redox Signal., 19, 1522, 10.1089/ars.2012.4803 Chen-Roetling, 2005, Cultured astrocytes from heme oxygenase-1 knockout mice are more vulnerable to heme-mediated oxidative injury, J. Neurosci. Res., 82, 802, 10.1002/jnr.20681 Chen-Roetling, 2015, Astrocyte overexpression of heme oxygenase-1 improves outcome after intracerebral hemorrhage, Stroke, 46, 1093, 10.1161/STROKEAHA.115.008686 Chen-Roetling, 2017, Astrocyte heme oxygenase-1 reduces mortality and improves outcome after collagenase-induced intracerebral hemorrhage, Neurobiol. Dis., 102, 140, 10.1016/j.nbd.2017.03.008 Chopra, 1995, Differential effects of cysteamine on heat shock protein induction and cytoplasmic granulation in astrocytes and glioma cells, Brain Res. Mol. Brain Res., 31, 173, 10.1016/0169-328X(95)00049-X Chopra, 1997, A cellular stress model for the differential expression of glial lysosomal cathepsins in the aging nervous system, Exp. Neurol., 147, 221, 10.1006/exnr.1997.6616 Ciechanover, 2003, The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg, Neuron, 40, 427, 10.1016/S0896-6273(03)00606-8 Cisse, 1995, Experimental induction of corpora amylacea-like inclusions in rat astroglia, Neuropathol. Appl. Neurobiol., 21, 423, 10.1111/j.1365-2990.1995.tb01079.x Connor, 1997 Converso, 2006, HO-1 is located in liver mitochondria and modulates mitochondrial heme content and metabolism, FASEB J., 20, 1236, 10.1096/fj.05-4204fje Coppede, 2010, DNA repair in premature aging disorders and neurodegeneration, Curr. Aging Sci., 3, 3, 10.2174/1874609811003010003 Corral-Debrinski, 1994, Marked changes in mitochondrial DNA deletion levels in Alzheimer brains, Genomics, 23, 471, 10.1006/geno.1994.1525 Dalman, 1999, Neonatal hyperbilirubinaemia—a vulnerability factor for mental disorder?, Acta Psychiatr. Scand., 100, 469, 10.1111/j.1600-0447.1999.tb10899.x Davis, 1997, Selective impairments of mitochondrial respiratory chain activity during aging and ischemic brain damage, Acta Neurochir. Suppl. (Wien), 70, 56 Deininger, 2000, Heme oxygenase (HO)-1 expressing macrophages/microglial cells accumulate during oligodendroglioma progression, Brain Res., 882, 1, 10.1016/S0006-8993(00)02594-4 Del Tredici, 2010, Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson’s disease, Acta Neuropathol., 119, 703, 10.1007/s00401-010-0665-2 Delisle, 2000, [Neurodegenerative disease associated with a mutation of codon 279 (N279K) in exon 10 of Tau protein], Bull. Acad. Natl. Med., 184, 799 Dennery, 2000, Regulation and role of heme oxygenase in oxidative injury, Curr. Top. Cell. Regul., 36, 181, 10.1016/S0070-2137(01)80008-X Desjardins, 1992, Vitamin E protects hypothalamic beta-endorphin neurons from estradiol neurotoxicity, Endocrinology, 131, 2482, 10.1210/endo.131.5.1425446 Desmard, 2007, Mitochondrial and cellular heme-dependent proteins as targets for the bioactive function of the heme oxygenase/carbon monoxide system, Antioxid. Redox Signal., 9, 2139, 10.1089/ars.2007.1803 Desole, 1995, Cellular defence mechanisms in the striatum of young and aged rats subchronically exposed to manganese, Neuropharmacology, 34, 289, 10.1016/0028-3908(94)00140-N Devic, 2011, Salivary alpha-synuclein and DJ-1: potential biomarkers for Parkinson’s disease, Brain, 134, e178, 10.1093/brain/awr015 Dexter, 2013, Parkinson disease: from pathology to molecular disease mechanisms, Free Radic. Biol. Med., 62, 132, 10.1016/j.freeradbiomed.2013.01.018 Di Domenico, 2012, 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., 32, 277, 10.3233/JAD-2012-121045 Di Domenico, 2015, Bach1 overexpression in Down syndrome correlates with the alteration of the HO-1/BVR-a system: insights for transition to Alzheimer’s disease, J. Alzheimers Dis., 44, 1107, 10.3233/JAD-141254 Di Monte, 1995, Iron-mediated bioactivation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in glial cultures, Glia, 15, 203, 10.1002/glia.440150213 Dik, 2005, Serum inflammatory proteins and cognitive decline in older persons, Neurology, 64, 1371, 10.1212/01.WNL.0000158281.08946.68 Dore, 1999, Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury, Proc. Natl. Acad. Sci. U. S. A., 96, 2445, 10.1073/pnas.96.5.2445 Droge, 2002, Free radicals in the physiological control of cell function, Physiol. Rev., 82, 47, 10.1152/physrev.00018.2001 Du, 2014, miR-17 extends mouse lifespan by inhibiting senescence signaling mediated by MKP7, Cell Death Dis., 5, e1355, 10.1038/cddis.2014.305 Durante, 2003, Heme oxygenase-1 in growth control and its clinical application to vascular disease, J. Cell. Physiol., 195, 373, 10.1002/jcp.10274 Dwyer, 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, 10.1016/0169-328X(94)00273-H Dwyer, 1995, Differential localization of heme oxygenase and NADPH-diaphorase in spinal cord neurons, Neuroreport, 6, 973, 10.1097/00001756-199505090-00006 Emir, 2012, Elevated pontine and putamenal GABA levels in mild-moderate Parkinson disease detected by 7 tesla proton MRS, PLoS One, 7, e30918, 10.1371/journal.pone.0030918 Exner, 2004, The role of heme oxygenase-1 promoter polymorphisms in human disease, Free Radic. Biol. Med., 37, 1097, 10.1016/j.freeradbiomed.2004.07.008 Fan, 2011, The heme oxygenase system and oral diseases, Oral Dis., 17, 252, 10.1111/j.1601-0825.2010.01732.x Fatima, 2014, The miRNAome of the postpartum dairy cow liver in negative energy balance, BMC Genom., 15, 279, 10.1186/1471-2164-15-279 Ffytche, 2017, The psychosis spectrum in Parkinson disease, Nat. Rev. Neurol., 13, 81, 10.1038/nrneurol.2016.200 Fink S. Las Vegas Gunman’s Brain Exam Only Deepens Mystery of His Actions. New York Times. New York, https://www.nytimes.com/2018/02/09/us/las-vegas-attack-paddock-brain-autopsy.html, 2018. Frankel, 1999, Cysteamine pretreatment of the astroglial substratum (mitochondrial iron sequestration) enhances PC12 cell vulnerability to oxidative injury, Exp. Neurol., 160, 376, 10.1006/exnr.1999.7214 Frankel, 2000, Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively-challenged astroglia, J. Cell. Physiol., 185, 80, 10.1002/1097-4652(200010)185:1<80::AID-JCP7>3.0.CO;2-W Fukuda, 1996, Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury, Brain Res., 736, 68, 10.1016/0006-8993(96)00680-4 Fukuyama, 1994, Altered cerebral energy metabolism in Alzheimer’s disease: a PET study, J. Nucl. Med., 35, 1 Funke, 2009, Genetic analysis of heme oxygenase-1 (HO-1) in German Parkinson’s disease patients, J. Neural Transm., 116, 853, 10.1007/s00702-009-0237-6 Gabriel, 1998, Association of elevated alpha 1-antichymotrypsin with cognitive impairment in a prospective study of the very old, Am. J. Psychiatry, 155, 698, 10.1176/ajp.155.5.698 Galbraith, 1999, Heme oxygenase: who needs it?, Proc. Soc. Exp. Biol. Med., 222, 299, 10.1046/j.1525-1373.1999.d01-147.x Gan, 2014, Oxidative stress-mediated activation of extracellular signal-regulated kinase contributes to mild cognitive impairment-related mitochondrial dysfunction, Free Radic. Biol. Med., 75, 230, 10.1016/j.freeradbiomed.2014.07.021 Garringer, 2016, Effect of systemic Iron overload and a chelation therapy in a mouse model of the neurodegenerative disease hereditary ferritinopathy, PLoS One, 11, e0161341, 10.1371/journal.pone.0161341 Gennuso, 2004, Bilirubin protects astrocytes from its own toxicity by inducing up-regulation and translocation of multidrug resistance-associated protein 1 (Mrp1), Proc. Natl. Acad. Sci. U. S. A., 101, 2470, 10.1073/pnas.0308452100 Gertz, 1985, Glycogen accumulation of the aging human brain, Mech. Ageing Dev., 31, 25, 10.1016/0047-6374(85)90024-7 Gibson, 1998, Abnormalities of mitochondrial enzymes in Alzheimer disease, J. Neural Transm., 105, 855, 10.1007/s007020050099 Gill, 2018, Heme oxygenase-1 promoter region (GT)n polymorphism associates with increased neuroimmune activation and risk for encephalitis in HIV infection, J. Neuroinflamm., 15, 70, 10.1186/s12974-018-1102-z Gollin, 1992, Alpha 1-antitrypsin and alpha 1-antichymotrypsin are in the lesions of Alzheimer’s disease, Neuroreport, 3, 201, 10.1097/00001756-199202000-00020 Graziadei, 1997, Unidirectional upregulation of the synthesis of the major iron proteins, transferrin-receptor and ferritin, in HepG2 cells by the acute-phase protein alpha1-antitrypsin, J. Hepatol., 27, 716, 10.1016/S0168-8278(97)80089-X Graziadei, 1998, Modulation of iron metabolism in monocytic THP-1 cells and cultured human monocytes by the acute-phase protein alpha1-antitrypsin, Exp. Hematol., 26, 1053 Griffiths, 2009, Analysis of neurosterols by GC-MS and LC-MS/MS, J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 877, 2778, 10.1016/j.jchromb.2009.05.017 1998, Consensus report of the Working Group on: “Molecular and Biochemical Markers of Alzheimer’s Disease”. The Ronald and Nancy Reagan Research Institute of the Alzheimer’s Association and the National Institute on Aging Working Group, Neurobiol. Aging, 19, 109, 10.1016/S0197-4580(98)00022-0 Gupta, 2014, Neurotherapeutic effects of novel HO-1 inhibitors in vitro and in a transgenic mouse model of Alzheimer’s disease, J. Neurochem., 131, 778, 10.1111/jnc.12927 Gwiazda, 2002, Low cumulative manganese exposure affects striatal GABA but not dopamine, Neurotoxicology, 23, 69, 10.1016/S0161-813X(02)00002-5 Hadziahmetovic, 2011, The oral iron chelator deferiprone protects against iron overload-induced retinal degeneration, Invest. Ophthalmol. Vis. Sci., 52, 959, 10.1167/iovs.10-6207 Ham, 2000, Heme oxygenase-1 induction and mitochondrial iron sequestration in astroglia exposed to amyloid peptides, Cell. Mol. Biol., 46, 587 Hamdi, 2016, Erythroid cell mitochondria receive endosomal iron by a "kiss-and-run" mechanism, Biochim. Biophys. Acta, 1863, 2859, 10.1016/j.bbamcr.2016.09.008 Hara, 1996, Expression of heme oxygenase and inducible nitric oxide synthase mRNA in human brain tumors, Biochem. Biophys. Res. Commun., 224, 153, 10.1006/bbrc.1996.0999 Hascalovici, 2009, Impact of heme oxygenase-1 on cholesterol synthesis, cholesterol efflux and oxysterol formation in cultured astroglia, J. Neurochem., 108, 72, 10.1111/j.1471-4159.2008.05741.x Hascalovici, 2009, Brain sterol dysregulation in sporadic AD and MCI: relationship to heme oxygenase-1, J. Neurochem., 110, 1241, 10.1111/j.1471-4159.2009.06213.x Hascalovici, 2014, Neural HO-1/sterol interactions in vivo: implications for Alzheimer’s disease, Neuroscience, 10.1016/j.neuroscience.2014.09.001 Hattori, 1991, Immunohistochemical studies on complexes I, II, III, and IV of mitochondria in Parkinson’s disease, Ann. Neurol., 30, 563, 10.1002/ana.410300409 Haydon, 2006, Astrocyte control of synaptic transmission and neurovascular coupling, Physiol. Rev., 86, 1009, 10.1152/physrev.00049.2005 He, 2013, miR-138 protects cardiomyocytes from hypoxia-induced apoptosis via MLK3/JNK/c-jun pathway, Biochem. Biophys. Res. Commun., 441, 763, 10.1016/j.bbrc.2013.10.151 Heidker, 2016, Intersections of pathways involving biotin and iron relative to therapeutic mechanisms for progressive multiple sclerosis, Discov. Med., 22, 381 Hirai, 2001, Mitochondrial abnormalities in Alzheimer’s disease, J. Neurosci., 21, 3017, 10.1523/JNEUROSCI.21-09-03017.2001 Hirose, 2003, Age-associated increases in heme oxygenase-1 and ferritin immunoreactivity in the autopsied brain, Leg. Med. Tokyo, 5, S360, 10.1016/S1344-6223(02)00133-5 Hollister, 1994, Impaired autonomic nervous system-habituation in those at genetic risk for schizophrenia, Arch. Gen. Psychiatry, 51, 552, 10.1001/archpsyc.1994.03950070044009 Horvath, 2011, Knockdown of GAD67 protein levels normalizes neuronal activity in a rat model of Parkinson’s disease, J. Gene Med., 13, 188, 10.1002/jgm.1555 Howell, 2013, Global microRNA expression profiling: curcumin (diferuloylmethane) alters oxidative stress-responsive microRNAs in human ARPE-19 cells, Mol. Vis., 19, 544 Hsu, 2015, Signal peptide peptidase-mediated nuclear localization of heme oxygenase-1 promotes cancer cell proliferation and invasion independent of its enzymatic activity, Oncogene, 34, 2360, 10.1038/onc.2014.166 Huang, 2005, Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment, J. Neurosci. Res., 80, 268, 10.1002/jnr.20444 Hui, 2011, Long-term overexpression of heme oxygenase 1 promotes tau aggregation in mouse brain by inducing tau phosphorylation, J. Alzheimers Dis., 26, 299, 10.3233/JAD-2011-102061 Huisman, 2004, A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson’s disease, Mov. Disord., 19, 687, 10.1002/mds.10713 Hung, 2008, Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4-phenylpyridinium-induced neurotoxicity, Mol. Pharmacol., 74, 1564, 10.1124/mol.108.048611 Hutchison, 2013, Evidence for miR-181 involvement in neuroinflammatory responses of astrocytes, Glia, 61, 1018, 10.1002/glia.22483 Jagust, 2013, Vulnerable neural systems and the borderland of brain aging and neurodegeneration, Neuron, 77, 219, 10.1016/j.neuron.2013.01.002 Jarvis, 1990, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity in the rat: characterization and age-dependent effects, Synapse, 5, 104, 10.1002/syn.890050204 Jefferies, 1996, Reactive microglia specifically associated with amyloid plaques in Alzheimer’s disease brain tissue express melanotransferrin, Brain Res., 712, 122, 10.1016/0006-8993(95)01407-1 Jenner, 2003, Oxidative stress in Parkinson’s disease, Ann. Neurol., 53, S26, 10.1002/ana.10483 Jozkowicz, 2007, Heme oxygenase-1 in tumors: is it a false friend?, Antioxid. Redox Signal., 9, 2099, 10.1089/ars.2007.1659 Kadoya, 1995, Preischemic but not postischemic zinc protoporphyrin treatment reduces infarct size and edema accumulation after temporary focal cerebral ischemia in rats, Stroke, 26, 1035, 10.1161/01.STR.26.6.1035 Kamis, 2015, Sex and laterality differences in Parkinsonian impairment and transcranial ultrasound in never-treated schizophrenics and their first degree relatives in an Andean population, Schizophr. Res., 164, 250, 10.1016/j.schres.2015.01.035 Kessler, 2018, Two-year observational study of deferiprone in superficial siderosis, CNS Neurosci. Ther., 24, 187, 10.1111/cns.12792 Kim, 2004, Caveolae compartmentalization of heme oxygenase-1 in endothelial cells, FASEB J., 18, 1080, 10.1096/fj.03-1391com Kimpara, 1997, Microsatellite polymorphism in the human heme oxygenase-1 gene promoter and its application in association studies with Alzheimer and Parkinson disease, Hum. Genet., 100, 145, 10.1007/s004390050480 Kinobe, 2006, Selectivity of imidazole-dioxolane compounds for in vitro inhibition of microsomal haem oxygenase isoforms, Br. J. Pharmacol., 147, 307, 10.1038/sj.bjp.0706555 Kirkwood, 1991, The biology of aging, Science (80), 252, 1864, 10.1126/science.252.5014.1864 Kirkwood, 1991, Evolution of senescence: late survival sacrificed for reproduction, Philos. Trans. R. Soc. Lond., B, Biol. Sci., 332, 15, 10.1098/rstb.1991.0028 Kish, 1986, Elevated gamma-aminobutyric acid level in striatal but not extrastriatal brain regions in Parkinson’s disease: correlation with striatal dopamine loss, Ann. Neurol., 20, 26, 10.1002/ana.410200106 Kitamuro, 2003, Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells, J. Biol. Chem., 278, 9125, 10.1074/jbc.M209939200 Klionsky, 2016, Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition), Autophagy, 12, 1, 10.1080/15548627.2015.1100356 Koeppen, 1999, Neuroprotection in intracerebral hemorrhage with tin-protoporphyrin, Ann. Neurol., 46, 938 Koizumi, 2007, Human heme oxygenase-1 deficiency: a lesson on serendipity in the discovery of the novel disease, Pediatr. Int., 49, 125, 10.1111/j.1442-200X.2007.02353.x Kole, 2011, miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis, Genes Dev., 25, 125, 10.1101/gad.1975411 Kolomeets, 2010, Ultrastructural abnormalities of astrocytes in the hippocampus in schizophrenia and duration of illness: a postortem morphometric study, World J. Biol. Psychiatry, 11, 282, 10.3109/15622970902806124 Kontos, 1985, Appearance of superoxide anion radical in cerebral extracellular space during increased prostaglandin synthesis in cats, Circ. Res., 57, 142, 10.1161/01.RES.57.1.142 Kren, 2009, MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis, RNA Biol., 6, 65, 10.4161/rna.6.1.7534 Krobert, 1997, Astrocytes promote or impair the survival and function of embryonic ventral mesencephalon co-grafts: effects of astrocyte age and expression of recombinant brain-derived neurotrophic factor, Exp. Neurol., 145, 511, 10.1006/exnr.1997.6483 Kruger, 1998, Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease, Nat. Genet., 18, 106, 10.1038/ng0298-106 Kumar, 2007, Effects of serotonin on perifornical-lateral hypothalamic area neurons in rat, Eur. J. Neurosci., 25, 201, 10.1111/j.1460-9568.2006.05268.x Lang, 2011, A critical appraisal of the premotor symptoms of Parkinson’s disease: potential usefulness in early diagnosis and design of neuroprotective trials, Mov. Disord., 26, 775, 10.1002/mds.23609 Lassmann, 2016, Oxidative stress and its impact on neurons and glia in multiple sclerosis lesions, Biochim. Biophys. Acta, 1862, 506, 10.1016/j.bbadis.2015.09.018 Lavrovsky, 1996, Downregulation of the human heme oxygenase gene by glucocorticoids and identification of 56b regulatory elements, Biochem. Biophys. Res. Commun., 218, 759, 10.1006/bbrc.1996.0135 Le, 1999, Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury, J. Neurosci. Res., 56, 652, 10.1002/(SICI)1097-4547(19990615)56:6<652::AID-JNR11>3.0.CO;2-5 Lee, 2001, Accumulation of peroxidase-positive granules with ageing in SAMP and 10 SAMR1 mouse brains, Korean J. Anat., 34, 645 Lee, 2006, Heme-oxygenase-1 promotes polychlorinated biphenyl mixture aroclor 1254-induced oxidative stress and dopaminergic cell injury, Toxicol. Sci., 90, 159, 10.1093/toxsci/kfj052 Leoni, 2011, Oxysterols as biomarkers in neurodegenerative diseases, Chem. Phys. Lipids, 164, 515, 10.1016/j.chemphyslip.2011.04.002 LeVine, 2004, The role of iron in the pathogenesis of experimental allergic encephalomyelitis and multiple sclerosis, Ann. N. Y. Acad. Sci., 1012, 252, 10.1196/annals.1306.021 Li, 2007, Carbon monoxide produced by heme oxygenase-1 in response to nitrosative stress induces expression of glutamate-cysteine ligase in PC12 cells via activation of phosphatidylinositol 3-kinase and Nrf2 signaling, J. Biol. Chem., 282, 28577, 10.1074/jbc.M701916200 Li, 2012, Control of mitochondrial activity by miRNAs, J. Cell. Biochem., 113, 1104, 10.1002/jcb.24004 Li, 2013, MicroRNA-138 plays a role in hypoxic pulmonary vascular remodelling by targeting Mst1, Biochem. J., 452, 281, 10.1042/BJ20120680 Li Volti, 2004, Immunocytochemical localization and expression of heme oxygenase-1 in primary astroglial cell cultures during differentiation: effect of glutamate, Biochem. Biophys. Res. Commun., 315, 517, 10.1016/j.bbrc.2004.01.090 Licastro, 2000, Increased plasma levels of interleukin-1, interleukin-6 and alpha-1-antichymotrypsin in patients with Alzheimer’s disease: peripheral inflammation or signals from the brain?, J. Neuroimmunol., 103, 97, 10.1016/S0165-5728(99)00226-X Licht-Mayer, 2015, Cell type-specific Nrf2 expression in multiple sclerosis lesions, Acta Neuropathol., 130, 263, 10.1007/s00401-015-1452-x Lin, 2007, Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress, J. Biol. Chem., 282, 20621, 10.1074/jbc.M607954200 Lin, 2007, 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., 27, 1010, 10.1038/sj.jcbfm.9600412 Lin, 2008, Catalytic inactive heme oxygenase-1 protein regulates its own expression in oxidative stress, Free Radic. Biol. Med., 44, 847, 10.1016/j.freeradbiomed.2007.11.012 Lin, 2014, Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy, Int. J. Mol. Sci., 15, 1625, 10.3390/ijms15011625 Lin, 2015, Heme oxygenase-1 modulates microRNA expression in cultured astroglia: implications for chronic brain disorders, Glia, 63, 1270, 10.1002/glia.22823 Liu, 1996, Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats, FASEB J., 10, 1532, 10.1096/fasebj.10.13.8940299 Llesuy, 1994, Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage, Biochim. Biophys. Acta, 1223, 9, 10.1016/0167-4889(94)90067-1 Loboda, 2008, Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities, Antioxid. Redox Signal., 10, 1767, 10.1089/ars.2008.2043 Loboda, 2016, Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism, Cell. Mol. Life Sci., 73, 3221, 10.1007/s00018-016-2223-0 Lu, 2000, Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis, J. Neurol. Sci., 177, 95, 10.1016/S0022-510X(00)00343-9 Ma, 2013, The balance mediated by miRNAs and the heme oxygenase 1 feedback loop contributes to biological effects, J. Cell. Biochem., 114, 2637, 10.1002/jcb.24631 Maes, 2006, Characterization of alpha1-antitrypsin as a heme oxygenase-1 suppressor in Alzheimer plasma, Neurobiol. Dis., 24, 89, 10.1016/j.nbd.2006.06.009 Maines, 1998, Neuronal overexpression of heme oxygenase-1 correlates with an attenuated exploratory behavior and causes an increase in neuronal NADPH diaphorase staining, J. Neurochem., 70, 2057, 10.1046/j.1471-4159.1998.70052057.x Manganaro, 1995, Redox perturbations in cysteamine-stressed astroglia: implications for inclusion formation and gliosis in the aging brain, Free Radic. Biol. Med., 19, 823, 10.1016/0891-5849(95)02008-X Mateo, 2010, Serum heme oxygenase-1 levels are increased in Parkinson’s disease but not in Alzheimer’s disease, Acta Neurol. Scand., 121, 136, 10.1111/j.1600-0404.2009.01261.x Mathew, 2011, Alzheimer’s disease: cholesterol a menace?, Brain Res. Bull., 86, 1, 10.1016/j.brainresbull.2011.06.006 Matsumoto, 1999, Psychological stress-induced enhancement of brain lipid peroxidation via nitric oxide systems and its modulation by anxiolytic and anxiogenic drugs in mice, Brain Res., 839, 74, 10.1016/S0006-8993(99)01715-1 Mattson, 2002, Contributions of mitochondrial alterations, resulting from bad genes and a hostile environment, to the pathogenesis of Alzheimer’s disease, Int. Rev. Neurobiol., 53, 387, 10.1016/S0074-7742(02)53014-2 Mattson, 2006, Ageing and neuronal vulnerability, Nat. Rev. Neurosci., 7, 278, 10.1038/nrn1886 Matz, 1996, Heme-oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage, Brain Res., 713, 211, 10.1016/0006-8993(95)01511-6 Mehindate, 2001, Proinflammatory cytokines promote glial heme oxygenase-1 expression and mitochondrial iron deposition: implications for multiple sclerosis, J. Neurochem., 77, 1386, 10.1046/j.1471-4159.2001.00354.x Mehler-Wex, 2006, Dopaminergic dysbalance in distinct basal ganglia neurocircuits: implications for the pathophysiology of Parkinson’s disease, schizophrenia and attention deficit hyperactivity disorder, Neurotox. Res., 10, 167, 10.1007/BF03033354 Meyer, 2008, Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge, Neuropsychopharmacology, 33, 441, 10.1038/sj.npp.1301413 Minoshima, 1997, Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease, Ann. Neurol., 42, 85, 10.1002/ana.410420114 Mishra, 2012, Anthropometerical association of the craniofacial dysmorphology with schizophrenia, J. Clin. Diagn. Res., 6, 1620 Miyaoka, 2000, Schizophrenia-associated idiopathic unconjugated hyperbilirubinemia (Gilbert’s syndrome), J. Clin. Psychiatry, 61, 868, 10.4088/JCP.v61n1110 Miyaoka, 2005, Urinary excretion of biopyrrins, oxidative metabolites of bilirubin, increases in patients with psychiatric disorders, Eur. Neuropsychopharmacol., 15, 249, 10.1016/j.euroneuro.2004.11.002 Moccia, 2015, Increased bilirubin levels in de novo Parkinson’s disease, Eur. J. Neurol., 22, 954, 10.1111/ene.12688 Morris, 2005, PCP: from pharmacology to modelling schizophrenia, Curr. Opin. Pharmacol., 5, 101, 10.1016/j.coph.2004.08.008 Muller, 1991, Coincidence of schizophrenia and hyperbilirubinemia, Pharmacopsychiatry, 24, 225, 10.1055/s-2007-1014472 Mydlarski, 1998, Astrocyte granulogenesis and the cellular stress response Mydlarski, 1998, The peroxidase-positive subcortical glial sysytem Mydlarski, M., Deschenes, J., Schipper, H., 2003. Expression of heme oxygenase-1 in the human eye. Assoc Res Vis Ophthalmo (ARVO). Ft. Lauderdale: Invest Ophthalmol Vis Sci, p. E-Abstract 649. Nagao, 2014, Argyrophilic grain disease as a neurodegenerative substrate in late-onset schizophrenia and delusional disorders, Eur. Arch. Psychiatry Clin. Neurosci., 264, 317, 10.1007/s00406-013-0472-6 Nakagami, 1993, A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin, Biochim. Biophys. Acta, 1158, 189, 10.1016/0304-4165(93)90013-X Nakaso, 2000, Oxidative stress-related proteins A170 and heme oxygenase-1 are differently induced in the rat cerebellum under kainate-mediated excitotoxicity, Neurosci. Lett., 282, 57, 10.1016/S0304-3940(00)00836-3 Nalls, 2014, Genetic comorbidities in Parkinson’s disease, Hum. Mol. Genet., 23, 831, 10.1093/hmg/ddt465 Nathan, 1998, Antioxidant and prooxidant actions of estrogens: potential physiological and clinical implications, Semin. Reprod. Endocrinol., 16, 309, 10.1055/s-2007-1016289 Nishi, 2010, MicroRNA-15b modulates cellular ATP levels and degenerates mitochondria via Arl2 in neonatal rat cardiac myocytes, J. Biol. Chem., 285, 4920, 10.1074/jbc.M109.082610 Nishimura, 2000, The carbohydrate deposits detected by histochemical methods in the molecular layer of the dentate gyrus in the hippocampal formation of patients with schizophrenia, Down’s syndrome and dementia, and aged person, Glycoconj. J., 17, 815, 10.1023/A:1010996911581 Noble, 1990, Endogenous peroxidatic activity in astrocytes after spinal cord injury, J. Comp. Neurol., 296, 674, 10.1002/cne.902960411 Oddo, 2003, Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Abeta and synaptic dysfunction, Neuron, 39, 409, 10.1016/S0896-6273(03)00434-3 Ogawa, 2002, [Heme metabolism in stress response], Nippon. Eiseigaku Zasshi, 56, 615, 10.1265/jjh.56.615 Ondo, 2003, Flumazenil, a GABA antagonist, may improve features of Parkinson's disease, Mov. Disord., 18, 683, 10.1002/mds.10426 Orihara, 2003, Immunohistochemical study on the induction of heme oxygenase-1 by traumatic brain injury, Leg. Med. Tokyo, 5, S278, 10.1016/S1344-6223(02)00149-9 Ouyang, 2013, Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia, Glia, 61, 1784, 10.1002/glia.22556 Oz, 2006, Proton MRS of the unilateral substantia nigra in the human brain at 4 tesla: detection of high GABA concentrations, Magn. Reson. Med., 55, 296, 10.1002/mrm.20761 Panahian, 1999, Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice, J. Neurochem., 72, 1187, 10.1111/j.1471-4159.1999.721187.x Panizzon, 1996, Neuroprotection against CA1 injury with metalloporphyrins, Neuroreport, 7, 662, 10.1097/00001756-199601310-00067 Park, 2017, 4-Hydroxyestradiol induces mammary epithelial cell transformation through Nrf2-mediated heme oxygenase-1 overexpression, Oncotarget, 8, 164, 10.18632/oncotarget.10516 Pennington, 2008, Proteomic analysis reveals protein changes within layer 2 of the insular cortex in schizophrenia, Proteomics, 8, 5097, 10.1002/pmic.200800415 Perry, 2003, Oxidative damage in the olfactory system in Alzheimer’s disease, Acta Neuropathol. (Berl.), 106, 552, 10.1007/s00401-003-0761-7 Petronilli, 1993, Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria, J. Biol. Chem., 268, 21939, 10.1016/S0021-9258(20)80631-0 Piantadosi, 2006, Carbon monoxide, oxidative stress, and mitochondrial permeability pore transition, Free Radic. Biol. Med., 40, 1332, 10.1016/j.freeradbiomed.2005.11.020 Pirici, 2014, Corpora amylacea in the brain form highly branched three-dimensional lattices, Rom. J. Morphol. Embryol., 55, 1071 Pisa, 2016, Corpora Amylacea of brain tissue from neurodegenerative diseases are stained with specific antifungal antibodies, Front. Neurosci., 10, 86, 10.3389/fnins.2016.00086 Pizzimenti, 2009, MicroRNA expression changes during human leukemic HL-60 cell differentiation induced by 4-hydroxynonenal, a product of lipid peroxidation, Free Radic. Biol. Med., 46, 282, 10.1016/j.freeradbiomed.2008.10.035 Poli, 2017, Is aceruloplasminemia treatable? Combining iron chelation and fresh-frozen plasma treatment, Neurol. Sci., 38, 357, 10.1007/s10072-016-2756-x Policastro, 2004, Imbalance of antioxidant enzymes in tumor cells and inhibition of proliferation and malignant features by scavenging hydrogen peroxide, Mol. Carcinog., 39, 103, 10.1002/mc.20001 Polymeropoulos, 1997, Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease, Science (80), 276, 2045, 10.1126/science.276.5321.2045 Powell, 2007, Gilbert’s syndrome in a patient with predominantly negative symptoms of schizophrenia, Int. J. Psychiatry Clin. Pract., 11, 239, 10.1080/13651500600811735 Prabakaran, 2004, Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress, Mol. Psychiatry, 9, 684, 10.1038/sj.mp.4001511 Pruessner, 2017, Interplay of hippocampal volume and hypothalamus-pituitary-adrenal axis function as markers of stress vulnerability in men at ultra-high risk for psychosis, Psychol. Med., 47, 471, 10.1017/S0033291716002658 Puchades, 2003, Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer’s disease, Brain Res. Mol. Brain Res., 118, 140, 10.1016/j.molbrainres.2003.08.005 Qato, 1985, Prevention of neonatal hyperbilirubinaemia in non-human primates by Zn-protoporphyrin, Biochem. J., 226, 51, 10.1042/bj2260051 Radhakrishnan, 2011, Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia, J. Pediatr. Hematol. Oncol., 33, 74, 10.1097/MPH.0b013e3181fd2aae Radhakrishnan, 2011, Association between unconjugated bilirubin and schizophrenia, Psychiatry Res., 189, 480, 10.1016/j.psychres.2011.03.003 Rajdev, 1998, Acute phencyclidine neurotoxicity in rat forebrain: induction of haem oxygenase-1 and attenuation by the antioxidant dimethylthiourea, Eur. J. Neurosci., 10, 3840, 10.1046/j.1460-9568.1998.00392.x Reichmann, 1994 Reitz, 2013, Dyslipidemia and the risk of Alzheimer’s disease, Curr. Atheroscler. Rep., 15, 307, 10.1007/s11883-012-0307-3 Roberts, 2015, Seeking a mechanism for the toxicity of oligomeric alpha-synuclein, Biomolecules, 5, 282, 10.3390/biom5020282 Rohn, 2015, Corpora Amylacea in Neurodegenerative Diseases: Cause or Effect?, Int. J. Neurol. Neurother., 2 Rouault, 2005, Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis, Nat. Rev. Mol. Cell Biol., 6, 345, 10.1038/nrm1620 Rozema, 2007, Dynamic PolyConjugates for targeted in vivo delivery of siRNA to hepatocytes, Proc. Natl. Acad. Sci. U. S. A., 104, 12982, 10.1073/pnas.0703778104 Rukova, 2014, Genome-wide methylation profiling of schizophrenia, Balkan J. Med. Genet., 17, 15, 10.2478/bjmg-2014-0070 Rybakova, 2012, Receptor-mediated oxidative stress in murine cerebellar neurons is accompanied by phosphorylation of MAP (ERK 1/2) kinase, Curr. Aging Sci., 5, 225, 10.2174/1874609811205030009 Ryter, 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, 10.1016/S0891-5849(99)00223-3 Ryter, 2006, Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications, Physiol. Rev., 86, 583, 10.1152/physrev.00011.2005 Sahlas, 2002, Role of heme oxygenase-1 in the biogenesis of corpora amylacea, Biogerontology, 3, 223, 10.1023/A:1016223109601 Sainz, 2018, Blood gene expression profile predicts response to antipsychotics, Front. Mol. Neurosci., 11, 10.3389/fnmol.2018.00073 Scacchi, 2001, Plasma alpha1-antichymotrypsin in Alzheimer’s disease; relationships with APOE genotypes, Neurobiol. Aging, 22, 413, 10.1016/S0197-4580(00)00246-3 Scapagnini, 2002, Gene expression profiles of heme oxygenase isoforms in the rat brain, Brain Res., 954, 51, 10.1016/S0006-8993(02)03338-3 Schallner, 2017, Carbon monoxide preserves circadian rhythm to reduce the severity of subarachnoid hemorrhage in mice, Stroke, 48, 2565, 10.1161/STROKEAHA.116.016165 Schipper, 1993, Role of peroxidase-positive astrocytes in estradiol-related hypothalamic damage Schipper, 1996, Astrocytes, brain aging, and neurodegeneration, Neurobiol. Aging, 17, 467, 10.1016/0197-4580(96)00014-0 Schipper, 1998, Experimental induction of corpora amylacea in adult rat brain, Microsc. Res. Tech., 43, 43, 10.1002/(SICI)1097-0029(19981001)43:1<43::AID-JEMT7>3.0.CO;2-B Schipper, 1998, Glial iron sequestration and neurodegeneration Schipper, 1999, Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases, Neurotox. Res., 1, 57, 10.1007/BF03033339 Schipper, 2000, Heme oxygenase-1: role in brain aging and neurodegeneration, Exp. Gerontol., 35, 821, 10.1016/S0531-5565(00)00148-0 Schipper, 2001, Mitochondrial iron deposition in aging astroglia: mechanisms and disease implications Schipper, 2004, Brain iron deposition and the free radical-mitochondrial theory of ageing, Ageing Res. Rev., 3, 265, 10.1016/j.arr.2004.02.001 Schipper, 2004, Heme oxygenase expression in human central nervous system disorders, Free Radic. Biol. Med., 37, 1995, 10.1016/j.freeradbiomed.2004.09.015 Schipper, 2004, Heme oxygenase-1: transducer of pathological brain iron sequestration under oxidative stress, Ann. N. Y. Acad. Sci., 1012, 84, 10.1196/annals.1306.007 Schipper, 2004, Redox neurology: visions of an emerging subspecialty Schipper, 2012, Neurodegeneration with brain iron accumulation - clinical syndromes and neuroimaging, Biochim. Biophys. Acta, 1822, 350, 10.1016/j.bbadis.2011.06.016 Schipper, 2015, Is glial heme oxygenase-1 suppression in neurodegenerative disorders permissive for neural repair?, Neural Regen. Res., 10, 208, 10.4103/1673-5374.152371 Schipper, 1995, Mitochondrial constituents of corpora amylacea and autofluorescent astrocytic inclusions in senescent human brain, Glia, 14, 55, 10.1002/glia.440140108 Schipper, 2015, A heme oxygenase-1 transducer model of degenerative and developmental brain disorders, Int. J. Mol. Sci., 16, 5400, 10.3390/ijms16035400 Schipper, 1981, Role of the gonads in the histologic aging of the hypothalamic arcuate nucleus, Biol. Reprod., 25, 413, 10.1095/biolreprod25.2.413 Schipper, 1990, Gomori-positive astrocytes in primary culture: effects of in vitro age and cysteamine exposure, Dev. Brain Res., 54, 71, 10.1016/0165-3806(90)90066-8 Schipper, 1990, Effects of progestins on the estradiol-related accumulation of astrocytic granules in the hypothalamic arcuate nucleus, Brain Res., 527, 176, 10.1016/0006-8993(90)91080-Z Schipper, 1991, Catechol oxidation by peroxidase-positive astrocytes in primary culture: an electron spin resonance study, J. Neurosci., 11, 2170, 10.1523/JNEUROSCI.11-07-02170.1991 Schipper, 1993, Cysteamine gliopathy in situ: a cellular stress model for the biogenesis of astrocytic inclusions, J. Neuropathol. Exp. Neurol., 52, 399, 10.1097/00005072-199307000-00007 Schipper, 1994, The 21-aminosteroid antioxidant, U74389F, prevents estradiol-induced depletion of hypothalamic beta-endorphin in adult female rats, Brain Res., 652, 161, 10.1016/0006-8993(94)90332-8 Schipper, 1995, Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain, Ann. Neurol., 37, 758, 10.1002/ana.410370609 Schipper, 1998, Neural heme oxygenase-1 expression in idiopathic Parkinson’s disease, Exp. Neurol., 150, 60, 10.1006/exnr.1997.6752 Schipper, 1998, Astrocyte mitochondria: a substrate for iron deposition in the aging rat substantia nigra, Exp. Neurol., 152, 188, 10.1006/exnr.1998.6854 Schipper, 1999, Mitochondrial iron sequestration in dopamine-challenged astroglia: role of heme oxygenase-1 and the permeability transition pore, J. Neurochem., 72, 1802, 10.1046/j.1471-4159.1999.0721802.x Schipper, 2000, Evaluation of heme oxygenase-1 as a systemic biological marker of sporadic AD, Neurology, 54, 1297, 10.1212/WNL.54.6.1297 Schipper, 2002, Role of porphyrin sequestration in the biogenesis of iron-laden astrocytic inclusions in primary culture, Dev. Neurosci., 24, 169, 10.1159/000065692 Schipper, 2006, Glial heme oxygenase-1 expression in Alzheimer disease and mild cognitive impairment, Neurobiol. Aging, 27, 252, 10.1016/j.neurobiolaging.2005.01.016 Schipper, 2009, Suppression of glial HO-1 activity as a potential neurotherapeutic intervention in AD, Curr. Alzheimer Res., 6, 424, 10.2174/156720509789207985 Schipper, 2009, Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement, J. Neurochem., 110, 469, 10.1111/j.1471-4159.2009.06160.x Schliebs, 2011, The cholinergic system in aging and neuronal degeneration, Behav. Brain Res., 221, 555, 10.1016/j.bbr.2010.11.058 Schluesener, 2001, Heme oxygenase-1 in lesions of human cerebral malaria, Acta Neuropathol. (Berl.), 101, 65, 10.1007/s004010000250 Selkoe, 1991, The molecular pathology of Alzheimer’s disease, Neuron, 6, 487, 10.1016/0896-6273(91)90052-2 Shahed, 2001, Re-emergence of childhood stuttering in Parkinson’s disease: a hypothesis, Mov. Disord., 16, 114, 10.1002/1531-8257(200101)16:1<114::AID-MDS1004>3.0.CO;2-2 Shetty, 1999, Vulnerability of the dentate gyrus to aging and intracerebroventricular administration of kainic acid, Exp. Neurol., 158, 491, 10.1006/exnr.1999.7107 Shivakumar, 2014, Do schizophrenia patients age early?, Asian J. Psychiatr., 10, 3, 10.1016/j.ajp.2014.02.007 Simone, 2009, Ionizing radiation-induced oxidative stress alters miRNA expression, PLoS One, 4, e6377, 10.1371/journal.pone.0006377 Smith, 1994, Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer’s disease, Am. J. Pathol., 145, 42 Smith, 2010, Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment, J. Alzheimers Dis., 19, 363, 10.3233/JAD-2010-1239 Snow, 1996, Psychosis in neurodegenerative disease, Semin. Clin. Neuropsychiatry, 1, 282 Snyder, 1998, Nitric oxide and carbon monoxide: parallel roles as neural messengers, Brain Res. Brain Res. Rev., 26, 167, 10.1016/S0165-0173(97)00032-5 Song, 2004 Song, 2006, Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia, J. Cell. Physiol., 206, 655, 10.1002/jcp.20509 Song, 2009, The Parkinson disease-associated A30P mutation stabilizes alpha-synuclein against proteasomal degradation triggered by heme oxygenase-1 over-expression in human neuroblastoma cells, J. Neurochem., 110, 719, 10.1111/j.1471-4159.2009.06165.x Song, 2012, Schizophrenia-like features in transgenic mice overexpressing human HO-1 in the astrocytic compartment, J. Neurosci., 32, 10841, 10.1523/JNEUROSCI.6469-11.2012 Song, 2012, Unregulated brain iron deposition in transgenic mice over-expressing HMOX1 in the astrocytic compartment, J. Neurochem., 123, 325, 10.1111/j.1471-4159.2012.07914.x Song, 2014, Astroglial heme oxygenase-1 and the origin of corpora amylacea in aging and degenerating neural tissues, Exp. Neurol., 254, 78, 10.1016/j.expneurol.2014.01.006 Song, 2017, Parkinsonian features in aging GFAP.HMOX1 transgenic mice overexpressing human HO-1 in the astroglial compartment, Neurobiol. Aging, 58, 163, 10.1016/j.neurobiolaging.2017.06.017 Song, 2017, Cysteine-rich whey protein isolate (Immunocal(R)) ameliorates deficits in the GFAP.HMOX1 mouse model of schizophrenia, Free Radic. Biol. Med., 110, 162, 10.1016/j.freeradbiomed.2017.05.025 Song, 2018, Evaluation of salivary heme oxygenase-1 as a potential biomarker of early Parkinson’s disease, Mov. Disord., 10.1002/mds.27328 Sossi, 2010, Dopamine turnover increases in asymptomatic LRRK2 mutations carriers, Mov. Disord., 25, 2717, 10.1002/mds.23356 Srebro, 1971, Periventricular Gomori-positive glia in brains of X-irradiated rats, Brain Res., 35, 463, 10.1016/0006-8993(71)90488-4 Srebro, 2008, The glial Gomori-positive material is sulfane sulpfur, Folia Histochem. Cytobiol., 46, 73, 10.2478/v10042-008-0010-y Sripada, 2012, Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA, PLoS One, 7, e44873, 10.1371/journal.pone.0044873 Stahnke, 2007, Differential upregulation of heme oxygenase-1 (HSP32) in glial cells after oxidative stress and in demyelinating disorders, J. Mol. Neurosci., 32, 25, 10.1007/s12031-007-0005-8 Stevens, 1982, Neuropathology of schizophrenia, Arch. Gen. Psychiatry, 39, 1131, 10.1001/archpsyc.1982.04290100011003 St-Jacques, 1999, Acceleration of ageing-related gliopathic changes and hippocampal dysfunction following intracerebroventricular infusion of cysteamine in adult rats, Neuroscience, 90, 1103, 10.1016/S0306-4522(98)00487-4 Stocker, 1987, Bilirubin is an antioxidant of possible physiological importance, Science (80), 235, 1043, 10.1126/science.3029864 Stokes, 1999, Cytotoxic and genotoxic potential of dopamine, J. Neurosci. Res., 55, 659, 10.1002/(SICI)1097-4547(19990315)55:6<659::AID-JNR1>3.0.CO;2-C Storm, 2002, Mitotic brain cells are just as prone to mitochondrial deletions as neurons: a large-scale single-cell PCR study of the human caudate nucleus, Exp. Gerontol., 37, 1389, 10.1016/S0531-5565(02)00121-3 Suliman, 2007, The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy, J. Clin. Invest., 117, 3730 Sultana, 2013, Lipid peroxidation triggers neurodegeneration: a redox proteomics view into the Alzheimer disease brain, Free Radic. Biol. Med., 62, 157, 10.1016/j.freeradbiomed.2012.09.027 Sun, 2002, Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene, EMBO J., 21, 5216, 10.1093/emboj/cdf516 Suttner, 1999, Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron, FASEB J., 13, 1800, 10.1096/fasebj.13.13.1800 Suzuki, 1999, Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats, J. Clin. Invest., 104, 59, 10.1172/JCI5357 Suzuki, 2003, Intracranial heme metabolism and cerebral vasospasm after aneurysmal subarachnoid hemorrhage, Stroke, 34, 2796, 10.1161/01.STR.0000103743.62248.12 Suzuki, 2003, Cadmium induces nuclear export of Bach1, a transcriptional repressor of heme oxygenase-1 gene, J. Biol. Chem., 278, 49246, 10.1074/jbc.M306764200 Syapin, 2008, Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders, Br. J. Pharmacol., 155, 623, 10.1038/bjp.2008.342 Taille, 2005, Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle, J. Biol. Chem., 280, 25350, 10.1074/jbc.M503512200 Takahashi, 2000, Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer’s disease, Neuron, 28, 461, 10.1016/S0896-6273(00)00125-2 Takao, 2013, Deficiency of schnurri-2, an MHC enhancer binding protein, induces mild chronic inflammation in the brain and confers molecular, neuronal, and behavioral phenotypes related to schizophrenia, Neuropsychopharmacology, 38, 1409, 10.1038/npp.2013.38 Takeda, 2000, Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau, J. Biol. Chem., 275, 5395, 10.1074/jbc.275.8.5395 Tanaka, 2000, Pharmacogenomics and therapeutic target validation in cerebral vasospasm, J. Cardiovasc. Pharmacol., 36, S1, 10.1097/00005344-200000006-00002 Tanno, 1998, mtDNA polymorphisms in Japanese sporadic Alzheimer’s disease, Neurobiol. Aging, 19, S47, 10.1016/S0197-4580(98)00028-1 Tomas, 2015, Environmental modulations of the number of midbrain dopamine neurons in adult mice, J. Vis. Exp., 95, 52329 Trakshel, 1988, Resolution of the rat brain heme oxygenase activity: absence of a detectable amount of the inducible form (HO-1), Arch. Biochem. Biophys., 260, 732, 10.1016/0003-9861(88)90503-6 van Horssen, 2008, Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression, Free Radic. Biol. Med., 45, 1729, 10.1016/j.freeradbiomed.2008.09.023 van Horssen, 2010, Nrf2 and DJ1 are consistently upregulated in inflammatory multiple sclerosis lesions, Free Radic. Biol. Med., 49, 1283, 10.1016/j.freeradbiomed.2010.07.013 Vasilev, 2003, Age-related differences in MK-801- and amphetamine-induced locomotor and stereotypic activities of rats, Neurobiol. Aging, 24, 715, 10.1016/S0197-4580(02)00232-4 Vaya, 2007, Effects of heme oxygenase-1 expression on sterol homeostasis in rat astroglia, Free Radic. Biol. Med., 42, 864, 10.1016/j.freeradbiomed.2006.12.022 Verkhratsky, 2016, Astrogliopathology in neurological, neurodevelopmental and psychiatric disorders, Neurobiol. Dis., 85, 254, 10.1016/j.nbd.2015.03.025 Verma, 1993, Carbon monoxide: a putative neural messenger, Science (80), 259, 381, 10.1126/science.7678352 Vincent, 1994, Brain heme oxygenase isoenzymes and nitric oxide synthase are co-localized in select neurons, Neuroscience, 63, 223, 10.1016/0306-4522(94)90018-3 Volles, 2002, Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson’s disease-linked mutations and occurs by a pore-like mechanism, Biochemistry, 41, 4595, 10.1021/bi0121353 Voloboueva, 2007, Inhibition of mitochondrial function in astrocytes: implications for neuroprotection, J. Neurochem., 102, 1383, 10.1111/j.1471-4159.2007.04634.x Volta, 2017, Initial elevations in glutamate and dopamine neurotransmission decline with age, as does exploratory behavior, in LRRK2 G2019S knock-in mice, Elife, 6, 10.7554/eLife.28377 Wagner, 1978, A microprobe analysis of Gomori-positive glial cells in the rat arcuate nucleus, Histochemistry, 55, 147, 10.1007/BF00493517 Wagner-Ecker, 2010, MicroRNA expression after ionizing radiation in human endothelial cells, Radiat. Oncol., 5, 25, 10.1186/1748-717X-5-25 Wang, 2007, Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage, Brain, 130, 1643, 10.1093/brain/awm095 Wang, 1995, A cellular stress model for the sequestration of redox-active glial iron in the aging and degenerating nervous system, J. Neurochem., 64, 1868, 10.1046/j.1471-4159.1995.64041868.x Wang, 2014, Effects of downregulation of microRNA-181a on H2O2-induced H9c2 cell apoptosis via the mitochondrial apoptotic pathway, Oxid. Med. Cell. Longev., 2014, 10.1155/2014/960362 Wang, 2015, Salivary biomarkers of oxidative stress: A critical review, Free Radic. Biol. Med., 85, 95, 10.1016/j.freeradbiomed.2015.04.005 Weiss, 1996, Divergent effects of alpha 1-antitrypsin on the regulation of iron metabolism in human erythroleukaemic (K562) and myelomonocytic (THP-1) cells, Biochem. J., 319, 897, 10.1042/bj3190897 Weng, 2014, Inhibition of miR-17 and miR-20a by oridonin triggers apoptosis and reverses chemoresistance by derepressing BIM-S, Cancer Res., 74, 4409, 10.1158/0008-5472.CAN-13-1748 Williams, 1957, Pleiotropy, natural selection, and the evolution of senescence, Evolution (N. Y.), 11, 398 Wilson, 2004, Religious orders study: overview and change in cognitive and motor speed, Aging Neuropsychol. Cogn., 11, 280, 10.1080/13825580490511125 Winograd-Gurvich, 2006, Negative symptoms: a review of schizophrenia, melancholic depression and Parkinson’s disease, Brain Res. Bull., 70, 312, 10.1016/j.brainresbull.2006.06.007 Woodford, 1980, An ultrastructural study of the corpora amylacea of the optic nerve head and retina, Am. J. Ophthalmol., 90, 492, 10.1016/S0002-9394(14)75018-4 Wu, 1997, Increased dopamine activity associated with stuttering, Neuroreport, 8, 767, 10.1097/00001756-199702100-00037 Xu, 2010, miR-17* suppresses tumorigenicity of prostate cancer by inhibiting mitochondrial antioxidant enzymes, PLoS One, 5, e14356, 10.1371/journal.pone.0014356 Xu, 2012, miR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2, Biochem. J., 446, 291, 10.1042/BJ20120386 Yachie, 1999, Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency, J. Clin. Invest., 103, 129, 10.1172/JCI4165 Yang, 2015, Association of histamine N-methyltransferase Thr105Ile polymorphism with Parkinson’s disease and schizophrenia in Han Chinese: a case-control study, PLoS One, 10, e0119692, 10.1371/journal.pone.0119692 Yang, 2017, High-glucose-Derived oxidative stress-dependent heme Oxygenase-1 expression from astrocytes contributes to the neuronal apoptosis, Mol. Neurobiol., 54, 470, 10.1007/s12035-015-9666-4 Yasukawa, 2007, Increased urinary excretion of biopyrrins, oxidative metabolites of bilirubin, in patients with schizophrenia, Psychiatry Res., 153, 203, 10.1016/j.psychres.2006.04.009 Yu, 2003, Correlation of oxidative stress and the loss of the nicotinic receptor alpha 4 subunit in the temporal cortex of patients with Alzheimer’s disease, Neurosci. Lett., 338, 13, 10.1016/S0304-3940(02)01361-7 Yuan, 2008, The homeostasis of iron and suppression of HO-1 involved in the protective effects of nimodipine on neurodegeneration induced by aluminum overloading in mice, Eur. J. Pharmacol., 586, 100, 10.1016/j.ejphar.2008.02.033 Zhang, 1992, Mitochondrial oxidative stress after carbon monoxide hypoxia in the rat brain, J. Clin. Invest., 90, 1193, 10.1172/JCI115980 Zhang, 2017, Distinct role of heme oxygenase-1 in early- and late-stage intracerebral hemorrhage in 12-month-old mice, J. Cereb. Blood Flow Metab., 37, 25, 10.1177/0271678X16655814 Zukor, 2009, HO-1-mediated macroautophagy: A mechanism for unregulated iron deposition in aging and degenerating neural tissues, J. Neurochem., 109, 776, 10.1111/j.1471-4159.2009.06007.x