Nrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression

Molecular Psychiatry

Volumn 22, Issue 12, 2017, Pages 1701-1713

  Bouvier, E ^a,b,c   Brouillard, F ^d,e   Molet, J ^a,b,c   Claverie, D ^a,b,c,f   Cabungcal, J H ^g   Cresto, N ^a,b,c   Doligez, N ^a,b,c   Rivat, C ^a,b,c   Do, K Q ^g   Bernard, C ^h   Benoliel, J J ^a,b,c,i   Becker, C ^a,b,c,d  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^f INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^g LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^h AIX MARSEILLE UNIVERSITÉ   (France)

ⁱ PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; ENZYME; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; NFE2L2 PROTEIN, MOUSE; NFE2L2 PROTEIN, RAT; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; FEMALE; HOMEOSTASIS; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; STRESS; ANIMAL; C57BL MOUSE; DISEASE MODEL; DISEASE PREDISPOSITION; DOMINANT-SUBORDINATE RELATIONSHIP; DRUG EFFECT; GENETICS; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIOXIDANTS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; DOMINANCE-SUBORDINATION; HIPPOCAMPUS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEOME; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY;

EID: 84988422070     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.144     Document Type: Article

References (68)

1. McEwen BS. The brain on stress: toward an integrative approach to brain, body and behavior. Perspect Psychol Sci 2013; 8: 673-675.
2. McEwen BS. Biomarkers for assessing population and individual health and disease related to stress and adaptation. Metabolism 2015; 64: S2-S10.
3. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005; 6: 463-475.
4. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007; 131: 391-404.
5. Blugeot A, Rivat C, Bouvier E, Molet J, Mouchard A, Zeau B et al. Vulnerability to depression: from brain neuroplasticity to identification of biomarkers. J Neurosci 2011; 31: 12889-12899.
6. Miczek KA, Nikulina EM, Takahashi A, Covington HE 3rd, Yap JJ, Boyson CO et al. Gene expression in aminergic and peptidergic cells during aggression and defeat: relevance to violence, depression and drug abuse. Behav Genet 2011; 41: 787-802.
7. Terracciano A, Lobina M, Piras MG, Mulas A, Cannas A, Meirelles O et al. Neuroticism, depressive symptoms, and serum BDNF. Psychosom Med 2011; 73: 638-642.
8. Lang UE, Hellweg R, Gallinat J. BDNF serum concentrations in healthy volunteers are associated with depression-related personality traits. Neuropsychopharmacology 2004; 29: 795-798.
9. Minelli A, Zanardini R, Bonvicini C, Sartori R, Pedrini L, Gennarelli M et al. BDNF serum levels, but not BDNF Val66Met genotype, are correlated with personality traits in healthy subjects. Eur Arch Psychiatry Clin Neurosci 2011; 261: 323-329.
10. Avila-Costa MR, Colin-Barenque L, Fortoul TI, Machado-Salas JP, Espinosa-Villanueva J, Rugerio-Vargas C et al. Motor impairments in an oxidative stress model and its correlation with cytological changes on rat striatum and prefrontal cortex. Int J Neurosci 2001; 108: 193-200.
11. Do KQ, Cabungcal JH, Frank A, Steullet P, Cuenod M. Redox dysregulation, neurodevelopment, and schizophrenia. Curr Opin Neurobiol 2009; 19: 220-230.
12. Hovatta I, Juhila J, Donner J. Oxidative stress in anxiety and comorbid disorders. Neurosci Res 2010; 68: 261-275.
13. Maes M, Kubera M, Obuchowiczwa E, Goehler L, Brzeszcz J. Depression's multiple comorbidities explained by (neuro)inflammatory and oxidative & nitrosative stress pathways. Neuro Endocrinol Lett 2011; 32: 7-24.
14. Bergamini CM, Gambetti S, Dondi A, Cervellati C. Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des 2004; 10: 1611-1626.
15. Mates JM. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 2000; 153: 83-104.
16. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006; 312: 1882-1883.
17. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999; 13: 76-86.
18. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 2011; 85: 241-272.
19. Singh S, Vrishni S, Singh BK, Rahman I, Kakkar P. Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases. Free Radic Res 2010; 44: 1267-1288.
20. Soriano FX, Baxter P, Murray LM, Sporn MB, Gillingwater TH, Hardingham GE. Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin. Mol Cells 2009; 27: 279-282.
21. Biteau B, Labarre J, Toledano MB. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 2003; 425: 980-984.
22. Abbas K, Breton J, Planson AG, Bouton C, Bignon J, Seguin C et al. Nitric oxide activates an Nrf2/sulfiredoxin antioxidant pathway in macrophages. Free Radic Biol Med 2011; 51: 107-114.
23. Halliwell B. Oxidative stress and neurodegeneration: where are we now? J Neurochem 2006; 97: 1634-1658.
24. Maes M, Fisar Z, Medina M, Scapagnini G, Nowak G, Berk M. New drug targets in depression: inflammatory, cell-mediated immune, oxidative and nitrosative stress, mitochondrial, antioxidant, and neuroprogressive pathways. And new drug candidates-Nrf2 activators and GSK-3 inhibitors. Inflammopharmacology 2012; 20: 127-150.
25. Martín-de-Saavedra MD, Budni J, Cunha MP, Gómez-Rangel V, Lorrio S, Del Barrio L et al. Nrf2 participates in depressive disorders through an anti-inflammatory mechanism. Psychoneuroendocrinology 2013; 38: 2010-2022.
26. de Boer SF, van der Vegt BJ, Koolhaas JM. Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav Genet 2003; 33: 485-501.
27. Andre J, Zeau B, Pohl M, Cesselin F, Benoliel JJ, Becker C. Involvement of cholecystokininergic systems in anxiety-induced hyperalgesia in male rats: behavioral and biochemical studies. J Neurosci 2005; 25: 7896-7904.
28. Becker C, Thiebot MH, Touitou Y, Hamon M, Cesselin F, Benoliel JJ. Enhanced cortical extracellular levels of cholecystokinin-like material in a model of anticipation of social defeat in the rat. J Neurosci 2001; 21: 262-269.
29. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res 1997; 387: 147-163.
30. Shih AY, Li P, Murphy TH. A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 2005; 25: 10321-10335.
31. Benoliel JJ, Mauborgne A, Bourgoin S, Legrand JC, Hamon M, Cesselin F. Opioid control of the in vitro release of cholecystokinin-like material from the rat substantia nigra. J Neurochem 1992; 58: 916-922.
32. Wilcox CS, Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 2008; 60: 418-469.
33. Wilcox CS. Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol Ther 2010; 126: 119-145.
34. Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y et al. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci USA 2010; 107: 2687-2692.
35. Becker C, Bouvier E, Ghestem A, Siyoucef S, Claverie D, Camus F et al. Predicting and treating stress-induced vulnerability to epilepsy and depression. Ann Neurol 2015; 78: 128-136.
36. Flint DH, Tuminello JF, Emptage MH. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 1993; 268: 22369-22376.
37. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM et al. GO:TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004; 20: 3710-3715.
38. Wassmann S, Wassmann K, Nickenig G. Modulation of oxidant and antioxidant enzyme expression and function in vascular cells. Hypertension 2004; 44: 381-386.
39. Cocheme HM, Logan A, Prime TA, Abakumova I, Quin C, McQuaker SJ et al. Using the mitochondria-targeted ratiometric mass spectrometry probe MitoB to measure H2O2 in living Drosophila. Nat Protoc 2012; 7: 946-958.
40. Rothman SM, Mattson MP. Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med 2010; 12: 56-70.
41. Bell KF, Hardingham GE. CNS peroxiredoxins and their regulation in health and disease. Antioxid Redox Signal 2011; 14: 1467-1477.
42. Sartorius A, Hellweg R, Litzke J, Vogt M, Dormann C, Vollmayr B et al. Correlations and discrepancies between serum and brain tissue levels of neurotrophins after electroconvulsive treatment in rats. Pharmacopsychiatry 2009; 42: 270-276.
43. Schmidt HD, Duman RS. Peripheral BDNF produces antidepressant-likeeffects in cellular and behavioral models. Neuropsychopharmacology 2010; 35: 2378-2391.
44. Zhang R, Kang KA, Piao MJ, Ko DO, Wang ZH, Chang WY et al. Preventive effect of 7,8-dihydroxyflavone against oxidative stress induced genotoxicity. Biol Pharm Bull 2009; 32: 166-171.
45. Chen J, Chua KW, Chua CC, Yu H, Pei A, Chua BH et al. Antioxidant activity of 7,8-dihydroxyflavone provides neuroprotection against glutamate-induced toxicity. Neurosci Lett 2011; 499: 181-185.
46. Gupta VK, You Y, Li JC, Klistorner A, Graham SL. Protective effects of 7,8-dihydroxyflavone on retinal ganglion and RGC-5 cells against excitotoxic and oxidative stress. J Mol Neurosci 2013; 49: 96-104.
47. Phalen TJ, Weirather K, Deming PB, Anathy V, Howe AK, van der Vliet A et al. Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery. J Cell Biol 2006; 175: 779-789.
48. Rhee SG, Woo HA, Kil IS, Bae SH. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. J Biol Chem 2012; 287: 4403-4410.
49. Przedborski S. Peroxiredoxin-2 links Cdk5 to neurodegeneration. Nat Med 2007; 13: 907-909.
50. Conrad CD. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 2006; 5: 41-60.
51. McEwen BS. Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann NY Acad Sci 2010; 1204: E38-E59.
52. Serhan CN. The resolution of inflammation: the devil in the flask and in the details. FASEB J 2011; 25: 1441-1448.
53. Troncoso Brindeiro CM, Lane PH, Carmines PK. Tempol prevents altered K(+) channel regulation of afferent arteriolar tone in diabetic rat kidney. Hypertension 2012; 59: 657-664.
54. Xiang M, Namani A, Wu S, Wang X. Nrf2: bane or blessing in cancer? J Cancer Res Clin Oncol 2014; 140: 1251-1259.
55. Becker C, Zeau B, Rivat C, Blugeot A, Hamon M, Benoliel JJ. Repeated social defeat-induced depression-like behavioral and biological alterations in rats: involvement of cholecystokinin. Mol Psychiatry 2008; 13: 1079-1092.
56. Krishnan V, Nestler EJ. The molecular neurobiology of depression. Nature 2008; 455: 894-902.
57. Ota KT, Duman RS. Environmental and pharmacological modulations of cellular plasticity: role in the pathophysiology and treatment of depression. Neurobiol Dis 2013; 57: 28-37.
58. Carri MT, Ferri A, Cozzolino M, Calabrese L, Rotilio G. Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Res Bull 2003; 61: 365-374.
59. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003; 53: S26-S36, discussion S-8.
60. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R 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.
61. Piec I, Listrat A, Alliot J, Chambon C, Taylor RG, Bechet D. Differential proteome analysis of aging in rat skeletal muscle. FASEB J 2005; 19: 1143-1145.
62. Ciavardelli D, Silvestri E, Del Viscovo A, Bomba M, De Gregorio D, Moreno M et al. Alterations of brain and cerebellar proteomes linked to Abeta and tau pathology in a female triple-transgenic murine model of Alzheimer's disease. Cell Death Dis 2010; 1: e90.
63. Foley TD, Melideo SL, Healey AE, Lucas EJ, Koval JA. Phenylarsine oxide binding reveals redox-active and potential regulatory vicinal thiols on the catalytic subunit of protein phosphatase 2A. Neurochem Res 2011; 36: 232-240.
64. Golden SA, Christoffel DJ, Heshmati M, Hodes GE, Magida J, Davis K et al. Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat Med 2013; 19: 337-344.
65. Raps SP, Lai JC, Hertz L, Cooper AJ. Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res 1989; 493: 398-401.
66. van Muiswinkel FL, Kuiperij HB. The Nrf2-ARE Signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders. Curr Drug Targets CNS Neurol Disord 2005; 4: 267-281.
67. Fernandes BS, Gama CS, Cereser KM, Yatham LN, Fries GR, Colpo G et al. Brain-derived neurotrophic factor as a state-marker of mood episodes in bipolar disorders: a systematic review and meta-regression analysis. J Psychiatr Res 2011; 45: 995-1004.
68. Roth TL, Lubin FD, Funk AJ, Sweatt JD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 2009; 65: 760-769.