Nrf2 participates in depressive disorders through an anti-inflammatory mechanism

Psychoneuroendocrinology

Volumn 38, Issue 10, 2013, Pages 2010-2022

  Martín de Saavedra, María Dolores ^a,b   Budni, Josiane ^d   Cunha, Mauricio P ^d   Gómez Rangel, Vanessa ^a,b   Lorrio, Silvia ^a,b,c   del Barrio, Laura ^a,b   Lastres Becker, Isabel ^c,e,f   Parada, Esther ^a,b   Tordera, Rosa María ^g   Rodrigues, Ana Lùcia S ^d   Cuadrado, Antonio ^c,e,f   López, Manuela G ^a,b  

^a INSTITUTO TEÓFILO HERNANDO   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^d FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^e INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^f INSTITUTO DE SALUD CARLOS III   (Spain)

^g UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Depression; Inflammation; Nrf2; Rofecoxib; Sulforaphane; Trophic factors

Indexed keywords

DOPAMINE; GLUTAMIC ACID; ROFECOXIB; SEROTONIN; SULFORAPHANE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DEPRESSION; GLIOSIS; HIPPOCAMPUS; KNOCKOUT MOUSE; MACROGLIA; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION;

DEPRESSION; INFLAMMATION; NRF2; ROFECOXIB; SULFORAPHANE; TROPHIC FACTORS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BEHAVIOR, ANIMAL; DEPRESSIVE DISORDER; DOPAMINE; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; NF-E2-RELATED FACTOR 2; SEROTONIN; SIGNAL TRANSDUCTION;

EID: 84883852983     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.03.020     Document Type: Article

References (53)

1. Alam J., Cook J.L. How many transcription factors does it take to turn on the heme oxygenase-1 gene?. Am. J. Respir. Cell Mol. Biol. 2007, 36:166-174.
2. Asnis G.M., De La Garza R. 2nd Interferon-induced depression in chronic hepatitis C: a review of its prevalence, risk factors, biology, and treatment approaches. J. Clin. Gastroenterol. 2006, 40:322-335.
3. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J. Neuroimmunol. 2004, 155:119-126.
4. Ben Menachem-Zidon O., Goshen I., Kreisel T., Ben Menahem Y., Reinhartz E., Ben Hur T., Yirmiya R. Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 2008, 33:2251-2262.
5. Capuron L., Neurauter G., Musselman D.L., Lawson D.H., Nemeroff C.B., Fuchs D., Miller A.H. Interferon-alpha-induced changes in tryptophan metabolism. Relationship to depression and paroxetine treatment. Biol. Psychiatry. 2003, 54:906-914.
6. Czeh B., Simon M., Schmelting B., Hiemke C., Fuchs E. Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 2006, 31:1616-1626.
7. Chen X.L., Kunsch C. Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr. Pharm. Des. 2004, 10:879-891.
8. Dembo G., Park S.B., Kharasch E.D. Central nervous system concentrations of cyclooxygenase-2 inhibitors in humans. Anesthesiology 2005, 102:409-415.
9. Dwivedi Y., Rizavi H.S., Conley R.R., Roberts R.C., Tamminga C.A., Pandey G.N. Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch. Gen. Psychiat. 2003, 60:804-815.
10. Felger J.C., Alagbe O., Hu F., Mook D., Freeman A.A., Sanchez M.M., Kalin N.H., Ratti E., Nemeroff C.B., Miller A.H. Effects of interferon-alpha on rhesus monkeys: a nonhuman primate model of cytokine-induced depression. Biol. Psychiat. 2007, 62:1324-1333.
11. Gensel J.C., Schonberg D.L., Alexander J.K., McTigue D.M., Popovich P.G. Semi-automated Sholl analysis for quantifying changes in growth and differentiation of neurons and glia. J. Neurosci. Methods 2010, 190:71-79.
12. Goni-Allo B., Ramos M., Herv'as I., Lasheras B., Aguirre N. Studies on striatal neurotoxicity caused by the 3,4-methylenedioxymethamphetamine/malonate combination: implications for serotonin/dopamine interactions. J. Psychopharmacol. 2006, 20:245-256.
13. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiat. 2008, 13:717-728.
14. Guillemin G.J., Kerr S.J., Pemberton L.A., Smith D.G., Smythe G.A., Armati P.J., Brew B.J. IFN-beta1b induces kynurenine pathway metabolism in human macrophages: potential implications for multiple sclerosis treatment. J. Interferon Cytokine Res. 2001, 21:1097-10101.
15. Gwak Y.S., Crown E.D., Unabia G.C., Hulsebosch C.E. Propentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat. Pain 2008, 138:410-422.
16. Hashimoto K., Sawa A., Iyo M. Increased levels of glutamate in brains from patients with mood disorders. Biol. Psychiat. 2007, 62:1310-1316.
17. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71:171-186.
18. Hunsberger J.G., Newton S.S., Bennett A.H., Duman C.H., Russell D.S., Salton S.R., Duman R.S. Antidepressant actions of the exercise-regulated gene VGF. Nat. Med. 2007, 13:1476-1482.
19. Innamorato N.G., Jazwa A., Rojo A.I., Garcia C., Fernandez-Ruiz J., Grochot-Przeczek A., Stachurska A., Jozkowicz A., Dulak J., Cuadrado A. Different susceptibility to the Parkinson's toxin MPTP in mice lacking the redox master regulator Nrf2 or its target gene heme oxygenase-1. PLoS One 2010, 5:e11838.
20. Innamorato N.G., Rojo A.I., Garcia-Yague A.J., Yamamoto M., de Ceballos M.L., Cuadrado A. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol. 2008, 181:680-689.
21. Irwin M.R., Miller A.H. Depressive disorders and immunity: 20 years of progress and discovery. Brain Behav. Immun. 2007, 21:374-383.
22. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I., Yamamoto M., Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236:313-322.
23. Jain N.K., Kulkarni S.K., Singh A. Lipopolysaccharide-mediated immobility in mice: reversal by cyclooxygenase enzyme inhibitors. Methods Find. Exp. Clin. Pharmacol. 2001, 23:441-444.
24. Jazwa A., Rojo A.I., Innamorato N.G., Hesse M., Fernandez-Ruiz J., Cuadrado A. Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid. Redox Signal. 2011, 14:2347-23460.
25. Kaster M.P., Budni J., Binfare R.W., Santos A.R., Rodrigues A.L. The inhibition of different types of potassium channels underlies the antidepressant-like effect of adenosine in the mouse forced swimming test. Prog. Neuropsychopharmacol. Biol. Psychiat. 2007, 31:690-696.
26. Kaster M.P., Gadotti V.M., Calixto J.B., Santos A.R., Rodrigues A.L. Depressive-like behavior induced by tumor necrosis factor-alpha in mice. Neuropharmacology 2012, 62:419-426.
27. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 2008, 105:751-756.
28. Krishnan V., Han M.H., Graham D.L., Berton O., Renthal W., Russo S.J., Laplant Q., Graham A., Lutter M., Lagace D.C., Ghose S., Reister R., Tannous P., Green T.A., Neve R.L., Chakravarty S., Kumar A., Eisch A.J., Self D.W., Lee F.S., Tamminga C.A., Cooper D.C., Gershenfeld H.K., Nestler E.J. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
29. Lee J.M., Johnson J.A. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J. Biochem. Mol. Biol. 2004, 37:139-143.
30. Maes M. The cytokine hypothesis of depression: inflammation, oxidative & nitrosative stress (IO&NS) and leaky gut as new targets for adjunctive treatments in depression. Neuro. Endocrinol. Lett. 2008, 29:287-291.
31. Maes M., Bosmans E., De Jongh R., Kenis G., Vandoolaeghe E., Neels H. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 1997, 9:853-858.
32. Maes M., Scharpe S., Bosmans E., Vandewoude M., Suy E., Uyttenbroeck W., Cooreman W., Vandervorst C., Raus J. Disturbances in acute phase plasma proteins during melancholia: additional evidence for the presence of an inflammatory process during that illness. Prog. Neuropsychopharmacol. Biol. Psychiat. 1992, 16:501-515.
33. Maes M., Stevens W.J., Declerck L.S., Bridts C.H., Peeters D., Schotte C., Cosyns P. Significantly increased expression of T-cell activation markers (interleukin-2 and HLA-DR) in depression: further evidence for an inflammatory process during that illness. Prog. Neuropsychopharmacol. Biol. Psychiat. 1993, 17:241-255.
34. McNally L., Bhagwagar Z., Hannestad J. Inflammation, glutamate, and glia in depression: a literature review. CNS Spectr. 2008, 13:501-510.
35. Mikova O., Yakimova R., Bosmans E., Kenis G., Maes M. Increased serum tumor necrosis factor alpha concentrations in major depression and multiple sclerosis. Eur. Neuropsychopharmacol. 2001, 11:203-208.
36. Nestler E.J., Carlezon W.A. The mesolimbic dopamine reward circuit in depression. Biol. Psychiat. 2006, 59:1151-1159.
37. Nowacka M.M., Obuchowicz E. Vascular endothelial growth factor (VEGF) and its role in the central nervous system: a new element in the neurotrophic hypothesis of antidepressant drug action. Neuropeptides 2012, 46:1-10.
38. Reichenberg A., Yirmiya R., Schuld A., Kraus T., Haack M., Morag A., Pollmacher T. Cytokine-associated emotional and cognitive disturbances in humans. Arch. Gen. Psychiat. 2010, 58:445-452.
39. Rojo A.I., Innamorato N.G., Martin-Moreno A.M., De Ceballos M.L., Yamamoto M., Cuadrado A. Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 2010, 58:588-598.
40. Rojo A.I., Rada P., Egea J., Rosa A.O., Lopez M.G., Cuadrado A. Functional interference between glycogen synthase kinase-3 beta and the transcription factor Nrf2 in protection against kainate-induced hippocampal cell death. Mol. Cell Neurosci. 2008, 39:125-132.
41. Sakash J.B., Byrne G.I., Lichtman A., Libby P. Cytokines induce indoleamine 2,3-dioxygenase expression in human atheroma-asociated cells: implications for persistent Chlamydophila pneumoniae infection. Infect. Immun. 2002, 70:3959-3961.
42. Schildkraut J.J. The catecholamine hypothesis of affective disorders: a review of supporting evidence. J. Neuropsychiat. Clin. Neurosci. 1965, 7:524-533. discussion 523-4.
43. Singal A., Tirkey N., Chopra K. Reversal of LPS-induced immobility in mice by green tea polyphenols: possible COX-2 mechanism. Phytother. Res. 2004, 18:723-728.
44. Siuciak J.A., Lewis D.R., Wiegand S.J., Lindsay R.M. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol. Biochem. Behav. 1997, 56:131-137.
45. Sluzewska A., Rybakowski J.K., Sobieska M., Bosnians E., Pollet H., Wiktorowicz K. Increased levels of alpha-1-acid glycoprotein and interleukin-6 in refractory depression. Depression 1995, 3:170-175.
46. Smith R.S. The macrophage theory of depression. Med. Hypotheses 1991, 35:298-306.
47. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berlin) 1985, 85:367-370.
48. Thimmulappa R.K., Lee H., Rangasamy T., Reddy S.P., Yamamoto M., Kensler T.W., Biswal S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Invest. 2006, 116:984-995.
49. Warner-Schmidt J.L., Duman R.S. VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4647-4652.
50. Warner-Schmidt J.L., Duman R.S. VEGF as a potential target for therapeutic intervention in depression. Curr. Opin. Pharmacol. 2008, 8:14-19.
51. Yirmiya R., Pollak Y., Morag M., Reichenberg A., Barak O., Avitsur R., Shavit Y., Ovadia H., Weidenfeld J., Morag A., Newman M.E., Pollmacher T. Illness, cytokines, and depression. Ann. N. Y. Acad. Sci. 2000, 917:478-487.
52. Zhao J., Moore A.N., Redell J.B., Dash P.K. Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J. Neurosci. 2007, 27:10240-10248.
53. Zhao X., Sun G., Zhang J., Strong R., Dash P.K., Kan Y.W., Grotta J.C., Aronowski J. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke 2007, 38:3280-3286.