Antidepressant-like effect of ascorbic acid is associated with the modulation of mammalian target of rapamycin pathway

Journal of Psychiatric Research

Volumn 48, Issue 1, 2014, Pages 16-24

  Moretti, Morgana ^a   Budni, Josiane ^a   Freitas, Andiara Espíndola ^a   Rosa, Priscila Batista ^a   Rodrigues, Ana Lúcia S ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Antidepressant; Ascorbic acid; Depression; GSK 3 ; Heme oxygenase; MTOR

Indexed keywords

1 (4 METHOXYBENZYL) 3 (5 NITRO 2 THIAZOLYL)UREA; 2 MORPHOLINO 8 PHENYLCHROMONE; ASCORBIC ACID; DRUG VEHICLE; GLYCOGEN SYNTHASE KINASE 3BETA; HEME OXYGENASE 1; LITHIUM CHLORIDE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN ZINC; RAPAMYCIN; S6 KINASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; EXPERIMENTAL TEST; HIPPOCAMPUS; LOCOMOTION; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TAIL SUSPENSION TEST;

ANTIDEPRESSANT; ASCORBIC ACID; DEPRESSION; GSK-3Β; HEME-OXYGENASE; MTOR;

ANIMALS; ANTIDEPRESSIVE AGENTS; ASCORBIC ACID; DEPRESSION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ENZYME INHIBITORS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GUANYLATE KINASE; HINDLIMB SUSPENSION; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; MALE; MEMBRANE PROTEINS; MICE; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84888435014     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2013.10.014     Document Type: Article

References (60)

1. Amr M., El-Mogy A., Shams T., Vieira K., Lakhan S.E. Efficacy of vitamin C as an adjunct to fluoxetine therapy in pediatric major depressive disorder: a randomized, double-blind, placebo-controlled pilot study. Nutr J 2013, 12.
2. Badr G., Bashandy S., Ebaid H., Mohany M., Sayed D. Notice of disputed authorship to: vitamin C supplementation reconstitutes polyfunctional T cells in streptozotocin-induced diabetic rats. Eur J Nutr 2012, 51:635.
3. Becker J.C., Grosser N., Boknik P., Schroder H., Domschke W., Pohle T. Gastroprotection by vitamin C-a heme oxygenase-1-dependent mechanism?. Biochem Biophys Res Commun 2003, 312:507-512.
4. Berman R.M., Cappiello A., Anand A., Oren D.A., Heninger G.R., Charney D.S., et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000, 47:351-354.
5. Bettio L.E.B., Cunha M.P., Budni J., Pazini F.L., Oliveira A., Colla A.R., et al. Guanosine produces an antidepressant-like effect through the modulation of NMDA receptors, nitric oxide-cGMP and PI3K/mTOR pathways. Behav Brain Res 2012, 234:137-148.
6. Beurel E., Song L., Jope R.S. Inhibition of glycogen synthase kinase-3 is necessary for the rapid antidepressant effect of ketamine in mice. Mol Psychiatry 2011, 16:1068-1070.
7. Binfaré R.W., Rosa A.O., Lobato K.R., Santos A.R., Rodrigues A.L.S. Ascorbic acid administration produces an antidepressant-like effect: evidence for the involvement of monoaminergic neurotransmission. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:530-540.
8. Brody S. High-dose ascorbic acid increases intercourse frequency and improves mood: a randomized controlled clinical trial. Biol Psychiatry 2002, 52:371-374.
9. Budni J., Lobato K.R., Binfaré R.W., Freitas A.E., Costa A.P., Martin-de-Saavedra M.D., et al. Involvement of PI3K, GSK-3beta and PPARgamma in the antidepressant-like effect of folic acid in the forced swimming test in mice. JPsychopharmacol 2012, 26:714-723.
10. Cantley L.C. The phosphoinositide 3-kinase pathway. Sci 2002, 296:1655-1657.
11. Chandran A., Iyo A.H., Jernigan C.S., Legutko B., Austin M.C., Karolewicz B. Reduced phosphorylation of the mTOR signaling pathway components in the amygdala of rats exposed to chronic stress. Prog Neuropsychopharmacol Biol Psychiatry 2013, 40:240-245.
12. Cocchi P., Silenzi M., Calabri G., Salvi G. Antidepressant effect of vitamin C. Pediatrics 1980, 65:862-863.
13. Cordova F.M., Aguiar A.S., Peres T.V., Lopes M.W., Goncalves F.M., Remor A.P., et al. Invivo manganese exposure modulates Erk, Akt and Darpp-32 in the striatum of developing rats, and impairs their motor function. PLoS One 2012, 7:e33057.
14. Coyle J.T., Duman R.S. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 2003, 38:157-160.
15. Dal-Cim T., Molz S., Egea J., Parada E., Romero A., Budni J., et al. Guanosine protects human neuroblastoma SH-SY5Y cells against mitochondrial oxidative stress by inducing heme oxigenase-1 via PI3K/Akt/GSK-3beta pathway. Neurochem Int 2012, 61:397-404.
16. Deschwanden A., Karolewicz B., Feyissa A.M., Treyer V., Ametamey S.M., Johayem A., et al. Reduced metabotropic glutamate receptor 5 density in major depression determined by [C-11]ABP688 PET and postmortem study. Am J Psychiatry 2011, 168:727-734.
17. Dwivedi Y., Rizavi H.S., Teppen T., Zhang H., Mondal A., Roberts R.C., et al. Lower phosphoinositide 3-kinase (PI 3-kinase) activity and differential expression levels of selective catalytic and regulatory PI 3-kinase subunit isoforms in prefrontal cortex and hippocampus of suicide subjects. Neuropsychopharmacol 2008, 33:2324-2340.
18. Dwyer J.M., Lepack A.E., Duman R.S. mTOR activation is required for the antidepressant effects of mGluR(2/3) blockade. Int J Neuropsychopharmacol 2012, 15:429-434.
19. Feyissa A.M., Chandran A., Stockmeier C.A., Karolewicz B. Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:70-75.
20. Frost R.A., Pereyra E., Lang C.H. Ethyl pyruvate preserves IGF-I sensitivity toward mTOR substrates and protein synthesis in C2C12 myotubes. Endocrinol 2011, 152:151-163.
21. Gould T.D., Einat H., Bhat R., Manji H.K. AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int J Neuropsychopharmacol 2004, 7:387-390.
22. Gozzelino R., Jeney V., Soares M.P. Mechanisms of cell protection by heme oxygenase-1. Ann Rev Pharmacol Toxicol 2010, 50:323-354.
23. Helmer K.S., Suliburk J.W., Mercer D.W. Ketamine-induced gastroprotection during endotoxemia: role of heme-oxygenase-1. Dig Dis Sci 2006, 51:1571-1581.
24. Huang Y.N., Wang J.Y., Lee C.T., Lin C.H., Lai C.C., Wang J.Y. L-Ascorbate attenuates methamphetamine neurotoxicity through enhancing the induction of endogenous heme oxygenase-1. Toxicol Appl Pharmacol 2012, 265:241-252.
25. Jernigan C.S., Goswami D.B., Austin M.C., Iyo A.H., Chandran A., Stockmeier C.A., et al. The mTOR signaling pathway in the prefrontal cortex is compromised in major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1774-1779.
26. Jourdi H., Hsu Y.T., Zhou M., Qin Q., Bi X., Baudry M. Positive AMPA receptor modulation rapidly stimulates BDNF release and increases dendritic mRNA translation. JNeurosci 2009, 29:8688-8697.
27. Kaidanovich-Beilin O., Milman A., Weizman A., Pick C.G., Eldar-Finkelman H. Rapid antidepressive-like activity of specific glycogen synthase kinase-3 inhibitor and its effect on beta-catenin in mouse hippocampus. Biol Psychiatry 2004, 55:781-784.
28. Karege F., Perroud N., Burkhardt S., Schwald M., Ballmann E., La Harpe R., et al. Alteration in kinase activity but not in protein levels of protein kinase B and glycogen synthase kinase-3 beta in ventral prefrontal cortex of depressed suicide victims. Biol Psychiatry 2007, 61:240-245.
29. Kaster M.P., Gadotti V.M., Calixto J.B., Santos A.R., Rodrigues A.L.S. Depressive-like behavior induced by tumor necrosis factor-alpha in mice. Neuropharmacol 2012, 62:419-426.
30. Kennedy S.G., Wagner A.J., Conzen S.D., Jordan J., Bellacosa A., Tsichlis P.N., et al. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev 1997, 11:701-713.
31. Khanzode S.D., Dakhale G.N., Khanzode S.S., Saoji A., Palasodkar R. Oxidative damage and major depression: the potential antioxidant action of selective serotonin re-uptake inhibitors. Redox Rep 2003, 8:365-370.
32. Kocanova S., Buytaert E., Matroule J.Y., Piette J., Golab J., de Witte P., et al. Induction of heme-oxygenase 1 requires the p38(MAPK) and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 2007, 12:731-741.
33. Koike H., Iijima M., Chaki S. Involvement of the mammalian target of rapamycin signaling in the antidepressant-like effect of group II metabotropic glutamate receptor antagonists. Neuropharmacol 2011, 61:1419-1423.
34. Ku B.M., Joo Y., Mun J., Roh G.S., Kang S.S., Cho G.J., et al. Heme oxygenase protects hippocampal neurons from ethanol-induced neurotoxicity. Neurosci Lett 2006, 405:168-171.
35. Kuo C.H., Yonehara N., Hata F., Yoshida H. Subcellular distribution of ascorbic acid in rat brain. Jpn J Pharmacol 1978, 28:789-791.
36. Li N., Lee B., Liu R.J., Banasr M., Dwyer J.M., Iwata M., et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Sci 2010, 329:959-964.
37. Li N., Liu R.J., Dwyer J.M., Banasr M., Lee B., Son H., et al. Glutamate N-methyl-d-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol Psychiatry 2011, 69:754-761.
38. Liu R.J., Fuchikami M., Dwyer J.M., Lepack A.E., Duman R.S., Aghajanian G.K. GSK-3 inhibition potentiates the synaptogenic and antidepressant-like effects of subthreshold doses of ketamine. Neuropsychopharmacol 2013, 38:2268-2277.
39. Majewska M.D., Bell J.A., London E.D. Regulation of the NMDA receptor by redox phenomena: inhibitory role of ascorbate. Brain Res 1990, 537:328-332.
40. Moretti M., Budni J., Dos Santos D.B., Antunes A., Daufenbach J.F., Manosso L.M., et al. Protective effects of ascorbic acid on behavior and oxidative status of restraint-stressed mice. JMol Neurosci 2013, 49:68-79.
41. Moretti M., Budni J., Ribeiro C.M., Rodrigues A.L.S. Involvement of different types of potassium channels in the antidepressant-like effect of ascorbic acid in the mouse tail suspension test. Eur J Pharmacol 2012, 687:21-27.
42. Moretti M., Colla A., de Oliveira Balen G., dos Santos D.B., Budni J., de Freitas A.E., et al. Ascorbic acid treatment, similarly to fluoxetine, reverses depressive-like behavior and brain oxidative damage induced by chronic unpredictable stress. JPsychiatr Res 2012, 46:331-340.
43. Moretti M., Freitas A.E., Budni J., Fernandes S.C., Balen Gde O., Rodrigues A.L.S. Involvement of nitric oxide-cGMP pathway in the antidepressant-like effect of ascorbic acid in the tail suspension test. Behav Brain Res 2011, 225:328-333.
44. Nemeroff C.B. The burden of severe depression: a review of diagnostic challenges and treatment alternatives. JPsychiatr Res 2007, 41:189-206.
45. Oh D.H., Park Y.C., Kim S.H. Increased glycogen synthase kinase-3beta mRNA level in the hippocampus of patients with major depression: a study using the stanley neuropathology consortium integrative database. Psychiatry Investig 2010, 7:202-207.
46. Oishi J., Doi H., Kawakami N. Nutrition and depressive symptoms in community-dwelling elderly persons in Japan. Acta Med Okayama 2009, 63:9-17.
47. Peterson G.L. Asimplification of the protein assay method of Lowry etal. which is more generally applicable. Anal Biochem 1977, 83:346-356.
48. Rebec G.V., Pierce R.C. Avitamin as neuromodulator - ascorbate release into the extracellular fluid of the brain regulates dopaminergic and glutamatergic transmission. Progress in Neurobiology 1994, 43:537-565.
49. Rice M.E. Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci 2000, 23:209-216.
50. Rosa A.O., Kaster M.P., Binfaré R.W., Morales S., Martin-Aparicio E., Navarro-Rico M.L., et al. Antidepressant-like effect of the novel thiadiazolidinone NP031115 in mice. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:1549-1556.
51. Rosa K.A., Gadotti V.M., Rosa A.O., Rodrigues A.L.S., Calixto J.B., Santos A.R. Evidence for the involvement of glutamatergic system in the antinociceptive effect of ascorbic acid. Neurosci Lett 2005, 381:185-188.
52. Shi H.S., Zhu W.L., Liu J.F., Luo Y.X., Si J.J., Wang S.J., et al. PI3K/Akt signaling pathway in the basolateral amygdala mediates the rapid antidepressant-like effects of trefoil factor 3. Neuropsychopharmacol 2012, 37:2671-2683.
53. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacol (Berl) 1985, 85:367-370.
54. Suliburk J.W., Ward J.L., Helmer K.S., Adams S.D., Zuckerbraun B.S., Mercer D.W. Ketamine-induced hepatoprotection: the role of heme oxygenase-1. Am J Physiol Gastrointest Liver Physiol 2009, 296:G1360-G1369.
55. Surh Y.J., Kundu J.K., Li M.H., Na H.K., Cha Y.N. Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress. Arch Pharm Res 2009, 32:1163-1176.
56. Takizawa S., Hirabayashi H., Matsushima K., Tokuoka K., Shinohara Y. Induction of heme oxygenase protein protects neurons in cortex and striatum, but not in hippocampus, against transient forebrain ischemia. JCerebral Blood Flow Metabol 1998, 18:559-569.
57. Trivedi M.H., Fava M., Wisniewski S.R., Thase M.E., Quitkin F., Warden D., et al. Medication augmentation after the failure of SSRIs for depression. NEngl J Med 2006, 354:1243-1252.
58. Wang H., Brown J., Gu Z., Garcia C.A., Liang R., Alard P., et al. Convergence of the mammalian target of rapamycin complex 1- and glycogen synthase kinase 3-beta-signaling pathways regulates the innate inflammatory response. JImmunol 2011, 186:5217-5226.
59. Zarate C.A., Singh J.B., Carlson P.J., Brutsche N.E., Ameli R., Luckenbaugh D.A., et al. Arandomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 2006, 63:856-864.
60. Zuo D.Y., Zhang Y.H., Cao Y., Wu C.F., Tanaka M., Wu Y.L. Effect of acute and chronic MK-801 administration on extracellular glutamate and ascorbic acid release in the prefrontal cortex of freely moving mice on line with open-field behavior. Life Sci 2006, 78:2172-2178.