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Combined actions of blueberry extract and lithium on neurochemical changes observed in an experimental model of mania: exploiting possible synergistic effects

  • Luiza Spohr
  • Mayara Sandrielly Pereira Soares
  • Pathise Souto Oliveira
  • Bruna da Silveira de Mattos
  • Natália Pontes Bona
  • Nathalia Stark Pedra
  • Fernanda Cardoso Teixeira
  • Carlus Augustu Tavares do Couto
  • Vitor Clasen Chaves
  • Flávio Henrique Reginatto
  • Meibel Teixeira Lisboa
  • Anderson Schwingel Ribeiro
  • Claiton Leoneti Lencina
  • Francieli Moro Stefanello
  • Roselia Maria Spanevello
Original Article
  • 9 Downloads

Abstract

Bipolar disorder is a psychiatric disease characterized by recurrent episodes of mania and depression. Blueberries contain bioactive compounds with important pharmacological effects such as neuroprotective and antioxidant actions. The aim of this study was to investigate the effects of blueberry extract and/or lithium on oxidative stress, and acetylcholinesterase (AChE) and Na+, K+-ATPase activity in an experimental ketamine-induced model of mania. Male Wistar rats were pretreated with vehicle, blueberry extract (200 mg/kg), and/or lithium (45 mg/kg or 22.5 mg/kg twice daily) for 14 days. Between the 8th and 14th days, the animals also received an injection of ketamine (25 mg/kg) or vehicle. On the 15th day the animals received a single injection of ketamine; after 30 min, the locomotor activity was evaluated in an open field test. Ketamine administration induced an increase in locomotor activity. In the cerebral cortex, hippocampus and striatum, ketamine also induced an increase in reactive oxygen species, lipid peroxidation and nitrite levels, as well a decrease in antioxidant enzyme activity. Pretreatment with blueberry extract or lithium was able to prevent this change. Ketamine increased the AChE and Na+, K+-ATPase activity in brain structures, while the blueberry extract partially prevented these alterations. In addition, our results showed that the neuroprotective effect was not potentiated when lithium and blueberry extract treatment were given together. In conclusion, our findings suggest that blueberry extract has a neuroprotective effect against an experimental model of mania. However, more studies should be performed to evaluate its effects as an adjuvant therapy.

Keywords

Bipolar disorder Hyperlocomotion Anthocyanins Oxidative stress Acetylcholinesterase Na+, K+-ATPase 

Notes

Acknowledgments

This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico and Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS). This study was finaced in part by the Coordenação de Aperfeiçoamento de de Nível Superior - Brasil (CAPES) - Finance code 001.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. Adam-Vizi V (2005) Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid Redox Signal 7:1140–1149.  https://doi.org/10.1089/ars.2005.7.1140 CrossRefPubMedGoogle Scholar
  2. Adam-Vizi V, Chinopoulos C (2006) Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol Sci 27:639–645.  https://doi.org/10.1016/j.tips.2006.10.005 CrossRefPubMedGoogle Scholar
  3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126.  https://doi.org/10.1016/S0076-6879(84)05016-3 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ahn SH, Kim HJ, Jeong I, Hong YJ, Kim MJ, Rhie DJ, Jo YH, Hahn SJ, Yoon SH (2011) Grape seed proanthocyanidin extract inhibits glutamate-induced cell death through inhibition of calcium signals and nitric oxide formation in cultured rat hippocampal neurons. BMC Neurosci 12:1–12.  https://doi.org/10.1186/1471-2202-12-78 CrossRefGoogle Scholar
  5. Aksenov MY, Markesbery WR (2001) Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett 302:141–145.  https://doi.org/10.1016/S0304-3940(01)01636-6 CrossRefPubMedGoogle Scholar
  6. Ali SF, Lebel CP, Bondy SC (1992) Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13:637–648PubMedGoogle Scholar
  7. Andreazza AC, Kauer-Sant'anna M, Frey BN, Bond DJ, Kapczinski F, Young LT, Yatham LN (2008) Oxidative stress markers in bipolar disorder: a meta-analysis. J Affect Disord 111:135–144.  https://doi.org/10.1016/j.jad.2008.04.013 CrossRefPubMedGoogle Scholar
  8. Andreazza AC, Kapczinski F, Kauer-Sant’anna M, Walz JC, Bond DJ, Gonçalves CA, Young LT, Yatham LN (2009) 3-Nitrotyrosine and glutathione antioxidant system in patients in the early and late stages of bipolar disorder. J Psychiatry Neurosci 34:263–271PubMedPubMedCentralGoogle Scholar
  9. Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8:111–120.  https://doi.org/10.1080/10284150500078117 CrossRefPubMedGoogle Scholar
  10. Arnaiz G, Ordieres G (2014) Brain Na+,K+-ATPase activity in aging and disease. Int J Biomed Sci 10:85–102Google Scholar
  11. Bhuiyan MI, Kim HB, Kim SY, Cho KO (2011) The neuroprotective potential of cyanidin-3-glucoside fraction extracted from mulberry following oxygen-glucose deprivation. Korean J Physiol Pharmacol 15:353–361.  https://doi.org/10.4196/kjpp.2011.15.6.353 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bordignon CLJ, Francescatto V, Nienow AA, Calvete E, Reginatto FH (2009) Influência do pH da solução extrativa no teor de antocianinas em frutos de morango. Ciênc Tecnol Aliment 29:183–188.  https://doi.org/10.1590/S0101-20612009000100028 CrossRefGoogle Scholar
  13. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Carvalho FB, Mello CF, Marisco PC, Tonello R, Girardi BA, Ferreira J, Oliveira MS, Rubin MA (2012) Spermidine decreases Na(+),K(+)-ATPase activity through NMDA receptor and protein kinase G activation in the hippocampus of rats. Eur J Pharmacol 684:79–86.  https://doi.org/10.1016/j.ejphar.2012.03.046 CrossRefPubMedGoogle Scholar
  15. Chan KM, Delfert D, Junger KD (1986) A direct colorimetric assay for Ca2+− stimulated activity. Anal Biochem 220:375–380.  https://doi.org/10.1016/0003-2697(86)90640-8 CrossRefGoogle Scholar
  16. Chan WH, Su HC, Hung MH, Sun WZ, Fan SZ, Hsiao PN, Ueng TH (2008) Induction of hepatic glutathione S-transferase and UDP-glucuronosyltransferase activities by ketamine in rats. Acta Anaesthesiol Taiwanica 46:2–7.  https://doi.org/10.1016/S1875-4597(08)60013-2 CrossRefGoogle Scholar
  17. Chen G, Zeng WZ, Yuan PX, Huang LD, Jiang YM, Zhao ZH, Manji HK (1999) The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 72:879–882.  https://doi.org/10.1046/j.1471-4159.1999.720879.x CrossRefPubMedGoogle Scholar
  18. Cho YW (1995) Lithium-induced inhibition of Na+,K+-ATPase and ca+-ATPase activities in rat brain synaptosome. J Korean Med Sci 10:7–13.  https://doi.org/10.3346/jkms.1995.10.1.7 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Choi DY, Lee YJ, Hong JT, Lee HJ (2012) Antioxidant properties of natural polyphenols and their therapeutic potentials for Alzheimer's disease. Brain Res Bull 87:144–153.  https://doi.org/10.1016/j.brainresbull.2011.11.014 CrossRefPubMedGoogle Scholar
  20. Chowdhury MI, Hasan M, Islam MS, Sarwar MS, Amin MN, Uddin SMN, Rahaman MZ, Banik S, Hussain MS, Yokota K, Hasnat A (2017) Elevated serum MDA and depleted non-enzymatic antioxidants, macro-minerals and trace elements are associated with bipolar disorder. J Trace Elem Med Biol 39:162–168.  https://doi.org/10.1016/j.jtemb.2016.09.012 CrossRefPubMedGoogle Scholar
  21. Cummings JL (2000) Cholinesterase inhibitors: expanding applications. Lancet 356:2024–2025.  https://doi.org/10.1016/S0140-6736(00)03393-6 CrossRefPubMedGoogle Scholar
  22. De Oliveira L, Fraga DB, De Luca RD, Canever L, Ghedim FV, Matos MP, Streck EL, Quevedo J, Zugno AI (2011) Behavioral changes and mitochondrial dysfunction in a rat model of schizophrenia induced by ketamine. Metab Brain Dis 26:69–77.  https://doi.org/10.1007/s11011-011-9234-1 CrossRefPubMedGoogle Scholar
  23. Debom G, Gazal M, Soares MSP, Couto CAT, Mattos B, Lencina C, Kaster MP, Ghisleni GC, Tavares R, Braganhol E, Chaves VC, Reginatto FH, Stefanello F, Spanevello RM (2016) Preventive effects of blueberry extract on behavioral and biochemical dysfunctions in rats submitted to a model of manic behavior induced by ketamine. Brain Res Bull 127:260–269.  https://doi.org/10.1016/j.brainresbull.2016.10.008 CrossRefPubMedGoogle Scholar
  24. Del Bo C, Martini D, Porrini M, Klimis-Zacasc D, Riso P (2015) Berries and oxidative stress markers: an overview of human intervention studies. Food Funct 6:2890–2917.  https://doi.org/10.1039/c5fo00657k CrossRefPubMedGoogle Scholar
  25. Dickerson F, Stallings C, Vaughan C, Origoni A, Khushalani S, Yolken R (2012) Antibodies to the glutamate receptor in mania. Bipolar Disord 14:547–553.  https://doi.org/10.1111/j.1399-5618.2012.01028.x CrossRefPubMedGoogle Scholar
  26. Digby GJ, Noetzel MJ, Bubser M, Utley TJ, Walker AG, Byun NE, Lebois EP, Xiang Z, Sheffler DJ, Cho HP, Davis AA, Nemirovsky NE, Mennenga SE, Camp BW, Bimonte-Nelson HA, Bode J, Italiano K, Morrison R, Daniels JS, Niswender CM, Olive MF, Lindsley CW, Jones CK, Conn PJ (2012) Novel allosteric agonists of M1 muscarinic acetylcholine receptors induce brain region-specific responses that correspond with behavioral effects in animal models. J Neurosci 32:8532–8544.  https://doi.org/10.1523/JNEUROSCI.0337-12.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Dobrota D, Matejovicova M, Kurella E, Boldyrev A (1999) Na/K–ATPase under oxidative stress: molecular mechanisms of injury. Cell Mol Neurobiol 19:141–149CrossRefPubMedGoogle Scholar
  28. Duan TT, Tan JW, Yuan Q, Cao J, Zhou QX, Xu L (2013) Acute ketamine induces hippocampal synaptic depression and spatial memory impairment through dopamine D1/D5 receptors. Psychopharmacology 2283:451–461.  https://doi.org/10.1007/s00213-013-3048-2 CrossRefGoogle Scholar
  29. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95.  https://doi.org/10.1016/0006-2952(61)90145-9 CrossRefGoogle Scholar
  30. Erecinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 43:37–71.  https://doi.org/10.1016/0301-0082(94)90015-9 CrossRefPubMedGoogle Scholar
  31. Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421.  https://doi.org/10.1016/0076-6879(90)86134-H CrossRefPubMedGoogle Scholar
  32. Fernandes I, Faria A, Callau C, Freitas V, Mateus N (2014) Bioavailability of anthocyanins and derivatives. J Funct Foods 7:54–56.  https://doi.org/10.1016/j.jff.2013.05.010 CrossRefGoogle Scholar
  33. Ferrars RM, Czank C, Zhang Q, Botting NP, Kroon PA, Cassidy A, Kay CD (2014) The pharmacokinetics of anthocyanins and their metabolites in humans. Br J Pharmacol 171:3268–3282.  https://doi.org/10.1111/bph.12676 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Fornaro M, De Berardis D, Koshy AS, Perna G, Valchera A, Vancampfort D, Stubbs B (2016) Prevalence and clinical features associated with bipolar disorder polypharmacy: a systematic review. Neuropsychiatr Dis Treat 12:719–735.  https://doi.org/10.2147/NDT.S100846 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gazal M, Valente MR, Acosta BA, Kaufmann FN, Braganhol E, Lencina CL, Stefanello FM, Ghisleni G, Kaster MP (2014) Neuroprotective and antioxidant effects of curcumin in a ketamine-induced model of mania in rats. Eur J Pharmacol 5:132–139.  https://doi.org/10.1016/j.ejphar.2013.12.028 CrossRefGoogle Scholar
  36. Ghedim FV, Fraga DB, Deroza PF, Oliveira MB, Valvassori SS, Steckert AV, Budni J, Dal-pizzol F, Quevedo J, Zugno AL (2012) Evaluation of behavioral and neurochemical changes induced by ketamine in rats: implications as an animal model of mania. J Psychiatr Res 46:1569–1575.  https://doi.org/10.1016/j.jpsychires.2012.08.010 CrossRefPubMedGoogle Scholar
  37. Gutierres JM, Carvalho FB, Schetinger MRC, Marisco P, Agostinho P, Rodrigues M, Rubin MA, Schmatz R, Silva CR, Cognato GP, Farias JG, Signor C, Morsch VM, Mazzanti CM, Bogo M, Bonan CD, Spanevello R (2014) Anthocyanins restore behavioral and biochemical changes caused by streptozotocin-induced sporadic dementia of Alzheimer’s type. Life Sci 96:7–17.  https://doi.org/10.1016/j.lfs.2013.11.014 CrossRefPubMedGoogle Scholar
  38. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  39. Halliwell B (2012) Free radicals and antioxidants: updating a personal view. Nutr Rev 70:257–265.  https://doi.org/10.1111/j.1753-4887.2012.00476.x CrossRefPubMedGoogle Scholar
  40. Han K, Kitano-Okada T, Seo J, Kim S, Saski K, Shimada K, Fukushima M (2015) Characterization of anthocyanins and proanthocyanidins of adzuki bean extracts and their antioxidant activity. J Funct Foods 14:692–701.  https://doi.org/10.1016/j.jff.2015.02.018 CrossRefGoogle Scholar
  41. Hemaiswarya S, Kruthiventi K, Doble M (2008) Synergism between natural products and antibiotics against infectious diseases. Phytomedicine 15:639–652.  https://doi.org/10.1016/j.phymed.2008.06.008 CrossRefGoogle Scholar
  42. Jing P, Zhang JY, Ouyang Q, Wu J, Zhang XJ (2012) Lithium treatment induces proteasomal degradation of over-expressed acetylcholinesterase (AChE-S) and inhibit GSK3β. Chem Biol Interact 203:309–313.  https://doi.org/10.1016/j.cbi.2012.08.010 CrossRefPubMedGoogle Scholar
  43. Kamiloglu S, Capanoglu E, Grootaert C, Camp V (2015) Anthocyanin absorption and metabolism by human intestinal Caco-2 cells—a review. Int J Mol Sci 16:21555–21574.  https://doi.org/10.3390/ijms160921555 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kapczinski F, Quevedo J (2016) Transtorno bipolar: teoria e clínica. Artmed, Porto AlegreGoogle Scholar
  45. Kreilaus F, Spiro AS, Hannan AJ, Garner B, Jenner AM (2016) Therapeutic effects of anthocyanins and environmental enrichment in R6/1 Huntington's disease mice. J Huntingtons Dis 5:285–296.  https://doi.org/10.3233/JHD-160204 CrossRefPubMedGoogle Scholar
  46. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275.  https://doi.org/10.1074/jbc.270.46.27489 CrossRefPubMedGoogle Scholar
  47. Machado-Vieira R, Soares JC (2007) Transtornos de humor refratários a tratamento. Rev Bras Psiquiatr 29:48–54.  https://doi.org/10.1590/S1516-44462006005000058 CrossRefGoogle Scholar
  48. Machado-Vieira R, Andreazza AC, Viale CI, Zanatto V, VJr C, Da Silva Vargas R, Kapczinski F, Portela LV, Souza DO, Salvador M, Gentil V (2007) Oxidative stress parameters in unmedicated and treated bipolar subjects during initial manic episode: a possible role for lithium antioxidant effects. Neurosci Lett 421:33–46.  https://doi.org/10.1016/j.neulet.2007.05.016 CrossRefPubMedGoogle Scholar
  49. Manji HK, Moore GJ, Chen G (2000) Lithium up-regulates the cytoprotective protein Bcl-2 in the CNS in vivo: a role for neurotrophic and neuroprotective effects in manic depressive illness. J Clin Psychiatry 61:82–96PubMedGoogle Scholar
  50. Mansur RB, Rizzo LB, Santos CM, Asevedo E, Cunha GR, Noto MN, Pedrini M, Zeni-Graiff M, Gouvea ES, Cordeiro Q, Reininghaus EZ, McIntyre RS, Brietzke E (2016) Bipolar disorder course, impaired glucose metabolism and antioxidant enzymes activities: a preliminary report. J Psychiatr Res 80:38–44.  https://doi.org/10.1016/j.jpsychires.2016.05.014 CrossRefPubMedGoogle Scholar
  51. Marín L, Miguélez E, Villar C, Lombó F (2015) Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int 2015:905–215.  https://doi.org/10.1155/2015/905215 CrossRefGoogle Scholar
  52. McKnight RF, Adida M, Budge K, Stockton S, Goodwin GM, Geddes JR (2012) Lithium toxicity profile: a systematic review and meta-analysis. Lancet 379:721–728.  https://doi.org/10.1016/S0140-6736(11)61516-X CrossRefPubMedGoogle Scholar
  53. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175PubMedGoogle Scholar
  54. Moreno RA, Moreno DH, Ratzke R (2005) Diagnóstico, tratamento e prevenção da mania e da hipomania no transtorno bipolar. Rev Psiquiatr Clin 32:39–48.  https://doi.org/10.1590/S0101-60832005000700007 CrossRefGoogle Scholar
  55. Nabavi SM, Daglia M, Braidy N, Nabavi SF (2017) Natural products, micronutrients, and nutraceuticals for the treatment of depression: a short review. Nutr Neurosci 20:180–194.  https://doi.org/10.1080/1028415X.2015.1103461 CrossRefPubMedGoogle Scholar
  56. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169.  https://doi.org/10.1038/nn.2647 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Obermayer J, Verhoog MB, Luchicchi A, Mansvelder HD (2017) Cholinergic modulation of cortical microcircuits is Layer-specific: evidence from rodent, monkey and human brain. Front Neural Circuit 11.  https://doi.org/10.3389/fncir.2017.00100
  58. Oliveira PS, Chaves VC, Bona NP, Soares MSP, Cardoso JS, Vasconcellos FA, Tavares RG, Vizzotto M, Da Silva LMC, Grecco FB, Gamaro GD, Spanevello RM, Lencina CL, Reginatto FH, Stefanello FM (2017) Eugenia uniflora fruit (red type) standardized extract: a potential pharmacological tool to diet-induced metabolic syndrome damage management. Biomed Pharmacother 92:935–941.  https://doi.org/10.1016/j.biopha.2017.05.131 CrossRefPubMedGoogle Scholar
  59. Papandreou MA, Tsachaki M, Efthimiopoulos S, Cordopatis P, Lamari FN, Margarity M (2011) Memory enhancing effects of saffron in aged mice are correlated with antioxidant protection. Behav Brain Res 219:197–204.  https://doi.org/10.1016/j.bbr.2011.01.007 CrossRefPubMedGoogle Scholar
  60. Phillips ML, Kupfer DJ (2013) Bipolar disorder diagnosis: challenges and future directions. Lancet 381:1663–1671.  https://doi.org/10.1016/S0140-6736(13)60989-7 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pisoschi A, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74.  https://doi.org/10.1016/j.ejmech.2015.04.040 CrossRefPubMedGoogle Scholar
  62. Riobó NA, Clementi E, Melani M, Boveris A, Cadenas E, Moncada S, Poderoso JJ (2001) Nitric oxide inhibits mitochondrial NADH: ubiquinone reductase activity through peroxynitrite formation. Biochem J 359:139–145.  https://doi.org/10.1042/bj3590139 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sagar R, Pattanayak RD (2017) Potential biomarkers for bipolar disorder: where do we stand? Indian J Med Res 145:7–16.  https://doi.org/10.4103/ijmr.IJMR_1386_16 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sigitova E, Fišar Z, Hroudová J, Cikánková T, Raboch J (2016) Biological hypotheses and biomarkers of bipolar disorder. Psychiatry Clin Neurosci 71:77–103.  https://doi.org/10.1111/pcn.12476 CrossRefGoogle Scholar
  65. Smeriglio A, Barreca D, Bellocco E, Trombetta D (2016) Chemistry, pharmacology and health benefits of anthocyanins. Phytother Res 30:1265–1286.  https://doi.org/10.1002/ptr.5642 CrossRefPubMedGoogle Scholar
  66. Sperling LE, Steinert G, Boutter J, Landgraf D, Hescheler J, Pollet D, Layer PG (2008) Characterisation of cholinesterase expression during murine embryonic stem cell differentiation. Chem Biol Interact 175:156–160.  https://doi.org/10.1016/j.cbi.2008.05.034 CrossRefPubMedGoogle Scholar
  67. Stuehr DJ, Nathan CF (1989) Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med 169:1543–1555.  https://doi.org/10.1084/jem.169.5.1543 CrossRefPubMedGoogle Scholar
  68. Tan S, Lam WP, Wai MSM, Yu WA, Yew DT (2012) Chronic ketamine administration modulates midbrain dopamine system in mice. PLoS One 7:439–447.  https://doi.org/10.1371/journal.pone.0043947 CrossRefGoogle Scholar
  69. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84.  https://doi.org/10.1016/j.biocel.2006.07.001 CrossRefGoogle Scholar
  70. Venâncio C, Félix L, Almeida V, Coutinho J, Antunes L, Peixoto F, Summavielle T (2015) Acute ketamine impairs mitochondrial function and promotes superoxide dismutase activity in the rat brain. Anesth Analg 120:320–328.  https://doi.org/10.1213/ANE.0000000000000539 CrossRefPubMedGoogle Scholar
  71. Walker ER, McGee RE, Druss BG (2015) Mortality in mental disorders and global disease burden implications: a systematic review and meta-analysis. JAMA Psychiatry 72:334–341.  https://doi.org/10.1001/jamapsychiatry.2014.2502 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Wang C, Sadovova N, Patterson TA, Zou X, Fu X, Hanig JP, Paule MG, Ali SF, Zhang X, Slikker JW (2008) Protective effects of 7-nitroindazole on ketamine-induced neurotoxicity in rat forebrain culture. Neurotoxicology 29:613–620.  https://doi.org/10.1016/j.neuro.2008.03.007 CrossRefPubMedGoogle Scholar
  73. Wu Y, Zhou Q, Chen X, Li X, Wang Y, Zhang J (2017) Comparison and screening of bioactive phenolic compounds in different blueberry cultivars: evaluation of anti-oxidation and α-glucosidase inhibition effect. Food Res Int 100:312–324.  https://doi.org/10.1016/j.foodres.2017.07.004 CrossRefPubMedGoogle Scholar
  74. Yamaguchi I, Walk SF, Jose PA, Felder RA (1996) Dopamine D2L receptors stimulate Na+,K+-ATPase activity in murine LTK-cells. Mol Pharmacol 49:373–378PubMedGoogle Scholar
  75. Yang ZJ, Torbey M, Li X, Bernardy J, Golden WC, Martin LJ, Koehler RC (2007) Dopamine receptor modulation of hypoxic-ischemic neuronal injury in striatum of newborn piglets. J Cereb Blood Flow Metab 27:1339–1351.  https://doi.org/10.1038/sj.jcbfm.9600440 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yanik M, Vural H, Tutkun H, Zoroğlu SS, Savaş HA, Herken H, Koçyiğit A, Keleş H, Akyol O (2004) The role of the arginine-nitric oxide pathway in the pathogenesis of bipolar affective disorder. Eur Arch Psychiatry Clin Neurosci 254:43–47.  https://doi.org/10.1007/s00406-004-0453-x CrossRefPubMedGoogle Scholar
  77. Zugno AI, Valvassori SS, Scherer EBS, Mattos C, Matté C, Ferreira CL, Rezin GT, Wyse ATS, Quevedo J, Streck EL (2009) Na+,K+-ATPase activity in an animal model of mania. J Neural Transm (Vienna) 116:431–436.  https://doi.org/10.1007/s00702-009-0198-9 CrossRefGoogle Scholar
  78. Zuo DY, Wu YL, Yao WX, Cao Y, Wu CF, Tanaka M (2007) Effect of MK-801 and ketamine on hydroxyl radical generation in the posterior cingulate and retrosplenial cortex of free-moving mice, as determined by in vivo microdialysis. Pharmacol Biochem Behav 86:1–7.  https://doi.org/10.1016/j.pbb.2006.05.010 CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Luiza Spohr
    • 1
  • Mayara Sandrielly Pereira Soares
    • 1
  • Pathise Souto Oliveira
    • 1
  • Bruna da Silveira de Mattos
    • 1
  • Natália Pontes Bona
    • 1
  • Nathalia Stark Pedra
    • 1
  • Fernanda Cardoso Teixeira
    • 1
  • Carlus Augustu Tavares do Couto
    • 1
  • Vitor Clasen Chaves
    • 2
  • Flávio Henrique Reginatto
    • 2
  • Meibel Teixeira Lisboa
    • 3
  • Anderson Schwingel Ribeiro
    • 3
  • Claiton Leoneti Lencina
    • 4
  • Francieli Moro Stefanello
    • 1
  • Roselia Maria Spanevello
    • 1
  1. 1.Programa de Pós-Graduação em Bioquímica e Bioprospecção, Centro de Ciências Químicas, Farmacêuticas e de AlimentosUniversidade Federal de PelotasPelotasBrazil
  2. 2.Programa de Pós-Graduação em Biotecnologia e BiociênciasUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  3. 3.Programa de Pós-Graduação em Química, Centro de Ciências Químicas, Farmacêuticas e de Alimentos, Laboratório de Metrologia QuímicaUniversidade Federal de PelotasPelotasBrazil
  4. 4.Curso de Farmácia, Centro de Ciências Químicas, Farmacêuticas e de AlimentosUniversidade Federal de PelotasPelotasBrazil

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