Psidium Exotic and Native Species from Brazil Abolish Depression-like Behavior and Oxidative Stress induced by Corticosterone in Mice

Abstract

Depression is a highly prevalent neuropsychiatric disorder worldwide. One currently accepted hypothesis of this pathogenesis is the hypothalamic–pituitary–adrenal axis dysfunction, which involves oxidative stress and brain damage. Therefore, antioxidants, such as phenolic compounds, could be used in depression. In this study, we investigated the antidepressant-like and antioxidant effects of an aqueous extract of the leaves of three species of the genus Psidium, Myrtaceae family, in mice. The exotic Psidium guajava L. and the natives Psidium guineense Sw. and Psidium cattleianum Sabine (10, 1, and 0.1 mg/kg, respectively) and fluoxetine (10 mg/kg) were administered orally (p. o.) once daily for 21 days, with or without corticosterone (20 mg/kg). After behavioral assessments (tail suspension, splash, and open-field tests), the hippocampus, prefrontal cortex, liver, kidneys, and plasma were examined to determine the oxidative stress status. The three extracts and fluoxetine treatment decreased the immobility time and counteracted the oxidative stress induced by corticosterone administration. The phenolic compounds identified as major components of the extracts, quercetin in P. guajava and P. guineense and o-coumaric acid in P. cattleianum, may be involved in the biological activities. Therefore, the aqueous leaf extracts of P. guajava, P. cattleianum, and P. guineense could be potential antidepressants helpful in treating depression and other diseases with elevated nitro-oxidative stress.

Keywords

antidepressant - corticosterone - Psidium cattleianum - Psidium guajava - Psidium guineense - Myrtaceae

Publication History

Received: 28 February 2024

Accepted after revision: 27 August 2024

Accepted Manuscript online:
27 August 2024

Article published online:
18 September 2024

• References

• 1 WHO. Depressive Disorder (Depression). Geneva: World Health Organization; 2023. Accessed May 21, 2024 at: https://www.who.int/news-room/fact-sheets/detail/depression
• 2 Otte C, Gold SM, Penninx BW, Pariante CM, Etkin A, Fava M, Mohr DC, Schatzberg AF. Major depressive disorder. Nat Rev Dis Primers 2016; 2: 1-21
• 3 Umehara H, Numata S, Watanabe SY, Hatakeyama Y, Kinoshita M, Tomioka Y, Nakahara K, Nikawa T, Ohmori T. Altered KYN/TRP, Gln/Glu, and Met/methionine sulfoxide ratios in the blood plasma of medication-free patients with major depressive disorder. Sci Rep 2017; 7: 1-8
• 4 Maric NP, Adzic M. Pharmacological modulation of HPA axis in depression New avenues for potential therapeutic benefits. Psychiatr Danub 2013; 25: 299-305
• 5 Maes M, Galecki P, Chang YS, Berk M. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35: 676-692
• 6 Maurya PK, Noto C, Rizzo LB, Rios AC, Nunes SO, Barbosa DS, Sethi S, Zeni M, Mansur RB, Maes M, Brietzke E. The role of oxidative and nitrosative stress in accelerated aging and major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2016; 65: 134-144
• 7 Spiers JG, Chen HJC, Sernia C, Lavidis NA. Activation of the hypothalamic-pituitary-adrenal stress axis induces cellular oxidative stress. Front Neurosci 2015; 9: 1-6
• 8 Weng L, Guo X, Li Y, Yang X, Han Y. Apigenin reverses depression-like behavior induced by chronic corticosterone treatment in mice. Eur J Pharmacol 2016; 774: 50-54
• 9 Vaváková M, Ďuračková Z, Trebatická J. Markers of oxidative stress and neuroprogression in depression disorder. Oxid Med Cell Longev 2015; 16: 259-264
• 10 Evans-Lacko S, Aguilar-Gaxiola S, Al-Hamzawi A, Alonso J, Benjet C, Bruffaerts R, Chiu WT, Florescu S, de Girolamo G, Gureje O, Haro JM, He Y, Hu C, Karam EG, Kawakami N, Lee S, Lund C, Kovess-Masfety V, Levinson D, Navarro-Mateu F, Pennell BE, Sampson NA, Scott KM, Tachimori H, Ten Have M, Viana MC, Williams DR, Wojtyniak BJ, Zarkov Z, Kessler RC, Chatterji S, Thornicroft G. Socio-economic variations in the mental health treatment gap for people with anxiety, mood, and substance use disorders: results from the WHO World Mental Health (WMH) surveys. Psychol Med 2018; 48: 1560-1571
• 11 Grundmann O, Lv Y, Kelber O, Butterweck V. Mechanism of St. Johnʼs wort extract (STW3-VI) during chronic restraint stress is mediated by the interrelationship of the immune, oxidative defense, and neuroendocrine system. Neuropharmacology 2010; 58: 767-773
• 12 Nikfarjam M, Rakhshan R, Ghaderi H. Comparison of effect of Lavandula officinalis and venlafaxine in treating depression: A double blind clinical trial. J Clin Diagn Res 2017; 11: KC01-KC04
• 13 Santos LS, Alves Filho EG, Ribeiro PRV, Zocolo GJ, Silva SM, de Lucena EPP, Alves RE, de Brito ES. Chemotaxonomic evaluation of different species from the Myrtaceae family by UPLC-qToF/MS-MS coupled to supervised classification based on genus. Biochem Syst Ecol 2020; 90: 104028
• 14 Cavichioli N, Dalmagro AP, Sasse OR, Junges LH, Rebelo AM, Reinke CK, Zeni ALB. Antidepressant-like effect and phenolic profile of Brazilian native and exotic species from Psidium genus . Chem Biodivers 2022; 19: e202200242
• 15 Koriem KMM, Arbid MS, Saleh HN. Antidiarrheal and protein conservative activities of Psidium guajava in diarrheal rats. J Integr Med 2019; 17: 57-65
• 16 Ojewole JAO. Antiinflammatory and analgesic effects of Psidium guajava Linn. (Myrtaceae) leaf aqueous extract in rats and mice. Methods Find Exp Clin Pharmacol 2006; 28: 441-446
• 17 Tella T, Masola B, Mukaratirwa S. The effect of Psidium guajava aqueous leaf extract on liver glycogen enzymes, hormone sensitive lipase and serum lipid profile in diabetic rats. Biomed Pharmacother 2019; 109: 2441-2446
• 18 Alvarenga FQ, Mota BCF, Leite MN, Fonseca JM, Oliveira DA, de Royo VA, Silva MLA, Esperandim V, Borges A, Laurentiz RS. In vivo analgesic activity, toxicity and phytochemical screening of the hydroalcoholic extract from the leaves of Psidium cattleianum Sabine. J Ethnopharmacol 2013; 150: 280-284
• 19 Brighenti FL, Gaetti-Jardim E, Danelon M, Evangelista GV, Delbem ACB. Effect of Psidium cattleianum leaf extract on enamel demineralisation and dental biofilm composition in situ . Arch Oral Biol 2012; 57: 1034-1040
• 20 Camargo A, Dalmagro AP, Rikel L, da Silva EB, Simão da Silva KAB, Zeni ALB. Cholecalciferol counteracts depressive-like behavior and oxidative stress induced by repeated corticosterone treatment in mice. Eur J Pharmacol 2018; 833: 451-461
• 21 Nguyen ET, Streicher J, Berman S, Caldwell JL, Ghisays V, Estrada CM, Wulsin AC, Solomon MB. A mixed glucocorticoid/mineralocorticoid receptor modulator dampens endocrine and hippocampal stress responsivity in male rats. Physiol Behav 2017; 178: 82-92
• 22 Freitas AE, Egea J, Buendia I, Gómez-Rangel V, Parada E, Navarro E, Casas AI, Wojnicz A, Ortiz JA, Cuadrado A, Ruiz-Nuño A, Rodrigues ALS, Lopez MG. Agmatine, by improving neuroplasticity markers and inducing Nrf2, prevents corticosterone-induced depressive-like behavior in mice. Mol Neurobiol 2016; 53: 3030-3045
• 23 Pazini FL, Cunha MP, Azevedo D, Rosa JM, Colla A, de Oliveira J, Ramos-Hryb AB, Brocardo PS, Gil-Mohapel J, Rodrigues ALS. Creatine prevents corticosterone-Induced reduction in hippocampal proliferation and differentiation: possible implication for its antidepressant effect. Mol Neurobiol 2017; 54: 6245-6260
• 24 Dalmagro AP, Camargo A, Pedron NB, Garcia SAM, Zeni ALB. Morus nigra leaves extract revokes the depressive-like behavior, oxidative stress, and hippocampal damage induced by corticosterone: A pivotal role of the phenolic syringic acid. Behav Pharmacol 2020; 31: 397-406
• 25 Zeni ALB, Camargo A, Dalmagro AP. Ferulic acid reverses depression-like behavior and oxidative stress induced by chronic corticosterone treatment in mice. Steroids 2017; 125: 131-136
• 26 Zeni ALB, Camargo A, Dalmagro AP. Lutein prevents corticosterone-induced depressive-like behavior in mice with the involvement of antioxidant and neuroprotective activities. Pharmacol Biochem Behav 2019; 179: 63-72
• 27 Klinedinst NJ, Regenold WT. A mitochondrial bioenergetic basis of depression. J Bioenerg Biomembr 2015; 47: 155-171
• 28 Gibson SA, Korade Ž, Shelton RC. Oxidative stress and glutathione response in tissue cultures from persons with major depression. J Psychiatr Res 2012; 46: 1326-1332
• 29 Ng F, Berk M, Dean O, Bush AI. Oxidative stress in psychiatric disorders: Evidence base and therapeutic implications. Int J Neuropsychopharmacol 2008; 11: 851-876
• 30 Rebai R, Jasmin L, Boudah A. The antidepressant effect of melatonin and fluoxetine in diabetic rats is associated with a reduction of the oxidative stress in the prefrontal and hippocampal cortices. Brain Res Bull 2017; 134: 142-150
• 31 Ribaudo G, Bortoli M, Ongaro A, Oselladore E, Gianoncelli A, Zagotto G, Orian L. Fluoxetine scaffold to design tandem molecular antioxidants and green catalysts. RSC Adv 2020; 10: 18583-18593
• 32 Camargo A, Dalmagro AP, Rebelo AM, Reinke CK, Zeni ALB. Phenolic profile, antidepressant-like and neuroprotective effects of Maclura tinctoria leaves extract. Nat Prod Res 2022; 36: 4692-4695
• 33 Gupta D, Radhakrishnan M, Kurhe Y. Effect of a novel 5-HT3 receptor antagonist 4i, in corticosterone-induced depression-like behavior and oxidative stress in mice. Steroids 2015; 96: 95-102
• 34 Perić I, Costina V, Stanisavljević A, Findeisen P, Filipovic D. Proteomic characterization of hippocampus of chronically socially isolated rats treated with fluoxetine: Depression-like behaviour and fluoxetine mechanism of action. Neuropharmacology 2018; 135: 268-283
• 35 Lenzi J, Rodrigues AF, Rós AS, de Castro AB, de Lima DD, Magro DDD, Zeni ALB. Ferulic acid chronic treatment exerts antidepressant-like effect: Role of antioxidant defense system. Metab Brain Dis 2015; 30: 1453-1463
• 36 Mehta V, Parashar A, Udayabanu M. Quercetin prevents chronic unpredictable stress induced behavioral dysfunction in mice by alleviating hippocampal oxidative and inflammatory stress. Physiol Behav 2017; 171: 69-78
• 37 Lee B, Sur B, Kwon S, Yeom M, Shim I, Lee H, Hahm DH. Chronic administration of catechin decreases depression and anxiety-like behaviors in a rat model using chronic corticosterone injections. Biomol Ther 2013; 21: 313-322
• 38 Zhu JX, Shan JL, Hu WQ, Zeng JX, Shu JC. Gallic acid activates hippocampal BDNF-Akt-mTOR signaling in chronic mild stress. Metab Brain Dis 2019; 34: 93-101
• 39 Saber FR, Abdelbary GA, Salama MM, Saleh DO, Fathy MM, Soliman FM. UPLC/QTOF/MS profiling of two Psidium species and the in-vivo hepatoprotective activity of their nano-formulated liposomes. Food Res Int 2018; 105: 1029-1038
• 40 Steru L, Chermat R, Thierry B, Simon P. The tail suspension test: A new method for screening antidepressants in mice. Psychopharmacology (Berl) 1985; 85: 367-370
• 41 Willner P. Chronic mild stress (CMS) revisited: Consistency and behavioural- neurobiological concordance in the effects of CMS. Neuropsychobiology 2005; 52: 90-110
• 42 Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-358
• 43 Reznick AZ, Packer L. Oxidative damage to proteins: Spectrophotometric method for carbonyl assay. Methods Enzymol 1994; 233: 357-363
• 44 Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959; 82: 70-77
• 45 Weselsky P, Benedikt R. Ueber einige azoverbindungen. Ber Dtsch Chem Ges 1879; 12: 226-230
• 46 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275