Skip to main content
Top
Published in: Metabolic Brain Disease 5/2018

01-10-2018 | Original Article

The antioxidant gallic acid induces anxiolytic-, but not antidepressant-like effect, in streptozotocin-induced diabetes

Authors: Mariana Machado Pereira, Helen de Morais, Eldevan dos Santos Silva, Claudia Rita Corso, Eliana Rezende Adami, Rose Maria Carlos, Alexandra Acco, Janaina Menezes Zanoveli

Published in: Metabolic Brain Disease | Issue 5/2018

Login to get access

Abstract

The physiopathology of anxiety or depression related to diabetes is still poorly understood. The treatment with antidepressant drugs is a huge challenge due to theirs adherence low rate and many adverse effects. Thus, the seeking for a better treatment for these associated diseases is of utmost importance. Given that the oxidative stress in different tissues occurs in diabetes and anxiety or depression as well, the antioxidant gallic acid becomes an interesting compound to be investigated. Thus, the effects of long-term treatment with gallic acid (0, 10, 20 and 40 mg/kg; gavage) were evaluated in diabetic (DBT) animals submitted to the elevated plus-maze (EPM), the light-dark transition (LDT) tests and modified forced swim test (mFST). Also, indirect parameters of oxidative stress, lipid peroxidation (LPO) and reduced glutathione (GSH) levels were evaluated in the hippocampus (HIP) and prefrontal cortex (PFC). The results showed that DBT animals presented a decrease in the spent time in the open arms, in the end arm exploration and head dips when evaluated in the EPM test; moreover, a decrease in the spent time in the lit compartment of LDT test was observed, suggesting an anxiogenic-like behavior. During the mFST, an increase in the mean counts of immobility and a decrease in the mean counts of swimming and climbing were observed, indicating a depressive-like behavior. These aversive behaviors were more pronounced when compared to normoglycemic (NGL) animals and streptozotocin-treated animals that not become DBT. In addition, DBT rats showed an increase in the oxidative stress parameters in the HIP and PFC that was reversed by the gallic acid treatment (lowest dose - 10 mg/kg), i.e., the treatment decreased the elevated LPO levels and increased the reduced GSH in the HIP and PFC. Also, gallic acid treatment was able to produce an anxiolytic-like effect in the EPM and LDT tests, but not antidepressant–like effect in the FST. Taken together, the results suggest that the antioxidant/neuroprotective effect of gallic acid treatment in HIP and PFC of DBT animals may be essential to the anxiolytic-like effect.
Literature
go back to reference Aksu I, Ates M, Baykara B et al (2012) Anxiety correlates to decreased blood and prefrontal cortex IGF-1 levels in streptozotocin induced diabetes. Neurosci Lett 531:176–181CrossRefPubMed Aksu I, Ates M, Baykara B et al (2012) Anxiety correlates to decreased blood and prefrontal cortex IGF-1 levels in streptozotocin induced diabetes. Neurosci Lett 531:176–181CrossRefPubMed
go back to reference Anderson RJ, Freedland KE, Clouse RE et al (2001) The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care 24:1069–1078CrossRefPubMed Anderson RJ, Freedland KE, Clouse RE et al (2001) The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care 24:1069–1078CrossRefPubMed
go back to reference Anwer T, Sharma M, Pillai KK et al (2012) Protective effect of Withania somnifera against oxidative stress and pancreatic β-cell damage in type 2 diabetic rats. Acta Pol Pharm Drug Res 69:1095–1101 Anwer T, Sharma M, Pillai KK et al (2012) Protective effect of Withania somnifera against oxidative stress and pancreatic β-cell damage in type 2 diabetic rats. Acta Pol Pharm Drug Res 69:1095–1101
go back to reference Aswar U, Chepurwar S, Shintre S et al (2017) Telmisartan attenuates diabetes induced depression in rats. Pharmacol Rep 69:358–364CrossRefPubMed Aswar U, Chepurwar S, Shintre S et al (2017) Telmisartan attenuates diabetes induced depression in rats. Pharmacol Rep 69:358–364CrossRefPubMed
go back to reference Baburao JA, Anand JV (2012) Vitamin E, its beneficial role in diabetes mellitus (DM) and its complications. J Clin Diagn Res 6:1624–1628 Baburao JA, Anand JV (2012) Vitamin E, its beneficial role in diabetes mellitus (DM) and its complications. J Clin Diagn Res 6:1624–1628
go back to reference Bambolkar S, Sainani GS (1995) Evaluation of oxidative stress in diabetics with or without vascular complications. J Assoc Physicians India 43:10–12PubMed Bambolkar S, Sainani GS (1995) Evaluation of oxidative stress in diabetics with or without vascular complications. J Assoc Physicians India 43:10–12PubMed
go back to reference Bilici M, Efe H, Koroglu MA et al (2001) Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 6:43–51CrossRef Bilici M, Efe H, Koroglu MA et al (2001) Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 6:43–51CrossRef
go back to reference Blois MS (1958) Antioxidant determinations by use of a stable free radical. Nature 181:1199–1200CrossRef Blois MS (1958) Antioxidant determinations by use of a stable free radical. Nature 181:1199–1200CrossRef
go back to reference Borsini F, Podhorna J, Marazziti D (2002) Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 163:121–124CrossRefPubMed Borsini F, Podhorna J, Marazziti D (2002) Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 163:121–124CrossRefPubMed
go back to reference Bouayed J, Rammal H, Soulimani R (2009) Oxidative stress and anxiety: relationship and cellular pathways. Oxidative Med Cell Longev 2:63–67CrossRef Bouayed J, Rammal H, Soulimani R (2009) Oxidative stress and anxiety: relationship and cellular pathways. Oxidative Med Cell Longev 2:63–67CrossRef
go back to reference Caiaffo V, Oliveira BDR, De Sá FB et al (2016) Anti-inflammatory, antiapoptotic, and antioxidant activity of fluoxetine. Pharma Res Per 4:231 Caiaffo V, Oliveira BDR, De Sá FB et al (2016) Anti-inflammatory, antiapoptotic, and antioxidant activity of fluoxetine. Pharma Res Per 4:231
go back to reference Caletti G, Olguins DB, Pedrollo EF et al (2012) Antidepressant effect of taurine in diabetic rats. Amino Acids 43:1525–1533CrossRefPubMed Caletti G, Olguins DB, Pedrollo EF et al (2012) Antidepressant effect of taurine in diabetic rats. Amino Acids 43:1525–1533CrossRefPubMed
go back to reference Can OD, Oztürk Y, Ozkay UD (2011) Effects of insulin and St. John's wort treatments on anxiety, locomotory activity, depression, and active learning parameters of streptozotocin-diabetic rats. Planta Med 77:1970–1976CrossRefPubMed Can OD, Oztürk Y, Ozkay UD (2011) Effects of insulin and St. John's wort treatments on anxiety, locomotory activity, depression, and active learning parameters of streptozotocin-diabetic rats. Planta Med 77:1970–1976CrossRefPubMed
go back to reference Champaneri S, Wand GS, Malhotra SS et al (2010) Biological basis of depression in adults with diabetes. Curr Diab Rep 10:396–405CrossRefPubMed Champaneri S, Wand GS, Malhotra SS et al (2010) Biological basis of depression in adults with diabetes. Curr Diab Rep 10:396–405CrossRefPubMed
go back to reference Chen F, Wu AB, Chen CY (2004) The influence of treatments on the free radical scavenging activity of burdock and variations of its activity. Food Chem 86:479–484CrossRef Chen F, Wu AB, Chen CY (2004) The influence of treatments on the free radical scavenging activity of burdock and variations of its activity. Food Chem 86:479–484CrossRef
go back to reference Chhillar R, Dhingra D (2013) Antidepressant-like activity of gallic acid in mice subjected to unpredictable chronic mild stress. Fundam Clin Pharmacol 27:409–418CrossRefPubMed Chhillar R, Dhingra D (2013) Antidepressant-like activity of gallic acid in mice subjected to unpredictable chronic mild stress. Fundam Clin Pharmacol 27:409–418CrossRefPubMed
go back to reference Clavijo M, Carvalho JJ, Rios M et al (2006) Psychiatric disorders in patients with diabetes type 2 at medical care and training district of Rio Branco-Acre. Brazil. Arq Neuropsiquiatr 64:807–813CrossRefPubMed Clavijo M, Carvalho JJ, Rios M et al (2006) Psychiatric disorders in patients with diabetes type 2 at medical care and training district of Rio Branco-Acre. Brazil. Arq Neuropsiquiatr 64:807–813CrossRefPubMed
go back to reference Collins MM, Corcoran P, Perry IJ (2009) Anxiety and depression symptoms in patients with diabetes. Diabet Med 26:153–161CrossRefPubMed Collins MM, Corcoran P, Perry IJ (2009) Anxiety and depression symptoms in patients with diabetes. Diabet Med 26:153–161CrossRefPubMed
go back to reference Cryan JF, Markou A, Lucki I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23:238–245CrossRefPubMed Cryan JF, Markou A, Lucki I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23:238–245CrossRefPubMed
go back to reference da Silva Dias IC, Carabelli B, Ishii DK et al (2016) Indoleamine-2,3- Dioxygenase/Kynurenine pathway as a potential pharmacological target to treat depression associated with diabetes. Mol Neurobiol 53:6997–7009CrossRefPubMed da Silva Dias IC, Carabelli B, Ishii DK et al (2016) Indoleamine-2,3- Dioxygenase/Kynurenine pathway as a potential pharmacological target to treat depression associated with diabetes. Mol Neurobiol 53:6997–7009CrossRefPubMed
go back to reference de Morais H, de Souza CP, da Silva LM et al (2014) Increased oxidative stress in prefrontal cortex and hippocampus is related to depressive-like behavior in streptozotocin-diabetic rats. Behav Brain Res 258:52–64CrossRefPubMed de Morais H, de Souza CP, da Silva LM et al (2014) Increased oxidative stress in prefrontal cortex and hippocampus is related to depressive-like behavior in streptozotocin-diabetic rats. Behav Brain Res 258:52–64CrossRefPubMed
go back to reference de Morais H, de Souza CP, da Silva LM et al (2016) Anandamide reverses depressive-like behavior, neurochemical abnormalities and oxidative-stress parameters in streptozotocin-diabetic rats: Role of CB1 receptors. Eur Neuropsychopharmacol 26:1590–1600CrossRefPubMed de Morais H, de Souza CP, da Silva LM et al (2016) Anandamide reverses depressive-like behavior, neurochemical abnormalities and oxidative-stress parameters in streptozotocin-diabetic rats: Role of CB1 receptors. Eur Neuropsychopharmacol 26:1590–1600CrossRefPubMed
go back to reference Dhingra D, Chhillar R, Gupta A (2012) Antianxiety-like activity of gallic acid in unstressed and stressed mice: possible involvement of nitriergic system. Neurochem Res 37(3):487–494CrossRefPubMed Dhingra D, Chhillar R, Gupta A (2012) Antianxiety-like activity of gallic acid in unstressed and stressed mice: possible involvement of nitriergic system. Neurochem Res 37(3):487–494CrossRefPubMed
go back to reference Dipnal JF, Pasco JA, Meyer D et al (2015) The association between dietary patterns, diabetes and depression. J Affect Disord 174:215–224CrossRef Dipnal JF, Pasco JA, Meyer D et al (2015) The association between dietary patterns, diabetes and depression. J Affect Disord 174:215–224CrossRef
go back to reference Egede LE, Ellis C (2010) Diabetes and depression: global perspectives. Diabetes Res Clin Pract 87:302–312CrossRefPubMed Egede LE, Ellis C (2010) Diabetes and depression: global perspectives. Diabetes Res Clin Pract 87:302–312CrossRefPubMed
go back to reference Gambeta E, de Souza CP, de Morais H et al (2016) Reestablishment of the hyperglycemia to the normal levels seems not to be essential to the anxiolytic-like effect induced by insulin. Metab Brain Dis 31:563–571CrossRefPubMed Gambeta E, de Souza CP, de Morais H et al (2016) Reestablishment of the hyperglycemia to the normal levels seems not to be essential to the anxiolytic-like effect induced by insulin. Metab Brain Dis 31:563–571CrossRefPubMed
go back to reference Gasparovic AC, Lovakovic T, Zarkovic N (2010) Oxidative stress and antioxidants: biological response modifiers of oxidative homeostasis in cancer. Period Biol 112:433–439 Gasparovic AC, Lovakovic T, Zarkovic N (2010) Oxidative stress and antioxidants: biological response modifiers of oxidative homeostasis in cancer. Period Biol 112:433–439
go back to reference Gomez R, Barros HM (2000) Ethopharmacology of the antidepressant effect of clonazepam in diabetic rats. Pharmacol Biochem Behav 66:329–335CrossRefPubMed Gomez R, Barros HM (2000) Ethopharmacology of the antidepressant effect of clonazepam in diabetic rats. Pharmacol Biochem Behav 66:329–335CrossRefPubMed
go back to reference Grigsby AB, Anderson RJ, Freedland KE et al (2002) Prevalence of anxiety in adults with diabetes: a systematic review. J Psychosom Rev 53:1053–1060CrossRef Grigsby AB, Anderson RJ, Freedland KE et al (2002) Prevalence of anxiety in adults with diabetes: a systematic review. J Psychosom Rev 53:1053–1060CrossRef
go back to reference Gupta D, Kurhe Y, Radhakrishnan M (2014) Antidepressant effects of insulin in streptozotocin induced diabetic mice: Modulation of brain serotonin system. Physiol Behav 129:73–78CrossRefPubMed Gupta D, Kurhe Y, Radhakrishnan M (2014) Antidepressant effects of insulin in streptozotocin induced diabetic mice: Modulation of brain serotonin system. Physiol Behav 129:73–78CrossRefPubMed
go back to reference Herken H, Gurel A, Selek S et al (2007) Adenosine deaminase, nitric oxide, superoxide dismutase, and xanthine oxidase in patients with major depression: impact of antidepressant treatment. Arch Med Res 38:247–252CrossRefPubMed Herken H, Gurel A, Selek S et al (2007) Adenosine deaminase, nitric oxide, superoxide dismutase, and xanthine oxidase in patients with major depression: impact of antidepressant treatment. Arch Med Res 38:247–252CrossRefPubMed
go back to reference Huether G, Schuff-Werner P (1996) Platelet serotonin acts as a locally releasable antioxidant. Adv Exp Med Biol 398:299–306CrossRefPubMed Huether G, Schuff-Werner P (1996) Platelet serotonin acts as a locally releasable antioxidant. Adv Exp Med Biol 398:299–306CrossRefPubMed
go back to reference Inoue M, Suzuki R, Sakaguchi N et al (1995) Selective induction of cell death in cancer cells by gallic acid. Biol Pharm Bull 18:1526–1530CrossRefPubMed Inoue M, Suzuki R, Sakaguchi N et al (1995) Selective induction of cell death in cancer cells by gallic acid. Biol Pharm Bull 18:1526–1530CrossRefPubMed
go back to reference Jiang ZY, Woollard AC, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856CrossRefPubMed Jiang ZY, Woollard AC, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856CrossRefPubMed
go back to reference Kade IJ, Rocha JB (2013) Gallic acid modulates cerebral oxidative stress conditions and activities of enzyme-dependent signaling systems in streptozotocin-treated rats. Neurochem Res 38:761–771CrossRefPubMed Kade IJ, Rocha JB (2013) Gallic acid modulates cerebral oxidative stress conditions and activities of enzyme-dependent signaling systems in streptozotocin-treated rats. Neurochem Res 38:761–771CrossRefPubMed
go back to reference Kamei J, Miyata S, Morita K et al (2003) Effects of selective serotonin reuptake inhibitors on immobility time in the tail suspension test in streptozotocin-induced diabetic mice. Pharmacol Biochem Behav 75:247–254CrossRefPubMed Kamei J, Miyata S, Morita K et al (2003) Effects of selective serotonin reuptake inhibitors on immobility time in the tail suspension test in streptozotocin-induced diabetic mice. Pharmacol Biochem Behav 75:247–254CrossRefPubMed
go back to reference Kanazawa LKS, Vecchia DD, Wendler EM et al (2016) Quercetin reduces manic-like behavior and brain oxidative stress induced by paradoxical sleep deprivation in mice. Free Radic Biol Med 99:79–86CrossRefPubMed Kanazawa LKS, Vecchia DD, Wendler EM et al (2016) Quercetin reduces manic-like behavior and brain oxidative stress induced by paradoxical sleep deprivation in mice. Free Radic Biol Med 99:79–86CrossRefPubMed
go back to reference Khanzode SD, Dakhale GN, Khanzode SS et al (2003) Oxidative damage and major depression: the potential antioxidant action of selective serotonin re-uptake inhibitors. Redox Rep 8:365–370CrossRefPubMed Khanzode SD, Dakhale GN, Khanzode SS et al (2003) Oxidative damage and major depression: the potential antioxidant action of selective serotonin re-uptake inhibitors. Redox Rep 8:365–370CrossRefPubMed
go back to reference Kim DO, Lee KW, Lee HJ et al (2002) Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J Agric Food Chem 50:3713–3717CrossRefPubMed Kim DO, Lee KW, Lee HJ et al (2002) Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J Agric Food Chem 50:3713–3717CrossRefPubMed
go back to reference Kroes BH, van den Berg AJ, Quarles van Ufford HC et al (1992) Anti-inflammatory activity of gallic acid. Planta Med 58:499–504CrossRefPubMed Kroes BH, van den Berg AJ, Quarles van Ufford HC et al (1992) Anti-inflammatory activity of gallic acid. Planta Med 58:499–504CrossRefPubMed
go back to reference Kurhe Y, Mahesh R (2015) Ondansetron attenuates co-morbid depression and anxiety associated with obesity by inhibiting the biochemical alterations and improving serotonergic neurotransmission. Pharmacol Biochem Behav 136:107–116CrossRefPubMed Kurhe Y, Mahesh R (2015) Ondansetron attenuates co-morbid depression and anxiety associated with obesity by inhibiting the biochemical alterations and improving serotonergic neurotransmission. Pharmacol Biochem Behav 136:107–116CrossRefPubMed
go back to reference Latha RC, Daisy P (2011) Insulin-secretagogue, antihyperlipidemic and other protective effects of gallic acid isolated from terminalia bellerica Roxb.in streptozotocin-induced diabetic rats. Chem Biol Interact 189:112–118CrossRefPubMed Latha RC, Daisy P (2011) Insulin-secretagogue, antihyperlipidemic and other protective effects of gallic acid isolated from terminalia bellerica Roxb.in streptozotocin-induced diabetic rats. Chem Biol Interact 189:112–118CrossRefPubMed
go back to reference Lee W, Lee SY, Son YJ et al (2015) Gallic acid decreases inflammatory cytokine secretion through histone acetyltransferase/histone deacetylase regulation in high glucose-induced human monocytes. J Med Food 18:793–801CrossRefPubMed Lee W, Lee SY, Son YJ et al (2015) Gallic acid decreases inflammatory cytokine secretion through histone acetyltransferase/histone deacetylase regulation in high glucose-induced human monocytes. J Med Food 18:793–801CrossRefPubMed
go back to reference Lin EH, Von Korff M, Alonso J et al (2008) Mental disorders among persons with diabetes--results from the World Mental Health Surveys. J Psychosom Res 65:571–580CrossRefPubMedPubMedCentral Lin EH, Von Korff M, Alonso J et al (2008) Mental disorders among persons with diabetes--results from the World Mental Health Surveys. J Psychosom Res 65:571–580CrossRefPubMedPubMedCentral
go back to reference Mansouri MT, Soltani M, Naghizadeh B et al (2014) A possible mechanism for the anxiolytic-like effect of gallic acid in the rat elevated plus maze. Pharmacol Biochem Behav 117:40–46CrossRefPubMed Mansouri MT, Soltani M, Naghizadeh B et al (2014) A possible mechanism for the anxiolytic-like effect of gallic acid in the rat elevated plus maze. Pharmacol Biochem Behav 117:40–46CrossRefPubMed
go back to reference Mishra K, Ojha H, Chaudhury NK (2012) Estimation of antiradical properties of using DPPH assay: a critical review and results. Food Chem 130:1036–1043CrossRef Mishra K, Ojha H, Chaudhury NK (2012) Estimation of antiradical properties of using DPPH assay: a critical review and results. Food Chem 130:1036–1043CrossRef
go back to reference Moretti M, Colla A, de Oliveira Balen G et al (2012) Ascorbic acid treatment, similarly to fluoxetine, reverses depressive-like behavior and brain oxidative damage induced by chronic unpredictable stress. J Psychiatr Res 46:331–340CrossRefPubMed Moretti M, Colla A, de Oliveira Balen G et al (2012) Ascorbic acid treatment, similarly to fluoxetine, reverses depressive-like behavior and brain oxidative damage induced by chronic unpredictable stress. J Psychiatr Res 46:331–340CrossRefPubMed
go back to reference Patel SS, Goyal RK (2011) Prevention of diabetes-induced myocardial dysfunction in rats using the juice of the Emblica officinalis fruit. Exp Clin Cardiol 16:87–91PubMedPubMedCentral Patel SS, Goyal RK (2011) Prevention of diabetes-induced myocardial dysfunction in rats using the juice of the Emblica officinalis fruit. Exp Clin Cardiol 16:87–91PubMedPubMedCentral
go back to reference Pellow S, Chopin P, File SE et al (1985) Validation of open: closed arm entries in the elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167CrossRefPubMed Pellow S, Chopin P, File SE et al (1985) Validation of open: closed arm entries in the elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167CrossRefPubMed
go back to reference Porsolt RD, Bertin A, Blavet N et al (1979) Immobility induced by forced swimming in rats: effects of agents wich modify central catecholamine and serotonin activity. Eur J Pharmacol 57:201–210CrossRefPubMed Porsolt RD, Bertin A, Blavet N et al (1979) Immobility induced by forced swimming in rats: effects of agents wich modify central catecholamine and serotonin activity. Eur J Pharmacol 57:201–210CrossRefPubMed
go back to reference Punithavathi VR, Prince PS, Kumar R (2011) Antihyperglycaemic, antilipid peroxidative and antioxidant effects of gallic acid on streptozotocin induced diabetic wistar rats. Eur J Pharmacol 650:465–471CrossRefPubMed Punithavathi VR, Prince PS, Kumar R (2011) Antihyperglycaemic, antilipid peroxidative and antioxidant effects of gallic acid on streptozotocin induced diabetic wistar rats. Eur J Pharmacol 650:465–471CrossRefPubMed
go back to reference Rebai R, Jasmin L, Boudah A (2017) 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 134:142–150CrossRefPubMed Rebai R, Jasmin L, Boudah A (2017) 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 134:142–150CrossRefPubMed
go back to reference Redivo DD, Schreiber AK, Adami ER et al (2016) Effect of omega-3 polyunsaturated fatty acid treatment over mechanical allodynia and depressive-like behavior associated with experimental diabetes. Behav Brain Res 298:57–64CrossRefPubMed Redivo DD, Schreiber AK, Adami ER et al (2016) Effect of omega-3 polyunsaturated fatty acid treatment over mechanical allodynia and depressive-like behavior associated with experimental diabetes. Behav Brain Res 298:57–64CrossRefPubMed
go back to reference Renn BN, Feliciano L, Segal DL (2011) The bidirectional relationship of depression and diabetes: a systematic review. Clin Psychol Rev 31:1239–1246CrossRefPubMed Renn BN, Feliciano L, Segal DL (2011) The bidirectional relationship of depression and diabetes: a systematic review. Clin Psychol Rev 31:1239–1246CrossRefPubMed
go back to reference Roy T, Lloyd CE (2012) Epidemiology of depression and diabetes: a systematic review. J Affect Disord 142:S8–S21CrossRefPubMed Roy T, Lloyd CE (2012) Epidemiology of depression and diabetes: a systematic review. J Affect Disord 142:S8–S21CrossRefPubMed
go back to reference Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192–205CrossRefPubMed Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192–205CrossRefPubMed
go back to reference Sharma P, Bhardwaj P, Singh R (2016) Administration of lactobacillus casei and bifidobacterium bifidum ameliorated hyperglycemia, dyslipidemia, and oxidative stress in diabetic rats. Int J Prev Med 22:102 Sharma P, Bhardwaj P, Singh R (2016) Administration of lactobacillus casei and bifidobacterium bifidum ameliorated hyperglycemia, dyslipidemia, and oxidative stress in diabetic rats. Int J Prev Med 22:102
go back to reference Siba IP, Bortolanza M, Frazão Vital MAB et al (2017) Fish oil prevents rodent anxious states comorbid with diabetes: a putative involvement of nitric oxide modulation. Behav Brain Res 326:173–186CrossRefPubMed Siba IP, Bortolanza M, Frazão Vital MAB et al (2017) Fish oil prevents rodent anxious states comorbid with diabetes: a putative involvement of nitric oxide modulation. Behav Brain Res 326:173–186CrossRefPubMed
go back to reference Singh P, Rahul MK, Vijay T et al (2013) Anxiolytic effect of chronic administration of gallic acid in rats. J appl pharm sci 3:101–104 Singh P, Rahul MK, Vijay T et al (2013) Anxiolytic effect of chronic administration of gallic acid in rats. J appl pharm sci 3:101–104
go back to reference Stanely MPP, Kumar MR, Selvakumari CJ (2011) Effects of gallic acid on brain lipid peroxide and lipid metabolism in streptozotocin-induced diabetic wistar rats. J Biochem Mol Toxicol 25:101–107CrossRef Stanely MPP, Kumar MR, Selvakumari CJ (2011) Effects of gallic acid on brain lipid peroxide and lipid metabolism in streptozotocin-induced diabetic wistar rats. J Biochem Mol Toxicol 25:101–107CrossRef
go back to reference Todorović N, Filipović D (2017) The antidepressant- and anxiolytic-like effects of fluoxetine and clozapine in chronically isolated rats involve inhibition of hippocampal TNF-α. Pharmacol Biochem Behav 17:30419–30417 Todorović N, Filipović D (2017) The antidepressant- and anxiolytic-like effects of fluoxetine and clozapine in chronically isolated rats involve inhibition of hippocampal TNF-α. Pharmacol Biochem Behav 17:30419–30417
go back to reference Vicente MA, Zangrossi HJR (2014) Involvement of 5-HT2C and 5-HT1A receptors of the basolateral nucleus of the amygdala in the anxiolytic effect of chronic antidepressant treatment. Neuropharmacology 79:127–135CrossRefPubMed Vicente MA, Zangrossi HJR (2014) Involvement of 5-HT2C and 5-HT1A receptors of the basolateral nucleus of the amygdala in the anxiolytic effect of chronic antidepressant treatment. Neuropharmacology 79:127–135CrossRefPubMed
go back to reference Wayhs CA, Manfredini V, Sitta A et al (2010) Protein and lipid oxidative damage in streptozotocin-induced diabetic rats submitted to forced swimming test: the insulin and clonazepam effect. Metab Brain Dis 25:297–304CrossRefPubMed Wayhs CA, Manfredini V, Sitta A et al (2010) Protein and lipid oxidative damage in streptozotocin-induced diabetic rats submitted to forced swimming test: the insulin and clonazepam effect. Metab Brain Dis 25:297–304CrossRefPubMed
go back to reference Wayhs CA, Mescka CP, Guerreiro G et al (2014) Diabetic encephalopathy-related depression: experimental evidence that insulin and clonazepam restore antioxidant status in rat brain. Cell Biochem Funct 32:711–719CrossRefPubMed Wayhs CA, Mescka CP, Guerreiro G et al (2014) Diabetic encephalopathy-related depression: experimental evidence that insulin and clonazepam restore antioxidant status in rat brain. Cell Biochem Funct 32:711–719CrossRefPubMed
go back to reference Wrighten SA, Piroli GG, Grillo CA et al (2009) A look inside the diabetic brain: contributors to diabetes-induced brain aging. Biochim Biophys Acta 1792:444–453CrossRefPubMed Wrighten SA, Piroli GG, Grillo CA et al (2009) A look inside the diabetic brain: contributors to diabetes-induced brain aging. Biochim Biophys Acta 1792:444–453CrossRefPubMed
go back to reference Yu Z, Song F, Jin YC et al (2018) Comparative pharmacokinetics of gallic acid after oral administration of gallic acid monohydrate in normal and isoproterenol-induced myocardial infarcted rats. Front Pharmacol 9:328CrossRefPubMedPubMedCentral Yu Z, Song F, Jin YC et al (2018) Comparative pharmacokinetics of gallic acid after oral administration of gallic acid monohydrate in normal and isoproterenol-induced myocardial infarcted rats. Front Pharmacol 9:328CrossRefPubMedPubMedCentral
go back to reference Zanoveli JM, de Morais H, Dias IC et al (2016) Depression associated with diabetes: from pathophysiology to treatment. Curr Diabetes Rev 12:165–178CrossRefPubMed Zanoveli JM, de Morais H, Dias IC et al (2016) Depression associated with diabetes: from pathophysiology to treatment. Curr Diabetes Rev 12:165–178CrossRefPubMed
Metadata
Title
The antioxidant gallic acid induces anxiolytic-, but not antidepressant-like effect, in streptozotocin-induced diabetes
Authors
Mariana Machado Pereira
Helen de Morais
Eldevan dos Santos Silva
Claudia Rita Corso
Eliana Rezende Adami
Rose Maria Carlos
Alexandra Acco
Janaina Menezes Zanoveli
Publication date
01-10-2018
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 5/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-018-0264-9

Other articles of this Issue 5/2018

Metabolic Brain Disease 5/2018 Go to the issue