Insulin reverses anxiety-like behavior evoked by streptozotocin-induced diabetes in mice

Aksu I, Ates M, Baykara B, Kiray M, Sisman AR, Buyuk E et al (2012) Anxiety correlates to decreased blood and prefrontal cortex IGF-1 levels in streptozotocin induced diabetes. Neurosci Lett 531:176–181 Antony S, Kumar TP, Kuruvilla KP, George N, Paulose CS (2010) Decreased GABA receptor binding in the cerebral cortex of insulin induced hypoglycemic and streptozotocin induced diabetic rats. Neurochem Res 35:1516–1521 Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behavior in mice: a review. Behav Brain Res 125:141–149 Bhardwaj SK, Sandhu SK, Sharma P, Kaur G (1999) Impact of diabetes on CNS: role of signal transduction cascade. Brain Res Bull 49:155–162 Biala G, Kruk M (2008) Calcium channel antagonists suppress cross-tolerance to the anxiogenic effects of D-amphetamine and nicotine in the mouse elevated plus maze test. Prog Neuropsychopharmacol Biol Psychiatry 32:54–61 Bitar MILAD, Koulu MARKKU, Rapoport SI, Linnoila MARKKU (1986) Diabetes-induced alteration in brain monoamine metabolism in rats. J Pharmacol Exp Ther 236:432–437 Bourin M, Hascoët M (2003) The mouse light/dark box test. Eur J Pharmacol 463:55–65 Can ÖD, Öztürk Y, Özkay ÜD (2011) Effects of insulin and St. John’s Wort treatments on anxiety, locomotor activity, depression, and active learning parameters of streptozotocin-diabetic rats. Planta Med 77:1970–1976 Carobrez AP, Bertoglio LJ (2005) Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 29:1193–1205 Casarrubea M, Sorbera F, Crescimanno G (2009) Structure of rat behavior in hole-board: I) multivariate analysis of response to anxiety. Physiol Behav 96:174–179 Chan O, Inouye K, Riddell MC, Vranic M, Matthews SG (2003) Diabetes and the hypothalamo-pituitary-adrenal (HPA) axis. Minerva Endocrinol 28:87–102 Chu PC, Lin MT, Shian LR, Leu SY (1986) Alterations in physiologic functions and in brain monoamine content in streptozocin-diabetic rats. Diabetes 35:481–485 Clavijo M, Carvhalo JJ, Rios M, Ries de Oliveira I (2006) Psychiatric disorders in patients with diabetes type 2 at medical care and training district of Rio Branco-Acre, Brazil. Arq Neuropsiquiatr 64(3-B):807–813 Collins MM, Corcoran P, Perry IJ (2009) Anxiety and depression symptoms in patients with diabetes. Diabetic Med 26:153–161 Costall B, Jones BJ, Kelly ME, Naylor R, Tomkins DM (1989) Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol Biochem Behav 32:777–785 Craft S, Watson GS (2004) Insulin and neurodegenerative disease: shared and specific mechanisms. Lancet Neurol 3:169–178 Crandall EA, Gills MA, Fernstrom JD (1981) Reduction in brain serotonin synthesis rate in streptozotocin-diabetic rats. Endocrinology 109:310–312 Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9:37–44 Crawley JN, Goodwin FK (1980) Preliminary report of a simple animal behavior for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13:167–170 Cruz APM, Frei F, Graeff FG (1994) Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol Biochem Behav 49:171–176 Curzon G, Fernando JCR (1977) Drugs altering insulin secretion: effects of plasma and brain concentrations of aromatic amino acids and on brain 5-hydroxytryptamine turnover. Br J Pharmacol 60:401–408 Duarte A, Santos M, Seica R, Resende de Oliveira C (2000) Effect of oxidative stress on the uptake of GABA and glutamate in synaptosomes isolated from diabetic rat brain. Neuroendocrinology 72:179–186 Francis GJ, Martinez JA, Liu WQ, Xu K, Ayer A, Fine J et al (2008) Intranasal insulin prevents cognitive decline, cerebral atrophy and white matter changes in murine type I diabetic encephalopathy. Brain 131:3311–3334 Fraser LM, Brown RE, Hussin A, Fontana M, Whittaker A, O’Leary TP et al (2010) Measuring anxiety-and locomotion-related behaviors in mice: a new way of using old tests. Psychopharmacology 211:99–112 Gerozissis K (2003) Brain insulin: regulation, mechanisms of action and functions. Cell Mol Neurobiol 23:1–25 Go Y, Kitaoka H, Hanafusa T (2013). Effects of diabetes and diabetes control on susceptibility to learned helplessness in streptozotocin-induced diabetic rats. Diabetol Int 1–9.doi:10.1007/s13340.013.1032.0 Gomez R, Vargas CR, Wajner M, Barros HM (2003) Lower in vivo brain extracellular GABA concentration in diabetic rats during forced swimming. Brain Res 968:281–284 Grigsby AB, Anderson RJ, Freedland KE, Clouse RE, Lustman PJ (2002) Prevalence of anxiety in adults with diabetes: a systematic review. J Psychosom Res 53:1053–1060 Harada K, Aota M, Inoue T, Matsuda R, Mihara T, Yamaji T et al (2006) Anxiolytic activity of a novel potent serotonin 5-HT2C receptor antagonist FR260010: a comparison with diazepam and buspirone. Eur J Pharmacol 553:171–184 Herzer M, Hood KK (2010) Anxiety symptoms in adolescents with type 1 diabetes: association with blood glucose monitoring and glycemic control. J Pediatr Psychol 35:415–425 Hilakivi-Clarke LA, Wozniak KM, Durcan MJ, Linnoila M (1990) Behavior of streptozotocin diabetic mice in test of exploration, locomotion, anxiety, depression and aggression. Physiol Behav 48:429–433 Ho N, Balu DT, Hilario MR, Blendy JA, Lucki I (2012) Depressive phenotypes evoked by experimental diabetes are reversed by insulin. Physiol Behav 105:702–708 Hutter N, Schnurr A, Baumeister H (2010) Healthcare costs in patients with diabetes mellitus and comorbid mental disorders-a systematic review. Diabetologia 53:2470–2479 Kamei J, Ohsawa M, Tsuji M, Takeda H, Matsumiya T (2001) Modification of the effects of benzodiazepines on the exploratory behaviors of mice on a hole-board by diabetes. Jpn J Pharmacol 86:47–54 Kliethermes CL, Crabbe JC (2006) Pharmacological and genetic influences on hole-board behaviors in mice. Pharmacol Biochem Behav 85:57–65 Klodzinska A, Tatarczyńska E, Chojnacka-Wójcik E, Nowak G, Cosford ND, Pilc A (2004) Anxiolytic-like effects of MTEP, a potent and selective mGlu5 receptor agonist does not involve GABA(A) signaling. Neuropharmacology 47:42–50 Kneussel M (2002) Dynamic regulation of GABA (A) receptors at synaptic sites. Brain Res Rev 39:74–83 Kong WX, Chen SW, Li YL, Zhang YJ, Wang R, Min L, Mi X (2006) Effects of taurine on rat behaviors in three anxiety models. Pharmacol Biochem Behav 83:271–276 Kumar TP, Antony S, Gireesh G, George N, Paulose CS (2010) Curcumin modulates dopaminergic receptor, CREB and phospholipase C gene expression in the cerebral cortex and cerebellum of streptozotocin induced diabetic rats. J Biomed Sci 17:43–53 Lenzen S (2008) The mechanisms of alloxan and streptozotocin induced diabetes. Diabetologia 51:216–226 Li C, Barker L, Ford ES, Zhang X, Strine TW, Mokdad AH (2008) Diabetes and anxiety in US adults: findings from the 2006 Behavioral Risk Factor Surveillance System. Diabetic Med 25:878–881 Lin EH, Korff MV (2008) Mental disorders among persons with diabetes: results from the World Mental Health Surveys. J Psychosom Res 65:571–580 Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185 Lister RG (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46:321–340 MacKenzie RG, Trulson ME (1978) Effects of insulin and streptozotocin-induced diabetes on brain tryptophan and serotonin metabolism in rats. J Neurochem 30:205–211 Mi XJ, Chen SW, Wang WJ, Wang R, Zhang YJ, Li WJ et al (2005) Anxiolytic-like effect of paeonol in mice. Pharmacol Biochem Behav 81:683–687 Millan MJ (2003) The neurobiology and control of anxious states. Prog Neurobiol 70:83–244 Nemeroff CB (2002) The role of GABA in the pathophysiology and treatment of anxiety disorders. Psychopharmacol Bull 37:133–146 Park CR (2001) Cognitive effects of insulin in the central nervous system. Neurosci Biobehav Rev 25:311–323 Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167 Pijl H, Edo AM (2002) Modulation of monoaminergic neural circuits: potential for the treatment of type 2 diabetes mellitus. Treat Endocrinol 1:71–78 Plastino M, Fava A, Pirritano D, Cotronei P, Sacco N, Sperlì T et al (2010) Effects of insulinic therapy on cognitive impairment in patients with Alzheimer disease and diabetes mellitus type-2. J Neurol Sci 288:112–116 Ramanathan M, Jaiswal AK, Bhattachayra SK (1998) Differential effects of diazepam on anxiety in streptozotocin induced diabetic and non-diabetic rats. Psychopharmacology 135:361–367 Reagan LP (2012) Diabetes as a chronic metabolic stressor: causes, consequences and clinical complications. Exp Neurol 233:68–78 Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24:855–872 Shaban MC, Fosbury J, Kerr D, Cavan DA (2006) The prevalence of depression and anxiety in adults with type 1 diabetes. Diabetic Med 23:1381–1384 Shekhar A, McCann UD, Meaney MJ, Blanchard DC, Davis M, Frey KA et al (2001) Summary of a National Institute of Mental Health workshop: developing animal models of anxiety disorders. Psychopharmacology (Berl) 157:327–339 Shpakov A, Chistyakova O, Derkach K, Bondareva V (2011) Hormonal signaling systems of the brain in diabetes mellitus. In: Chang RC (ed) Neurodegenerative diseases. Intech Open Access Publisher, Rijeka, Croatia, pp 349–386 Silva MI, de Aquino Neto MR, Teixeira Neto PF, Moura BA, do Amaral JF, de Sousa DP et al (2007) Central nervous system activity of acute administration of isopulegol in mice. Pharmacol Biochem Behav 88:141–147 Smith KS, Engin E, Meloni EG, Rudolph U (2012) Benzodiazepine-induced anxiolysis and reduction of conditioned fear are mediated by distinct GABAA receptor subtypes in mice. Neuropharmacology 63:250–258 Smith KJ, Béland M, Clyde M, Gariépy G, Pagé V, Badawi G et al (2013) Association of diabetes with anxiety: A systematic review and meta-analysis. J Psychosom Res 74:89–99 Szkudelski T (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:536–546 Torres RC, Prevatto JP, Silva PMR, Martinsand MA, Carvalho VF (2013) From Type-1 Diabetes HPA Axis to the Disease Complications. J Diabetes Metab S12:002. doi:10.4172/2155-6156.S12-002 Trulson ME, Himmel CD (1983) Decreased brain dopamine synthesis rate and increased (3H) spiroperido binding in streptozotocin-diabetic rats. J Neurochem 40:1456–1459 Trulson ME, Jacoby JH, MacKenzie RG (1986) Streptozotocin-induced diabetes reduces brain serotonin synthesis in rats. J Neurochem 46:1068–1072 Tsigos C, Chrousos GP (2002) Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53:865–871 Vetiska SM, Ahmadian G, Ju W, Liu L, Wymann MP, Wang YT (2007) GABAA receptor-associated phosphoinositide 3-kinase is required for insulin-induced recruitment of postsynaptic GABAA receptors. Neuropharmacology 52:146–155 Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature protocols 2:322–328 Wall PM, Messier C (2001) Methodological and conceptual issues in the use of the elevated plus-maze as a psychological measurement instrument of animal anxiety-like behavior. Neurosci Biobehav Rev 25:275–286 Wei XY, Yang JY, Wang JH, Wu CF (2007) Anxiolytic effect of saponins from Panax quinquefolium in mice. J Ethnopharmacol 111:613–618 Whiting DR, Guariguata L, Weil C, Shaw J (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pr 94:311–321 Zhang Y, Wang W, Zhang J (2004) Effects of novel anxiolytic 4-butyl-alpha-agarofuran on levels of monoamine neurotransmitters in rats. Eur J Pharmacol 504:39–44 Zhao WQ, Chen H, Quon MJ, Alkon DL (2004) Insulin and the insulin receptor in experimental models of learning and memory. Eur J Pharmacol 490:71–81