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

Metabolic Brain Disease

Volumn 29, Issue 3, 2014, Pages 737-746

  Gupta, Deepali ^a   Radhakrishnan, Mahesh ^a   Kurhe, Yeshwant ^a  

^a BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

Author keywords

Anxiety like behavior; Elevated plus maze; Hole board; Insulin; Light dark test; Streptozotocin induced diabetes

Indexed keywords

DIAZEPAM; GLUCOSE; INSULIN; INSULIN GLARGINE; ANXIOLYTIC AGENT; GLUCOSE BLOOD LEVEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AVERSION; BLOOD GLUCOSE MONITORING; CONTROLLED STUDY; DIABETES CONTROL; ELEVATED PLUS MAZE TEST; EXPLORATORY BEHAVIOR; GLUCOSE BLOOD LEVEL; HOLE BOARD TEST; INSULIN TREATMENT; LATENT PERIOD; LIGHT-DARK TEST; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; REARING; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; ANIMAL BEHAVIOR; COMPLICATION; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; ETIOLOGY; FEMALE; MALE; MOTOR ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIAZEPAM; EXPLORATORY BEHAVIOR; FEMALE; INSULIN; MALE; MICE; MOTOR ACTIVITY;

EID: 84906726591     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-014-9540-5     Document Type: Article

References (73)

1. 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
2. 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
3. Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behavior in mice: a review. Behav Brain Res 125:141-149 (Pubitemid 33000452)
4. 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 (Pubitemid 29319265)
5. 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
6. 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 (Pubitemid 16184238)
7. Bourin M, Hascoët M (2003) The mouse light/dark box test. Eur J Pharmacol 463:55-65
8. 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
9. 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 (Pubitemid 41446895)
10. 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
11. Chan O, Inouye K, Riddell MC, Vranic M, Matthews SG (2003) Diabetes and the hypothalamo-pituitary-adrenal (HPA) axis. Minerva Endocrinol 28:87-102
12. 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 (Pubitemid 16078463)
13. 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 (Pubitemid 44610642)
14. Collins MM, Corcoran P, Perry IJ (2009) Anxiety and depression symptoms in patients with diabetes. Diabetic Med 26:153-161
15. 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 (Pubitemid 19162403)
16. Craft S, Watson GS (2004) Insulin and neurodegenerative disease: shared and specific mechanisms. Lancet Neurol 3:169-178 (Pubitemid 38229951)
17. Crandall EA, Gills MA, Fernstrom JD (1981) Reduction in brain serotonin synthesis rate in streptozotocin-diabetic rats. Endocrinology 109:310-312 (Pubitemid 11042491)
18. Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9:37-44
19. Crawley JN, Goodwin FK (1980) Preliminary report of a simple animal behavior for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13:167-170
20. Cruz APM, Frei F, Graeff FG (1994) Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol Biochem Behav 49: 171-176 (Pubitemid 24297273)
21. 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 (Pubitemid 8110282)
22. 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
23. 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
24. 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
25. Gerozissis K (2003) Brain insulin: regulation, mechanisms of action and functions. Cell Mol Neurobiol 23:1-25
26. 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
27. 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 (Pubitemid 36349687)
28. 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 (Pubitemid 36040653)
29. 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 (Pubitemid 44779607)
30. 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
31. 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 (Pubitemid 20325167)
32. 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
33. 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
34. 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
35. Kliethermes CL, Crabbe JC (2006) Pharmacological and genetic influences on hole-board behaviors in mice. Pharmacol Biochem Behav 85:57-65 (Pubitemid 44772910)
36. 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
37. Kneussel M (2002) Dynamic regulation of GABA (A) receptors at synaptic sites. Brain Res Rev 39:74-83
38. 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
39. 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
40. Lenzen S (2008) The mechanisms of alloxan and streptozotocin induced diabetes. Diabetologia 51:216-226
41. 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
42. Lin EH, Korff MV (2008)Mental disorders among persons with diabetes: results from the World Mental Health Surveys. J Psychosom Res 65: 571-580
43. Lister RG(1987) The use of a plus-maze tomeasure anxiety in themouse. Psychopharmacology 92:180-185
44. Lister RG (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46:321-340
45. MacKenzie RG, Trulson ME (1978) Effects of insulin and streptozotocininduced diabetes on brain tryptophan and serotonin metabolism in rats. J Neurochem 30:205-211
46. 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 (Pubitemid 40966816)
47. Millan MJ (2003) The neurobiology and control of anxious states. Prog Neurobiol 70:83-244
48. Nemeroff CB (2002) The role of GABA in the pathophysiology and treatment of anxiety disorders. Psychopharmacol Bull 37:133-146
49. Park CR (2001) Cognitive effects of insulin in the central nervous system. Neurosci Biobehav Rev 25:311-323
50. 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 (Pubitemid 16239568)
51. Pijl H, Edo AM (2002) Modulation of monoaminergic neural circuits: potential for the treatment of type 2 diabetes mellitus. Treat Endocrinol 1:71-78 (Pubitemid 36828427)
52. Plastino M, Fava A, Pirritano D, Cotronei P, Sacco N, Sperlì Tet 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
53. Ramanathan M, Jaiswal AK, Bhattachayra SK (1998) Differential effects of diazepam on anxiety in streptozotocin induced diabetic and nondiabetic rats. Psychopharmacology 135:361-367 (Pubitemid 28254842)
54. Reagan LP (2012) Diabetes as a chronic metabolic stressor: causes, consequences and clinical complications. Exp Neurol 233:68-78
55. 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
56. 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 (Pubitemid 44787805)
57. 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 (Pubitemid 32988479)
58. 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
59. Silva MI, de Aquino Neto MR, Teixeira Neto PF, Moura BA, do Amaral JF, de Sousa DP et al (2007) Central nervous systemactivity of acute administration of isopulegol inmice. Pharmacol Biochem Behav 88: 141-147 (Pubitemid 350115997)
60. A receptor subtypes in mice. Neuropharmacology 63:250-258
61. Smith KJ, Béland M, Clyde M, Gariépy G, PagéV, Badawi G et al (2013) Association of diabetes with anxiety: A systematic review and meta-analysis. J Psychosom Res 74:89-99
62. Szkudelski T (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:536-546
63. 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
64. Trulson ME, Himmel CD (1983) Decreased brain dopamine synthesis rate and increased (3H) spiroperido binding in streptozotocin-diabetic rats. J Neurochem 40:1456-1459 (Pubitemid 13079902)
65. Trulson ME, Jacoby JH, MacKenzie RG (1986) Streptozotocin-induced diabetes reduces brain serotonin synthesis in rats. J Neurochem 46: 1068-1072 (Pubitemid 16010952)
66. Tsigos C, Chrousos GP (2002) Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53: 865-871 (Pubitemid 35282615)
67. 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 (Pubitemid 46039779)
68. 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 (Pubitemid 47040046)
69. 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 (Pubitemid 32506878)
70. Wei XY, Yang JY, Wang JH, Wu CF (2007) Anxiolytic effect of saponins from Panax quinquefolium in mice. J Ethnopharmacol 111:613-618
71. 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
72. 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 (Pubitemid 39410721)
73. 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 (Pubitemid 38482161)