Long-term corticosterone exposure decreases insulin sensitivity and induces depressive-like behaviour in the C57BL/6NCrl mouse

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Van Donkelaar, Eva L ^a   Vaessen, Koen R D ^a,b   Pawluski, Jodi L ^a,c,d   Sierksma, Annerieke S ^a,e,f   Blokland, Arjan ^g   Cañete, Ramón ^h   Steinbusch, Harry W M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d OHIO UNIVERSITY   (United States)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g MAASTRICHT UNIVERSITY   (Netherlands)

^h HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; GLUCOSE; INSULIN; GLUCOSE BLOOD LEVEL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; C57BL/6N MOUSE; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; ELEVATED ZERO MAZE TEST; FLUID INTAKE; FORCED SWIM TEST; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HOMEOSTASIS MODEL ASSESSMENT OF INSULIN RESISTANCE; IMMOBILITY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LOCOMOTION; LONG TERM EXPOSURE; MALE; METABOLIC PARAMETERS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OPEN FIELD TEST; PILOT STUDY; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SWIMMING;

ANIMALS; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; CORTICOSTERONE; DEPRESSION; DISEASE MODELS, ANIMAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PILOT PROJECTS; PITUITARY-ADRENAL SYSTEM; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84907901414     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106960     Document Type: Article

References (49)

1. Gillespie CF, Nemeroff CB (2005) Hypercortisolemia and depression. Psychosomatic medicine 67 Suppl 1: S26-28.
2. Bao AM, Meynen G, Swaab DF (2008) The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res Rev 57: 531-553.
3. Reus VI, Wolkowitz OM (2001) Antiglucocorticoid drugs in the treatment of depression. Expert opinion on investigational drugs 10: 1789-1796.
4. Haas JT, Biddinger SB (2009) Dissecting the role of insulin resistance in the metabolic syndrome. Curr Opin Lipidol 20: 206-210.
5. Anderson RJ, Freedland KE, Clouse RE, Lustman PJ (2001) The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care 24: 1069-1078.
6. Gavard JA, Lustman PJ, Clouse RE (1993) Prevalence of depression in adults with diabetes. An epidemiological evaluation. Diabetes Care 16: 1167-1178.
7. Reagan LP, Grillo CA, Piroli GG (2008) The As and Ds of stress: metabolic, morphological and behavioral consequences. European journal of pharmacology 585: 64-75.
8. Craft S (2005) Insulin resistance syndrome and Alzheimer's disease: age- and obesity-related effects on memory, amyloid, and inflammation. Neurobiology of aging 26 Suppl 1: 65-69.
9. Haan MN (2006) Therapy Insight: type 2 diabetes mellitus and the risk of lateonset Alzheimer's disease. Nature clinical practice Neurology 2: 159-166.
10. Caraci F, Copani A, Nicoletti F, Drago F (2010) Depression and Alzheimer's disease: neurobiological links and common pharmacological targets. Eur - J Pharmacol 626: 64-71.
11. Biessels GJ, Kappelle LJ (2005) Increased risk of Alzheimer's disease in Type II diabetes: insulin resistance of the brain or insulin-induced amyloid pathology? Biochem Soc Trans 33: 1041-1044.
12. Briones A, Gagno S, Martisova E, Dobarro M, Aisa B, et al. (2011) Stressinduced anhedonia is associated with an increase in Alzheimer's disease-related markers. Br J Pharmacol 165: 897-907.
13. Solas M, Aisa B, Mugueta MC, Del Rio J, Tordera RM, et al. (2010) Interactions between age, stress and insulin on cognition: implications for Alzheimer's disease. Neuropsychopharmacology 35: 1664-1673.
14. Solas M, Aisa B, Tordera RM, Mugueta MC, Ramirez MJ (2013) Stress contributes to the development of central insulin resistance during aging: Implications for Alzheimer's disease. Biochim Biophys Acta 1832: 2332-2339.
15. Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, et al. (2008) Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18: 1085-1088.
16. Elliott EM, Mattson MP, Vanderklish P, Lynch G, Chang I, et al. (1993) Corticosterone exacerbates kainate-induced alterations in hippocampal tau immunoreactivity and spectrin proteolysis in vivo. Journal of neurochemistry 61: 57-67.
17. Budas G, Coughlan CM, Seckl JR, Breen KC (1999) The effect of corticosteroids on amyloid beta precursor protein/amyloid precursor-like protein expression and processing in vivo. Neuroscience letters 276: 61-64.
18. Gasparini L, Gouras GK, Wang R, Gross RS, Beal MF, et al. (2001) Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. The Journal of neuroscience 21: 2561-2570.
19. Zhao L, Teter B, Morihara T, Lim GP, Ambegaokar SS, et al. (2004) Insulindegrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention. The Journal of Neuroscience 24: 11120-11126.
20. Stoothoff WH, Johnson GV (2005) Tau phosphorylation: physiological and pathological consequences. Biochimica et biophysica acta 1739: 280-297.
21. Aznar S, Knudsen GM (2011) Depression and Alzheimer's disease: is stress the initiating factor in a common neuropathological cascade? J Alzheimers Dis 23: 177-193.
22. Riederer P, Bartl J, Laux G, Grunblatt E (2011) Diabetes type II: a risk factor for depression-Parkinson-Alzheimer? Neurotox Res 19: 253-265.
23. Sierksma AS, van den Hove DL, Steinbusch HW, Prickaerts J (2010) Major depression, cognitive dysfunction and Alzheimer's disease: is there a link? Eur J Pharmacol 626: 72-82.
24. Zhao Y, Ma R, Shen J, Su H, Xing D, et al. (2008) A mouse model of depression induced by repeated corticosterone injections. European journal of pharmacology 581: 113-120.
25. Severino C, Brizzi P, Solinas A, Secchi G, Maioli M, et al. (2002) Low-dose dexamethasone in the rat: a model to study insulin resistance. American journal of physiology Endocrinology and metabolism 283: E367-373.
26. Karatsoreos IN, Bhagat SM, Bowles NP, Weil ZM, Pfaff DW, et al. (2010) Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151: 2117- 2127.
27. Sierksma AS, Prickaerts J, Chouliaras L, Rostamian S, Delbroek L, et al. (2013) Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice. Neurobiol Aging 34: 319-337.
28. Hem A, Smith AJ, Solberg P (1998) Saphenous vein puncture for blood sampling of the mouse, rat, hamster, gerbil, guinea pig, ferret and mink. Laboratory animals 32: 364-368.
29. Andrikopoulos S, Blair AR, Deluca N, Fam BC, Proietto J (2008) Evaluating the glucose tolerance test in mice. Am J Physiol Endocrinol Metab 295: E1323- 1332.
30. Ferrannini E, Mari A (1998) How to measure insulin sensitivity. Journal of hypertension: 895-906.
31. Gounarides JS, Korach-Andre M, Killary K, Argentieri G, Turner O, et al. (2008) Effect of dexamethasone on glucose tolerance and fat metabolism in a diet-induced obesity mouse model. Endocrinology 149: 758-766.
32. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412- 419.
33. Lee S, Muniyappa R, Yan X, Chen H, Yue LQ, et al. (2008) Comparison between surrogate indexes of insulin sensitivity and resistance and hyperinsulinemic euglycemic clamp estimates in mice. Am J Physiol Endocrinol Metab 294: E261-270.
34. Shepherd JK, Grewal SS, Fletcher A, Bill DJ, Dourish CT (1994) Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 116: 56-64.
35. Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Archives internationales de pharmacodynamie et de thérapie 229: 327-336.
36. Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266: 730-732.
37. Detke MJ, Lucki I (1996) Detection of serotonergic and noradrenergic antidepressants in the rat forced swimming test: the effects of water depth. Behavioural Brain Research 73: 43-46.
38. Lucki I (1997) The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behavioural pharmacology 8: 523- 532.
39. Walsh RN, Cummins RA (1976) The Open-Field Test: a critical review. Psychol Bull 83: 482-504.
40. Ennaceur A, Michalikova S, Chazot PL (2006) Models of anxiety: responses of rats to novelty in an open space and an enclosed space. Behav Brain Res 171: 26-49.
41. Gardier AM, Bourin M (2001) Appropriate use of "knockout" mice as models of depression or models of testing the efficacy of antidepressants. Psychopharmacology (Berl) 153: 393-394.
42. Herrmann M, Henneicke H, Street J, Modzelewski J, Kalak R, et al. (2009) The challenge of continuous exogenous glucocorticoid administration in mice. Steroids 74: 245-249.
43. Dallman MF, Pecoraro N, Akana SF, La Fleur SE, Gomez F, et al. (2003) Chronic stress and obesity: a new view of "comfort food". Proc Natl Acad Sci U S A 100: 11696-11701.
44. Nandi A, Kitamura Y, Kahn CR, Accili D (2004) Mouse models of insulin resistance. Physiol Rev 84: 623-647.
45. Grundy SM (2004) Metabolic syndrome: part I. Endocrinol Metab Clin North Am 33: ix-xi.
46. Cryan JF, Slattery DA (2007) Animal models of mood disorders: Recent developments. Current opinion in psychiatry 20: 1-7.
47. Gourley SL, Kiraly DD, Howell JL, Olausson P, Taylor JR (2008) Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol Psychiatry 64: 884-890.
48. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, et al. (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62: 479-493.
49. Bindra D, Thompson WR (1953) An evaluation of defecation and urination as measures of fearfulness. J Comp Physiol Psychol 46: 43-45.