Unpredictable chronic mild stress induces anxiety and depression-like behaviors and inactivates AMP-activated protein kinase in mice

Brain Research

Volumn 1576, Issue , 2014, Pages 81-90

  Zhu, Shenghua ^a   Wang, Junhui ^b,f   Zhang, Yaribo ^c   Li, Victor ^d   Kong, Jiming ^a   He, Jue ^e   Li, Xin Min ^f  

^a UNIVERSITY OF MANITOBA   (Canada)

^b SHANDONG MENTAL HEALTH CENTER   (China)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e HENAN UNIVERSITY   (China)

^f UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Adenosine monophosphate activated protein kinase; Anxiety; Depression; Unpredictable chronic mild stress

Indexed keywords

DREBRIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; NERVE PROTEIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; FORCED SWIM TEST; IMMOBILITY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; TAIL SUSPENSION TEST; UNPREDICTABLE CHRONIC MILD STRESS; WEIGHT GAIN; ANIMAL; BODY WEIGHT; C57BL MOUSE; COMPLICATION; ENZYME ACTIVATION; ENZYMOLOGY; EXERCISE; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; LEARNED HELPLESSNESS; MAZE TEST; MENTAL STRESS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN PROCESSING;

MUS; PHOS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANXIETY; BODY WEIGHT; CEREBRAL CORTEX; DEPRESSION; ENZYME ACTIVATION; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; FEMALE; HELPLESSNESS, LEARNED; HYDROXYMETHYLGLUTARYL COA REDUCTASES; MAZE LEARNING; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84926076426     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.06.002     Document Type: Article

References (50)

1. American Psychiatric Association, 2013. Diagnostic and Statistical Manual of Mental Disorders, fifth ed. Arlington, VA.
2. Aoki, C., Kojima, N., Sabaliauskas, N., Shah, L., Ahmed, T.H., Oakford, J., Ahmed, T., Yamazaki, H., Hanamura, K., Shirao, T., 2009. Drebrin a knockout eliminates the rapid form of homeostatic synaptic plasticity at excitatory synapses of intact adult cerebral cortex. J. Comp. Neurol. 517, 105-121.
3. Berton, O., Nestler, E.J., 2006. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7, 137-151.
4. Bondi, C.O., Rodriguez, G., Gould, G.G., Frazer, A., Morilak, D.A., 2008. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33, 320-331.
5. Carling, D., 2004. The AMP-activated protein kinase cascade - a unifying system for energy control. Trends Biochem. Sci. 29, 18-24.
6. Christoffel, D.J., Golden, S.A., Russo, S.J., 2011. Structural and synaptic plasticity in stress-related disorders. Rev. Neurosci. 22, 535-549.
7. Culmsee, C., Monnig, J., Kemp, B.E., Mattson, M.P., 2001. AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation. J. Mol. Neurosci. 17, 45-58.
8. David, D.J., Samuels, B.A., Rainer, Q., Wang, J.W., Marsteller, D., Mendez, I., Drew, M., Craig, D.A., Guiard, B.P., Guilloux, J.P., Artymyshyn, R.P., Gardier, A.M., Gerald, C., Antonijevic, I.A., Leonardo, E.D., Hen, R., 2009. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493.
9. Fava, M., 2003. Diagnosis and definition of treatment-resistant depression. Biol. Psychiatry 53, 649-659.
10. Gadalla, A.E., Pearson, T., Currie, A.J., Dale, N., Hawley, S.A., Sheehan, M., Hirst, W., Michel, A.D., Randall, A., Hardie, D.G., Frenguelli, B.G., 2004. AICA riboside both activates AMP-activated protein kinase and competes with adenosine for the nucleoside transporter in the CA1 region of the rat hippocampus. J. Neurochem. 88, 1272-1282.
11. Greengard, P., Valtorta, F., Czernik, A.J., Benfenati, F., 1993. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780-785.
12. Hardie, D.G., 2003. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144, 5179-5183.
13. Hayashi, K., Ishikawa, R., Ye, L.H., He, X.L., Takata, K., Kohama, K., Shirao, T., 1996. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J. Neurosci. 16, 7161-7170.
14. He, J., Xu, H., Yang, Y., Zhang, X., Li, X.M., 2005. Chronic administration of quetiapine alleviates the anxiety-like behavioral changes induced by a neurotoxic regimen of dl-amphetamine in rats. Behav. Brain Res. 160, 178-187.
15. Iio, W., Tokutake, Y., Matsukawa, N., Tsukahara, T., Chohnan, S., Toyoda, A., 2012. Anorexic behavior and elevation of hypothalamic malonyl-CoA in socially defeated rats. Biochem. Biophys. Res. Commun. 421, 301-304.
16. Janz, R., Sudhof, T.C., Hammer, R.E., Unni, V., Siegelbaum, S.A., Bolshakov, V.Y., 1999. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24, 687-700.
17. Keedwell, P.A., Andrew, C., Williams, S.C., Brammer, M.J., Phillips, M.L., 2005. The neural correlates of anhedonia in major depressive disorder. Biol. Psychiatry 58, 843-853.
18. Kobayashi, R., Sekino, Y., Shirao, T., Tanaka, S., Ogura, T., Inada, K., Saji, M., 2004. Antisense knockdown of drebrin A, a dendritic spine protein, causes stronger preference, impaired pre-pulse inhibition, and an increased sensitivity to psychostimulant. Neurosci. Res. 49, 205-217.
19. Krishnan, V., Nestler, E.J., 2008. The molecular neurobiology of depression. Nature 455, 894-902.
20. Lee, Y., Kim, E.K., 2013. AMP-activated protein kinase as a key molecular link between metabolism and clockwork. Exp. Mol. Med. 45, e33.
21. Luo, C., Xu, H., Li, X.M., 2005. Quetiapine reverses the suppression of hippocampal neurogenesis caused by repeated restraint stress. Brain Res. 1063, 32-39.
22. Mayberg, H.S., Lozano, A.M., Voon, V., McNeely, H.E., Seminowicz, D., Hamani, C., Schwalb, J.M., Kennedy, S.H., 2005. Deep brain stimulation for treatment-resistant depression. Neuron 45, 651-660.
23. Mayorga, A.J., Lucki, I., 2001. Limitations on the use of the C57BL/6 mouse in the tail suspension test. Psychopharmacology (Berl.) 155, 110-112.
24. McCullough, L.D., Zeng, Z., Li, H., Landree, L.E., McFadden, J., Ronnett, G.V., 2005. Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J. Biol. Chem. 280, 20493-20502.
25. Mineur, Y.S., Belzung, C., Crusio, W.E., 2006. Effects of unpredictable chronic mild stress on anxiety and depressionlike behavior in mice. Behav. Brain Res. 175, 43-50.
26. Mineur, Y.S., Prasol, D.J., Belzung, C., Crusio, W.E., 2003. Agonistic behavior and unpredictable chronic mild stress in mice. Behav. Genet. 33, 513-519.
27. Minokoshi, Y., Alquier, T., Furukawa, N., Kim, Y.B., Lee, A., Xue, B., Mu, J., Foufelle, F., Ferre, P., Birnbaum, M.J., Stuck, B.J., Kahn, B. B., 2004. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569-574.
28. Moussavi, S., Chatterji, S., Verdes, E., Tandon, A., Patel, V., Ustun, B., 2007. Depression, chronic diseases, and decrements in health: results from the World Health Surveys. Lancet 370, 851-858.
29. Mozhui, K., Karlsson, R.M., Kash, T.L., Ihne, J., Norcross, M., Patel, S., Farrell, M.R., Hill, E.E., Graybeal, C., Martin, K.P., Camp, M., Fitzgerald, P.J., Ciobanu, D.C., Sprengel, R., Mishina, M., Wellman, C.L., Winder, D.G., Williams, R.W., Holmes, A., 2010. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J. Neurosci. 30, 5357-5367.
30. Park, H.G., Yi, H., Kim, S.H., Yu, H.S., Ahn, Y.M., Lee, Y.H., Roh, M.S., Kim, Y.S., 2011. The effect of cyclosporine A on the phosphorylation of the AMPK pathway in the rat hippocampus. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1933-1937.
31. Porsolt, R.D., Bertin, A., Jalfre, M., 1977. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327-336.
32. Pothion, S., Bizot, J.C., Trovero, F., Belzung, C., 2004. Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 155, 135-146.
33. Radley, J.J., Rocher, A.B., Miller, M., Janssen, W.G., Liston, C., Hof, P.R., McEwen, B.S., Morrison, J.H., 2006. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb. Cortex 16, 313-320.
34. Rapp, S., Baader, M., Hu, M., Jennen-Steinmetz, C., Henn, F.A., Thome, J., 2004. Differential regulation of synaptic vesicle proteins by antidepressant drugs. Pharmacogen. J. 4, 110-113.
35. Rossler, A.S., Joubert, C., Chapouthier, G., 2000. Chronic mild stress alleviates anxious behavior in female mice in two situations. Behav. Process. 49, 163-165.
36. Schmitt, U., Tanimoto, N., Seeliger, M., Schaeffel, F., Leube, R.E., 2009. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162, 234-243.
37. Shirao, T., Sekino, Y., 2001. Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci. Res. 40, 1-7.
38. Spasic, M.R., Callaerts, P., Norga, K.K., 2009. AMP-activated protein kinase (AMPK) molecular crossroad for metabolic control and survival of neurons. Neuroscientist 15, 309-316.
39. Steru, L., Chermat, R., Thierry, B., Simon, P., 1985. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 85, 367-370.
40. Strekalova, T., Spanagel, R., Dolgov, O., Bartsch, D., 2005. Stress-induced hyperlocomotion as a confounding factor in anxiety and depression models in mice. Behav. Pharmacol. 16, 171-180.
41. Surget, A., Tanti, A., Leonardo, E.D., Laugeray, A., Rainer, Q., Touma, C., Palme, R., Griebel, G., Ibarguen-Vargas, Y., Hen, R., Belzung, C., 2011. Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16, 1177-1188.
42. Takahashi, H., Sekino, Y., Tanaka, S., Mizui, T., Kishi, S., Shirao, T., 2003. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J. Neurosci. 23, 6586-6595.
43. Taksande, B.G., Faldu, D.S., Dixit, M.P., Sakaria, J.N., Aglawe, M.M., Umekar, M.J., Kotagale, N.R., 2013. Agmatine attenuates chronic unpredictable mild stress induced behavioral alteration in mice. Eur. J. Pharmacol. 720, 115-120.
44. Thome, J., Pesold, B., Baader, M., Hu, M., Gewirtz, J.C., Duman, R.S., Henn, F.A., 2001. Stress differentially regulates synaptophysin and synaptotagmin expression in hippocampus. Biol. Psychiatry 50, 809-812.
45. Xu, H., Chen, Z., He, J., Haimanot, S., Li, X., Dyck, L., Li, X.M., 2006. Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16, 551-559.
46. Xu, H., He, J., Richardson, J.S., Li, X.M., 2004. The response of synaptophysin and microtubule-associated protein 1 to restraint stress in rat hippocampus and its modulation by venlafaxine. J. Neurochem. 91, 1380-1388.
47. Xu, H., Qing, H., Lu, W., Keegan, D., Richardson, J.S., Chlan-Fourney, J., Li, X.M., 2002. Quetiapine attenuates the immobilization stress-induced decrease of brain-derived neurotrophic factor expression in rat hippocampus. Neurosci. Lett. 321, 65-68.
48. Xu, S.X., Zhou, Z.Q., Li, X.M., Ji, M.H., Zhang, G.F., Yang, J.J., 2013. The activation of adenosine monophosphate-activated protein kinase in rat hippocampus contributes to the rapid antidepressant effect of ketamine. Behav. Brain Res. 253, 305-309.
49. Yan, B., He, J., Xu, H., Zhang, Y., Bi, X., Thakur, S., Gendron, A., Kong, J., Li, X.M., 2007. Quetiapine attenuates the depressive and anxiolytic-like behavioural changes induced by global cerebral ischemia in mice. Behav. Brain Res. 182, 36-41.
50. Zhao, Y., Shen, J., Su, H., Li, B., Xing, D., Du, L., 2008. Chronic corticosterone injections induce a decrease of ATP levels and sustained activation of AMP-activated protein kinase in hippocampal tissues of male mice. Brain Res. 1191, 148-156.