Metabolic factors-triggered inflammatory response drives antidepressant effects of exercise in CUMS rats

Psychiatry Research

Volumn 228, Issue 3, 2015, Pages 257-264

  Liu, Weina ^a,b   Wang, Hongmei ^a,b   Wang, Yangkai ^c   Li, Haipeng ^d   Ji, Liu ^a,b  

^a East China Normal University   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

Antidepressant; Exercise; Inflammatory response; Metabolic factors

Indexed keywords

CRYOPYRIN; GHRELIN; GHRELIN RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; STAT3 PROTEIN; ANTIDEPRESSANT AGENT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PHOSPHOTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BINDING AFFINITY; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXERCISE; GENE EXPRESSION; HORMONE BINDING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; THERAPY EFFECT; TREATMENT RESPONSE; ANIMAL; DRIVE; DRUG EFFECTS; EXPLORATORY BEHAVIOR; KINESIOTHERAPY; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; PHOSPHORYLATION; PHYSIOLOGY; PSYCHOLOGY; SWIMMING;

ANIMALS; ANTIDEPRESSIVE AGENTS; DEPRESSION; DEPRESSIVE DISORDER; DRIVE; EXERCISE THERAPY; EXPLORATORY BEHAVIOR; GLYCOGEN SYNTHASE KINASE 3; LEPTIN; MALE; MOTOR ACTIVITY; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PHYSICAL CONDITIONING, ANIMAL; RATS; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84938742387     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2015.05.102     Document Type: Article

References (58)

1. Agudelo L.Z., Femenia T., Orhan F., Porsmyr-Palmertz M., Goiny M., Martinez-Redondo V., Correia J.C., Izadi M., Bhat M., Schuppe-Koistinen I., Pettersson A.T., Ferreira D.M., Krook A., Barres R., Zierath J.R., Erhardt S., Lindskog M., Ruas J.L. Skeletal muscle PGC-1alpha1 modulates kynurenine metabolism and mediates resilience to stress-induced depression. Cell 2014, 159:33-45.
2. Aguilar-Valles A., Kim J., Jung S., Woodside B., Luheshi G.N. Role of brain transmigrating neutrophils in depression-like behavior during systemic infection. Mol. Psychiatry 2014, 19:599-606.
3. Alcocer-Gomez E., de Miguel M., Casas-Barquero N., Nunez-Vasco J., Sanchez-Alcazar J.A., Fernandez-Rodriguez A., Cordero M.D. NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav. Immun. 2014, 36:111-117.
4. Beaulieu J.M., Gainetdinov R.R., Caron M.G. Akt/GSK3 signaling in the action of psychotropic drugs. Annu. Rev. Pharmacol. Toxicol. 2009, 49:327-347.
5. Besedovsky H.O., Del R.A. Physiologic versus diabetogenic effects of interleukin-1: a question of weight. Curr. Pharm. Des. 2014, 20:4733-4740.
6. Burniston J.G., Kenyani J., Gray D., Guadagnin E., Jarman I.H., Cobley J.N., Cuthbertson D.J., Chen Y.W., Wastling J.M., Lisboa P.J., Koch L.G., Britton S.L. Conditional independence mapping of DIGE data reveals PDIA3 protein species as key nodes associated with muscle aerobic capacity. J. Proteomics 2014, 106:230-245.
7. Chen G., Henter I.D., Manji H.K. Translational research in bipolar disorder: emerging insights from genetically based models. Mol. Psychiatry 2010, 15:883-895.
8. Chiu C.T., Liu G., Leeds P., Chuang D.M. Combined treatment with the mood stabilizers lithium and valproate produces multiple beneficial effects in transgenic mouse models of Huntington's disease. Neuropsychopharmacology 2011, 36:2406-2421.
9. Chuang J.C., Krishnan V., Yu H.G., Mason B., Cui H., Wilkinson M.B., Zigman J.M., Elmquist J.K., Nestler E.J., Lutter M. A beta3-adrenergic-leptin-melanocortin circuit regulates behavioral and metabolic changes induced by chronic stress. Biol. Psychiatry 2010, 67:1075-1082.
10. Chung H., Li E., Kim Y., Kim S., Park S. Multiple signaling pathways mediate ghrelin-induced proliferation of hippocampal neural stem cells. J. Endocrinol. 2013, 218:49-59.
11. Contarteze R.V., Manchado F.B., Gobatto C.A., De Mello M.A. Stress biomarkers in rats submitted to swimming and treadmill running exercises. Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 2008, 151:415-422.
12. Decker T., Kovarik P. Serine phosphorylation of STATs. Oncogene 2000, 19:2628-2637.
13. Deligiannidis K.M., Rothschild A.J., Barton B.A., Kroll-Desrosiers A.R., Meyers B.S., Flint A.J., Whyte E.M., Mulsant B.H. A gender analysis of the study of pharmacotherapy of psychotic depression (STOP-PD): gender and age as predictors of response and treatment-associated changes in body mass index and metabolic measures. J. Clin. Psychiatry 2013, 74:1003-1009.
14. Doherty G.H., Beccano-Kelly D., Yan S.D., Gunn-Moore F.J., Harvey J. Leptin prevents hippocampal synaptic disruption and neuronal cell death induced by amyloid beta. Neurobiol. Aging 2013, 34:226-237.
15. Donegan J.J., Girotti M., Weinberg M.S., Morilak D.A. A novel role for brain interleukin-6: facilitation of cognitive flexibility in rat orbitofrontal cortex. J. Neurosci. 2014, 34:953-962.
16. Du J., Wei Y., Liu L., Wang Y., Khairova R., Blumenthal R., Tragon T., Hunsberger J.G., Machado-Vieira R., Drevets W., Wang Y.T., Manji H.K. A kinesin signaling complex mediates the ability of GSK-3beta to affect mood-associated behaviors. Proc. Natl. Acad. Sci. USA 2010, 107:11573-11578.
17. Eikelis N., Esler M., Barton D., Dawood T., Wiesner G., Lambert G. Reduced brain leptin in patients with major depressive disorder and in suicide victims. Mol. Psychiatry 2006, 11:800-801.
18. Fang Z.H., Lee C.H., Seo M.K., Cho H., Lee J.G., Lee B.J., Park S.W., Kim Y.H. Effect of treadmill exercise on the BDNF-mediated pathway in the hippocampus of stressed rats. Neurosci. Res. 2013, 76:187-194.
19. Garza J.C., Guo M., Zhang W., Lu X.Y. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J. Biol. Chem. 2008, 283:18238-18247.
20. Garza J.C., Guo M., Zhang W., Lu X.Y. Leptin restores adult hippocampal neurogenesis in a chronic unpredictable stress model of depression and reverses glucocorticoid-induced inhibition of GSK-3beta/beta-catenin signaling. Mol. Psychiatry 2012, 17:790-808.
21. Giordano A., Murano I., Mondini E., Perugini J., Smorlesi A., Severi I., Barazzoni R., Scherer P.E., Cinti S. Obese adipocytes show ultrastructural features of stressed cells and die of pyroptosis. J. Lipid Res. 2013, 54:2423-2436.
22. Guo M., Lu Y., Garza J.C., Li Y., Chua S.C., Zhang W., Lu B., Lu X.Y. Forebrain glutamatergic neurons mediate leptin action on depression-like behaviors and synaptic depression. Transl. Psychiatry 2012, 2:e83.
23. Hand L.E., Usan P., Cooper G.J., Xu L.Y., Ammori B., Cunningham P.S., Aghamohammadzadeh R., Soran H., Greenstein A., Loudon A.S., Bechtold D.A., Ray D.W. Adiponectin induces A20 expression in adipose tissue to confer metabolic benefit. Diabetes 2015, 64:128-136.
24. Handschin C., Spiegelman B.M. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 2008, 454:463-469.
25. Hsu Y.W., Pan Y.J., Cho Y.M., Liou T.H., Chou P., Wang P.S. Aging effects on exercise-induced alternations in plasma acylated ghrelin and leptin in male rats. Eur. J. Appl. Physiol. 2011, 111:809-817.
26. Israel M.A., Yuan S.H., Bardy C., Reyna S.M., Mu Y., Herrera C., Hefferan M.P., Van Gorp S., Nazor K.L., Boscolo F.S., Carson C.T., Laurent L.C., Marsala M., Gage F.H., Remes A.M., Koo E.H., Goldstein L.S. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 2012, 482:216-220.
27. Jerlhag E., Egecioglu E., Landgren S., Salome N., Heilig M., Moechars D., Datta R., Perrissoud D., Dickson S.L., Engel J.A. Requirement of central ghrelin signaling for alcohol reward. Proc. Natl. Acad. Sci. USA 2009, 106:11318-11323.
28. Karege F., Perroud N., Burkhardt S., Fernandez R., Ballmann E., La Harpe R., Malafosse A. Protein levels of beta-catenin and activation state of glycogen synthase kinase-3beta in major depression. A study with postmortem prefrontal cortex. J. Affect. Disord. 2012, 136:185-188.
29. Kim H., Chen L., Lim G., Sung B., Wang S., McCabe M.F., Rusanescu G., Yang L., Tian Y., Mao J. Brain indoleamine 2,3-dioxygenase contributes to the comorbidity of pain and depression. J. Clin. Investig. 2012, 122:2940-2954.
30. Liu J., Perez S.M., Zhang W., Lodge D.J., Lu X.Y. Selective deletion of the leptin receptor in dopamine neurons produces anxiogenic-like behavior and increases dopaminergic activity in amygdala. Mol. Psychiatry 2011, 16:1024-1038.
31. Liu W., Sheng H., Xu Y., Liu Y., Lu J., Ni X. Swimming exercise ameliorates depression-like behavior in chronically stressed rats: relevant to proinflammatory cytokines and IDO activation. Behav. Brain Res. 2013, 242:110-116.
32. Lu M., Yang J.Z., Geng F., Ding J.H., Hu G. Iptakalim confers an antidepressant effect in a chronic mild stress model of depression through regulating neuro-inflammation and neurogenesis. Int. J. Neuropsychopharmacol. 2014, 17:1501-1510.
33. Lu X.Y. The leptin hypothesis of depression: a potential link between mood disorders and obesity?. Curr. Opin. Pharmacol. 2007, 7:648-652.
34. Lu X.Y., Kim C.S., Frazer A., Zhang W. Leptin: a potential novel antidepressant. Proc. Natl. Acad. Sci. USA 2006, 103:1593-1598.
35. Lutter M., Sakata I., Osborne-Lawrence S., Rovinsky S.A., Anderson J.G., Jung S., Birnbaum S., Yanagisawa M., Elmquist J.K., Nestler E.J., Zigman J.M. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nature Neuroscience 2008, 11:752-753.
36. Meyer R.M., Burgos-Robles A., Liu E., Correia S.S., Goosens K.A. A ghrelin-growth hormone axis drives stress-induced vulnerability to enhanced fear. Molecular Psychiatry 2014, 19:1284-1294.
37. Morales-Garcia J.A., Susin C., Alonso-Gil S., Perez D.I., Palomo V., Perez C., Conde S., Santos A., Gil C., Martinez A., Perez-Castillo A. Glycogen synthase kinase-3 inhibitors as potent therapeutic agents for the treatment of Parkinson disease. ACS Chemical Neuroscience 2013, 4:350-360.
38. Nakazato M., Murakami N., Date Y., Kojima M., Matsuo H., Kangawa K., Matsukura S. A role for ghrelin in the central regulation of feeding. Nature 2001, 409:194-198.
39. Niswender K.D., Morton G.J., Stearns W.H., Rhodes C.J., Myers M.J., Schwartz M.W. Intracellular signalling. Key enzyme in leptin-induced anorexia. Nature 2001, 413:794-795.
40. Pan Y., Chen X.Y., Zhang Q.Y., Kong L.D. Microglial NLRP3 inflammasome activation mediates IL-1beta-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun. 2014, 41:90-100.
41. Petit-Demouliere B., Chenu F., Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology 2005, 177:245-255.
42. Ra S.M., Kim H., Jang M.H., Shin M.C., Lee T.H., Lim B.V., Kim C.J., Kim E.H., Kim K.M., Kim S.S. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci. Lett. 2002, 333:123-126.
43. Schellekens H., Finger B.C., Dinan T.G., Cryan J.F. Ghrelin signalling and obesity: at the interface of stress, mood and food reward. Pharmacol. Ther. 2012, 135:316-326.
44. Schroder K., Zhou R., Tschopp J. The NLRP3 inflammasome: a sensor for metabolic danger?. Science 2010, 327:296-300.
45. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
46. Stieg M.R., Sievers C., Farr O., Stalla G.K., Mantzoros C.S. Leptin: a hormone linking activation of neuroendocrine axes with neuropathology. Psychoneuroendocrinology 2014, 51C:47-57.
47. Surget A., Wang Y., Leman S., Ibarguen-Vargas Y., Edgar N., Griebel G., Belzung C., Sibille E. Corticolimbic transcriptome changes are state-dependent and region-specific in a rodent model of depression and of antidepressant reversal. Neuropsychopharmacology 2009, 34:1363-1380.
48. Svenningsson P., Tzavara E.T., Carruthers R., Rachleff I., Wattler S., Nehls M., McKinzie D.L., Fienberg A.A., Nomikos G.G., Greengard P. Diverse psychotomimetics act through a common signaling pathway. Science 2003, 302:1412-1415.
49. Szymanska M., Suska A., Budziszewska B., Jaworska-Feil L., Basta-Kaim A., Leskiewicz M., Kubera M., Gergont A., Kroczka S., Kacinski M., Lason W. Prenatal stress decreases glycogen synthase kinase-3 phosphorylation in the rat frontal cortex. Pharmacol. Rep. 2009, 61:612-620.
50. Thornton T.M., Pedraza-Alva G., Deng B., Wood C.D., Aronshtam A., Clements J.L., Sabio G., Davis R.J., Matthews D.E., Doble B., Rincon M. Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science 2008, 320:667-670.
51. Tschop M., Smiley D.L., Heiman M.L. Ghrelin induces adiposity in rodents. Nature 2000, 407:908-913.
52. Vandanmagsar B., Youm Y.H., Ravussin A., Galgani J.E., Stadler K., Mynatt R.L., Ravussin E., Stephens J.M., Dixit V.D. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 2011, 17:179-188.
53. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 1987, 93:358-364.
54. Zhang X., Zhang G., Zhang H., Karin M., Bai H., Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 2008, 135:61-73.
55. Zhang Y., Liu L., Peng Y.L., Liu Y.Z., Wu T.Y., Shen X.L., Zhou J.R., Sun D.Y., Huang A.J., Wang X., Wang Y.X., Jiang C.L. Involvement of inflammasome activation in lipopolysaccharide-induced mice depressive-like behaviors. CNS Neurosci. Ther. 2014, 20:119-124.
56. Zheng H., Liu Y., Li W., Yang B., Chen D., Wang X., Jiang Z., Wang H., Wang Z., Cornelisson G., Halberg F. Beneficial effects of exercise and its molecular mechanisms on depression in rats. Behav. Brain Res. 2006, 168:47-55.
57. Zunszain P.A., Horowitz M.A., Cattaneo A., Lupi M.M., Pariante C.M. Ketamine: synaptogenesis, immunomodulation and glycogen synthase kinase-3 as underlying mechanisms of its antidepressant properties. Mol. Psychiatry 2013, 18:1236-1241.
58. Zuurbier C.J., Jong W.M., Eerbeek O., Koeman A., Pulskens W.P., Butter L.M., Leemans J.C., Hollmann M.W. Deletion of the innate immune NLRP3 receptor abolishes cardiac ischemic preconditioning and is associated with decreased Il-6/STAT3 signaling. PLoS One 2012, 7:e40643.