Apigenin ameliorates chronic mild stress-induced depressive behavior by inhibiting interleukin-1β production and NLRP3 inflammasome activation in the rat brain

Behavioural Brain Research

Volumn 296, Issue , 2016, Pages 318-325

  Li, Ruipeng ^a   Wang, Xiangxiang ^a   Qin, Tingting ^a   Qu, Rong ^b   Ma, Shiping ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Apigenin; Chronic unpredictable mild stress; Depression; NLRP3 inflammasome; Peroxisome proliferator activated receptor

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; APIGENIN; CRYOPYRIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SUCROSE; 2-CHLORO-5-NITROBENZANILIDE; ANILIDE; CARRIER PROTEIN; INFLAMMASOME; NOD-LIKE RECEPTOR 3, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR DISORDER; CHRONIC STRESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEPRESSION; DISEASE SEVERITY; DOWN REGULATION; LOCOMOTION; MALE; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUCROSE PREFERENCE TEST; UPREGULATION; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; MENTAL STRESS; SPRAGUE DAWLEY RAT;

ANILIDES; ANIMALS; APIGENIN; BEHAVIOR, ANIMAL; CARRIER PROTEINS; DEPRESSION; DISEASE MODELS, ANIMAL; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; PPAR GAMMA; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84943385476     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.09.031     Document Type: Article

References (41)

1. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Arch. Gen. Psychiatry 2005, 62:593-602. 10.1001/archpsyc.62.6.593.
2. Culpepper L. Why do you need to move beyond first-line therapy for major depression?. J. Clin. Psychiatry 2010, 71:4-9. 10.4088/JCP.9104su1c.01.
3. Leonard B., Maes M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci. Biobehav. Rev. 2012, 36:764-785. 10.1016/j.neubiorev.2011.12.005.
4. Gárate I., García-Bueno B., Madrigal J.L., Bravo L., Berrocoso E., Caso J.R., et al. Origin and consequences of brain Toll-like receptor 4 pathway stimulation in an experimental model of depression. J. Neuroinflamm. 2011, 8:151. 10.1186/1742-2094-8-151.
5. Maes M., Song C., Yirmiya R. Targeting IL-1 in depression. Expert Opin. 2012, 16:1097-1112.
6. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., et al. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 2008, 13:717-728. 10.1038/sj.mp.4002055.
7. Piletz J.E., Halaris A., Iqbal O., Hoppensteadt D., Fareed J., Zhu H., et al. Pro-inflammatory biomakers in depression: treatment with venlafaxine. World J. Biol. Psychiatry 2009, 10:313-323. 10.3109/15622970802573246.
8. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:751-756. 10.1073/pnas.0708092105.
9. Gdek-Michalska A., Tadeusz J., Rachwalska P., Bugajski J. Cytokines, prostaglandins and nitric oxide in the regulation of stress-response systems. Pharmacol. Rep. 2013, 65:1655-1662. 10.1016/s1734-1140(13)71527-5.
10. Iwata M., Ota K.T., Duman R.S. The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav. Immun. 2013, 31:105-114. 10.1016/j.bbi.2012.12.008.
11. Latz E. The inflammasomes: mechanisms of activation and function. Curr. Opin. Immunol. 2010, 22:28-33. 10.1016/j.coi.2009.12.004.
12. Alcocer-Gómez E., de Miguel M., Casas-Barquero N., Núñez-Vasco J., Sánchez-Alcazar J.A., Fernández-Rodríguez A., et al. NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav. Immun. 2014, 36:111-117. 10.1016/j.bbi.2013.10.017.
13. Pan Y., Chen X.Y., Zhang Q.Y., Kong L.D. Microglial NLRP3 inflammasome activation mediates IL-1β-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun. 2014, 1-11. 10.1016/j.bbi.2014.04.007.
14. Miean K.H., Mohamed S. Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. J. Agric. Food Chem. 2001, 49:3106-3112. 10.1021/jf000892m.
15. Zhang X., Wang G., Gurley E.C., Zhou H. Flavonoid apigenin inhibits lipopolysaccharide-induced inflammatory response through multiple mechanisms in macrophages. PLoS One 2014, 9:e107072. 10.1371/journal.pone.0107072.
16. Han X.H., Hong S.S., Hwang J.S., Lee M.K., Hwang B.Y., Ro J.S. Monoamine oxidase inhibitory components from cayratia japonica. Arch. Pharm. Res. 2007, 30:13-17.
17. Nakazawa T., Yasuda T., Ueda J., Ohsawa K. Antidepressant-like effects of apigenin and 2,4,5-trimethoxycinnamic acid from perilla frutescens in the forced swimming test. Biol. Pharm. Bull. 2003, 26:474-480. 10.1248/bpb.26.474.
18. Yi L., Li J., Li Y., Pan Y., Xu Q., Kong L. Antidepressant-like behavioral and neurochemical effects of the citrus-associated chemical apigenin. Life Sci. 2008, 82:741-751. 10.1016/j.lfs.2008.01.007.
19. Liu Q., Yang Q., Hu H., Yang L., Yang Y., Chou G., et al. Bioactive diterpenoids and flavonoids from the aerial parts of Scoparia dulcis. J. Nat. Prod. 2014, 77:1594-1600.
20. Delerive P., Fruchart J.C., Staels B. Peroxisome proliferator-activated receptors in inflammation control. J. Endocrinol. 2001, 169:453-459. 10.1677/joe.0.1690453.
21. Farooq R.K., Isingrini E., Tanti A., Le Guisquet A.M., Arlicot N., Minier F., et al. Is unpredictable chronic mild stress (UCMS) a reliable model to study depression-induced neuroinflammation?. Behav. Brain Res. 2012, 231:130-137. 10.1016/j.bbr.2012.03.020.
22. Jiang H., Wang Z., Wang Y., Xie K., Zhang Q., Luan Q., et al. Antidepressant-like effects of curcumin in chronic mild stress of rats: involvement of its anti-inflammatory action. Prog. Neuro-psychopharmacol. Biol. Psychiatry 2013, 47:33-39. 10.1016/j.pnpbp.2013.07.009.
23. Sadaghiani M.S., Javadi-Paydar M., Gharedaghi M.H., Fard Y.Y., Dehpour A.R. Antidepressant-like effect of pioglitazone in the forced swimming test in mice: the role of PPAR-gamma receptor and nitric oxide pathway. Behav. Brain Res. 2011, 224:336-343. 10.1016/j.bbr.2011.06.011.
24. Wang Z., Zhang Q., Yuan L., Wang S., Liu L., Yang X., Li G.L.D. The effects of curcumin on depressive-like behavior in mice after lipopolysaccharide administration. Behav. Brain Res. 2014, 274:282-290. 10.1016/j.ejphar.2005.06.002.
25. Li L.F., Yang J., Ma S.P., Qu R. Magnolol treatment reversed the glial pathology in an unpredictable chronic mild stress-induced rat model of depression. Eur. J. Pharmacol. 2013, 711:42-49. 10.1016/j.ejphar.2013.04.008.
26. You Z., Luo C., Zhang W., Chen Y., He J., Zhao Q., et al. Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav. Brain Res. 2011, 225:135-141. 10.1016/j.bbr.2011.07.006.
27. Hwang J., Zheng L.T., Ock J., Lee M.G., Kim S.H., Lee H.W., et al. Inhibition of glial inflammatory activation and neurotoxicity by tricyclic antidepressants. Neuropharmacology 2008, 55:826-834. 10.1016/j.neuropharm.2008.06.045.
28. Rinwa P., Kumar A. Quercetin suppress microglial neuroinflammatory response and induce antidepressent-like effect in olfactory bulbectomized rats. Neuroscience 2013, 255:86-98. 10.1016/j.neuroscience.2013.09.044.
29. Norman G.J., Karelina K., Zhang N., Walton J.C., Morris J.S., Devriesa C. Stress and IL-1beta contribute to the development of depressive-like behavior following peripheral nerve injury. Mol. Psychiatry 2010, 15:404-414. 10.1038/mp.2009.91.
30. Kaushik D.K., Gupta M., Kumawat K.L., Basu A. Nlrp3 inflammasome: key mediator of neuroinflammation in murine japanese encephalitis. PLoS One 2012, 7. 10.1371/journal.pone.0032270.
31. Maslanik T., Mahaffey L., Tannura K., Beninson L., Greenwood B.N., Fleshner M. The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain Behav. Immun. 2013, 28:54-62. 10.1016/j.bbi.2012.10.014.
32. Zhang Y., Liu L., Peng Y.L., Liu Y.Z., Wu T.Y., Shen X.L., et al. Involvement of inflammasome activation in lipopolysaccharide-induced mice depressive-like behaviors. CNS Neurosci. Ther. 2014, 20:119-124. 10.1111/cns.12170.
33. Zhang X., Zhang J.-H., Chen X.-Y., Hu Q.-H., Wang M.-X., Jin R., et al. Reactive oxygen species-induced TXNIP drives fructose-mediated hepatic inflammation and lipid accumulation through NLRP3 inflammasome activation. Antioxid. Redox Signal. 2015, 22:848-870. 10.1089/ars.2014.5868.
34. Drevets W.C., Price J.L., Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 2008, 213:93-118. 10.1007/s00429-008-0189-x.
35. Garrido-Mesa N., Zarzuelo A., Gálvez J. Minocycline: far beyond an antibiotic. Br. J. Pharmacol. 2013, 169:337-352. 10.1111/bph.12139.
36. Guo H., Kong S., Chen W., Dai Z., Lin T., Su J., et al. Apigenin mediated protection of OGD-evoked neuron-like injury in differentiated PC12Cells. Neurochem. Res. 2014, 39:2197-2210. 10.1007/s11064-014-1421-0.
37. Ha S.K., Lee P., Park J.A., Oh H.R., Lee S.Y., Park J.H., et al. Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem. Int. 2008, 52:878-886. 10.1016/j.neuint.2007.10.005.
38. García-Bueno B., Pérez-Nievas B.G., Leza J.C. Is there a role for the nuclear receptor PPARγ in neuropsychiatric diseases?. Int. J. Neuropsychopharmacol. 2010, 13:1411-1429. 10.1017/S1461145710000970.
39. Kemp D.E., Schinagle M., Gao K., Conroy C., Ganocy S.J., Ismail-Beigi F., et al. PPAR-γ agonism as a modulator of mood: proof-of-concept for pioglitazone in bipolar depression. CNS Drugs 2014, 28:571-581. 10.1007/s40263-014-0158-2.
40. Ahmed A.A.E., Al-Rasheed N.M. Antidepressant-like effects of rosiglitazone, a PPARγ agonist, in the rat forced swim and mouse tail suspension tests. Behav. Pharmacol. 2009, 20:635-642. 10.1097/FBP.0b013e328331b9bf.
41. Kempster S.L., Belteki G., Forhead A.J., Fowden A.L., Catalano R.D., Lam B.Y., et al. Developmental control of the Nlrp6 inflammasome and a substrate, IL-18, in mammalian intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G253-G263. 10.1152/ajpgi.00397.2010.