Icariin attenuates lipopolysaccharide-induced microglial activation and resultant death of neurons by inhibiting TAK1/IKK/NF-κB and JNK/p38 MAPK pathways

International Immunopharmacology

Volumn 10, Issue 6, 2010, Pages 668-678

  Zeng, Ke Wu ^a   Fu, Hong ^a   Liu, Geng Xin ^a   Wang, Xue Mei ^a  

^a PEKING UNIVERSITY FIRST HOSPITAL   (China)

Author keywords

Icariin; Microglia; Mitogen activated protein kinase (MAPK); Neuroinflammatory; Nuclear factor B (NF B)

Indexed keywords

CYCLOOXYGENASE 2; I KAPPA B KINASE; ICARIIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PROSTAGLANDIN E2; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; EMBRYO; ENZYME INHIBITION; GENE EXPRESSION; IMMUNOSUPPRESSIVE TREATMENT; MICROGLIA; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CELL DEATH; CEREBRAL CORTEX; CYCLOOXYGENASE 2; CYTOKINES; DINOPROSTONE; ENCEPHALITIS; FLAVONOIDS; I-KAPPA B KINASE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; MAP KINASE KINASE KINASES; MICROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 77951880056     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2010.03.010     Document Type: Article

References (50)

1. Bo{double acute}ttcher T., von Mering M., Ebert S., Meyding-Lamadé U., Kuhnt U., Gerber J., et al. Differential regulation of Toll-like receptor mRNAs in experimental murine central nervous system infections. Neurosci Lett 344 (2003) 17-20
2. McKimmie C.S., and Fazakerley J.K. In response to pathogens, glial cells dynamically and differentially regulate Toll-like receptor gene expression. J Neuroimmunol 169 (2005) 116-125
3. Harry G.J., and Kraft A.D. Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 4 (2008) 1265-1277
4. Boje K.M. Nitric oxide neurotoxicity in neurodegenerative diseases. Front Biosci 9 (2004) 763-776
5. Block M.L. NADPH oxidase as a therapeutic target in Alzheimer's disease. BMC Neurosci 9 Suppl 2 (2008) 1-8
6. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., et al. Tumor necrosis factor-α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281 (2006) 21362-21368
7. Gruol D.L., and Nelson T.E. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol Neurobiol 15 (1997) 307-339
8. Hartlage-Rübsamen M., Lemke R., and Schliebs R. Interleukin-1beta, inducible nitric oxide synthase, and nuclear factor-kappaB are induced in morphologically distinct microglia after rat hippocampal lipopolysaccharide/interferon-gamma injection. J Neurosci Res 57 (1999) 388-398
9. Damman O., and Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42 (1997) 1-8
10. Zandi E., Rothwarf D.M., Delhase M., Hayakawa M., and Karin M. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91 (1997) 243-252
11. Lee J., Mira-Arbibe L., and Ulevitch R.J. TAK1 regulates multiple protein kinase cascades activated by bacterial lipopolysaccharide. J Leukoc Biol 68 (2000) 909-915
12. Shim J.H., Xiao C.C., Paschal A.E., Bailey S.T., Rao P., Hayden M.S., et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 19 (2005) 2668-2681
13. Wu X.F., and Sun S.C. Retroviral oncoprotein Tax deregulates NF-κB by activating TAK1 and mediating the physical association of TAK1-IKK. EMBO Rep 8 (2007) 510-515
14. Karin M., and Delhase M. The IκB kinase (IKK) and NF-κB: key elements of proinflammatory signalling. Semin Immunol 12 (2000) 85-98
15. Park J.S., Woo M.S., Kim D.H., Hyun J.W., Kim W.K., Lee J.C., et al. Anti-inflammatory mechanisms of isoflavone metabolites in lipopolysaccharide-stimulated microglial cells. J Pharmacol Exp Ther 320 (2007) 1237-1245
16. Bhat N.R., Zhang P., Lee J.C., and Hogan E.L. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J Neurosci 18 (1998) 1633-1641
17. Waetzig V., Czeloth K., Hidding U., Mielke K., Kanzow M., Brecht S., et al. c-Jun N-terminal kinases (JNKs) mediate proinflammatory actions of microglia. Glia 50 (2005) 235-246
18. Zhang P., Hogan E.L., and Bhat N.R. Activation of JNK/SAPK in primary glial cultures: II. differential activation of kinase isoforms corresponds to their differential expression. Neurochem Res 23 (1998) 219-225
19. 2 in vitro. Pharmacol Res 52 (2005) 174-182
20. Liang H.R., Vuorela P., Vuorela H., and Hiltunen R. Isolation and immunomodulatory effect of flavonol glycosides from Epimedium hunanense. Planta Med 63 (1997) 316-319
21. Pan Y., Kong L., Xia X., Zhang W., Xia Z., and Jiang F. Antidepressant-like effect of icariin and its possible mechanism in mice. Pharmacol Biochem Behav 82 (2005) 686-694
22. Chung B.H., Kim J.D., Kim C.K., Kim J.H., Won M.H., Lee H.S., et al. Icariin stimulates angiogenesis by activating the MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways in human endothelial cells. Biochem Biophys Res Commun 376 (2008) 404-408
23. Ding L., Liang X.G., Hu Y., Zhu D.Y., and Lou Y.J. Involvement of p38 MAPK and reactive oxygen species in icariin-induced cardiomyocyte differentiation of murine embryonic stem cells in vitro. Stem Cells Dev 17 (2008) 751-760
24. Wu J.F., Dong J.C., and Xu C.Q. Effect of icariin on inflammation model stimulated by lipopolysaccharide in vitro and in vivo. Zhongguo Zhong Xi Yi Jie He Za Zhi 29 (2009) 330-334
25. Liu M.H., Sun J.S., Tsai S.W., Sheu S.Y., and Chen M.H. Icariin protects murine chondrocytes from lipopolysaccharide-induced inflammatory responses and extracellular matrix degradation. Nutr Res 30 (2010) 57-65
26. Luo Y., Nie J., Gong Q., Lu Y., Wu Q., and Shi J. Protective effect of icariin against learning and memory deficits induced by aluminium in rats. Clin Exp Pharmacol Physiol 34 (2007) 792-795
27. Xu R., Wu Q., Luo Y., Gong Q., Yu L., Huang X., et al. Protective effect of icariin on cognitive deficits induced by chronic cerebral hypoperfusion in rats. Clin Exp Pharmacol Physiol 36 (2009) 810-815
28. Liu X., Fan X.L., Zhao Y., Luo G.R., Li X.P., Li R., et al. Estrogen provides neuroprotection against activated microglia-induced dopaminergic neuronal injury through both estrogen receptor-α and estrogen receptor-β in microglia. J Neurosci Res 81 (2005) 653-665
29. 15N] nitrate in biological samples. Anal Biochem 126 (1982) 131-138
30. Pan X.D., Chen X.C., Zhu Y.G., Chen L.M., Zhang J., Huang T.W., et al. Tripchlorolide protects neuronal cells from microglia-mediated beta-amyloid neurotoxicity through inhibiting NF-κB and JNK signaling. Glia 57 (2009) 1227-1238
31. Xie Z., Smith C.J., and Van Eldik L.J. Activated glia induce neuron death via MAP Kinase signaling pathways involving JNK and p38. Glia 45 (2004) 170-179
32. Goslin K., and Banker G. Rat hippocampal neurons in low density culture. In: Banker G., and Goslin K. (Eds). Culturing nerve cells (1991), MIT Press, Cambridge, MA 251-281
33. Moon D.O., Choi Y.H., Kim N.D., Park Y.M., and Kim G.Y. Anti-inflammatory effect of β-lapachone in lipopolysaccharide-stimulated BV2 microglia. Int Immunopharmacol 7 (2007) 506-514
34. Bi X.L., Yang J.Y., Dong Y.X., Wang J.M., Cui Y.H., Ikeshima T., et al. Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int Immunopharmacol 5 (2005) 185-193
35. Wang T., Qin L., Liu B., Liu Y., Wilson B., Eling T.E., et al. Role of reactive oxygen species in LPS-induced production of prostaglandin E2 in microglia. J Neurochem 88 (2004) 939-947
36. Lin S.T., Wang Y., Xue Y., Feng D.C., Xu Y., and Xu L.Y. Tetrandrine suppresses LPS-induced astrocyte activation via modulating IKKs-IκBα-NF-κB signaling pathway. Mol Cell Biochem 315 (2008) 41-49
37. JO'Neill L.A., and Kaltschmidt C. NF-κB: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20 (1997) 252-258
38. Mercurio F., and Manning A.M. Multiple signals converging on NF-κB. Curr Opin Cell Biol 11 (1999) 226-232
39. Irie T., Muta T., and Takeshige K. TAK1 mediates an activation signal from toll-like receptor(s) to nuclear factor-κB in lipopolysaccharide-stimulated macrophages. FEBS Lett 467 (2000) 160-164
40. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., and Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412 (2001) 346-351
41. Madhavan S., Anghelina M., Sjostrom D., Dossumbekova A., Guttridge D.C., and Agarwal S. Biomechanical signals suppress TAK1 activation to inhibit NF-κB transcriptional activation in fibrochondrocytes. J Immunol 179 (2007) 6246-6254
42. Takaesu G., Surabhi R.M., Park K.J., Tsuji J.N., Matsumoto K., and Gaynor R.B. TAK1 is critical for IκB kinase-mediated activation of the NF-κB pathway. J Mol Biol 326 (2003) 105-115
43. Kaminska B. MAPK signalling pathways as molecular targets for anti-inflammatory therapy-from molecular mechanisms to therapeutic benefits. Biochim Biophys Acta 1754 (2005) 253-262
44. Wang L., Zhang L., Chen Z.B., Wu J.Y., Zhang X., and Xu Y. Icariin enhances neuronal survival after oxygen and glucose deprivation by increasing SIRT1. Eur J Pharmacol 609 (2009) 40-44
45. Yang M.S., Ji K.A., Jeon S.B., Jin B.K., Kim S.U., Jou I., et al. Interleukin-13 enhances cyclooxygenase-2 expression in activated rat brain microglia: implications for death of activated microglia. J Immunol 177 (2006) 1323-1329
46. Oliveira A., Candelario-Jalil E., Bhatia H.S., Lieb K., Hull M., and Fiebich B.L. Regulation of prostaglandin E2 synthase expression in activated primary rat microglia: evidence for uncoupled regulation of mPGES-1 and COX-2. Glia 56 (2008) 844-855
47. Hsu H.Y., and Wen M.H. Lipopolysaccaride-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem 277 (2002) 22131-22139
48. Kim S.H., Smith C.J., and Van Eldik L.J. Importance of MAPK pathways for microglial preinflammatory production cytokine IL-1β. Neurobiol Aging 25 (2004) 431-439
49. Klegeris A., McGeer E.G., and McGeer P.L. Therapeutic approaches to inflammation in neurodegenerative disease. Curr Opin Neurol 20 (2007) 351-357
50. Kim H.P., Son K.H., Chang H.W., and Kang S.S. Anti-inflammatory plant flavonoids and cellular action mechanisms. J Pharmacol Sci 96 (2004) 229-245