Tetramethylpyrazine inhibits production of nitric oxide and inducible nitric oxide synthase in lipopolysaccharide-induced N9 microglial cells through blockade of MAPK and PI3K/Akt signaling pathways, and suppression of intracellular reactive oxygen species

Journal of Ethnopharmacology

Volumn 129, Issue 3, 2010, Pages 335-343

  Liu, Hong Tao ^a   Du, Yu Guang ^b   He, Jun Lin ^a   Chen, Wen Juan ^a   Li, Wen Ming ^a   Yang, Zhu ^a   Wang, Ying Xiong ^a   Yu, Chao ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

Author keywords

Inducible nitric oxide synthase; Inflammation; Microglial cell; Mitogen activated protein kinase; PI3 kinase; Tetramethylpyrazine

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; NITRITE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TETRAMETHYLPYRAZINE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL LYSATE; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; DRUG EXPOSURE; FLUORESCENCE; INHIBITION KINETICS; MICROGLIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; CYTOSOL; DOSE-RESPONSE RELATIONSHIP, DRUG; FREE RADICAL SCAVENGERS; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; ONCOGENE PROTEIN V-AKT; PYRAZINES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77953355877     PISSN: 03788741     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jep.2010.03.037     Document Type: Article

References (50)

1. Bae J.H., Jang B.C., Suh S.I., Ha E., Baik H.H., Kim S.S., Lee M.Y., Shin D.H. Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells. Neuroscience Letters 2006, 398:151-154.
2. Bal-Price A., Brown G.C. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. Journal of Neuroscience 2001, 21:6480-6491.
3. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., Landreth G.E. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. Journal of Neuroscience 2003, 23:2665-2674.
4. Bhat N.R., Fan F. Adenovirus infection induces microglial activation: involvement of mitogen-activated protein kinase pathways. Brain Research 2002, 948:93-101.
5. Bi X.L., Yang J.Y., Dong Y.X., Wang J.M., Cui Y.H., Ikeshima T., Zhao Y.Q., Wu C.F. Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. International Immunopharmacology 2005, 5:185-193.
6. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nature Reviews Neuroscience 2007, 8:57-69.
7. Brochu S., Olivier M., Rivest S. Neuronal activity and transcription of proinflammatory cytokines, IkappaBalpha, and iNOS in the mouse brain during acute endotoxemia and chronic infection with Trypanosoma brucei. Journal of Neuroscience Research 1999, 57:801-816.
8. Chang Y., Lee J.J., Hsieh C.Y., Hsiao G., Chou D.S., Sheu J.R. Inhibitory effects of ketamine on lipopolysaccharide-induced microglial activation. Mediators of Inflammation 2009, 2009:705379.
9. Fu Y.S., Lin Y.Y., Chou S.C., Tsai T.H., Kao L.S., Hsu S.Y., Cheng F.C., Shih Y.H., Cheng H., Fu Y.Y., Wang J.Y. Tetramethylpyrazine inhibits activities of glioma cells and glutamate neuro-excitotoxicity: potential therapeutic application for treatment of gliomas. Neuro-Oncology 2008, 10:139-152.
10. Garrido G., Delgado R., Lemus Y., Rodríguez J., García D., Núñez-Sellés A.J. Protection against septic shock and suppression of tumor necrosis factor alpha and nitric oxide production on macrophages and microglia by a standard aqueous extract of Mangifera indica L. (VIMANG). Pharmacological Research 2004, 50:165-172.
11. Hwang S.Y., Jung J.S., Lim S.J., Kim J.Y., Kim T.H., Cho K.H., Han I.O. LY294002 inhibits interferon-gamma-stimulated inducible nitric oxide synthase expression in BV2 microglial cells. Biochemical and Biophysical Research Communications 2004, 318:691-697.
12. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002, 40:156-163.
13. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
14. Jung H.W., Yoon C.H., Park K.M., Han H.S., Park Y.K. Hexane fraction of Zingiberis Rhizoma Crudus extract inhibits the production of nitric oxide and proinflammatory cytokines in LPS-stimulated BV2 microglial cells via the NF-kappaB pathway. Food and Chemical Toxicology 2009, 47:1190-1197.
15. Kang J., Park E.J., Jou I., Kim J.H., Joe E.H. Reactive oxygen species mediate A beta(25-35)-induced activation of BV-2 microglia. Neuroreport 2001, 12:1449-1452.
16. Kao T.K., Ou Y.C., Kuo J.S., Chen W.Y., Liao S.L., Wu C.W., Chen C.J., Ling N.N., Zhang Y.H., Peng W.H. Neuroprotection by tetramethylpyrazine against ischemic brain injury in rats. Neurochemistry International 2006, 48:166-176.
17. Kauffmann-Zeh A., Rodriguez-Viciana P., Ulrich E., Gilbert C., Coffer P., Downward J., Evan G. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 1997, 385:544-548.
18. Kilic B., Kruse M., Stahlmann R. The in vitro effects of quinupristin/dalfopristin, erythromycin and levofloxacin at low concentrations on the expression of different cell adhesion molecules on the surface of endothelial cells (Eahy926). Toxicology 2006, 218:30-38.
19. Kim W.K., Hwang S.Y., Oh E.S., Piao H.Z., Kim K.W., Han I.O. TGF-beta1 represses activation and resultant death of microglia via inhibition of phosphatidylinositol 3-kinase activity. Journal of Immunology 2004, 172:7015-7023.
20. Koh K., Cha Y., Kim S., Kim J. tBHQ inhibits LPS-induced microglial activation via Nrf2-mediated suppression of p38 phosphorylation. Biochemical and Biophysical Research Communications 2009, 380:449-453.
21. Lee W.S., Yang H.Y., Kao P.F., Liu J.C., Chen C.H., Cheng T.H., Chan P. Tetramethylpyrazine downregulates angiotensin II-induced endothelin-1 gene expression in vascular endothelial cells. Clinical and Experimental Pharmacology and Physiology 2005, 32:845-850.
22. Liang C.C., Hong C.Y., Chen C.F., Tsai T.H. Measurement and pharmacokinetic study of tetramethylpyrazine in rat blood and its regional brain tissue by high-performance liquid chromatography. Journal of Chromatography B: Biomedical Sciences and Application 1999, 724:303-309.
23. Liu C.F., Lin M.H., Lin C.C., Chang H.W., Lin S.C. Protective effect of tetramethylpyrazine on absolute ethanol-induced renal toxicity in mice. Journal of Biomedical Science 2002, 9:299-302.
24. Ma J., Hwang Y.K., Cho W.H., Han S.H., Hwang J.K., Han J.S. Macelignan attenuates activations of mitogen-activated protein kinases and nuclear factor kappa B induced by lipopolysaccharide in microglial cells. Biological & Pharmaceutical Bulletin 2009, 32:1085-1090.
25. Marcocci L., Maguire J.J., Droy-Lefaix M.T., Packer L. The nitric oxide-scavenging properties of Ginkgo biloba extract EGb 761. Biochemical and Biophysical Research Communications 1994, 201:748-755.
26. Meng X.L., Yang J.Y., Chen G.L., Zhang L.J., Wang L.H., Li J., Wang J.M., Wu C.F. RV09, a novel resveratrol analogue, inhibits NO and TNF-alpha production by LPS-activated microglia. International Immunopharmacology 2008, 8:1074-1082.
27. Min K.J., Pyo H.K., Yang M.S., Ji K.A., Jou I., Joe E.H. Gangliosides activate microglia via protein kinase C and NADPH oxidase. Glia 2004, 48:197-206.
28. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews 1991, 43:109-142.
29. Mukaida N., Ishikawa Y., Ikeda N., Fujioka N., Watanabe S., Kuno K., Matsushima K. Novel insight into molecular mechanism of endotoxin shock: biochemical analysis of LPS receptor signaling in a cell-free system targeting NF-kappaB and regulation of cytokine production/action through beta2 integrin in vivo. Journal of Leukocyte Biology 1996, 59:145-151.
30. Nizamutdinova I.T., Jeong J.J., Xu G.H., Lee S.H., Kang S.S., Kim Y.S., Chang K.C., Kim H.J. Hesperidin, hesperidin methyl chalone and phellopterin from Poncirus trifoliata (Rutaceae) differentially regulate the expression of adhesion molecules in tumor necrosis factor-alpha-stimulated human umbilical vein endothelial cells. International Immunopharmacology 2008, 8:670-678.
31. Ock J., Kim S., Suk K. Anti-inflammatory effects of a fluorovinyloxyacetamide compound KT-15087 in microglia cells. Pharmacological Research 2009, 59:414-422.
32. Oh Y.T., Lee J.Y., Lee J., Kim H., Yoon K.S., Choe W., Kang I. Oleic acid reduces lipopolysaccharide-induced expression of iNOS and COX-2 in BV2 murine microglial cells: possible involvement of reactive oxygen species, p38 MAPK, and IKK/NF-kappaB signaling pathways. Neuroscience Letters 2009, 464:93-97.
33. Pawate S., Shen Q., Fan F., Bhat N.R. Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. Journal of Neuroscience Research 2004, 77:540-551.
34. Qi X., Ackermann C., Sun D., Liu R., Sheng M., Hou H. The prediction of plasma and brain levels of 2,3,5,6-tetramethylpyrazine following transdermal application. AAPS PharmSci. 2002, 4:E46.
35. Qin L., Liu Y., Wang T., Wei S.J., Block M.L., Wilson B., Liu B., Hong J.S. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. Journal of Biological Chemistry 2004, 279:1415-1421.
36. Rajan S., Ye J., Bai S., Huang F., Guo Y.L. NF-kappaB, but not p38 MAP kinase, is required for TNF-alpha-induced expression of cell adhesion molecules in endothelial cells. Journal of Cellular Biochemistry 2008, 105:477-486.
37. Sheu J.R., Kan Y.C., Hung W.C., Lin C.H., Yen M.H. The antiplatelet activity of tetramethylpyrazine is mediated through activation of NO synthase. Life Science 2000, 67:937-947.
38. So E.C., Wong K.L., Huang T.C., Tasi S.C., Liu C.F. Tetramethylpyrazine protects mice against thioacetamide-induced acute hepatotoxicity. Journal of Biomedical Science 2002, 9:410-414.
39. Stoll G., Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Progress in Neurobiology 1999, 58:233-247.
40. Tan Z. Neural protection by naturopathic compounds-an example of tetramethylpyrazine from retina to brain. Journal of Ocular Biology, Diseases, and Informatics 2009, 2:57-64.
41. Tarozzi A., Morroni F., Hrelia S., Angeloni C., Marchesi A., Cantelli-Forti G., Hrelia P. Neuroprotective effects of anthocyanins and their in vivo metabolites in SH-SY5Y cells. Neuroscience Letter 2007, 424:36-40.
42. Tsai T.H., Liang C. Pharmacokinetics of tetramethylpyrazine in rat blood and brain using microdialysis. International Journal of Pharmaceutics 2001, 216:61-66.
43. Wang B., Navath R.S., Romero R., Kannan S., Kannan R. Anti-inflammatory and anti-oxidant activity of anionic dendrimer-N-acetyl cysteine conjugates in activated microglial cells. International Journal of Pharmaceutics 2009, 377:159-168.
44. Wu C.C., Liao M.H., Chen S.J., Yen M.H. Tetramethylpyradizine prevents inducible NO synthase expression and improves survival in rodent models of endotoxic shock. Naunyn-Schmiedeberg's Archives of Pharmacology 1999, 360:435-444.
45. Xie Q.W., Kashiwabara Y., Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. Journal of Biological Chemistry 1994, 269:4705-4708.
46. Xu S.Z., Zhong W., Watson N.M., Dickerson E., Wake J.D., Lindow S.W., Newton C.J., Atkin S.L. Fluvastatin reduces oxidative damage in human vascular endothelial cells by upregulating Bcl-2. Journal of Thrombosis and Haemostasis 2008, 6:692-700.
47. Zhang Z., Wei T., Hou J., Li G., Yu S., Xin W. Tetramethylpyrazine scavenges superoxide anion and decreases nitric oxide production in human polymorphonuclear leukocytes. Life Science 2003, 72:2465-2472.
48. Zheng H., Chen X.L., Han Z.X., Wang S.Y., Chen Z.W. Effect of Ligustrazine on liver injury after burn trauma. Burns 2006, 32:328-334.
49. Zhou Y., Hu C.P., Deng P.Y., Deng H.W., Li Y.J. The protective effects of ligustrazine on schemia-reperfusion and DPPH free radical-induced myocardial injury in isolated rat hearts. Planta Med. 2004, 70:818-822.
50. Zhu Y.M., Azahri N.S., Yu D.C., Woll P.J. Effects of COX-2 inhibition on expression of vascular endothelial growth factor and interleukin-8 in lung cancer cells. BMC Cancer 2008, 8:218.