1-O-tigloyl-1-O-deacetyl-nimbolinin B inhibits LPS-stimulated inflammatory responses by suppressing NF-κB and JNK activation in microglia cells

Journal of Pharmacological Sciences

Volumn 125, Issue 4, 2014, Pages 364-374

  Tao, Li ^a   Zhang, Fali ^a   Hao, Lili ^a   Wu, Jing ^a   Jia, Jia ^a   Liu, Jiang Yun ^a   Zheng, Long Tai ^a   Zhen, Xuechu ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

1 O tigloyl 1 O deacetyl nimbolinin B; Inflammation; Lipopolysaccharide; Microglia; Neuroprotection

Indexed keywords

1 O TIGLOYL 1 O DEACETYL NIMBOLININ B; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CYCLOOXYGENASE 2; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LIMONOID; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NIMBOLININ A; NIMBOLININ B; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 1-O-TIGLOYL-1-O-DEACETYLNIMBOLININ B; ANTIINFLAMMATORY AGENT; NEUROPROTECTIVE AGENT; PTGS2 PROTEIN, MOUSE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN CELL; CELL ASSAY; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; FRUIT; GENE EXPRESSION; GENE REPRESSION; HT 22 CELL; MELIA; MELIA TOOSENDAN; MICROGLIA; MOUSE; NERVE CELL CULTURE; NEUROBLASTOMA CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED; CHEMISTRY; CYTOLOGY; GENETICS; HIPPOCAMPUS; INFLAMMATION; ISOLATION AND PURIFICATION; METABOLISM; MOLECULARLY TARGETED THERAPY; NEURODEGENERATIVE DISEASES;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELLS, CULTURED; CYCLOOXYGENASE 2; HIPPOCAMPUS; INFLAMMATION; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIMONINS; LIPOPOLYSACCHARIDES; MELIA; MICE; MICROGLIA; MOLECULAR TARGETED THERAPY; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84906960196     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.14025FP     Document Type: Article

References (57)

1. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007; 8:57-69.
2. Amor S, Puentes F, Baker D., van der Valk P. Inflammation in neurodegenerative diseases. Immunology. 2010; 129:154-169.
3. Streit WJ. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia. 2002; 40:133-139.
4. Nakajima K, Kohsaka S. Microglia: activation and their significance in the central nervous system. J Biochem. 2001; 130: 169-175.
5. Furuyashiki T. Roles of dopamine and inflammation-related molecules in behavioral alterations caused by repeated stress. J Pharmacol Sci. 2012; 120:63-69.
6. Meda L, Cassatella MA, Szendrei G.I., Otvos L Jr, Baron P, Villalba M, et al. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature. 1995; 374:647-650.
7. Dandona P, Ghanim H, Chaudhuri A., Dhindsa S, Kim SS. Macronutrient intake induces oxidative and inflammatory stress: potential relevance to atherosclerosis and insulin resistance. Exp Mol Med. 2010; 42:245-253.
8. McGeer PL, McGeer EG. Glial cell reactions in neurodegenerative diseases: pathophysiology and therapeutic interventions. Alzheimer Dis Assoc Disord. 1998; 12 Suppl 2:S1-S6.
9. Nakamura Y, Si QS, Kataoka K. Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci Res. 1999; 35:95-100.
10. Gao HM, Liu B, Hong JS. Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J Neurosci. 2003; 23:6181-6187.
11. McGeer PL, Schwab C, Parent A., Doudet D. Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration. Ann Neurol. 2003; 54:599-604.
12. Manners GD. Citrus limonoids: analysis, bioactivity, and biomedical prospects. J Agric Food Chem. 2007; 55:8285-8294.
13. Roy A, Saraf S. Limonoids: overview of significant bioactive triterpenes distributed in plants kingdom. Biol Pharm Bull. 2006; 29:191-201.
14. Morgan ED. Azadirachtin, a scientific gold mine. Bioorg Med Chem. 2009; 17:4096-4105.
15. Xie F, Zhang M, Zhang C.F., Wang ZT, Yu BY, Kou JP. Anti-inflammatory and analgesic activities of ethanolic extract and two limonoids from Melia toosendan fruit. J Ethnopharmacol. 2008; 117:463-466.
16. Zhang Y, Tang CP, Ke C.Q., Li XQ, Xie H, Ye Y. Limonoids from the fruits of Melia toosendan. Phytochemistry. 2012; 73:106-113.
17. Alam A, Haldar S, Thulasiram H.V., Kumar R., Goyal M, Iqbal MS, et al. Novel anti-inflammatory activity of epoxyazadiradione against macrophage migration inhibitory factor: inhibition of tautomerase and proinflammatory activities of macrophage migration inhibitory factor. J Biological Chem. 2012; 287: 24844-24861.
18. Su S, Shen L, Zhang Y., Liu J, Cai J, Hao L., et al. Characterization of tautomeric limonoids from the fruits of Melia toosendan. Phytochem Lett. 2013; 6:418-424.
19. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci. 1986; 6: 2163-2178.
20. Lee S, Suk K. Heme oxygenase-1 mediates cytoprotective effects of immunostimulation in microglia. Biochem Pharmacol. 2007; 74:723-729.
21. Zheng LT, Hwang J, Ock J., Lee MG, Lee WH, Suk K. The antipsychotic spiperone attenuates inflammatory response in cultured microglia via the reduction of proinflammatory cytokine expression and nitric oxide production. J Neurochem. 2008; 107: 1225-1235.
22. Oh GS, Pae HO, Lee B.S., Kim BN, Kim JM, Kim HR, et al. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med. 2006; 41:106-119.
23. Park SY, Lee H, Hur J., Kim SY, Kim H, Park JH, et al. Hypoxia induces nitric oxide production in mouse microglia via p38 mitogen-activated protein kinase pathway. Brain Res Mol Brain Res. 2002; 107:9-16.
24. Zheng LT, Ock J, Kwon B.M., Suk K. Suppressive effects of flavonoid fisetin on lipopolysaccharide-induced microglial activation and neurotoxicity. Int Immunopharmacol. 2008; 8: 484-494.
25. Ananth C, Gopalakrishnakone P, Kaur C. Induction of inducible nitric oxide synthase expression in activated microglia following domoic acid (DA)-induced neurotoxicity in the rat hippocampus. Neurosci Lett. 2003; 338:49-52.
26. Sung B, Pandey MK, Aggarwal BB. Fisetin, an inhibitor of cyclin-dependent kinase 6, down-regulates nuclear factor-kappaB-regulated cell proliferation, antiapoptotic and metastatic gene products through the suppression of TAK-1 and receptor-interacting protein-regulated IkappaBalpha kinase activation. Mol Pharmacol. 2007; 71:1703-1714.
27. Merson TD, Binder MD, Kilpatrick TJ. Role of cytokines as mediators and regulators of microglial activity in inflammatory demyelination of the CNS. Neuromol Med. 2010; 12:99-132.
28. Zheng LT, Ryu GM, Kwon B.M., Lee WH, Suk K. Anti-inflammatory effects of catechols in lipopolysaccharide-stimulated microglia cells: inhibition of microglial neurotoxicity. Eur J Pharmacol. 2008; 588:106-113.
29. Nishioku T, Matsumoto J, Dohgu S., Sumi N, Miyao K, Takata F., et al. Tumor necrosis factor-alpha mediates the blood-brain barrier dysfunction induced by activated microglia in mouse brain microvascular endothelial cells. J Pharmacol Sci. 2010; 112:251-254.
30. Lee SJ, Bai SK, Lee K.S., Namkoong S., Na HJ, Ha KS, et al. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing I(kappa)B kinase-dependent NF-kappaB activation. Mol Cells. 2003; 16:97-105.
31. Kang CH, Jayasooriya RG, Choi Y.H., Moon SK, Kim WJ, Kim G Y. beta-Ionone attenuates LPS-induced pro-inflammatory mediators such as NO, PGE2 and TNF-alpha in BV2 microglial cells via suppression of the NF-kappaB and MAPK pathway. Toxicol In Vitro. 2013; 27:782-787.
32. More SV, Park JY, Kim B.W., Kumar H., Lim HW, Kang SM, et al. Anti-neuroinflammatory activity of a novel cannabinoid derivative by inhibiting the NF-kappaB signaling pathway in lipo-polysaccharide-induced BV-2 microglial cells. J Pharmacol Sci. 2013; 121:119-130.
33. Kang G, Kong PJ, Yuh Y.J., Lim SY, Yim SV, Chun W, et al. Curcumin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression by inhibiting activator protein 1 and nuclear factor kappab bindings in BV2 microglial cells. J Pharmacol Sci. 2004; 94:325-328.
34. Wang S, Wang H, Guo H., Kang L, Gao X, Hu L. Neuroprotection of Scutellarin is mediated by inhibition of microglial inflammatory activation. Neuroscience. 2011; 185:150-160.
35. Jongeneel CV. Transcriptional regulation of the tumor necrosis factor alpha gene. Immunobiology. 1995; 193:210-216.
36. Kim BW, Koppula S, Kim I.S., Lim HW, Hong SM, Han SD, et al. Anti-neuroinflammatory activity of Kamebakaurin from Isodon japonicus via inhibition of c-Jun NH(2)-terminal kinase and p38 mitogen-activated protein kinase pathway in activated microglial cells. J Pharmacol Sci. 2011; 116:296-308.
37. Park HY, Han MH, Park C, Jin C.Y., Kim GY, Choi IW, et al. Anti-inflammatory effects of fucoidan through inhibition of NF-kappaB, MAPK and Akt activation in lipopolysaccharide-induced BV2 microglia cells. Food Chem Toxicol. 2011; 49: 1745-1752.
38. Minghetti L, Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol. 1998; 54:99-125.
39. Qian L, Flood PM, Hong JS. Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm. 2010; 117:971-979.
40. Takata K, Kitamura Y. Molecular approaches to the treatment, prophylaxis, and diagnosis of Alzheimer's disease: tangle formation, amyloid-beta, and microglia in Alzheimer's disease. J Pharmacol Sci. 2012; 118:331-337.
41. Kim YS, Joh TH. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med. 2006; 38:333-347.
42. Cacci E, Ajmone-Cat MA, Anelli T., Biagioni S, Minghetti L. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia. 2008; 56:412-425.
43. Boje KM, Arora PK. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 1992; 587:250-256.
44. Chao CC, Hu S, Molitor T.W., Shaskan EG, Peterson PK. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol. 1992; 149:2736-2741.
45. Smith JA, Das A, Ray S.K., Banik NL. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull. 2012; 87:10-20.
46. Saccani S, Pantano S, Natoli G. Two waves of nuclear factor kappaB recruitment to target promoters. J Exp Med. 2001; 193: 1351-1359.
47. Ramirez-Carrozzi VR, Braas D, Bhatt D.M., Cheng CS, Hong C, Doty KR, et al. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell. 2009; 138:114-128.
48. Lebron F, Vassallo R, Puri V., Limper AH. Pneumocystis carinii cell wall beta-glucans initiate macrophage inflammatory responses through NF-kappaB activation. J Biol Chem. 2003; 278:25001-25008.
49. Karin M, Yamamoto Y, Wang QM. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov. 2004; 3:17-26.
50. Viatour P, Merville MP, Bours V, Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci. 2005; 30:43-52.
51. Jeon NR, Koppula S, Kim B.W., Park SH, Lee HW, Choi DK. MMHD [(S, E)-2-methyl-1-(2-methylthiazol-4-yl) hexa-1,5-dien-ol], a novel synthetic compound derived from epothilone, suppresses nuclear factor-kappaB-mediated cytokine expression in lipopolysaccharide-stimulated BV-2 microglia. J Pharmacol Sci. 2010; 112:158-166.
52. Kavitha K, Vidya Priyadarsini R, Anitha P, Ramalingam K., Sakthivel R, Purushothaman G, et al. Nimbolide, a neem limonoid abrogates canonical NF-kappaB and Wnt signaling to induce caspase-dependent apoptosis in human hepatocarcinoma (HepG2) cells. Eur J Pharmacol. 2012; 681:6-14.
53. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine. 2008; 42:145-151.
54. Kim SH, Smith CJ, Van Eldik LJ. Importance of MAPK pathways for microglial pro-inflammatory cytokine IL-1 beta production. Neurobiol Aging. 2004; 25:431-439.
55. Aguirre Moreno AC, Campos Pena V, Villeda Hernandez J, Leon Rivera I, Montiel Arcos E. Ganoderma lucidum reduces kainic acid-induced hippocampal neuronal damage via inflammatory cytokines and glial fibrillary acid protein expression. Proc West Pharmacol Soc. 2011; 54:78-79.
56. Chinta SJ, Rajagopalan S, Ganesan A., Andersen JK. A possible novel anti-inflammatory mechanism for the pharmacological prolyl hydroxylase inhibitor 3,4-dihydroxybenzoate: implications for use as a therapeutic for Parkinson's disease. Parkinsons Dis. 2012; 2012:364684.
57. Han L, Yin K, Zhang S., Wu Z, Wang C, Zhang Q., et al. Dale-sconols B inhibits lipopolysaccharide induced inflammation and suppresses NF-kappaB and p38/JNK activation in microglial cells. Neurochem Int. 2013; 62:913-921.