Inhibition of nitric oxide production by the carbazole compound LCY-2-CHO via blockade of activator protein-1 and CCAAT/enhancer-binding protein activation in microglia

Biochemical Pharmacology

Volumn 76, Issue 4, 2008, Pages 507-519

  Chang, Ling Chu ^a   Tsao, Lo Ti ^b   Chang, Chi Sen ^b   Chen, Chun Jung ^b   Huang, Li Jiau ^c   Kuo, Sheng Chu ^c   Lin, Ruey Hseng ^a   Wang, Jih Pyang ^b,c  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Activator protein 1; CCAAT enhancer binding protein; Inducible nitric oxide synthase; LCY 2 CHO; Microglial cells; Nitric oxide

Indexed keywords

9 (2 CHLOROBENYL) 9H CARBAZOL 3 CARBALDEHYDE; CARBAZOLE DERIVATIVE; CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; NITRIC OXIDE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DOWN REGULATION; DRUG ACTIVITY; DRUG INHIBITION; DRUG STRUCTURE; DRUG SYNTHESIS; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CARBAZOLES; CCAAT-ENHANCER-BINDING PROTEINS; CELLS, CULTURED; INTERFERON TYPE II; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NUCLEAR PROTEINS; RATS; RNA, MESSENGER; TRANSCRIPTION FACTOR AP-1;

EID: 48149087558     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.06.002     Document Type: Article

References (45)

1. Liu B., Gao H.M., Wang J.Y., Jeohn G.H., Cooper C.L., and Hong J.S. Role of nitric oxide in inflammation-mediated neurodegeneration. Annal N Y Acad Sci 962 (2002) 318-331
2. Marletta M.A. Nitric oxide synthase structure and mechanism. J Biol Chem 268 (1993) 12231-12234
3. Chao C.C., Hu S., Molitor T.W., Shaskan E.G., and Peterson P.K. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149 (1992) 2736-2741
4. Saha R.N., and Pahan K. Regulation of inducible nitric oxide synthase gene in glial cells. Antioxid Redox Signal 8 (2006) 929-947
5. Lee C.Y., Kuo S.C., Teng C.M., and Huang L.J. Synthesis antiplatelet activity of 9-benzyl-3-hydroxymethylcarbazoles. Chin Pharm J 54 (2002) 25-34
6. Lee C.Y., Huang L.J., Wang J.P., and Kuo S.C. Anti-inflammatory activity of 9-substituted benzyl-3-substituted carbazole derivatives. Chin Pharm J 54 (2002) 35-40
7. Tsao L.T., Lee C.Y., Huang L.J., Kuo S.C., and Wang J.P. Inhibition of lipopolysaccharide-stimulated nitric oxide production in RAW 264.7 macrophages by a synthetic carbazole, LCY-2-CHO. Biochem Pharmacol 63 (2002) 1961-1968
8. Ho F.M., Lai C.C., Huang L.J., Kuo T.C., Chao C.M., and Lin W.W. The anti-inflammatory carbazole, LCY-2-CHO, inhibits lipopolysaccharide-induced inflammatory mediator expression through inhibition of the p38 mitogen-activated protein kinase signaling pathway in macrophages. Br J Pharmacol 141 (2004) 1037-1047
9. Ho F.M., Kang H.C., Lee S.T., Chao Y., Chen Y.C., Huang L.J., et al. The anti-inflammatory actions of LCY-2-CHO, a carbazole analogue, in vascular smooth muscle cells. Biochem Pharmacol 74 (2007) 298-308
10. Hsu M.J., Chao Y., Chang Y.H., Ho F.M., Huang L.J., Huang Y.L., et al. Cell apoptosis induced by a synthetic carbazole compound LCY-2-CHO is mediated through activation of caspase and mitochondrial pathways. Biochem Pharmacol 70 (2005) 102-112
11. Corradin S.B., Manuel J., Donini S.D., Quattrocchi E., and Ricciardi-Castagnoli P. Inducible nitric oxide synthase activity of cloned murine microglial cells. Glia 7 (1993) 255-262
12. Bocchini V., Mazzolla R., Barluzzi R., Blasi E., Sick P., and Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J Neurosci Res 31 (1992) 616-621
13. Wang M.J., Huang H.M., Hsieh S.J., Jeng K.C., and Kuo J.S. Resveratrol inhibits interleukin-6 production in cortical mixed glial cells under hypoxia/hypoglycemia followed by reoxygenation. J Neuroimmunol 112 (2001) 28-34
14. Chen C.C., Wang J.K., and Lin S.B. Antisense oligonucleotides targeting protein kinase C-α, -βI, or -δ but not -η inhibit lipopolysaccharide-induced nitric oxide synthase expression in RAW 264.7 macrophages: involvement of a nuclear factor κB-dependent mechanism. J Immunol 161 (1998) 6206-6214
15. Velasco M., Diaz-Guerra M.J., Diaz-Achirica P., Rivas L., and Bosca L. Macrophage triggering with cecropin A and melittin-derived peptides induces type II nitric oxide synthase expression. J Immunol 158 (1997) 4437-4443
16. Tsi C.J., Chao Y., Chen C.W., and Lin W.W. Aurintricarboxylic acid protects against cell death caused by lipopolysaccharide in macrophages by decreasing inducible nitric-oxide synthase induction via IκB kinase, extracellular signal-regulated kinase, and p38 mitogen-activated protein kinase inhibition. Mol Pharmacol 62 (2002) 90-101
17. Woo K.J., Lim J.H., Suh S.I., Kwon Y.K., Shin S.W., Kim S.C., et al. Differential inhibitory effects of baicalein and baicalin on LPS-induced cycloxoxygenase-2 expression through inhibition of C/EBPβ DNA-binding activity. Immunobiology 221 (2006) 359-368
18. Chen C.J., Rung S.L., Liao S.L., and Chen S.Y. Inhibition of inducible nitric oxide synthase expression by baicalein in endotoxin-cytokine-stimulated microglia. Biochem Pharmacol 67 (2004) 957-965
19. Lockhart B.P., Cressey K.C., and Lepagnol J.M. Suppression of nitric oxide formation by tyrosine kinase inhibitors in murine N9 microglia. Br J Pharmacol 123 (1998) 879-889
20. Garvey E.P., Oplinger J.A., Furfine E.S., Kiff R.J., Laszlo F., Whittle B.J., et al. 1400 W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 272 (1997) 4959-4963
21. Kim M.O., Si Q., Zhou J.N., Pestell R.G., Brosnan C.F., Locker J., et al. Interferon-β activates multiple signaling cascades in primary human microglia. J Neurochem 81 (2002) 1361-1371
22. Descombes P., and Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67 (1991) 569-579
23. Karin M., Liu Z., and Zandi E. AP-1 function and regulation. Curr Opin Cell Biol 9 (1997) 240-246
24. Chrivia J.C., Kwok R.P., Lamb N., Hagiwara M., Montminy M.R., and Goodman R.H. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365 (1993) 855-859
25. Williams S.C., Baer M., Dillner A.J., and Johnson P.F. CRP2 (C/EBPβ) contains a bipartite regulatory domain that controls transcriptional activation, DNA-binding and cell specificity. EMBO J 14 (1995) 3170-3183
26. Ejarque-Ortiz A., Mediana M.G., Tusell J.M., Perez-Gonzalez A.P., Serratosa J., and Saura J. Upregulation of CCAAT/enhancer-binding protein β in activated asrocytes and microglia. Glia 55 (2007) 178-188
27. Bradley M.N., Zhou L., and Smale S.T. C/EBPβ regulation in lipopolysaccharide-stimulated macrophages. Mol Cell Biol 23 (2003) 4841-4858
28. 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-α gene expression in endotoxin-stimulated primary glial cultures. J Neurosci 18 (1998) 1633-1641
29. Krens S.F.G., Spaink H.P., and Snaar-Jagalska B.E. Functions of the MAPK family in vertebrate-development. FEBS Lett 580 (2006) 4984-4990
30. Hambleton J., Weinstein S.L., Lem L., and DeFranco A.L. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc Natl Acad Sci USA 93 (1996) 2774-2778
31. Cano E., and Mahadevan L.C. Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20 (1995) 117-122
32. Derijard B., Hibi M., Wu I.H., Barrett T., Su B., Deng T., et al. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76 (1994) 1025-1037
33. Waldmann I., Walde S., and Kehlenbach R.H. Nuclear import of c-Jun is mediated by multiple transport receptors. J Biol Chem 282 (2007) 27685-27692
34. Carter A.B., Knudtson K.L., Monick M.M., and Hunninghake G.W. The p38 mitogen-activated protein kinase is required for NF-κB-dependent gene expression. The role of TATA-binding protein (TBP). J Biol Chem 274 (1999) 30858-30863
35. Kitamura Y., Takahashi H., Normura Y., and Taniguchi T. Possible involvement of Janus kinase Jak2 in interferon-γ induction of nitric oxide synthase in rat glial cells. Eur J Pharmacol 306 (1996) 297-306
36. Gao J., Morrison D.C., Parmely T.J., Russell S.W., and Murphy W.J. An interferon-γ-activated site (GSA) is necessary for full expression of the mouse iNOS gene in response to interferon-γ and lipopolysaccharide. J Biol Chem 272 (1997) 1226-1230
37. Sprott K.M., Chumley M.J., Hanson J.M., and Dobrowsky R.T. Decreased activity and enhanced nuclear export of CCAAT-enhancer-binding protein β during inhibition of adipogenesis by ceramide. Biochem J 365 (2002) 181-191
38. Lee S.J., and Kim S.G. Role of p90 ribosomal S6-kinase-1 in oltipraz-induced specific phosphorylation of CCAAT/enhancer-binding protein-β for GSTA2 gene transactivation. Mol Pharmacol 69 (2006) 385-396
39. Nakajima T., Kinoshita S., Sasagawa T., Sasaki K., Naruto M., Kishimoto T., et al. Phosphorylation at threonine-235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6. Proc Natl Acad Sci USA 90 (1993) 2207-2211
40. Zhang Y., Sif S., and DeWille J. The mouse C/EBPδ gene promoter is regulated by STAT3 and Sp1 transcriptional activators, chromatin remodeling and c-Myc repression. J Cell Biochem 102 (2007) 1256-1270
41. Chinery R., Brockman J.A., Dransfield D.T., and Coffey R.J. Antioxidant-induced nuclear translocation of CCAAT/Enhancer-binding protein β. A critical role for protein kinase A-mediated phosphorylation of Ser299. J Biol Chem 272 (1997) 30356-30361
42. Hagiwara M., Brindle P., Harootunian A., Armstrong R., Rivier J., Vale W., et al. Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol 13 (1993) 4852-4859
43. Nakamura Y., Si Q.S., and Kataoka K. Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci Res 35 (1999) 95-100
44. Zhang B., Yang L., Konishi Y., Maeda N., Sakanaka M., and Tanaka J. Suppressive effects of phosphodiesterase type IV inhibitors in rat cultured microglial cells: comparison with other types of cAMP-elevating agents. Neuropharmacology 42 (2002) 262-269
45. Akira S. IL-6-regulated transcription factors. Int J Biochem Cell Biol 29 (1997) 1401-1418