Oroxylin A exerts anti-inflammatory activity on lipopolysaccharide-induced mouse macrophage via Nrf2/ARE activation

Biochemistry and Cell Biology

Volumn 92, Issue 5, 2014, Pages 337-348

  Ye, Ming ^a   Wang, Qing ^b   Zhang, Weifeng ^a   Li, Zhiyu ^a   Wang, Yajing ^a   Hu, Rong ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b WUXI NO 2 PEOPLE S HOSPITAL   (China)

Author keywords

Inflammation; Lipopolysaccharide (LPS); Macrophages; Nuclear factor erythroid 2 related factor 2 (Nrf2); Oroxylin A

Indexed keywords

DISEASES; MACROPHAGES; PROTEINS;

ANTI-INFLAMMATORY ACTIVITY; ANTIOXIDANT RESPONSE ELEMENTS; INFLAMMATION; INFLAMMATORY DISEASE; LIPOPOLYSACCHARIDES; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; OROXYLIN A; THERAPEUTIC STRATEGY;

PATHOLOGY;

BETA ACTIN; CYCLOOXYGENASE 2; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LAMIN A; LIPOPOLYSACCHARIDE; LUCIFERASE; MESSENGER RNA; NADP(H) QUINONE OXIDOREDUCTASE; OROXYLIN A; PROTEASOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; 5,7-DIHYDROXY-6-METHOXY-2-PHENYLCHROMEN-4-ONE; FLAVONOID; NFE2L2 PROTEIN, MOUSE; NONSTEROID ANTIINFLAMMATORY AGENT; NQO1 PROTEIN, MOUSE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL NUCLEUS; CELL VIABILITY ASSAY; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UBIQUITINATION; UPREGULATION; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; CYCLOOXYGENASE 2; FLAVONOIDS; HEME OXYGENASE-1; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; NITRIC OXIDE SYNTHASE TYPE II; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; UBIQUITINATION;

EID: 84910010311     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/bcb-2014-0030     Document Type: Article

References (50)

1. Akira S. Uematsu S. Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell, 124 (4): 783-801. 10.1016/j.cell.2006.02.015. 16497588.
2. Chen X.L. Varner S.E. Rao A.S. Grey J.Y. Thomas S. Cook C.K. et al 2003. Laminar flow induction of antioxidant response element-mediated genes in endothelial cells. A novel anti-inflammatory mechanism. J. Biol. Chem. 278 (2): 703-711. 10.1074/jbc.M203161200. 12370194.
3. Chen Y. Yang L. Lee T.J. 2000. Oroxylin A inhibition of lipopolysaccharide-induced iNOS and COX-2 gene expression via suppression of nuclear factor-kappaB activation. Biochem. Pharmacol. 59 (11): 1445-1457. 10.1016/S0006-2952(00)00255-0. 10751555.
4. Chi Y.S. Lim H. Park H. Kim H.P. 2003. Effects of wogonin, a plant flavone from Scutellaria radix, on skin inflammation: in vivo regulation of inflammation-associated gene expression. Biochem. Pharmacol. 66 (7): 1271-1278. 10.1016/S0006-2952(03)00463-5. 14505806.
5. Chung S.W. Chen Y.H. Yet S.F. Layne M.D. Perrella M.A. 2006. Endotoxin-induced down-regulation of Elk-3 facilitates heme oxygenase-1 induction in macrophages. J. Immunol. 176 (4): 2414-2420. 10.4049/jimmunol.176.4.2414. 16456000.
6. Chung W.Y. Park J.H. Kim M.J. Kim H.O. Hwang J.K. Lee S.K. Park K.K. 2007. Xanthorrhizol inhibits 12-O-tetradecanoylphorbol-13-acetate-induced acute inflammation and two-stage mouse skin carcinogenesis by blocking the expression of ornithine decarboxylase, cyclooxygenase-2 and inducible nitric oxide synthase through mitogen-activated protein kinases and/or the nuclear factor-kappa B. Carcinogenesis, 28 (6): 1224-1231. 10.1093/carcin/bgm005. 17234720.
7. Dhakshinamoorthy S. Jaiswal A.K. 2001. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene, 20 (29): 3906-3917. 10.1038/sj.onc.1204506. 11439354.
8. Guha M. Mackman N. 2001. LPS induction of gene expression in human monocytes. Cell Signal. 13 (2): 85-94. 10.1016/S0898-6568(00)00149-2. 11257452.
9. Innamorato N.G. Rojo A.I. Garcia-Yague A.J. Yamamoto M. de Ceballos M.L. Cuadrado A. 2008. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol. 181 (1): 680-689. 10.4049/jimmunol.181.1.680. 18566435.
10. Ishii T. Itoh K. Sato H. Bannai S. 1999. Oxidative stress-inducible proteins in macrophages. Free Radic. Res. 31 (4): 351-355. 10.1080/10715769900300921. 10517540.
11. Itoh K. Wakabayashi N. Katoh Y. Ishii T. Igarashi K. Engel J.D. Yamamoto M. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13 (1): 76-86. 10.1101/gad.13.1.76. 9887101.
12. Jiang Q. Akashi S. Miyake K. Petty H.R. 2000. Lipopolysaccharide induces physical proximity between CD14 and toll-like receptor 4 (TLR4) prior to nuclear translocation of NF-kappa B. J. Immunol. 165 (7): 3541-3544. 10.4049/jimmunol.165.7.3541. 11034352.
13. Kundu J.K. Surh Y.J. 2008. Inflammation: gearing the journey to cancer. Mutat. Res. 659 (1-2): 15-30. 10.1016/j.mrrev.2008.03.002. 18485806.
14. Kwak M.K. Itoh K. Yamamoto M. Kensler T.W. 2002. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 22 (9): 2883-2892. 10.1128/MCB.22.9.2883-2892.2002. 11940647.
15. Lee J.M. Johnson J.A. 2004. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J. Biochem. Mol. Biol. 37 (2): 139-143. 10.5483/BMBRep.2004.37.2.139. 15469687.
16. Lee I.S. Lim J. Gal J. Kang J.C. Kim H.J. Kang B.Y. Choi H.J. 2011. Anti-inflammatory activity of xanthohumol involves heme oxygenase-1 induction via NRF2-ARE signaling in microglial BV2 cells. Neurochem. Int. 58 (2): 153-160. 10.1016/j.neuint.2010.11.008. 21093515.
17. Li H.B. Chen F. 2005. Isolation and purification of baicalein, wogonin and oroxylin A from the medicinal plant Scutellaria baicalensis by high-speed counter-current chromatography. J. Chromatogr. A, 1074 (1-2): 107-110. 10.1016/j.chroma.2005.03.088. 15941045.
18. Liu P.W. Chen M.F. Tsai A.P. Lee T.J. 2012. STAT1 mediates oroxylin a inhibition of iNOS and pro-inflammatory cytokines expression in microglial BV-2 cells. PLoS One 7 (12): e50363. 10.1371/journal.pone.0050363. 23236370.
19. Lu Y.C. Yeh W.C. Ohashi P.S. 2008. LPS/TLR4 signal transduction pathway. Cytokine, 42 (2): 145-151. 10.1016/j.cyto.2008.01.006. 18304834.
20. Luo C. Urgard E. Vooder T. Metspalu A. 2011. The role of COX-2 and Nrf2/ARE in anti-inflammation and antioxidative stress: Aging and anti-aging. Med. Hypotheses, 77 (2): 174-178. 10.1016/j.mehy.2011.04.002. 21530094.
21. Ma Q. Kinneer K. Bi Y. Chan J.Y. Kan Y.W. 2004. Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem. J. 377 (1): 205-213. 10.1042/BJ20031123. 14510636.
22. Maines M.D. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37: 517-554. 10.1146/annurev.pharmtox.37.1.517. 9131263.
23. McMahon M. Itoh K. Yamamoto M. Chanas S.A. Henderson C.J. McLellan L.I. et al 2001. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res. 61 (8): 3299-3307. 11309284.
24. Middleton E. Jr. Kandaswami C. Theoharides T.C. 2000. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 52 (4): 673-751. 11121513.
25. Mo C. Wang L. Zhang J. Numazawa S. Tang H. Tang X. et al 2014. The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid. Redox Signal. 20 (4): 574-588. 10.1089/ars.2012.5116. 23875776.
26. Mohan S. Epstein J.B. 2003. Carcinogenesis and cyclooxygenase: the potential role of COX-2 inhibition in upper aerodigestive tract cancer. Oral Oncol. 39 (6): 537-546. 10.1016/S1368-8375(03)00035-6. 12798395.
27. Nguyen T. Sherratt P.J. Huang H.C. Yang C.S. Pickett C.B. 2003. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J. Biol. Chem. 278 (7): 4536-4541. 10.1074/jbc.M207293200. 12446695.
28. Oh G.S. Kim H.J. Choi J.H. Shen A. Choe S.K. Karna A. et al 2014. Pharmacological activation of NQO1 increases NAD(+) levels and attenuates cisplatin-mediated acute kidney injury in mice. Kidney Int. 85 (3): 547-560. 10.1038/ki.2013.330. 24025646.
29. Onyiah J.C. Sheikh S.Z. Maharshak N. Steinbach E.C. Russo S.M. Kobayashi T. et al 2013. Carbon monoxide and heme oxygenase-1 prevent intestinal inflammation in mice by promoting bacterial clearance. Gastroenterology, 144 (4): 789-798. 10.1053/j.gastro.2012.12.025. 23266559.
30. Park E.J. Kim Y.M. Park S.W. Kim H.J. Lee J.H. Lee D.U. Chang K.C. 2013. Induction of HO-1 through p38 MAPK/Nrf2 signaling pathway by ethanol extract of Inula helenium L. reduces inflammation in LPS-activated RAW 264.7 cells and CLP-induced septic mice. Food Chem. Toxicol. 55: 386-395. 10.1016/j.fct.2012.12.027. 23298677.
31. Purdom-Dickinson S.E. Sheveleva E.V. Sun H. Chen Q.M. 2007. Translational control of nrf2 protein in activation of antioxidant response by oxidants. Mol. Pharmacol. 72 (4): 1074-1081. 10.1124/mol.107.035360. 17652445.
32. Ramana K.V. Fadl A.A. Tammali R. Reddy A.B. Chopra A.K. Srivastava S.K. 2006. Aldose reductase mediates the lipopolysaccharide-induced release of inflammatory mediators in RAW264.7 murine macrophages. J. Biol. Chem. 281 (44): 33019-33029. 10.1074/jbc.M603819200. 16956889.
33. Rhee S.H. Hwang D. 2000. Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J. Biol. Chem. 275 (44): 34035-34040. 10.1074/jbc.M007386200. 10952994.
34. Rushworth S.A. Ogborne R.M. Charalambos C.A. O'Connell M.A. 2006. Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem. Biophys. Res. Commun. 341 (4): 1007-1016. 10.1016/j.bbrc.2006.01.065. 16460683.
35. Seo K. Yang J.H. Kim S.C. Ku S.K. Ki S.H. Shin S.M. 2014. The Antioxidant Effects of Isorhamnetin Contribute to Inhibit COX-2 Expression in Response to Inflammation: A Potential Role of HO-1. Inflammation, 37 (3): 712-722. 10.1007/s10753-013-9789-6. 24337631.
36. Shin K.M. Kim Y.H. Park W.S. Kang I. Ha J. Choi J.W. et al 2004. Inhibition of methanol extract from the fruits of Kochia scoparia on lipopolysaccharide-induced nitric oxide, prostaglandin [correction of prostagladin] E2, and tumor necrosis factor-alpha production from murine macrophage RAW 264.7 cells. Biol. Pharm. Bull. 27 (4): 538-543. 10.1248/bpb.27.538. 15056862.
37. Siegel D. Gustafson D.L. Dehn D.L. Han J.Y. Boonchoong P. Berliner L.J. Ross D. 2004. NAD(P)H:quinone oxidoreductase 1: role as a superoxide scavenger. Mol. Pharmacol. 65 (5): 1238-1247. 10.1124/mol.65.5.1238. 15102952.
38. Song X. Chen Y. Sun Y. Lin B. Qin Y. Hui H. et al 2012. Oroxylin A, a classical natural product, shows a novel inhibitory effect on angiogenesis induced by lipopolysaccharide. Pharmacol. Rep. 64 (5): 1189-1199. 10.1016/S1734-1140(12)70915-5. 23238475.
39. Stewart D. Killeen E. Naquin R. Alam S. Alam J. 2003. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 278 (4): 2396-2402. 10.1074/jbc.M209195200. 12441344.
40. Sun Y. Lu N. Ling Y. Gao Y. Chen Y. Wang L. et al 2009. Oroxylin A suppresses invasion through down-regulating the expression of matrix metalloproteinase-2/9 in MDA-MB-435 human breast cancer cells. Eur. J. Pharmacol. 603 (1-3): 22-28. 10.1016/j.ejphar.2008.12.008. 19100732.
41. Thimmulappa R.K. Scollick C. Traore K. Yates M. Trush M.A. Liby K.T. et al 2006. Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-Imidazolide. Biochem. Biophys. Res. Commun. 351 (4): 883-889. 10.1016/j.bbrc.2006.10.102. 17097057.
42. Thimmulappa R.K. Fuchs R.J. Malhotra D. Scollick C. Traore K. Bream J.H. et al 2007. Preclinical evaluation of targeting the Nrf2 pathway by triterpenoids (CDDO-Im and CDDO-Me) for protection from LPS-induced inflammatory response and reactive oxygen species in human peripheral blood mononuclear cells and neutrophils. Antioxid. Redox Signal. 9 (11): 1963-1970. 10.1089/ars.2007.1745. 17822364.
43. Toshchakov V. Jones B.W. Perera P.Y. Thomas K. Cody M.J. Zhang S. et al 2002. TLR4, but not TLR2, mediates IFN-beta-induced STAT1alpha/beta-dependent gene expression in macrophages. Nat. Immunol. 3 (4): 392-398. 10.1038/ni774. 11896392.
44. Woo C.H. Lim J.H. Kim J.H. 2004. Lipopolysaccharide induces matrix metalloproteinase-9 expression via a mitochondrial reactive oxygen species-p38 kinase-activator protein-1 pathway in Raw 264.7 cells. J. Immunol. 173 (11): 6973-6980. 10.4049/jimmunol.173.11.6973. 15557194.
45. Woo J. Iyer S. Cornejo M.C. Mori N. Gao L. Sipos I. et al 1998. Stress protein-induced immunosuppression: inhibition of cellular immune effector functions following overexpression of haem oxygenase (HSP 32). Transpl. Immunol. 6 (2): 84-93. 10.1016/S0966-3274(98)80022-1. 9777696.
46. Wu M.L. Ho Y.C. Lin C.Y. Yet S.F. 2011. Heme oxygenase-1 in inflammation and cardiovascular disease. Am. J. Cardiovasc. Dis. 1 (2): 150-158. 22254194.
47. Yao J. Hu R. Sun J. Lin B. Zhao L. Sha Y. Zhu B. You Q.D. Yan T. Guo Q.L. 2014. Oroxylin A prevents inflammation-related tumor through down-regulation of inflammatory gene expression by inhibiting NF-kappaB signaling. Mol Carcinog 53 (2): 145-158. 10.1002/mc.21958.
48. Yeh C.H. Shih H.C. Hong H.M. Lee S.S. Yang M.L. Chen C.J. Kuan Y.H. 2013. Protective effect of wogonin on proinflammatory cytokine generation via Jak1/3-STAT1/3 pathway in lipopolysaccharide stimulated BV2 microglial cells. Toxicol. Ind. Health. In press. 10.1177/0748233713485886. 23595745.
49. Zhang Y. Zhang L. Wu J. Di C. Xia Z. 2013. Heme oxygenase-1 exerts a protective role in ovalbumin-induced neutrophilic airway inflammation by inhibiting Th17 cell-mediated immune response. J. Biol. Chem. 288 (48): 34612-34626. 10.1074/jbc.M113.494369. 24097973.
50. Zhu H. Li Y. 2012. NAD(P)H: quinone oxidoreductase 1 and its potential protective role in cardiovascular diseases and related conditions. Cardiovasc. Toxicol. 12 (1): 39-45. 10.1007/s12012-011-9136-9. 21818552.