The antioxidant effects of isorhamnetin contribute to inhibit COX-2 expression in response to inflammation: A potential role of HO-1

Inflammation

Volumn 37, Issue 3, 2014, Pages 712-722

  Seo, Kyuhwa ^a   Yang, Ji Hye ^a   Kim, Sang Chan ^b   Ku, Sae Kwang ^b   Ki, Sung Hwan ^a   Shin, Sang Mi ^a  

^a Chosun University   (South Korea)

^b Daegu Haany University   (South Korea)

Author keywords

anti inflammation; cyclooxygenase 2; heme oxygenase 1; isorhamnetin; reactive oxygen species

Indexed keywords

CARRAGEENAN; CYCLOOXYGENASE 2; DRUG METABOLITE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; ISORHAMNETIN; LACTATE DEHYDROGENASE; MESSENGER RNA; PROTOPORPHYRIN TIN; QUERCETIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; 3-METHYLQUERCETIN; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; CYCLOOXYGENASE 2 INHIBITOR; HEME OXYGENASE; HMOX1 PROTEIN, RAT; LIPOPOLYSACCHARIDE; METALLOPORPHYRIN; NFE2L2 PROTEIN, RAT; NITRIC OXIDE; PROTOPORPHYRIN; PTGS2 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL CULTURE; CELL VIABILITY ASSAY; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; NONHUMAN; PAW EDEMA; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ACTIVE TRANSPORT; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; EDEMA; ENZYMOLOGY; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOUSE; SPRAGUE DAWLEY RAT;

RATTUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; APOPTOSIS; CELL LINE; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; EDEMA; HEME OXYGENASE (DECYCLIZING); INFLAMMATION; L-LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDES; MACROPHAGES; METALLOPORPHYRINS; MICE; NF-E2-RELATED FACTOR 2; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PROTOPORPHYRINS; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 84902544770     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-013-9789-6     Document Type: Article

References (50)

1. Oberholzer, A., C. Oberholzer, and L.L. Moldawer. 2001. Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 16: 83-96. (Pubitemid 33596740)
2. Rocha, V.Z., and P. Libby. 2009. Obesity, inflammation, and atherosclerosis. Nature Reviews Cardiology 6: 399-409.
3. Ben-Neriah, Y., and M. Karin. 2011. Inflammation meets cancer, with NF-[kappa]B as the matchmaker. Nature Immunology 12: 715-723.
4. Maling, H.M., M.E. Webster, M.A. Williams, W. Saul, and W. Anderson. 1974. Inflammation induced by histamine, serotonin, bradykinin and compound 48/80 in the rat: Antagonists and mechanisms of action. Journal of Pharmacology and Experimental Therapeutics 191: 300-310.
5. Mosser, D.M., and J.P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nature Reviews Immunology 8: 958-969.
6. Cannon, P.J. 1984. Eicosanoids and the blood vessel wall. Circulation 70: 523-528. (Pubitemid 14020647)
7. Leslie, J.B., and W.D. Watkins. 1985. Eicosanoids in the central nervous system. Journal of Neurosurgery 63: 659-668. (Pubitemid 16198950)
8. Williams, C.S., M. Mann, and R.N. DuBois. 1999. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18: 7908-7916. (Pubitemid 30066236)
9. Baeuerle, P.A., and D. Baltimore. 1996. NF-κB: Ten years after. Cell 87: 13-20.
10. Kiritoshi, S., T. Nishikawa, K. Sonoda, D. Kukidome, T. Senokuchi, T. Matsuo, T. Matsumura, H. Tokunaga, M. Brownlee, and E. Araki. 2003. Reactive oxygen species from mitochondria induce cyclooxy-genase-2 gene expression in human mesangial cells: Potential role in diabetic nephropathy. Diabetes 52: 2570-2577. (Pubitemid 37210547)
11. Barbieri, S.S., S. Eligini, M. Brambilla, E. Tremoli, and S. Colli. 2003. Reactive oxygen species mediate cyclooxygenase-2 induction during monocyte to macrophage differentiation: Critical role of NADPH oxidase. Cardiovascular Research 60: 187-197. (Pubitemid 38373491)
12. Drummond, G.R., S. Selemidis, K.K. Griendling, and C.G. Sobey. 2011. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nature Reviews Drug Discovery 10: 453-471.
13. Cathcart, M.K. 2004. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: Contributions to atherosclerosis. Arteriosclerosis, Thrombosis, and Vascular Biology 24: 23-28. (Pubitemid 38082407)
14. Li, N., M.I. Venkatesan, A. Miguel, R. Kaplan, C. Gujuluva, J. Alam, and A. Nel. 2000. Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. The Journal of Immunology 165: 3393-3401.
15. Ryter, S.W., and A.M. Choi. 2005. Heme oxygenase-1: Redox regulation of a stress protein in lung and cell culture models. Antioxidants and Redox Signaling 7: 80-91. (Pubitemid 40187927)
16. Zabalgoitia, M., J.T. Colston, S.V. Reddy, J.W. Holt, R.F. Regan, D.E. Stec, J.M. Rimoldi, A.J. Valente, and B. Chandrasekar. 2008. Carbon monoxide donors or heme oxygenase-1 (HO-1) overexpression blocks interleukin-18-mediated NF-κB-PTEN-dependent human cardiac endothelial cell death. Free Radical Biology and Medicine 44: 284-298.
17. - production in a two-hit model of alcohol intoxication and burn injury. The Journal of Immunology 180: 6933-6940.
18. Pengfei, L., D. Tiansheng, H. Xianglin, and W. Jianguo. 2009. Antioxidant properties of isolated isorhamnetin from the sea buckthorn marc. Plant Foods for Human Nutrition 64: 141-145.
19. Teng, B.-S., Y.-H. Lu, Z.-T. Wang, X.-Y. Tao, and D.-Z. Wei. 2006. In vitro anti-tumor activity of isorhamnetin isolated from Hippophae rhamnoides L. against BEL-7402 cells. Pharmacological Research 54: 186-194. (Pubitemid 44119198)
20. Yang, J.H., S.C. Kim, B.Y. Shin, S.H. Jin, M.J. Jo, K.H. Jegal, Y.W. Kim, J.R. Lee, S.K. Ku, I.J. Cho, and S.H. Ki. 2013. O-methylated flavonol isorhamnetin prevents acute inflammation through blocking of NF-κB activation. Food and Chemical Toxicology 59: 362-372.
21. Kang, T.J., J.S. Moon, S.K. Lee, and D.S. Yim. 2011. Polyacetylene compound from Cirsium japonicum var. ussuriense inhibits the LPS-induced inflammatory reaction via suppression of NF-κB activity in RAW 264.7 cells. Biomolecules & Therapeutics 19: 97-101.
22. Lim, H.J., H. Li, J.Y. Kim, and J.H. Ryu. 2011. Quercetin derivatives from Siegesbeckia glabrescens inhibit the expression of COX-2 through the suppression of NF-κB activation in microglia. Biomolecules & Therapeutics 19: 27-32.
23. Jaeschke, H. 2000. Reactive oxygen and mechanisms of inflammatory liver injury. Journal of Gastroenterology and Hepatology 15: 718-724. (Pubitemid 30615053)
24. Park, H.S., H.Y. Jung, E.Y. Park, J. Kim, W.J. Lee, and Y.S. Bae. 2004. Cutting edge: Direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-κB. The Journal of Immunology 173: 3589-3593. (Pubitemid 39280716)
25. Sanchez, M., F. Lodi, R. Vera, I.C. Villar, A. Cogolludo, R. Jimenez, L. Moreno, M. Romero, J. Tamargo, F. Perez-Vizcaino, and J. Duarte. 2007. Quercetin and isorhamnetin prevent endothelial dysfunction, superoxide production, and overexpression of p47phox induced by angiotensin II in rat aorta. The Journal of Nutrition 137: 910-915. (Pubitemid 46596886)
26. Cha, J.Y., J.Y. Jung, J.Y. Jung, J.R. Lee, I.J. Cho, S.K. Ku, S.H. Byun, Y.-T. Ahn, C.W. Lee, S.C. Kim, and W.G. An. 2013. Inhibitory effects of traditional herbal formula Pyungwi-San on inflammatory response in vitro and in vivo. Evidence-Based Complementary and Alternative Medicine 2013: 1-19.
27. Sohn, K.H., M.J. Jo, W.J. Cho, J.R. Lee, I.J. Cho, S.C. Kim, Y.W. Kim, and S.Y. Jee. 2012. Bojesodok-eum, a herbal prescription, ameliorates acute inflammation in association with the inhibition of NF-B-mediated nitric oxide and proinflammatory cytokine production. Evidence-Based Complementary and Alternative Medicine 2012: 12.
28. Huang, S.-S., C.-S. Chiu, T.-H. Lin, M.-M. Lee, C.-Y. Lee, S.-J. Chang, W.-C. Hou, G.-J. Huang, and J.-S. Deng. 2013. Antioxidant and anti-inflammatory activities of aqueous extract of Centipeda minima. Journal of Ethnopharmacology 147: 395-405.
29. Higgs, G.A., K.E. Eakins, K.G. Mugridge, S. Moncada, and J.R. Vane. 1980. The effects of non-steroid anti-inflammatory drugs on leukocyte migration in carrageenin-induced inflammation. European Journal of Pharmacology 66: 81-86. (Pubitemid 10048837)
30. Almeida, A.P., B.M. Bayer, Z. Horakova, and M.A. Beaven. 1980. Influence of indomethacin and other anti-inflammatory drugs on mobilization and production of neutrophils: studies with carrageenaninduced inflammation in rats. Journal of Pharmacology and Experimental Therapeutics 214: 74-79. (Pubitemid 10032385)
31. Handy, R.L.C., and P.K. Moore. 1998. A comparison of the effects of L-NAME, 7-NI and L-NIL on carrageenan-induced hindpaw oedema and NOS activity. British Journal of Pharmacology 123: 1119-1126. (Pubitemid 28120509)
32. Nantel, F., D. Denis, R. Gordon, A. Northey, M. Cirino, K.M. Metters, and C.C. Chan. 1999. Distribution and regulation of cyclooxygenase-2 in carrageenan-induced inflammation. British Journal of Pharmacology 128: 853-859. (Pubitemid 29494701)
33. Old, L. 1985. Tumor necrosis factor (TNF). Science 230: 630-632. (Pubitemid 16190956)
34. Wagener, F.A.D.T.G., H.-D. Volk, D. Willis, N.G. Abraham, M.P. Soares, G.J. Adema, and C.G. Figdor. 2003. Different faces of the heme-heme oxygenase system in inflammation. Pharmacological Reviews 55: 551-571. (Pubitemid 37013215)
35. Kapturczak, M.H., C. Wasserfall, T. Brusko, M. Campbell-Thompson, T.M. Ellis, M.A. Atkinson, and A. Agarwal. 2004. Heme oxygenase-1 modulates early inflammatory responses: Evidence from the heme oxygenase-1-deficient mouse. The American Journal of Pathology 165: 1045-1053. (Pubitemid 39129309)
36. Nakahira, K., H.P. Kim, X.H. Geng, A. Nakao, X. Wang, N. Murase, P.F. Drain, X. Wang, M. Sasidhar, E.G. Nabel, T. Takahashi, N.W. Lukacs, S.W. Ryter, K. Morita, and A.M.K. Choi. 2006. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. The Journal of Experimental Medicine 203: 2377-2389. (Pubitemid 44498371)
37. Park, E.J., Y.M. Kim, S.W. Park, H.J. Kim, J.H. Lee, D.-U. Lee, and K.C. Chang. 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 and Chemical Toxicology 55:386-395.
38. Motterlini, R., R. Foresti, R. Bassi, and C.J. Green. 2000. Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radical Biology and Medicine 28: 1303-1312. (Pubitemid 30417475)
39. Chung, S.W., Y.-H. Chen, S.-F. Yet, M.D. Layne, and M.A. Perrella. 2006. Endotoxin-induced down-regulation of Elk-3 facilitates heme oxygenase-1 induction in macrophages. The Journal of Immunology 176: 2414-2420. (Pubitemid 43201691)
40. Kim, K.H., J.H. Lyu, S.T. Koo, S.-R. Oh, H.-K. Lee, K.-S. Ahn, R.T. Sadikot, and M. Joo. 2011. MyD88 is a mediator for the activation of Nrf2. Biochemical and Biophysical Research Communications 404:46-51.
41. Yang, J.H., Shin, B.Y., Han, J.Y., Kim, M.G., Wi, J.E., Kim, Y.W., Cho, I.J., Kim, S.C., Shin, S.M., and Ki, S.H. Isorhamnetin protects against oxidative stress by activating Nrf2 and inducing the expression of its target genes. Toxicology and Applied Pharmacology. doi:10.1016/j.taap.2013.10.026.
42. Mo, C., Wang, L., Zhang, J., Numazawa, S., Tang, H., Tang, X., Han, X., Li, J., Yang, M., Wang, Z., Wei, D., and Xiao, H. 2013. 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. Antioxidants and Redox Signaling. doi:10.1089/ars.2012.5116.
43. Karin, M., Y. Cao, F.R. Greten, and Z.-W. Li. 2002. NF-κB in cancer: From innocent bystander to major culprit. Nature Reviews Cancer 2: 301-310. (Pubitemid 37328783)
44. Piskula, M.K., and J. Terao. 1998. Accumulation of (-)-epicatechin metabolites in rat plasma after oral administration and distribution of conjugation enzymes in rat tissues. The Journal of Nutrition 128: 1172-1178. (Pubitemid 28317683)
45. Lan, K., X. Jiang, and J. He. 2007. Quantitative determination of isorhamnetin, quercetin and kaempferol in rat plasma by liquid chromatography with electrospray ionization tandem mass spectrometry and its application to the pharmacokinetic study of isorhamnetin. Rapid Communications in Mass Spectrometry 21: 112-120. (Pubitemid 46095469)
46. Ader, P., A. Wessmann, and S. Wolffram. 2000. Bioavailability and metabolism of the flavonol quercetin in the pig. Free Radical Biology and Medicine 28: 1056-1067. (Pubitemid 30314704)
47. Lin, W.-N., C.-C. Lin, H.-Y. Cheng, and C.-M. Yang. 2011. Regulation of cyclooxygenase-2 and cytosolic phospholipase A2 gene expression by lipopolysaccharide through the RNA-binding protein HuR: Involvement of NADPH oxidase, reactive oxygen species and mitogen-activated protein kinases. British Journal of Pharmacology 163: 1691-1706.
48. Ramachandran, L., K.A. Manu, M.K. Shanmugam, F. Li, K.S. Siveen, S. Vali, S. Kapoor, T. Abbasi, R. Surana, D.T. Smoot, H. Ashktorab, P. Tan, K.S. Ahn, C.W. Yap, A.P. Kumar, and G. Sethi. 2012. Isorhamnetin inhibits proliferation and invasion and induces apoptosis through the modulation of peroxisome proliferator-activated receptor ã activation pathway in gastric cancer. Journal of Biological Chemistry 287: 38028-38040.
49. Marx, N., B. Kehrle, K. Kohlhammer, M. Grüb, W. Koenig, V. Hombach, P. Libby, and J. Plutzky. 2002. PPAR activators as antiinflammatory mediators in human T lymphocytes: Implications for atherosclerosis and transplantation- associated arteriosclerosis. Circulation Research 90: 703-710. (Pubitemid 34640890)
50. von Knethen, A., H. Neb, V. Morbitzer, M.V. Schmidt, A.-M. Kuhn, L. Kuchler, and B. Brüne. 2011. PPARγ stabilizes HO-1 mRNA in monocytes/macrophages which affects IFN-β expression. Free Radical Biology and Medicine 51: 396-405.