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

Volumn 55, Issue , 2013, Pages 386-395

  Park, Eun Jung ^a   Kim, Young Min ^a   Park, Sang Won ^a   Kim, Hye Jung ^a   Lee, Jae Heun ^a   Lee, Dong Ung ^b   Chang, Ki Churl ^a  

^a Gyeongsang National University School of Medicine   (South Korea)

^b Dongguk University   (South Korea)

Author keywords

HMGB1; HO 1; Inflammation; Mice; Multiple organ failure; P38 MAPK

Indexed keywords

ALANINE AMINOTRANSFERASE; ALCOHOL; ANTIINFLAMMATORY AGENT; ASPARTATE AMINOTRANSFERASE; CREATININE; CYCLOOXYGENASE 2; HEME OXYGENASE 1; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INULA HELENIUM EXTRACT; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; NITROGEN; PLANT EXTRACT; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UREA; VASCULAR CELL ADHESION MOLECULE 1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL INFILTRATION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DRUG EFFECT; DRUG MECHANISM; ELECAMPANE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; INULA; MALE; MOUSE; NONHUMAN; ORGAN INJURY; PLANT ROOT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SEPSIS; SURVIVAL RATE; UREA NITROGEN BLOOD LEVEL;

ANIMALS; CELL LINE; ENZYME INDUCTION; ETHANOL; HEME OXYGENASE-1; INFLAMMATION; INULA; LIPOPOLYSACCHARIDES; MICE; NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLANT EXTRACTS; SEPSIS; SIGNAL TRANSDUCTION;

EID: 84873715853     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.12.027     Document Type: Article

References (34)

1. Andersson U., Erlandsson-Harris H. HMGB1 is a potent trigger of arthritis. J. Int. Med. 2004, 255:344-350.
2. Ardoin S.P., Pisetsky D.S. The role of cell death in the pathogenesis of autoimmune disease: HMGB1 and microparticles as intercellular mediators of inflammation. Mod. Rheumatol. 2008, 18:319-326.
3. Bustin M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 1999, 19:5237-5246.
4. Dorn D.C., Alexenizer M., Hengstler J.G., Dorn A. Tumor cell specific toxicity of Inula helenium extracts. Phytother. Res. 2006, 20:970-980.
5. Ha Y.M., Kim M.Y., Park M.K., Lee Y.S., Kim Y.M., Kim H.J., Lee J.H., Chang K.C. Higenamine reduces HMGB1 during hypoxia-induced brain injury by induction of heme oxygenase-1 through PI3K/Akt/Nrf-2 signal pathways. Apoptosis 2012, 17:463-474.
6. Ishikawa K., Sugawara D., Wang X., Suzuki K., Itabe H., Maruyama Y., Lusis A.J. Hemeoxygenase-1inhibits atherosclerotic lesion formation in ldl-receptor knockout mice. Circ. Res. 2001, 88:506-512.
7. Jang H.J., Kim Y.M., Tsoyi K., Park E.J., Lee Y.S., Kim H.J., Joe Y., Chung H.T., Chang K.C. Ethyl pyruvate induces heme oxygenase-1 through p38 mitogen-activated protein kinase activation by depletion of glutathione in RAW 264.7 cells and improves survival in septic animals. Antioxid. Redox. Signal 2012, 17:878-889.
8. Joe Y., Zheng M., Kim H.J., Kim S., Uddin M.J., Park C., Ryu do.G., Kang S.S., Ryoo S., Ryter S.W., Chang K.C., Chung H.T. Salvianolic acid B exerts vasoprotective effects through the modulation of heme oxygenase-1 and arginase activities. J. Pharmacol. Exp. Ther. 2012, 341:850-858.
9. Jun M.S., Kim H.S., Kim Y.M., Kim H.J., Park E.J., Lee J.H., Lee K.R., Kim Y.S., Chang K.C. Ethanol extract of Prunella vulgaris var. lilacina inhibits HMGB1 release by induction of heme oxygenase-1 in LPS-activated RAW 264.7 cells and CLP induced septic mice. Phytother. Res. 2012, 26:605-612.
10. Kalinina N., Agrotis A., Antropova Y., DiVitto G., Kanellakis P., Kostolias G., Ilyinskaya O., Tararak E., Bobik A. Increased expression of the DNA-binding cytokine HMGB1 in human atherosclerotic lesions: role of activated macrophages and cytokines. Arterioscler. Thromb. Vasc. Biol. 2004, 24:2320-2325.
11. Kang Y.J., Lee Y.S., Lee G.W., Lee D.H., Ryu J.C., Yun-Choi H.S., Chang K.C. Inhibition of activation of nuclear factor kappaB is responsible for inhibition of inducible nitric oxide synthase expression by higenamine, an active component of aconite root. J. Pharmacol. Exp. Ther. 1999, 291:314-320.
12. Kim H.J., Tsoy I., Park J.M., Chung J.I., Shin S.C., Chang K.C. Anthocyanins from soybean seed coat inhibit the expression of TNF-alpha-induced genes associated with ischemia/reperfusion in endothelial cell by NF-kappaB-dependent pathway and reduce rat myocardial damages incurred by ischemia and reperfusion in vivo. FEBS Lett. 2006, 580:1391-1397.
13. Kim J.H., Kyung C.Y., Lee K.S., Cho D.H., Baek Y.Y., Lee D.K., Ha K.S., Choe J., Won M.H., Jeoung D., Lee H., Kwon Y.G., Kim Y.M. Functional dissection of Nrf2-dependent phase II genes in vascular inflammation and endotoxic injury using Keap1 siRNA. Free Rad. Biol. Med. 2012, 53:629-640.
14. Kobayashi H., Takeno M., Saito T., Takeda Y., Kirino Y., Noyori K., Hayashi T., Ueda A., Ishigatsubo Y. Regulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis. Arth. Rheum. 2006, 54:1132-1142.
15. Konishi T., Shimada Y., Nagao T., Okabe H., Konoshima T. Antiproliferative sesquiterpene lactones from the roots of Inula helenium. Bio. Pharm. Bull. 2002, 25:1370-1372.
16. Lotze M.T., Tracey K.J. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 2005, 5:331-342.
17. Naidu S., Vijayan V., Santoso S., Kietzmann T., Immenschuh S. Inhibition and genetic deficiency of p38 MAPK up-regulates heme oxygenase-1 gene expression via Nrf2. J. Immunol. 2009, 182:7048-7057.
18. Niedick I., Froese N., Oumard A., Mueller P.P., Nourbakhsh M., Hauser H., Köster M. Nucleolar localization and mobility analysis of the NF-kappaB repressing factor NRF. J. Cell. Sci. 2004, 117(Pt 16):3447-3458.
19. Otterbein L.E., Lee P.J., Chin B.Y., Petrache I., Camhi S.L., Alam J., Choi A.M. Protective effects of heme oxygenase-1 in acute lung injury. Chest 1999, 116(1 Suppl.):61S-63S.
20. Pullikotil P., Chen H., Muniyappa R., Greenberg C.C., Yang S., Reiter C.E., Lee J.W., Chung J.H., Quon M.J. Epigallocatechin gallate induces expression of heme oxygenase-1 in endothelial cells via p38 MAPK and Nrf-2 that suppresses proinflammatory actions of TNF-α. J. Nutr. Biochem. 2011, 23:1134-1145.
21. Qiu J., Luo M., Wang J., Dong J., Li H., Leng B., Zhang Q., Dai X., Zhang Y., Niu X., Deng X. Isoalantolactone protects against Staphylococcus aureus pneumonia. FEMS Microbiol. Lett. 2011, 324:147-155.
22. Reboll M.R., Schweda A.T., Bartels M., Franke R., Frank R., Nourbakhsh M. Mapping of NRF binding motifs of NF-kappaB p65 subunit. J. Biochem. 2011, 150:553-562.
23. Ryter S.W., Choi A.M. Therapeutic applications of carbon monoxide in lung disease. Curr. Opin. Pharmacol. 2006, 6:257-262.
24. Sacerdoti D., Colombrita C., Ghattas M.H., Ismaeil E.F., Scapagnini G., Bolognesi M., Volti G.L., Abraham N.G. Heme oxygenase-1 transduction in endothelial cells causes downregulation of monocyte chemoattractant protein-1 and of genes involved in inflammation and growth. Cell. Mol. Biol. 2005, 51:363-370.
25. Seo J.Y., Lim S.S., Kim J.R., Lim J.S., Ha Y.R., Lee I.A., Kim E.J., Park J.H., Kim J.S. Nrf2-mediated induction of detoxifying enzymes by alantolactone present in Inula helenium. Phytother. Res. 2008, 22:1500-1505.
26. Shin J.H., Kim S.W., Jin Y., Kim I.D., Lee J.K. Ethyl pyruvate-mediated Nrf2 activation and hemeoxygenase 1 induction in astrocytes confer protective effects via autocrine and paracrine mechanisms. Neurochem. Int. 2012, 61:89-99.
27. Slot C. Plasma creatinine determination. A new and specific Jaffe reaction method. Scand. J. Clin. Lab. Invest. 1965, 17:381-387.
28. Takamiya R., Hung C.C., Hall S.R., Fukunaga K., Nagaishi T., Maeno T., Owen C., Macias A.A., Fredenburgh L.E., Ishizaka A., Blumberg R.S., Baron R.M., Perrella M.A. High-mobility group box 1 contributes to lethality of endotoxemia in heme oxygenase-1-deficient mice. Am. J. Res. Cell. Mol. Biol. 2009, 41:129-135.
29. Tsoyi K., Lee T.Y., Lee Y.S., Kim H.J., Seo H.G., Lee J.H., Chang K.C. Hemeoxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high-mobility group box 1 release in vitro and improve survival of mice in LPS- and cecal ligation and puncture-induced sepsis model in vivo. Mol. Pharm. 2009, 76:173-182.
30. Tsoyi K., Jang H.J., Nizamutdinova I.T., Kim Y.M., Lee Y.S., Kim H.J., Seo H.G., Lee J.H., Chang K.C. Metformin inhibits HMGB1 release in LPS-treated RAW 264.7 cells and increases survival rate of endotoxaemic mice. Br. J. Pharmacol. 2011, 162:1498-1508.
31. Tsoyi K., Jang H.J., Lee Y.S., Kim Y.M., Kim H.J., Seo H.G., Lee J.H., Kwak J.H., Lee D.U., Chang K.C. (+)-Nootkatone and (+)-valencene from rhizomes of Cyperus rotundus increase survival rates in septic mice due to heme oxygenase-1 induction. J Ethnopharmacol. 2011, 137:1311-1317.
32. Verma I.M., Stevenson J.K., Schwarz E.M., Antwerp D.V., Miyamoto S. Rel/NFkappaB/I kappaB family: intimate tales of association and dissociation. Genes Dev. 1995, 9:2723-2735.
33. Wang L.J., Lee T.S., Lee F.Y., Pai R.C., Chau L.Y. Expression of hemeoxygenase-1 inatherosclerotic lesions. Am. J. Path. 1998, 152:711-720.
34. Zhang S., Zhong J., Yang P., Gong F., Wang C.Y. HMGB1, an innate alarmin, in the pathogenesis of type 1 diabetes. Int. J. Clin. Exp. Path. 2009, 3:24-38.