Induction of heme oxygenase-1 inhibits cell death in crotonaldehyde-stimulated HepG2 cells via the PKC-δ -p38 -Nrf2 pathway

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Lee, Seung Eun ^a   Yang, Hana ^a   Jeong, Seong Il ^a   Jin, Young Ho ^a   Park, Cheung Seog ^a   Park, Yong Seek ^a  

^a Kyung Hee University Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CROTONALDEHYDE; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C DELTA; PROTOPORPHYRIN ZINC; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LIVER CELL CARCINOMA; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; UPREGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ALDEHYDES; APOPTOSIS; CELL CYCLE; CELL NUCLEUS; CELL SURVIVAL; ENVIRONMENTAL POLLUTANTS; ENZYME INHIBITORS; GENE KNOCKDOWN TECHNIQUES; HEME OXYGENASE-1; HEP G2 CELLS; HUMANS; NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE C-DELTA; PROTOPORPHYRINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84864375081     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041676     Document Type: Article

References (53)

1. Kawaguchi-Niida M, Shibata N, Morikawa S, Uchida K, Yamamoto T, et al. (2006) Crotonaldehyde accumulates in glial cells of Alzheimer's disease brain. Acta Neuropathol 111: 422-429.
2. Liu XY, Yang ZH, Pan XJ, Zhu MX, Xie JP, (2010) Crotonaldehyde induces oxidative stress and caspase-dependent apoptosis in human bronchial epithelial cells. Toxicol Lett 195: 90-98.
3. IARC (1995) Crotonaldehyde. IARC 63: 373-391.
4. Dong JZ, Moldoveanu SC, (2004) Gas chromatography-mass spectrometry of carbonyl compounds in cigarette mainstream smoke after derivatization with 2,4-dinitrophenylhydrazine. J Chromatogr A 1027: 25-35.
5. Chen PX, Moldoveanu SC, (2003) Mainstream smoke chemical analyses for 2R4F Kentucky reference cigarette. Beiträge zur Tabakforschung international 20: 448-458.
6. Eiserich JP, van der Vliet A, Handelman GJ, Halliwell B, Cross CE, (1995) Dietary antioxidants and cigarette smoke-induced biomolecular damage: a complex interaction. Am J Clin Nutr 62: 1490S-1500S.
7. Simon SA, Liedtke W, (2008) How irritating: the role of TRPA1 in sensing cigarette smoke and aerogenic oxidants in the airways. J Clin Invest 118: 2383-2386.
8. Chung FL, Tanaka T, Hecht SS, (1986) Induction of liver tumors in F344 rats by crotonaldehyde. Cancer Res 46: 1285-1289.
9. Fernandes PH, Kanuri M, Nechev LV, Harris TM, Lloyd RS, (2005) Mammalian cell mutagenesis of the DNA adducts of vinyl chloride and crotonaldehyde. Environ Mol Mutagen 45: 455-459.
10. Neudecker T, Eder E, Deininger C, Henschler D, (1989) Crotonaldehyde is mutagenic in Salmonella typhimurium TA100. Environ Mol Mutagen 14: 146-148.
11. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, et al. (2007) Alpha,beta-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am J Respir Cell Mol Biol 37: 617-623.
12. Esterbauer H, Schaur RJ, Zollner H, (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128.
13. Stein S, Lao Y, Yang IY, Hecht SS, Moriya M, (2006) Genotoxicity of acetaldehyde- and crotonaldehyde-induced 1,N2-propanodeoxyguanosine DNA adducts in human cells. Mutat Res 608: 1-7.
14. Hecht SS, McIntee EJ, Wang M, (2001) New DNA adducts of crotonaldehyde and acetaldehyde. Toxicology 166: 31-36.
15. Liu XY, Yang ZH, Pan XJ, Zhu MX, Xie JP, (2010) Gene expression profile and cytotoxicity of human bronchial epithelial cells exposed to crotonaldehyde. Toxicol Lett 197: 113-122.
16. Jeong SI, Lee SE, Yang H, Park CS, Cho JJ, et al. (2011) Genome-wide analysis of gene expression by crotonaldehyde in human umbilical vein endothelial cells. Mol Cell Toxicol 7: 127-134.
17. Ryter SW, Alam J, Choi AM, (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650.
18. Pae HO, Jeong SO, Koo BS, Ha HY, Lee KM, et al. (2008) Tranilast, an orally active anti-allergic drug, up-regulates the anti-inflammatory heme oxygenase-1 expression but down-regulates the pro-inflammatory cyclooxygenase-2 and inducible nitric oxide synthase expression in RAW264.7 macrophages. Biochem Biophys Res Commun 371: 361-365.
19. Seidel P, Goulet S, Hostettler K, Tamm M, Roth M, (2010) DMF inhibits PDGF-BB induced airway smooth muscle cell proliferation through induction of heme-oxygenase-1. Respir Res 11: 145.
20. Lee BW, Chun SW, Kim SH, Lee Y, Kang ES, et al. (2011) Lithospermic acid B protects beta-cells from cytokine-induced apoptosis by alleviating apoptotic pathways and activating anti-apoptotic pathways of Nrf2-HO-1 and Sirt1. Toxicol Appl Pharmacol 252: 47-54.
21. Jozkowicz A, Was H, Dulak J, (2007) Heme oxygenase-1 in tumors: is it a false friend? Antioxid Redox Signal 9: 2099-2117.
22. Doi K, Akaike T, Fujii S, Tanaka S, Ikebe N, et al. (1999) Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer 80: 1945-1954.
23. Cullinan SB, Diehl JA, (2004) PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem 279: 20108-20117.
24. Bloom DA, Jaiswal AK, (2003) Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H: quinone oxidoreductase-1 gene expression. J Biol Chem 278: 44675-44682.
25. Kobayashi M, Yamamoto M, (2005) Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 7: 385-394.
26. Huang HC, Nguyen T, Pickett CB, (2002) Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 277: 42769-42774.
27. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, et al. (2003) Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal 5: 155-162.
28. Li Volti G, Wang J, Traganos F, Kappas A, Abraham NG, (2002) Differential effect of heme oxygenase-1 in endothelial and smooth muscle cell cycle progression. Biochem Biophys Res Commun 296: 1077-1082.
29. Akagi R, Takahashi T, Sassa S, (2005) Cytoprotective effects of heme oxygenase in acute renal failure. Contrib Nephrol 148: 70-85.
30. Wang GW, Hamid T, Keith RJ, Zhou GH, Partridge CR, et al. (2010) Cardioprotective and Antiapoptotic Effects of Heme Oxygenase-1 in the Failing Heart. Circulation 121: 1912-U1978.
31. Miyake M, Fujimoto K, Anai S, Ohnishi S, Kuwada M, et al. (2011) Heme oxygenase-1 promotes angiogenesis in urothelial carcinoma of the urinary bladder. Oncol Rep 25: 653-660.
32. Sass G, Leukel P, Schmitz V, Raskopf E, Ocker M, et al. (2008) Inhibition of heme oxygenase 1 expression by small interfering RNA decreases orthotopic tumor growth in livers of mice. Int J Cancer 123: 1269-1277.
33. Merritt AJ, Potten CS, Watson AJ, Loh DY, Nakayama K, et al. (1995) Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia. J Cell Sci 108 (Pt 6): 2261-2271.
34. Schwartsburd PM, (2004) Age-promoted creation of a pro-cancer microenvironment by inflammation: pathogenesis of dyscoordinated feedback control. Mech Ageing Dev 125: 581-590.
35. Padmanabhan B, Tong KI, Ohta T, Nakamura Y, Scharlock M, et al. (2006) Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol Cell 21: 689-700.
36. Singh A, Misra V, Thimmulappa RK, Lee H, Ames S, et al. (2006) Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med 3: e420.
37. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD, (2008) Dual roles of Nrf2 in cancer. Pharmacol Res 58: 262-270.
38. Luczaj W, Skrzydlewska E, (2003) DNA damage caused by lipid peroxidation products. Cell Mol Biol Lett 8: 391-413.
39. Eder E, Schuler D, Budiawan (1999) Cancer risk assessment for crotonaldehyde and 2-hexenal: an approach. IARC Sci Publ pp. 219-232.
40. Yang H, Lee SE, Jeong SI, Park CS, Jin YH, et al. (2011) Up-regulation of Heme Oxygenase-1 by Korean Red Ginseng Water Extract as a Cytoprotective Effect in Human Endothelial Cells. J Ginseng Res 35: 352-359.
41. Choi AM, Alam J, (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15: 9-19.
42. Nath KA, Balla G, Vercellotti GM, Balla J, Jacob HS, et al. (1992) Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90: 267-270.
43. Ohnishi M, Katsuki H, Unemura K, Izumi Y, Kume T, et al. (2010) Heme oxygenase-1 contributes to pathology associated with thrombin-induced striatal and cortical injury in organotypic slice culture. Brain Res 1347: 170-178.
44. Kim YS, Pi SH, Lee YM, Lee SI, Kim EC, (2009) The anti-inflammatory role of heme oxygenase-1 in lipopolysaccharide and cytokine-stimulated inducible nitric oxide synthase and nitric oxide production in human periodontal ligament cells. J Periodontol 80: 2045-2055.
45. Rushworth SA, Ogborne RM, Charalambos CA, O'Connell MA, (2006) Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem Biophys Res Commun 341: 1007-1016.
46. Hwang YP, Jeong HG, (2008) The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett 582: 2655-2662.
47. Lee SE, Jeong SI, Kim GD, Yang H, Park CS, et al. (2011) Upregulation of heme oxygenase-1 as an adaptive mechanism for protection against crotonaldehyde in human umbilical vein endothelial cells. Toxicol Lett 201: 240-248.
48. Randle LE, Goldring CE, Benson CA, Metcalfe PN, Kitteringham NR, et al. (2008) Investigation of the effect of a panel of model hepatotoxins on the Nrf2-Keap1 defence response pathway in CD-1 mice. Toxicology 243: 249-260.
49. Kalejta RF, Brideau AD, Banfield BW, Beavis AJ, (1999) An integral membrane green fluorescent protein marker, Us9-GFP, is quantitatively retained in cells during propidium iodide-based cell cycle analysis by flow cytometry. Exp Cell Res 248: 322-328.
50. Hsieh JK, Fredersdorf S, Kouzarides T, Martin K, Lu X, (1997) E2F1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev 11: 1840-1852.
51. Lee SE, Lee SH, Ryu DS, Park CS, Park KS, et al. (2010) Differentially-expressed genes related to atherosclerosis in acrolein-stimulated human umbilical vein endothelial cells. Biochip Journal 4: 264-271.
52. Lee SE, Jeong SI, Yang H, Park CS, Jin YH, et al. (2011) Fisetin induces Nrf2-mediated HO-1 expression through PKC-delta and p38 in human umbilical vein endothelial cells. J Cell Biochem 112: 2352-2360.
53. Lee SE, Lee NJ, Lee SH, Park CS, Ahn HJ, et al. (2010) Uncaria rhynchophylla induces heme oxygenase-1 as a cytoprotective effect in RAW 264.7 macrophages. Mol Cell Toxicol 6: 33-40.