Aryl hydrocarbon receptor modulates NADPH oxidase activity via direct transcriptional regulation of p40phox expressions

Molecular Pharmacology

Volumn 83, Issue 5, 2013, Pages 1133-1140

  Wada, Taira ^a   Sunaga, Hiroshi ^a   Ohkawara, Reiko ^a   Shimba, Shigeki ^a  

^a NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLCHOLANTHRENE; AROMATIC HYDROCARBON RECEPTOR; P40 PHOX PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; RECEPTORS, ARYL HYDROCARBON; TRANSCRIPTION, GENETIC;

EID: 84876587549     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.083303     Document Type: Article

References (52)

1. Beyer TA, Xu W, Teupser D, auf dem Keller U, Bugnon P, Hildt E, Thiery J, Kan YW, and Werner S (2008) Impaired liver regeneration in Nrf2 knockout mice: Role of ROS-mediated insulin/IGF-1 resistance. EMBO J 27:212-223.
2. Bokoch GM and Knaus UG (2003) NADPH oxidases: Not just for leukocytes anymore! Trends Biochem Sci 28:502-508. (Pubitemid 38340415)
3. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
4. Chessa TA, Anderson KE, Hu Y, Xu Q, Rausch O, Stephens LR, and Hawkins PT (2010) Phosphorylation of threonine 154 in p40phox is an important physiological signal for activation of the neutrophil NADPH oxidase. Blood 116:6027-6036.
5. De Minicis S and Brenner DA (2007) NOX in liver fibrosis. Arch Biochem Biophys 462:266-272. (Pubitemid 46856330)
6. Dong B and Matsumura F (2008) Roles of cytosolic phospholipase A2 and Src kinase in the early action of 2,3,7,8-tetrachlorodibenzo-p-dioxin through a nongenomic pathway in MCF10A cells. Mol Pharmacol 74:255-263. (Pubitemid 351872176)
7. El Benna J, Dang PM, Andrieu V, Vergnaud S, Dewas C, Cachia O, Fay M, Morel F, Chollet-Martin S, and Hakim J et al. (1999) P40phox associates with the neutrophil Triton X-100-insoluble cytoskeletal fraction and PMA-activated membrane skeleton: A comparative study with P67phox and P47phox. J Leukoc Biol 66: 1014-1020. (Pubitemid 30010528)
8. Ellson CD, Davidson K, Ferguson GJ, O'Connor R, Stephens LR, and Hawkins PT (2006) Neutrophils from p40phox2/2 mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing. J Exp Med 203: 1927-1937. (Pubitemid 44188467)
9. Fang C and Zhang QY (2010) The role of small-intestinal P450 enzymes in protection against systemic exposure of orally administered benzo[a]pyrene. J Pharmacol Exp Ther 334:156-163.
10. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SST, Kimura S, Nebert DW, Rudikoff S, Ward JM, and Gonzalez FJ (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268: 722-726.
11. Granger DN (1988) Role of xanthine oxidase and granulocytes in ischemiareperfusion injury. Am J Physiol 255:H1269-H1275.
12. Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307-340.
13. Kopf PG, Huwe JK, and Walker MK (2008) Hypertension, cardiac hypertrophy, and impaired vascular relaxation induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are associated with increased superoxide. Cardiovasc Toxicol 8:181-193.
14. Landers JP and Bunce NJ (1991) The Ah receptor and the mechanism of dioxin toxicity. Biochem J 276:273-287.
15. Levin I, Petrasek J, and Szabo G (2012) The presence of p47phox in liver parenchymal cells is a key mediator in the pathogenesis of alcoholic liver steatosis. Alcohol Clin Exp Res 36:1397-1406.
16. Li SL, Valente AJ, Zhao SJ, and Clark RA (1997) PU.1 is essential for p47phox promoter activity in myeloid cells. J Biol Chem 272:17802-17809. (Pubitemid 27311221)
17. Li SL, Valente AJ, Qiang M, Schlegel W, Gamez M, and Clark RA (2002) Multiple PU.1 sites cooperate in the regulation of p40phox transcription during granulocytic differentiation of myeloid cells. Blood 99:4578-4587. (Pubitemid 34627230)
18. Lin PH, Lin CH, Huang CC, Chuang MC, and Lin P (2007) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces oxidative stress, DNA strand breaks, and poly(ADP-ribose) polymerase-1 activation in human breast carcinoma cell lines. Toxicol Lett 172:146-158. (Pubitemid 47189732)
19. Lin L, Pang W, Chen K, Wang F, Gengler J, Sun Y, and Tong Q (2012) Adipocyte expression of PU.1 transcription factor causes insulin resistance through upregulation of inflammatory cytokine gene expression and ROS production. Am J Physiol Endocrinol Metab 302:E1550-E1559.
20. Miao W, Hu L, Scrivens PJ, and Batist G (2005) Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: Direct cross-talk between phase I and II drugmetabolizing enzymes. J Biol Chem 280:20340-20348. (Pubitemid 40776732)
21. Miller JD, Chu Y, Brooks RM, Richenbacher WE, Peña-Silva R, and Heistad DD (2008) Dysregulation of antioxidant mechanisms contributes to increased oxidative stress in calcific aortic valvular stenosis in humans. J Am Coll Cardiol 52:843-850.
22. Mimura J, Yamashita K, Nakamura K, Morita M, Takagi TN, Nakao K, Ema M, Sogawa K, Yasuda M, and Katsuki M et al. (1997) Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes Cells 2:645-654. (Pubitemid 127688610)
23. Mizuki K, Kadomatsu K, Hata K, Ito T, Fan QW, Kage Y, Fukumaki Y, Sakaki Y, Takeshige K, and Sumimoto H (1998) Functional modules and expression of mouse p40phox and p67phox, SH3-domain-containing proteins involved in the phagocyte NADPH oxidase complex. Eur J Biochem 251:573-582. (Pubitemid 28108949)
24. Morel Y, Mermod N, and Barouki R (1999) An autoregulatory loop controlling CYP1A1 gene expression: Role of H2O2 and NFI. Mol Cell Biol 19:6825-6832. (Pubitemid 29441866)
25. Paik YH, Iwaisako K, Seki E, Inokuchi S, Schnabl B, Osterreicher CH, Kisseleva T, and Brenner DA (2011) The nicotinamide adenine dinucleotide phosphate oxidase (NOX) homologues NOX1 and NOX2/gp91phox mediate hepatic fibrosis in mice. Hepatology 53:1730-1741.
26. Parola M and Robino G (2001) Oxidative stress-related molecules and liver fibrosis. J Hepatol 35:297-306. (Pubitemid 32803489)
27. Pinel-Marie ML, Sparfel L, Desmots S, and Fardel O (2009) Aryl hydrocarbon receptor-dependent induction of the NADPH oxidase subunit NCF1/p47 phox expression leading to priming of human macrophage oxidative burst. Free Radic Biol Med 47:825-834.
28. Pohjanvirta R and Tuomisto J (1994) Short-term toxicity of 2,3,7,8-tetrachlorodibenzop-dioxin in laboratory animals: Effects, mechanisms, and animal models. Pharmacol Rev 46:483-549.
29. Poland A and Knutson JC (1982) 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Annu Rev Pharmacol Toxicol 22:517-554.
30. Poli G and Parola M (1997) Oxidative damage and fibrogenesis. Free Radic Biol Med 22:287-305. (Pubitemid 26399335)
31. Puntarulo S and Cederbaum AI (1992) Effect of phenobarbital and 3-methylcholanthrene treatment on NADPH-and NADH-dependent production of reactive oxygen intermediates by rat liver nuclei. Biochim Biophys Acta 1116:17-23.
32. Reyes H, Reisz-Porszasz S, and Hankinson O (1992) Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256:1193-1195.
33. Rodriguez R and Redman R (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:3175-3176. (Pubitemid 40328016)
34. Safe SH (1986) Comparative toxicology and mechanism of action of polychlorinated dibenzo-p-dioxins and dibenzofurans. Annu Rev Pharmacol Toxicol 26:371-399. (Pubitemid 16090967)
35. Schlezinger JJ, White RD, and Stegeman JJ (1999) Oxidative inactivation of cytochrome P-450 1A (CYP1A) stimulated by 3,39,4,49-tetrachlorobiphenyl: Production of reactive oxygen by vertebrate CYP1As. Mol Pharmacol 56:588-597. (Pubitemid 29406886)
36. Schmidt JV and Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55-89. (Pubitemid 26422709)
37. Schmidt JV, Su GH, Reddy JK, Simon MC, and Bradfield CA (1996) Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 93:6731-6736. (Pubitemid 26230378)
38. Senft AP, Dalton TP, Nebert DW, Genter MB, Hutchinson RJ, and Shertzer HG (2002) Dioxin increases reactive oxygen production in mouse liver mitochondria. Toxicol Appl Pharmacol 178:15-21. (Pubitemid 34084726)
39. Selemidis S, Dusting GJ, Peshavariya H, Kemp-Harper BK, and Drummond GR (2007) Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 75:349-358. (Pubitemid 46961925)
40. Stohs SJ, Shara MA, Alsharif NZ, Wahba ZZ, and al-Bayati ZA (1990) 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced oxidative stress in female rats. Toxicol Appl Pharmacol 106:126-135.
41. Straub AC, Clark KA, Ross MA, Chandra AG, Li S, Gao X, Pagano PJ, Stolz DB, and Barchowsky A (2008) Arsenic-stimulated liver sinusoidal capillarization in mice requires NADPH oxidase-generated superoxide. J Clin Invest 118:3980-3989.
42. Sugihara K, Okayama T, Kitamura S, Yamashita K, Yasuda M, Miyairi S, Minobe Y, and Ohta S (2008) Comparative study of aryl hydrocarbon receptor ligand activities of six chemicals in vitro and in vivo. Arch Toxicol 82:5-11.
43. Suh CI, Stull ND, Li XJ, Tian W, Price MO, Grinstein S, Yaffe MB, Atkinson S, and Dinauer MC (2006) The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgIIA receptor-induced phagocytosis. J Exp Med 203: 1915-1925. (Pubitemid 44188466)
44. Suzuki S, Kumatori A, Haagen IA, Fujii Y, Sadat MA, Jun HL, Tsuji Y, Roos D, and Nakamura M (1998) PU.1 as an essential activator for the expression of gp91phox gene in human peripheral neutrophils, monocytes, and B lymphocytes. Proc Natl Acad Sci USA 95:6085-6090.
45. Wada T, Shimba S, and Tezuka M (2006) Transcriptional regulation of the hypoxia inducible factor-2a (HIF-2a) gene during adipose differentiation in 3T3-L1 cells. Biol Pharm Bull 29:49-54. (Pubitemid 43036692)
46. Wada T, Kang HS, Angers M, Gong H, Bhatia S, Khadem S, Ren S, Ellis E, Strom SC, and Jetten AM et al. (2008) Identification of oxysterol 7a-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor alpha (RORa) (NR1F1) target gene and a functional cross-talk between RORa and liver X receptor (NR1H3). Mol Pharmacol 73:891-899. (Pubitemid 351397893)
47. Walisser JA, Glover E, Pande K, Liss AL, and Bradfield CA (2005) Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types. Proc Natl Acad Sci USA 102:17858-17863. (Pubitemid 41803587)
48. Watabe Y, Nazuka N, Tezuka M, and Shimba S (2010) Aryl hydrocarbon receptor functions as a potent coactivator of E2F1-dependent trascription activity. Biol Pharm Bull 33:389-397.
49. Wientjes FB, Hsuan JJ, Totty NF, and Segal AW (1993) p40Phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem J 296:557-561.
50. Xie W, Barwick JL, Simon CM, Pierce AM, Safe S, Blumberg B, Guzelian PS, and Evans RM (2000) Reciprocal activation of xenobiotic response genes by nuclear receptors SXR/PXR and CAR. Genes Dev 14:3014-3023.
51. Yang MS, Li D, Lin T, Zheng JJ, Zheng W, and Qu JY (2008) Increase in intracellular free/bound NAD[P]H as a cause of Cd-induced oxidative stress in the HepG(2) cells. Toxicology 247:6-10.
52. Zhan S, Vazquez N, Zhan S, Wientjes FB, Budarf ML, Schrock E, Ried T, Green ED, and Chanock SJ (1996) Genomic structure, chromosomal localization, start of transcription, and tissue expression of the human p40-phox, a new component of the nicotinamide adenine dinucleotide phosphate-oxidase complex. Blood 88: 2714-2721. (Pubitemid 26327525)