Abstract
The nutritional profile of an individual can influence the toxicity of persistent environmental toxicants. Polychlorinated biphenyls (PCBs), prevalent environmental pollutants, are highly lipid-soluble toxic compounds that biomagnify through trophic levels and pose cancer, neurocognitive, and atherosclerotic risk to human populations. There is a growing body of knowledge that PCBs can initiate inflammatory responses in vivo, and this inflammation can be either exacerbated or ameliorated by nutrition. Data indicate that diets high in certain dietary lipids such as omega-6 fatty acids can worsen PCB-induced vascular toxicity while diets enriched with bioactive food components such as polyphenols and omega-3 polyunsaturated fatty acids can improve the toxicant-induced inflammation. There is evidence that bioactive nutrients protect through multiple cell signaling pathways, but we have shown that lipid raft caveolae and the antioxidant defense controller nuclear factor (erythroid-derived 2)-like 2 (Nrf2) both play a predominant role in nutritional modulation of PCB-induced vascular toxicity. Interestingly, there appears to be an intimate cross-talk between caveolae-related proteins and cellular Nrf2, and focusing on the use of specific bioactive food components that simultaneously alter both pathways may produce a more effective and efficient cytoprotective response to toxicant exposure. The use of nutrition as a protective tool is an economically beneficial means to address the toxicity of persistent environmental toxicants and may become a sensible means to protect human populations from PCB-induced vascular inflammation and associated chronic diseases.
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References
Arsenescu V, Arsenescu RI, King V, Swanson H, Cassis LA (2008) Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ Heal Perspect 116(6):761–768. doi:10.1289/ehp.10554
Baird L, Dinkova-Kostova AT (2011) The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 85(4):241–272. doi:10.1007/s00204-011-0674-5
Baker PR, Schopfer FJ, O’Donnell VB, Freeman BA (2009) Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free Radic Biol Med 46(8):989–1003. doi:10.1016/j.freeradbiomed.2008.11.021
Baum SJ, Kris-Etherton PM, Willett WC, Lichtenstein AH, Rudel LL, Maki KC, Whelan J, Ramsden CE, Block RC (2012) Fatty acids in cardiovascular health and disease: a comprehensive update. Journal of clinical lipidology 6(3):216–234. doi:10.1016/j.jacl.2012.04.077
Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nature reviews Drug discovery 5(6):493–506. doi:10.1038/nrd2060
Borniquel S, Jansson EA, Cole MP, Freeman BA, Lundberg JO (2010) Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease. Free Radic Biol Med 48(4):499–505. doi:10.1016/j.freeradbiomed.2009.11.014
Butler Walker J, Seddon L, McMullen E, Houseman J, Tofflemire K, Corriveau A, Weber JP, Mills C, Smith S, Van Oostdam J (2003) Organochlorine levels in maternal and umbilical cord blood plasma in Arctic Canada. Sci Total Environ 302(1–3):27–52
Byun EB, Choi HG, Sung NY, Byun EH (2012) Green tea polyphenol epigallocatechin-3-gallate inhibits TLR4 signaling through the 67-kDa laminin receptor on lipopolysaccharide-stimulated dendritic cells. Biochem Biophys Res Commun 426(4):480–485. doi:10.1016/j.bbrc.2012.08.096
Carpenter D (2011) Exposure to polychlorinated biphenyls is associated with an increased risk of hypertension and cardiovascular disease. Epidemiology 22(1):S147–S147. doi:10.1097/01.ede.0000392123.34740.fc
Choi YJ, Arzuaga X, Kluemper CT, Caraballo A, Toborek M, Hennig B (2010) Quercetin blocks caveolae-dependent pro-inflammatory responses induced by co-planar PCBs. Environ Int 36(8):931–934. doi:10.1016/j.envint.2009.06.009
Ciftci O, Ozdemir I (2011) Protective effects of quercetin and chrysin against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induced oxidative stress, body wasting and altered cytokine productions in rats. Immunopharmacol Immunotoxicol 33(3):504–508. doi:10.3109/08923973.2010.543686
Crinnion WJ (2011) Polychlorinated biphenyls: persistent pollutants with immunological, neurological, and endocrinological consequences. Alternative medicine review: a journal of clinical therapeutic 16(1):5–13
Dirinck E, Jorens PG, Covaci A, Geens T, Roosens L, Neels H, Mertens I, Van Gaal L (2011) Obesity and persistent organic pollutants: possible obesogenic effect of organochlorine pesticides and polychlorinated biphenyls. Obesity (Silver Spring, Md) 19(4):709–714. doi:10.1038/oby.2010.133
Fam SS, Murphey LJ, Terry ES, Zackert WE, Chen Y, Gao L, Pandalai S, Milne GL, Roberts LJ, Porter NA, Montine TJ, Morrow JD (2002) Formation of highly reactive A-ring and J-ring isoprostane-like compounds (A4/J4-neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 277(39):36076–36084. doi:10.1074/jbc.M205638200
Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, Lisanti MP (2004) Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol 24(1):98–105. doi:10.1161/01.atv.0000101182.89118.e5
Freeman BA, Baker PR, Schopfer FJ, Woodcock SR, Napolitano A, D’ischia M (2008) Nitro-fatty acid formation and signaling. J Biol Chem 283(23):15515–15519. doi:10.1074/jbc.R800004200
Fresno M, Alvarez R, Cuesta N (2011) Toll-like receptors, inflammation, metabolism and obesity. Arch Physiol Biochem 117(3):151–164. doi:10.3109/13813455.2011.562514
Ganguly R, Pierce GN (2012) Trans fat involvement in cardiovascular disease. Molecular nutrition & food research 56(7):1090–1096. doi:10.1002/mnfr.201100700
Gao L, Wang J, Sekhar KR, Yin H, Yared NF, Schneider SN, Sasi S, Dalton TP, Anderson ME, Chan JY, Morrow JD, Freeman ML (2007) Novel n-3 fatty acid oxidation products activate Nrf2 by destabilizing the association between Keap1 and Cullin3. J Biol Chem 282(4):2529–2537. doi:10.1074/jbc.M607622200
Giesy JP, Kannan K, Blankenship AL, Jones PD, Hilscherova K (2000) Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): implications for risk assessment. Central European journal of public health 8(Suppl):43–45
Gomez Candela C, Bermejo Lopez LM, Loria Kohen V (2011) Importance of a balanced omega 6/omega 3 ratio for the maintenance of health: nutritional recommendations. Nutricion hospitalaria: organo oficial de la Sociedad Espanola de Nutricion Parenteral y Enteral 26(2):323–329. doi:10.1590/s0212-16112011000200013
Goncharov A, Haase RF, Santiago-Rivera A, Morse G, McCaffrey RJ, Rej R, Carpenter DO (2008) High serum PCBs are associated with elevation of serum lipids and cardiovascular disease in a Native American population. Environ Res 106(2):226–239. doi:10.1016/j.envres.2007.10.006
Gustavsson P, Hogstedt C (1997) A cohort study of Swedish capacitor manufacturing workers exposed to polychlorinated biphenyls (PCBs). American journal of industrial medicine 32(3):234–239
Ha MH, Lee DH, Jacobs DR (2007) Association between serum concentrations of persistent organic pollutants and self-reported cardiovascular disease prevalence: results from the National Health and Nutrition Examination Survey, 1999-2002. Environ Heal Perspect 115(8):1204–1209. doi:10.1289/ehp.10184
Han SG, Eum SY, Toborek M, Smart E, Hennig B (2010) Polychlorinated biphenyl-induced VCAM-1 expression is attenuated in aortic endothelial cells isolated from caveolin-1 deficient mice. Toxicol Appl Pharmacol 246(1–2):74–82. doi:10.1016/j.taap.2010.04.009
Han SG, Han SS, Toborek M, Hennig B (2012) EGCG protects endothelial cells against PCB 126-induced inflammation through inhibition of AhR and induction of Nrf2-regulated genes. Toxicol Appl Pharmacol 261(2):181–188. doi:10.1016/j.taap.2012.03.024
Harris DL, Niaz MS, Morrow JD, Mary K, Ramesh A (2009) Diet as a modifier of benzo(a)pyrene metabolism and benzo(a)pyrene—induced colon tumors in ApcMin mice. Interdisciplinary Studies on Environmental Chemistry—Environmental Research in Asia 2:227–238
Hayes JD, Dinkova-Kostova AT, McMahon M (2009) Cross-talk between transcription factors AhR and Nrf2: lessons for cancer chemoprevention from dioxin. Toxicological sciences: an official journal of the Society of Toxicology 111(2):199–201. doi:10.1093/toxsci/kfp168
Hennig B, Slim R, Toborek M, Robertson LW (1999) Linoleic acid amplifies polychlorinated biphenyl-mediated dysfunction of endothelial cells. J Biochem Mol Toxicol 13(2):83–91
Hennig B, Reiterer G, Majkova Z, Oesterling E, Meerarani P, Toborek M (2005a) Modification of environmental toxicity by nutrients: implications in atherosclerosis. Cardiovasc Toxicol 5(2):153–160
Hennig B, Reiterer G, Toborek M, Matveev SV, Daugherty A, Smart E, Robertson LW (2005b) Dietary fat interacts with PCBs to induce changes in lipid metabolism in mice deficient in low-density lipoprotein receptor. Environ Heal Perspect 113(1):83–87
Hennig B, Oesterling E, Toborek M (2007) Environmental toxicity, nutrition, and gene interactions in the development of atherosclerosis. Nutrition, metabolism, and cardiovascular diseases: NMCD 17(2):162–169. doi:10.1016/j.numecd.2006.01.003
Hennig B, Ormsbee L, McClain CJ, Watkins BA, Blumberg B, Bachas LG, Sanderson W, Thompson C, Suk WA (2012) Nutrition can modulate the toxicity of environmental pollutants: implications in risk assessment and human health. Environ Heal Perspect 120(6):771–774. doi:10.1289/ehp.1104712
Hopf NB, Ruder AM, Succop P (2009) Background levels of polychlorinated biphenyls in the U.S. population. Sci Total Environ 407(24):6109–6119. doi:10.1016/j.scitotenv.2009.08.035
Itoh K, Mimura J, Yamamoto M (2010) Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxidants & redox signaling 13(11):1665–1678. doi:10.1089/ars.2010.3222
Kang HJ, Hong YB, Kim HJ, Wang A, Bae I (2012) Bioactive food components prevent carcinogenic stress via Nrf2 activation in BRCA1 deficient breast epithelial cells. Toxicol Lett 209(2):154–160. doi:10.1016/j.toxlet.2011.12.002
Kansanen E, Bonacci G, Schopfer FJ, Kuosmanen SM, Tong KI, Leinonen H, Woodcock SR, Yamamoto M, Carlberg C, Yla-Herttuala S, Freeman BA, Levonen AL (2011) Electrophilic nitro-fatty acids activate NRF2 by a KEAP1 cysteine 151-independent mechanism. J Biol Chem 286(16):14019–14027. doi:10.1074/jbc.M110.190710
Khoo NK, Freeman BA (2010) Electrophilic nitro-fatty acids: anti-inflammatory mediators in the vascular compartment. Curr Opin Pharmacol 10(2):179–184. doi:10.1016/j.coph.2009.11.003
Kim J, Cha YN, Surh YJ (2010) A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res 690(1–2):12–23. doi:10.1016/j.mrfmmm.2009.09.007
Kim S, Jin Y, Choi Y, Park T (2011) Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 81(11):1343–1351. doi:10.1016/j.bcp.2011.03.012
Kuehn BM (2011) Environmental pollutants tied to atherosclerosis. JAMA: the journal of the American Medical Association 306(19):2081. doi:10.1001/jama.2011.1666
Kuipers RS, de Graaf DJ, Luxwolda MF, Muskiet MH, Dijck-Brouwer DA, Muskiet FA (2011) Saturated fat, carbohydrates and cardiovascular disease. The Netherlands journal of medicine 69(9):372–378
Leiherer A, Mundlein A, Drexel H (2013) Phytochemicals and their impact on adipose tissue inflammation and diabetes. Vasc Pharmacol 58(1–2):3–20. doi:10.1016/j.vph.2012.09.002
Li W, Liu H, Zhou JS, Cao JF, Zhou XB, Choi AM, Chen ZH, Shen HH (2012) Caveolin-1 inhibits expression of antioxidant enzymes through direct interaction with nuclear erythroid 2 p45-related factor-2 (Nrf2). J Biol Chem 287(25):20922–20930. doi:10.1074/jbc.M112.352336
Lim EJ, Smart EJ, Toborek M, Hennig B (2007) The role of caveolin-1 in PCB77-induced eNOS phosphorylation in human-derived endothelial cells. Am J Physiol Heart Circ Physiol 293(6):H3340–H3347. doi:10.1152/ajpheart.00921.2007
Lim EJ, Majkova Z, Xu S, Bachas L, Arzuaga X, Smart E, Tseng MT, Toborek M, Hennig B (2008) Coplanar polychlorinated biphenyl-induced CYP1A1 is regulated through caveolae signaling in vascular endothelial cells. Chemico-biological interactions 176(2–3):71–78. doi:10.1016/j.cbi.2008.08.007
Lundqvist C, Zuurbier M, Leijs M, Johansson C, Ceccatelli S, Saunders M, Schoeters G, ten Tusscher G, Koppe JG (2006) The effects of PCBs and dioxins on child health. Acta paediatrica (Oslo, Norway: 1992) Supplement 95(453):55–64. doi:10.1080/08035320600886257
Majkova Z, Smart E, Toborek M, Hennig B (2009) Up-regulation of endothelial monocyte chemoattractant protein-1 by coplanar PCB77 is caveolin-1-dependent. Toxicol Appl Pharmacol 237(1):1–7. doi:10.1016/j.taap.2009.02.016
Majkova Z, Toborek M, Hennig B (2010) The role of caveolae in endothelial cell dysfunction with a focus on nutrition and environmental toxicants. Journal of cellular and molecular medicine 14(10):2359–2370. doi:10.1111/j.1582-4934.2010.01064.x
Majkova Z, Layne J, Sunkara M, Morris AJ, Toborek M, Hennig B (2011) Omega-3 fatty acid oxidation products prevent vascular endothelial cell activation by coplanar polychlorinated biphenyls. Toxicol Appl Pharmacol 251(1):41–49. doi:10.1016/j.taap.2010.11.013
Miao X, Bai Y, Su W, Cui W, Xin Y, Wang Y, Tan Y, Miao L, Fu Y, Su G, Cai L (2012) Sulforaphane prevention of diabetes-induced aortic damage was associated with the up-regulation of Nrf2 and its down-stream antioxidants. Nutrition & metabolism 9(1):84. doi:10.1186/1743-7075-9-84
Moore RJ, Jackson KG, Minihane AM (2009) Green tea (Camellia sinensis) catechins and vascular function. Br J Nutr 102(12):1790–1802. doi:10.1017/s0007114509991218
Morita K, Matsueda T, Iida T (1997) Effect of green tea (matcha) on gastrointestinal tract absorption of polychlorinated biphenyls, polychlorinated dibenzofurans and polychlorinated dibenzo-p-dioxins in rats. Fukuoka igaku zasshi = Hukuoka acta medica 88(5):162–168
Moysich KB, Shields PG, Freudenheim JL, Schisterman EF, Vena JE, Kostyniak P, Greizerstein H, Marshall JR, Graham S, Ambrosone CB (1999) Polychlorinated biphenyls, cytochrome P4501A1 polymorphism, and postmenopausal breast cancer risk. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 8(1):41–44
Mozaffarian D, Wu JH (2011) Omega-3 fatty acids and cardiovascular disease: effects on risk factors, molecular pathways, and clinical events. J Am Coll Cardiol 58(20):2047–2067. doi:10.1016/j.jacc.2011.06.063
Muller J, Pfaffl MW (2012) Synergetic downregulation of 67 kDa laminin receptor by the green tea (Camellia sinensis) secondary plant compound epigallocatechin gallate: a new gateway in metastasis prevention? BMC Complem Altern M 12:258. doi:10.1186/1472-6882-12-258
Musiek ES, Brooks JD, Joo M, Brunoldi E, Porta A, Zanoni G, Vidari G, Blackwell TS, Montine TJ, Milne GL, McLaughlin B, Morrow JD (2008) Electrophilic cyclopentenone neuroprostanes are anti-inflammatory mediators formed from the peroxidation of the omega-3 polyunsaturated fatty acid docosahexaenoic acid. J Biol Chem 283(29):19927–19935. doi:10.1074/jbc.M803625200
Nadtochiy SM, Redman EK (2011) Mediterranean diet and cardioprotection: the role of nitrite, polyunsaturated fatty acids, and polyphenols. Nutrition (Burbank, Los Angeles County, Calif) 27(7–8):733–744. doi:10.1016/j.nut.2010.12.006
Nair S, Barve A, Khor TO, Shen GX, Lin W, Chan JY, Cai L, Kong AN (2010) Regulation of Nrf2- and AP-1-mediated gene expression by epigallocatechin-3-gallate and sulforaphane in prostate of Nrf2-knockout or C57BL/6J mice and PC-3 AP-1 human prostate cancer cells. Acta Pharmacologica Sinica 31(9):1223–1240. doi:10.1038/aps.2010.147
Nebert DW, Karp CL (2008) Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J Biol Chem 283(52):36061–36065. doi:10.1074/jbc.R800053200
Niture SK, Jain AK, Jaiswal AK (2009) Antioxidant-induced modification of INrf2 cysteine 151 and PKC-delta-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. Journal of cell science 122(Pt 24):4452–4464. doi:10.1242/jcs.058537
Panneerselvam M, Patel HH, Roth DM (2012) Caveolins and heart diseases. Advances in experimental medicine and biology 729:145–156. doi:10.1007/978-1-4614-1222-9_10
Pavlides S, Gutierrez-Pajares JL, Danilo C, Lisanti MP, Frank PG (2012) Atherosclerosis, caveolae and caveolin-1. Advances in experimental medicine and biology 729:127–144. doi:10.1007/978-1-4614-1222-9_9
Poudyal H, Panchal SK, Diwan V, Brown L (2011) Omega-3 fatty acids and metabolic syndrome: effects and emerging mechanisms of action. Progress in lipid research 50(4):372–387. doi:10.1016/j.plipres.2011.06.003
Rechner AR, Kuhnle G, Bremner P, Hubbard GP, Moore KP, Rice-Evans CA (2002) The metabolic fate of dietary polyphenols in humans. Free Radic Biol Med 33(2):220–235
Rudolph TK, Rudolph V, Edreira MM, Cole MP, Bonacci G, Schopfer FJ, Woodcock SR, Franek A, Pekarova M, Khoo NK, Hasty AH, Baldus S, Freeman BA (2010) Nitro-fatty acids reduce atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 30(5):938–945. doi:10.1161/atvbaha.109.201582
Schettgen T, Gube M, Esser A, Alt A, Kraus T (2012) Plasma polychlorinated biphenyls (PCB) levels of workers in a transformer recycling company, their family members, and employees of surrounding companies. Journal of toxicology and environmental health Part A 75(8–10):414–422. doi:10.1080/15287394.2012.674905
Singh S, Vrishni S, Singh BK, Rahman I, Kakkar P (2010) Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases. Free Radic Res 44(11):1267–1288. doi:10.3109/10715762.2010.507670
Slim R, Toborek M, Robertson LW, Hennig B (1999) Antioxidant protection against PCB-mediated endothelial cell activation. Toxicological sciences: an official journal of the Society of Toxicology 52(2):232–239
Sowa G (2012) Caveolae, caveolins, cavins, and endothelial cell function: new insights. Front Physiol 2:120. doi:10.3389/fphys.2011.00120
Terao J (2009) Dietary flavonoids as antioxidants. Forum of nutrition 61:87–94. doi:10.1159/000212741
Toborek M, Barger SW, Mattson MP, Espandiari P, Robertson LW, Hennig B (1995) Exposure to polychlorinated biphenyls causes endothelial cell dysfunction. J Biochem Toxicol 10(4):219–226
Tompkins LM, Wallace AD (2007) Mechanisms of cytochrome P450 induction. J Biochem Mol Toxicol 21(4):176–181
Tsujita T, Li L, Nakajima H, Iwamoto N, Nakajima-Takagi Y, Ohashi K, Kawakami K, Kumagai Y, Freeman BA, Yamamoto M, Kobayashi M (2011) Nitro-fatty acids and cyclopentenone prostaglandins share strategies to activate the Keap1-Nrf2 system: a study using green fluorescent protein transgenic zebrafish. Genes to cells: devoted to molecular & cellular mechanisms 16(1):46–57. doi:10.1111/j.1365-2443.2010.01466.x
Turkez H, Geyikoglu F, Yousef MI (2012) Ameliorative effect of docosahexaenoic acid on 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced histological changes, oxidative stress, and DNA damage in rat liver. Toxicol Ind Heal 28(8):687–696. doi:10.1177/0748233711420475
Tutel’yan VA, Gapparov MM, Telegin LY, Devichenskii VM, Pevnitskii LA (2003) Flavonoids and resveratrol as regulators of Ah-receptor activity: protection from dioxin toxicity. Bulletin of experimental biology and medicine 136(6):533–539
Uemura H (2012) Associations of exposure to dioxins and polychlorinated biphenyls with diabetes: based on epidemiological findings. Nihon eiseigaku zasshi Japanese journal of hygiene 67(3):363–374
Urpi-Sarda M, Zamora-Ros R, Lamuela-Raventos R, Cherubini A, Jauregui O, de la Torre R, Covas MI, Estruch R, Jaeger W, Andres-Lacueva C (2007) HPLC-tandem mass spectrometric method to characterize resveratrol metabolism in humans. Clin Chem 53(2):292–299. doi:10.1373/clinchem.2006.071936
Urpi-Sarda M, Casas R, Chiva-Blanch G, Romero-Mamani ES, Valderas-Martinez P, Arranz S, Andres-Lacueva C, Llorach R, Medina-Remon A, Lamuela-Raventos RM, Estruch R (2012) Virgin olive oil and nuts as key foods of the Mediterranean diet effects on inflammatory biomakers related to atherosclerosis. Pharmacological research: the official journal of the Italian Pharmacological Society 65(6):577–583. doi:10.1016/j.phrs.2012.03.006
Wang LX, Heredia A, Song H, Zhang Z, Yu B, Davis C, Redfield R (2004) Resveratrol glucuronides as the metabolites of resveratrol in humans: characterization, synthesis, and anti-HIV activity. J Pharm Sci 93(10):2448–2457. doi:10.1002/jps.20156
Wang L, Reiterer G, Toborek M, Hennig B (2008) Changing ratios of omega-6 to omega-3 fatty acids can differentially modulate polychlorinated biphenyl toxicity in endothelial cells. Chemico-biological interactions 172(1):27–38. doi:10.1016/j.cbi.2007.11.003
Wang JJ, Zheng Y, Sun L, Wang L, Yu PB, Li HL, Tian XP, Dong JH, Zhang L, Xu J, Shi W, Ma TY (2011) CYP1A1 Ile462Val polymorphism and susceptibility to lung cancer: a meta-analysis based on 32 studies. European journal of cancer prevention: the official journal of the European Cancer Prevention Organisation (ECP) 20(6):445–452. doi:10.1097/CEJ.0b013e328345f937
Watkins BA, Hannon K, Ferruzzi M, Li Y (2007) Dietary PUFA and flavonoids as deterrents for environmental pollutants. J Nutr Biochem 18(3):196–205. doi:10.1016/j.jnutbio.2006.12.002
Wu JM, Wang ZR, Hsieh TC, Bruder JL, Zou JG, Huang YZ (2001) Mechanism of cardioprotection by resveratrol, a phenolic antioxidant present in red wine (review). International journal of molecular medicine 8(1):3–17
Wu J, Liu J, Waalkes MP, Cheng ML, Li L, Li CX, Yang Q (2008) High dietary fat exacerbates arsenic-induced liver fibrosis in mice. Experimental biology and medicine (Maywood, NJ) 233(3):377–384. doi:10.3181/0710-rm-269
Yeager RL, Reisman SA, Aleksunes LM, Klaassen CD (2009) Introducing the “TCDD-inducible AhR-Nrf2 gene battery”. Toxicological sciences: an official journal of the Society of Toxicology 111(2):238–246. doi:10.1093/toxsci/kfp115
Zheng Y, Toborek M, Hennig B (2010) Epigallocatechin gallate-mediated protection against tumor necrosis factor-alpha-induced monocyte chemoattractant protein-1 expression is heme oxygenase-1 dependent. Metab Clin Exp 59(10):1528–1535. doi:10.1016/j.metabol.2010.01.018
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This work was supported by NIH/NIEHS grant P42ES007380. NIEHS T32 (ES07266) and the Kentucky Agricultural Experiment Station.
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Petriello, M.C., Newsome, B. & Hennig, B. Influence of nutrition in PCB-induced vascular inflammation. Environ Sci Pollut Res 21, 6410–6418 (2014). https://doi.org/10.1007/s11356-013-1549-5
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DOI: https://doi.org/10.1007/s11356-013-1549-5