Teratogenic effects of polar compounds in oxidized frying oil
Main Article Content
Abstract
Although deep-fried foods are very popular, the safety of oxidized frying oil (OFO), which is ingested with fried food, is a concern. Consequently, food safety regulations in many countries set an upper limit of 25% polar compounds (PC). The PC comprises all oxidatively altered components in used oils; they may be regarded as a xenobiotic or endocrine-disrupting chemical, as they activate PPARa and induce expression of detoxifying cytochrome P450 monoxygenase and phase II conjugation enzymes to facilitate their own catabolism. Recently, we reported that pregnant C57BL/6J mice fed PC had a higher incidence of fetuses with congenital malformations. This review summarizes the chemical reactions and PC composition in OFO, effects of PC on modulating transcriptional activity of xenobiotic receptors including aryl hydrocarbon receptor, constitutive androstane receptor, pregnane X receptor and PPARa, the importance of retinoic acid (RA) in organogenesis of developing embryos, as well as teratogenic effects of PC. Plausible underlying mechanisms are also discussed. We speculate that the pathogenesis of congenital malformations is disturbed RA metabolism via crosstalks between xenobiotic receptors.
Article Details
How to Cite
CHAO, Pei-Min; LIN, Yu-Shun.
Teratogenic effects of polar compounds in oxidized frying oil.
Medical Research Archives, [S.l.], v. 4, n. 8, dec. 2016.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/911>. Date accessed: 24 nov. 2024.
Keywords
oxidized frying oil, polar compounds, teratogenesis, retinoic acid, cytochrome P450
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
Adams MK, Belvaeva OV, Wu L, et al. The retinaldehyde reductase activity of DHRS3 is reciprocally activated by retinol dehydrogenase 10 to control retinoid homeostasis. J Biol Chem. 2014; 289(21): 14868–14880.
Andreola F, Hayhurst GP, Luo G, et al. Mouse liver CYP2C39 is a novel retinoic acid 4-hydroxylase. Its down-regulation offers a molecular basis for liver retinoid accumulation and fibrosis in aryl hydrocarbon receptor-null mice. J Biol Chem. 2004; 279(5): 3434-3438.
Artman N. The chemical and biological properties of heated and oxidized fats. Adv Lipids Res. 1969; 7: 245-330.
Ashique AM, May SR, Kane MA, et al. Morphological defects in a novel Rdh10 mutant that has reduced retinoic acid biosynthesis and signaling. Genesis. 2012; 50(5): 415–423.
Bansal S, Leu AN, Gonzalez FJ, et al. Mitochondrial targeting of cytochrome P450 (CYP) 1B1 and its role in polycyclic aromatic hydrocarbon-induced mitochondrial dysfunction. J Biol Chem. 2014; 289(14): 9936-9951.
Birringer M, Drogan D, Brigelius-Flohe R. Tocopherols are metabolized in HepG2 cells by side chain -oxidation and consecutive -oxidation. Free Radic Biol Med. 2001; 31(2): 226-232.
Boily MH, Berube VE, Spear PA, et al. Hepatic retinoids of bullfrogs in relation to agricultural pesticides. Environ Toxicol Chem. 2005; 24(5): 1099–1106.
Brandsch C, Eder K. Effects of peroxidation products in thermoxidised dietary oil in female rats during rearing, pregnancy and lactation on their reproductive performance and the antioxidative status of their offspring. Br J Nutr. 2004; 92(2): 267–275.
Champoux L, Rodrigue J, Trudeau S, et al. Contamination and biomarkers in the great blue heron, an indicator of the state of the st Lawrence river. Ecotoxicology. 2006; 15(1): 83–96.
Chao PM, Chao CY, Lin FJ, Huang CJ. Oxidized frying oil up-regulates hepatic acyl-CoA oxidase and cyptochrome P450 4A1 genes in rats and activates PPAR. J Nutr. 2001; 131(12): 3166-3174.
Chao PM, Huang HL, Liao CH, et al. A high oxidized frying oil content diet is less adipogenic, but induces glucose intolerance in rodents. Br J Nutr. 2007; 98(1): 63-71.
Chen YC, Chen BH. Determination of polycyclic aromatic hydrocarbons in fumes from fried chicken legs. J Agric Food Chem. 2003; 51(14): 4162-4167.
Chiang YF, Shaw HM, Yang MF, et al. Dietary oxidized frying oil causes oxidative damage of pancreatic islets and impairment of insulin secretion, effects associated with vitamin E deficiency. Br J Nutr. 2011; 105(9): 1311-1319.
Choe E, Min DB. Chemistry of deep-fat frying oils. J Food Sci. 2007; 72(5): R77–86.
Chow CK. Biological effects of oxidized fatty acids. In: Chow CK, editor. Fatty Acids in Foods and Their Health Implications. CRC Press; 2007, 3th ed., p. 855-878.
Cohn JS. Oxidized fat in the diet, postprandial lipaemia and cardiovascular disease. Curr Opin Lipidol. 2002; 13(1): 19-24.
Delerive P, Furman C, Teissier E, et al. Oxidized phospholipids activate PPAR in a phospholipase A2- dependent manner. FEBS Lett. 2000; 471(1): 34–38.
Desvergne B, Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev. 1999; 20(5): 649–688.
Dobarganes C, Ma´rquez-Ruiz G. Possible adverse effects of frying with vegetable oils. Br J Nutr. 2015; 113(suppl 2): S49–57.
Dobarganes MC, Ma´rquez-Ruiz G. Formation and analysis of oxidized monomeric, dimeric and higher oligomeric triglycerides. In: Erickson MD, editor. Deep frying: Chemistry, Nutrition and Practical Applications. Champaign: AOCS Press; 2007. p. 87–110.
Eder K. The effects of a dietary oxidized oil on lipid metabolism in rats. Lipids. 1999; 34: 717-725.
Ekins S, Kortagere S, Iyer M, et al. Challenges predicting ligand-receptor interactions of promiscuous proteins: the nuclear receptor PXR. PLoS Comput Biol. 2009; 5(12): e1000594.
Fan LQ, Brown-Borg H, Brown S, et al. PPARalpha activators down-regulate CYP2C7, a retinoic acid and testosterone hydroxylase. Toxicology. 2004; 203(1-3): 41-48.
Firestone D. Regulation of frying fat and oil. In: Erickson MD, editor. Deep frying: Chemistry, Nutrition and Practical Applications. Champaign: AOCS Press; 2007. p. 373–85.
Gao YT, Blot WJ, Zheng W, et al. Lung cancer among Chinese women. Int J Cancer. 1987; 40(5): 604-609.
Ghanayem BI, McDaniel LP, Churchwell MI, et al. Role of CYP2E1 in the epoxidation of acrylamide to glycidamide and formation of DNA and hemoglobin adducts. Toxicol Sci. 2005; 88(2): 311-318.
Gilardi F, Desvergne B. RXRs: collegial partners. Subcell Biochem. 2014; 70: 75-102.
Goldbeter A, Gonze D, Pourquié O. Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev Dyn. 2007; 236(6): 1495-1508.
Gonz'alez-Munoz MJ, Bastida S, S'anchez-Muniz FJ. Short term in vivo digestibility of triglyceride polymers, dimmers, and monomers of thermoxidized palm olein used in deep frying. J Agric Food Chem. 1998; 46(12): 5188-5193.
Huang CF, Lin YS, Chiang ZC, et al. Oxidized frying oil and its polar fraction fed to pregnant mice are teratogenic and alter mRNA expressions of vitamin A metabolism genes in the liver of dams and their fetuses. J Nutr Biochem. 2014; 25(5): 549–556.
Huang CJ, Cheung NS, Lu VR. Effects of deteriorated frying oil and dietary protein levels on liver microsomal enzymes in rats. J Am Oil Chem Soc. 1988; 65(11): 1796-1803.
Huang WC, Kang ZC, Li YJ, Shaw HM. Effects of oxidized frying oil on proteins related to alpha-tocopherol metabolism in rat liver. J Clin Biochem Nutr. 2009; 45(1):20-28.
Indart A, Viana M, Grootveld MC, et al. Teratogenic actions of thermally-stressed culinary oils in rats. Free Radic Res. 2002; 36(10): 1051-1058.
Issemann I, Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature. 1990; 347(6294): 645-650.
Kanner J. Dietary advanced lipid oxidation endproducts are risk factors to human health. Mol Nutr Food Res. 2007; 51(9): 1094-1101.
Koch A, Ko¨nig B, Spielmann J, et al. Thermally oxidized oil increases the expression of insulin-induced genes and inhibits activation of sterol regulatory element-binding protein-2 in rat liver. J Nutr. 2007; 137(9): 2018-2023.
Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 1998; 139 (10): 4252-4263.
Lee LM, Leung CY, Tang WW, et al. A paradoxical teratogenic mechanism for retinoic acid. Proc Natl Acad Sci U S A. 2012; 109(34): 13668–13673.
Lei Z, Chen W, Zhang M, Napoli JL. Reduction of all-trans-retinal in the mouse liver peroxisome fraction by the short-chain dehydrogenase/reductase RRD: induction by the PPAR alpha ligand clofibrate. Biochemistry. 2003; 42(14): 4190–4196.
Liao CH, Shaw HM, Chao PM. Impairment of glucose metabolism in mice induced by dietary oxidized frying oil is different from that induced by conjugated linoleic acid. Nutrition. 2008; 24(7-8): 744-752.
Lin YS, Lin TY, Wu JJ, et al. Peroxisome proliferator-activated receptor α deficiency by itself disturbs retinoic acid metabolism but is not the main contributor to teratogenesis elicited by polar compounds from oxidized frying oil. Manuscript in review.
Liu JF, Huang CJ. Tissue -tocopherol retention in male rats is compromised by feeding diets containing oxidized frying oil. J Nutr. 1995; 125(12): 3071-3080.
Liu JF, Huang CJ. Dietary oxidized frying oil enhances tissue -tocopherol depletion and radioisotope tracer excretion in vitamin E-deficient rats. J Nutr. 1996; 126(9): 2227-2235.
LopezCarrillo L, TorresArreola L, TorresSanchez L, et al. Is DDT use a public health problem in Mexico? Environ Health Perspect. 1996; 104(6): 584-588.
Lu YF, Lo YC. Effect of deep frying oil given with and without dietary cholesterol on lipid metabolism in rats. Nutr Res. 1995; 15(12): 1783-1792.
Marmesat S, Rodrigues E, Velasco J, Dobarganes C. Quality of used frying fats and oils: comparison of rapid tests based on chemical and physical oil properties. Int J Food Sci Technol. 2007; 42(5): 601–608.
Ma´rquez-Ruiz G, Guevel G, Dobarganes MC. Application of chromatographic techniques to evaluate enzymatic hydrolysis of oxidized and polymeric triglycerides by pancreatic lipase ‘in vitro’. J Am Oil Chem Soc. 1998; 75(2): 119–126.
Marshall H, Morrison A, Studer M, et al. Retinoids and Hox genes. FASEB J. 1996; 10(9): 969–978.
Martin JC, Joffre FM, Siess H, et al. Cyclic fatty acid monomers from heated oil modify the activities of lipid synthesizing and oxidizing enzymes in rat liver. J Nutr. 2000; 130(6): 1524–1530.
Mic FA, Haselbeck RJ, Cuenca AE, Duester G. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development. 2002; 129(9): 2271-2282.
Miyagawa K, Hirai K, Takezoe R. Tocopherol and fluorescence levels in deep-frying oil and their measurement for oil assessment. J Am Oil Chem Soc. 1991; 68(3): 163-166.
Moreira RG, Castell-Perez ME, Barrufet MA. Fried product processing and characteristics. In: Deep-Fat Frying: Fundamentals and Applications. Gaithersburg, Md.: Chapman & Hall Food Science Book. 1991:11-31.
Nagy L, Tontonoz PJ, Alvarez GA, et al. Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR. Cell. 1998; 93(2): 229–240.
Nawar WW. Chemical changes in lipids produced by thermal processing. J Chem Edu. 1984; 61(4): 299–302.
Nebert DW, Russell DW. Clinical importance of the cytochromes P450. Lancet. 2002; 360(9340): 1155-1162.
Novak J, Benisek M, Hilscherova K. Disruption of retinoid transport, metabolism and signaling by environmental pollutants. Environ Int. 2008; 34(6): 898–913.
Pares X, Farres J, Kedishvili N, Duester G. Medium-chain and short-chain dehydrogenases/reductases in retinoid metabolism. Cell Mol Life Sci. 2008; 65(24): 3936–3949.
Parker RS, Sontag TJ, Swanson JE. Cytochrome P4503A dependent metabolism of tocopherols and inhibition by sesamin. Biochem Biophys Res Commun. 2000; 277(3): 531-534.
Pennimpede T, Cameron DA, MacLean GA, et al. The role of CYP26 enzymes in defining appropriate retinoic acid exposure during embryogenesis. Birth Defects Res A Clin Mol Teratol. 2010; 88(10): 883-894.
Reijntjes S, Blentic A, Gale E, Maden M. The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol. 2005; 285(1): 224-237.
Richter CA, Birnbaum LS, Farabollini F, et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007; 24(2): 199-224.
Romero A, Bastida S, Sánchez-Muniz FJ. Cyclic fatty acid monomer formation in domestic frying of frozen foods in sunflower oil and high oleic acid sunflower oil without oil replenishment. Food Chem Toxicol. 2006; 44(10): 1674-1681.
Ross AC, Zolfaghari R. Cytochrome P450s in the regulation of cellular retinoic acid metabolism. Annu Rev Nutr. 2011; 31: 65-87.
Saguy S, Dana D. Integrated approach to deep fat frying: engineering, nutrition, health and consumer aspects. J Food Eng. 2003; 56(2-3): 143–152.
Scott HM, Hutchison GR, Mahood IK, et al. Role of androgens in fetal testis development and dysgenesis. Endocrinology. 2007; 148(5): 2027-2036.
Shoeb M, Ansari NH, Srivastava SK, Ramana KV. 4-hydroxynonenal in the pathogenesis and progression of human diseases. Curr Med Chem. 2014; 21(2): 230–237.
Stevens JF, Maier CS. Acrolein: Sources, metabolism, and biomolecular interactions relevant to human health and disease. Mol Nutr Food Res. 2008; 52(1):7-25.
Sulzle A, Hirche F, Eder K. Thermally oxidized dietary fat upregulates the expression of target genes of PPAR alpha in rat liver. J Nutr. 2004; 134(6): 1375-1383.
Tang YL, Huang CJ. Dietary oxidized frying oil decreased plasma and liver vitamin A in rats. Nutr Sci J. 1998; 23: 265–279
Tareke E, Rydberg P, Karlsson P, et al. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem. 2002; 50(7): 4998-5006.
Tay S, Dickmann L, Dixit V, Isoherranen N. A comparison of the roles of peroxisome proliferator-activated receptor and retinoic acid receptor on CYP26 regulation. Mol Pharmacol. 2010; 77(2): 218-227.
Tickle C, Alberts B, Wolpert L, Lee J. Local application of retinoic acid to the limb bond mimics the action of the polarizing region. Nature. 1982; 296(5857): 564-566.
Tolson AH, Wang H. Regulation of drug-metabolizing enzymes by xenobiotic receptors: PXR and CAR. Adv Drug Deliv Rev. 2010; 62(13): 1238–1249.
Totani N, Yawata M, Takada M, Moriya M. Acrylamide content of commercial frying oil. J Oleo Sci. 2007; 56(2): 103-106.
Ulven SM, Gundersen TE, Weedon MS, et al. Identification of endogenous retinoids, enzymes, binding proteins, and receptors during early postimplantation development in mouse: important role of retinal dehydrogenase type 2 in synthesis of all-trans-retinoic acid. Dev Biol. 2000; 220(2): 379-391.
Van Wauwe JP, Coene MC, Goossens J, et al. Effects of cytochrome P-450 inhibitors on the in vivo metabolism of all-trans-retinoic acid in rats. J Pharmacol Exp Ther. 1990; 252(1): 365-369.
Wenzl T, Simon R, Klieiner J, Anklam E. Analytical methods for polycyclic aromatic hydrocarbons (PAHs) in food and the environment needed for new food legislation in the European Union. Trends Anal Chem. 2006; 25(7): 716–725.
Wilson JG, Roth CB, Warkany J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat. 1953; 92(2): 189-217.
Wilson R, Fernie CE, Scrimgeour CM, et al. Dietary epoxy fatty acids are absorbed in healthy women. Eur J Clin Invest. 2002; 32(2): 79–83.
Wilson R, Lyall K, Smyth L, et al. Dietary hydroxy fatty acids are absorbed in humans: implications for the measurement of oxidative stress in vivo. Free Radic Biol Med. 2002; 32(2): 162–168.
You L, Casanova M, Archibeque-Engle S, et al. Impaired male sexual development in perinatal Sprague-Dawley and Long-Evans hooded rats exposed in utero and lactationally to p,p '-DDE. Toxicol Sci. 1998; 45(2): 162-173.
Andreola F, Hayhurst GP, Luo G, et al. Mouse liver CYP2C39 is a novel retinoic acid 4-hydroxylase. Its down-regulation offers a molecular basis for liver retinoid accumulation and fibrosis in aryl hydrocarbon receptor-null mice. J Biol Chem. 2004; 279(5): 3434-3438.
Artman N. The chemical and biological properties of heated and oxidized fats. Adv Lipids Res. 1969; 7: 245-330.
Ashique AM, May SR, Kane MA, et al. Morphological defects in a novel Rdh10 mutant that has reduced retinoic acid biosynthesis and signaling. Genesis. 2012; 50(5): 415–423.
Bansal S, Leu AN, Gonzalez FJ, et al. Mitochondrial targeting of cytochrome P450 (CYP) 1B1 and its role in polycyclic aromatic hydrocarbon-induced mitochondrial dysfunction. J Biol Chem. 2014; 289(14): 9936-9951.
Birringer M, Drogan D, Brigelius-Flohe R. Tocopherols are metabolized in HepG2 cells by side chain -oxidation and consecutive -oxidation. Free Radic Biol Med. 2001; 31(2): 226-232.
Boily MH, Berube VE, Spear PA, et al. Hepatic retinoids of bullfrogs in relation to agricultural pesticides. Environ Toxicol Chem. 2005; 24(5): 1099–1106.
Brandsch C, Eder K. Effects of peroxidation products in thermoxidised dietary oil in female rats during rearing, pregnancy and lactation on their reproductive performance and the antioxidative status of their offspring. Br J Nutr. 2004; 92(2): 267–275.
Champoux L, Rodrigue J, Trudeau S, et al. Contamination and biomarkers in the great blue heron, an indicator of the state of the st Lawrence river. Ecotoxicology. 2006; 15(1): 83–96.
Chao PM, Chao CY, Lin FJ, Huang CJ. Oxidized frying oil up-regulates hepatic acyl-CoA oxidase and cyptochrome P450 4A1 genes in rats and activates PPAR. J Nutr. 2001; 131(12): 3166-3174.
Chao PM, Huang HL, Liao CH, et al. A high oxidized frying oil content diet is less adipogenic, but induces glucose intolerance in rodents. Br J Nutr. 2007; 98(1): 63-71.
Chen YC, Chen BH. Determination of polycyclic aromatic hydrocarbons in fumes from fried chicken legs. J Agric Food Chem. 2003; 51(14): 4162-4167.
Chiang YF, Shaw HM, Yang MF, et al. Dietary oxidized frying oil causes oxidative damage of pancreatic islets and impairment of insulin secretion, effects associated with vitamin E deficiency. Br J Nutr. 2011; 105(9): 1311-1319.
Choe E, Min DB. Chemistry of deep-fat frying oils. J Food Sci. 2007; 72(5): R77–86.
Chow CK. Biological effects of oxidized fatty acids. In: Chow CK, editor. Fatty Acids in Foods and Their Health Implications. CRC Press; 2007, 3th ed., p. 855-878.
Cohn JS. Oxidized fat in the diet, postprandial lipaemia and cardiovascular disease. Curr Opin Lipidol. 2002; 13(1): 19-24.
Delerive P, Furman C, Teissier E, et al. Oxidized phospholipids activate PPAR in a phospholipase A2- dependent manner. FEBS Lett. 2000; 471(1): 34–38.
Desvergne B, Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev. 1999; 20(5): 649–688.
Dobarganes C, Ma´rquez-Ruiz G. Possible adverse effects of frying with vegetable oils. Br J Nutr. 2015; 113(suppl 2): S49–57.
Dobarganes MC, Ma´rquez-Ruiz G. Formation and analysis of oxidized monomeric, dimeric and higher oligomeric triglycerides. In: Erickson MD, editor. Deep frying: Chemistry, Nutrition and Practical Applications. Champaign: AOCS Press; 2007. p. 87–110.
Eder K. The effects of a dietary oxidized oil on lipid metabolism in rats. Lipids. 1999; 34: 717-725.
Ekins S, Kortagere S, Iyer M, et al. Challenges predicting ligand-receptor interactions of promiscuous proteins: the nuclear receptor PXR. PLoS Comput Biol. 2009; 5(12): e1000594.
Fan LQ, Brown-Borg H, Brown S, et al. PPARalpha activators down-regulate CYP2C7, a retinoic acid and testosterone hydroxylase. Toxicology. 2004; 203(1-3): 41-48.
Firestone D. Regulation of frying fat and oil. In: Erickson MD, editor. Deep frying: Chemistry, Nutrition and Practical Applications. Champaign: AOCS Press; 2007. p. 373–85.
Gao YT, Blot WJ, Zheng W, et al. Lung cancer among Chinese women. Int J Cancer. 1987; 40(5): 604-609.
Ghanayem BI, McDaniel LP, Churchwell MI, et al. Role of CYP2E1 in the epoxidation of acrylamide to glycidamide and formation of DNA and hemoglobin adducts. Toxicol Sci. 2005; 88(2): 311-318.
Gilardi F, Desvergne B. RXRs: collegial partners. Subcell Biochem. 2014; 70: 75-102.
Goldbeter A, Gonze D, Pourquié O. Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev Dyn. 2007; 236(6): 1495-1508.
Gonz'alez-Munoz MJ, Bastida S, S'anchez-Muniz FJ. Short term in vivo digestibility of triglyceride polymers, dimmers, and monomers of thermoxidized palm olein used in deep frying. J Agric Food Chem. 1998; 46(12): 5188-5193.
Huang CF, Lin YS, Chiang ZC, et al. Oxidized frying oil and its polar fraction fed to pregnant mice are teratogenic and alter mRNA expressions of vitamin A metabolism genes in the liver of dams and their fetuses. J Nutr Biochem. 2014; 25(5): 549–556.
Huang CJ, Cheung NS, Lu VR. Effects of deteriorated frying oil and dietary protein levels on liver microsomal enzymes in rats. J Am Oil Chem Soc. 1988; 65(11): 1796-1803.
Huang WC, Kang ZC, Li YJ, Shaw HM. Effects of oxidized frying oil on proteins related to alpha-tocopherol metabolism in rat liver. J Clin Biochem Nutr. 2009; 45(1):20-28.
Indart A, Viana M, Grootveld MC, et al. Teratogenic actions of thermally-stressed culinary oils in rats. Free Radic Res. 2002; 36(10): 1051-1058.
Issemann I, Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature. 1990; 347(6294): 645-650.
Kanner J. Dietary advanced lipid oxidation endproducts are risk factors to human health. Mol Nutr Food Res. 2007; 51(9): 1094-1101.
Koch A, Ko¨nig B, Spielmann J, et al. Thermally oxidized oil increases the expression of insulin-induced genes and inhibits activation of sterol regulatory element-binding protein-2 in rat liver. J Nutr. 2007; 137(9): 2018-2023.
Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 1998; 139 (10): 4252-4263.
Lee LM, Leung CY, Tang WW, et al. A paradoxical teratogenic mechanism for retinoic acid. Proc Natl Acad Sci U S A. 2012; 109(34): 13668–13673.
Lei Z, Chen W, Zhang M, Napoli JL. Reduction of all-trans-retinal in the mouse liver peroxisome fraction by the short-chain dehydrogenase/reductase RRD: induction by the PPAR alpha ligand clofibrate. Biochemistry. 2003; 42(14): 4190–4196.
Liao CH, Shaw HM, Chao PM. Impairment of glucose metabolism in mice induced by dietary oxidized frying oil is different from that induced by conjugated linoleic acid. Nutrition. 2008; 24(7-8): 744-752.
Lin YS, Lin TY, Wu JJ, et al. Peroxisome proliferator-activated receptor α deficiency by itself disturbs retinoic acid metabolism but is not the main contributor to teratogenesis elicited by polar compounds from oxidized frying oil. Manuscript in review.
Liu JF, Huang CJ. Tissue -tocopherol retention in male rats is compromised by feeding diets containing oxidized frying oil. J Nutr. 1995; 125(12): 3071-3080.
Liu JF, Huang CJ. Dietary oxidized frying oil enhances tissue -tocopherol depletion and radioisotope tracer excretion in vitamin E-deficient rats. J Nutr. 1996; 126(9): 2227-2235.
LopezCarrillo L, TorresArreola L, TorresSanchez L, et al. Is DDT use a public health problem in Mexico? Environ Health Perspect. 1996; 104(6): 584-588.
Lu YF, Lo YC. Effect of deep frying oil given with and without dietary cholesterol on lipid metabolism in rats. Nutr Res. 1995; 15(12): 1783-1792.
Marmesat S, Rodrigues E, Velasco J, Dobarganes C. Quality of used frying fats and oils: comparison of rapid tests based on chemical and physical oil properties. Int J Food Sci Technol. 2007; 42(5): 601–608.
Ma´rquez-Ruiz G, Guevel G, Dobarganes MC. Application of chromatographic techniques to evaluate enzymatic hydrolysis of oxidized and polymeric triglycerides by pancreatic lipase ‘in vitro’. J Am Oil Chem Soc. 1998; 75(2): 119–126.
Marshall H, Morrison A, Studer M, et al. Retinoids and Hox genes. FASEB J. 1996; 10(9): 969–978.
Martin JC, Joffre FM, Siess H, et al. Cyclic fatty acid monomers from heated oil modify the activities of lipid synthesizing and oxidizing enzymes in rat liver. J Nutr. 2000; 130(6): 1524–1530.
Mic FA, Haselbeck RJ, Cuenca AE, Duester G. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development. 2002; 129(9): 2271-2282.
Miyagawa K, Hirai K, Takezoe R. Tocopherol and fluorescence levels in deep-frying oil and their measurement for oil assessment. J Am Oil Chem Soc. 1991; 68(3): 163-166.
Moreira RG, Castell-Perez ME, Barrufet MA. Fried product processing and characteristics. In: Deep-Fat Frying: Fundamentals and Applications. Gaithersburg, Md.: Chapman & Hall Food Science Book. 1991:11-31.
Nagy L, Tontonoz PJ, Alvarez GA, et al. Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR. Cell. 1998; 93(2): 229–240.
Nawar WW. Chemical changes in lipids produced by thermal processing. J Chem Edu. 1984; 61(4): 299–302.
Nebert DW, Russell DW. Clinical importance of the cytochromes P450. Lancet. 2002; 360(9340): 1155-1162.
Novak J, Benisek M, Hilscherova K. Disruption of retinoid transport, metabolism and signaling by environmental pollutants. Environ Int. 2008; 34(6): 898–913.
Pares X, Farres J, Kedishvili N, Duester G. Medium-chain and short-chain dehydrogenases/reductases in retinoid metabolism. Cell Mol Life Sci. 2008; 65(24): 3936–3949.
Parker RS, Sontag TJ, Swanson JE. Cytochrome P4503A dependent metabolism of tocopherols and inhibition by sesamin. Biochem Biophys Res Commun. 2000; 277(3): 531-534.
Pennimpede T, Cameron DA, MacLean GA, et al. The role of CYP26 enzymes in defining appropriate retinoic acid exposure during embryogenesis. Birth Defects Res A Clin Mol Teratol. 2010; 88(10): 883-894.
Reijntjes S, Blentic A, Gale E, Maden M. The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol. 2005; 285(1): 224-237.
Richter CA, Birnbaum LS, Farabollini F, et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007; 24(2): 199-224.
Romero A, Bastida S, Sánchez-Muniz FJ. Cyclic fatty acid monomer formation in domestic frying of frozen foods in sunflower oil and high oleic acid sunflower oil without oil replenishment. Food Chem Toxicol. 2006; 44(10): 1674-1681.
Ross AC, Zolfaghari R. Cytochrome P450s in the regulation of cellular retinoic acid metabolism. Annu Rev Nutr. 2011; 31: 65-87.
Saguy S, Dana D. Integrated approach to deep fat frying: engineering, nutrition, health and consumer aspects. J Food Eng. 2003; 56(2-3): 143–152.
Scott HM, Hutchison GR, Mahood IK, et al. Role of androgens in fetal testis development and dysgenesis. Endocrinology. 2007; 148(5): 2027-2036.
Shoeb M, Ansari NH, Srivastava SK, Ramana KV. 4-hydroxynonenal in the pathogenesis and progression of human diseases. Curr Med Chem. 2014; 21(2): 230–237.
Stevens JF, Maier CS. Acrolein: Sources, metabolism, and biomolecular interactions relevant to human health and disease. Mol Nutr Food Res. 2008; 52(1):7-25.
Sulzle A, Hirche F, Eder K. Thermally oxidized dietary fat upregulates the expression of target genes of PPAR alpha in rat liver. J Nutr. 2004; 134(6): 1375-1383.
Tang YL, Huang CJ. Dietary oxidized frying oil decreased plasma and liver vitamin A in rats. Nutr Sci J. 1998; 23: 265–279
Tareke E, Rydberg P, Karlsson P, et al. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem. 2002; 50(7): 4998-5006.
Tay S, Dickmann L, Dixit V, Isoherranen N. A comparison of the roles of peroxisome proliferator-activated receptor and retinoic acid receptor on CYP26 regulation. Mol Pharmacol. 2010; 77(2): 218-227.
Tickle C, Alberts B, Wolpert L, Lee J. Local application of retinoic acid to the limb bond mimics the action of the polarizing region. Nature. 1982; 296(5857): 564-566.
Tolson AH, Wang H. Regulation of drug-metabolizing enzymes by xenobiotic receptors: PXR and CAR. Adv Drug Deliv Rev. 2010; 62(13): 1238–1249.
Totani N, Yawata M, Takada M, Moriya M. Acrylamide content of commercial frying oil. J Oleo Sci. 2007; 56(2): 103-106.
Ulven SM, Gundersen TE, Weedon MS, et al. Identification of endogenous retinoids, enzymes, binding proteins, and receptors during early postimplantation development in mouse: important role of retinal dehydrogenase type 2 in synthesis of all-trans-retinoic acid. Dev Biol. 2000; 220(2): 379-391.
Van Wauwe JP, Coene MC, Goossens J, et al. Effects of cytochrome P-450 inhibitors on the in vivo metabolism of all-trans-retinoic acid in rats. J Pharmacol Exp Ther. 1990; 252(1): 365-369.
Wenzl T, Simon R, Klieiner J, Anklam E. Analytical methods for polycyclic aromatic hydrocarbons (PAHs) in food and the environment needed for new food legislation in the European Union. Trends Anal Chem. 2006; 25(7): 716–725.
Wilson JG, Roth CB, Warkany J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat. 1953; 92(2): 189-217.
Wilson R, Fernie CE, Scrimgeour CM, et al. Dietary epoxy fatty acids are absorbed in healthy women. Eur J Clin Invest. 2002; 32(2): 79–83.
Wilson R, Lyall K, Smyth L, et al. Dietary hydroxy fatty acids are absorbed in humans: implications for the measurement of oxidative stress in vivo. Free Radic Biol Med. 2002; 32(2): 162–168.
You L, Casanova M, Archibeque-Engle S, et al. Impaired male sexual development in perinatal Sprague-Dawley and Long-Evans hooded rats exposed in utero and lactationally to p,p '-DDE. Toxicol Sci. 1998; 45(2): 162-173.