Impact of gestational bisphenol A on oxidative stress and free fatty acids: Human association and interspecies animal testing studies

Endocrinology (United States)

Volumn 156, Issue 3, 2015, Pages 911-922

  Veiga Lopez, Almudena ^a,e   Pennathur, Subramaniam ^b   Kannan, Kurunthachalam ^c   Patisaul, Heather B ^d   Dolinoy, Dana C ^a   Zeng, Lixia ^b   Padmanabhan, Vasantha ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c WADSWORTH CENTER   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; 4,4' ISOPROPYLIDENEDIPHENOL; ADRENIC ACID; ARACHIDIC ACID; BEHENIC ACID; BIOLOGICAL MARKER; DOCOSAHEXAENOIC ACID; EICOSADIENOIC ACID; EICOSENOIC ACID; ERUCIC ACID; FATTY ACID; GAMMA LINOLENIC ACID; ICOSAPENTAENOIC ACID; ICOSATETRAENOIC ACID; ICOSATRIENOIC ACID; LINOLEIC ACID; LINOLENIC ACID; MYRISTIC ACID; OLEIC ACID; PALMITIC ACID; PALMITOLEIC ACID; STEARIC ACID; UNCLASSIFIED DRUG; VACCENIC ACID; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE; POLLUTANT;

ADIPOSE TISSUE; ADULT; ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; FEMALE; FEMALE ANIMAL; FETUS; FIRST TRIMESTER PREGNANCY; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; MALE; MATERNAL BLOOD; MOTHER; MOUSE; MYRISTOLEIC ACID; NEWBORN; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; RISK FACTOR; SHEEP; SPECIES COMPARISON; UMBILICAL CORD BLOOD; ANIMAL; BLOOD; CHEMISTRY; DRUG EFFECTS; FETUS BLOOD; HYPOPITUITARISM; MATERNAL EXPOSURE; METABOLISM; POLLUTANT; PREGNANCY; SPECIES DIFFERENCE;

ADULT; ANIMALS; BENZHYDRYL COMPOUNDS; BIOMARKERS; ENVIRONMENTAL POLLUTANTS; FATTY ACIDS, NONESTERIFIED; FEMALE; FETAL BLOOD; FETUS; HUMANS; HYPOPITUITARISM; MATERNAL EXPOSURE; MICE; OXIDATIVE STRESS; PHENOLS; PREGNANCY; RATS; SPECIES SPECIFICITY;

EID: 84923917036     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1863     Document Type: Article

References (82)

1. WHO Report World Health Organization (WHO)/United Nations Environment Programme (UNEP). State of the science of endocrine disrupting chemicals-2012. Bergman A, Heindel JJ, Jobling S, Kidd KA, Zoeller RT, eds. 2014 Available at http://www.who.int/ceh/publications/endocrine/en/. Accessed December 18, 2014.
2. Vandenberg LN, Hunt PA, Myers JP, Vom Saal FS. Human exposures to bisphenol A: mismatches between data and assumptions. Rev Environ Health. 2013;28(1):37-58.
3. Ikezuki Y, Tsutsumi O, Takai Y, Kamei Y, Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod. 2002;17(11):2839-2841.
4. Ranjit N, Siefert K, Padmanabhan V. Bisphenol-A and disparities in birth outcomes: a review and directions for future research. J Perinatol. 2010;30(1):2-9.
5. Zhang T, Sun H, Kannan K. Blood and urinary bisphenol A concentrations in children, adults, and pregnant women from china: partitioning between blood and urine and maternal and fetal cord blood. Environ Sci Technol. 2013;47(9):4686-4694.
6. Schug TT, Janesick A, Blumberg B, Heindel JJ. Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol. 2011;127(3-5):204-215.
7. Fenichel P, Chevalier N, Brucker-Davis F. Bisphenol A: an endocrine and metabolic disruptor. Ann Endocrinol (Paris). 2013;74(3):211-220.
8. Peretz J, Vrooman L, Ricke WA, et al. Bisphenol A and reproductive health: update of experimental and human evidence, 2007-2013. Environ Health Perspect. 2014;122(8):775-786.
9. Lang IA, Galloway TS, Scarlett A, et al. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA. 2008;300(11):1303-1310.
10. Silver MK, O'Neill MS, Sowers MR, Park SK. Urinary bisphenol A and type-2 diabetes in U.S. adults: data fromNHANES2003-2008. PLoS One. 2011;6(10):e26868.
11. Teppala S, Madhavan S, Shankar A. Bisphenol A and metabolic syndrome: results from NHANES. Int J Endocrinol. 2012;2012:598180.
12. Alonso-Magdalena P, Vieira E, Soriano S, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010;118(9):1243-1250.
13. Jiang Y, Liu J, Li Y, et al. Prenatal exposure to bisphenol A at the reference dose impairs mitochondria in the heart of neonatal rats. J Appl Toxicol. 2014;34(9):1012-1022.
14. Ryan KK, HallerAM,Sorrell JE, Woods SC, Jandacek RJ, Seeley RJ. Perinatal exposure to bisphenol-a and the development of metabolic syndrome in CD-1 mice. Endocrinology. 2010;151(6):2603-2612.
15. Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316(2):129-139.
16. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440(7086):944-948.
17. Silins I, Högberg J. Combined toxic exposures and human health: biomarkers of exposure and effect. Int J Environ Res Public Health. 2011;8(3):629-647.
18. Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, Ben-Jonathan N. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect. 2008;116(12):1642-1647.
19. Yang YJ, Hong YC,Oh SY, et al. Bisphenol A exposure is associated with oxidative stress and inflammation in postmenopausal women. Environ Res. 2009;109(6):797-801.
20. Kim JH, Sartor MA, Rozek LS, et al. Perinatal bisphenolAexposure promotes dose-dependent alterations of the mouse methylome. BMC Genomics. 2014;15:30.
21. Veiga-Lopez A, Luense LJ, Christenson LK, Padmanabhan V. Developmental programming: gestational bisphenol-A treatment alters trajectory of fetal ovarian gene expression. Endocrinology. 2013;154(5):1873-1884.
22. Savabieasfahani M, Kannan K, Astapova O, Evans NP, Padmanabhan V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology. 2006;147(12):5956-5966.
23. Padmanabhan V, Siefert K, Ransom S, et al. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol. 2008;28(4):258-263.
24. Calafat AM, Weuve J, Ye X, et al. Exposure to bisphenolAand other phenols in neonatal intensive care unit premature infants. Environ Health Perspect. 2009;117(4):639-644.
25. Patisaul HB, Sullivan AW, Radford ME, et al. Anxiogenic effects of developmental bisphenol A exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy. PLoS One. 2012;7(9):e43890.
26. Patisaul HB, Roberts SC, Mabrey N, et al. Accumulation and endocrine disrupting effects of the flame retardant mixture Firemaster ® 550 in rats: an exploratory assessment. J Biochem Mol Toxicol. 2013;27(2):124-136.
27. Doerge DR, Twaddle NC, Vanlandingham M, Brown RP, Fisher JW. Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol. 2011;255(3):261-270.
28. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003;23(15):5293-5300.
29. Becker JB, Arnold AP, Berkley KJ, et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology. 2005;146(4):1650-1673.
30. Weinhouse C, Anderson OS, Bergin IL, et al. Dose-dependent incidence of hepatic tumors in adult mice following perinatal exposure to bisphenol A. Environ Health Perspect. 2014;122(5):485-491.
31. Takahashi O, Oishi S. Testicular toxicity of dietarily or parenterally administered bisphenol A in rats and mice. Food Chem Toxicol. 2003;41(7):1035-1044.
32. Sieli PT, Jašarevic E, Warzak DA, et al. Comparison of serum bisphenolAconcentrations in mice exposed to bisphenolAthrough the diet versus oral bolus exposure. Environ Health Perspect. 2011;119(9):1260-1265.
33. Anderson OS, Nahar MS, Faulk C, et al. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ Mol Mutagen. 2012;53(5):334-342.
34. Vandenberg LN, Gerona RR, Kannan K, et al. A round robin approach to the analysis of bisphenol a (BPA) in human blood samples. Environ Health. 2014;13(1):25.
35. Liao C, Kannan K. Determination of free and conjugated forms of bisphenol A in human urine and serum by liquid chromatography-tandem mass spectrometry. Environ Sci Technol. 2012;46(9):5003-5009.
36. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911-917.
37. Tserng KY, Kliegman RM, Miettinen EL, Kalhan SC. A rapid, simple, and sensitive procedure for the determination of free fatty acids in plasma using glass capillary column gas-liquid chromatography. J Lipid Res. 1981;22(5):852-858.
38. Vivekanandan-Giri A, Byun J, Pennathur S. Quantitative analysis of amino acid oxidation markers by tandem mass spectrometry. Methods Enzymol. 2011;491:73-89.
39. Vivekanadan-Giri A, Wang JH, Byun J, Pennathur S. Mass spectrometric quantification of amino acid oxidation products identifies oxidative mechanisms of diabetic end-organ damage. Rev Endocr Metab Disord. 2008;9(4):275-287.
40. Weber D, Stuetz W, Bernhard W, et al. Oxidative stress markers and micronutrients in maternal and cord blood in relation to neonatal outcome. Eur J Clin Nutr. 2014;68(2):215-222.
41. Badham HJ, Renaud SJ, Wan J, Winn LM. Benzene-initiated oxidative stress: effects on embryonic signaling pathways. Chem-Biol Interact. 2010;184(1-2):218-221.
42. Sulkowski ZL, Chen T, Midha S, Zavacki AM, Sajdel-Sulkowska EM. Maternal thimerosal exposure results in aberrant cerebellar oxidative stress, thyroid hormone metabolism, and motor behavior in rat pups; sex- and strain-dependent effects. Cerebellum. 2012;11(2):575-586.
43. Mitra S, Srivastava A, Khanna S, Khandelwal S. Consequences of tributyltin chloride induced stress in Leydig cells: an ex-vivo approach. Environ Toxicol Pharmacol. 2014;37(2):850-860.
44. Stewart T, Jung FF, Manning J, Vehaskari VM. Kidney immune cell infiltration and oxidative stress contribute to prenatally programmed hypertension. Kidney Int. 2005;68(5):2180-2188.
45. Cambonie G, Comte B, Yzydorczyk C, et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvasdoi: cular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007;292(3):R1236-R1245.
46. Banks BA, Ischiropoulos H, McClelland M,Ballard PL, Ballard RA. Plasma 3-nitrotyrosine is elevated in premature infants who develop bronchopulmonary dysplasia. Pediatrics. 1998;101(5):870-874.
47. Groenendaal F, Lammers H, Smit D, Nikkels PG. Nitrotyrosine in brain tissue of neonates after perinatal asphyxia. Arch Dis Child Fetal Neonatal Ed. 2006;91(6):F429-F433.
48. Escobar J, Teramo K, Stefanovic V, et al. Amniotic fluid oxidative and nitrosative stress biomarkers correlate with fetal chronic hypoxia in diabetic pregnancies. Neonatology. 2013;103(3):193-198.
49. Hulak M, Gazo I, Shaliutina A, Linhartova P. In vitro effects of bisphenol A on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Comp Biochem Physiol C Toxicol Pharmacol. 2013;158(2):64-71.
50. Xu H, Yang M, Qiu W, Pan C, Wu M. The impact of endocrinedisrupting chemicals on oxidative stress and innate immune response in zebrafish embryos. Environ Toxicol Chem. 2013;32(8):1793-1799.
51. Popa DS, Bolfa P, Kiss B, et al. Influence of Genista tinctoria L. or methylparaben on subchronic toxicity of bisphenol A in rats. Biomed Environ Sci. 2014;27(2):85-96.
52. Nunez AA, Kannan K, Giesy JP, Fang J, Clemens LG. Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. Chemosphere. 2001;42(8):917-922.
53. Nishimura Y, Nakai Y, Tanaka A, Nagao T, Fukushima N. Longterm exposure of 3T3 fibroblast cells to endocrine disruptors alters sensitivity to oxidative injury. Cell Biol Int. 2014;38(7):868-874.
54. Bartesaghi S, Ferrer-Sueta G, Peluffo G, et al. Protein tyrosine nitration in hydrophilic and hydrophobic environments. Amino Acids. 2007;32(4):501-515.
55. Pennathur S, Heinecke JW. Mechanisms of oxidative stress in diabetes: implications for the pathogenesis of vascular disease and antioxidant therapy. Front Biosci. 2004;9:565-574.
56. Pennathur S, Ido Y, Heller JI, et al. Reactive carbonyls and polyunsaturated fatty acids produce a hydroxyl radical-like species: a potential pathway for oxidative damage of retinal proteins in diabetes. J Biol Chem. 2005;280(24):22706-22714.
57. Smith CK, Vivekanandan-Giri A, Tang C, et al. Neutrophil extracellular trap-derived enzymes oxidize high-density lipoprotein: an additional proatherogenic mechanism in systemic lupus erythematosus. Arthritis Rheumatol. 2014;66(9):2532-2544.
58. Vivekanandan-Giri A, Slocum JL, Byun J, et al. High density lipoprotein is targeted for oxidation by myeloperoxidase in rheumatoid arthritis. Ann Rheum Dis. 2013;72(10):1725-1731.
59. Shu L, Vivekanandan-Giri A, Pennathur S, et al. Establishing 3-nitrotyrosine as a biomarker for the vasculopathy of Fabry disease. Kidney Int. 2014;86(1):58-66.
60. Souza JM, Daikhin E, Yudkoff M, Raman CS, Ischiropoulos H. Factors determining the selectivity of protein tyrosine nitration. Arch Biochem Biophys. 1999;371(2):169-178.
61. Kanski J, Behring A, Pelling J, Schoneich C. Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging. Am J Physiol-Heart C. 2005;288(1):H371-H381.
62. Kunitomo M, Yamaguchi Y, Kagota S, Otsubo K. Beneficial effect of coenzyme Q10 on increased oxidative and nitrative stress and inflammationandindividual metaboliccomponentsdeveloping in a ratmodel of metabolic syndrome. J Pharmacol Sci. 2008;107(2):128-137.
63. Kumar Y, Liang C, Limmon GV, et al. Molecular analysis of serum and bronchoalveolar lavage in a mouse model of influenza reveals markers of disease severity that can be clinically useful in humans. PLoS One. 2014;9(2):e86912.
64. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endo-crine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293-342.
65. Hotchkiss AK, Rider CV, Blystone CR, et al. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci. 2008;105(2):235-259.
66. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta. 2006;1757(5-6):509-517.
67. Moon MK, Kim MJ, Jung IK, et al. Bisphenol A impairs mitochondrial function in the liver at doses below the no observed adverse effect level. J Korean Med Sci. 2012;27(6):644-652.
68. Rueda-Clausen CF, Dolinsky VW, Morton JS, Proctor SD, Dyck JR, Davidge ST. Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes. 2011;60(2):507-516.
69. Roghair RD,Miller FJ Jr, Scholz TD,Lamb FS, Segar JL. Endothelial superoxide production is altered in sheep programmed by early gestation dexamethasone exposure. Neonatology. 2008;93(1):19-27.
70. Prescott SL, Dunstan JA. Prenatal fatty acid status and immune development: the pathways and the evidence. Lipids. 2007;42(9):801-810.
71. Lumia M, Luukkainen P, Tapanainen H, et al. Dietary fatty acid composition during pregnancy and the risk of asthma in the offspring. Pediatr Allergy Immunol. 2011;22(8):827-835.
72. Chen X, Scholl TO. Association of elevated free fatty acids during late pregnancy with preterm delivery. Obstet Gynecol. 2008;112(2 pt 1):297-303.
73. Lorentzen B, Drevon CA, Endresen MJ, Henriksen T. Fatty acid pattern of esterified and free fatty acids in sera of women with normal and pre-eclamptic pregnancy. Br J Obstet Gynaecol. 1995;102(7):530-537.
74. Wolever TM, Bentum-Williams A, Jenkins DJ. Physiological modulation of plasma free fatty acid concentrations by diet. Metabolic implications in nondiabetic subjects. Diabetes Care. 1995;18(7):962-970.
75. Mayneris-Perxachs J, Guerendiain M, Castellote AI, et al. Plasma fatty acid composition, estimated desaturase activities, and their relation with the metabolic syndrome in a population at high risk of cardiovascular disease. Clin Nutr. 2014;33(1):90-97.
76. Wang X, Lin H, Gu Y. Multiple roles of dihomo-γ-linolenic acid against proliferation diseases. Lipids Health Dis. 2012;11:25.
77. Anderson OS, Peterson KE, Sanchez BN, Zhang ZZ, Mancuso P, Dolinoy DC. Perinatal bisphenol A exposure promotes hyperactivity with corresponding hormonal responses. FASEB J. 2013;27.
78. Wan Y, Choi K, Kim S, et al. Hydroxylated polybrominated diphenyl ethers and bisphenol A in pregnant women and their matching fetuses: placental transfer and potential risks. Environ Sci Technol. 2010;44(13):5233-5239.
79. Unal ER, Lynn T, Neidich J, et al. Racial disparity in maternal and fetal-cord bisphenol A concentrations. J Perinatol. 2012;32(11):844-850.
80. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Persp. 2002;110(11):A703-A707.
81. Uchida K, Suzuki A, Kobayashi Y, et al. Bisphenol-A administration during pregnancy results in fetal exposure in mice and monkeys. J Health Sci. 2002;48(6):579-582.
82. Gerona RR, Woodruff TJ, Dickenson CA, et al. Bisphenol-A (BPA), BPA glucuronide, and BPA sulfate in midgestation umbilical cord serum in a northern and central California population. Environ Sci Technol. 2013;47(21):12477-12485.