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Sex-dependent effects of developmental exposure to bisphenol A and ethinyl estradiol on metabolic parameters and voluntary physical activity

Published online by Cambridge University Press:  18 September 2015

S. A. Johnson
Affiliation:
Bond Life Sciences Center, University of Missouri, Columbia, MO, USA Department of Biomedical Sciences, University of Missouri, Columbia, MO, USA
M. S. Painter
Affiliation:
Bond Life Sciences Center, University of Missouri, Columbia, MO, USA Department of Biomedical Sciences, University of Missouri, Columbia, MO, USA
A. B. Javurek
Affiliation:
Bond Life Sciences Center, University of Missouri, Columbia, MO, USA Department of Biomedical Sciences, University of Missouri, Columbia, MO, USA
M. R. Ellersieck
Affiliation:
Agriculture Experimental Station-Statistics, University of Missouri, Columbia, MO, USA
C. E. Wiedmeyer
Affiliation:
Veterinary Medical Diagnostic Laboratory, Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, MO, USA
J. P. Thyfault
Affiliation:
Department of Nutrition and Exercise Physiology, Research Service-Harry S. Truman Memorial Veterans Medical Center, Medicine-Division of Gastroenterology and Hepatology, University of Missouri, Columbia, Missouri, MO, USA Department of Molecular and Integrative Physiology, Kansas University Medical Center, Kansas City, KS, USA
C. S. Rosenfeld*
Affiliation:
Bond Life Sciences Center, University of Missouri, Columbia, MO, USA Department of Biomedical Sciences, University of Missouri, Columbia, MO, USA Genetics Area Program, University of Missouri, Columbia, MO, USA Thompson Center for Autism and Neurobehavioral Disorders, University of Missouri, Columbia, MO, USA
*
*Address for correspondence: C. S. Rosenfeld, Biomedical Sciences and Bond Life Sciences Center, University of Missouri, 440F Bond Life Sciences Center, 1201 E. Rollins Rd., Columbia, MO 65211, USA. (Email rosenfeldc@missouri.edu)

Abstract

Endocrine disrupting chemicals (EDC) have received considerable attention as potential obesogens. Past studies examining obesogenic potential of one widespread EDC, bisphenol A (BPA), have generally focused on metabolic and adipose tissue effects. However, physical inactivity has been proposed to be a leading cause of obesity. A paucity of studies has considered whether EDC, including BPA, affects this behavior. To test whether early exposure to BPA and ethinyl estradiol (EE, estrogen present in birth control pills) results in metabolic and such behavioral disruptions, California mice developmentally exposed to BPA and EE were tested as adults for energy expenditure (indirect calorimetry), body composition (echoMRI) and physical activity (measured by beam breaks and voluntary wheel running). Serum glucose and metabolic hormones were measured. No differences in body weight or food consumption were detected. BPA-exposed females exhibited greater variation in weight than females in control and EE groups. During the dark and light cycles, BPA females exhibited a higher average respiratory quotient than control females, indicative of metabolizing carbohydrates rather than fats. Various assessments of voluntary physical activity in the home cage confirmed that during the dark cycle, BPA and EE-exposed females were significantly less active in this setting than control females. Similar effects were not observed in BPA or EE-exposed males. No significant differences were detected in serum glucose, insulin, adiponectin and leptin concentrations. Results suggest that females developmentally exposed to BPA exhibit decreased motivation to engage in voluntary physical activity and altered metabolism of carbohydrates v. fats, which could have important health implications.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. CDC Centers for Disease Control and Prevention, Division of Nutrition, Physical Activity, and Obesity; CDC 24/7: Saving Lives, Protecting People. Adult Obesity Facts. http://www.cdc.gov/obesity/data/adult.html.Google Scholar
2. Scully, T. Diabetes in numbers. Nature. 2012; 485, S2S3.Google Scholar
3. Roundtable on Obesity Solutions; Food and Nutrition Board; Institute of Medicine. In The Current State of Obesity Solutions in the United States: Workshop Summary, 2014. National Academies Press: Washington, DC.Google Scholar
4. Brownson, RC, Boehmer, TK, Luke, DA. Declining rates of physical activity in the United States: what are the contributors? Annu Rev Public Health. 2005; 26, 421443.CrossRefGoogle ScholarPubMed
5. Gray, CE, Larouche, R, Barnes, JD, et al. Are we driving our kids to unhealthy habits? Results of the active healthy kids Canada 2013 report card on physical activity for children and youth. Int J Environ Res Public Health. 2014; 11, 60096020.Google Scholar
6. Ziviani, J, Wadley, D, Ward, H, et al.. A place to play: socioeconomic and spatial factors in children’s physical activity. Aust Occup Ther J. 2008; 55, 211.Google Scholar
7. Baillie-Hamilton, PF. Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med. 2002; 8, 185192.Google Scholar
8. Diamanti-Kandarakis, E, Bourguignon, JP, Giudice, LC, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009; 30, 293342.Google Scholar
9. Galloway, T, Cipelli, R, Guralnick, J, et al. Daily bisphenol A excretion and associations with sex hormone concentrations: results from the InCHIANTI adult population study. Environ Health Perspect. 2010; 118, 16031608.Google Scholar
10. He, Y, Miao, M, Herrinton, LJ, et al. Bisphenol A levels in blood and urine in a Chinese population and the personal factors affecting the levels. Environ Res. 2009; 109, 629633.CrossRefGoogle Scholar
11. Biedermann, S, Tschudin, P, Grob, K. Transfer of bisphenol A from thermal printer paper to the skin. Anal Bioanal Chem. 2010; 398, 571576.CrossRefGoogle ScholarPubMed
12. Grand View Research. Global bisphenol A (BPA) market by appliation (appliances, automotive, consumer, construction, electrical & electronics) expected to reach USD 20.03 billion by 2020. Retrieved 24 July 2014 from http://www.digitaljournal.com/pr/2009287.Google Scholar
13. Environment Canada. Screening assessment for the challenge phenol, 4,4’ -(1-methylethylidene)bis-(bisphenol A) Chemical Abstracts Service Registry Number 80-05-7. (ed. Ministers of the Environment and of Health), 2008; pp. 1–107.Google Scholar
14. Vandenberg, LN, Maffini, MV, Sonnenschein, C, Rubin, BS, Soto, AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev. 2009; 30, 7595.Google Scholar
15. Calafat, AM, Ye, X, Wong, LY, Reidy, JA, Needham, LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008; 116, 3944.Google Scholar
16. vom Saal, FS, Akingbemi, BT, Belcher, SM, et al. Chapel Hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol. 2007; 24, 131138.CrossRefGoogle Scholar
17. Vandenberg, LN, Hauser, R, Marcus, M, Olea, N, Welshons, WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24, 139177.CrossRefGoogle ScholarPubMed
19. Balakrishnan, B, Henare, K, Thorstensen, EB, Ponnampalam, AP, Mitchell, MD. Transfer of bisphenol A across the human placenta. Am J Obstet Gynecol. 2010; 202, 393, e391e397.Google Scholar
20. 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, 28392841.Google Scholar
21. Kawamoto, Y, Matsuyama, W, Wada, M, et al. Development of a physiologically based pharmacokinetic model for bisphenol A in pregnant mice. Toxicol Appl Pharmacol. 2007; 224, 182191.Google Scholar
22. Nishikawa, M, Iwano, H, Yanagisawa, R, et al. Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ Health Perspect. 2010; 118, 11961203.CrossRefGoogle ScholarPubMed
23. Vandenberg, LN, Chahoud, I, Heindel, JJ, et al.. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect. 2010; 118, 10551070.CrossRefGoogle ScholarPubMed
24. Bhandari, R, Xiao, J, Shankar, A. Urinary bisphenol A and obesity in U.S. children. Am J Epidemiol. 2013; 177, 12631270.Google Scholar
25. Braun, JM, Lanphear, BP, Calafat, AM, et al. Early-life bisphenol A exposure and child body mass index: a prospective cohort study. Environ Health Perspect. 2014; 122, 12391245.Google Scholar
26. Carwile, JL, Michels, KB. Urinary bisphenol A and obesity: NHANES 2003-2006. Environ Res. 2011; 111, 825830.CrossRefGoogle ScholarPubMed
27. Fenichel, P, Chevalier, N, Brucker-Davis, F. Bisphenol A: an endocrine and metabolic disruptor. Ann Endocrinol (Paris). 2013; 74, 211220.Google Scholar
28. Khalil, N, Ebert, JR, Wang, L, et al. Bisphenol A and cardiometabolic risk factors in obese children. Sci Total Environ. 2014; 470–471, 726732.Google Scholar
29. Ko, A, Hwang, MS, Park, JH, et al.. Association between urinary bisphenol A and waist circumference in Korean adults. Toxicol Res. 2014; 30, 3944.Google Scholar
30. Li, DK, Miao, M, Zhou, Z, et al. Urine bisphenol-A level in relation to obesity and overweight in school-age children. PLoS One. 2013; 8, e65399.Google Scholar
31. Mackay, H, Patterson, ZR, Khazall, R, et al.. Organizational effects of perinatal exposure to bisphenol-A and diethylstilbestrol on arcuate nucleus circuitry controlling food intake and energy expenditure in male and female CD-1 mice. Endocrinology. 2013; 154, 14651475.CrossRefGoogle ScholarPubMed
32. Manikkam, M, Tracey, R, Guerrero-Bosagna, C, Skinner, MK. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One. 2013; 8, e55387.CrossRefGoogle ScholarPubMed
33. Marmugi, A, Lasserre, F, Beuzelin, D, et al. Adverse effects of long-term exposure to bisphenol A during adulthood leading to hyperglycaemia and hypercholesterolemia in mice. Toxicology. 2014; 325c, 133143.Google Scholar
34. Schneyer, A. Getting big on BPA: role for BPA in obesity? Endocrinology. 2011; 152, 33013303.CrossRefGoogle ScholarPubMed
35. Schug, TT, Janesick, A, Blumberg, B, Heindel, JJ. Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol. 2011; 127, 204215.Google Scholar
36. Shankar, A, Teppala, S, Sabanayagam, C. Urinary bisphenol a levels and measures of obesity: results from the national health and nutrition examination survey 2003-2008. ISRN Endocrinol. 2012; 2012, 965243.Google Scholar
37. Somm, E, Schwitzgebel, VM, Toulotte, A, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect. 2009; 117, 15491555.Google Scholar
38. Trasande, L, Attina, TM, Blustein, J. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA. 2012; 308, 11131121.CrossRefGoogle ScholarPubMed
39. Valvi, D, Casas, M, Mendez, MA, et al. Prenatal bisphenol a urine concentrations and early rapid growth and overweight risk in the offspring. Epidemiology. 2013; 24, 791799.Google Scholar
40. van Esterik, JC, Dolle, ME, Lamoree, MH, et al. Programming of metabolic effects in C57BL/6JxFVB mice by exposure to bisphenol A during gestation and lactation. Toxicology. 2014; 321, 4052.CrossRefGoogle ScholarPubMed
41. Wang, T, Li, M, Chen, B, et al. Urinary bisphenol A (BPA) concentration associates with obesity and insulin resistance. J Clin Endocrinol Metab. 2012; 97, E223E227.Google Scholar
42. Wei, J, Lin, Y, Li, Y, et al. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology. 2011; 152, 30493061.Google Scholar
43. Heindel, JJ, Schug, TT. The obesogen hypothesis: current status and implications for human health. Curr Enviro Health Rpt. 2014; 1, 333340.CrossRefGoogle Scholar
44. Garcia-Arevalo, M, Alonso-Magdalena, P, Rebelo Dos Santos, J, et al. Exposure to bisphenol-A during pregnancy partially mimics the effects of a high-fat diet altering glucose homeostasis and gene expression in adult male mice. PLoS One. 2014; 9, e100214.Google Scholar
45. Alonso-Magdalena, P, Garcia-Arevalo, M, Quesada, I, Nadal, A. Bisphenol-A treatment during pregnancy in mice: a new window of susceptibility for the development of diabetes in mothers later in life. Endocrinology. 2015; 156, 16591670.CrossRefGoogle ScholarPubMed
46. Miyawaki, J, Sakayama, K, Kato, H, Yamamoto, H, Masuno, H. Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb. 2007; 14, 245252.Google Scholar
47. Anderson, OS, Peterson, KE, Sanchez, BN, et al. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J. 2013; 27, 17841792.Google Scholar
48. Harley, KG, Aguilar Schall, R, Chevrier, J, et al. Prenatal and postnatal bisphenol A exposure and body mass index in childhood in the CHAMACOS cohort. Environ Health Perspect. 2013; 121, 514520.Google Scholar
49. Ryan, KK, Haller, AM, Sorrell, JE, et al.. Perinatal exposure to bisphenol-A and the development of metabolic syndrome in CD-1 mice. Endocrinology. 2010; 151, 26032612.Google Scholar
50. Wang, J, Sun, B, Hou, M, Pan, X, Li, X. The environmental obesogen bisphenol A promotes adipogenesis by increasing the amount of 11beta-hydroxysteroid dehydrogenase type 1 in the adipose tissue of children. Int J Obes (Lond). 2013; 37, 9991005.CrossRefGoogle ScholarPubMed
51. Ohlstein, J, Strong, AL, McLachlan, JA, et al.. Bisphenol A enhances adipogenic differentiation of human adipose stromal/stem cells. J Mol Endocrinol. 2014; 53, 345353.Google Scholar
52. Boucher, JG, Husain, M, Rowan-Carroll, A, et al.. Identification of mechanisms of action of bisphenol A-induced human preadipocyte differentiation by transcriptional profiling. Obesity (Silver Spring). 2014; 22, 23332343.CrossRefGoogle ScholarPubMed
53. Boucher, JG, Boudreau, A, Atlas, E. Bisphenol A induces differentiation of human preadipocytes in the absence of glucocorticoid and is inhibited by an estrogen-receptor antagonist. Nutr Diabetes. 2014; 4, e102.Google Scholar
54. Bastos Sales, L, Kamstra, JH, Cenijn, PH, et al.. Effects of endocrine disrupting chemicals on in vitro global DNA methylation and adipocyte differentiation. Toxicol In Vitro. 2013; 27, 16341643.Google Scholar
55. Hugo, ER, Brandebourg, TD, Woo, JG, et al.. Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect. 2008; 116, 16421647.Google Scholar
56. Ronn, M, Lind, L, Orberg, J, et al. Bisphenol A is related to circulating levels of adiponectin, leptin and ghrelin, but not to fat mass or fat distribution in humans. Chemosphere. 2014; 112, 4248.Google Scholar
57. Perez-Leighton, CE, Boland, K, Teske, JA, Billington, C, Kotz, CM. Behavioral responses to orexin, orexin receptor gene expression, and spontaneous physical activity contribute to individual sensitivity to obesity. Am J Physiol Endocrinol Metab. 2012; 303, E865E874.Google Scholar
58. Perez-Leighton, CE, Grace, M, Billington, CJ, Kotz, CM. Role of spontaneous physical activity in prediction of susceptibility to activity based anorexia in male and female rats. Physiol Behav. 2014; 135, 104111.Google Scholar
59. Perez-Leighton, CE, Boland, K, Billington, CJ, Kotz, CM. High and low activity rats: elevated intrinsic physical activity drives resistance to diet-induced obesity in non-bred rats. Obesity (Silver Spring). 2013; 21, 353360.Google Scholar
60. Bauer, UE, Briss, PA, Goodman, RA, Bowman, BA. Prevention of chronic disease in the 21st century: elimination of the leading preventable causes of premature death and disability in the USA. Lancet. 2014; 384, 4552.CrossRefGoogle ScholarPubMed
61. Garcia, LM, da Silva, KS, Del Duca, GF, da Costa, FF, Nahas, MV. Sedentary behaviors, leisure-time physical inactivity, and chronic diseases in Brazilian workers: a cross sectional study. J Phys Act Health. 2014; 11, 16221634.CrossRefGoogle ScholarPubMed
62. Goedecke, JH, Micklesfield, LK. The effect of exercise on obesity, body fat distribution and risk for type 2 diabetes. Med Sport Sci. 2014; 60, 8293.CrossRefGoogle ScholarPubMed
63. Ward, PW. Inactivity, not gluttony, causes obesity. BMJ. 2014; 348, g2717.CrossRefGoogle Scholar
64. Booth, FW, Roberts, CK, Laye, MJ. Lack of exercise is a major cause of chronic diseases. Compr Physiol. 2012; 2, 11431211.Google Scholar
65. Knight, JA. Physical inactivity: associated diseases and disorders. Ann Clin Lab Sci. 2012; 42, 320337.Google Scholar
66. Schottenfeld, D, Beebe-Dimmer, JL, Buffler, PA, Omenn, GS. Current perspective on the global and United States cancer burden attributable to lifestyle and environmental risk factors. Annu Rev Public Health. 2013; 34, 97117.Google Scholar
67. Booth, FW, Laye, MJ, Lees, SJ, Rector, RS, Thyfault, JP. Reduced physical activity and risk of chronic disease: the biology behind the consequences. Eur J Appl Physiol. 2008; 102, 381390.Google Scholar
68. Bauman, AE, Reis, RS, Sallis, JF, et al. Correlates of physical activity: why are some people physically active and others not? Lancet. 2012; 380, 258271.Google Scholar
69. Kelly, SA, Nehrenberg, DL, Hua, K, et al. Parent-of-origin effects on voluntary exercise levels and body composition in mice. Physiol Genomics. 2010; 40, 111120.Google Scholar
70. Kelly, SA, Pomp, D. Genetic determinants of voluntary exercise. Trends Genet. 2013; 29, 348357.Google Scholar
71. Roberts, MD, Brown, JD, Company, JM, et al. Phenotypic and molecular differences between rats selectively bred to voluntarily run high vs. low nightly distances. Am J Physiol Regul Integr Comp Physiol. 2013; 304, R1024R1035.CrossRefGoogle ScholarPubMed
72. Williams, SA, Jasarevic, E, Vandas, GM, et al. Effects of developmental bisphenol A exposure on reproductive-related behaviors in California mice (Peromyscus californicus): a monogamous animal model. PLoS One. 2013; 8, e55698.Google Scholar
73. Jasarevic, E, Sieli, PT, Twellman, EE, et al. Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc Natl Acad Sci USA. 2011; 108, 1171511720.Google Scholar
74. Jasarevic, E, Williams, SA, Vandas, GM, et al. Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring. Horm Behav. 2013; 63, 180189.Google Scholar
75. Krugner-Higby, L, Shadoan, M, Carlson, C, et al. Type 2 diabetes mellitus, hyperlipidemia, and extremity lesions in California mice (Peromyscus californicus) fed commercial mouse diets. Comp Med. 2000; 50, 412418.Google ScholarPubMed
76. Sieli, PT, Jasarevic, E, Warzak, DA, et al. Comparison of serum bisphenol A concentrations in mice exposed to bisphenol A through the diet versus oral bolus exposure. Environ Health Perspect. 2011; 119, 12601265.CrossRefGoogle ScholarPubMed
77. vom Saal, FS, Richter, CA, Ruhlen, RR, et al.. The importance of appropriate controls, animal feed, and animal models in interpreting results from low-dose studies of bisphenol A. Birth Defects Res A Clin Mol Teratol. 2005; 73, 140145.Google Scholar
79. Hong, J, Stubbins, RE, Smith, RR, Harvey, AE, Núñez, NP. Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr J. 2009; 8, 1111.Google Scholar
80. Peromyscus genetic stock center, department of animal resources, University of South Carolina. http://stkctr.biol.sc.edu/wild-stock/p_calif.html.Google Scholar
81. Campi, KL, Jameson, CE, Trainor, BC. Sexual dimorphism in the brain of the monogamous California mouse (Peromyscus californicus). Brain Behav Evol. 2013; 81, 236249.CrossRefGoogle ScholarPubMed
82. Greenberg, GD, Laman-Maharg, A, Campi, KL, et al. Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the Stria terminalis. Front Behav Neurosci. 2014; 7, 223.Google Scholar
83. Steppan, S, Adkins, R, Anderson, J. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol. 2004; 53, 533553.Google Scholar
84. Jasarevic, E, Bailey, DH, Crossland, JP, et al. Evolution of monogamy, paternal investment, and female life history in Peromyscus . J Comp Psychol. 2013; 127, 91102.Google Scholar
85. Rosenfeld, CS, Johnson, SA, Ellersieck, MR, Roberts, RM. Interactions between parents and parents and pups in the monogamous California mouse (Peromyscus californicus). PloS One. 2013; 8, e75725.Google Scholar
86. Gubernick, DJ, Alberts, JR. The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol. 1987; 101, 169177.Google Scholar
87. Alonso-Magdalena, P, Ropero, AB, Soriano, S, et al. Bisphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol Cell Endocrinol. 2012; 355, 201207.Google Scholar
88. De Coster, S, van Larebeke, N. Endocrine-disrupting chemicals: associated disorders and mechanisms of action. J Environ Pub Health. 2012; 2012, 713696.Google Scholar
89. Rubin, BS. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011; 127, 2734.Google Scholar
90. Galgani, JE, Moro, C, Ravussin, E. Metabolic flexibility and insulin resistance. Am J Physiol. 2008; 295, E1009E1017.Google Scholar
91. Thyfault, JP, Rector, RS, Noland, RC. Metabolic inflexibility in skeletal muscle: a prelude to the cardiometabolic syndrome? Journal of the CardioMetabolic Syndrome. 2006; 1, 184189.Google Scholar
92. Rosenfeld, CS, Trainor, BC. Environmental health factors and sexually dimorphic differences in behavioral disruptions. Curr Environ Health Rep. 2014; 1, 287301.Google Scholar
93. Rhodes, JS, Garland, T Jr, Gammie, SC. Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behav Neurosci. 2003; 117, 12431256.Google Scholar
94. Waters, RP, Pringle, RB, Forster, GL, et al. Selection for increased voluntary wheel-running affects behavior and brain monoamines in mice. Brain Res. 2013; 1508, 922.Google Scholar
95. Hill, LE, Droste, SK, Nutt, DJ, Linthorst, AC, Reul, JM. Voluntary exercise alters GABA(A) receptor subunit and glutamic acid decarboxylase-67 gene expression in the rat forebrain. J Psychopharmacol. 2010; 24, 745756.Google Scholar
96. Meeusen, R. Exercise and the brain: insight in new therapeutic modalities. Ann Transplant. 2005; 10, 4951.Google ScholarPubMed
97. Tarr, BA, Kellaway, LA St, Clair Gibson, A, Russell, VA. Voluntary running distance is negatively correlated with striatal dopamine release in untrained rats. Behav Brain Res. 2004; 154, 493499.Google Scholar
98. Kolb, EM, Rezende, EL, Holness, L, et al. Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model of brain evolution. J Exp Biol. 2013; 216(Pt 3), 515523.Google Scholar
99. Teske, JA, Perez-Leighton, CE, Billington, CJ, Kotz, CM. Role of the locus coeruleus in enhanced orexin A-induced spontaneous physical activity in obesity-resistant rats. Am J Physiol Regul Integr Comp Physiol. 2013; 305, R1337R1345.Google Scholar
100. Chen, F, Zhou, L, Bai, Y, Zhou, R, Chen, L. Sex differences in the adult HPA axis and affective behaviors are altered by perinatal exposure to a low dose of bisphenol A. Brain Res. 2014; 1571, 1224.Google Scholar
101. Elsworth, JD, Jentsch, JD, Vandevoort, CA, et al. Prenatal exposure to bisphenol A impacts midbrain dopamine neurons and hippocampal spine synapses in non-human primates. Neurotoxicology. 2013; 35, 113120.Google Scholar
102. Kunz, N, Camm, EJ, Somm, E, et al. Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation. Int J Dev Neurosci. 2011; 29, 3743.Google Scholar
103. Leranth, C, Hajszan, T, Szigeti-Buck, K, Bober, J, MacLusky, NJ. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci USA. 2008; 105, 1418714191.Google Scholar
104. Tiwari, SK, Agarwal, S, Chauhan, LK, Mishra, VN, Chaturvedi, RK. Bisphenol-A impairs myelination potential during development in the hippocampus of the rat brain. Mol Neurobiol. 2014; 51, 13951416.Google Scholar
105. Xu, XB, He, Y, Song, C, et al. Bisphenol a regulates the estrogen receptor alpha signaling in developing hippocampus of male rats through estrogen receptor. Hippocampus. 2014; 24, 15701580.Google Scholar
106. Zhang, Q, Xu, X, Li, T, et al.. Exposure to bisphenol-A affects fear memory and histone acetylation of the hippocampus in adult mice. Horm Behav. 2014; 65, 106113.Google Scholar
107. Cao, J, Joyner, L, Mickens, JA, Leyrer, SM, Patisaul, HB. Sex-specific Esr2 mRNA expression in the rat hypothalamus and amygdala is altered by neonatal bisphenol A exposure. Reproduction. 2014; 147, 537554.Google Scholar
108. Cao, J, Rebuli, ME, Rogers, J, et al. Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala. Toxicol Sci. 2013; 133, 157173.Google Scholar
109. Kundakovic, M, Gudsnuk, K, Franks, B, et al. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci USA. 2013; 110, 99569961.Google Scholar
110. McCaffrey, KA, Jones, B, Mabrey, N, et al.. Sex specific impact of perinatal bisphenol A (BPA) exposure over a range of orally administered doses on rat hypothalamic sexual differentiation. Neurotoxicology. 2013; 36, 5562.Google Scholar
111. Panagiotidou, E, Zerva, S, Mitsiou, DJ, Alexis, MN, Kitraki, E. Perinatal exposure to low-dose bisphenol A affects the neuroendocrine stress response in rats. J Endocrinol. 2014; 220, 207218.Google Scholar
112. Tiwari, SK, Agarwal, S, Chauhan, LK, Mishra, VN, Chaturvedi, RK. Bisphenol-A impairs myelination potential during development in the hippocampus of the rat brain. Mol Neurobiol. 2014; 51, 13951416.Google Scholar
113. Viberg, H, Lee, I. A single exposure to bisphenol A alters the levels of important neuroproteins in adult male and female mice. Neurotoxicology. 2012; 33, 13901395.Google Scholar
114. Xu, XB, He, Y, Song, C, et al. Bisphenol A regulates the estrogen receptor alpha signaling in developing hippocampus of male rats through estrogen receptor. Hippocampus. 2014; 24, 15701580.Google Scholar
115. Leranth, C, Szigeti-Buck, K, Maclusky, NJ, Hajszan, T. Bisphenol A prevents the synaptogenic response to testosterone in the brain of adult male rats. Endocrinology. 2008; 149, 988994.Google Scholar
116. Narita, M, Miyagawa, K, Mizuo, K, Yoshida, T, Suzuki, T. Changes in central dopaminergic systems and morphine reward by prenatal and neonatal exposure to bisphenol-A in mice: evidence for the importance of exposure period. Addict Biol. 2007; 12, 167172.Google Scholar
117. Nakamura, K, Itoh, K, Yoshimoto, K, Sugimoto, T, Fushiki, S. Prenatal and lactational exposure to low-doses of bisphenol A alters brain monoamine concentration in adult mice. Neurosci Lett. 2010; 484, 6670.Google Scholar
118. Tian, YH, Baek, JH, Lee, SY, Jang, CG. Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice. Synapse. 2010; 64, 432439.CrossRefGoogle ScholarPubMed
119. Yaoi, T, Itoh, K, Nakamura, K, et al. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem Biophys Res Commun. 2008; 376, 563567.Google Scholar
120. Werme, M, Messer, C, Olson, L, et al. Delta FosB regulates wheel running. J Neurosci. 2002; 22, 81338138.Google Scholar
121. Alyea, RA, Watson, CS. Differential regulation of dopamine transporter function and location by low concentrations of environmental estrogens and 17beta-estradiol. Environ Health Perspect. 2009; 117, 778783.Google Scholar
122. Jones, DC, Miller, GW. The effects of environmental neurotoxicants on the dopaminergic system: a possible role in drug addiction. Biochem Pharmacol. 2008; 76, 569581.Google Scholar
123. Matsuda, S, Saika, S, Amano, K, Shimizu, E, Sajiki, J. Changes in brain monoamine levels in neonatal rats exposed to bisphenol A at low doses. Chemosphere. 2010; 78, 894906.Google Scholar
124. Nakamura, K, Itoh, K, Yoshimoto, K, Sugimoto, T, Fushiki, S. Prenatal and lactational exposure to low-doses of bisphenol A alters brain monoamine concentration in adult mice. Neurosci Lett. 2010; 484, 6670.Google Scholar
125. Tanida, T, Warita, K, Ishihara, K, et al. Fetal and neonatal exposure to three typical environmental chemicals with different mechanisms of action: mixed exposure to phenol, phthalate, and dioxin cancels the effects of sole exposure on mouse midbrain dopaminergic nuclei. Toxicol Lett. 2009; 189, 4047.Google Scholar
126. Zhou, R, Zhang, Z, Zhu, Y, Chen, L, Sokabe, M. Deficits in development of synaptic plasticity in rat dorsal striatum following prenatal and neonatal exposure to low-dose bisphenol A. Neuroscience. 2009; 159, 161171.Google Scholar
127. Garland, T Jr, Schutz, H, Chappell, MA, et al. The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol. 2011; 214(Pt 2), 206229.Google Scholar
128. Chen, ZY, Jing, D, Bath, KG, et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science. 2006; 314, 140143.Google Scholar
129. Berchtold, NC, Kesslak, JP, Pike, CJ, Adlard, PA, Cotman, CW. Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus. Eur J Neurosci. 2001; 14, 19922002.Google Scholar
130. Teske, JA, Billington, CJ, Kotz, CM. Mechanisms underlying obesity resistance associated with high spontaneous physical activity. Neuroscience. 2014; 256, 91100.Google Scholar
131. Kotz, C, Nixon, J, Butterick, T, et al.. Brain orexin promotes obesity resistance. Ann N Y Acad Sci. 2012; 1264, 7286.Google Scholar
132. Perez-Leighton, CE, Billington, CJ, Kotz, CM. Orexin modulation of adipose tissue. Biochim Biophys Acta. 2014; 1842, 440445.Google Scholar
133. Nojima, K, Takata, T, Masuno, H. Prolonged exposure to a low-dose of bisphenol A increases spontaneous motor activity in adult male rats. J Physiol Sci. 2013; 63, 311315.Google Scholar
134. Ishido, M, Yonemoto, J, Morita, M. Mesencephalic neurodegeneration in the orally administered bisphenol A-caused hyperactive rats. Toxicol Lett. 2007; 173, 6672.CrossRefGoogle ScholarPubMed
135. Farabollini, F, Porrini, S, Dessi-Fulgheri, F. Perinatal exposure to the estrogenic pollutant bisphenol A affects behavior in male and female rats. Pharmacol Biochem Behav. 1999; 64, 687694.Google Scholar
136. Baker, MS, Li, G, Kohorst, JJ, Waterland, RA. Fetal growth restriction promotes physical inactivity and obesity in female mice. Int J Obes (Lond). 2013; 39, 98104.Google Scholar
137. Bodin, J, Bolling, AK, Samuelsen, M, et al. Long-term bisphenol A exposure accelerates insulitis development in diabetes-prone NOD mice. Immunopharmacol Immunotoxicol. 2013; 35, 349358.Google Scholar
138. Moon, MK, Jeong, IK, Jung Oh, T, et al. Long-term oral exposure to bisphenol A induces glucose intolerance and insulin resistance. J Endocrinol. 2015; 226, 3542.Google Scholar
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