Skip to main content Accessibility help
×
Home
Hostname: page-component-559fc8cf4f-s5ss2 Total loading time: 0.366 Render date: 2021-02-25T13:33:47.849Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

In vivo and in vitro bisphenol A exposure effects on adiposity

Published online by Cambridge University Press:  29 August 2018

M. Desai
Affiliation:
Perinatal Research Laboratory, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA Department of Obstetrics and Gynecology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA
M. G. Ferrini
Affiliation:
Department of Health and Life Sciences Department of Internal Medicine, Charles R. Drew University, Los Angeles, CA, USA
J. K. Jellyman
Affiliation:
Perinatal Research Laboratory, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
G. Han
Affiliation:
Perinatal Research Laboratory, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
M. G. Ross
Affiliation:
Perinatal Research Laboratory, Department of Obstetrics and Gynecology, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA Department of Obstetrics and Gynecology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA Department of Obstetrics and Gynaecology, Charles R. Drew University, Los Angeles, CA, USA
Corresponding
E-mail address:

Abstract

In utero exposure to the ubiquitous plasticizer, bisphenol A (BPA) is associated with offspring obesity. As adipogenesis is a critical factor contributing to obesity, we determined the effects of in vivo maternal BPA and in vitro BPA exposure on newborn adipose tissue at the stem-cell level. For in vivo studies, female rats received BPA before and during pregnancy and lactation via drinking water, and offspring were studied for measures of adiposity signals. For in vitro BPA exposure, primary pre-adipocyte cell cultures from healthy newborns were utilized. We studied pre-adipocyte proliferative and differentiation effects of BPA and explored putative signal factors which partly explain adipose responses and underlying epigenetic mechanisms mediated by BPA. Maternal BPA-induced offspring adiposity, hypertrophic adipocytes and increased adipose tissue protein expression of pro-adipogenic and lipogenic factors. Consistent with in vivo data, in vitro BPA exposure induced a dose-dependent increase in pre-adipocyte proliferation and increased adipocyte lipid content. In vivo and in vitro BPA exposure promotes the proliferation and differentiation of adipocytes, contributing to an enhanced capacity for lipid storage. These findings reinforce the marked effects of BPA on adipogenesis and highlight the susceptibility of stem-cell populations during early life with long-term consequence on metabolic homeostasis.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

Access options

Get access to the full version of this content by using one of the access options below.

References

1. Janesick, A, Blumberg, B. Obesogens, stem cells and the developmental programming of obesity. Int J Androl. 2012; 35, 437448.CrossRefGoogle ScholarPubMed
2. Richter, CA, Birnbaum, LS, Farabollini, F, et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol. 2007; 24, 199224.CrossRefGoogle ScholarPubMed
3. Rubin, BS, Soto, AM. Bisphenol A: perinatal exposure and body weight. Mol Cell Endocrinol. 2009; 304, 5562.CrossRefGoogle ScholarPubMed
4. 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.CrossRefGoogle ScholarPubMed
5. Angle, BM, Do, RP, Ponzi, D, et al. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod Toxicol. 2013; 42, 256268.CrossRefGoogle Scholar
6. Susiarjo, M, Xin, F, Bansal, A, et al. Bisphenol A exposure disrupts metabolic health across multiple generations in the mouse. Endocrinology. 2015; 156, 20492058.CrossRefGoogle ScholarPubMed
7. Alonso-Magdalena, P, Morimoto, S, Ripoll, C, Fuentes, E, Nadal, A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect. 2006; 114, 106112.CrossRefGoogle ScholarPubMed
8. 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, 12431250.CrossRefGoogle ScholarPubMed
9. vom Saal, FS, Nagel, SC, Coe, BL, Angle, BM, Taylor, JA. The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol Cell Endocrinol. 2012; 354, 7484.CrossRefGoogle ScholarPubMed
10. Hill, JO, Wyatt, HR, Peters, JC. Energy balance and obesity. Circulation. 2012; 126, 126132.CrossRefGoogle ScholarPubMed
11. Ailhaud, G, Grimaldi, P, Negrel, R. Cellular and molecular aspects of adipose tissue development. Annu Rev Nutr. 1992; 12, 207233.CrossRefGoogle ScholarPubMed
12. Hausman, DB, DiGirolamo, M, Bartness, TJ, Hausman, GJ, Martin, RJ. The biology of white adipocyte proliferation. Obes Rev. 2001; 2, 239254.CrossRefGoogle ScholarPubMed
13. Morrison, RF, Farmer, SR. Insights into the transcriptional control of adipocyte differentiation. J Cell Biochem. 1999; 32–33(Suppl.), 5967.3.0.CO;2-1>CrossRefGoogle Scholar
14. Rosen, ED, Walkey, CJ, Puigserver, P, Spiegelman, BM. Transcriptional regulation of adipogenesis. Genes Dev. 2000; 14, 12931307.Google ScholarPubMed
15. Darlington, GJ, Ross, SE, MacDougald, OA. The role of C/EBP genes in adipocyte differentiation. J Biol Chem. 1998; 273, 3005730060.CrossRefGoogle ScholarPubMed
16. Lane, MD, Lin, FT, MacDougald, OA, Vasseur-Cognet, M. Control of adipocyte differentiation by CCAAT/enhancer binding protein alpha (C/EBP alpha). Int J Obes Relat Metab Disord. 1996; 20(Suppl. 3), S91S96.Google Scholar
17. Rosen, ED, Spiegelman, BM. PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem. 2001; 276, 3773137734.CrossRefGoogle ScholarPubMed
18. 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.CrossRefGoogle ScholarPubMed
19. Chamorro-Garcia, R, Kirchner, S, Li, X, et al. Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor gamma-independent mechanism. Environ Health Perspect. 2012; 120, 984989.CrossRefGoogle ScholarPubMed
20. Masuno, H, Iwanami, J, Kidani, T, Sakayama, K, Honda, K. Bisphenol a accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. Toxicol Sci. 2005; 84, 319327.CrossRefGoogle ScholarPubMed
21. Yee, JK, Lee, WN, Ross, MG, et al. Peroxisome proliferator-activated receptor gamma modulation and lipogenic response in adipocytes of small-for-gestational age offspring. Nutr Metab (Lond). 2012; 9, 62.CrossRefGoogle ScholarPubMed
22. Carwile, JL, Luu, HT, Bassett, LS, et al. Polycarbonate bottle use and urinary bisphenol A concentrations. Environ Health Perspect. 2009; 117, 13681372.CrossRefGoogle ScholarPubMed
23. Muhamad, MS, Salim, MR, Lau, WJ, Yusop, Z. A review on bisphenol A occurrences, health effects and treatment process via membrane technology for drinking water. Environ Sci Pollut Res Int. 2016; 23, 1154911567.CrossRefGoogle ScholarPubMed
24. Makris, KC, Andra, SS, Jia, A, et al. Association between water consumption from polycarbonate containers and bisphenol A intake during harsh environmental conditions in summer. Environ Sci Technol. 2013; 47, 33333343.CrossRefGoogle Scholar
25. Le, HH, Carlson, EM, Chua, JP, Belcher, SM. Bisphenol A is released from polycarbonate drinking bottles and mimics the neurotoxic actions of estrogen in developing cerebellar neurons. Toxicol Lett. 2008; 176, 149156.CrossRefGoogle ScholarPubMed
26. Mendoza-Rodriguez, CA, Garcia-Guzman, M, Baranda-Avila, N, et al. Administration of bisphenol A to dams during perinatal period modifies molecular and morphological reproductive parameters of the offspring. Reprod Toxicol. 2011; 31, 177183.CrossRefGoogle ScholarPubMed
27. Kabuto, H, Amakawa, M, Shishibori, T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci. 2004; 74, 29312940.CrossRefGoogle ScholarPubMed
28. Nakajima, Y, Goldblum, RM, Midoro-Horiuti, T. Fetal exposure to bisphenol A as a risk factor for the development of childhood asthma: an animal model study. Environ Health. 2012; 11, 8.CrossRefGoogle Scholar
29. Schonfelder, G, Wittfoht, W, Hopp, H, et al. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect. 2002; 110, A703A707.CrossRefGoogle ScholarPubMed
30. Yoshida, M, Shimomoto, T, Katashima, S, et al. Maternal exposure to low doses of bisphenol a has no effects on development of female reproductive tract and uterine carcinogenesis in Donryu rats. J Reprod Dev. 2004; 50, 349360.CrossRefGoogle ScholarPubMed
31. 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, e43890.CrossRefGoogle ScholarPubMed
32. Weinstock, M. Prenatal stressors in rodents: effects on behavior. Neurobiol Stress. 2017; 6, 313.CrossRefGoogle ScholarPubMed
33. Mueller, BR, Bale, TL. Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity. Physiol Behav. 2006; 88, 605614.CrossRefGoogle ScholarPubMed
34. Hohwu, L, Li, J, Olsen, J, Sorensen, TI, Obel, C. Severe maternal stress exposure due to bereavement before, during and after pregnancy and risk of overweight and obesity in young adult men: a Danish National Cohort Study. PLoS One. 2014; 9, e97490.CrossRefGoogle ScholarPubMed
35. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983; 65, 5563.CrossRefGoogle ScholarPubMed
36. Desai, M, Guang, H, Ferelli, M, Kallichanda, N, Lane, RH. Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring. Reprod Sci. 2008; 15, 785796.CrossRefGoogle ScholarPubMed
37. Vandenberg, LN, Hauser, R, Marcus, M, Olea, N, Welshons, WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24, 139177.CrossRefGoogle Scholar
38. Kosarac, I, Kubwabo, C, Lalonde, K, Foster, W. A novel method for the quantitative determination of free and conjugated bisphenol A in human maternal and umbilical cord blood serum using a two-step solid phase extraction and gas chromatography/tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2012; 898, 9094.CrossRefGoogle ScholarPubMed
39. Padmanabhan, V, Siefert, K, Ransom, S, et al. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol. 2008; 28, 258263.CrossRefGoogle ScholarPubMed
40. Welshons, WV, Nagel, SC, vom Saal, FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology. 2006; 147(6 Suppl.), S56S69.CrossRefGoogle ScholarPubMed
41. Harley, KG, Aguilar, SR, 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.CrossRefGoogle ScholarPubMed
42. Rochester, JR. Bisphenol A and human health: a review of the literature. Reprod Toxicol. 2013; 42, 132155.CrossRefGoogle ScholarPubMed
43. 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
44. 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.CrossRefGoogle ScholarPubMed
45. Bansal, A, Rashid, C, Xin, F, et al. Sex- and dose-specific effects of maternal bisphenol A exposure on pancreatic islets of first- and second-generation adult mice offspring. Environ Health Perspect. 2017; 125, 097022.CrossRefGoogle ScholarPubMed
46. 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.CrossRefGoogle ScholarPubMed
47. Vandenberg, LN, Colborn, T, Hayes, TB, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012; 33, 378455.CrossRefGoogle ScholarPubMed
48. Melnick, R, Lucier, G, Wolfe, M, et al. Summary of the National Toxicology Program’s report of the endocrine disruptors low-dose peer review. Environ Health Perspect. 2002; 110, 427431.CrossRefGoogle ScholarPubMed
49. Diel, P, Schmidt, S, Vollmer, G, et al. Comparative responses of three rat strains (DA/Han, Sprague-Dawley and Wistar) to treatment with environmental estrogens. Arch Toxicol. 2004; 78, 183193.CrossRefGoogle ScholarPubMed
50. 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.CrossRefGoogle ScholarPubMed
51. Gao, L, Wang, HN, Zhang, L, et al. Effect of perinatal bisphenol A exposure on serum lipids and lipid enzymes in offspring rats of different sex. Biomed Environ Sci. 2016; 29, 686689.Google ScholarPubMed
52. Schneyer, A. Getting big on BPA: role for BPA in obesity? Endocrinology. 2011; 152, 33013303.CrossRefGoogle ScholarPubMed
53. 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.CrossRefGoogle ScholarPubMed
54. Tremblay-Franco, M, Cabaton, NJ, Canlet, C, et al. Dynamic metabolic disruption in rats perinatally exposed to low doses of bisphenol-A. PLoS One. 2015; 10, e0141698.CrossRefGoogle Scholar
55. 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
56. Nagel, SC, vom Saal, FS, Welshons, WV. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J Steroid Biochem Mol Biol. 1999; 69, 343357.CrossRefGoogle Scholar
57. Montano, MM, Welshons, WV, vom Saal, FS. Free estradiol in serum and brain uptake of estradiol during fetal and neonatal sexual differentiation in female rats. Biol Reprod. 1995; 53, 11981207.CrossRefGoogle ScholarPubMed
58. Nunez, EA, Benassayag, C, Savu, L, Vallette, G, Delorme, J. Oestrogen binding function of alpha 1-fetoprotein. J Steroid Biochem. 1979; 11, 237243.CrossRefGoogle ScholarPubMed
59. Milligan, SR, Khan, O, Nash, M. Competitive binding of xenobiotic oestrogens to rat alpha-fetoprotein and to sex steroid binding proteins in human and rainbow trout (Oncorhynchus mykiss) plasma. Gen Comp Endocrinol. 1998; 112, 8995.CrossRefGoogle ScholarPubMed
60. Hudak, CS, Sul, HS. Pref-1, a gatekeeper of adipogenesis. Front Endocrinol(Lausanne). 2013; 4, 79.Google ScholarPubMed
61. Wang, Y, Hudak, C, Sul, HS. Role of preadipocyte factor 1 in adipocyte differentiation. Clin Lipidol. 2010; 5, 109115.CrossRefGoogle ScholarPubMed
62. Wang, Y, Sul, HS. Pref-1 regulates mesenchymal cell commitment and differentiation through Sox9. Cell Metab. 2009; 9, 287302.CrossRefGoogle ScholarPubMed
63. Ailhaud, G, Amri, E, Bardon, S, et al. The adipocyte: relationships between proliferation and adipose cell differentiation. Am Rev RespirDis. 1990; 142(6 Pt 2), S57S59.CrossRefGoogle ScholarPubMed
64. Faust, IM, Miller, WH Jr, Sclafani, A, et al. Diet-dependent hyperplastic growth of adipose tissue in hypothalamic obese rats. Am J Physiol. 1984; 247(6 Pt 2), R1038R1046.Google ScholarPubMed
65. Miller, WH Jr., Faust, IM, Hirsch, J. Demonstration of de novo production of adipocytes in adult rats by biochemical and radioautographic techniques. J Lipid Res. 1984; 25, 336347.Google ScholarPubMed
66. Wabitsch, M. The acquisition of obesity: insights from cellular and genetic research. Proc Nutr Soc. 2000; 59, 325330.CrossRefGoogle ScholarPubMed
67. Masuno, H, Kidani, T, Sekiya, K, et al. Bisphenol A in combination with insulin can accelerate the conversion of 3T3-L1 fibroblasts to adipocytes. J Lipid Res. 2002; 43, 676684.Google ScholarPubMed
68. Phrakonkham, P, Viengchareun, S, Belloir, C, et al. Dietary xenoestrogens differentially impair 3T3-L1 preadipocyte differentiation and persistently affect leptin synthesis. J Steroid Biochem Mol Biol. 2008; 110, 95103.CrossRefGoogle ScholarPubMed
69. Sargis, RM, Johnson, DN, Choudhury, RA, Brady, MJ. Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity (SilverSpring). 2010; 18, 12831288.CrossRefGoogle ScholarPubMed
70. 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.CrossRefGoogle ScholarPubMed
71. Valentino, R, D'Esposito, V, Passaretti, F, et al. Bisphenol-A impairs insulin action and up-regulates inflammatory pathways in human subcutaneous adipocytes and 3T3-L1 cells. PLoS One. 2013; 8, e82099.CrossRefGoogle ScholarPubMed
72. Lee, JE, Ge, K. Transcriptional and epigenetic regulation of PPARgamma expression during adipogenesis. Cell Biosci. 2014; 4, 29.CrossRefGoogle ScholarPubMed
73. Bauer, RC, Sasaki, M, Cohen, DM, et al. Tribbles-1 regulates hepatic lipogenesis through posttranscriptional regulation of C/EBPalpha. J Clin Invest. 2015; 125, 38093818.CrossRefGoogle ScholarPubMed
74. Bastos, SL, 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.CrossRefGoogle Scholar
75. Kundakovic, M, Champagne, FA. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav Immun. 2011; 25, 10841093.CrossRefGoogle Scholar
76. Adamo, A, Sese, B, Boue, S, et al. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat Cell Biol. 2011; 13, 652659.CrossRefGoogle ScholarPubMed
77. Fujiki, K, Kano, F, Shiota, K, Murata, M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol. 2009; 7, 38.CrossRefGoogle ScholarPubMed
78. Musri, MM, Carmona, MC, Hanzu, FA, et al. Histone demethylase LSD1 regulates adipogenesis. J Biol Chem. 2010; 285, 3003430041.CrossRefGoogle ScholarPubMed
79. Zych, J, Stimamiglio, MA, Senegaglia, AC, et al. The epigenetic modifiers 5-aza-2'-deoxycytidine and trichostatin A influence adipocyte differentiation in human mesenchymal stem cells. Braz J Med Biol Res. 2013; 46, 405416.CrossRefGoogle ScholarPubMed
80. Hervouet, E, Vallette, FM, Cartron, PF. Dnmt3/transcription factor interactions as crucial players in targeted DNA methylation. Epigenetics. 2009; 4, 487499.CrossRefGoogle ScholarPubMed
81. Strakovsky, RS, Wang, H, Engeseth, NJ, et al. Developmental bisphenol A (BPA) exposure leads to sex-specific modification of hepatic gene expression and epigenome at birth that may exacerbate high-fat diet-induced hepatic steatosis. Toxicol Appl Pharmacol. 2015; 284, 101112.CrossRefGoogle ScholarPubMed
82. Lejonklou, MH, Dunder, L, Bladin, E, et al. Effects of low-dose developmental bisphenol A exposure on metabolic parameters and gene expression in male and female fischer 344 rat offspring. Environ Health Perspect. 2017; 125, 067018.CrossRefGoogle ScholarPubMed
83. 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.CrossRefGoogle ScholarPubMed
84. Yang, TC, Peterson, KE, Meeker, JD, et al. Bisphenol A and phthalates in utero and in childhood: association with child BMI z-score and adiposity. Environ Res. 2017; 156, 326333.CrossRefGoogle ScholarPubMed
85. Rubin, BS, Paranjpe, M, DaFonte, T, et al. Perinatal BPA exposure alters body weight and composition in a dose specific and sex specific manner: the addition of peripubertal exposure exacerbates adverse effects in female mice. Reprod Toxicol. 2017; 68, 130144.CrossRefGoogle Scholar
86. Susiarjo, M, Sasson, I, Mesaros, C, Bartolomei, MS. Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet. 2013; 9, e1003401.CrossRefGoogle ScholarPubMed
87. Ding, S, Fan, Y, Zhao, N, et al. High-fat diet aggravates glucose homeostasis disorder caused by chronic exposure to bisphenol A. J Endocrinol. 2014; 221, 167179.CrossRefGoogle ScholarPubMed
88. Perreault, L, McCurdy, C, Kerege, AA, et al. Bisphenol A impairs hepatic glucose sensing in C57BL/6 male mice. PLoS One. 2013; 8, e69991.CrossRefGoogle ScholarPubMed
89. Grundy, D. Principles and standards for reporting animal experiments in The. Journal of Physiology and Experimental Physiology. Exp Physiol . 2015; 100, 755758.Google ScholarPubMed

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 63
Total number of PDF views: 221 *
View data table for this chart

* Views captured on Cambridge Core between 29th August 2018 - 25th February 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

In vivo and in vitro bisphenol A exposure effects on adiposity
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

In vivo and in vitro bisphenol A exposure effects on adiposity
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

In vivo and in vitro bisphenol A exposure effects on adiposity
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *