Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-14T13:10:00.121Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of prenatal bisphenol-A exposure and postnatal overfeeding on cardiovascular function in female sheep

Published online by Cambridge University Press:  04 November 2016

S. M. J. MohanKumar ,
T. D. Rajendran ,
A. K. Vyas ,
V. Hoang ,
N. Asirvatham-Jeyaraj ,
A. Veiga-Lopez ,
N. B. Olivier ,
V. Padmanabhan  and
P. S. MohanKumar
S. M. J. MohanKumar
Affiliation:
Department of Veterinary Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA, USA
T. D. Rajendran
Affiliation:
Department of Small Animal Clinical Sciences, Michigan State University, East Lansing, MI, USA
A. K. Vyas
Affiliation:
Pediatrics and Human Development, Michigan State University, East Lansing, MI, USA
V. Hoang
Affiliation:
Pediatrics and Human Development, Michigan State University, East Lansing, MI, USA
N. Asirvatham-Jeyaraj
Affiliation:
Pharmacology & Toxicology, Michigan State University, East Lansing, MI, USA
A. Veiga-Lopez
Affiliation:
Department of Animal Sciences, Michigan State University, East Lansing, MI, USA Department of Pediatrics, University of Michigan, Ann Arbor, MI, USA
N. B. Olivier
Affiliation:
Department of Small Animal Clinical Sciences, Michigan State University, East Lansing, MI, USA
V. Padmanabhan
Affiliation:
Department of Pediatrics, University of Michigan, Ann Arbor, MI, USA
P. S. MohanKumar*
Affiliation:
Department of Veterinary Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA, USA
*
*Address for correspondence: Professor P. S. MohanKumar, Department of Veterinary Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, 501 D.W. Brooks Drive, Rm H370, Athens, GA 30602, USA. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Bisphenol-A (BPA) is a widely used endocrine-disrupting chemical. Prenatal exposure to BPA is known to affect birth weight, but its impact on the cardiovascular system has not been studied in detail. In this study, we investigated the effects of prenatal BPA treatment and its interaction with postnatal overfeeding on the cardiovascular system. Pregnant sheep were given daily subcutaneous injections of corn oil (control) or BPA (0.5 mg/kg/day in corn oil) from day 30 to day 90 of gestation. A subset of female offspring of these dams were overfed to increase body weight to ~30% over that of normal fed controls. Cardiovascular function was assessed using non-invasive echocardiography and cuff blood pressure (BP) monitoring at 21 months of age. Ventricular tissue was analyzed for gene expression of cardiac markers of hypertrophy and collagen at the end of the observation period. Prenatal BPA exposure had no significant effect on BP or morphometric measures. However, it increased atrial natriuretic peptide gene expression in the ventricles and reduced collagen expression in the right ventricle. Overfeeding produced a marked increase in body weight and BP. There were compensatory increases in left ventricular area and internal diameter. Prenatal BPA treatment produced a significant increase in interventricular septal thickness when animals were overfed. However, it appeared to block the increase in BP and left ventricular area caused by overfeeding. Taken together, these results suggest that prenatal BPA produces intrinsic changes in the heart that are capable of modulating morphological and functional parameters when animals become obese in later life.

Keywords

blood pressurecardiac gene expressioncardio-metabolic programmingechocardiographyendocrine disruptors
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 1 , February 2017 , pp. 65 - 74
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Michalowicz, J. Bisphenol A – sources, toxicity and biotransformation. Environ Toxicol Pharmacol. 2014; 37, 738–758.CrossRefGoogle ScholarPubMed
2. Hoekstra, EJ, Simoneau, C. Release of bisphenol A from polycarbonate: a review. Crit Rev Food Sci Nutr. 2013; 53, 386–402.Google Scholar
3. Ranjit, N, Siefert, K, Padmanabhan, V. Bisphenol-A and disparities in birth outcomes: a review and directions for future research. J Perinatol. 2010; 30, 2–9.Google Scholar
4. Vandenberg, LN, Hauser, R, Marcus, M, Olea, N, Welshons, WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24, 139–177.Google Scholar
5. Liao, C, Kannan, K. Widespread occurrence of bisphenol A in paper and paper products: implications for human exposure. Environ Sci Technol. 2011; 45, 9372–9379.Google Scholar
6. Geens, T, Roosens, L, Neels, H, Covaci, A. Assessment of human exposure to bisphenol-A, triclosan and tetrabromobisphenol-A through indoor dust intake in Belgium. Chemosphere. 2009; 76, 755–760.CrossRefGoogle ScholarPubMed
7. Padmanabhan, V, Siefert, K, Ransom, S, et al. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol. 2008; 28, 258–263.Google Scholar
8. Rochester, JR. Bisphenol A and human health: a review of the literature. Reprod Toxicol. 2013; 42, 132–155.CrossRefGoogle Scholar
9. Sun, Y, Irie, M, Kishikawa, N, et al. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr. 2004; 18, 501–507.Google Scholar
10. Golub, MS, Wu, KL, Kaufman, FL, et al. Bisphenol A: developmental toxicity from early prenatal exposure. Birth Defects Res B Dev Reprod Toxicol. 2010; 89, 441–466.CrossRefGoogle ScholarPubMed
11. Yan, S, Chen, Y, Dong, M, et al. Bisphenol A and 17beta-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PLoS One. 2011; 6, e25455.Google Scholar
12. Posnack, NG, Jaimes, R 3rd, Asfour, H, et al. Bisphenol A exposure and cardiac electrical conduction in excised rat hearts. Environ Health Perspect. 2014; 122, 384–390.CrossRefGoogle ScholarPubMed
13. Yan, S, Song, W, Chen, Y, et al. Low-dose bisphenol A and estrogen increase ventricular arrhythmias following ischemia-reperfusion in female rat hearts. Food Chem Toxicol. 2013; 56, 75–80.Google Scholar
14. Belcher, SM, Chen, Y, Yan, S, Wang, HS. Rapid estrogen receptor-mediated mechanisms determine the sexually dimorphic sensitivity of ventricular myocytes to 17beta-estradiol and the environmental endocrine disruptor bisphenol A. Endocrinology. 2012; 153, 712–720.Google Scholar
15. Patel, BB, Kasneci, A, Bolt, AM, et al. Chronic exposure to bisphenol A reduces successful cardiac remodeling after an experimental myocardial infarction in male C57bl/6n mice. Toxicol Sci. 2015; 146, 101–115.Google Scholar
16. Padmanabhan, V, Veiga-Lopez, A. Sheep models of polycystic ovary syndrome phenotype. Mol Cell Endocrinol. 2013; 373, 8–20.Google Scholar
17. Burrell, JH, Boyn, AM, Kumarasamy, V, et al. Growth and maturation of cardiac myocytes in fetal sheep in the second half of gestation. Anat Rec A Discov Mol Cell Evol Biol. 2003; 274, 952–961.Google Scholar
18. Thompson, JA, Piorkowska, K, Gagnon, R, Richardson, BS, Regnault, TR. Increased collagen deposition in the heart of chronically hypoxic ovine fetuses. J Dev Orig Health Dis. 2013; 4, 470–478.Google Scholar
19. Prins, GS, Tang, WY, Belmonte, J, Ho, SM. Developmental exposure to bisphenol A increases prostate cancer susceptibility in adult rats: epigenetic mode of action is implicated. Fertil Steril. 2008; 89, e41.Google Scholar
20. Veiga-Lopez, A, Moeller, J, Sreedharan, R, et al. Developmental programming: interaction between prenatal BPA exposure and postnatal adiposity on metabolic variables in female sheep. Am J Physiol Endocrinol Metab. 2016; 310, E238–E247.Google Scholar
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, 1873–1884.Google Scholar
22. Steckler, TL, Herkimer, C, Dumesic, DA, Padmanabhan, V. Developmental programming: excess weight gain amplifies the effects of prenatal testosterone excess on reproductive cyclicity – implication for polycystic ovary syndrome. Endocrinology. 2009; 150, 1456–1465.Google Scholar
23. Aitken, GD, Raizis, AM, Yandle, TG, et al. The characterization of ovine genes for atrial, brain, and C-type natriuretic peptides. Domest Anim Endocrinol. 1999; 16, 115–121.CrossRefGoogle ScholarPubMed
24. Livak, KJ, Schmittgen, TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25, 402–408.Google Scholar
25. Rademaker, MT, Richards, AM. Cardiac natriuretic peptides for cardiac health. Clin Sci (Lond). 2005; 108, 23–36.Google Scholar
26. Charles, CJ, Prickett, TC, Espiner, EA, et al. Regional sampling and the effects of experimental heart failure in sheep: differential responses in A, B and C-type natriuretic peptides. Peptides. 2006; 27, 62–68.Google Scholar
27. Rademaker, MT, Charles, CJ, Espiner, EA, et al. Comparative bioactivity of atrial and brain natriuretic peptides in an ovine model of heart failure. Clin Sci (Lond). 1997; 92, 159–165.Google Scholar
28. Cameron, VA, Rademaker, MT, Ellmers, LJ, et al. Atrial (ANP) and brain natriuretic peptide (BNP) expression after myocardial infarction in sheep: ANP is synthesized by fibroblasts infiltrating the infarct. Endocrinology. 2000; 141, 4690–4697.Google Scholar
29. Gardner, DG. Natriuretic peptides: markers or modulators of cardiac hypertrophy? Trends Endocrinol Metab. 2003; 14, 411–416.Google Scholar
30. Nishimura, T, Mizukawa, K, Nakao, K, et al. Atrial natriuretic polypeptide (ANP)-immunoreactivity and specific atrial granules in cardiac myocytes of stroke-prone spontaneously hypertensive rat (SHRSP). Arch Histol Cytol. 1994; 57, 1–7.Google Scholar
31. Horio, T, Nishikimi, T, Yoshihara, F, et al. Inhibitory regulation of hypertrophy by endogenous atrial natriuretic peptide in cultured cardiac myocytes. Hypertension. 2000; 35, 19–24.Google Scholar
32. Hijazi, A, Guan, H, Cernea, M, Yang, K. Prenatal exposure to bisphenol A disrupts mouse fetal lung development. FASEB J. 2015; 29, 4968–4977.CrossRefGoogle ScholarPubMed
33. Spanier, AJ, Kahn, RS, Kunselman, AR, et al. Bisphenol a exposure and the development of wheeze and lung function in children through age 5 years. JAMA Pediatr. 2014; 168, 1131–1137.Google Scholar
34. Graham, HK, Trafford, AW. Spatial disruption and enhanced degradation of collagen with the transition from compensated ventricular hypertrophy to symptomatic congestive heart failure. Am J Physiol Heart Circ Physiol. 2007; 292, H1364–H1372.CrossRefGoogle ScholarPubMed
35. Alpert, MA. Obesity cardiomyopathy: pathophysiology and evolution of the clinical syndrome. Am J Med Sci. 2001; 321, 225–236.CrossRefGoogle ScholarPubMed
36. Gottdiener, JS, Reda, DJ, Williams, DW, Materson, BJ. Left atrial size in hypertensive men: influence of obesity, race and age. Department of Veterans Affairs Cooperative Study Group on Antihypertensive Agents. J Am Coll Cardiol. 1997; 29, 651–658.Google Scholar
37. de Simone, G, Devereux, RB, Roman, MJ, Alderman, MH, Laragh, JH. Relation of obesity and gender to left ventricular hypertrophy in normotensive and hypertensive adults. Hypertension. 1994; 23, 600–606.Google Scholar
38. Vasan, RS. Cardiac function and obesity. Heart. 2003; 89, 1127–1129.Google Scholar
39. Matthews, KA, Kuller, LH, Sutton-Tyrrell, K, Chang, Y-F. Changes in cardiovascular risk factors during the perimenopause and postmenopause and carotid artery atherosclerosis in healthy women. Stroke. 2001; 32, 1104–1111.Google Scholar
40. Alexander, JK. Obesity and the heart. Heart Dis Stroke. 1993; 2, 317–321.Google Scholar
41. Veiga-Lopez, A, Kannan, K, Liao, C, et al. Gender-specific effects on gestational length and birth weight by early pregnancy BPA exposure. J Clin Endocrinol Metab. 2015; 100, E1394–E1403.CrossRefGoogle ScholarPubMed