Milk lipid composition is modified by perinatal exposure to bisphenol A

Molecular and Cellular Endocrinology

Volumn 411, Issue , 2015, Pages 258-267

  Altamirano, Gabriela A ^a   Muñoz de Toro, Mónica ^a   Luque, Enrique H ^a   Gómez, Ayelén L ^a   Delconte, Melisa B ^a   Kass, Laura ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Bisphenol A; Lactation; Mammary gland differentiation; Milk fat globules; Milk fatty acid profile

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; FATTY ACID; LIPID; MILK FAT; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CONTROLLED STUDY; EXPOSURE; FEMALE; GESTATION PERIOD; GROWTH; LACTATION; LIPID COMPOSITION; MAMMARY GLAND; MILK; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; WEIGHT GAIN; ANIMAL; CHEMISTRY; DRUG EFFECTS; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; BENZHYDRYL COMPOUNDS; FEMALE; LACTATION; LIPIDS; MILK; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

EID: 84930178410     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.05.007     Document Type: Article

References (57)

1. Acevedo N., Davis B., Schaeberle C.M., Sonnenschein C., Soto A.M. Perinatally administered bisphenol a as a potential mammary gland carcinogen in rats. Environ. Health Perspect 2013, 121:1040-1046.
2. Anderson S.M., Rudolph M.C., McManaman J.L., Neville M.C. Key stages in mammary gland development. Secretory activation in the mammary gland: it's not just about milk protein synthesis!. Breast Cancer Res 2007, 9:204.
3. Andreoli M.F., Stoker C., Rossetti M.F., Alzamendi A., Castrogiovanni D., Luque E.H., et al. Withdrawal of dietary phytoestrogens in adult male rats affects hypothalamic regulation of food intake, induces obesity and alters glucose metabolism. Mol. Cell. Endocrinol 2015, 401:111-119.
4. Angle B.M., Do R.P., Ponzi D., Stahlhut R.W., Drury B.E., Nagel S.C., 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, 42:256-268.
5. Barber M.C., Clegg R.A., Travers M.T., Vernon R.G. Lipid metabolism in the lactating mammary gland. Biochim. Biophys. Acta 1997, 1347:101-126.
6. Bionaz M., Loor J.J. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 2008, 9:366.
7. Blanchette-Mackie E.J., Dwyer N.K., Barber T., Coxey R.A., Takeda T., Rondinone C.M., et al. Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res 1995, 36:1211-1226.
8. Boudalia S., Berges R., Chabanet C., Folia M., Decocq L., Pasquis B., et al. A multi-generational study on low-dose BPA exposure in Wistar rats: effects on maternal behavior, flavor intake and development. Neurotoxicol. Teratol 2014, 41:16-26.
9. Chamorro-Garcia R., Sahu M., Abbey R.J., Laude J., Pham N., Blumberg B. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ. Health Perspect 2013, 121:359-366.
10. Chen M., Xu B., Ji W., Qiao S., Hu N., Hu Y., et al. Bisphenol A alters n-6 fatty acid composition and decreases antioxidant enzyme levels in rat testes: a LC-QTOF-based metabolomics study. PLoS ONE 2012, 7:e44754.
11. Cikos S., Bukovska A., Koppel J. Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol. Biol 2007, 8:113.
12. de Alaniz M.J., Marra C.A. Glucocorticoid and mineralocorticoid hormones depress liver delta 5 desaturase activity through different mechanisms. Lipids 1992, 27:599-604.
13. Dewettinck K., Rombaut R., Thienpont N., Le T., Messens K. Nutritional and technological aspects of milk fat globule membrane material. Int. Dairy J. 2007, 18:436-457.
14. Doerge D.R., Twaddle N.C., Vanlandingham M., Fisher J.W. Pharmacokinetics of bisphenol A in neonatal and adult CD-1 mice: inter-species comparisons with Sprague-Dawley rats and rhesus monkeys. Toxicol. Lett 2011, 207:298-305.
15. Durando M., Kass L., Piva J., Sonnenschein C., Soto A.M., Luque E.H., et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ. Health Perspect 2007, 115:80-86.
16. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem 1957, 226:497-509.
17. Fontana A.R., Munoz de Toro M., Altamirano J.C. One-step derivatization and preconcentration microextraction technique for determination of bisphenol A in beverage samples by gas chromatography-mass spectrometry. J. Agric. Food Chem 2011, 59:3559-3565.
18. German J.B., Dillard C.J. Composition, structure and absorption of milk lipids: a source of energy, fat-soluble nutrients and bioactive molecules. Crit. Rev. Food Sci. Nutr 2006, 46:57-92.
19. Guilloteau P., Zabielski R., Hammon H.M., Metges C.C. Adverse effects of nutritional programming during prenatal and early postnatal life, some aspects of regulation and potential prevention and treatments. J. Physiol. Pharmacol 2009, 60(Suppl. 3):17-35.
20. Hsieh C.W., Millward C.A., DeSantis D., Pisano S., Machova J., Perales J.C., et al. Reduced milk triglycerides in mice lacking phosphoenolpyruvate carboxykinase in mammary gland adipocytes and white adipose tissue contribute to the development of insulin resistance in pups. J. Nutr 2009, 139:2257-2265.
21. Hurtado de Catalfo G.E., de Alaniz M.J., Marra C.A. Influence of commercial dietary oils on lipid composition and testosterone production in interstitial cells isolated from rat testis. Lipids 2009, 44:345-357.
22. Kang Y., Hengbo S., Jun L., Wangsheng Z., Huibin T., Huaiping S. PPARG modulated lipid accumulation in dairy GMEC via regulation of ADRP gene. J. Cell. Biochem 2015, 116:192-201.
23. Kass L., Altamirano G.A., Bosquiazzo V.L., Luque E.H., Muñoz-de-Toro M. Perinatal exposure to xenoestrogens impairs mammary gland differentiation and modifies milk composition in Wistar rats. Reprod. Toxicol 2012, 33:390-400.
24. Liang G., Yang J., Horton J.D., Hammer R.E., Goldstein J.L., Brown M.S. Diminished hepatic response to fasting/refeeding and liver X receptor agonists in mice with selective deficiency of sterol regulatory element-binding protein-1c. J. Biol. Chem 2002, 277:9520-9528.
25. Listenberger L.L., Ostermeyer-Fay A.G., Goldberg E.B., Brown W.J., Brown D.A. Adipocyte differentiation-related protein reduces the lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. J. Lipid Res 2007, 48:2751-2761.
26. Lubrano C., Genovesi G., Specchia P., Costantini D., Mariani S., Petrangeli E., et al. Obesity and metabolic comorbidities: environmental diseases?. Oxid. Med. Cell. Longev 2013, 2013:640673.
27. Marmugi A., Ducheix S., Lasserre F., Polizzi A., Paris A., Priymenko N., et al. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology 2012, 55:395-407.
28. Marra C.A., de Alaniz M.J. Mineralocorticoids modify rat liver delta 6 desaturase activity and other parameters of lipid metabolism. Biochem. Int 1990, 22:483-493.
29. McManaman J.L. Formation of milk lipids: a molecular perspective. Clin. Lipidol 2009, 4:391-401.
30. McManaman J.L. Lipid transport in the lactating mammary gland. J. Mammary Gland Biol. Neoplasia 2014, 19:35-42.
31. McManaman J.L., Palmer C.A., Wright R.M., Neville M.C. Functional regulation of xanthine oxidoreductase expression and localization in the mouse mammary gland: evidence of a role in lipid secretion. J. Physiol 2002, 545:567-579.
32. McManaman J.L., Russell T.D., Schaack J., Orlicky D.J., Robenek H. Molecular determinants of milk lipid secretion. J. Mammary Gland Biol. Neoplasia 2007, 12:259-268.
33. Mehlem A., Hagberg C.E., Muhl L., Eriksson U., Falkevall A. Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease. Nat. Protoc 2013, 8:1149-1154.
34. Mesilati-Stahy R., Mida K., Argov-Argaman N. Size-dependent lipid content of bovine milk fat globule and membrane phospholipids. J. Agric. Food Chem 2011, 59:7427-7435.
35. Moral R., Wang R., Russo I.H., Lamartiniere C.A., Pereira J., Russo J. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J. Endocrinol 2008, 196:101-112.
36. Morrison B., Cutler M.L. The contribution of adhesion signaling to lactogenesis. J. Cell Commun. Signal 2010, 4:131-139.
37. Muñoz-de-Toro M., Markey C.M., Wadia P.R., Luque E.H., Rubin B.S., Sonnenschein C., et al. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146:4138-4147.
38. Newbold R.R. Impact of environmental endocrine disrupting chemicals on the development of obesity. Hormones (Athens) 2010, 9:206-217.
39. Palanza P.L., Howdeshell K.L., Parmigiani S., vom Saal F.S. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ. Health Perspect 2002, 110(Suppl. 3):415-422.
40. Passos M.C., Ramos C.F., Moura E.G. Short and long term effects on malnutrition in rats during lactation on the body weight of offspring. Nutr. Res 2000, 20:1603-1611.
41. Paulose T., Speroni L., Sonnenschein C., Soto A.M. Estrogens in the wrong place at the wrong time: fetal BPA exposure and mammary cancer. Reprod. Toxicol 2014, 10.1016/j.reprotox.2014.09.012.
42. Ramos J.G., Varayoud J., Kass L., Rodriguez H., Costabel L., Muñoz-De-Toro M., et al. Bisphenol a induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 2003, 144:3206-3215.
43. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., et al. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol 2007, 24:199-224.
44. Rochester J.R. Bisphenol A and human health: a review of the literature. Reprod. Toxicol 2013, 42:132-155.
45. Rodriguez-Cruz M., Sanchez R., Sanchez A.M., Kelleher S.L., Sanchez-Munoz F., Maldonado J., et al. Participation of mammary gland in long-chain polyunsaturated fatty acid synthesis during pregnancy and lactation in rats. Biochim. Biophys. Acta 2011, 1811:284-293.
46. Rubin B.S. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J. Steroid Biochem. Mol. Biol 2011, 127:27-34.
47. Rudolph M.C., Monks J., Burns V., Phistry M., Marians R., Foote M.R., et al. Sterol regulatory element binding protein and dietary lipid regulation of fatty acid synthesis in the mammary epithelium. Am. J. Physiol. Endocrinol. Metab 2010, 299:E918-E927.
48. Russell T.D., Palmer C.A., Orlicky D.J., Fischer A., Rudolph M.C., Neville M.C., et al. Cytoplasmic lipid droplet accumulation in developing mammary epithelial cells: roles of adipophilin and lipid metabolism. J. Lipid Res 2007, 48:1463-1475.
49. Russell T.D., Schaack J., Orlicky D.J., Palmer C., Chang B.H., Chan L., et al. Adipophilin regulates maturation of cytoplasmic lipid droplets and alveolae in differentiating mammary glands. J. Cell Sci 2011, 124:3247-3253.
50. Shi H., Luo J., Zhu J., Li J., Sun Y., Lin X., et al. PPAR gamma regulates genes involved in triacylglycerol synthesis and secretion in mammary gland epithelial cells of dairy goats. PPAR Res 2013, 2013:310948.
51. Soto A.M., Brisken C., Schaeberle C., Sonnenschein C. Does cancer start in the womb? Altered mammary gland development and predisposition to breast cancer due to in utero exposure to endocrine disruptors. J. Mammary Gland Biol. Neoplasia 2013, 18:199-208.
52. Taylor J.A., Vom Saal F.S., Welshons W.V., Drury B., Rottinghaus G., Hunt P.A., et al. Similarity of bisphenol A pharmacokinetics in rhesus monkeys and mice: relevance for human exposure. Environ. Health Perspect 2011, 119:422-430.
53. Tharp A.P., Maffini M.V., Hunt P.A., VandeVoort C.A., Sonnenschein C., Soto A.M. Bisphenol A alters the development of the rhesus monkey mammary gland. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:8190-8195.
54. Vandenberg L.N., Maffini M.V., Sonnenschein C., Rubin B.S., Soto A.M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev 2009, 30:75-95.
55. Vandenberg L.N., Chahoud I., Heindel J.J., Padmanabhan V., Paumgartten F.J., Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ. Health Perspect 2010, 118:1055-1070.
56. Vom Saal F.S., Nagel S.C., Coe B.L., Angle B.M., Taylor J.A. The estrogenic endocrine disrupting chemical bisphenol A (BPA) and obesity. Mol. Cell. Endocrinol 2012, 354:74-84.
57. Zhang H.Y., Xue W.Y., Li Y.Y., Ma Y., Zhu Y.S., Huo W.Q., et al. Perinatal exposure to 4-nonylphenol affects adipogenesis in first and second generation rats offspring. Toxicol. Lett 2014, 225:325-332.