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Bisphenol A in the Gut: Another Break in the Wall?

  • Viorica Braniste
  • Marc Audebert
  • Daniel Zalko
  • Eric HoudeauEmail author
Chapter
Part of the Research and Perspectives in Endocrine Interactions book series (RPEI)

Abstract

From animal studies, a consensus exists that the synthetic estrogen bisphenol A (BPA), a plastic monomer widely used in the food-packaging industry, is able to disrupt endocrine signalling pathways during development, with persisting effects later in life. Although the fetal and then the adult gut expresses functional estrogen receptors (ERs), the endocrine impact of BPA on the intestinal barrier function remains largely unexplored. The intestinal epithelium and mucosal immune cells provide a first line of defence designed to restrict the passage of harmful substances from the lumen. Intestinal permeability is high at birth, permitting lumen-to-mucosa exchanges involved in the maturation process of the gut immune system. As a barrier to the external environment, gut epithelium is renewed constantly during life. Renewal of gut epithelial cells occurs in less than ~96 h, starting from fetal stage, and is dependent on controlled cell stimulation and proliferation by various signalling pathways. Lessons learned from ER-deficient mice underline the importance of estrogen signalling in growth, organization and maintenance of a normal epithelial barrier. In rats, BPA was recently shown to interact with ERs in the adult gut by mimicking the estradiol-mediated decrease of epithelial permeability through genomic pathways. This effect also occurs in neonates when low doses of BPA (5 μg/kg BW/day: tenfold below the tolerable daily intake for humans) are orally administered to pregnant and then lactating rats. A perinatal exposure to BPA also reduces epithelial cell proliferation in the colon of neonates, while the overall decrease of intestinal permeability remains apparent in adulthood only in female offspring. As a consequence, adult females perinatally exposed to BPA have been shown to develop severe inflammatory responses in a rat model of inflammatory bowel disease, demonstrating enhanced expression and production of T-Helper 1 cytokines in inflamed areas. In mice, a mother-to-infant transport of maternal BPA is consistent with the ability of the chemical to reach the fetus through the placental barrier: BPA is present in the amniotic fluid and accumulates in the maturing gut. Although BPA, once absorbed by maternal gut, is rapidly deactivated by first pass conjugation in the liver, recent studies emphasize that BPA at low, environmentally relevant levels can transfer across the human placenta, mainly in an estrogen-active, unconjugated form. It is now thought that BPA ingested by dams has repercussions on the education of the immune system by reducing intestinal permeability from fetal stages and promotes severe inflammatory response later in life.

Keywords

Intestinal Permeability Endocrine Disruptor Intestinal Barrier Function Perinatal Exposure Severe Inflammatory Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aksglaede L, Juul A, Leffers H, Skakkebaek NE, Andersson AM (2006) The sensitivity of the child to sex steroids: possible impact of exogenous estrogens. Hum Reprod Update 12:341–349PubMedCrossRefGoogle Scholar
  2. Bakker J, Baum MJ (2008) Role for estradiol in female-typical brain and behavioral sexual differentiation. Front Neuroendocrinol 29:1–16PubMedCrossRefGoogle Scholar
  3. Balakrishnan B, Henare K, Thorstensen EB, Ponnampalam AP, Mitchell MD (2010) Transfer of bisphenol A across the human placenta. Am J Obstet Gynecol 202(393):e391–e397Google Scholar
  4. Barone M, Tanzi S, Lofano K, Scavo MP, Guido R, Demarinis L, Principi MB, Bucci A, Di Leo A (2008) Estrogens, phytoestrogens and colorectal neoproliferative lesions. Genes Nutr 3:7–13PubMedCrossRefGoogle Scholar
  5. Bondesson M, Jonsson J, Pongratz I, Olea N, Cravedi JP, Zalko D, Hakansson H, Halldin K, Di Lorenzo D, Behl C, Manthey D, Balaguer P, Demeneix B, Fini JB, Laudet V, Gustafsson JA (2009) A CASCADE of effects of bisphenol A. Reprod Toxicol 28:563–567PubMedCrossRefGoogle Scholar
  6. Borghoff SJ, Birnbaum LS (1985) Age-related changes in glucuronidation and deglucuronidation in liver, small intestine, lung, and kidney of male Fischer rats. Drug Metab Dispos 13:62–67PubMedGoogle Scholar
  7. Brandenberger AW, Tee MK, Lee JY, Chao V, Jaffe RB (1997) Tissue distribution of estrogen receptors alpha (ER-alpha) and beta (ER-beta) mRNA in the midgestational human fetus. J Clin Endocrinol Metab 82:3509–3512PubMedCrossRefGoogle Scholar
  8. Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E (2009) Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J Physiol 587(Pt 13):3317–3328PubMedCrossRefGoogle Scholar
  9. Braniste V, Jouault A, Gaultier E, Polizzi A, Buisson-Brenac C, Leveque M, Martin PG, Theodorou V, Fioramonti J, Houdeau E (2010) Impact of oral bisphenol A at reference doses on intestinal barrier function and sex differences after perinatal exposure in rats. Proc Natl Acad Sci USA 107:448–453PubMedCrossRefGoogle Scholar
  10. Brede C, Fjeldal P, Skjevrak I, Herikstad H (2003) Increased migration levels of bisphenol A from polycarbonate baby bottles after dishwashing, boiling and brushing. Food Addit Contam 20:684–689PubMedCrossRefGoogle Scholar
  11. Brotons JA, Olea-Serrano MF, Villalobos M, Pedraza V, Olea N (1995) Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 103:608–612PubMedCrossRefGoogle Scholar
  12. Burridge E (2003) Bisphenol A product profile. Eur Chem News 17:14–20Google Scholar
  13. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL (2005) Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113:391–395PubMedCrossRefGoogle Scholar
  14. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL (2008) Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ Health Perspect 116:39–44PubMedCrossRefGoogle Scholar
  15. Campbell-Thompson M, Lynch IJ, Bhardwaj B (2001) Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res 61:632–640PubMedGoogle Scholar
  16. Cao XL, Corriveau J, Popovic S (2010) Sources of low concentrations of bisphenol A in canned beverage products. J Food Prot 73:1548–1551PubMedGoogle Scholar
  17. Carwile JL, Luu HT, Bassett LS, Driscoll DA, Yuan C, Chang JY, Ye X, Calafat AM, Michels KB (2009) Polycarbonate bottle use and urinary bisphenol A concentrations. Environ Health Perspect 117:1368–1372PubMedGoogle Scholar
  18. Catassi C, Bonucci A, Coppa GV, Carlucci A, Giorgi PL (1995) Intestinal permeability changes during the first month: effect of natural versus artificial feeding. J Pediatr Gastroenterol Nutr 21:383–386PubMedCrossRefGoogle Scholar
  19. Chen AC, Berhow MA, Tappenden KA, Donovan SM (2005) Genistein inhibits intestinal cell proliferation in piglets. Pediatr Res 57:192–200PubMedCrossRefGoogle Scholar
  20. Colborn T (2004) Neurodevelopment and endocrine disruption. Environ Health Perspect 112:944–949PubMedCrossRefGoogle Scholar
  21. Cosnes J, Carbonnel F, Carrat F, Beaugerie L, Gendre JP (1999) Oral contraceptive use and the clinical course of Crohn’s disease: a prospective cohort study. Gut 45:218–222PubMedCrossRefGoogle Scholar
  22. Dong P, Yang Y, Wang WP (2010) The role of intestinal bifidobacteria on immune system development in young rats. Early Hum Dev 86:51–58PubMedCrossRefGoogle Scholar
  23. El-Tawil AM (2008) Oestrogens and Crohn’s disease: the missed link. Andrologia 40:141–145CrossRefGoogle Scholar
  24. Emmerson E, Campbell L, Ashcroft GS, Hardman MJ (2009) Unique and synergistic roles for 17beta-estradiol and macrophage migration inhibitory factor during cutaneous wound closure are cell type specific. Endocrinology 150:2749–2757PubMedCrossRefGoogle Scholar
  25. Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjold M, Gustafsson JA (1997) Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 82:4258–4265PubMedCrossRefGoogle Scholar
  26. Fini JB, Dolo L, Cravedi JP, Demeneix B, Zalko D (2009) Metabolism of the endocrine disruptor BPA by Xenopus laevis tadpoles. Ann NY Acad Sci 1163:394–397PubMedCrossRefGoogle Scholar
  27. Fruzzetti F, Lazzarini V, Ricci C, Quirici B, Gambacciani M, Paoletti AM, Genazzani AR (2007) Effect of an oral contraceptive containing 30 microg ethinylestradiol plus 3 mg drospirenone on body composition of young women affected by premenstrual syndrome with symptoms of water retention. Contraception 76:190–194PubMedCrossRefGoogle Scholar
  28. Garcia Rodriguez LA, Gonzalez-Perez A, Johansson S, Wallander MA (2005) Risk factors for inflammatory bowel disease in the general population. Aliment Pharmacol Ther 22:309–315PubMedCrossRefGoogle Scholar
  29. Geibel JP (2005) Secretion and absorption by colonic crypts. Annu Rev Physiol 67:471–490PubMedCrossRefGoogle Scholar
  30. Harnish DC, Albert LM, Leathurby Y, Eckert AM, Ciarletta A, Kasaian M, Keith JC Jr (2004) Beneficial effects of estrogen treatment in the HLA-B27 transgenic rat model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 286:G118–G125PubMedCrossRefGoogle Scholar
  31. Heimeier RA, Das B, Buchholz DR, Shi YB (2009) The xenoestrogen bisphenol A inhibits postembryonic vertebrate development by antagonizing gene regulation by thyroid hormone. Endocrinology 150:2964–2973PubMedCrossRefGoogle Scholar
  32. Heitkemper MM, Cain KC, Jarrett ME, Burr RL, Hertig V, Bond EF (2003) Symptoms across the menstrual cycle in women with irritable bowel syndrome. Am J Gastroenterol 98:420–430PubMedCrossRefGoogle Scholar
  33. Hofer N, Diel P, Wittsiepe J, Wilhelm M, Kluxen FM, Degen GH (2010) Investigations on the estrogenic activity of the metallohormone cadmium in the rat intestine. Arch Toxicol 84:541–552PubMedCrossRefGoogle Scholar
  34. Holladay SD, Xiao S, Diao H, Barber J, Nagy T, Ye X, Gogal RM Jr (2010) Perinatal bisphenol A exposure in C57B6/129svj male mice: potential altered cytokine/chemokine production in adulthood. Int J Environ Res Public Health 7:2845–2852PubMedCrossRefGoogle Scholar
  35. Houdeau E, Moriez R, Leveque M, Salvador-Cartier C, Waget A, Leng L, Bueno L, Bucala R, Fioramonti J (2007) Sex steroid regulation of macrophage migration inhibitory factor in normal and inflamed colon in the female rat. Gastroenterology 132:982–993PubMedCrossRefGoogle Scholar
  36. Howe SR, Borodinsky L (1998) Potential exposure to bisphenol A from food-contact use of polycarbonate resins. Food Addit Contam 15:370–375PubMedGoogle Scholar
  37. Inoue K, Kato K, Yoshimura Y, Makino T, Nakazawa H (2000) Determination of bisphenol A in human serum by high-performance liquid chromatography with multi-electrode electrochemical detection. J Chromatogr B Biomed Sci Appl 749:17–23PubMedCrossRefGoogle Scholar
  38. Inoue H, Yuki G, Yokota H, Kato S (2003) Bisphenol A glucuronidation and absorption in rat intestine. Drug Metab Dispos 31:140–144PubMedCrossRefGoogle Scholar
  39. Iwamuro S, Sakakibara M, Terao M, Ozawa A, Kurobe C, Shigeura T, Kato M, Kikuyama S (2003) Teratogenic and anti-metamorphic effects of bisphenol A on embryonic and larval Xenopus laevis. Gen Comp Endocrinol 133:189–198PubMedCrossRefGoogle Scholar
  40. Kane SV, Reddy D (2008) Hormonal replacement therapy after menopause is protective of disease activity in women with inflammatory bowel disease. Am J Gastroenterol 103:1193–1196PubMedCrossRefGoogle Scholar
  41. Kim HS, Han SY, Yoo SD, Lee BM, Park KL (2001) Potential estrogenic effects of bisphenol-A estimated by in vitro and in vivo combination assays. J Toxicol Sci 26:111–118PubMedCrossRefGoogle Scholar
  42. Konstantinopoulos PA, Kominea A, Vandoros G, Sykiotis GP, Andricopoulos P, Varakis I, Sotiropoulou-Bonikou G, Papavassiliou AG (2003) Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour’s dedifferentiation. Eur J Cancer 39:1251–1258PubMedCrossRefGoogle Scholar
  43. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863–870PubMedCrossRefGoogle Scholar
  44. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252–4263PubMedCrossRefGoogle Scholar
  45. Kurebayashi H, Nagatsuka S, Nemoto H, Noguchi H, Ohno Y (2005) Disposition of low doses of 14C-bisphenol A in male, female, pregnant, fetal, and neonatal rats. Arch Toxicol 79:243–252PubMedCrossRefGoogle Scholar
  46. Lee YJ, Ryu HY, Kim HK, Min CS, Lee JH, Kim E, Nam BH, Park JH, Jung JY, Jang DD, Park EY, Lee KH, Ma JY, Won HS, Im MW, Leem JH, Hong YC, Yoon HS (2008) Maternal and fetal exposure to bisphenol A in Korea. Reprod Toxicol 25:413–419PubMedCrossRefGoogle Scholar
  47. Lopez-Cervantes J, Paseiro-Losada P (2003) Determination of bisphenol A in, and its migration from, PVC stretch film used for food packaging. Food Addit Contam 20:596–606PubMedCrossRefGoogle Scholar
  48. Masyuk AI, Marinelli RA, LaRusso NF (2002) Water transport by epithelia of the digestive tract. Gastroenterology 122:545–562PubMedCrossRefGoogle Scholar
  49. Matthews JB, Twomey K, Zacharewski TR (2001) In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol 14:149–157PubMedCrossRefGoogle Scholar
  50. Mayer L (2010) Evolving paradigms in the pathogenesis of IBD. J Gastroenterol 45:9–16PubMedCrossRefGoogle Scholar
  51. Milligan SR, Khan O, Nash M (1998) 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 112:89–95PubMedCrossRefGoogle Scholar
  52. Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, Hataya Y, Shimatsu A, Kuzuya H, Nakao K (2002) Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 87:5185–5190PubMedCrossRefGoogle Scholar
  53. Morreale de Escobar G (2001) The role of thyroid hormone in fetal neurodevelopment. J Pediatr Endocrinol Metab 14(Suppl 6):1453–1462PubMedGoogle Scholar
  54. Moussa L, Grimaldi C, Paul F, Braniste V, Tondereau V, Eutamene H, Bueno L, Fioramonti J, Houdeau E, Theodorou V (2010) Protective effect of a phytoestrogen-enriched diet on the increase in visceral sensitivity and intestinal permeability induced by acute stress in female rats. Gastroenterology 138:S27CrossRefGoogle Scholar
  55. Nam SH, Seo YM, Kim MG (2010) Bisphenol A migration from polycarbonate baby bottle with repeated use. Chemosphere 79:949–952PubMedCrossRefGoogle Scholar
  56. Nishikawa M, Iwano H, Yanagisawa R, Koike N, Inoue H, Yokota H (2010) Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ Health Perspect 118:1196–1203PubMedCrossRefGoogle Scholar
  57. O’Leary KA, Day AJ, Needs PW, Mellon FA, O’Brien NM, Williamson G (2003) Metabolism of quercetin-7- and quercetin-3-glucuronides by an in vitro hepatic model: the role of human beta-glucuronidase, sulfotransferase, catechol-O-methyltransferase and multi-resistant protein 2 (MRP2) in flavonoid metabolism. Biochem Pharmacol 65:479–491PubMedCrossRefGoogle Scholar
  58. O’Mahony F, Harvey BJ (2008) Sex and estrous cycle-dependent rapid protein kinase signaling actions of estrogen in distal colonic cells. Steroids 73(9–10):889–894PubMedCrossRefGoogle Scholar
  59. Oelkers WK (1996) Effects of estrogens and progestogens on the renin-aldosterone system and blood pressure. Steroids 61:166–171PubMedCrossRefGoogle Scholar
  60. Olea N, Pulgar R, Perez P, Olea-Serrano F, Rivas A, Novillo-Fertrell A, Pedraza V, Soto AM, Sonnenschein C (1996) Estrogenicity of resin-based composites and sealants used in dentistry. Environ Health Perspect 104:298–305PubMedCrossRefGoogle Scholar
  61. Pepe GJ, Burch MG, Albrecht ED (2006) Developmental regulation of the sodium/hydrogen ion exchangers and their regulatory factors in baboon placental syncytiotrophoblast. Endocrinology 147:2986–2996PubMedCrossRefGoogle Scholar
  62. Pfaffl MW, Lange IG, Meyer HH (2003) The gastrointestinal tract as target of steroid hormone action: quantification of steroid receptor mRNA expression (AR, ERalpha, ERbeta and PR) in 10 bovine gastrointestinal tract compartments by kinetic RT-PCR. J Steroid Biochem Mol Biol 84:159–166PubMedCrossRefGoogle Scholar
  63. Routledge EJ, White R, Parker MG, Sumpter JP (2000) Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 275:35986–35993PubMedCrossRefGoogle Scholar
  64. Sajiki J, Yonekubo J (2004) Leaching of bisphenol A (BPA) from polycarbonate plastic to water containing amino acids and its degradation by radical oxygen species. Chemosphere 55:861–867PubMedCrossRefGoogle Scholar
  65. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I (2002) Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 110:A703–A707PubMedCrossRefGoogle Scholar
  66. Seibel J, Molzberger AF, Hertrampf T, Laudenbach-Leschowski U, Degen GH, Diel P (2008) In utero and postnatal exposure to a phytoestrogen-enriched diet increases parameters of acute inflammation in a rat model of TNBS-induced colitis. Arch Toxicol 82:941–950PubMedCrossRefGoogle Scholar
  67. Seibel J, Molzberger AF, Hertrampf T, Laudenbach-Leschowski U, Diel P (2009) Oral treatment with genistein reduces the expression of molecular and biochemical markers of inflammation in a rat model of chronic TNBS-induced colitis. Eur J Nutr 48:213–220PubMedCrossRefGoogle Scholar
  68. Shaw SY, Blanchard JF, Bernstein CN (2010) Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol 105:2687–2692PubMedCrossRefGoogle Scholar
  69. Shih DQ, Targan SR (2009) Insights into IBD pathogenesis. Curr Gastroenterol Rep 11:473–480PubMedCrossRefGoogle Scholar
  70. Sperker B, Backman JT, Kroemer HK (1997) The role of beta-glucuronidase in drug disposition and drug targeting in humans. Clin Pharmacokinet 33:18–31PubMedCrossRefGoogle Scholar
  71. Speyer CL, Rancilio NJ, McClintock SD, Crawford JD, Gao H, Sarma JV, Ward PA (2005) Regulatory effects of estrogen on acute lung inflammation in mice. Am J Physiol Cell Physiol 288:C881–C890PubMedCrossRefGoogle Scholar
  72. Swedenborg E, Ruegg J, Makela S, Pongratz I (2009) Endocrine disruptive chemicals: mechanisms of action and involvement in metabolic disorders. J Mol Endocrinol 43:1–10PubMedCrossRefGoogle Scholar
  73. Takeyama J, Suzuki T, Inoue S, Kaneko C, Nagura H, Harada N, Sasano H (2001) Expression and cellular localization of estrogen receptors alpha and beta in the human fetus. J Clin Endocrinol Metab 86:2258–2262PubMedCrossRefGoogle Scholar
  74. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9:799–809PubMedCrossRefGoogle Scholar
  75. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139–177PubMedCrossRefGoogle Scholar
  76. Verdu EF, Deng Y, Bercik P, Collins SM (2002) Modulatory effects of estrogen in two murine models of experimental colitis. Am J Physiol Gastrointest Liver Physiol 283:G27–G36PubMedGoogle Scholar
  77. Wada-Hiraike O, Imamov O, Hiraike H, Hultenby K, Schwend T, Omoto Y, Warner M, Gustafsson JA (2006) Role of estrogen receptor beta in colonic epithelium. Proc Natl Acad Sci USA 103:2959–2964PubMedCrossRefGoogle Scholar
  78. Wagner CL, Taylor SN, Johnson D (2008) Host factors in amniotic fluid and breast milk that contribute to gut maturation. Clin Rev Allergy Immunol 34:191–204PubMedCrossRefGoogle Scholar
  79. Welshons WV, Nagel SC, vom Saal FS (2006) Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147(6 Suppl):S56–S69PubMedCrossRefGoogle Scholar
  80. WHO (2010) Joint FAO/WHO expert meeting to review toxicological and health aspects of bisphenol A, Ottawa, CanadaGoogle Scholar
  81. Wilson ME, Westberry JM, Prewitt AK (2008) Dynamic regulation of estrogen receptor-alpha gene expression in the brain: a role for promoter methylation? Front Neuroendocrinol 29:375–385PubMedCrossRefGoogle Scholar
  82. Yamada H, Furuta I, Kato EH, Kataoka S, Usuki Y, Kobashi G, Sata F, Kishi R, Fujimoto S (2002) Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod Toxicol 16:735–739PubMedCrossRefGoogle Scholar
  83. Yan H, Takamoto M, Sugane K (2008) Exposure to Bisphenol A prenatally or in adulthood promotes T(H)2 cytokine production associated with reduction of CD4CD25 regulatory T cells. Environ Health Perspect 116:514–519PubMedCrossRefGoogle Scholar
  84. Yen TH, Wright NA (2006) The gastrointestinal tract stem cell niche. Stem Cell Rev 2:203–212PubMedCrossRefGoogle Scholar
  85. Zalko D, Soto AM, Dolo L, Dorio C, Rathahao E, Debrauwer L, Faure R, Cravedi JP (2003) Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 111:309–319PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Viorica Braniste
    • 1
  • Marc Audebert
    • 2
  • Daniel Zalko
    • 2
  • Eric Houdeau
    • 3
    Email author
  1. 1.UMR 1054 Neuro-Gastroenteorolgy & NutritionToulouseFrance
  2. 2.UMR 1089 Xénobiotiques, INRA, ToxalimToulouseFrance
  3. 3.Neurogastroenterology & Nutrition Unit, UMR 1054Institut National de la Recherche Agronomique, ToxAlimToulouseFrance

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