Advertisement

Bisphenol S exposure affects gene expression related to intestinal glucose absorption and glucose metabolism in mice

  • Raja Rezg
  • Anne Abot
  • Bessem Mornagui
  • Claude Knauf
Research Article
  • 65 Downloads

Abstract

Bisphenol S, an industrial chemical, has raised concerns for both human and ecosystem health. Yet, health hazards posed by bisphenol S (BPS) exposure remain poorly studied. Compared to all tissues, the intestine and the liver are among the most affected by environmental endocrine disruptors. The aim of this study was to investigate the molecular effect of BPS on gene expression implicated in the control of glucose metabolism in the intestine (apelin and its receptor APJ, SGLT1, GLUT2) and in the liver (glycogenolysis and/or gluconeogenesis key enzymes (glucose-6-phosphatase (G6Pase) and phosphoenolpyruvate carboxykinase (PEPCK)) and pro-inflammatory cytokine expression (TNF-α and IL-1β)). BPS at 25, 50, and 100 μg/kg was administered to mice in water drink for 10 weeks. In the duodenum, BPS exposure reduces significantly mRNA expression of sodium glucose transporter 1 (SGLT1), glucose transporter 2 (GLUT2), apelin, and APJ mRNA. In the liver, BPS exposure increases the expression of G6Pase and PEPCK, but does not affect pro-inflammatory markers. These data suggest that alteration of apelinergic system and glucose transporters expression could contribute to a disruption of intestinal glucose absorption, and that BPS stimulates glycogenolysis and/or gluconeogenesis in the liver. Collectively, we reveal that BPS heightens the risk of metabolic syndrome.

Keywords

Bisphenol S Health hazards Glucose transporters (SGLT1/GLUT2) Apelinergic system Intestinal glucose absorption 

Notes

Acknowledgements

This work was supported by the Tunisian Ministry of Higher Education and Scientific Research. We are grateful to Institut Français de Tunisie (IFT SSHN2015) for financial support. We thank particularly Dr Jalloul Bouajila from Faculty of Pharmacy of Toulouse (France) for technical assistance.

Compliance with ethical standards

Animals were treated in the respect of ethic and deontology, and all the procedure was accorded with Guidelines for Ethical Conduct in the Care and Use of Animals.

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG (2002) Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32:435–443CrossRefGoogle Scholar
  2. Bertrand C, Valet P, Castan-Laurell I (2015) Apelin and energy metabolism. Front Physiol 6:115CrossRefGoogle Scholar
  3. Chaves-Almagro C, Castan-Laurell I, Dray C, Knauf C, Valet P, Masri B (2015) Apelin receptors: from signaling to antidiabetic strategy. Eur J Pharmacol 763:149–159CrossRefGoogle Scholar
  4. Chen D, Kannan K, Tan H, Zheng Z, Feng YL, Wu Y, Widelka M (2016) Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity-a review. Environ Sci Technol 50:5438–5453CrossRefGoogle Scholar
  5. Chu J, Zhang H, Huang X, Lin Y, Shen T, Chen B, Man Y, Wang S, Li J (2013) Apelin ameliorates TNF-alpha-induced reduction of glycogen synthesis in the hepatocytes through G protein-coupled receptor APJ. PLoS One 8:e57231CrossRefGoogle Scholar
  6. Cryer PE (2008) Hypoglycemia: still the limiting factor in the glycemic management of diabetes. Endocr Pract 14:750–756CrossRefGoogle Scholar
  7. Dray C, Knauf C, Daviaud D, Waget A, Boucher J, Buleon M, Cani PD, Attane C, Guigne C, Carpene C, Burcelin R, Castan-Laurell I, Valet P (2008) Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 8:437–445CrossRefGoogle Scholar
  8. Dray C, Sakar Y, Vinel C, Daviaud D, Masri B, Garrigues L, Wanecq E, Galvani S, Negre-Salvayre A, Barak LS, Monsarrat B, Burlet-Schiltz O, Valet P, Castan-Laurell I, Ducroc R (2013) The intestinal glucose-apelin cycle controls carbohydrate absorption in mice. Gastroenterology 144:771–780CrossRefGoogle Scholar
  9. Galyon KD, Farshidi F, Han G, Ross MG, Desai M, Jellyman JK (2017) Maternal bisphenol A exposure alters rat offspring hepatic and skeletal muscle insulin signaling protein abundance. Am J Obstet Gynecol 216:290.e1–290.e9CrossRefGoogle Scholar
  10. Helies-Toussaint C, Peyre L, Costanzo C, Chagnon MC, Rahmani R (2014) Is bisphenol S a safe substitute for bisphenol A in terms of metabolic function? An in vitro study. Toxicol Appl Pharmacol 280:224–235CrossRefGoogle Scholar
  11. Ivry Del Moral L, Le Corre L, Poirier H, Niot I, Truntzer T, Merlin JF, Rouimi P, Besnard P, Rahmani R, Chagnon MC (2016) Obesogen effects after perinatal exposure of 4,4′-sulfonyldiphenol (Bisphenol S) in C57BL/6 mice. Toxicology 357–358:11–20CrossRefGoogle Scholar
  12. Kataria A, Levine D, Wertenteil S, Vento S, Xue J, Rajendiran K, Kannan K, Thurman JM, Morrison D, Brody R, Urbina E, Attina T, Trasande L, Trachtman H (2017) Exposure to bisphenols and phthalates and association with oxidant stress, insulin resistance, and endothelial dysfunction in children. Pediatr Res 81:857–864CrossRefGoogle Scholar
  13. Kinch CD, Ibhazehiebo K, Jeong JH, Habibi HR, Kurrasch DM (2015) Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. Proc Natl Acad Sci U S A 112:1475–1480CrossRefGoogle Scholar
  14. Ladeiras-Lopes R, Ferreira-Martins J, Leite-Moreira AF (2008) The apelinergic system: the role played in human physiology and pathology and potential therapeutic applications. Arq Bras Cardiol 90:343–349CrossRefGoogle Scholar
  15. Liao C, Kannan K (2014) A survey of alkylphenols, bisphenols, and triclosan in personal care products from China and the United States. Arch Environ Contam Toxicol 67:50–59CrossRefGoogle Scholar
  16. Liao C, Liu F, Alomirah H, Loi VD, Mohd MA, Moon HB, Nakata H, Kannan K (2012a) Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ Sci Technol 46:6860–6866CrossRefGoogle Scholar
  17. Liao C, Liu F, Guo Y, Moon HB, Nakata H, Wu Q, Kannan K (2012b) Occurrence of eight bisphenol analogues in indoor dust from the United States and several Asian countries: implications for human exposure. Environ Sci Technol 46:9138–9145CrossRefGoogle Scholar
  18. Liao C, Liu F, Kannan K (2012c) Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol a residues. Environ Sci Technol 46:6515–6522CrossRefGoogle Scholar
  19. O'Carroll AM, Lolait SJ, Harris LE, Pope GR (2013) The apelin receptor APJ: journey from an orphan to a multifaceted regulator of homeostasis. J Endocrinol 219:R13–R35CrossRefGoogle Scholar
  20. O'Harte FPM, Parthsarathy V, Hogg C, Flatt PR (2018) Long-term treatment with acylated analogues of apelin-13 amide ameliorates diabetes and improves lipid profile of high-fat fed mice. PLoS One 13:e0202350CrossRefGoogle Scholar
  21. Rajapakse N, Silva E, Kortenkamp A (2002) Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ Health Perspect 110:917–921CrossRefGoogle Scholar
  22. Rezg R, Mornagui B, El-Fazaa S, Gharbi N (2010) Organophosphorus pesticides as food chain contaminants and type 2 diabetes: a review. Trends Food Sci Technol 21:345–357CrossRefGoogle Scholar
  23. Rezg R, El-Fazaa S, Gharbi N, Mornagui B (2014) Bisphenol A and human chronic diseases: current evidences, possible mechanisms, and future perspectives. Environ Int 64:83–90CrossRefGoogle Scholar
  24. Rezg R, Abot A, Mornagui B, Aydi S, Knauf C (2018) Effects of bisphenol S on hypothalamic neuropeptides regulating feeding behavior and apelin/APJ system in mice. Ecotoxicol Environ Saf 161:459–466CrossRefGoogle Scholar
  25. Rizza RA, Cryer PE, Gerich JE (1979) Role of glucagon, catecholamines, and growth hormone in human glucose counterregulation. Effects of somatostatin and combined alpha- and beta-adrenergic blockade on plasma glucose recovery and glucose flux rates after insulin-induced hypoglycemia. J Clin Invest 64:62–71CrossRefGoogle Scholar
  26. Rochester JR, Bolden AL (2015) Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect 123:643–650CrossRefGoogle Scholar
  27. Rosenfeld CS (2017) Neuroendocrine disruption in animal models due to exposure to bisphenol A analogues. Front Neuroendocrinol 47:123–133CrossRefGoogle Scholar
  28. Rosenmai AK, Dybdahl M, Pedersen M, Alice van Vugt-Lussenburg BM, Wedebye EB, Taxvig C, Vinggaard AM (2014) Are structural analogues to bisphenol a safe alternatives? Toxicol Sci 139:35–47CrossRefGoogle Scholar
  29. Scholze J, Alegria E, Ferri C, Langham S, Stevens W, Jeffries D, Uhl-Hochgraeber K (2010) Epidemiological and economic burden of metabolic syndrome and its consequences in patients with hypertension in Germany, Spain and Italy; a prevalence-based model. BMC Public Health 10:529CrossRefGoogle Scholar
  30. Sprague JE, Arbelaez AM (2011) Glucose counterregulatory responses to hypoglycemia. Pediatr Endocrinol Rev 9:463–473 quiz 474–5Google Scholar
  31. Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX, Kawamata Y, Fukusumi S, Hinuma S, Kitada C, Kurokawa T, Onda H, Fujino M (1998) Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 251:471–476CrossRefGoogle Scholar
  32. Whiting DR, Guariguata L, Weil C, Shaw J (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94:311–321CrossRefGoogle Scholar
  33. Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89:3–9CrossRefGoogle Scholar
  34. Xu J, Huang G, Guo TL (2016) Developmental bisphenol a exposure modulates immune-related diseases. Toxics 4:1–23Google Scholar
  35. Yu X, Xue J, Yao H, Wu Q, Venkatesan AK, Halden RU, Kannan K (2015) Occurrence and estrogenic potency of eight bisphenol analogs in sewage sludge from the U.S. EPA targeted national sewage sludge survey. J Hazard Mater 299:733–739CrossRefGoogle Scholar
  36. Yue P, Jin H, Aillaud M, Deng AC, Azuma J, Asagami T, Kundu RK, Reaven GM, Quertermous T, Tsao PS (2010) Apelin is necessary for the maintenance of insulin sensitivity. Am J Physiol Endocrinol Metab 298:E59–E67CrossRefGoogle Scholar
  37. Zhao C, Tang Z, Yan J, Fang J, Wang H, Cai Z (2017) Bisphenol S exposure modulate macrophage phenotype as defined by cytokines profiling, global metabolomics and lipidomics analysis. Sci Total Environ 592:357–365CrossRefGoogle Scholar
  38. Zhao F, Jiang G, Wei P, Wang H, Ru S (2018) Bisphenol S exposure impairs glucose homeostasis in male zebrafish (Danio rerio). Ecotoxicol Environ Saf 147:794–802CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Raja Rezg
    • 1
  • Anne Abot
    • 2
    • 3
  • Bessem Mornagui
    • 4
  • Claude Knauf
    • 2
    • 3
  1. 1.High Institute of Biotechnology of Monastir, Laboratory of Bioresources: Integrative Biology and Valorisation BIOLIVALUniversity of MonastirMonastir 5000Tunisia
  2. 2.Institut National de la Santé et de la Recherche Médicale (INSERM), U1220Université Paul Sabatier, UPS, Institut de Recherche en Santé Digestive et Nutrition (IRSD), CHU PurpanToulouse Cedex 3France
  3. 3.NeuroMicrobiota, European Associated Laboratory (EAL) INSERM/UCLToulouseFrance
  4. 4.Faculty of Sciences of Gabes, Laboratoire de Biodiversité et valorisation des bioressources des zones arides, LR18ES36University of GabesGabes 6072Tunisia

Personalised recommendations