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.
Similar content being viewed by others
References
Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG (2002) Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32:435–443
Bertrand C, Valet P, Castan-Laurell I (2015) Apelin and energy metabolism. Front Physiol 6:115
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 763:149–159
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 50:5438–5453
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:e57231
Cryer PE (2008) Hypoglycemia: still the limiting factor in the glycemic management of diabetes. Endocr Pract 14:750–756
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 8:437–445
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 144:771–780
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.e9
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 280:224–235
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 357–358:11–20
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 81:857–864
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 112:1475–1480
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 90:343–349
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 67:50–59
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 46:6860–6866
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 46:9138–9145
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 46:6515–6522
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–R35
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:e0202350
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 110:917–921
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 21:345–357
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 64:83–90
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 161:459–466
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 64:62–71
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 123:643–650
Rosenfeld CS (2017) Neuroendocrine disruption in animal models due to exposure to bisphenol A analogues. Front Neuroendocrinol 47:123–133
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 139:35–47
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 10:529
Sprague JE, Arbelaez AM (2011) Glucose counterregulatory responses to hypoglycemia. Pediatr Endocrinol Rev 9:463–473 quiz 474–5
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 251:471–476
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 94:311–321
Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89:3–9
Xu J, Huang G, Guo TL (2016) Developmental bisphenol a exposure modulates immune-related diseases. Toxics 4:1–23
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 299:733–739
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–E67
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 592:357–365
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 147:794–802
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Responsible editor: Philippe Garrigues
Highlights:
• BPS exposure disturbed gene expression of intestinal glucose absorption in male mice.
• BPS exposure impairs hepatic glycogenolysis and/or gluconeogenesis enzymes gene expression.
• Postnatal exposure to bisphenol S at low doses can present a risk factor of metabolic syndrome.
Rights and permissions
About this article
Cite this article
Rezg, R., Abot, A., Mornagui, B. et al. Bisphenol S exposure affects gene expression related to intestinal glucose absorption and glucose metabolism in mice. Environ Sci Pollut Res 26, 3636–3642 (2019). https://doi.org/10.1007/s11356-018-3823-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-3823-z