Bisphenol A (BPA) aggravates multiple low-dose streptozotocin-induced type 1 diabetes in C57BL/6 mice

Journal of Immunotoxicology

Volumn 14, Issue 1, 2017, Pages 160-168

  Cetkovic Cvrlje, Marina ^a   Thinamany, Sinduja ^a   Bruner, Kylie A ^a  

^a ST CLOUD STATE UNIVERSITY   (United States)

Author keywords

Bisphenol A (BPA); Multiple low dose streptozotocin (MLDSTZ) induced autoimmune mouse T1D; T cells; Type 1 diabetes (T1D)

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; GAMMA INTERFERON; GLUCOSE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; AUTACOID; BENZHYDRYL DERIVATIVE; CYTOKINE; PHENOL DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CELL COUNT; CELL POPULATION; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; GLUCOSE BLOOD LEVEL; GLUCOSE LEVEL; IMMUNOMODULATION; IMMUNOPHENOTYPING; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; SPLENIC T CELL; T LYMPHOCYTE SUBPOPULATION; AIR POLLUTANT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; DISEASE EXACERBATION; EXPERIMENTAL DIABETES MELLITUS; HUMAN; IMMUNOLOGY; METABOLISM; PANCREAS ISLET BETA CELL; PATHOLOGY; T LYMPHOCYTE; TOXICITY;

AIR POLLUTANTS, OCCUPATIONAL; ANIMALS; BENZHYDRYL COMPOUNDS; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION MEDIATORS; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; PHENOLS; T-LYMPHOCYTES;

EID: 85040726056     PISSN: 1547691X     EISSN: 15476901     Source Type: Journal    
DOI: 10.1080/1547691X.2017.1334722     Document Type: Article

References (53)

1. Acconcia F, Pallottini V, Marino M. 2015. Molecular mechanisms of action of BPA. Dose-Response. 13:1-9
2. Alizadeh M, Ota F, Hosoi K, Kato M, Sakai T, Satter M. 2006. Altered allergic cytokine and antibody response in mice treated with bisphenol A. J Med Invest. 53:70-80
3. Bodin J, Bølling A, Becher R, Kuper F, Løvik M, Nygaard U. 2014. Transmaternal bisphenol A exposure accelerates diabetes Type 1 development in NOD mice. Toxicol Sci. 137:311-323
4. Bodin J, Bølling A, Samuelsen M, Becher R, Løvik M, Nygaard U. 2013. Long-term bisphenol A exposure accelerates insulitis development in diabetes-prone NOD mice. Immunopharmacol Immunotoxicol. 35:349-358
5. Bodin J, Stene L, Nygaard U. 2015. Can exposure to environmental chemicals increase the risk of diabetes Type 1 development? Biomed Res Int. 2015:208947
6. Calafat A, Kuklenyik Z, Reidy J, Caudill S, Ekong J, Needham L. 2005. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect. 113:391-395
7. Calafat A, Ye X, Wong L, Reidy J, Needham L. 2008. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004 Environ Health Perspect. 116:39-44
8. Canesi L, Betti M, Lorusso L, Ciacci C, Gallo G. 2005. 'In vivo' effects of bisphenol A in Mytilus hemocytes: Modulation of kinase-mediated signalling pathways. Aquat Toxicol. 71:73-84
9. Carwile J, Michels K. 2011. Urinary bisphenol A and obesity: NHANES 2003-2006 Environ Res. 111:825-830.
10. [USFDA] Center for Food Safety and Applied Nutrition. 2010. Exposure to bisphenol A for infants, toddlers and adults from the consumption of infant formula, toddler food and adult (Canned) food; [accessed 2017 Mar 8]. http://www.regulations.gov/#!documentDetail;D=FDA-2010-N-0100-0009;oldLink=false.
11. Cetkovic-Cvrlje M, Dragt A, Vassiley A, Liu X, Uckun F. 2003 Targeting JAK3 with JANEX-1 for prevention of autoimmune Type 1 diabetes in NOD mice. Clin Immunol. 106:213-225.
12. Cetkovic-Cvrlje M, Gerling I, Muir A, Atkinson M, Elliot J, Leiter E. 1997. Retardation or acceleration of diabetes in NOD/Lt mice mediated by intra-thymic administration of candidate b-cell antigens. Diabetes. 46:1975-1982.
13. Cetkovic-Cvrlje M, Olson M, Ghate K. 2012 Targeting Janus tyrosine kinase 3 (JAK3) with an inhibitor induces secretion of TGF-b by CD4+ T-cells. Cell Mol Immunol. 9:350-360.
14. Cetkovic-Cvrlje M, Olson M, Schindler B, Gong H. 2016. Exposure to DDT metabolite p,p0-DDE increases autoimmune Type 1 diabetes incidence in NOD mouse model. J Immuno Toxicol. 13:108-118.
15. Cetkovic-Cvrlje M, Uckun F. 2004. Dual targeting of Bruton’s tyrosine kinase and JAK3 with rationally designed inhibitors prevents graft-vs.-host disease (GVHD) in a murine allogeneic bone marrow transplantation model. Br J Haematol. 126:821-827.
16. Cetkovic-Cvrlje M, Uckun F. 2005. Effect of targeted disruption of signal transducer and activator of transcription (Stat)4 and Stat6 genes on the autoimmune diabetes development induced by multiple low doses of streptozotocin. Clin Immunol. 114:299-306
17. Chailurkit L, Aekplakorn W, Ongphiphadhanakul B. 2014. The relationship between circulating estradiol and thyroid autoimmunity in males. Eur J Endocrinol. 170:63-67
18. Dabelea D, Mayer-Davis E, Saydah S, Imperatore G, Linder B, Divers J, Bell R, Badaru A, Talton J, Crume T, et al. 2014. Prevalence of Type 1 and Type 2 diabetes among children and adolescents from 2001 to 2009. JAMA 311:1778-1786
19. Delclos K, Camacho L, Lewis S, Vanlandingham M, Latendresse J, Olson G, Davis J, Patton R, Gamboa da Costa G, Woodling K, et al. 2014. Toxicity evaluation of bisphenol A administered by gavage to Sprague Dawley rats from gestation day 6 through postnatal day 90 Toxicol Sci. 139:174-197
20. Dietert R, DeWitt J, Germolec D, Zelikoff J. 2010. Breaking patterns of environmentally influenced disease for health risk reduction: Immune perspectives. Environ Health Perspect. 118:1091-1099.
21. [EFSA] European Food Safety Authority. 2006. Opinion of scientific panel on food additives, flavorings, processing aids and materials in contact with food; on request from commission related to 2,2-bis(4-hydroxyphenyl)propane (bisphenol A). EFSA J. 428:13-75.
22. EFSA. 2015. Scientific opinion on bisphenol A (2015); [accessed 2017 Mar 8]. http://www.efsa.europa.eu/sites/default/files/corporate_publications/files/factsheetbpa150121.pdf.
23. [FDA] Food and Drug Administration. 2008. Draft assessment of bisphenol A for use in food contact applications. Silver Spring (MD): US Food and Drug Administration.
24. Goto M, Takano-Ishikawa Y, Ono H, Yoshida M, Yamaki K, Shinmoto H. 2007. Orally-administered bisphenol A disturbed antigen-specific immune responses in naïve condition. Biosci Biotechnol Biochem. 7:2136-2143
25. Heindel J, Newbold R, Bucher J, Camacho L, Delclos K, Sherry M, Vanlandingham M, Mona I. 2015. NIEHS/FDA CLARITY-BPA research program update. Reprod Toxicol. 58:33-44.
26. Karpuzoglu-Sahin E, Hissong B, Ansar Ahmed S. 2001. IFNc levels are upregulated by 17-b-estradiol and diethylstilbestrol. J Reprod Immunol. 52:113-127
27. Kharrazian D. 2014. The potential roles of bisphenol A (BPA) pathogenesis in autoimmunity. Autoimmune Dis. 2014:743616
28. Knip M, Simell O. 2012. Environmental triggers of Type 1 diabetes. Cold Spring Harb Perspect Med. 2:a007690
29. Kuiper J, Moran M, Cetkovic-Cvrlje M. 2016. Exposure to polychlorinated biphenyl-153 decreases incidence of autoimmune Type 1 diabetes in nonobese diabetic mice. J Immunotoxicol. 13:850-860.
30. LaKind J, Goodman M, Naiman D. 2012. Use of NHANES data to link chemical exposures to chronic diseases: A cautionary tale. PLoS One. 7:e51086
31. Lee G, Goosens K. 2015. Sampling blood from the lateral tail vein of rat. J Vis Exp. 99:e52766
32. Lee M, Chung S, Kang B, Park J, Lee C, Hwang S, Kim T. 2003. Enhanced interleukin-4 production in CD4+ T-cells and elevated immunoglobulin E levels in antigen-primed mice by bisphenol A and nonylphenol, endocrine disruptors: Involvement of nuclear factor-AT and Ca2+. Immunology. 109:76-86
33. Like A, Rossini A. 1976. Streptozotocin-induced pancreatic insulitis: New model of diabetes mellitus. Science. 193:415
34. Lin Y, Sun X, Qiu L, Huang Q, Fang C, Ye T, Wei J. 2013. Exposure to bisphenol A induces dysfunction of insulin secretion and apoptosis through the damage of mitochondria in rat insulinoma (INS-1) cells. Cell Death Dis. 4:e460
35. Melzer D, Rice N, Lewis C, Henley W, Galloway T. 2010. Association of urinary bisphenol A concentration with heart disease: Evidence from NHANES 2003/06. PLoS One. 5:e8673
36. Muller A, Schott-Ohly P, Dohle C, Gleichmann H. 2002. Differential regulation of TH1-type and TH2-type cytokine profiles in pancreatic islets of C57BL/6 and BALB/c mice by multiple low doses of streptozotocin. Immunobiology. 205:35-50.
37. Sakowicz-Burkiewicz M, Kocbuch K, Grden M, Szutowicz A, Pawelczyk T. 2006. Diabetes-induced decrease of adenosine kinase expression impairs the proliferation potential of diabetic rat T-lymphocytes. Immunology. 118:402-412
38. Shelby M. 2008. NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. NTP CERHR MON. 22:1-64
39. Shoda L, Young D, Ramanujan S, Whiting C, Atkinson M, Bluestone J, Eisenbarth G, Mathis D, Rossini A, Campbell S, et al. 2005. A comprehensive review of interventions in the NOD mouse and implications for translation. Immunity. 23:115-126
40. Sia C. 2005. Imbalance in TH cell polarization and its relevance in Type 1 diabetes mellitus. Rev Diabet Stud. 2:182-186
41. Silver M, O’Neill M, Sowers M, Park S. 2011. Urinary bisphenol A and Type-2 diabetes in U.S. adults: Data from NHANES 2003-2008. PLoS One. 6:e26868
42. Sowlat M, Lotfi S, Yunesian M, Ahmadkhaniha R, Rastkari N. 2016. The association between bisphenol A exposure and Type-2 diabetes: A world systematic review. Environ Sci Pollut Res Int. 23: 21125-21140
43. Spanier A, Kahn R, Kunselman A, Hornung R, Xu Y, Calafat A, Lanphear B. 2012. Pre-natal exposure to bisphenol A and child wheeze from birth to 3-years-of-age. Environ Health Perspect. 120:916-920
44. Taylor K, Novak R, Anderson H, Birnbaum L, Blystone C, DeVito M, Jacobs D, Kohrle J, Lee D, Rylander L, et al. 2013. Evaluation of the association between persistent organic pollutants (POPs) and diabetes in epidemiological studies: A national toxicology program workshop review. Environ Health Perspect. 121:774-783
45. Teppala S, Madhavan S, Shankar A. 2012Bisphenol A and metabolic syndrome: Results from NHANES. Int J Endocrinol. 2012:598180.
46. ter Veld M, Zawadzka E, van den Berg J, van den Saag P, Rietjens I, Murk A. 2008. Food-associated estrogenic compounds induce estrogen receptormediated luciferase gene expression in transgenic male mice. Chem Biol Interact. 174:126-133.
47. [WHO] World Health Organization. 2010 Joint FAO/WHO expert meeting to review toxicological and health aspects of bisphenol A: Summary report. Ottawa, CA: World Health Organization [accessed 2017 Mar 8]. http://www.who.int/foodsafety/chem/chemicals/BPASummary2010.pdf.
48. Wildner G, Kaufmann U. 2013. What causes relapses of autoimmune diseases? The etiological role of autoreactive T-cells. Autoimmun Rev. 12:1070-1075
49. Willhite C, Ball G, McLellan C. 2008. Derivation of a bisphenol A oral reference dose (RfD) and drinking-water equivalent concentration. J Toxicol Environ Health. 11:69-146
50. Yan H, Takamoto M. Sugane 2008. Exposure to bisphenol A prenatally or in adulthood promotes TH2 cytokine production associated with reduction of CD4CD25 regulatory T cells. Environ Health Perspect. 116:514-519
51. Yoshino S, Yamaki K, Li X, Sai T, Yanagisawa R, Takano H, Taneda S, Hayashi H, Mori Y. 2004. Prenatal exposure to bisphenol A up-regulates immune responses, including T-helper 1 and T-helper 2 responses, in mice. Immunology. 112:489-495
52. Yoshino S, Yamaki K, Yanagisawa R, Takano H, Hayashi H, Mori Y. 2003. Effects of bisphenol A on antigen-specific antibody production, proliferative responses of lymphoid cells, and TH1 and TH2 immune responses in mice. Br J Pharmacol. 138:1271-1276
53. Youn J, Park H, Lee J, Jung I, Choi K, Kim K, Cho K. 2002. Evaluation of the immune response following exposure of mice to bisphenol A: Induction of TH1 cytokine and prolactin by BPA exposure in the mouse spleen cells. Arch Pharm Res. 25:946-953