Di(2-ethylhexyl) phthalate-induced apoptosis in rat INS-1 cells is dependent on activation of endoplasmic reticulum stress and suppression of antioxidant protection

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 3, 2015, Pages 581-594

  Sun, Xia ^a   Lin, Yi ^a   Huang, Qiansheng ^a   Shi, Junpeng ^a   Qiu, Ling ^a   Kang, Mei ^a   Chen, Yajie ^a   Fang, Chao ^a   Ye, Ting ^a   Dong, Sijun ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Apoptosis; Di(2 ethylhexyl) phthalate; Endoplasmic reticulum stress; Oxidative damage; cells

Indexed keywords

EUKARYOTA; RATTUS;

ACTIVATING TRANSCRIPTION FACTOR 4; ANTIOXIDANT; ATF4 PROTEIN, RAT; CALCIUM; DDIT3 PROTEIN, RAT; GLUCOSE; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; HSPA5 PROTEIN, RAT; INITIATION FACTOR 2; INSULIN; MEMBRANE PROTEIN; NFE2L2 PROTEIN, RAT; PERK KINASE; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PROTEIN KINASE R; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; APOPTOSIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; RAT; SECRETION (PROCESS);

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CALCIUM; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DIETHYLHEXYL PHTHALATE; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; GLUCOSE; HEAT-SHOCK PROTEINS; INSULIN; MEMBRANE GLYCOPROTEINS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTOR CHOP;

EID: 84923292535     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12409     Document Type: Article

References (56)

1. Kelley KE, Hernández-Díaz S, Chaplin EL, et al. Identification of phthalates in medications and dietary supplement formulations in the United States and Canada. Environ Health Perspect. 2012; 120: 379-84.
2. Schettler T. Human exposure to phthalates via consumer products. Int J Androl. 2006; 29: 134-9.
3. CDC. Fourth national report on human exposure to environmental chemicals, Updated Tables. Available at http://www.cdc.gov/exposurereport/pdf/FourthReport_UpdatedTables_Sep2012.pdf. 2012.
4. Saravanabhavan G, Guay M, Langlois É, et al. Biomonitoring of phthalate metabolites in the Canadian population through the Canadian Health Measures Survey (2007-2009). Int J Hyg Environ Health. 2013; 216: 652-61.
5. Stahlhut RW, van Wijngaarden E, Dye TD, et al. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult US males. Environ Health Perspect. 2007; 115: 876-82.
6. Svensson K, Hernández-Ramírez RU, Burguete-García A, et al. Phthalate exposure associated with self-reported diabetes among Mexican women. Environ Res. 2011; 111: 792-6.
7. James-Todd T, Stahlhut R, Meeker JD, et al. Urinary phthalate metabolite concentrations and diabetes among women in the National Health and Nutrition Examination Survey (NHANES) 2001-2008. Environ Health Perspect. 2012; 120: 1307-13.
8. Selvaraj J, Balasubramanian K, Pei F, et al. Phthalate is associated with insulin resistance in adipose tissue of male rat: role of antioxidant vitamins. J Cell Biochem. 2013; 114: fm i-fm iv.
9. Srinivasan C, Khan AI, Balaji V, et al. Diethyl hexyl phthalate-induced changes in insulin signaling molecules and the protective role of antioxidant vitamins in gastrocnemius muscle of adult male rat. Toxicol Appl Pharmacol. 2011; 257: 155-64.
10. Butler AE, Janson J, Bonner-Weir S, et al. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003; 52: 102-10.
11. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans. 2008; 36: 343-7.
12. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radical Biol Med. 1996; 20: 463-6.
13. Dzhekova-Stojkova S, Bogdanska J, Stojkova Z. Peroxisome proliferators: their biological and toxicological effects. Clin Chem Lab Med. 2001; 39: 468-74.
14. Ferguson KK, Loch-Caruso R, Meeker JD. Exploration of oxidative stress and inflammatory markers in relation to urinary phthalate metabolites: NHANES 1999-2006. Environ Sci Technol. 2012; 46: 477-85.
15. Giral P, Ratziu V, Couvert P, et al. Plasma bilirubin and gamma-glutamyltransferase activity are inversely related in dyslipidemic patients with metabolic syndrome: relevance to oxidative stress. Atherosclerosis. 2010; 210: 607-13.
16. Erkekoglu P, Rachidi W, Yuzugullu OG, et al. Evaluation of cytotoxicity and oxidative DNA damaging effects of di (2-ethylhexyl)-phthalate (DEHP) and mono (2-ethylhexyl)-phthalate (MEHP) on MA-10 Leydig cells and protection by selenium. Toxicol Appl Pharmacol. 2010; 248: 52-62.
17. Wang W, Craig ZR, Basavarajappa MS, et al. Di (2-ethylhexyl) phthalate inhibits growth of mouse ovarian antral follicles through an oxidative stress pathway. Toxicol Appl Pharmacol. 2012; 258: 288-95.
18. Bhandary B, Marahatta A, Kim H-R, et al. An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. Int J Mol Sci. 2012; 14: 434-56.
19. Guan L, Han B, Li Z, et al. Sodium selenite induces apoptosis by ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in human acute promyelocytic leukemia NB4 cells. Apoptosis. 2009; 14: 218-25.
20. Fonseca SG, Gromada J, Urano F. Endoplasmic reticulum stress and pancreatic β-cell death. Trends Endocrinol Metab. 2011; 22: 266-74.
21. Lin Y, Wei J, Li Y, et al. Developmental exposure to di (2-ethylhexyl) phthalate impairs endocrine pancreas and leads to long-term adverse effects on glucose homeostasis in the rat. Am J Physiol Endocrinol Metabol. 2011; 301: E527-38.
22. Tetz LM, Cheng A, Korte C, et al. Mono-2-ethylhexyl phthalate induces oxidative stress responses in human placental cells in vitro. Toxicol Appl Pharmacol. 2013; 268: 47-54.
23. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. 1991; 266: 17067-71.
24. Asfari M, Janjic D, Meda P, et al. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology. 1992; 130: 167-78.
25. Merglen A, Theander S, Rubi B, et al. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology. 2004; 145: 667-78.
26. Janjic D, Maechler P, Sekine N, et al. Free radical modulation of insulin release in INS-1 cells exposed to alloxan. Biochem Pharmacol. 1999; 57: 639-48.
27. Hohmeier HE, Newgard CB. Cell lines derived from pancreatic islets. Mol Cell Endocrinol. 2004; 228: 121-8.
28. Xu D, Deng X, Fang E, et al. Determination of 23 phthalic acid esters in food by liquid chromatography tandem mass spectrometry. J Chromatogr. 2014; 1324: 49-56.
29. Schecter A, Lorber M, Guo Y, et al. Phthalate concentrations and dietary exposure from food purchased in New York State. Environ Health Perspect. 2013; 121: 473.
30. NTP-CERHR. NTP-CHRHR (National Toxicology Program, Center for the Evaluation of Risks to Human Reproduction) expert panel report on di(2-ethylhexyl) phthalate. Alexandria, VA: Center for the Evaluation of Risks to Human Reproduction, US Department of Health and Human Services; 2003. Available at http://cerhr.niehs.gov/news/index.html. Accessed March 27.
31. Inoue K, Kawaguchi M, Yamanaka R, et al. Evaluation and analysis of exposure levels of di (2-ethylhexyl) phthalate from blood bags. Clin Chim Acta. 2005; 358: 159-66.
32. Commission E. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR), Opinion on The appropriateness of existing methodologies to assess the potential risks associated with engineered and adventitious products of nanotechnologies. 2008.
33. Koch HM, Preuss R, Angerer JD. Di (2-ethylhexyl) phthalate (DEHP): human metabolism and internal exposure-an update and latest results1. Int J Androl. 2006; 29: 155-65.
34. Ambruosi B, Uranio MF, Sardanelli AM, et al. In vitro acute exposure to DEHP affects oocyte meiotic maturation, energy and oxidative stress parameters in a large animal model. PLoS ONE. 2011; 6: e27452.
35. Kristensen DM, Skalkam ML, Audouze K, et al. Many putative endocrine disruptors inhibit prostaglandin synthesis. Environ Health Perspect. 2011; 119: 534-41.
36. Wittassek M, Angerer J. Phthalates: metabolism and exposure. Int J Androl. 2008; 31: 131-8.
37. Ghosh J, Das J, Manna P, et al. Hepatotoxicity of di-(2-ethylhexyl) phthalate is attributed to calcium aggravation, ROS-mediated mitochondrial depolarization, and ERK/NF-κB pathway activation. Free Radical Biol Med. 2010; 49: 1779-91.
38. Chen X, Qin Q, Zhang W, et al. Activation of the PI3K-AKT-mTOR signaling pathway promotes DEHP-induced Hep3B cell proliferation. Food Chem Toxicol. 2013; 59: 325-33.
39. Zhang DD. Mechanistic studies of the Nrf2-Keap1 signaling pathway*. Drug Metab Rev. 2006; 38: 769-89.
40. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47: 89-116.
41. Pi J, Zhang Q, Fu J, et al. ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell function. Toxicol Appl Pharmacol. 2010; 244: 77-83.
42. Hansen HG, Schmidt JD, Søltoft CL, et al. Hyperactivity of the Ero1α oxidase elicits endoplasmic reticulum stress but no broad antioxidant response. J Biol Chem. 2012; 287: 39513-23.
43. Harding HP, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. 2003; 11: 619-33.
44. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol. 2006; 38: 317-32.
45. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998; 12: 982-95.
46. Marciniak SJ, Yun CY, Oyadomari S, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004; 18: 3066-77.
47. Itoh K, Mimura J, Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid Redox Signal. 2010; 13: 1665-78.
48. Novoa I, Zeng H, Harding HP, et al. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J Cell Biol. 2001; 153: 1011-22.
49. Morse E, Schroth J, You Y-H, et al. TRB3 is stimulated in diabetic kidneys, regulated by the ER stress marker CHOP, and is a suppressor of podocyte MCP-1. Am J Physiol Renal Physiol. 2010; 299: F965-72.
50. Qian B, Wang H, Men X, et al. TRIB3 is implicated in glucotoxicity-and endoplasmic reticulum-stress-induced beta-cell apoptosis. J Endocrinol. 2008; 199: 407-16.
51. 2+ sequestration in diabetic mouse islets of Langerhans. J Biol Chem. 1994; 269: 18279-82.
52. 2+, leading to induction of endoplasmic reticulum stress in pancreatic β-cells. Diabetes. 2005; 54: 452-61.
53. Kono T, Ahn G, Moss DR, et al. PPAR-γ activation restores pancreatic islet SERCA2 levels and prevents β-cell dysfunction under conditions of hyperglycemic and cytokine stress. Mol Endocrinol. 2012; 26: 257-71.
54. 2+ homeostasis in pancreatic β-cells. Diabetes. 2002; 51: 3245-53.
55. Carafoli E. Membrane transport of calcium: an overview. Methods Enzymol. 1988; 157: 3-11.
56. Blaustein MP, Lederer WJ. Sodium/calcium exchange: its physiological implications. Physiol Rev. 1999; 79: 763-854.