Diethyl hexyl phthalate-induced changes in insulin signaling molecules and the protective role of antioxidant vitamins in gastrocnemius muscle of adult male rat

Toxicology and Applied Pharmacology

Volumn 257, Issue 2, 2011, Pages 155-164

  Srinivasan, Chinnapaiyan ^a   Khan, Adam Ismail ^a   Balaji, Venkataraman ^a   Selvaraj, Jayaraman ^a   Balasubramanian, Karundevi ^a  

^a UNIVERSITY OF MADRAS   (India)

Author keywords

DEHP; GLUT4; Insulin; Skeletal muscle; Vitamin C; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; GLUCOSE; GLUCOSE TRANSPORTER 4; HYDROGEN PEROXIDE; HYDROXYL RADICAL; INSULIN; INSULIN RECEPTOR; OLIVE OIL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; GLUCOSE BLOOD LEVEL; GLUCOSE OXIDATION; GLUCOSE TRANSPORT; LIPID PEROXIDATION; MALE; MEMBRANE DAMAGE; NONHUMAN; RAT; SIGNAL TRANSDUCTION; STOMACH INTUBATION; TREATMENT DURATION;

AGE FACTORS; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BLOOD GLUCOSE; DIETHYLHEXYL PHTHALATE; INSULIN; LIPID PEROXIDATION; MALE; MUSCLE, SKELETAL; PROTECTIVE AGENTS; RATS; RECEPTOR, INSULIN; VITAMIN E;

ANIMALIA; RATTUS;

EID: 81855194401     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.08.022     Document Type: Article

References (56)

1. Ablake M., Itoh M., Terayama H., Hayashi S., Shoji S., Naito M., Takahashi K., Suna S., Jitsunari F. Di-(2-ethylhexyl) phthalate induces severe aspermatogenesis in mice; however, subsequent antioxidant vitamins supplementation accelerates regeneration of the seminiferous epithelium. Int. J. Androl. 2004, 27:274-281.
2. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:7915-7922.
3. Armoni M., Kritz N., Harel C., Bar-Yoseph F., Chen H., Quon M.J., Karneili E. Peroxisome proliferator-activated receptor-γ represses GLUT4 promoter activity in primary adipocyte and rosiglitazone alleviates this effect. J. Biochem. 2003, 278:30614-30623.
4. Baudry A., Leroux L., Jackerott M., Joshi R.L. Genetic manipulation of insulin signaling action and secretion in mice. Insights into glucose homeostasis and pathogenesis of type-2 diabetes. ENBO Rep. 2002, 3:323-328.
5. Baynes J.W. Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40:405-412.
6. Beaulieu J.M., Marion S., Rodriguiz R.M., Medvedev I.O., Sotnikova T.D., Ghisi V., Wetsel W.C., Lefkowitz R.J., Gainetdinov R.R., Caron M.G. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 2008, 132:125-136.
7. Bell F.P. Effects of phthalate esters on lipid metabolism in various tissues, cells and organelles in mammals. Environ. Health Perspect. 1982, 45:41-50.
8. Bouzakri K., Roques M., Gual P., Espinosa S., Guebre-Egziabher F., Riou J.P., Laville M., Le Marchand-Brustel Y., Tanti J.F., Vidal H. Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 2003, 52:1319-1325.
9. Burton G.W., Joyce A., Ingold Ku. Is vitamin E the only lipid-soluble, chain-breaking antioxidant in human blood plasma and erythrocyte membranes?. Arch. Biochem. Biophys. 1983, 221:281-290.
10. Chang C., Kokontis J., Liao S. Structural analysis of complementary DNA and amino acid sequence of the human and rat androgen receptors. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7211-7215.
11. Cheatham B., Kahn C.R. Insulin action and the insulin signaling network. Endocr. Rev. 1995, 16:117-142.
12. Cobellis L., Latini G., De Felice C., Razzi S., Paris I., Ruggieri F., Mazzeo P., Petraglia F. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum. Reprod. 2003, 18:1512-1515.
13. Colon I., Caro D., Bourdony C.J., Rosario O. Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development. Environ. Health Perspect. 2000, 108:895-900.
14. DeFronzo R.A. Pathogenesis of type 2 diabetes mellitus: metabolic and molecular implications for identifying diabetes genes. Diabetes 1997, 5:117-269.
15. Devasagayam T.P., Tarachand U. Decreased lipid peroxidation in rat kidneys during gestation. Biochem. Biophys. Res. Commun. 1987, 145:134-138.
16. Dhanya C.R., Gayathri N.S., Mithra K., Nair K.V., Kurup P.A. Vitamin E prevents deleterious effects of di (2-ethylhexyl) phthalate, a plasticizer used in PVC blood storage bags. Ind. J. Exp. Biol. 2004, 4:871-875.
17. Dombrowski L., Roy D., Mareotte B., Marette A. A new procedure for the isolation of plasma membrane, T-tubules and internal membranes from skeletal muscles. Amer. J. Physiol. 1996, 270:667-676.
18. Evans J.L., Goldfine I.D., Maddux B.A., Grodsky G.M. Are oxidative stress-activated signaling pathways mediators of insulin resistance and β-cell dysfunction?. Diabetes 2003, 52:1-8.
19. Gayathri N.S., Dhanya C.R., Indu A.R., Kurup P.A. Changes in some hormones by low doses of di (2-ethylhexyl) phthalate (DEHP), a commonly used plasticizer in PVC blood storage bags & medical tubing. Indian J. Med. Res. 2004, 119:139-144.
20. Gonzalez C.G., Alonso A., Balbin M., Diaz F., Fernandez S., Patterson A.M. Effects of pregnancy on insulin receptor in liver, skeletal muscle and adipose tissue of rats. Gynecol. Endocrinol. 2002, 16:93-205.
21. Gonzalez C., Alonso A., Fernandez R., Patterson A.M. Regulation of insulin receptor substrate-1 in the liver, skeletal muscle and adipose tissue of rats throughout pregnancy. Gynecol. Endocrinol. 2003, 17:187-197.
22. Hassid W.Z., Abraham S. Determination of glycogen with anthrone reagent. Methods Enzymol. 1957, 3:34-37.
23. Hirosumi J., Tuncman G., Chang L., Gorgun C.Z., Uysal K.T., Maeda K., Karin M., Hotamisligil G.S. A central role for JNK in obesity and insulin resistance. Nature 2002, 420:333-336.
24. Hirsch E., Costa C., Ciraolo E. Phosphoinositide 3-kinases as a common platform for multi-hormone signaling. J. Endocrinol. 2007, 194:243-256.
25. Ishihara M., Itoh M., Miyamoto K., Suna S., Takeuchi Y., Takenaka I., Jitsunari F. Spermatogenic disturbance induced by di-(2-ethylhexyl) phthalate is significantly prevented by treatment with antioxidant vitamins in the rat. Int. J. Androl. 2000, 23:85-94.
26. Jain G.C., Pareek H., Khajja B.S., Jain K., Jhalani S., Agarwal S., Sharma S. Modulation of di- (2-ethylhexyl) phthalate induced hepatic toxicity by Apium graveolens L. seeds extract in rats. Afr. J. Biochem. Res. 2009, 3:222-225.
27. Joost H.G., Thorens B. The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics and potential function of its novel members. Mol. Membr. Biol. 2001, 18:247-256.
28. Kahn C.R. Banting lecture. Insulin action, diabetogenesis, and the cause of type II diabetes. Diabetes 1994, 43:1066-1084.
29. Kane S., Sano H., Liu S.C., Asara J.M., Lane W.S., Garner C.C., Lienhard G.E. A method to identify serine kinase substrates: Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 2002, 277:22115-22118.
30. Kraft L.A., Johnson A.D. Epididymal carbohydrate metabolism. II. Substrates and pathway utilization of caput and cauda epididymal tissue from the rabbit, rat and mouse. Comp. Biochem. Physiol. B. 1972, 42:451-461.
31. Larance M., Ramm G., Stockli J., van Dam E.M., Winata S., Wasinger V., Simpson F., Graham M., Junutula J.R., Guilhaus M., James D.E. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem. 2005, 280:37803-37813.
32. Lee D.F., Kuo H.P., Chen C.T. IKK beta suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 2007, 130:440-455.
33. Lee Y.J., Lee E., Kim T.H., Choi J.S., Lee J., Jung K.K., Kwack S.J., Kim K.B., Kang T.S., Han S.Y., Lee B.M., Kim H.S. Effects of di (2-ethylhexyl) phthalate on regulation of steroidogenesis or spermatogenesis in testes of Sprague-Dawley rats. J. Heal. Sci. 2009, 55:380-388.
34. Liu Y., Wan Q., Guan O., Gao L., Zhao J. High-fat diet feeding impairs both the expression and activity of AMPKa in rats skeletal muscle. Biochem. Biophys. Res. Commun. 2006, 339:701-707.
35. Livingstone C., Collison M. Sex steroids and insulin resistance. Clin. Sci. 2002, 102:151-166.
36. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
37. Luan Bing, Zhao Jian, Wu Haiya, Duan Baoyu, Shu Guangwen, Wang Xiaoying, Li Dangsheng, Jia Weiping, Kang Jiuhong, Pei Gang Deficiency of a b-arrestin-2 signal complex contributes to insulin resistance. Nature 2009, 457:1146-1150.
38. Martinelli M.I., Mocchiutti N.O., Bernal C.A. Dietary di (2-ethylhexyl) phthalate-impaired glucose metabolism in experimental animals. Hum. Exp. Toxicol. 2006, 25:531-538.
39. Mushtaq M., Srivastava S.P., Seth P.K. Effect of di-2-ethylhexyl phthalate (DEHP) on glycogen metabolism in rat liver. Toxicology 1980, 16:153-161.
40. Oaks M.K., Raff H. Differentiation of the expression of aldosterone synthase and 1 α-hydroxylase mRNA in the rat adrenal cortex by reverse transcriptase-polymerase chain reaction. J. Steroid Biochem. Mol. Biol. 1995, 54:193-199.
41. Pick E., Keisari Y. Superoxide anion and H2O2 production by chemically elicited peritoneal macrophages-induction by multiple nonphagocytic stimuli. Cell. Immunol. 1981, 59:301-318.
42. Popovic M., Kaurinovic B., Trivic S., Mimica-Dukic N., Bursac M. Effect of celery (Apium graveolens) extracts on some biochemical parameters of oxidative stress in mice treated with carbon tetrachloride. Phytother. Res. 2006, 20:531-537.
43. Puntarulo S., Cederbaum A.I. Effect of oxygen concentration on microsomal oxidation of ethanol and generation of oxygen radicals. Biochem. J. 1988, 251:787-794.
44. Rengarajan S., Parthasarathy C., Anitha M., Balasubramanian K. Diethylhexyl phthalate impairs insulin binding and glucose oxidation in Chang liver cells. Toxicol. In Vitro 2007, 21:99-102.
45. Rusyn I., Kadiiska M.B., Dikalova A., Kono H., Yin M., Tsuchiya K., Mason R.P., Peters J.M., Gonzalez F.J., Segal B.H., Holland S.M., Thurman R.G. Phthalates rapidly increase production of reactive oxygen species in vivo: role of Kupffer cells. Mol. Pharmacol. 2001, 59:744-750.
46. Santhosh A., Nair K.G., Arun P., Deepadevi K.V., Manojkumar V., Lakshmi L.R., Kurup P.A. Effect of DEHP [di (2-ethyl hexyl) phthalate] on lipid peroxidation in liver in rats and in primary cultures of rat hepatocytes. Ind. J. Med. Res. 1998, 108:17-23.
47. Sharpe R.M. Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol. Lett. 2001, 120:221-232.
48. Shepherd P.R., Withers D.J., Siddle K. Phosphoinositide 3-kinase: the key switch mechanism in insulin signaling. Biochem. J. 1998, 333:471-490.
49. Stahlhut R.W., Wijngaarden E.V., Dye T.D., Cook S., Swan S.H. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ. Health Perspect. 2007, 115:876-882.
50. Sunny M.C., Remesh P., George K.E. Use of polymeric plasticizers in polyvinyl chloride to reduce conventional plasticizers migration for critical applications. J. Elastomers plast. 2004, 36:19-31.
51. Taniyama Y., Hitomi H., Shah A., Alexander R.W., Griendling K.K. Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1142-1147.
52. Valverde A.M., Navarro P., Teruel T., Conejo R., Benito M., Lorenzo M. Insulin and insulin-like growth factor I up-regulate GLUT4 gene expression in fetal brown adipocytes, in a phosphoinositide 3-kinase-dependent manner. Biochem. J. 1999, 337:397-405.
53. Vanhaesebroeck B., Alessi D.R. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 2000, 346:561-576.
54. Watson R.T., Pessin J.E. Bridging the gap between insulin signaling and GLUT4 translocation. Trends Biochem. Sci. 2006, 31:215-222.
55. Xu Y., Cook T.J., Knipp G.T. Effects of di-(2-ethylhexyl)-phthalate (DEHP) and its metabolites on fatty acid homeostasis regulating proteins in rat placental HRP-1 trophoblast cells. Toxicol. Sci. 2005, 84:287-300.
56. Zaid H., Antonescu C.N., Randhawa V.K., Klip A. Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem. J. 2008, 413:201-215.