Abnormal glucose homeostasis in adult female rat offspring after intrauterine ethanol exposure

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 5, 2007, Pages

  Yao, Xing Hai ^a   Nyomba, B L Grégoire ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Akt; Ethanol; Glucose transporter; Insulin resistance; Intrauterine environment; Protein kinase C

Indexed keywords

GLUCOSE TRANSPORTER 4; INSULIN; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C ZETA;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH WEIGHT; BODY WEIGHT; CELL MEMBRANE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; FEMALE; FETUS MONITORING; FOOD INTAKE; GASTROCNEMIUS MUSCLE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AGING; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; ETHANOL; FEEDING BEHAVIOR; FEMALE; HOMEOSTASIS; INSULIN RESISTANCE; MUSCLE, SKELETAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN KINASES; PTEN PHOSPHOHYDROLASE; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 34248155673     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00822.2006     Document Type: Article

References (55)

1. Aerts L, Van Assche FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol 38: 894-903, 2006.
2. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36: 62-67, 1993.
3. Beattie JO. Alcohol exposure and the fetus. Eur J Clin Nutr 46 Suppl 1: S7-S17, 1992.
4. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 341: 339-341, 1993.
5. Boloker J, Gertz SJ, Simmons RA. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 51: 1499-1506, 2002.
6. Burgering BM, Coffer PJ. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602, 1995.
7. Butler M, McKay RA, Popoff IJ, Gaarde WA, Witchell D, Murray SF, Dean NM, Bhanot S, Monia BP. Specific inhibition of PTEN expression reverses hyperglycemia in diabetic mice. Diabetes 51: 1028-1034, 2002.
8. Castells S, Mark E, Abaci F, Schwartz E. Growth retardation in fetal alcohol syndrome. Unresponsiveness to growth-promoting hormones. Dev Pharmacol Ther 3: 232-241, 1981.
9. Cheatham B, Vlahos CJ, Cheatham L, Wang L, Blenis J, Kahn CR. Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol Cell Biol 14: 4902-4911, 1994.
10. Chen L, Nyomba BL. Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 52: 454-462, 2003.
11. Chen L, Nyomba BL. Glucose intolerance and resistin expression in rat offspring exposed to ethanol in utero: modulation by postnatal high-fat diet. Endocrinology 144: 500-508, 2003.
12. Chen L, Nyomba BL. Whole body insulin resistance in rat offspring of mothers consuming alcohol during pregnancy or lactation: comparing prenatal and postnatal exposure. J Appl Physiol 96: 167-172, 2004.
13. Chen L, Yao XH, Nyomba BL. In vivo insulin signaling through PI3-kinase is impaired in skeletal muscle of adult rat offspring exposed to ethanol in utero. J Appl Physiol 99: 528-534, 2005.
14. Chen L, Zhang T, Nyomba BL. Insulin resistance of gluconeogenic pathways in neonatal rats after prenatal ethanol exposure. Am J Physiol Regul Integr Comp Physiol 286: R554-R559, 2004.
15. Cushman SW, Wardzala LJ. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane. J Biol Chem 255: 4758-4762, 1980.
16. DeFronzo RA. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37: 667-687, 1988.
17. Du K, Herzig S, Kulkarni RN, Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300: 1574-1577, 2003.
18. Elton CW, Pennington JS, Lynch SA, Carver FM, Pennington SN. Insulin resistance in adult rat offspring associated with maternal dietary fat and alcohol consumption. J Endocrinol 173: 63-71, 2002.
19. Farese RV. Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. Am J Physiol Endocrinol Metab 283: E1-E11, 2002.
20. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol 288: R368-R373, 2005.
21. He L, Simmen FA, Mehendale HM, Ronis MJ, Badger TM. Chronic ethanol intake impairs insulin signaling in rats by disrupting Akt association with the cell membrane. Role of TRB3 in inhibition of Akt/protein kinase B activation. J Biol Chem 281: 11126-11134, 2006.
22. Idris I, Gray S, Donnelly R. Protein kinase C activation: isozyme-specific effects on metabolism and cardiovascular complications in diabetes. Diabetologia 44: 659-673, 2001.
23. Imamura T, Huang J, Usui I, Satoh H, Bever J, Olefsky JM. Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin. Mol Cell Biol 23: 4892-4900, 2003.
24. Jansson T, Lambert GW. Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous system activity in the rat at 3-4 months of age. J Hypertens 17: 1239-1248, 1999.
25. Jones KL, Smith DW, Ulleland CN, Streissguth P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1: 1267-1271, 1973.
26. Kotani K, Ogawa W, Matsumoto M, Kitamura T, Sakaue H, Hino Y, Miyake K, Sano W, Akimoto K, Ohno S, Kasuga M. Requirement of atypical protein kinase C-lambda for insulin stimulation of glucose uptake but not for Akt activation in 3T3-L1 adipocytes. Mol Cell Biol 18: 6971-6982, 1998.
27. Kraegen EW, James DE, Bennett SP, Chisholm DJ. In vivo insulin sensitivity in the rat determined by euglycemic clamp. Am J Physiol Endocrinol Metab 245: E1-E7, 1983.
28. Lo YT, Tsao CJ, Liu IM, Liou SS, Cheng JT. Increase of PTEN gene expression in insulin resistance. Horm Metab Res 36: 662-666, 2004.
29. Lopez-Tejero D, Llobera M, Herrera E. Permanent abnormal response to a glucose load after prenatal ethanol exposure in rats. Alcohol 6: 469-473, 1989.
30. Muhajarine N, D'Arcy C, Edouard L. Prevalence and predictors of health risk behaviours during early pregnancy: Saskatoon Pregnancy and Health Study. Can J Public Health 88: 375-379, 1997.
31. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab 287: E863-E870, 2004.
32. Ozanne SE, Hales CN. The long-term consequences of intra-uterine protein malnutrition for glucose metabolism. Proc Nutr Soc 58: 615-619, 1999.
33. Pennington JS, Shuvaeva TI, Pennington SN. Maternal dietary ethanol consumption is associated with hypertriglyceridemia in adult rat offspring. Alcohol Clin Exp Res 26: 848-855, 2002.
34. Phipps K, Barker DJP, Hales CN, Fall CHD, Osmond C, Clark PMS. Fetal growth and impaired glucose-tolerance in men and women. Diabetologia 36: 225-228, 1993.
35. Radziuk J. Insulin sensitivity and its measurement: structural commonalities among the methods. J Clin Endocrinol Metab 85: 4426-4433, 2000.
36. Sadri P, Legare DJ, Takayama S, Lautt WW. Increased incidence of hepatic insulin-sensitizing substance (HISS)-dependent insulin resistance in female rats prenatally exposed to ethanol. Can J Physiol Pharmacol 83: 383-387, 2005.
37. Saha JK, Xia J, Grondin JM, Engle SK, Jakubowski JA. Acute hyperglycemia induced by ketamine/xylazine anesthesia in rats: mechanisms and implications for preclinical models. Exp Biol Med (Maywood) 230: 777-784, 2005.
38. Shepherd PR, Withers DJ, Siddle K. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem J 333: 471-490, 1998.
39. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50: 2279-2286, 2001.
40. Simpson F, Whitehead JP, James DE. GLUT4 - at the cross roads between membrane trafficking and signal transduction. Traffic 2: 2-11, 2001.
41. Somwar R, Niu W, Kim DY, Sweeney G, Randhawa VK, Huang C, Ramlal T, Klip A. Differential effects of phosphatidylinositol 3-kinase inhibition on intracellular signals regulating GLUT4 translocation and glucose transport. J Biol Chem 276: 46079-46087, 2001.
42. Song H, Shojima N, Sakoda H, Ogihara T, Fujishiro M, Katagiri H, Anai M, Onishi Y, Ono H, Inukai K, Fukushima Y, Kikuchi M, Shimano H, Yamada N, Oka Y, Asano T. Resistin is regulated by C/EBPs, PPARs, and signal-transducing molecules. Biochem Biophys Res Commun 299: 291-298, 2002.
43. Standaert ML, Bandyopadhyay G, Perez L, Price D, Galloway L, Poklepovic A, Sajan MP, Cenni V, Sirri A, Moscat J, Toker A, Farese RV. Insulin activates protein kinases C-zeta and C-lambda by an autophosphorylation- dependent mechanism and stimulates their translocation to GLUT4 vesicles and other membrane fractions in rat adipocytes. J Biol Chem 274: 25308-25316, 1999.
44. Sugden MC, Holness MJ. Gender-specific programming of insulin secretion and action. J Endocrinol 175: 757-767, 2002.
45. Ting JW, Lautt WW. The effect of acute, chronic, and prenatal ethanol exposure on insulin sensitivity. Pharmacol Ther 111: 346-373, 2006.
46. Urso T, Gavaler JS, Van Thiel DH. Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci 28: 1053-1056, 1981.
47. Villarroya F, Mampel T. Glucose tolerance and insulin response in offspring of ethanol-treated pregnant rats. Gen Pharmacol 16: 415-417, 1985.
48. Vollenweider P, Menard B, Nicod P. Insulin resistance, defective insulin receptor substrate 2-associated phosphatidylinositol-3′ kinase activation, and impaired atypical protein kinase C (zeta/lambda) activation in myotubes from obese patients with impaired glucose tolerance. Diabetes 51: 1052-1059, 2002.
49. Walker KS, Deak M, Paterson A, Hudson K, Cohen P, Alessi DR. Activation of protein kinase B beta and gamma isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: comparison with protein kinase B alpha. Biochem J 331: 299-308, 1998.
50. Whiteman EL, Cho H, Birnbaum MJ. Role of Akt/protein kinase B in metabolism. Trends Endocrinol Metab 13: 444-451, 2002.
51. Williams RJ, Gloster SP. Knowledge of fetal alcohol syndrome (FAS) among natives in northern Manitoba. J Stud Alcohol 60: 833-836, 1999.
52. Yacoub Wasef SZ, Robinson KA, Berkaw MN, Buse MG. Glucose, dexamethasone and the unfolded protein response regulate TRB3 mRNA expression in 3T3-L1 adipocytes and L6 myotubes. Am J Physiol Endocrinol Metab 291: E1274-E1280, 2006.
53. Yao XH, Chen L, Nyomba BL. Adult rats prenatally exposed to ethanol have increased gluconeogenesis and impaired insulin response of hepatic gluconeogenic genes. J Appl Physiol 100: 642-648, 2006.
54. Yeon JE, Califano S, Xu J, Wands JR, de la Monte SM. Potential role of PTEN phosphatase in ethanol-impaired survival signaling in the liver. Hepatology 38: 703-714, 2003.
55. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, Guzman C, Larrea F, Nathanielsz PW. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol 566: 225-236, 2005.