Chronic prenatal ethanol exposure increases adiposity and disrupts pancreatic morphology in adult guinea pig offspring

Nutrition and Diabetes

Volumn 2, Issue DECEMBER, 2012, Pages

  Dobson, C C ^a   Mongillo, D L ^a   Brien, D C ^b   Stepita, R ^c   Poklewska Koziell, M ^a   Winterborn, A ^a   Holloway, A C ^c   Brien, J F ^a,b   Reynolds, J N ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Adiposity; Fetal alcohol spectrum disorder; Guinea pig; Insulin sensitivity; Pancreatic morphology

Indexed keywords

ALCOHOL;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CATCH UP GROWTH; CONTROLLED STUDY; FEMALE; GUINEA PIG; INSULIN RELEASE; LONG TERM EXPOSURE; MALE; NONHUMAN; OBESITY; PANCREAS ISLET; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; WEANING; WHOLE BODY MRI;

EID: 84881161545     PISSN: None     EISSN: 20444052     Source Type: Journal    
DOI: 10.1038/nutd.2012.31     Document Type: Article

References (59)

1. Chudley AE, Conry J, Cook JL, Loock C, Rosales T, LeBlanc N et al. Fetal alcohol spectrum disorder: Canadian guidelines for diagnosis. CMAJ 2005; 172: S1-S21.
2. Sokol RJ, Delaney-Black V, Nordstrom B. Fetal alcohol spectrum disorder. JAMA 2003; 290: 2996-2999.
3. Goh JM, Bensley JG, Kenna K, Sozo F, Bocking AD, Brien J et al. Alcohol exposure during late gestation adversely affects myocardial development with implications for postnatal cardiac function. Am J Physiol Heart Circ Physiol 2011; 300: H645-H651.
4. Gray SP, Denton KM, Cullen-McEwen L, Bertram JF, Moritz KM. Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J Am Soc Nephrol 2010; 21: 1891-1902.
5. Sozo F, Vela M, Stokes V, Kenna K, Meikle PJ, De Matteo R et al. Effects of prenatal ethanol exposure on the lungs of postnatal lambs. Am J Physiol Lung Cell Mol Physiol 2011; 300: L139-L147.
6. Probyn ME, Zanini S, Ward LC, Bertram JF, Moritz KM. A rodent model of low- to moderate-dose ethanol consumption during pregnancy: patterns of ethanol consumption and effects on fetal and offspring growth. Reprod Fertil Dev 2012; 24: 859-870.
7. Chen L, Nyomba BL. Glucose intolerance and resistin expression in rat offspring exposed to ethanol in utero: modulation by postnatal high-fat diet. Endocrinology 2003; 144: 500-508.
8. 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 2004; 96: 167-172.
9. de la Monte SM, Wands JR. Role of central nervous system insulin resistance in fetal alcohol spectrum disorders. J Popul Ther Clin Pharmacol 2010; 17: e390-e404.
10. 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 2002; 173: 63-71.
11. 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 2006; 100: 642-648.
12. Yao XH, Nyomba BL. Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring. Am J Physiol Regul Integr Comp Physiol 2008; 294: R1797-R1806.
13. Stade B, Ali A, Bennett D, Campbell D, Johnston M, Lens C et al. The burden of prenatal exposure to alcohol: revised measurement of cost. Can J Clin Pharmacol 2009; 16: e91-102.
14. Lee K. Gender-specific relationships between alcohol drinking patterns and metabolic syndrome: the Korea National Health and Nutrition Examination Survey 2008. Public Health Nutr 2012; 15: 1917-1924.
15. Fan AZ, Russell M, Naimi T, Li Y, Liao Y, Jiles R et al. Patterns of alcohol consumption and the metabolic syndrome. J Clin Endocrinol Metab 2008; 93: 3833-3838.
16. Castells S, Mark E, Abaci F, Schwartz E. Growth retardation in fetal alcohol syndrome. Unresponsiveness to growth-promoting hormones. Dev Pharmacol Ther 1981; 3: 232-241.
17. Pennington JS, Shuvaeva TI, Pennington SN. Maternal dietary ethanol consumption is associated with hypertriglyceridemia in adult rat offspring. Alcohol Clin Exp Res 2002; 26: 848-855.
18. Zhao LN, Hao LP, Yang XF, Ying CJ, Yu D, Sun XF. The diabetogenic effects of excessive ethanol: reducing beta-cell mass, decreasing phosphatidylinositol 3-kinase activity and GLUT-4 expression in rats. Br J Nutr 2009; 101: 1467-1473.
19. Nishimura H, Shiota K. Summary of comparative embryology and teratology. In: Wilson C, Fraser FC (eds) Handbook of Teratology. Plenum Press: New York, 1977, pp 119-154.
20. Martensson L. The pregnant rabbit, guinea pig, sheep and rhesus monkey as models in reproductive physiology. Eur J Obstet Gynecol Reprod Biol 1984; 18: 169-182.
21. Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979; 3: 79-83.
22. Brien JF, Clarke DW. Disposition and fetal effects of ethanol during pregnancy. In: Kacew S, Lock S (eds) Toxicologic and Pharmacologic Principles in Pediatrics. Hemisphere Publishing Corporation: New York, 1988, pp 199-222.
23. Dobson CC, Mongillo DL, Poklewska-Koziell M, Winterborn A, Brien JF, Reynolds JN. Sensitivity of modified Biel-maze task, compared with Y-maze task, to measure spatial learning and memory deficits of ethanol teratogenicity in the guinea pig. Behav Brain Res 2012; 233: 162-168.
24. Elvidge H. Production of dated pregnant guinea pigs without postpartum matings. J Inst Animal Tech 1972; 23: 111-117.
25. Steenaart NA, Clarke DW, Brien JF. Gas-liquid chromatographic analysis of ethanol and acetaldehyde in blood with minimal artifactual acetaldehyde formation. J Pharmacol Methods 1985; 14: 199-212.
26. Li X, Youngren JF, Hyun B, Sakkas GK, Mulligan K, Majumdar S et al. Technical evaluation of in vivo abdominal fat and IMCL quantification using MRI and MRSI at 3 T. Magn Reson Imaging 2008; 26: 188-197.
27. Hu HH, Hines CD, Smith Jr DL, Reeder SB. Variations in T(2)* and fat content of murine brown and white adipose tissues by chemical-shift MRI. Magn Reson Imaging 2012; 30: 323-329.
28. Johnson DH, Flask CA, Ernsberger PR, Wong WC, Wilson DL. Reproducible MRI measurement of adipose tissue volumes in genetic and dietary rodent obesity models. J Magn Reson Imaging 2008; 28: 915-927.
29. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006; 31: 1116-1128.
30. Brien JF, Chan D, Green CR, Iqbal U, Gareri J, Kobus SM et al. Chronic prenatal ethanol exposure and increased concentration of fatty acid ethyl esters in meconium of term fetal Guinea pig. Ther Drug Monit 2006; 28: 345-350.
31. Iqbal U, Rikhy S, Dringenberg HC, Brien JF, Reynolds JN. Spatial learning deficits induced by chronic prenatal ethanol exposure can be overcome by non-spatial pre-training. Neurotoxicol Teratol 2006; 28: 333-341.
32. Shea KM, Hewitt AJ, Olmstead MC, Brien JF, Reynolds JN. Maternal ethanol consumption by pregnant guinea pigs causes neurobehavioral deficits and increases ethanol preference in offspring. Behav Pharmacol 2012; 23: 105-112.
33. 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 2004; 286: R554-R559.
34. Chen L, Nyomba BL. Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 2003; 52: 454-462.
35. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992; 35: 595-601.
36. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulindependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993; 36: 62-67.
37. Bertram CE, Hanson MA. Animal models and programming of the metabolic syndrome. Br Med Bull 2001; 60: 103-121.
38. Cettour-Rose P, Samec S, Russell AP, Summermatter S, Mainieri D, Carrillo-Theander C et al. Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome. Diabetes 2005; 54: 751-756.
39. Purohit V, Bode JC, Bode C, Brenner DA, Choudhry MA, Hamilton F et al. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol 2008; 42: 349-361.
40. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR et al. A transgenic model of visceral obesity and the metabolic syndrome. Science 2001; 294: 2166-2170.
41. Despres JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature 2006; 444: 881-887.
42. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697-738.
43. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 1997; 46: 1579-1585.
44. Kim KH, Oh SW, Kwon H, Park JH, Choi H, Cho B. Alcohol consumption and its relation to visceral and subcutaneous adipose tissues in healthy male Koreans. Ann Nutr Metab 2012; 60: 52-61.
45. Yokoyama H, Hiroshi H, Ohgo H, Hibi T, Saito I. Effects of excessive ethanol consumption on the diagnosis of the metabolic syndrome using its clinical diagnostic criteria. Intern Med 2007; 46: 1345-1352.
46. Dorn JM, Hovey K, Muti P, Freudenheim JL, Russell M, Nochajski TH et al. Alcohol drinking patterns differentially affect central adiposity as measured by abdominal height in women and men. J Nutr 2003; 133: 2655-2662.
47. Suter PM. Is alcohol consumption a risk factor for weight gain and obesity? Crit Rev Clin Lab Sci 2005; 42: 197-227.
48. Shelmet JJ, Reichard GA, Skutches CL, Hoeldtke RD, Owen OE, Boden G. Ethanol causes acute inhibition of carbohydrate, fat, and protein oxidation and insulin resistance. J Clin Invest 1988; 81: 1137-1145.
49. Bessembinders K, Wielders J, van de Wiel A. Severe hypertriglyceridemia influenced by alcohol (SHIBA). Alcohol Alcohol 2011; 46: 113-116.
50. Ginsberg H, Olefsky J, Farquhar JW, Reaven GM. Moderate ethanol ingestion and plasma triglyceride levels. A study in normal and hypertriglyceridemic persons. Ann Intern Med 1974; 80: 143-149.
51. Scherer T, O'Hare J, Diggs-Andrews K, Schweiger M, Cheng B, Lindtner C et al. Brain insulin controls adipose tissue lipolysis and lipogenesis. Cell Metab 2011; 13: 183-194.
52. Carpentier A, Mittelman SD, Bergman RN, Giacca A, Lewis GF. Prolonged elevation of plasma free fatty acids impairs pancreatic beta-cell function in obese nondiabetic humans but not in individuals with type 2 diabetes. Diabetes 2000; 49: 399-408.
53. Lee Y, Hirose H, Ohneda M, Johnson JH, McGarry JD, Unger RH. Beta-cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: impairment in adipocyte-beta-cell relationships. Proc Natl Acad Sci USA 1994; 91: 10878-10882.
54. Tushuizen ME, Bunck MC, Pouwels PJ, Bontemps S, van Waesberghe JH, Schindhelm RK et al. Pancreatic fat content and beta-cell function in men with and without type 2 diabetes. Diabetes Care 2007; 30: 2916-2921.
55. Kovanlikaya A, Mittelman SD, Ward A, Geffner ME, Dorey F, Gilsanz V. Obesity and fat quantification in lean tissues using three-point Dixon MR imaging. Pediatr Radiol 2005; 35: 601-607.
56. Baliunas DO, Taylor BJ, Irving H, Roerecke M, Patra J, Mohapatra S et al. Alcohol as a risk factor for type 2 diabetes: a systematic review and meta-analysis. Diabetes Care 2009; 32: 2123-2132.
57. Nguyen KH, Lee JH, Nyomba BL. Ethanol causes endoplasmic reticulum stress and impairment of insulin secretion in pancreatic beta-cells. Alcohol 2012; 46: 89-99.
58. Kim JY, Song EH, Lee HJ, Oh YK, Park YS, Park JW et al. Chronic ethanol consumption-induced pancreatic {beta}-cell dysfunction and apoptosis through glucokinase nitration and its down-regulation. J Biol Chem 2010; 285: 37251-37262.
59. Lee JH, Nguyen KH, Mishra S, Nyomba BL. Prohibitin is expressed in pancreatic beta-cells and protects against oxidative and proapoptotic effects of ethanol. FEBS J 2010; 277: 488-500.