High-fat intake during pregnancy and lactation exacerbates high-fat diet-induced complications in male offspring in mice

Endocrinology

Volumn 154, Issue 10, 2013, Pages 3565-3576

  Kruse, Michael ^a,d   Seki, Yoshinori ^a   Vuguin, Patricia M ^a,b,e   Du, Xiu Quan ^a   Fiallo, Ariana ^a   Glenn, Alan S ^a   Singer, Stephan ^c   Breuhahn, Kai ^c   Katz, Ellen B ^a   Charron, Maureen J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL AT MONTEFIORE   (United States)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^e Steven and Alexandra Cohen Children's Medical Center of New York   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 1; FATTY ACID SYNTHASE; FATTY ACID TRANSPORTER; GLUCOSE; GLUCOSE TRANSPORTER 4; GLYCEROL; INSULIN; LACTIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PLASMINOGEN ACTIVATOR INHIBITOR 1;

ADIPOCYTE; ADULT DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CELL SIZE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FAT INTAKE; FATTY LIVER; FEMALE; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; GLYCEROL BLOOD LEVEL; HISTOPATHOLOGY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LACTATE BLOOD LEVEL; LACTATION; LEAN BODY WEIGHT; LIPID METABOLISM; LIPID STORAGE; LIVER HISTOLOGY; LOW FAT DIET; MALE; MATERNAL NUTRITION; METABOLISM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROGENY; REAL TIME POLYMERASE CHAIN REACTION;

ADIPOGENESIS; ADIPOSE TISSUE, WHITE; ANIMALS; ANIMALS, OUTBRED STRAINS; BIOLOGICAL MARKERS; CELL SIZE; DIET, HIGH-FAT; DISEASE SUSCEPTIBILITY; FATTY LIVER; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION; GLUCOSE INTOLERANCE; INSULIN RESISTANCE; LACTATION; LIVER; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE; OBESITY; PREGNANCY; SEVERITY OF ILLNESS INDEX;

EID: 84884685537     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1877     Document Type: Article

References (47)

1. Buckley AJ, Jaquiery AL, Harding JE. Nutritional programming of adult disease. Cell Tissue Res. 2005;322:73-79. (Pubitemid 41677657)
2. Armitage JA, Taylor PD, Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005;565:3-8. (Pubitemid 40723685)
3. Seki Y, Williams L, Vuguin PM, Charron MJ. Minireview: epigenetic programming of diabetes and obesity: animal models. Endocrinology. 2012;153:1031-1038.
4. Ravelli AC, van der Meulen JH, Michels RP, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351:173-177. (Pubitemid 28037007)
5. Swenne I, Crace CJ, Milner RD. Persistent impairment of insulin secretory response to glucose in adult rats after limited period of protein-calorie malnutrition early in life. Diabetes. 1987;36:454-458. (Pubitemid 18023188)
6. Desai M, Crowther NJ, Ozanne SE, Lucas A, Hales CN. Adult glucose and lipid metabolism may be programmed during fetal life. Biochem Soc Trans. 1995;23:331-335.
7. Steyn NP, Mann J, Bennett PH, et al. Diet, nutrition and the prevention of type 2 diabetes. Public Health Nutr. 2004;7:147-165. (Pubitemid 38294515)
8. Chechi K, Cheema SK. Maternal diet rich in saturated fats has deleterious effects on plasma lipids of mice. Exp Clin Cardiol. 2006;11:129-135. (Pubitemid 44018293)
9. Samuelsson AM, Matthews PA, Argenton M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008;51:383-392. (Pubitemid 351159954)
10. ObenJA, Mouralidarane A, SamuelssonAM,et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol. 2010;52:913-920.
11. Parker L, Lamont DW, Unwin N, et al. A lifecourse study of risk for hyperinsulinaemia, dyslipidaemia and obesity (the central metabolic syndrome) at age 49-51 years. Diabet Med. 2003;20:406-415. (Pubitemid 36605627)
12. Hartil K, Vuguin PM, Kruse M, et al. Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero. Pediatr Res. 2009;66:368-373.
13. Stenbit AE, Tsao TS, Li J, et al. GLUT4heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat Med. 1997;3:1096-1101. (Pubitemid 27444450)
14. Bruce KD, Cagampang FR, Argenton M, et al. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology. 2009;50:1796-1808.
15. Souza-Mello V, Mandarim-de-Lacerda CA, Aguila MB. Hepatic structural alteration in adult programmed offspring (severe maternal protein restriction) is aggravated by post-weaning high-fat diet. Br J Nutr. 2007;98:1159-1169. (Pubitemid 350193784)
16. Langley-Evans SC. Developmental programming of health and disease. Proc Nutr Soc. 2006;65:97-105. (Pubitemid 43259989)
17. Rueda-Clausen CF, DolinskyVW,Morton JS, Proctor SD, Dyck JR, Davidge ST. Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome. Diabetes 60:507-516.
18. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000;279:E83-E87. (Pubitemid 30609948)
19. Stubbins RE, Najjar K, Holcomb VB, Hong J, Núñez NP. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes Metab. 2012;14:58-66.
20. Taicher GZ, Tinsley FC, Reiderman A, Heiman ML. Quantitative magnetic resonance (QMR) method for bone and whole-body-composition analysis. Anal Bioanal Chem. 2003;377:990-1002. (Pubitemid 40877830)
21. Ranalletta M, Du XQ, Seki Y, et al. Hepatic response to restoration of GLUT4 in skeletal muscle of GLUT4 null mice. Am J Physiol Endocrinol Metab. 2007;293:E1178-E1187. (Pubitemid 350106583)
22. Kubota N, Terauchi Y, Miki H, et al. PPARγ mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell. 1999;4:597-609. (Pubitemid 29531139)
23. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313-1321. (Pubitemid 40770284)
24. PastorMM, Proft M, Pascual-Ahuir A. Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J Biol Chem. 2009;284:30307-30317.
25. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413-1419. (Pubitemid 29258890)
26. Nivoit P, Morens C, Van Assche FA, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009;52:1133-1142.
27. Buckley AJ, Keserü B, Briody J, Thompson M, Ozanne SE, Thompson CH. Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism. 2005;54:500-507. (Pubitemid 40410452)
28. Ozanne SE, Hales CN. Lifespan: catch-up growth and obesity in male mice. Nature. 2004;427:411-412. (Pubitemid 38168484)
29. Bieswal F, Ahn MT, Reusens B, et al. The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring). 2006;14:1330-1343. (Pubitemid 46219658)
30. Siemelink M, Verhoef A, Dormans JA, Span PN, Piersma AH. Dietary fatty acid composition during pregnancy and lactation in the rat programs growth and glucose metabolism in the offspring. Diabetologia. 2002;45:1397-1403. (Pubitemid 35244892)
31. Li J, Houseknecht KL, Stenbit AE, Katz EB, Charron MJ. Reduced glucose uptake precedes insulin signaling defects in adipocytes from heterozygous GLUT4 knockout mice. FASEB J. 2000;14:1117-1125. (Pubitemid 30350393)
32. Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010;143:1084-1096.
33. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature. 2010;467:963-966.
34. Rett K, Wicklmayr M, Mehnert H. What is the clinical significance of insulin resistance? J Cardiovasc Pharmacol. 1992;20(suppl 11):S22-S26. (Pubitemid 23046841)
35. Rajkumar K, Murphy LJ. Enhanced gluconeogenesis and hepatic insulin resistance in insulin-like growth factor binding protein-1 transgenic mice. Biochim Biophys Acta. 1999;1426:491-497. (Pubitemid 29078565)
36. Jo J, Gavrilova O, Pack S, et al. 2009 Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput Biol. 5:e1000324.
37. Scherer PE. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes. 2006;55:1537-1545. (Pubitemid 44324105)
38. Lefterova MI, Mullican SE, Tomaru T, Qatanani M, Schupp M, LazarMA. Endoplasmic reticulum stress regulates adipocyte resistin expression. Diabetes. 2009;58:1879-1886.
39. Sewter C, Berger D, Considine RV, et al. Human obesity and type 2 diabetes are associated with alterations in SREBP1 isoform expression that are reproduced ex vivo by tumor necrosis factor-α. Diabetes. 2002;51:1035-1041. (Pubitemid 34438347)
40. Goossens GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav. 2008;94:206-218. (Pubitemid 351615418)
41. Hoffler U, Hobbie K, Wilson R, et al. Diet-induced obesity is associated with hyperleptinemia, hyperinsulinemia, hepatic steatosis, and glomerulopathy in C57Bl/6J mice. Endocrine. 2009;36:311-325.
42. Okamoto Y, Tanaka S, Haga Y. Enhanced GLUT2 gene expression in an oleic acid-induced in vitro fatty liver model. Hepatol Res. 2002;23:138-144. (Pubitemid 36113479)
43. Radford NB, Wan B, Richman A, et al. Cardiac dysfunction in mice lacking cytochrome-c oxidase subunit VIaH. Am J Physiol Heart Circ Physiol. 2002;282:H726-H733. (Pubitemid 34654999)
44. Xia W, Wan Y, Li YY, et al. PFOS prenatal exposure induce mitochondrial injury and gene expression change in hearts of weaned SD rats. Toxicology. 2011;282:23-29.
45. Bayol SA, Simbi BH, Fowkes RC, Stickland NC. A maternal "junk food" diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology. 2010;151:1451-1461.
46. Desai M, Byrne CD, Meeran K, Martenz ND, Bloom SR, Hales CN. Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet. Am J Physiol. 1997;273:G899-G904.
47. Mathers JC, McKay JA. Epigenetics - potential contribution to fetal programming. Adv Exp Med Biol. 2009;646:119-123.