Maternal overnutrition programs changes in the expression of skeletal muscle genes that are associated with insulin resistance and defects of oxidative phosphorylation in adult male rat offspring

Journal of Nutrition

Volumn 144, Issue 3, 2014, Pages 237-244

  Latouche, Celine ^a   Heywood, Sarah E ^a   Henry, Sarah L ^b   Ziemann, Mark ^a   Lazarus, Ross ^a   El Osta, Assam ^a   Armitage, James A ^a,b,c   Kingwell, Bronwyn A ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; COMPUTATIONAL BIOLOGY; DIET, HIGH-FAT; DNA COPY NUMBER VARIATIONS; FEMALE; GENE EXPRESSION PROFILING; INSULIN; INSULIN RESISTANCE; LACTATION; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OVERNUTRITION; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION;

EID: 84894234279     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.186775     Document Type: Article

References (55)

1. Alfaradhi MZ, Ozanne SE. Developmental programming in response to maternal overnutrition. Front Genet. 2011;2:27.
2. Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol. 2004;561:355-77.
3. Armitage JA, Lakasing L, Taylor PD, Balachandran AA, Jensen RI, Dekou V, Ashton N, Nyengaard JR, Poston L. Developmental programming of aortic and renal structure in offspring of rats fed fatrich diets in pregnancy. J Physiol. 2005;565:171-84.
4. Armitage JA, Poston L, Taylor PD. Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res. 2008;36:73-84.
5. 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.
6. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261:412-7.
7. Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185: 73-9.
8. Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71 Suppl 5:S1344-52.
9. Li M, Sloboda DM, Vickers MH. Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp Diabetes Res. 2011;2011:592408.
10. Shankar K, Kang P, Harrell A, Zhong Y, Marecki JC, Ronis MJ, Badger TM. Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology. 2010;151:2577-89.
11. Rajia S, Chen H, Morris MJ. Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet. J Neuroendocrinol. 2010;22:905-14.
12. Weisinger RS, Armitage JA, Chen N, Begg DP, Mathai ML, Jayasooriya AP, Sinclair AJ, Weisinger HS. Sodium appetite in adult rats following omega-3 polyunsaturated fatty acid deficiency in early development. Appetite. 2010;55:393-7.
13. Odaka Y, Nakano M, Tanaka T, Kaburagi T, Yoshino H, Sato-Mito N, Sato K. The influence of a high-fat dietary environment in the fetal period on postnatal metabolic and immune function. Obesity (Silver Spring). 2010;18:1688-94.
14. Zhang J, Zhang F, Didelot X, Bruce KD, Cagampang FR, Vatish M, Hanson M, Lehnert H, Ceriello A, Byrne CD. Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics. 2009;10:478.
15. Elahi MM, Cagampang FR, Mukhtar D, Anthony FW, Ohri SK, Hanson MA. Long-term maternal high-fat feeding from weaning through pregnancy and lactation predisposes offspring to hypertension, raised plasma lipids and fatty liver in mice. Br J Nutr. 2009;102:514-9.
16. Khan IY, Dekou V, Douglas G, Jensen R, Hanson MA, Poston L, Taylor PD. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol. 2005;288:R127-33.
17. Khan IY, Taylor PD, Dekou V, Seed PT, Lakasing L, Graham D, Dominiczak AF, Hanson MA, Poston L. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003;41:168-75.
18. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, Friedman JE, Grove KL. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009;119: 323-35.
19. Zhang X, Strakovsky R, Zhou D, Zhang Y, Pan YX. A maternal highfat diet represses the expression of antioxidant defense genes and induces the cellular senescence pathway in the liver of male offspring rats. J Nutr. 2011;141:1254-9.
20. Nivoit P, Morens C, Van Assche FA, Jansen E, Poston L, Remacle C, Reusens B. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009;52:1133-42.
21. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, Piersma AH, Ozanne SE, Twinn DF, Remacle C, 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;51:383-92.
22. Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare- Anane H, Persaud SJ, Jones PM, Petrie L, Hanson MA, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005;288:R134-9.
23. Bayol SA, Simbi BH, Stickland NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol. 2005;567:951-61.
24. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123:1939-51.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods. 2001;25:402-8.
26. Babraham Institute. FastQC [cited 2012 May 3]. Available from: http:// www.bioinformatics.babraham.ac.uk/projects/fastqc/.
27. Li H, Durbin R. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics. 2009;25:1754-60.
28. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol. 2010;1-21.
29. EMBL Heidelberg. HTSeq. 2010. Available from: http://www-huber.embl. de/users/anders/HTSeq/doc/overview.html.
30. Fred Hutchinson Cancer Research Centre. Bioconductor package. 2013. Available from: http://www.bioconductor.org/packages/2.11/bioc/html/ edgeR.html.
31. NCBI. Gene Expression Omnibus [cited 2013 Aug 13]. Available from: http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE49797.
32. Broad Institute. GSEA software [cited 2013 Aug 9]. Available from: http://www.broadinstitute.org/gsea/index.jsp.
33. Broad Institute. MSigDB [cited 2013 Aug 9]. Available from: http:// www.broadinstitute.org/gsea/msigdb/index.jsp.
34. Després JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature. 2006;444:881-7.
35. Gabriely I, Barzilai N. Surgical removal of visceral adipose tissue: effects on insulin action. Curr Diab Rep. 2003;3:201-6.
36. Gabriely I, Ma XH, Yang XM, Atzmon G, Rajala MW, Berg AH, Scherer P, Rossetti L, Barzilai N. Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes. 2002;51:2951-8.
37. Buckley AJ, Keseru 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;54:500-7.
38. Shelley P, Martin-Gronert MS, Rowlerson A, Poston L, Heales SJ, Hargreaves IP, McConnell JM, Ozanne SE, Fernandez-Twinn DS. Altered skeletal muscle insulin signaling and mitochondrial complex II- III linked activity in adult offspring of obese mice. Am J Physiol Regul Integr Comp Physiol. 2009;297:R675-81.
39. Yan X, Zhu MJ, Xu W, Tong JF, Ford SP, Nathanielsz PW, Du M. Upregulation of Toll-like receptor 4/nuclear factor-kappaB signaling is associated with enhanced adipogenesis and insulin resistance in fetal skeletal muscle of obese sheep at late gestation. Endocrinology. 2010;151:380-7.
40. Cox LA, Li C, Glenn JP, Lange K, Spradling KD, Nathanielsz PW, Jansson T. Expression of the placental transcriptome in maternal nutrient reduction in baboons is dependent on fetal sex. J Nutr. 2013;143:1698-708.
41. McCormick CM, Smythe JW, Sharma S, Meaney MJ. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res. 1995;84:55-61.
42. Page KC, Malik RE, Ripple JA, Anday EK. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. Am J Physiol Regul Integr Comp Physiol. 2009;297:R1049-57.
43. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez- Zamorano M, Ledesma H, Morales J, Larrea F, Nathanielsz PW. A low maternal protein diet during pregnancy and lactation has sex-and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006;571:221-30.
44. 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. 2005;566:225-36.
45. Dahlgren J, Nilsson C, Jennische E, Ho HP, Eriksson E, Niklasson A, Bjorntorp P, Albertsson Wikland K, Holmang A. Prenatal cytokine exposure results in obesity and gender-specific programming. Am J Physiol Endocrinol Metab. 2001;281:E326-34.
46. Sen S, Simmons RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes. 2010;59:3058-65.
47. Frias AE, Morgan TK, Evans AE, Rasanen J, Oh KY, Thornburg KL, Grove KL. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology. 2011;152:2456-64.
48. Masuyama H, Hiramatsu Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression. Endocrinology. 2012;153:2823-30.
49. Kim JA, Wei Y, Sowers JR. Role of mitochondrial dysfunction in insulin resistance. Circ Res. 2008;102:401-14.
50. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, Jeneson JA, Backes WH, van Echteld CJ, van Engelshoven JM, Mensink M, Schrauwen P. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia. 2007;50:113-20.
51. Morino K, Petersen KF, Shulman GI. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes. 2006;55 Suppl 2:S9-15.
52. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med. 2004;350:664-71.
53. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, Neschen S, White MF, Bilz S, Sono S, et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulinresistant offspring of type 2 diabetic parents. J Clin Invest. 2005;115: 3587-93.
54. Muller YL, Bogardus C, Pedersen O, Baier LA. Gly482Ser missense mutation in the peroxisome proliferator-activated receptor gamma coactivator-1 is associated with altered lipid oxidation and early insulin secretion in Pima Indians. Diabetes. 2003;52:895-8.
55. Skulachev VP. Membrane-linked systems preventing superoxide formation. Biosci Rep. 1997;17:347-66.