Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring

Endocrinology

Volumn 154, Issue 11, 2013, Pages 4113-4125

  Borengasser, Sarah J ^a,b   Zhong, Ying ^a   Kang, Ping ^a   Lindsey, Forrest ^a   Ronis, Martin J J ^a,b   Badger, Thomas M ^a,b   Gomez Acevedo, Horacio ^a,b   Shankar, Kartik ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; GLUCOSE TRANSPORTER 4; INSULIN; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ADIPOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; DNA METHYLATION; EX VIVO STUDY; FEMALE; GENE EXPRESSION; IMMUNOBLOTTING; LIPOGENESIS; MALE; MATERNAL CARE; MATERNAL OBESITY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SENSITIZATION; SEQUENCE ANALYSIS; STROMA CELL; TISSUE DIFFERENTIATION; TRANSCRIPTOMICS; UPREGULATION; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION; GENOME; INSULIN; LIPOGENESIS; MALE; OBESITY; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84886462809     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2255     Document Type: Article

References (49)

1. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA. 2012;307: 491-497.
2. NathanielszPW,Poston L, Taylor PD. In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Clin Perinatol. 2007;34:515-526, v
3. Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, Badger TM. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008;294:R528-R538.
4. Shankar K, Kang P, Harrell A, et al. Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology. 2010;151: 2577-2589.
5. McCurdy CE, Bishop JM, Williams SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009;119: 323-335.
6. Ainge H, Thompson C, Ozanne SE, Rooney KB.Asystematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond). 2011;35: 325-335.
7. Sen S, Simmons RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes. 2010;59: 3058-3065.
8. Catalano PM. Obesity and pregnancy-the propagation of a viscous cycle? J Clin Endocrinol Metab. 2003;88: 3505-3506.
9. Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care. 2009;32: 1076-1080.
10. Smith J, Cianflone K, Biron S, et al. Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab. 2009;94: 4275-4283.
11. Aagaard-Tillery KM, Grove K, Bishop J, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol. 2008; 41: 91-102.
12. Sandovici I, Smith NH, Nitert MD, et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci USA. 2011; 108: 5449-5454.
13. Lillycrop KA, Burdge GC. Epigenetic changes in early life and future risk of obesity. Int J Obes (Lond). 2011;35: 72-83.
14. Heerwagen MJ, Miller MR, Barbour LA, Friedman JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Physiol Regul Integr Comp Physiol. 2010;299:R711-R722.
15. Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008;118: 2316-2324.
16. Shankar K, Zhong Y, Kang P, et al. Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology. 2011;152: 4158-4170.
17. Borengasser SJ, Lau F, Kang P, et al. Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One. 2011;6:e24068.
18. Muhlhausler BS, Duffield JA, McMillen IC. Increased maternal nutrition stimulates peroxisome proliferator activated receptor-γ, adiponectin, and leptin messenger ribonucleic acid expression in adipose tissue before birth. Endocrinology. 2007;148: 878-885.
19. Long NM, Rule DC, Zhu MJ, Nathanielsz PW, Ford SP. Maternal obesity upregulates fatty acid and glucose transporters and increases expression of enzymes mediating fatty acid biosynthesis in fetal adipose tissue depots. J Anim Sci. 2012;90:2201-2210
20. Saad MJ, Araki E, Miralpeix M, Rothenberg PL, White MF, Kahn CR. Regulation of insulin receptor substrate-1 in liver and muscle of animal models of insulin resistance. J Clin Invest. 1992;90: 1839-1849.
21. Friedman JE, Ishizuka T, Liu S, et al. Reduced insulin receptor signaling in the obese spontaneously hypertensive Koletsky rat. Am J Physiol. 1997;273:E1014-E1023.
22. Gupta RK, Mepani RJ, Kleiner S, et al. Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab. 2012;15: 230-239.
23. Ronis MJ, Sharma N, Vantrease J, et al. Female mice lacking p47phox have altered adipose tissue gene expression and are protected against high fat-induced obesity. Physiol Genomics. 2013; 45: 351-366.
24. Wagoner B, Hausman DB, Harris RB. Direct and indirect effects of leptin on preadipocyte proliferation and differentiation. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1557-R1564.
25. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat Protoc. 2011;6: 468-481.
26. Smallwood SA, Tomizawa S, Krueger F, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43: 811-814.
27. Akalin A, Garrett-Bakelman FE, Kormaksson M, et al. Base-pair resolution DNA methylation sequencing reveals profoundly divergent epigenetic landscapes in acute myeloid leukemia. PLoS Genet. 2012;8:e1002781.
28. Wu H, Caffo B, Jaffee HA, Irizarry RA, Feinberg AP. Redefining CpG islands using hidden Markov models. Biostatistics. 2010;11: 499-514.
29. Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41: 178-186.
30. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enrichedGOterms in ranked gene lists. BMC Bioinformatics. 2009;10:48.
31. Hammarstedt A, Hedjazifar S, Jenndahl L, et al. WISP2 regulates preadipocyte commitment and PPARγ activation by BMP4. Proc Natl Acad Sci USA. 2013;110: 2563-2568.
32. Wang L, Jin Q, Lee JE, Su IH, Ge K. Histone H3K27 methyltransferase Ezh2 represses Wnt genes to facilitate adipogenesis. Proc Natl Acad Sci USA. 2010;107: 7317-7322.
33. 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.
34. 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.
35. Zhu MJ, Han B, Tong J, et al. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol. 2008;586: 2651-2664.
36. Cristancho AG, Lazar MA. Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol. 2011;12: 722-734.
37. Gupta RK, Arany Z, Seale P, et al. Transcriptional control of preadipocyte determination by Zfp423. Nature. 2010;464: 619-623.
38. Siersbaek R, Nielsen R, John S, et al. Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J. 2011;30: 1459-1472.
39. Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F, Kahn BB. Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem. 1993;268: 22243-22246.
40. Tozzo E, Shepherd PR, Gnudi L, Kahn BB. Transgenic GLUT-4 overexpression in fat enhances glucose metabolism: preferential effect on fatty acid synthesis. Am J Physiol. 1995;268:E956-E964.
41. Ishii S, Iizuka K, Miller BC, Uyeda K. Carbohydrate response element binding protein directly promotes lipogenic enzyme gene transcription. Proc Natl Acad Sci USA. 2004;101: 15597-15602.
42. Ceddia RB. The role of AMP-activated protein kinase in regulating white adipose tissue metabolism. Mol Cell Endocrinol. 2012;366: 194-203.
43. Villena JA, Viollet B, Andreelli F, Kahn A, Vaulont S, Sul HS. Induced adiposity and adipocyte hypertrophy in mice lacking the AMP-activated protein kinase-α2 subunit. Diabetes. 2004;53: 2242-2249.
44. Suter M, Bocock P, Showalter L, et al. Epigenomics: maternal highfat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J. 2011;25: 714-726.
45. Dudley KJ, Sloboda DM, Connor KL, Beltrand J, Vickers MH. Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation. PLoS One. 2011;6:e21662.
46. Harris RA, Wang T, Coarfa C, et al. Comparison of sequencingbased methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat Biotechnol. 2010;28: 1097-1105.
47. Meissner A, Mikkelsen TS, Gu H, et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature. 2008; 454: 766-770.
48. Li CC, Young PE, Maloney CA, et al. Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice. Epigenetics. 2013;8: 602-611.
49. Hartung T, Zhang L, Kanwar R, et al. Diametrically opposite methylome-transcriptome relationships in high- and low-CpG promoter genes in postmitotic neural rat tissue. Epigenetics. 2012;7: 421-428.