DNA methylation regulates hypothalamic gene expression linking parental diet during pregnancy to the offspring's risk of obesity in Psammomys obesus

International Journal of Obesity

Volumn 40, Issue 7, 2016, Pages 1079-1088

  Khurana, I ^a   Kaspi, A ^a   Ziemann, M ^a   Block, T ^a   Connor, T ^b   Spolding, B ^b   Cooper, A ^b   Zimmet, P ^a   El Osta, A ^a,c,d   Walder, K ^b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A8; DNA; GENOMIC DNA; GLUCOSE; INSULIN; METHYL CPG BINDING PROTEIN; RECEPTOR; TASTE RECEPTOR TAS1R1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARTICLE; BODY COMPOSITION; CHILDHOOD OBESITY; COMPARATIVE STUDY; CONTROLLED STUDY; DIETARY INTAKE; DNA METHYLATION; DNA SEQUENCE; ENERGY BALANCE; FEMALE; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; GLUCOSE BLOOD LEVEL; HYPOTHALAMUS; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LACTATION; LOW FAT DIET; MALE; MATERNAL NUTRITION; METABOLIC REGULATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; PSAMMOMYS OBESUS; RAT; STANDARD CHOW DIET; WEIGHT GAIN; ANIMAL; DISEASE MODEL; FETUS DEVELOPMENT; GERBIL; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOLOGY; PHYSIOLOGY; PRENATAL EXPOSURE;

ANIMALS; DIABETES MELLITUS, TYPE 2; DIET, FAT-RESTRICTED; DISEASE MODELS, ANIMAL; DNA METHYLATION; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION; GERBILLINAE; HYPOTHALAMUS; LACTATION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84976333826     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2016.64     Document Type: Article

References (68)

1. Barker DJ. The fetal and infant origins of adult disease. BMJ 1990; 301: 1111
2. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991; 303: 1019-1022
3. Li Y, Jaddoe VW, Qi L, He Y, Lai J, Wang J. Exposure to the Chinese famine in early life and the risk of hypertension in adulthood. J Hypertens 2011; 29: 1085-1092
4. Stöger R. The thrifty epigenotype: an acquired and heritable predisposition for obesity and diabetes?. Bioessays 2008; 30: 156-166
5. Dominguez-Salas P, Moore SE, Baker MS, Bergen AW, Cox SE, Dyer RA, et al. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Commun 2014; 5: 3746
6. Mozhui K, Smith AK, Tylavsky FA. Ancestry dependent DNA methylation and influence of maternal nutrition. PLoS One 2015; 10: e0118466
7. Schroeder JW, Conneely KN, Cubells JC, Kilaru V, Newport DJ, Knight BT, et al. Neonatal DNA methylation patterns associate with gestational age. Epigenetics 2011; 6: 1498-1504
8. Schulz LC. The Dutch Hunger Winter and the developmental origins of health and disease. Proc Natl Acad Sci USA 2010; 107: 16757-16758
9. Thurner S, Klimek P, Szell M, Duftschmid G, Endel G, Kautzky-Willer, et al. Quantification of excess risk for diabetes for those born in times of hunger, in an entire population of a nation, across a century. Proc Natl Acad Sci USA 2013; 110: 4703-4707
10. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 2008; 105: 17046-17049
11. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, et al. DNA methylation differences after exposure to prenatal famine are common and timing-And sex-specific. Hum Mol Genet 2009; 18: 4046-4053
12. Keating ST, El-Osta A. Epigenetics and metabolism. Circ Res 2015; 116: 715-736
13. King BM. The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight. Physiol Behav 2006; 87: 221-244
14. Dearden L, Ozanne SE. Early life origins of metabolic disease: developmental programming of hypothalamic pathways controlling energy homeostasis. Front Neuroendocrinol 2015; 39: 3-16
15. Gali Ramamoorthy T, Begum G, Harno E, White A. Developmental programming of hypothalamic neuronal circuits: impact on energy balance control. Front Neurosci 2015; 9: 126
16. Schneeberger M, Gomis R, Claret M. Hypothalamic and brainstem neuronal circuits controlling homeostatic energy balance. J Endocrinol 2014; 220: T25-T46
17. Hallschmid M, Benedict C, Schultes B, Born J, Kern W. Obese men respond to cognitive but not to catabolic brain insulin signaling. Int J Obes (Lond) 2008; 32: 275-282
18. Ross MG, Desai M. Developmental programming of appetite/satiety. Ann Nutr Metab 2014; 64: 36-44
19. Remacle C, Bieswal F, Bol V, Reusens B. Developmental programming of adult obesity and cardiovascular disease in rodents by maternal nutrition imbalance. Am J Clin Nutr 2011; 94: 1846S-1852S
20. Orozco-Solís R, Matos RJB, Guzmán-Quevedo O, Lopes de Souza S, Bihouée A, Houlgatte R, et al. Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One 2010; 5: e13537
21. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DIW, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008; 115: 1243-1249
22. van Dijk SJ, Molloy PL, Varinli H, Morrison JL, Muhlhausler BSMembers of EpiSCOPE. Epigenetics and human obesity. Int J Obes (Lond) 2015; 39: 85-97
23. Desai M, Jellyman JK, Ross MG. Epigenomics, gestational programming and risk of metabolic syndrome. Int J Obes (Lond) 2015; 39: 633-641
24. King AJF. The use of animal models in diabetes research. Br J Pharmacol 2012; 166: 877-894
25. Lavine RL, Voyles N, Perrino PV, Recant L. Functional abnormalities of islets of Langerhans of obese hyperglycemic mouse. Am J Physiol 1977; 233: E86-E90
26. Schmidt-Nielsen K, Haines HB, Hackel DB. Diabetes mellitus in the sand rat induced by standard laboratory diets. Science 1964; 143: 689-690
27. Marquie G, Duhault J, Hadjiisky P, Petkov P, Bouissou H. Diabetes mellitus in sand rats (Psammomys obesus): microangiopathy during development of the diabetic syndrome. Cell Mol Biol 1991; 37: 651-667
28. Walder KR, Fahey RP, Morton GJ, Zimmet PZ, Collier GR. Characterization of obesity phenotypes in Psammomys obesus (Israeli sand rats). Int J Exp Diabetes Res 2000; 1: 177-184
29. Kalderon B, Gutman A, Levy E, Shafrir E, Adler JH. Characterization of stages in development of obesity-diabetes syndrome in sand rat (Psammomys obesus). Diabetes 1986; 35: 717-724
30. Collier GR, McMillan JS, Windmill K, Walder K, Tenne-Brown J, de Silva, et al. Beacon: a novel gene involved in the regulation of energy balance. Diabetes 2000; 49: 1766-1771
31. Jowett JB, Elliott KS, Curran JE, Hunt N, Walder KR, Collier GR, et al. Genetic variation in BEACON influences quantitative variation in metabolic syndromerelated phenotypes. Diabetes 2004; 53: 2467-2472
32. Kaspi A, Ziemann M, Keating ST, Khurana I, Connor T, Spolding B, et al. Non-referenced genome assembly from epigenomic short-read data. Epigenetics 2014; 9: 1329-1338
33. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19: 1117-1123
34. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25: 1754-1760
35. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26: 139-140
36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403-410
37. Lonsdale J, Thomas J, Salvatore M, Phillips R, Lo E. The genotype-Tissue expression (GTEx) project. Nature 2013; 45: 580-585
38. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. EnsemblCompara GeneTrees: Complete, duplication-Aware phylogenetic trees in vertebrates. Genome Res 2009; 19: 327-335
39. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550
40. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA 2003; 100: 2538-2543
41. McMillen IC, Adam CL, Mühlhäusler BS. Early origins of obesity: programming the appetite regulatory system. J Physiol (Lond) 2005; 565: 9-17
42. Vimaleswaran KS, Tachmazidou I, Zhao JH, Hirschhorn JN, Dudbridge F, Loos RJF. Candidate genes for obesity-susceptibility show enriched association within a large genome-wide association study for BMI. Hum Mol Genet 2012; 21: 4537-4542
43. Dean M, Hamon Y, Chimini G. The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 2001; 42: 1007-1017
44. Quan Y, Barszczyk A, Feng Z-P, Sun H-S. Current understanding of K ATP channels in neonatal diseases: focus on insulin secretion disorders. Acta Pharmacol Sin 2011; 32: 765-780
45. Miki T, Liss B, Minami K, Shiuchi T, Saraya A, Kashima Y, et al. ATP-sensitive K+channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 2001; 4: 507-512
46. Pocai A, Lam TKT, Gutierrez-Juarez R, Obici S, Schwartz GJ, Bryan J, et al. Hypothalamic K(ATP) channels control hepatic glucose production. Nature 2005; 434: 1026-1031
47. Cook DL, Satin LS, Ashford ML, Hales CN. ATP-sensitive K+ channels in pancreatic beta-cells. Spare-channel hypothesis. Diabetes 1988; 37: 495-498
48. Seino S. ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu Rev Physiol 1999; 61: 337-362
49. Tarasov A, Dusonchet J, Ashcroft F. Metabolic regulation of the pancreatic beta-cell ATP-sensitive K+ channel: a pas de deux. Diabetes 2004; 53: S113-S122
50. Niswender KD, Morton GJ, Stearns WH, Rhodes CJ, Myers MG, Schwartz MW. Intracellular signalling. Key enzyme in leptin-induced anorexia. Nature 2001; 413: 794-795
51. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420: 629-635
52. Burridge K, Wennerberg K. Rho and Rac take center stage. Cell 2004; 116: 167-179
53. Huang H, Kong D, Byun KH, Ye C, Koda S, Lee DH, et al. Rho-kinase regulates energy balance by targeting hypothalamic leptin receptor signaling. Nat Neurosci 2012; 15: 1391-1398
54. Pistocchi A, Gaudenzi G, Carra S, Bresciani E, Del Giacco L, Cotelli F. Crucial role of zebrafish prox1 in hypothalamic catecholaminergic neurons development. BMC. Dev Biol 2008; 8: 27
55. Takeda Y, Jetten AM. Prospero-related homeobox 1 (Prox1) functions as a novel modulator of retinoic acid-related orphan receptors α-And ?-mediated transactivation. Nucleic Acids Res 2013; 41: 6992-7008
56. Millington GW. The role of proopiomelanocortin (POMC) neurones in feeding behaviour. Nutr Metab (Lond) 2007; 4: 18
57. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Grüters A. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 1998; 19: 155-157
58. Lu D, Willard D, Patel IR, Kadwell S, Overton L, Kost T, et al. Agouti protein is an antagonist of the melanocyte-stimulating-hormone receptor. Nature 1994; 371: 799-802
59. Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS. Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 1999; 96: 541-551
60. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJP, et al. An aminoacid taste receptor. Nature 2002; 416: 199-202
61. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJP, et al. The receptors for mammalian sweet and umami taste. Cell 2003; 115: 255-266
62. Ren X, Zhou L, Terwilliger R, Newton SS, de Araujo IE. Sweet taste signaling functions as a hypothalamic glucose sensor. Front Integr Neurosci 2009; 3: 12
63. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010; 466: 253-257
64. Jjingo D, Conley AB, Yi SV, Lunyak VV, Jordan IK. On the presence and role of human gene-body DNA methylation. Oncotarget 2012; 3: 462-474
65. Shukla S, Kavak E, Gregory M, Imashimizu M. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 2011; 479: 74-79
66. Yang X, Han H, De Carvalho DD, Lay FD, Jones PA, Liang G. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 2014; 26: 577-590
67. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 2001; 411: 480-484
68. Guerra-Crespo M, Pérez-Monter C, Janga SC, Castillo-Ramírez S, Gutiérrez-Rios RM, Joseph-Bravo P, et al. Transcriptional profiling of fetal hypothalamic TRH neurons. BMC Genomics 2010; 12: 222-222