Epigenetic changes in fetal hypothalamic energy regulating pathways are associated with maternal undernutrition and twinning

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1694-1703

  Begum, Ghazala ^a   Stevens, Adam ^b   Smith, Emma Bolton ^a   Connor, Kristin ^e,f   Challis, John R G ^f   Bloomfield, Frank ^c,d,e   White, Anne ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

^e National Research Centre for Growth and Development Auckland   (New Zealand)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

Glucocorticoid receptor; Methylation analysis; Proopiomelanocortin

Indexed keywords

DNA METHYLTRANSFERASE; GLUCOCORTICOID RECEPTOR; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENERGY BALANCE; ENZYME ACTIVITY; EPIGENETICS; FETUS; HISTONE ACETYLATION; HISTONE METHYLATION; HYPOTHALAMUS; MALNUTRITION; MATERNAL NUTRITION; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; SHEEP; TWIN PREGNANCY;

ANIMALS; DNA METHYLATION; ENERGY METABOLISM; EPIGENESIS, GENETIC; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYPOTHALAMUS; MALNUTRITION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PREGNANCY; PREGNANCY COMPLICATIONS; PRO-OPIOMELANOCORTIN; PROMOTER REGIONS, GENETIC; RANDOM ALLOCATION; RECEPTORS, GLUCOCORTICOID; SHEEP; TWINS;

OVIS ARIES;

EID: 84860912504     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-198762     Document Type: Article

References (54)

1. Hales, C. N., and Barker, D. J. (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595-601
2. Gluckman, P. D., Hanson, M. A., Cooper, C., and Thornburg, K. L. (2008) Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61-73
3. Barker, D. J. (2007) The origins of the developmental origins theory. J. Intern. Med. 261, 412-417
4. Hales, C. N., and Barker, D. J. (2001) The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5-20 (Pubitemid 34123501)
5. Poulsen, P., Grunnet, L. G., Pilgaard, K., Storgaard, H., Alibegovic, A., Sonne, M. P., Carstensen, B., Beck-Nielsen, H., and Vaag, A. (2009) Increased risk of type 2 diabetes in elderly twins. Diabetes 58, 1350-1355
6. The, N. S., Adair, L. S., and Gordon-Larsen, P. (2010) A study of the birth weight-obesity relation using a longitudinal cohort and sibling and twin pairs. Am. J. Epidemiol. 172, 549-557
7. Todd, S. E., Oliver, M. H., Jaquiery, A. L., Bloomfield, F. H., and Harding, J. E. (2009) Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr. Res. 65, 409-413
8. Buckler, J. M., and Green, M. (2004) A comparison of the early growth of twins and singletons. Ann. Hum. Biol. 31, 311-332 (Pubitemid 38852075)
9. Van Dommelen, P., de Gunst, M., van der Vaart, A., van Buuren, S., and Boomsma, D. (2008) Growth references for height, weight and body mass index of twins aged 0-2.5 years. Acta Paediatr. 97, 1099-1104
10. Poulsen, P., Vaag, A. A., Kyvik, K. O., Moller Jensen, D., and Beck-Nielsen, H. (1997) Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia 40, 439-446 (Pubitemid 27132614)
11. Monrad, R. N., Grunnet, L. G., Rasmussen, E. L., Malis, C., Vaag, A., and Poulsen, P. (2009) Age-dependent nongenetic influences of birth weight and adult body fat on insulin sensitivity in twins. J. Clin. Endocrinol. Metab. 94, 2394-2399
12. Brady, L. S., Smith, M. A., Gold, P. W., and Herkenham, M. (1990) Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 52, 441-447 (Pubitemid 20366597)
13. Wardlaw, S. L., McCarthy, K. C., and Conwell, I. M. (1998) Glucocorticoid regulation of hypothalamic proopiomelanocortin. Neuroendocrinology 67, 51-57 (Pubitemid 28039380)
14. Beaulieu, S., Gagne, B., and Barden, N. (1988) Glucocorticoid regulation of proopiomelanocortin messenger ribonucleic acid content of rat hypothalamus. Mol. Endocrinol. 2, 727-731
15. Zakrzewska, K. E., Sainsbury, A., Cusin, I., Rouru, J., Jeanrenaud, B., and Rohner-Jeanrenaud, F. (1999) Selective dependence of intracerebroventricular neuropeptide Y-elicited effects on central glucocorticoids. Endocrinology 140, 3183-3187 (Pubitemid 30650635)
16. Delahaye, F., Breton, C., Risold, P. Y., Enache, M., Dutriez-Casteloot, I., Laborie, C., Lesage, J., and Vieau, D. (2008) Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149, 470-475 (Pubitemid 351159317)
17. Coupe, B., Amarger, V., Grit, I., Benani, A., and Parnet, P. (2010) Nutritional programming affects hypothalamic organization and early response to leptin. Endocrinology 151, 702-713
18. Plagemann, A., Harder, T., Brunn, M., Harder, A., Roepke, K., Wittrock-Staar, M., Ziska, T., Schellong, K., Rodekamp, E., Melchior, K., and Dudenhausen, J. W. (2009) Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J. Physiol. 587, 4963-4976
19. Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., and Meaney, M. J. (2004) Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854 (Pubitemid 38989508)
20. Symonds, M. E., and Budge, H. (2009) Nutritional models of the developmental programming of adult health and disease. Proc. Nutr. Soc. 68, 173-178
21. Stevens, A., Begum, G., Cook, A., Connor, K., Rumball, C., Oliver, M., Challis, J., Bloomfield, F., and White, A. (2010) Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology 151, 3652-3664
22. Muhlhausler, B. S., McMillen, I. C., Rouzaud, G., Findlay, P. A., Marrocco, E. M., Rhind, S. M., and Adam, C. L. (2004) Appetite regulatory neuropeptides are expressed in the sheep hypothalamus before birth. J. Neuroendocrinol. 16, 502-507 (Pubitemid 38878281)
23. Langlais, D., Couture, C., Sylvain-Drolet, G., and Drouin, J. (2011) A pituitary-specific enhancer of the POMC gene with preferential activity in corticotrope cells. Mol. Endocrinol. 25, 348-359
24. De Souza, F. S., Santangelo, A. M., Bumaschny, V., Avale, M. E., Smart, J. L., Low, M. J., and Rubinstein, M. (2005) Identification of neuronal enhancers of the proopiomelanocortin gene by transgenic mouse analysis and phylogenetic footprinting. Mol. Cell. Biol. 25, 3076-3086 (Pubitemid 40464311)
25. Geng, C. D., Schwartz, J. R., and Vedeckis, W. V. (2008) A conserved molecular mechanism is responsible for the auto-up-regulation of glucocorticoid receptor gene promoters. Mol. Endocrinol. 22, 2624-2642
26. Portela, A., and Esteller, M. (2010) Epigenetic modifications and human disease. Nat. Biotechnol. 28, 1057-1068
27. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (Pubitemid 46802390)
28. Berger, S. L. (2007) The complex language of chromatin regulation during transcription. Nature 447, 407-412
29. Stevens, A., Begum, G., and White, A. (2011) Epigenetic changes in the hypothalamic pro-opiomelanocortin gene: a mechanism linking maternal undernutrition to obesity in the offspring? Eur. J. Pharmacol. 660, 194-201
30. Schwartz, J., and Rose, J. C. (1998) Development of the pituitary adrenal axis in fetal sheep twins. Am. J. Physiol. 274, R1-R8
31. Crosby, S. R., Stewart, M. F., Ratcliffe, J. G., and White, A. (1988) Direct measurement of the precursors of adrenocorticotropin in human plasma by two-site immunoradiometric assay. J. Clin. Endocrinol. Metab. 67, 1272-1277 (Pubitemid 19012964)
32. Sebert, S. P., Hyatt, M. A., Chan, L. L., Patel, N., Bell, R. C., Keisler, D., Stephenson, T., Budge, H., Symonds, M. E., and Gardner, D. S. (2009) Maternal nutrient restriction between early and midgestation and its impact upon appetite regulation after juvenile obesity. Endocrinology 150, 634-641
33. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25, 402-408 (Pubitemid 34164012)
34. Gupta, S., Dennis, J., Thurman, R. E., Kingston, R., Stamatoy-annopoulos, J. A., and Noble, W. S. (2008) Predicting human nucleosome occupancy from primary sequence. PLoS Comput. Biol. 4, e1000134
35. Dennis, J. H., Fan, H. Y., Reynolds, S. M., Yuan, G., Meldrim, J. C., Richter, D. J., Peterson, D. G., Rando, O. J., Noble, W. S., and Kingston, R. E. (2007) Independent and complementary methods for large-scale structural analysis of mammalian chromatin. Genome Res. 17, 928-939 (Pubitemid 46919727)
36. Ozsolak, F., Song, J. S., Liu, X. S., and Fisher, D. E. (2007) High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 25, 244-248 (Pubitemid 46227125)
37. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S. L., and Lander, E. S. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326
38. Bernstein, B. E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D. K., Huebert, D. J., McMahon, S., Karlsson, E. K., Kulbokas, E. J., 3rd, Gingeras, T. R., Schreiber, S. L., and Lander, E. S. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169-181 (Pubitemid 40174761)
39. Ohlsson, R., Bartkuhn, M., and Renkawitz, R. (2010) CTCF shapes chromatin by multiple mechanisms: the impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 119, 351-360
40. Ernst, J., and Kellis, M. (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 28, 817-825
41. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., Ku, M., Durham, T., Kellis, M., and Bernstein, B. E. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49
42. Surani, M. A., Hayashi, K., and Hajkova, P. (2007) Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762 (Pubitemid 46273582)
43. Schneider, E., Pliushch, G., El Hajj, N., Galetzka, D., Puhl, A., Schorsch, M., Frauenknecht, K., Riepert, T., Tresch, A., Muller, A. M., Coerdt, W., Zechner, U., and Haaf, T. (2010) Spatial, temporal and interindividual epigenetic variation of functionally important DNA methylation patterns. Nucleic Acids Res. 38, 3880-3890
44. Turner, B. M. (2009) Epigenetic responses to environmental change and their evolutionary implications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3403-3418
45. Newell-Price, J. (2003) Proopiomelanocortin gene expression and DNA methylation: implications for Cushing's syndrome and beyond. J. Endocrinol. 177, 365-372
46. Ho, S. M., and Tang, W. Y. (2007) Techniques used in studies of epigenome dysregulation due to aberrant DNA methylation: an emphasis on fetal-based adult diseases. Reprod. Toxicol. 23, 267-282
47. Razin, A., and Cedar, H. (1993) DNA methylation and embryogenesis. EXS 64, 343-357
48. Ikenasio-Thorpe, B. A., Breier, B. H., Vickers, M. H., and Fraser, M. (2007) Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J. Endocrinol. 193, 31-37 (Pubitemid 46638529)
49. Marino, J. S., Xu, Y., and Hill, J. W. (2011) Central insulin and leptin-mediated autonomic control of glucose homeostasis. Trends Endocrinol. Metab. 22, 275-285
50. Messeguer, X., Escudero, R., Farre, D., Nunez, O., Martinez, J., and Alba, M. M. (2002) PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18, 333-334 (Pubitemid 34183117)
51. Farre, D., Roset, R., Huerta, M., Adsuara, J. E., Rosello, L., Alba, M. M., and Messeguer, X. (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res. 31, 3651-3653 (Pubitemid 37442215)
52. Edwards, L. J., and McMillen, I. C. (2002) Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamopituitary adrenal axis in sheep during late gestation. Biol. Reprod. 66, 1562-1569 (Pubitemid 34462304)
53. Rumball, C. W., Bloomfield, F. H., Oliver, M. H., and Harding, J. E. (2009) Different periods of periconceptional undernutrition have different effects on growth, metabolic and endocrine status in fetal sheep. Pediatr. Res. 66, 605-613
54. Rumball, C. W., Harding, J. E., Oliver, M. H., and Bloomfield, F. H. (2008) Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose-insulin axis function in ovine pregnancy. J. Physiol. 586, 1399-1411 (Pubitemid 351321276)