Evidence for transgenerational metabolic programming in Drosophila

DMM Disease Models and Mechanisms

Volumn 6, Issue 5, 2013, Pages 1123-1132

  Buescher, Jessica L ^a   Musselman, Laura P ^a   Wilson, Christina A ^a   Lang, Tieming ^a   Keleher, Madeline ^a   Baranski, Thomas J ^a   Duncan, Jennifer G ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BODY COMPOSITION; CALORIE; DROSOPHILA; FEEDING; FEMALE; GENE EXPRESSION; LARVA; MALE; MATERNAL NUTRITION; METABOLIC ENGINEERING; NONHUMAN; NUTRITIONAL ASSESSMENT; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROGENY;

ANIMALS; BODY COMPOSITION; CARBOHYDRATES; CROSSES, GENETIC; DIET; DROSOPHILA MELANOGASTER; EPISTASIS, GENETIC; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION PROFILING; HEREDITY; INHERITANCE PATTERNS; LARVA; MALE; METABOLISM; OBESITY; PHENOTYPE;

EID: 84883872095     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.011924     Document Type: Article

References (45)

1. Aguila, J. R., Suszko, J., Gibbs, A. G. and Hoshizaki, D. K. (2007). The role of larval fat cells in adult Drosophila melanogaster. J. Exp. Biol. 210, 956-963.
2. Andres, A. J. and Thummel, C. S. (1994). Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol. 44, 565-573.
3. Backhaus, B. S. E., Sulkowski, E. and Schlote F. W. (1984). A semi-synthetic, generalpurpose medium for Drosophila melanogaster. Drosoph. Inf. Serv. 60, 210-212.
4. Baker, K. D. and Thummel, C. S. (2007). Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab. 6, 257-266.
5. Baker, J. L., Olsen, L. W. and Sørensen, T. I. (2007). Childhood body-mass index and the risk of coronary heart disease in adulthood. N. Engl. J. Med. 357, 2329-2337.
6. Birse, R. T., Choi, J., Reardon, K., Rodriguez, J., Graham, S., Diop, S., Ocorr, K., Bodmer, R. and Oldham, S. (2010). High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metab. 12, 533-544.
7. Boerschmann, H., Pflüger, M., Henneberger, L., Ziegler, A. G. and Hummel, S. (2010). Prevalence and predictors of overweight and insulin resistance in offspring of mothers with gestational diabetes mellitus. Diabetes Care 33, 1845-1849.
8. Bujold, M., Gopalakrishnan, A., Nally, E. and King-Jones, K. (2010). Nuclear receptor DHR96 acts as a sentinel for low cholesterol concentrations in Drosophila melanogaster. Mol. Cell. Biol. 30, 793-805.
9. Field, A. E., Cook, N. R. and Gillman, M. W. (2005). Weight status in childhood as a predictor of becoming overweight or hypertensive in early adulthood. Obes. Res. 13, 163-169.
10. Fraser, A., Tilling, K., Macdonald-Wallis, C., Sattar, N., Brion, M. J., Benfield, L., Ness, A., Deanfield, J., Hingorani, A., Nelson, S. M. et al. (2010). Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood. Circulation 121, 2557-2564.
11. Fujikawa, K., Takahashi, A., Nishimura, A., Itoh, M., Takano-Shimizu, T. and Ozaki, M. (2009). Characteristics of genes up-regulated and down-regulated after 24 h starvation in the head of Drosophila. Gene 446, 11-17.
12. Gemma, C., Sookoian, S., Alvariñas, J., García, S. I., Quintana, L., Kanevsky, D., González, C. D. and Pirola, C. J. (2009). Maternal pregestational BMI is associated with methylation of the PPARGC1A promoter in newborns. Obesity (Silver Spring) 17, 1032-1039.
13. Hochner, H., Friedlander, Y., Calderon-Margalit, R., Meiner, V., Sagy, Y., Avgil-Tsadok, M., Burger, A., Savitsky, B., Siscovick, D. S. and Manor, O. (2012). Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem Perinatal Family Follow-up Study. Circulation 125, 1381-1389.
14. Horne, I., Haritos, V. S. and Oakeshott, J. G. (2009). Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem. Mol. Biol. 39, 547-567.
15. Horner, M. A., Pardee, K., Liu, S., King-Jones, K., Lajoie, G., Edwards, A., Krause, H. M. and Thummel, C. S. (2009). The Drosophila DHR96 nuclear receptor binds cholesterol and regulates cholesterol homeostasis. Genes Dev. 23, 2711-2716.
16. Jünger, M. A., Rintelen, F., Stocker, H., Wasserman, J. D., Végh. M., Radimerski, T., Greenberg, M. E. and Hafen E. (2003). The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2, 20.
17. Juonala, M., Magnussen, C. G., Berenson, G. S., Venn, A., Burns, T. L., Sabin, M. A., Srinivasan, S. R., Daniels, S. R., Davis, P. H., Chen, W. et al. (2011). Childhood adiposity, adult adiposity, and cardiovascular risk factors. N. Engl. J. Med. 365, 1876-1885.
18. Kavanagh, K., Sajadian, S., Jenkins, K. A., Wilson, M. D., Carr, J. J., Wagner, J. D. and Rudel, L. L. (2010). Neonatal and fetal exposure to trans-fatty acids retards early growth and adiposity while adversely affecting glucose in mice. Nutr. Res. 30, 418-426.
19. Krauss, V. and Reuter, G. (2011). DNA methylation in Drosophila-a critical evaluation. Prog. Mol. Biol. Transl. Sci. 101, 177-191.
20. Li, J., Huang, J., Li, J. S., Hong, C., Huang, K. and Zheng, L. (2012). Accumulation of endoplasmic reticulum stress and lipogenesis in the liver through generational effects of high fat diets. J. Hepatol. 56, 900-907
21. McMillen, I. C. and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633.
22. Mitchell, M., Schulz, S. L., Armstrong, D. T. and Lane, M. (2009). Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biol. Reprod. 80, 622-630.
23. Musselman, L. P., Fink, J. L., Narzinski, K., Ramachandran, P. V., Hathiramani, S. S., Cagan, R. L. and Baranski, T. J. (2011). A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Model. Mech. 4, 842-849.
24. Na, J., Musselman, L. P., Pendse, J., Baranski, T. J., Bodmer, R., Ocorr, K. and Cagan, R. (2013). A Drosophila model of high sugar diet-induced cardiomyopathy. PLoS Genet. 9, e1003175.
25. Palanker, L., Tennessen, J. M., Lam, G. and Thummel, C. S. (2009). Drosophila HNF4 regulates lipid mobilization and beta-oxidation. Cell Metab. 9, 228-239.
26. Pasco, M. Y. and Léopold, P. (2012). High sugar-induced insulin resistance in Drosophila relies on the lipocalin Neural Lazarillo. PLoS ONE 7, e36583.
27. Pinney, S. E. and Simmons, R. A. (2012). Metabolic programming, epigenetics, and gestational diabetes mellitus. Curr. Diab. Rep. 12, 67-74.
28. Pistillo, D., Manzi, A., Tino, A., Boyl, P. P., Graziani, F. and Malva, C. (1998). The Drosophila melanogaster lipase homologs: a gene family with tissue and developmental specific expression. J. Mol. Biol. 276, 877-885.
29. Rajia, S., Chen, H. and Morris, M. J. (2010). Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet. J. Neuroendocrinol. 22, 905-914.
30. Reece, E. A. (2010). The fetal and maternal consequences of gestational diabetes mellitus. J. Matern. Fetal Neonatal Med. 23, 199-203.
31. Ringrose, L., Ehret, H. and Paro, R. (2004). Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol. Cell 16, 641-653.
32. Ruaud, A. F., Lam, G. and Thummel, C. S. (2011). The Drosophila NR4A nuclear receptor DHR38 regulates carbohydrate metabolism and glycogen storage. Mol. Endocrinol. 25, 83-91.
33. Schlegel, A. and Stainier, D. Y. (2007). Lessons from "lower" organisms: what worms, flies, and zebrafish can teach us about human energy metabolism. PLoS Genet. 3, e199.
34. Sieber, M. H. and Thummel, C. S. (2009). The DHR96 nuclear receptor controls triacylglycerol homeostasis in Drosophila. Cell Metab. 10, 481-490.
35. Simmons, R. A., Templeton, L. J. and Gertz, S. J. (2001). Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50, 2279-2286.
36. Sullivan, E. L., Smith, M. S. and Grove, K. L. (2011). Perinatal exposure to high-fat diet programs energy balance, metabolism and behavior in adulthood. Neuroendocrinology 93, 1-8.
37. Symonds, M. E., Sebert, S. P., Hyatt, M. A. and Budge, H. (2009). Nutritional programming of the metabolic syndrome. Nat. Rev. Endocrinol. 5, 604-610.
38. Tamashiro, K. L., Terrillion, C. E., Hyun, J., Koenig, J. I. and Moran, T. H. (2009). Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 58, 1116-1125.
39. Tan, C. Y. and Vidal-Puig, A. (2008). Adipose tissue expandability: the metabolic problems of obesity may arise from the inability to become more obese. Biochem. Soc. Trans. 36, 935-940.
40. Turdi, S., Ge, W., Hu, N., Bradley, K. M., Wang, X. and Ren, J. (2013). Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects. J. Mol. Cell. Cardiol. 55, 117-129.
41. Tzeng, T. Y., Lee, C. H., Chan, L. W. and Shen, C. K. (2007). Epigenetic regulation of the Drosophila chromosome 4 by the histone H3K9 methyltransferase dSETDB1. Proc. Natl. Acad. Sci. USA 104, 12691-12696.
42. Vickers, M. H., Clayton, Z. E., Yap, C. and Sloboda, D. M. (2011). Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sexspecific changes in fetal and neonatal endocrine function. Endocrinology 152, 1378-1387.
43. Warner, M. J. and Ozanne, S. E. (2010). Mechanisms involved in the developmental programming of adulthood disease. Biochem. J. 427, 333-347.
44. Waterland, R. A., Travisano, M., Tahiliani, K. G., Rached, M. T. and Mirza, S. (2008). Methyl donor supplementation prevents transgenerational amplification of obesity. Int. J. Obes. (Lond.) 32, 1373-1379.
45. Xu, X., Gopalacharyulu, P., Seppänen-Laakso, T., Ruskeepää, A. L., Aye, C. C., Carson, B. P., Mora, S., Orešič, M. and Teleman, A. A. (2012). Insulin signaling regulates fatty acid catabolism at the level of CoA activation. PLoS Genet. 8, e1002478.