Metabolomic and gene expression profiles exhibit modular genetic and dietary structure linking metabolic syndrome phenotypes in Drosophila

G3: Genes, Genomes, Genetics

Volumn 5, Issue 12, 2015, Pages 2817-2829

  Williams, Stephanie ^a   Dew Budd, Kelly ^a,b   Davis, Kristen ^a   Anderson, Julie ^a   Bishop, Ruth ^b   Freeman, Kenda ^a   Davis, Dana ^b   Bray, Katherine ^b   Perkins, Lauren ^b   Hubickey, Joana ^b   Reed, Laura K ^a,b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA   (United States)

Author keywords

Canalization; Drosophila; Genotype by environment interaction; Metabolic syndrome; metabolomics

Indexed keywords

CYTOCHROME P450; DISACCHARIDE; DOPAMINE; FAT; GLUCOSE; ISOLEUCINE; LEUCINE; LEVODOPA; LINOLENIC ACID; MALTOSE; N ARACHIDONOYL DOPAMINE; PHOSPHOLIPASE; SATURATED FATTY ACID; SUGAR; SUGAR ALCOHOL; TRIACYLGLYCEROL; TYROSINE; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIETARY INTAKE; DROSOPHILA MELANOGASTER; ENDOPHENOTYPE; ENERGY METABOLISM; FAT INTAKE; FOLLOW UP; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INTERACTION; GENETIC ANALYSIS; GENETIC LINE; GENOTYPE; HEREDITY; LARVA; METABOLIC SYNDROME X; METABOLOMICS; METAMORPHOSIS; NONHUMAN; OBESITY; PHENOTYPIC VARIATION; PHYSIOLOGICAL PROCESS; POPULATION; RESPIRATORY CHAIN; ANIMAL; ANIMAL FOOD; CLUSTER ANALYSIS; DROSOPHILA; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; METABOLOME; PHENOTYPE; POPULATION GENETICS;

ANIMAL FEED; ANIMALS; CLUSTER ANALYSIS; DROSOPHILA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDIES; GENETICS, POPULATION; GENOTYPE; METABOLIC SYNDROME X; METABOLOME; METABOLOMICS; PHENOTYPE; TRANSCRIPTOME;

EID: 84949993090     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.023564     Document Type: Article

References (55)

1. Adamski, J., and K. Suhre, 2013 Metabolomics platforms for genome wide association studies-linking the genome to the metabolome. Curr. Opin. Biotechnol. 24: 39-47.
2. Aftring, R. P., K. P. Block, and M. G. Buse, 1986 Leucine and isoleucine activate skeletal muscle branched-chain alpha-keto acid dehydrogenase in vivo. AJP-. Am. J. Physiol. 250: E599-E604.
3. Ayroles, J. F., and G. Gibson, 2006 Analysis of variance of microarray data. Methods Enzymol. 411: 214-233.
4. Bellocchio, L., C. Cervino, R. Pasquali, and U. Pagotto, 2008 The endocannabinoid system and energy metabolism. J. Neuroendocrinol. 20: 850-857.
5. Benoit, S. C., C. J. Kemp, C. F. Elias, W. Abplanalp, J. P. Herman et al., 2009 Palmitic acid mediates hypothalamic insulin resistance by altering PKC-theta subcellular localization in rodents. J. Clin. Invest. 119: 2577-2589.
6. Bhattacharya, S., C. B. Granger, D. Craig, C. Haynes, J. Bain et al., 2014 Validation of the association between a branched chain amino acid metabolite profile and extremes of coronary artery disease in patients referred for cardiac catheterization. Atherosclerosis 232: 191-196.
7. Bisogno, T., D. Melck, M. Yu. Bobrov, N. M. Gretskaya, V. V. Bezuglov et al., 2000 N-acyl-dopamines: novel synthetic CB(1) cannabinoid-receptor ligands and inhibitors of anandamide inactivation with cannabimimetic activity in vitro and in vivo. Biochem. J. 351: 817-824.
8. Bisogno, T., A. Ligresti, and V. Di Marzo, 2005 The endocannabinoid signalling system: biochemical aspects. Pharmacol. Biochem. Behav. 81: 224-238.
9. Bodmer, R., and T. V. Venkatesh, 1998 Heart development in Drosophila and vertebrates: conservation of molecular mechanisms. Dev. Genet. 22: 181-186.
10. Cao, H., K. Gerhold, J. R. Mayers, M. M. Wiest, S. M. Watkins et al., 2008 Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134: 933-944.
11. Chintapalli, V. R., M. Bratty Al, D. Korzekwa, D. G. Watson, and J. A. T. Dow, 2013 Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high resolution mass spectrometry. PLoS One 8: e78066.
12. Combaret, L., D. Dardevet, I. Rieu, M.-N. Pouch, D. Béchet et al., 2005 A leucine-supplemented diet restores the defective postprandial inhibition of proteasome-dependent proteolysis in aged rat skeletal muscle. J. Physiol. 569: 489-499.
13. Cota, D., K. Proulx, K. A. B. Smith, S. C. Kozma, G. Thomas et al., 2006 Hypothalamic mTOR signaling regulates food intake. Science 312: 927-930.
14. Danielsen, T. E., M. E. Moeller, and K. F. Rewitz, 2013 Nutrient signaling and developmental timing of maturation. Curr. Top. Dev. Biol. 105: 37-67.
15. de Loof, A., 2008 Ecdysteroids, juvenile hormone and insect neuropeptides: recent successes and remaining major challenges. Gen. Comp. Endocrinol. 155: 3-13.
16. Doi, M., I. Yamaoka, M. Nakayama, K. Sugahara, and F. Yoshizawa, 2007 Hypoglycemic effect of isoleucine involves increased muscle glucose uptake and whole body glucose oxidation and decreased hepatic gluconeogenesis. Am. J. Physiol. Endocrinol. Metab. 292: E1683-E1693.
17. Fattore, E., and R. Fanelli, 2013 Palm oil and palmitic acid: a review on cardiovascular effects and carcinogenicity. Int. J. Food Sci. Nutr. 64: 648-659.
18. Flatt, T., and T. J. Kawecki, 2007 Juvenile hormone as a regulator of the trade-offbetween reproduction and life span in Drosophila melanogaster. Evolution 61: 1980-1991.
19. Gibson, G., 2009 Decanalization and the origin of complex disease. Nat. Rev. Genet. 10: 134-140.
20. Gibson, G., and L. K. Reed, 2008 Cryptic genetic variation. Curr. Biol. 18: R989-R990.
21. Git, A., H. Dvinge, M. Salmon-Divon, M. Osborne, C. Kutter et al., 2010 Systematic comparison of microarray profiling, real-time PCR, and next-generation sequencing technologies for measuring differential microRNA expression. RNA 16: 991-1006.
22. Harbison, S. T., M. A. Carbone, J. F. Ayroles, E. A. Stone, R. F. Lyman et al., 2009 Co-regulated transcriptional networks contribute to natural genetic variation in Drosophila sleep. Nat. Genet. 41: 371-375.
23. Hoffman, J. M., Q. A. Soltow, S. Li, A. Sidik, D. P. Jones et al., 2014 Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster. Aging Cell 13: 596-604.
24. Hoffmann, J. A., and J.-M. Reichhart, 2002 Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3: 121-126.
25. Huang, D. W., B. T. Sherman, and R. A. Lempicki, 2009a Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
26. Huang, D. W., B. T. Sherman, and R. A. Lempicki, 2009b Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37: 1-13.
27. Huang, W. W., S. S. Richards, M. A. M. Carbone, D. D. Zhu, R. R. H. R. Anholt et al., 2012 Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc. Natl. Acad. Sci. USA 109: 15553-15559.
28. Johnson, E. S., K. R. Lindblom, A. Robeson, R. D. Stevens, O. R. Ilkayeva et al., 2013 Metabolomic profiling reveals a role for caspase-2 in lipoapoptosis. J. Biol. Chem. 288: 14463-14475.
29. Koyama, T., C. C. Mendes, and C. K. Mirth, 2013 Mechanisms regulating nutrition-dependent developmental plasticity through organ-specific effects in insects. Front. Physiol. 4: 263.
30. Mensink, R. P., P. L. Zock, A. D. M. Kester, and M. B. Katan, 2003 Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am. J. Clin. Nutr. 77: 1146-1155.
31. Mirth, C. K., J. W. Truman, and L. M. Riddiford, 2009 The ecdysone receptor controls the post-critical weight switch to nutrition-independent differentiation in Drosophila wing imaginal discs. Development 136: 2345-2353.
32. Monda, K. L., K. E. North, S. C. Hunt, D. C. Rao, M. A. Province et al., 2010 The genetics of obesity and the metabolic syndrome. Endocr. Metab. Immune Disord. Drug Targets 10: 86-108.
33. Morey, J. S., J. C. Ryan, and F. M. Van Dolah, 2006 Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol. Proced. Online 8: 175-193.
34. Musselman, L. P., J. L. Fink, K. Narzinski, P. V. Ramachandran, S. S. Hathiramani et al., 2011 A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Model. Mech. 4: 842-849.
35. O'Rahilly, S., and I. S. Farooqi, 2006 Genetics of obesity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361: 1095-1105.
36. Ogden, C. L., M. D. Carroll, B. K. Kit, and K. M. Flegal, 2014 Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 311: 806-814.
37. Patel, M. J., B. C. Batch, L. P. Svetkey, J. R. Bain, C. B. Turer et al., 2013 Race and sex differences in small-molecule metabolites and metabolic hormones in overweight and obese adults. OMICS 17: 627-635.
38. Ralevic, V., 2003 Cannabinoid modulation of peripheral autonomic and sensory neurotransmission. Eur. J. Pharmacol. 472: 1-21.
39. Reed, L. K., K. Lee, Z. Zhang, L. Rashid, A. Poe et al., 2014 Systems genomics of metabolic phenotypes in wild-type Drosophila melanogaster. Genetics 197: 781-793.
40. Reed, L. K., S. Williams, M. Springston, J. Brown, K. Freeman et al., 2010 Genotype-by-diet interactions drive metabolic phenotype variation in Drosophila melanogaster. Genetics 185: 1009-1019.
41. Riddiford, L. M., 2012 How does juvenile hormone control insect metamorphosis and reproduction? Gen. Comp. Endocrinol. 179: 477-484.
42. Rosenthal, J., A. Angel, and J. Farkas, 1974 Metabolic fate of leucine: a significant sterol precursor in adipose tissue and muscle. Am. J. Physiol. 226: 411-418.
43. Rulifson, E. J., S. K. Kim, and R. Nusse, 2002 Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-1120.
44. Scholtens, D. M., M. J. Muehlbauer, N. R. Daya, R. D. Stevens, A. R. Dyer et al. HAPO Study Cooperative Research Group, 2014 Metabolomics reveals broad-scale metabolic perturbations in hyperglycemic mothers during pregnancy. Diabetes Care 37: 158-166.
45. Schulz, L. O., P. H. Bennett, E. Ravussin, J. R. Kidd, K. K. Kidd, J. Esparza, and M. E. Valencia, 2006 Effects of traditional and Western environments on prevalence of type 2 diabetes in Pima Indians in Mexico and the U.S. Diabetes Care 29: 1866-1871.
46. Schwedes, C. C., and G. E. Carney, 2012 Ecdysone signaling in adult Drosophila melanogaster. J. Insect Physiol. 58: 293-302.
47. Shin, S.-Y., E. B. Fauman, A.-K. Petersen, J. Krumsiek, R. Santos et al., 2014 An atlas of genetic influences on human blood metabolites. Nat. Genet. 46: 543-550.
48. Stone, E. A., and J. F. Ayroles, 2009 Modulated modularity clustering as an exploratory tool for functional genomic inference. PLoS Genet. 5: e1000479.
49. Tennessen, J. M., and C. S. Thummel, 2011 Coordinating growth and maturation-insights from Drosophila. Curr. Biol. 21: R750-R757.
50. Tennessen, J. M., N. M. Bertagnolli, J. Evans, M. H. Sieber, J. Cox et al., 2014 Coordinated metabolic transitions during Drosophila embryogenesis and the onset of aerobic glycolysis. G3 (Bethesda) 4: 839-850.
51. Wessells, R. J., E. Fitzgerald, J. R. Cypser, M. Tatar, and R. Bodmer, 2004 Insulin regulation of heart function in aging fruit flies. Nat. Genet. 36: 1275-1281.
52. Yamada, Y., K. Kato, T. Hibino, K. Yokoi, and H. Matsuo, 2007 Prediction of genetic risk for metabolic syndrome. Atherosclerosis 191: 298-304.
53. Yamanaka, N., K. F. Rewitz, and M. B. O'Connor, 2013 Ecdysone control of developmental transitions: lessons from Drosophila research. Annu. Rev. Entomol. 58: 497-516.
54. Yang, Z.-H., H. Miyahara, and A. Hatanaka, 2011 Chronic administration of palmitoleic acid reduces insulin resistance and hepatic lipid accumulation in KK-Ay mice with genetic type 2 diabetes. Lipids Health Dis. 10: 120.
55. Zeanandin, G., M. Balage, S. M. Schneider, J. Dupont, X. Hébuterne et al., 2011 Differential effect of long-term leucine supplementation on skeletal muscle and adipose tissue in old rats: an insulin signaling pathway approach. Age (Omaha) 34: 371-387.