The effects of age and dietary restriction on the tissue-specific metabolome of Drosophila

Aging Cell

Volumn 14, Issue 5, 2015, Pages 797-808

  Laye, Matthew J ^a   Tran, Vilinh ^b   Jones, Dean P ^b   Kapahi, Pankaj ^a   Promislow, Daniel E L ^c  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Aging; Bioinformatics; Dietary restriction; Drosophila; Metabolome; Metabolomics

Indexed keywords

ABDOMEN; ADULT; AGE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; HEAD; HOMEOSTASIS; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; THORAX; TISSUE SPECIFICITY; ANIMAL; CALORIC RESTRICTION; DROSOPHILA MELANOGASTER; FOOD DEPRIVATION; METABOLISM; MULTIVARIATE ANALYSIS; PHYSIOLOGY;

ABDOMEN; AGING; ANIMALS; CALORIC RESTRICTION; DROSOPHILA MELANOGASTER; FEMALE; FOOD DEPRIVATION; MASS SPECTROMETRY; METABOLOME; MULTIVARIATE ANALYSIS;

EID: 84940889892     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12358     Document Type: Article

References (58)

1. Amar D, Safer H, Shamir R (2013) Dissection of regulatory networks that are altered in disease via differential co-expression. PLoS Comput. Biol. 9, e1002955.
2. Aris JP, Alvers AL, Ferraiuolo RA, Fishwick LK, Hanvivatpong A, Hu D, Kirlew C, Leonard MT, Losin KJ, Marraffini M, Seo AY, Swanberg V, Westcott JL, Wood MS, Leeuwenburgh C, Dunn WA Jr (2013) Autophagy and leucine promote chronological longevity and respiration proficiency during calorie restriction in yeast. Exp. Gerontol. 48, 1107-1119.
3. Avanesov AS, Ma S, Pierce KA, Yim SH, Lee BC, Clish CB, Gladyshev VN (2014) Age- and diet-associated metabolome remodeling characterizes the aging process driven by damage accumulation. eLife 3, e02077.
4. Berrougui H, Khalil A (2009) Age-associated decrease of high-density lipoprotein-mediated reverse cholesterol transport activity. Rejuvenation Res. 12, 117-126.
5. Bo TH, Dysvik B, Jonassen I (2004) LSimpute: accurate estimation of missing values in microarray data with least squares methods. Nucleic Acids Res. 32, e34.
6. Cabreiro F, Au C, Leung KY, Vergara-Irigaray N, Cocheme HM, Noori T, Weinkove D, Schuster E, Greene ND, Gems D (2013) Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153, 228-239.
7. Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ (2012) Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10, 515-519.
8. Chan EK, Rowe HC, Hansen BG, Kliebenstein DJ (2010) The complex genetic architecture of the metabolome. PLoS Genet. 6, e1001198.
9. Chintapalli VR, Al Bratty M, Korzekwa D, Watson DG, Dow JA (2013) Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high resolution mass spectrometry. PLoS ONE 8, e78066.
10. Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, Promislow DEL (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl. Environ. Microbiol. 73, 3470-3479.
11. Costell M, O'Connor JE, Grisolia S (1989) Age-Dependent Decrease of Carnitine Content in Muscle of Mice and Humans. Biochemical and biophysical research communications 161, 1135-1143.
12. De Guzman JM, Ku G, Fahey R, Youm YH, Kass I, Ingram DK, Dixit VD, Kheterpal I (2013) Chronic caloric restriction partially protects against age-related alteration in serum metabolome. Age (Dordr). 35, 1091-1104.
13. DiLeo MV, Strahan GD, den Bakker M, Hoekenga OA (2011) Weighted Correlation Network Analysis (WGCNA) applied to the tomato fruit metabolome. PLoS ONE 6, e26683.
14. Eisenberg T, Schroeder S, Andryushkova A, Pendl T, Kuttner V, Bhukel A, Marino G, Pietrocola F, Harger A, Zimmermann A, Moustafa T, Sprenger A, Jany E, Buttner S, Carmona-Gutierrez D, Ruckenstuhl C, Ring J, Reichelt W, Schimmel K, Leeb T, Moser C, Schatz S, Kamolz LP, Magnes C, Sinner F, Sedej S, Frohlich KU, Juhasz G, Pieber TR, Dengjel J, Sigrist SJ, Kroemer G, Madeo F (2014) Nucleocytosolic depletion of the energy metabolite acetyl-coenzyme a stimulates autophagy and prolongs lifespan. Cell Metab. 19, 431-444.
15. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span-from yeast to humans. Science 328, 321-326.
16. Forster MJ, Morris P, Sohal RS (2003) Genotype and age influence the effect of caloric intake on mortality in mice. FASEB J. 17, 690-692.
17. Fuchs S, Bundy JG, Davies SK, Viney JM, Swire JS, Leroi AM (2010) A metabolic signature of long life in Caenorhabditis elegans. BMC Biol. 8, 14.
18. Fukushima A, Kusano M, Redestig H, Arita M, Saito K (2011) Metabolomic correlation-network modules in Arabidopsis based on a graph-clustering approach. BMC Syst. Biol. 5, 1.
19. Hansen M, Hsu AL, Dillin A, Kenyon C (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic Rnai screen. PLoS Genet. 1, 119-128.
20. Hoffman JM, Soltow QA, Li S, Sidik A, Jones DP, Promislow DEL (2014) Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster. Aging Cell 13, 596-604.
21. Horrillo D, Sierra J, Arribas C, Garcia-San Frutos M, Carrascosa JM, Lauzurica N, Fernandez-Agullo T, Ros M (2011) Age-associated development of inflammation in Wistar rats: effects of caloric restriction. Arch. Physiol. Biochem. 117, 140-150.
22. Jones DP, Park Y, Ziegler TR (2012) Nutritional metabolomics: progress in addressing complexity in diet and health. Annu. Rev. Nutr. 32, 183-202.
23. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 14, 885-890.
24. Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW, Thomas EL, Kockel L (2010) With tor, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 11, 453-465.
25. Katewa SD, Demontis F, Kolipinski M, Hubbard A, Gill MS, Perrimon N, Melov S, Kapahi P (2012) Intramyocellular fatty-acid metabolism plays a critical role in mediating responses to dietary restriction in Drosophila melanogaster. Cell Metab. 16, 97-103.
26. Kennedy BK, Berger SL, Brunet A, Campisi J, Cuervo AM, Epel ES, Franceschi C, Lithgow GJ, Morimoto RI, Pessin JE, Rando TA, Richardson A, Schadt EE, Wyss-Coray T, Sierra F (2014) Geroscience: linking aging to chronic disease. Cell 159, 709-713.
27. Kronenberg G, Colla M, Endres M (2009) Folic acid, neurodegenerative and neuropsychiatric disease. Curr. Mol. Med. 9, 315-323.
28. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559.
29. Leek JT, Johnson WE, Parker HS, Jaffe AE, Storey JD (2012) The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics 28, 882-883.
30. Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow QA, Jones DP, Pulendran B (2013) Predicting network activity from high throughput metabolomics. PLoS Comput. Biol. 9, e1003123.
31. Lin MJ, Tang LY, Reddy MN, Shen CK (2005) DNA methyltransferase gene dDNMT2 and longevity of Drosophila. J. Biol. Chem. 280, 861-864.
32. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl Acad. Sci. USA 103, 1768-1773.
33. Mahoney LB, Denny CA, Seyfried TN (2006) Caloric restriction in C57BL/6J mice mimics therapeutic fasting in humans. Lipids Health Dis. 5, 13.
34. Mair W, Dillin A (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu. Rev. Biochem. 77, 727-754.
35. Menni C, Kastenmuller G, Petersen AK, Bell JT, Psatha M, Tsai PC, Gieger C, Schulz H, Erte I, John S, Brosnan MJ, Wilson SG, Tsaprouni L, Lim EM, Stuckey B, Deloukas P, Mohney R, Suhre K, Spector TD, Valdes AM (2013) Metabolomic markers reveal novel pathways of ageing and early development in human populations. Int. J. Epidemiol. 42, 1111-1119.
36. Mishur RJ, Rea SL (2012) Applications of mass spectrometry to metabolomics and metabonomics: detection of biomarkers of aging and of age-related diseases. Mass Spectrom. Rev. 31, 70-95.
37. Muller-Linow M, Weckwerth W, Hutt MT (2007) Consistency analysis of metabolic correlation networks. BMC Syst. Biol. 1, 44.
38. Niccoli T, Partridge L (2012) Ageing as a risk factor for disease. Curr. Biol. 22, R741-R752.
39. Palm W, Sampaio JL, Brankatschk M, Carvalho M, Mahmoud A, Shevchenko A, Eaton S (2012) Lipoproteins in Drosophila melanogaster-assembly, function, and influence on tissue lipid composition. PLoS Genet. 8, e1002828.
40. Parashar V, Rogina B (2009) dSir2 mediates the increased spontaneous physical activity in flies on calorie restriction. Aging (Albany NY) 1, 529-541.
41. Park LK, Friso S, Choi SW (2012) Nutritional influences on epigenetics and age-related disease. Proc. Nutr. Soc. 71, 75-83.
42. Pletcher SD, Macdonald SJ, Marguerie R, Certa U, Stearns SC, Goldstein DB, Partridge L (2002) Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr. Biol. 12, 712-723.
43. Pletcher SD, Libert S, Skorupa D (2005) Flies and their golden apples: the effect of dietary restriction on Drosophila aging and age-dependent gene expression. Ageing Res. Rev. 4, 451-480.
44. Redman LM, Huffman KM, Landerman LR, Pieper CF, Bain JR, Muehlbauer MJ, Stevens RD, Wenner BR, Kraus VB, Newgard CB, et al. (2011) Effect of Caloric Restriction with and without Exercise on Metabolic Intermediates in Nonobese Men and Women. The Journal of clinical endocrinology and metabolism 96, E312-321.
45. R Core Team (2013). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
46. Rezzi S, Martin FP, Shanmuganayagam D, Colman RJ, Nicholson JK, Weindruch R (2009) Metabolic shifts due to long-term caloric restriction revealed in nonhuman primates. Exp. Gerontol. 44, 356-362.
47. Richards SE, Wang Y, Claus SP, Lawler D, Kochhar S, Holmes E, Nicholson JK (2013) Metabolic phenotype modulation by caloric restriction in a lifelong dog study. J. Proteome Res. 12, 3117-3127.
48. Sarup P, Pedersen SM, Nielsen NC, Malmendal A, Loeschcke V (2012) The metabolic profile of long-lived Drosophila melanogaster. PLoS ONE 7, e47461.
49. Soltow QA, Jones DP, Promislow DE (2010) A network perspective on metabolism and aging. Integr. Comp. Biol. 50, 844-854.
50. Southworth LK, Owen AB, Kim SK (2009) Aging mice show a decreasing correlation of gene expression within genetic modules. PLoS Genet. 5, e1000776.
51. Tesson BM, Breitling R, Jansen RC (2010) DiffCoEx: a simple and sensitive method to find differentially coexpressed gene modules. BMC Bioinformatics 11, 497.
52. Tomas-Loba A, Bernardes de Jesus B, Mato JM, Blasco MA (2013) A metabolic signature predicts biological age in mice. Aging Cell 12, 93-101.
53. Wang X, Wang LP, Tang H, Shan WY, Wang X, Liu D, Wu YY, Tian Q, Wang JZ, Zhu LQ (2014) Acetyl-L-carnitine rescues scopolamine-induced memory deficits by restoring insulin-like growth factor II via decreasing p53 oxidation. Neuropharmacology 76(Pt A), 80-87.
54. Whitaker R, Gil MP, Ding F, Tatar M, Helfand SL, Neretti N (2014) Dietary switch reveals fast coordinated gene expression changes in Drosophila melanogaster. Aging (Albany NY) 6, 355-368.
55. Williams CM, Watanabe M, Guarracino MR, Ferraro MB, Edison AS, Morgan TJ, Boroujerdi AF, Hahn DA (2014) Cold adaptation shapes the robustness of metabolic networks in Drosophila melanogaster. Evolution 68, 3505-3523.
56. Young A (1997) Ageing and physiological functions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1837-1843.
57. Zhang D, Sun X, Liu J, Xie X, Cui W, Zhu Y (2015) Homocysteine accelerates senescence of endothelial cells via DNA hypomethylation of human telomerase reverse transcriptase. Arterioscler. Thromb. Vasc. Biol. 35, 71-78.
58. Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, Lu TA, Benzer S, Kapahi P (2009) 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139, 149-160.