Developmental Diet Partially Determines Age-Related Changes in Metabolism of Drosophila
DOI:
https://doi.org/10.15330/jpnubio.10.7-19Keywords:
aging, metabolism, carbohydrates, fruit fly, developmentAbstract
Aging and metabolism are inextricably linked and both are critical for longevity. Changes in energy metabolism occur during normal aging and may be partly improved through the alteration of lifestyle variables. Macronutrients have a significant impact on life-history traits, such as disease vulnerability, reproduction, longevity and stress resistance. We investigated the age-related changes in the metabolism of fruit flies Drosophila melanogaster fed different diets at the developmental stage. Adult flies were transferred to the fresh two types of food. Two-, 15- or 40-day-old flies of every experimental group were tested. We observed significant changes in carbohydrate and fat metabolism associated with developmental diet and age. Developmental nutrition influenced hemolymph glucose and triglyceride (TAG) levels in young and adult flies. Hence, the consumption of a fixed diet during a long period of the adult stage can equalize the impact of a developmental diet. Higher hemolymph glucose level was observed in flies fed by a medium composed of 5% yeast as compared to a Yeast-Molasses medium during development. However, higher TAG and lipid pool were associated with consumption of Yeast-Molasses medium during development. Carbohydrate storage declined with the simultaneous increase in lipid pool with age. The impact of developmental nutrition and age on carbohydrate and lipid metabolism are not associated with gender or nutrition during adult life. Insulin and insulin-growth-factor-like signaling and target of rapamycin (TOR) pathways may be considered as the potential mechanisms involved in the regulation of developmental pathways by dietary conditions. Our data clearly show the connection between nutritional conditions during development and metabolic alteration with aging in Drosophila.
References
Aguila, J. R., Suszko, J., Gibbs, A. G., & Hoshizaki, D. K. (2007). The role of larval fat cells in adult Drosophila melanogaster. Journal of Experimental Biology, 210, 956‒963. https://doi.org/10.1242/jeb.001586
Barker, D. J., Gluckman, P. D., Godfrey, K. M., Harding, J. E., Owens, J. A., & Robinson, J. S. (1993). Fetal nutrition and cardiovascular disease in adult life. The Lancet, 341(8850), 938‒941. https://doi.org/10.1016/0140-6736(93)91224-a
Broughton, S., Alic, N., Slack, C., Bass, T., Ikeya, T., Vinti, G., Tommasi, A. M., Driege, Y., Hafen, E., & Partridge, L. (2008). Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS ONE, 3, e3721. https://doi.org/10.1371/journal.pone.0003721
Clark, R. I., Salazar, A., Yamada, R., Fitz-Gibbon, S., Morselli, M., Alcaraz, J., Rana, A., Rera, M., Pellegrini, M., Ja, W. W., & Walker, D. W. (2015). Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Reports, 12, 1656‒1667. https://doi.org/10.1016/j.celrep.2015.08.004
de Magalhães, J. P., Wuttke, D., Wood, S. H., Plank, M., & Vora, C. (2012). Genome-environment interactions that modulate aging: powerful targets for drug discovery. Pharmacological Reviews, 64, 88‒101. https://doi.org/10.1124/pr.110.004499
Driver, C. J., & Lamb, M. J. (1980). Metabolic changes in ageing Drosophila melanogaster. Experimental Gerontology, 15, 167‒175. https://doi.org/10.1016/0531-5565(80)90061-3
Ferguson, M., Mockett, R. J., Shen, Y., Orr, W. C., & Sohal, R. S. (2005). Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster. The Biochemical Journal, 390, 501‒511. https://doi.org/10.1042/BJ20042130
Girardot, F., Lasbleiz, C., Monnier, V., & Tricoire, H. (2006). Specific age-related signatures in Drosophila body parts transcriptome. BMC Genomics, 7, 69. https://doi.org/10.1186/1471-2164-7-69
Henry, Y., Overgaard, J., & Colinet, H. (2020). Dietary nutrient balance shapes phenotypic traits of Drosophila melanogaster in interaction with gut microbiota. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 241, 110626. https://doi.org/10.1016/j.cbpa.2019.110626
Jang, T., & Lee, K. P. (2018). Comparing the impacts of macronutrients on life-history traits in larval and adult Drosophila melanogaster: the use of nutritional geometry and chemically defined diets. Journal of Experimental Biology, 221(Pt 21), jeb181115. https://doi.org/10.1242/jeb.181115
Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H., & Gáliková, M. (2020). The influence of developmental diet on reproduction and metabolism in Drosophila. BMC Ecology and Evolution, 20, 93. https://doi.org/10.1186/s12862-020-01663-y
Lozinsky, O. V., Lushchak, O. V., Storey, J. M., Storey, K. B., & Lushchak, V. I. (2012). Sodium nitroprusside toxicity in Drosophila melanogaster: delayed pupation, reduced adult emergence, and induced oxidative/nitrosative stress in eclosed flies. Archives of Insect Biochemistry & Physiology, 80(3), 166‒185. https://doi.org/10.1002/arch.21033
Lushchak, O. V., Rovenko, B. M., Gospodaryov, D. V., & Lushchak, V. I. (2011). Drosophila melanogaster larvae fed by glucose and fructose demonstrate difference in oxidative stress markers and antioxidant enzymes of adult flies. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160, 27‒34. https://doi.org/10.1016/j.cbpa.2011.04.019
May, C. M., Doroszuk, A., & Zwaan, B. J. (2015). The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster. Ecology & Evolution, 5, 1156‒1168. https://doi.org/10.1016/10.1002/ece3.1389
Musselman, L. P., Fink, J. L., Narzinski, K., Ramachandran, P. V., Hathiramani, S. S., Cagan, R. L., & Baranski, T. J. (2011). A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Disease Models & Mechanisms, 4, 842‒849. https://doi.org/10.1242/dmm.007948
Pletcher, S. D., Macdonald, S. J., Marguerie, R., Certa, U., Stearns, S. C., Goldstein, D. B., & Partridge, L. (2002). Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Current Biology, 12, 712‒723. https://doi.org/10.1016/s0960-9822(02)00808-4
Rovenko, B. M., Perkhulyn, N. V., Lushchak, O. V., Storey, J. M., Storey, K. B., & Lushchak, V. I. (2014). Molybdate partly mimics insulin-promoted metabolic effects in Drosophila melanogaster. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 165, 76‒82. https://doi.org/10.1016/j.cbpc.2014.06.002
Semaniuk, U. V., Gospodaryov, D. V., Feden'ko, K. M., Yurkevych, I. S., Vaiserman, A. M., Storey, K. B., Simpson, S. J., & Lushchak, O. (2018). Insulin-like peptides regulate feeding preference and metabolism in Drosophila. Frontiers in Physiology, 9, 1083. https://doi.org/10.3389/fphys.2018.01083
Semaniuk, U., Piskovatska, V., Strilbytska, O., Strutynska, T., Burdyliuk, N., Vaiserman, A., Bubalo, V., Storey, K. B., & Lushchak, O. (2021). Drosophila insulin-like peptides: from expression to functions – a review. Entomologia Experimentalis et Applicata, 169, 195‒208. https://doi.org/10.1111/eea.12981
Semaniuk, U., Strilbytska, O., Malinovska, K., Storey, K. B., Vaiserman, A., Lushchak, V., & Lushchak, O. (2021). Factors that regulate expression patterns of insulin-like peptides and their association with physiological and metabolic traits in Drosophila. Insect Biochemistry and Molecular Biology, 135, 103609. https://doi.org/10.1016/j.ibmb.2021.103609
Shukla, N., & Kolthur-Seetharam, U. (2022). Drosophila Sirtuin 6 mediates developmental diet-dependent programming of adult physiology and survival. Aging Cell, 21, e13576. https://doi.org/10.1111/acel.13576
Stefana, M. I., Driscoll, P. C., Obata, F., Pengelly, A. R., Newell, C. L., MacRae, J. I., & Gould, A. P. (2017). Developmental diet regulates Drosophila lifespan via lipid autotoxins. Nature Communication, 8, 1384.
Strilbytska, O. M., Semaniuk, U. V., Storey, K. B., Yurkevych, I. S., & Lushchak, O. (2020). Insulin signaling in intestinal stem and progenitor cells as an important determinant of physiological and metabolic traits in Drosophila. Cells, 9(4), 803. https://doi.org/10.3390/cells9040803
Strilbytska, O. M., Semaniuk, U. V., Burdyliyk, N. I., Bubalo, V., & Lushchak, O. V. (2022a). Developmental diet defines metabolic traits in larvae and adult Drosophila. The Ukrainian Biochemical Journal, 94, 53‒63. https://doi.org/10.15407/ubj94.01.053
Strilbytska, O., Strutynska, T., Semaniuk, U., Burdyliyk, N., Bubalo, V., & Lushchak, O. (2022b). Dietary sucrose determines stress resistance, oxidative damages, and antioxidant defense system in Drosophila. Scientifica (Cairo). 2022, 7262342. https://doi.org/10.1155/2022/7262342
Tanabe, K., Itoh, M., & Tonoki, A. (2017). Age-related changes in insulin-like signaling lead to intermediate-term memory impairment in Drosophila. Cell Reports, 18, 1598-605. https://doi.org/10.1016/j.celrep.2017.01.053
Tu, M. P., & Tatar, M. (2003). Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell, 2, 327‒233. https://doi.org/10.1046/j.1474-9728.2003.00064.x
Vaiserman, A., Koliada, A., & Lushchak, O. (2018). Developmental programming of aging trajectory. Ageing Research Reviews, 47, 105‒22. https://doi.org/10.1016/j.arr.2018.07.007
Yu, Z., Zhai, G., Singmann, P., He, Y., Xu, T., Prehn, C., Römisch-Margl, W., Lattka, E., Gieger, C., Soranzo, N., Heinrich, J., Standl, M., Thiering, E., Mittelstraß, K., Wichmann, H. E., Peters, A., Suhre, K., Li, Y., Adamski, J., Spector, T. D., Illig, T., & Wang-Sattler, R. (2012). Human serum metabolic profiles are age dependent. Aging Cell, 11, 960‒967. https://doi.org/10.1111/j.1474-9726.2012.00865.x
Yurkevych, I. S., Gray, L. J., Gospodaryov, D. V., Burdylyuk, N. I., Storey, K. B., Simpson, S. J., & Lushchak, O. (2020). Development of fly tolerance to consuming a high-protein diet requires physiological, metabolic and transcriptional changes. Biogerontology, 21, 619‒36. https://doi.org/10.1007/s10522-020-09880-0
Zhou, Q., Kerbl-Knapp, J., Zhang, F., Korbelius, M., Kuentzel, K. B., Vujić, N., Akhmetshina, A., Hörl, G., Paar, M., Steyrer, E., Kratky, D., & Madl, T. (2021). Metabolomic profiles of mouse tissues reveal an interplay between aging and energy metabolism. Metabolites, 12, 17. https://doi.org/10.3390/metabo12010017
Zúñiga-Hernández, J. M., Olivares, G. H., Olguín, P., & Glavic, A. (2023). Low-nutrient diet in Drosophila larvae stage causes enhancement in dopamine modulation in adult brain due epigenetic imprinting. Open Biology, 13, 230049. https://doi.org/10.1098/rsob.230049
