Ukr.Biochem.J. 2022; Volume 94, Issue 1, Jan-Feb, pp. 53-63

doi: https://doi.org/10.15407/ubj94.01.053

Developmental diet defines metabolic traits in larvae and adult Drosophila

02.05.2022   Uncategorized   No comments

O. M. Strilbytska1*, U. V. Semaniuk1, N. I. Burdyliyk1, V. Bubalo2, O. V. Lushchak1,3*

1Department of Biochemistry and Biotechnology, Vasyl Stefanyk Precarpathian National University, Ivano-Frankivsk, Ukraine;
2Laboratory of Experimental Toxicology and Mutagenesis, L. I. Medved’s Research Center of Preventive Toxicology, Food and Chemical Safety, MHU, Kyiv, Ukraine;
3Research and Development University, Ivano-Frankivsk, Ukraine;
*e-mail: olya_b08@ukr.net or oleh.lushchak@pnu.edu.ua

Received: 04 October 2021; Accepted: 21 January 2022

The influence of the developmental nutrition on adult metabolism and overall performance becomes a hot topic of modern evolutionary biology. We used fruit fly Drosophila melanogaster as a model and experimental nutrition media composed of different sucrose content (S) and dry yeast content (Y): 0S:2Y, 20S:2Y or 0S:5Y, 20S:5Y to show that the developmental nutrition conditions define metabolism in larvae and adults. The level of glucose, glycogen, triglycerids and total lipids in the larvae and flies body were measured with the diagnostic assay kits. We found that individuals developed on either low-yeast or high-sugar diet showed delayed developmental rate. When kept on the diets with high sucrose content the larvae and adult flies had lower weight and higher amount of lipids as energy reserves. Restriction of dry yeast content in the diet of larvae led to a decrease in glycogen storage and protein levels in larvae and adult flies. The results obtained indicate that the metabolic traits revealed in adult flies are the result of nutrition during development and may be associated with mechanisms of organisms adaptation to the developmental nutritional conditions.

Keywords: , , , , , , ,

References:

  1. Zhou LY, Deng MQ, Zhang Q, Xiao XH. Early-life nutrition and metabolic disorders in later life: a new perspective on energy metabolism. Chin Med J (Engl). 2020;133(16):1961-1970. PubMed, PubMedCentral, CrossRef
  2. Vickers MH, Sloboda DM. Strategies for reversing the effects of metabolic disorders induced as a consequence of developmental programming. Front Physiol. 2012;3:242. PubMed, PubMedCentral, CrossRef
  3. Bloomington Drosophila Stock Center. Indiana University Bloomington. https://bdsc.indiana.edu/information/recipes/index.html. Accessed 11 Dec 2018.
  4. Staats S, Lüersen K, Wagner AE, Rimbach G. Drosophila melanogaster as a Versatile Model Organism in Food and Nutrition Research. J Agric Food Chem. 2018;66(15):3737-3753.   PubMed, CrossRef
  5. Tu MP, Tatar M. Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell. 2003;2(6):327-333. PubMed, CrossRef
  6. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol. 2002;12(15):1293-1300. PubMed, CrossRef
  7. Lushchak OV, Rovenko BM, Gospodaryov DV, Lushchak VI. Drosophila melanogaster larvae fed by glucose and fructose demonstrate difference in oxidative stress markers and antioxidant enzymes of adult flies. Comp Biochem Physiol A Mol Integr Physiol. 2011;160(1):27-34. PubMed, CrossRef
  8. Rovenko BM, Lushchak VI, Lushchak OV. Carbohydrate restriction in the larval diet causes oxidative stress in adult insects of Drosophila melanogaster. Ukr Biokhim Zhurn. 2013;85(5):61-72. (In Ukrainian). PubMed, PubMedCentral, CrossRef
  9. Rovenko BM, Kubrak OI, Gospodaryov DV , Yurkevych IS, Sanz A , Lushchak OV, Lushchak VI. Restriction of glucose and fructose causes mild oxidative stress independently of mitochondrial activity and reactive oxygen species in Drosophila melanogaster. Comp Biochem Physiol A Mol Integr Physiol. 2015;187:27-39. PubMed, CrossRef
  10. Rovenko BM, Kubrak OI, Gospodaryov DV , Perkhulyn NV, Yurkevych IS, Sanz A, Lushchak OV, Lushchak VI. High sucrose consumption promotes obesity whereas its low consumption induces oxidative stress in Drosophila melanogaster. J Insect Physiol. 2015;79:42-54. PubMed, CrossRef
  11. Ormerod KG, LePine OK, Abbineni PS, Bridgeman JM, Coorssen JR, Mercier AJ, Tattersall GJ. Drosophila development, physiology, behavior, and lifespan are influenced by altered dietary composition. Fly (Austin). 2017;11(3):153-170. PubMed, PubMedCentral, CrossRef
  12.  Shingleton AW, Masandika JR, Thorsen LS, Zhu Y, Mirth CK. The sex-specific effects of diet quality versus quantity on morphology in Drosophila melanogaster. R Soc Open Sci. 2017;4(9):170375. PubMed, PubMedCentral, CrossRef
  13. Rovenko BM, Perkhulyn NV, Lushchak OV, Storey JM, Storey KB, Lushchak VI. Molybdate partly mimics insulin-promoted metabolic effects in Drosophila melanogaster. Comp Biochem Physiol C Toxicol Pharmacol. 2014;165:76-82. PubMed, CrossRef
  14. Linford NJ, Bilgir C, Ro J, Pletcher SD. Measurement of lifespan in Drosophila melanogaster. J Vis Exp. 2013;(71):50068. PubMed, PubMedCentral, CrossRef
  15. Rovenko BM, Perkhulyn NV, Gospodaryov DV, Sanz A, Lushchak OV, Lushchak VI. High consumption of fructose rather than glucose promotes a diet-induced obese phenotype in Drosophila melanogaster. Comp Biochem Physiol A Mol Integr Physiol. 2015;180:75-85. PubMed, CrossRef
  16. Kubrak OI, Lushchak OV, Zandawala M, Nässel DR. Systemic corazonin signalling modulates stress responses and metabolism in Drosophila. Open Biol. 2016;6(11):160152. PubMed, PubMedCentral, CrossRef
  17. Wawrik B, Harriman BH. Rapid, colorimetric quantification of lipid from algal cultures. J Microbiol Methods. 2010;80(3):262-266. PubMed, CrossRef
  18. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254. PubMed, CrossRef
  19. Skorupa DA, Dervisefendic A, Zwiener J, Pletcher SD. Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell. 2008;7(4):478-490. PubMed, PubMedCentral, CrossRef
  20. Lushchak O, Strilbytska OM, Yurkevych I, Vaiserman AM, Storey KB. Implications of amino acid sensing and dietary protein to the aging process. Exp Gerontol. 2019;115:69-78. PubMed, CrossRef
  21. Flatt JP. Energy metabolism and the control of lipogenesis in adipose tissue. Horm Metab Res. 1970;2:Suppl 2:93-101. PubMed
  22. Lushchak OV, Gospodaryov DV, Rovenko BM, Glovyak AD, Yurkevych IS, Klyuba VP, Shcherbij MV, Lushchak VI. Balance between macronutrients affects life span and functional senescence in fruit fly Drosophila melanogaster. J Gerontol A Biol Sci Med Sci. 2012;67(2):118-125. PubMed, CrossRef
  23. Davies LR, Schou MF, Kristensen TN, Loeschcke V. Linking developmental diet to adult foraging choice in Drosophila melanogaster. J Exp Biol. 2018;221(Pt 9):jeb175554. PubMed, CrossRef
  24. Musselman LP, Fink JL, Narzinski K, Ramachandran PV, Hathiramani SS, Cagan RL, Baranski TJ. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech. 2011;4(6):842-849. PubMed, PubMedCentral, CrossRef
  25. Krittika S, Lenka A, Yadav P. Evidence of dietary protein restriction regulating pupation height, development time and lifespan in Drosophila melanogaster. Biol Open. 2019;8(6):bio042952. PubMed, PubMedCentral, CrossRef
  26. Bruce KD, Hoxha S, Carvalho GB, Yamada R, Wang HD, Karayan P, He S, Brummel T, P Kapahi, Ja WW. High carbohydrate-low protein consumption maximizes Drosophila lifespan. Exp Gerontol. 2013;48(10):1129-1135. PubMed, PubMedCentral, CrossRef
  27. Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JW, Taylor PW, Soran N, Raubenheimer D. Lifespan and reproduction in Drosophila: New insights from nutritional geometry. Proc Natl Acad Sci USA. 2008;105(7):2498-2503. PubMed, PubMedCentral, CrossRef
  28. Solon-Biet SM, McMahon AC, Ballard JW, Ruohonen K, Wu LE, Cogger VC, Warren A, Huang X, Pichaud N, Melvin RG, Gokarn R, Khalil M, Turner N, Cooney GJ, Sinclair DA, Raubenheimer D, Le Couteur DG, Simpson SJ. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab. 2014;19(3):418-430. PubMed, PubMedCentral, CrossRef
  29. Flatt T, Tu MP, Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays. 2005;27(10):999-1010. PubMed, CrossRef
  30. Mirth CK, Riddiford LM. Size assessment and growth control: how adult size is determined in insects. Bioessays. 2007;29(4):344-355. PubMed, CrossRef
  31. Orme MH, Leevers SJ. Flies on steroids: the interplay between ecdysone and insulin signaling. Cell Metab. 2005;2(5):277-278. PubMed, CrossRef
  32. Pérez-Hedo M, Rivera-Perez C, Noriega FG. The insulin/TOR signal transduction pathway is involved in the nutritional regulation of juvenile hormone synthesis in Aedes aegypti. Insect Biochem Mol Biol. 2013;43(6):495-500. PubMed, PubMedCentral, CrossRef
  33. Graham P, Pick L. Drosophila as a model for diabetes and Ddiseases of insulin resistance. Curr Top Dev Biol. 2017;121:397-419. PubMed, PubMedCentral, CrossRef
  34. Mattila J, Hietakangas V. Regulation of Carbohydrate Energy Metabolism in Drosophila melanogaster. Genetics. 2017;207(4):1231-1253. PubMed, PubMedCentral, CrossRef
  35. Garrido D, Rubin T, Poidevin M, Maroni B, Le Rouzic A, Parvy JP, Montagne J. Fatty acid synthase cooperates with glyoxalase 1 to protect against sugar toxicity. PLoS Genet. 2015;11(2):e1004995. PubMed, PubMedCentral, CrossRef
  36. Bai Y, Li K, Shao J, Luo Q, Jin LH. Flos Chrysanthemi Indici extract improves a high-sucrose diet-induced metabolic disorder in Drosophila. Exp Ther Med. 2018;16(3):2564-2572. PubMed, PubMedCentral, CrossRef
  37. Warbrick-Smith J, Behmer ST, Lee KP, Raubenheimer D, Simpson SJ. Evolving resistance to obesity in an insect. Proc Natl Acad Sci USA. 2006;103(38):14045-14049. PubMed, PubMedCentral, CrossRef
  38. Heier C, Klishch S, Stilbytska O, Semaniuk U, Lushchak O. The Drosophila model to interrogate triacylglycerol biology. Biochim Biophys Acta Mol Cell Biol Lipids. 2021;1866(6):158924. PubMed, CrossRef
  39. Rehman N, Varghese J. Larval nutrition influences adult fat stores and starvation resistance in Drosophila. PLoS One. 2021;16(2):e0247175. PubMed, PubMedCentral, CrossRef
  40. Musselman LP, Fink JL, Baranski TJ. Similar effects of high-fructose and high-glucose feeding in a Drosophila model of obesity and diabetes. PLoS One. 2019;14(5):e0217096. PubMed, PubMedCentral, CrossRef
  41. Monaghan P. Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B Biol Sci. 2008;363(1497):1635-1645. PubMed, PubMedCentral, CrossRef
  42. Semaniuk U, Piskovatska V, Strilbytska O, Strutynska T, Burdyliuk N, Vaiserman A, Bubalo V, Storey KB, Lushchak O. Drosophila insulin-like peptides: from expression to functions – a review. Entomol Exp Applic. 2021;169(2):195-208. CrossRef
  43. Semaniuk U, Strilbytska O, Malinovska K, Storey KB, Vaiserman A, Lushchak V, Lushchak O. Factors that regulate expression patterns of insulin-like peptides and their association with physiological and metabolic traits in Drosophila. Insect Biochem Mol Biol. 2021;135:103609. PubMed
  44. Broughton SJ , Piper MDW, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, Partridge L. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA. 2005;102(8):3105-3110. PubMed, PubMedCentral, CrossRef
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