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Effects of specific amino acids on the metabolism of Drosophila melanogaster

  • School of Life Sciences, University of Science and Technology of China, Hefei 230027, China

Cite this:
https://doi.org/10.52396/JUST-2021-0116
  • Received Date: 22 April 2021
  • Rev Recd Date: 30 June 2021
  • Publish Date: 31 August 2021
    Abstract

  • Abstract

    To investigate the perception and effects of specific amino acids on animals, we took Drosophila melanogaster as a model organism, measured the dietary preference and uptake of 20 amino acids as well as detected the effect of different amino acids on adult motility. We found that male and female Drosophila preferentially sense and consume different amino acids, and threonine specifically affects the motility of adult females. We then fed the third instar larvae with four dietary conditions (starvation, threonine, sucrose, and threonine + sucrose) and analyzed the differentially expressed genes between groups by transcriptome profiling. Gene Ontology annotation and Kyoto Encyclopedia of Genes and Genomes pathway analysis revealed that threonine affects steroid hormone and redox signaling. We further validated 8 genes by real-time fluorescence quantitative PCR in both larvae and adults,and found that the biological responses of threonine may depend on developmental stages. Our findings lay a foundation for additional in-depth investigation of the sensing and metabolic regulation of specific amino acids and provide clues of its molecular mechanism at the gene expression level.

    Abstract

    To investigate the perception and effects of specific amino acids on animals, we took Drosophila melanogaster as a model organism, measured the dietary preference and uptake of 20 amino acids as well as detected the effect of different amino acids on adult motility. We found that male and female Drosophila preferentially sense and consume different amino acids, and threonine specifically affects the motility of adult females. We then fed the third instar larvae with four dietary conditions (starvation, threonine, sucrose, and threonine + sucrose) and analyzed the differentially expressed genes between groups by transcriptome profiling. Gene Ontology annotation and Kyoto Encyclopedia of Genes and Genomes pathway analysis revealed that threonine affects steroid hormone and redox signaling. We further validated 8 genes by real-time fluorescence quantitative PCR in both larvae and adults,and found that the biological responses of threonine may depend on developmental stages. Our findings lay a foundation for additional in-depth investigation of the sensing and metabolic regulation of specific amino acids and provide clues of its molecular mechanism at the gene expression level.
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    • References(28)
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    Wolfson R L, Sabatini D M. The dawn of the age of amino acid sensors for the mTORC1 pathway. Cell Metab., 2017, 26(2): 301-309.
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    Croset V, Schleyer M, Arguello J R, et al. A molecular and neuronal basis for amino acid sensing in the Drosophila larva. Sci. Rep., 2016, 6: 34871.
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    Barone M C, Bohmann D. Assessing neurodegenerative phenotypes in Drosophila dopaminergic neurons by climbing assays and whole brain immunostaining. J. Vis. Exp., 2013(74): e50339.
    [26]
    Zinke I, Schutz C S, Katzenberger J D, et al. Nutrient control of gene expression in Drosophila: Microarray analysis of starvation and sugar-dependent response. EMBO J., 2002, 21(22): 6162-6173.
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    Komljenovic A, Roux J, Wollbrett J, et al. BgeeDB, an R package for retrieval of curated expression datasets and for gene list expression localization enrichment tests. F1000Res., 2016, 5: 2748.
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    [1]
    Tabe Y, Lorenzi P L, Konopleva M. Amino acid metabolism in hematologic malignancies and the era of targeted therapy. Blood, 2019, 134(13): 1014-1023.
    [2]
    Li T, Le A. Glutamine metabolism in cancer. Adv. Exp. Med. Biol., 2018, 1063: 13-32.
    [3]
    Grohmann U, Bronte V. Control of immune response by amino acid metabolism. Immunol. Rev., 2010, 236: 243-264.
    [4]
    Martinez-Outschoorn U E, Peiris-Pages M, Pestell R G, et al. Cancer metabolism: A therapeutic perspective. Nat. Rev. Clin. Oncol., 2017, 14(1): 11-31.
    [5]
    Holecek M. Branched-chain amino acids in health and disease: Metabolism, alterations in blood plasma, and as supplements. Nutr. Metab. (Lond), 2018, 15: 33.
    [6]
    Wolfson R L, Sabatini D M. The dawn of the age of amino acid sensors for the mTORC1 pathway. Cell Metab., 2017, 26(2): 301-309.
    [7]
    Staats S, Luersen K, Wagner A E, et al. Drosophila melanogaster as a versatile model organism in food and nutrition research. J. Agric. Food Chem., 2018, 66(15): 3737-3753.
    [8]
    Castella C, Amichot M, Berge J B, et al. DSC1 channels are expressed in both the central and the peripheral nervous system of adult Drosophila melanogaster. Invert. Neurosci., 2001, 4(2): 85-94.
    [9]
    Rein K, Zockler M, Mader M T, et al. The Drosophila standard brain. Curr. Biol., 2002, 12(3): 227-231.
    [10]
    Zheng Z, Lauritzen J S, Perlman E, et al. A complete electron microscopy volume of the brain of adult Drosophila melanogaster. Cell, 2018, 174(3): 730-743.
    [11]
    Nassel D R, Liu Y, Luo J. Insulin/IGF signaling and its regulation in Drosophila. Gen. Comp. Endocrinol., 2015, 221: 255-266.
    [12]
    Oldham S. Obesity and nutrient sensing TOR pathway in flies and vertebrates: Functional conservation of genetic mechanisms. Trends Endocrinol. Metab., 2011, 22(2): 45-52.
    [13]
    Musselman L P, Kuhnlein R P. Drosophila as a model to study obesity and metabolic disease. J. Exp. Biol., 2018, 221(Pt Suppl 1): jeb163881; doi: 10.1242/jeb.163881.
    [14]
    Droujinine I A, Perrimon N. Interorgan communication pathways in physiology: Focus on Drosophila. Annu. Rev. Genet., 2016, 50: 539-570.
    [15]
    Graham P, Pick L. Drosophila as a model for diabetes and diseases of insulin resistance. Curr. Top. Dev. Biol., 2017, 121: 397-419.
    [16]
    Agrawal N, Delanoue R, Mauri A, et al. The Drosophila TNF Eiger is an adipokine that acts on insulin-producing cells to mediate nutrient response. Cell Metab., 2016, 23(4): 675-684.
    [17]
    Jayakumar S, Richhariya S, Reddy O V, et al. Drosophila larval to pupal switch under nutrient stress requires IP3R/Ca(2+) signalling in glutamatergic interneurons. Elife, 2016, 5: e17495.
    [18]
    Jayakumar S, Richhariya S, Deb B K, et al. A multicomponent neuronal response encodes the larval decision to pupariate upon amino acid starvation. J. Neurosci., 2018, 38(47): 10202-10219.
    [19]
    Ki Y, Lim C. Sleep-promoting effects of threonine link amino acid metabolism in Drosophila neuron to GABAergic control of sleep drive. Elife, 2019, 8: e40593.
    [20]
    Sonn J Y, Lee J, Sung M K, et al. Serine metabolism in the brain regulates starvation-induced sleep suppression in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A., 2018, 115(27): 7129-7134.
    [21]
    Yang Z, Huang R, Fu X, et al. A post-ingestive amino acid sensor promotes food consumption in Drosophila. Cell Res., 2018, 28(10): 1013-1025.
    [22]
    Lee B C, Kaya A, Ma S, et al. Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status. Nat. Commun., 2014, 5: 3592.
    [23]
    Obata F, Tsuda-Sakurai K, Yamazaki T, et al. Nutritional control of stem cell division through S-adenosylmethionine in Drosophila intestine. Dev. Cell, 2018, 44(6): 741-751.
    [24]
    Croset V, Schleyer M, Arguello J R, et al. A molecular and neuronal basis for amino acid sensing in the Drosophila larva. Sci. Rep., 2016, 6: 34871.
    [25]
    Barone M C, Bohmann D. Assessing neurodegenerative phenotypes in Drosophila dopaminergic neurons by climbing assays and whole brain immunostaining. J. Vis. Exp., 2013(74): e50339.
    [26]
    Zinke I, Schutz C S, Katzenberger J D, et al. Nutrient control of gene expression in Drosophila: Microarray analysis of starvation and sugar-dependent response. EMBO J., 2002, 21(22): 6162-6173.
    [27]
    Ashburner M, Ball C A, Blake J A, et al. Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet., 2000, 25(1): 25-29.
    [28]
    Komljenovic A, Roux J, Wollbrett J, et al. BgeeDB, an R package for retrieval of curated expression datasets and for gene list expression localization enrichment tests. F1000Res., 2016, 5: 2748.
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