Lipocalin gene expression is varied in developmental stages by larval nutritional stress in Drosophila

Lipocalin gene expression is varied in developmental stages by larval nutritional stress in Drosophila

Lipocalin genes NLaz, GLaz, and Karl are evolutionarily conserved genes in Drosophila melanogaster. There are studies on lipocalin gene expression differences under diverse diet conditions, but these studies have focused mainly on age-dependent expression profiles of these genes. The main aim of our study is to determine lipocalin expression in the developmental period by nutritional manipulation with an isofemale-based design. Three larval developmental periods have been researched under normal and restricted diets. We found significant differences between lines during their developmental time-related lipocalin expression. Here, we demonstrate that upregulations in the early developmental stages of lipocalin genes under stressful conditions resulted in unaffected developmental time. The possible reason for high expression is the activation of stress signal pathways in order to buffer the harmful effects of nutritional restriction. Our data showed that the early developmental period (48 72 h) is especially crucial to tolerate the dietary stress with respect to GLaz and NLaz expression. Results of this experiment have shown that the expression profiles of lipocalin genes have line-specific pathways to nutritional stress. Their expression depends on the genetic background corresponding to development time results. Our results highlight the transcriptional changes of lipocalins associated with developmental time in larvae, developed in a dietary-restricted medium.

___

  • Bass TM, Grandison RC, Wong R, Martinez P, Partridge L, Piper MDW (2007). Optimization of dietary restriction protocols in Drosophila. J Gerontol A Biol Sci Med Sci 62: 1071-1081.
  • Bijlsma R, Loeschcke V (2005). Environmental stress adaptation and evolution: an overview. J Evol Biol 18: 744-749.
  • Burger JMS, Hwangbo DS, Corby-Harris V, Promislow DEL (2007). The functional costs and benefits of dietary restriction in Drosophila. Ageing Cell 6: 63-71.
  • Chintapalli VR, Wang J, Dow JAT (2007). Using Fly Atlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720. 
  • Chippindale AK, Leroi AM, Kim SB, Rose MR (1993). Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and cost of reproduction. J Evol Biol 6: 171-193.
  • Chippindale AK, Leroi AM, Saing H, Borash DJ, Rose MR (1997). Phenotypic plasticity and selection in Drosophila life history evolution. 2. Diet mates and the cost of reproduction. J Evol Biol 10: 269-293.
  • Clancy DJ, Gems D, Hafen E, Leevers SJ, Partridge L (2002). Dietary restriction in long-lived dwarf flies. Science 296: 319.
  • Dassati S, Waldner A, Schweigreiter R (2014). Apolipoprotein D takes center stage in the stress response of the aging and degenerative brain. Neurobiol Aging 35: 1632-1642.
  • David JR, Gibert P, Legout H, Petavy G, Capy P, Moreteau B (2005). Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94: 3-12.
  • Doroszuk A, Jonker M, Pul N, Breit T, Zwaan B (2012). Transcriptome analysis of a long-lived natural Drosophila variant: a prominent role of stress- and reproduction-genes in lifespan extension. BMC Genomics 13: 167.
  • Flatt T, Heyland A (2011). Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and TradeOffs. Oxford, UK: Oxford University Press.
  • Flower D (1996). The lipocalin protein family: structure and function. Biochem J 318: 1-14.
  • Giannakou ME, Goss M, Jacobson J, Vinti G, Leevers SJ, Partridge L (2007). Dynamics of the action of dFOXO on adult mortality in Drosophila. Aging Cell 64: 29-38.
  • Güler P, Ayhan N, Koşukçu C, Önder BŞ (2014). The effects of larval diet restriction on developmental time pre-adult survival and wing length in Drosophila melanogaster. Turk J Zool 39: 395- 403.
  • Hull-Thompson J, Muffat J, Walker DW, Benzer S (2009). Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet 5: e1000460.
  • Jiang JC, Jaruga E, Repnevskaya MV, Jazwinski SM (2000). An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J 14: 2135-2137.
  • 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.
  • Koehn RK, Bayne RL (1989). Towards a physiological and genetical understanding of the energetics of the stress response. Biol J Linn Soc 37: 157-151.
  • Kolss M, Vijendravarma RK, Schwaller G, Kawecki TJ (2009). Lifehistory consequences of adaptation to larval nutritional stress in Drosophila. Evolution 63: 2389-2401.
  • Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA (2002). Calorie restriction extends Saccharomyces cerevisiae life span by increasing respiration. Nature 418: 344-348.
  • Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC T method.Methods 25: 402-408.
  • Matzkin LM, Johnson S, Paight C, Bozinovic G, Markow TA (2011). Dietary protein and sugar differentially affect development and metabolic pools in ecologically diverse Drosophila. J Nutr 141: 1127-1133.
  • Maynard JC, Pham T, Zheng T, Jockheck-Clark A, Rankin HB, Newgard CB, Spana EP, Nicchitta CV (2010). Gp93, the Drosophila GRP94 ortholog, is required for gut epithelial homeostasis and nutrient assimilation-coupled growth control. Dev Biol 339: 295-306. 
  • McCay CM, Crowell MF, Maynard LA (1935). The effect of retarded growth upon the length of lifespan and upon the ultimate body size. J Nutr 10: 63-79.
  • Mensch J, Lavagnino N, Carreira VP, Massaldi A, Hasson E, Fanara JJ (2008). Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction. BMC Dev Biol 8: 78.
  • Metaxakis A, Partridge L (2013). Dietary restriction extends lifespan in wild-derived populations of Drosophila melanogaster. PLoS ONE 8: e74681. 
  • Minois N (2000). Longevity and ageing: beneficial effects of exposure to mild stress. Biogerontology 1: 15-29.
  • Muffat J, Walker DW, Benzer S (2008). Human ApoD an apolipoprotein up-regulated in neurodegenerative diseases extends lifespan and increases stress resistance in Drosophila. P Nat Acad Sci USA 105: 7088-7093.
  • Neethu BK, Ramesh BY, Harini BP (2014). Enhanced protein diet accelerates the rate of development. A study in Drosophila nasutanasuta. International Journal of Advanced Research 2: 349-354.
  • Önder BŞ (2010). A comparison of two different diets and their restricted groups in relation to developmental time and viability in Drosophila melanogaster. Hacettepe Journal of Biology & Chemistry 38: 311-317.
  • Onder BS, Yilmaz M (2009). The effect of dietary restriction on developmental time in Drosophila melanogaster and its sibling D. simulans. Drosophila Information Service 92: 95-100.
  • Partridge L, Piper MDW, Mair W (2005). Dietary restriction in Drosophila. Mech Ageing Dev 126: 938-950.
  • Pasco MY, Léopold P (2012). High Sugar-Induced Insulin Resistance in Drosophila  relies on the lipocalin  Neural Lazarillo. PLoS ONE 7: e36583.
  • Rice  D, Barone S (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108: 511-533.
  • Robbins C (1983). Wildlife Feeding and Nutrition. New York, NY, USA: Academic Press.
  • Robertson FW (1960). The ecological genetics of growth in Drosophila: 1. Body size and developmental time on different diets. Genet Res 1: 288-304.
  • Rong YS, Titen SW, Xie HB, Golic MM, Bastiani M, Bandyopadhyay P, Olivera BM, Brodsky M, Rubin GM, Golic KG (2002). Targeted mutagenesis by homologous recombination in  D. melanogaster. Genes Dev 16: 1568-1581.
  • Roth GS, Ingram DK, Lane MA (1999). Calorie restriction in primates: will it work and how will we know? J Am Geriatr Soc 47: 896-903.
  • Ruiz M, Sanchez D, Canal I, Acebes I, Ganfornina MD (2011). Sex-dependent modulation of longevity by two Drosophila homologues of human apolipoprotein D GLaz and NLaz. Exp Geront 46: 579-589.
  • Ruiz M, Wicker-Thomas C, Sanchez D, Ganfornina MD (2012). Grasshopper Lazarillo, a GPI-anchored lipocalin, increases Drosophila longevity and stress resistance and functionally replaces its secreted homolog NLaz. Insect Biochem Mol Biol 42: 776-789.
  • Sanchez D, Ganfornina MD, Torres-Schumann S, Speese SD, Lora JM, Bastiani MJ (2000). Characterization of two novel lipocalins expressed in the Drosophila embryonic nervous system. Int J Dev Biol 44: 349-359.
  • Sanchez D, Lopez-Arias B, Torroja L, Canal I, Wang X, Bastiani MJ, Ganfornina MD (2006). Loss of glial lazarillo a homolog of apolipoprotein D reduces lifespan and stress resistance in Drosophila. Curr Biol 16: 680-686.
  • Schenk S, Saberi M, Olefsky JM (2008). Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 118: 2992-3002.
  • Shingleton AW, Christen KM, Peter WB (2008). Developmental model of static allometry in holometabolous insects. P Roy Soc Lond B Bio 1645: 1875-1885.
  • Stearns SC (1992). The Evolution of Life Histories. Oxford, UK: Oxford University Press.
  • Stearns SC, Ackermann M, Doebeli M, Kaiser M (2000). Experimental evolution of aging growth and reproduction in fruit flies. P Natl Acad Sci USA 7: 3309-3313.
  • Thompson J (2008). Endocrine control of stress and metabolic signaling in Drosophila melanogaster. PhD, University of Rochester, Rochester, NY, USA.
  • Torday JS, Rehan VR (2012). Evolutionary Biology: Cell-Cell Communication and Complex Disease. Hoboken, NJ, USA: Wiley-Blackwell.
  • Tu MP, Tatar M (2003). Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2: 327-333.
  • Walker DW, Muffat J, Rundel C, Benzer S (2006). Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Curr Biol 16: 674-679.
  • Wolf M, Nunes F, Henkel A, Heinick A, Paul RJ (2008). The MAP kinase JNK-1 of Caenorhabditis elegans: location activation and influences over temperature-dependent insulin-like signaling stress responses and fitness. J Cell Physiol 214: 721-729. 
  • Zhu CT, Ingelmo P, Rand DM (2014). G×G×E for lifespan in Drosophila: mitochondrial nuclear and dietary interactions that modify longevity. PLoS Genet 10: e1004354.