Abstract
Fasting increases survival to a severe cold stress in young and middle-aged wild-type flies, this effect being lowered or absent at old age. As an attempt to determine the mechanisms of this effect, genes involved in metabolism (dFOXO), autophagy (Atg7), innate immunity (Dif 1), and resistance to cold (Frost) were studied. The 12 mutant, RNAi and control lines tested in this study displayed an increased survival to cold after fasting. This shows that fasting has a robust effect on survival to cold in many genotypes, but the mechanism of this effect remains unknown. This mechanism does not seem to be linked to metabolic pathways often considered to play a critical role in ageing and longevity determinations (insulin/insulin-like growth factor-1 pathway and autophagy).
Similar content being viewed by others
References
Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC, Carrera P, Inhester T, Schultze JL, Hoch M (2010) FOXO-dependent regulation of innate immune homeostasis. Nature 463:369–373
Brown AE, Baumbach J, Cook PE, Ligoxygakis P (2009) Short-term starvation of immune deficient Drosophila improves survival to gram-negative bacterial infections. PLoS One 4(2):e4490
Bubliy OA, Loeschcke V (2005) Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. J Evol Biol 18:789–803
Bubliy OA, Kristensen TN, Kellermann V, Loeschcke V (2012) Plastic responses to four environmental stresses and cross-resistance in a laboratory population of Drosophila melanogaster. Funct Ecol 26:245–253
Colinet H, Lee SF, Hoffmann A (2010) Functional characterization of the Frost gene in Drosophila melanogaster: importance for recovery from chill coma. PLoS One 5(6):e10925
Go KG, Prenen GH, Korf J (1988) Protective effect of fasting upon cerebral hypoxic-ischemic injury. Metab Brain Dis 3:257–263
Hay N (2011) Interplay between FOXO, TOR, and Akt. Biochim Biophys Acta 1813:1965–1970
Hoffmann AA, Hallas R, Anderson AR, Telonis-Scott M (2005) Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. J Evol Biol 18:804–810
Juhász G, Erdi B, Sass M, Neufeld TP (2007) Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev 21:3061–3066
Jünger MA, Rintelen F, Stocker H, Wasserman JD, Végh M, Radimerski T, Greenberg ME, Hafen E (2003) The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2(3):20
Klass M, Hirsh D (1976) Non-ageing developmental variant of Caenorhabditis elegans. Nature 260:523–525
Le Bourg E (2007) Hormetic effects of repeated exposures to cold at young age on longevity, aging and resistance to heat or cold shocks in Drosophila melanogaster. Biogerontology 8:431–444
Le Bourg E (2011) The NF-kB like factor DIF has weaker effects on Drosophila melanogaster immune defenses than previously thought. J Comp Physiol B 181:741–750
Le Bourg E (2012) Combined effects of two mild stresses (cold and hypergravity) on longevity, behavioral aging, and resistance to severe stresses in Drosophila melanogaster. Biogerontology 13:313–328
Le Bourg E (2013) Fasting can protect young and middle-aged Drosophila melanogaster flies against a severe cold stress. Biogerontology 14:513–529
Le Bourg E, Médioni J (1991) Food restriction and longevity in Drosophila melanogaster. Age Nutr 2:90–94
Le Bourg E, Malod K, Massou I (2012) The NF-κB-like factor DIF could explain some positive effects of a mild stress on longevity, behavioral aging, and resistance to strong stresses in Drosophila melanogaster. Biogerontology 13:455–465
Le Rohellec M, Le Bourg E (2009) Contrasted effects of suppressing live yeast from food on longevity, aging and resistance to several stresses in Drosophila melanogaster. Exp Gerontol 44:695–707
Lee C, Longo VD (2011) Fasting vs dietary restriction in cellular protection and cancer treatment: from model organisms to patients. Oncogene 30:3305–3316
Loeb J, Northrop JH (1917) On the influence of food and temperature upon the duration of life. J Biol Chem 32:103–121
Marie C, Bralet AM, Gueldry S, Bralet J (1990) Fasting prior to transient cerebral ischemia reduces delayed neuronal necrosis. Metab Brain Dis 5:65–75
McPhee CK, Baehrecke EH (2009) Autophagy in Drosophila melanogaster. Biochim Biophys Acta 1793:1452–1460
Mitchell JR, Verweij M, Brand K, van de Ven M, Goemaere N, van den Engel S, Chu T, Forrer F, Müller C, de Jong M, van IJcken W, IJzermans JN, Hoeijmakers JH, de Bruin RW (2010) Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell 9:40–53
Moskalev AA, Plyusnina EN, Shaposhnikov MV (2011) Radiation hormesis and radioadaptive response in Drosophila melanogaster flies with different genetic backgrounds: the role of cellular stress-resistance mechanisms. Biogerontology 12:253–263
Puig O, Mattila J (2011) Understanding Forkhead box class O function: lessons from Drosophila melanogaster. Antioxid Redox Signal 14:635–647
Puig O, Tjian R (2005) Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev 19:2435–2446
Ren C, Finkel SE, Tower J (2009) Conditional inhibition of autophagy genes in adult Drosophila impairs immunity without compromising longevity. Exp Gerontol 44:228–235
Robertson LT, Mitchell JR (2013) Benefits of short-term dietary restriction in mammals. Exp Gerontol 48:1043–1048
Simonsen A, Cumming RC, Brech A, Isakson P, Schubert DR, Finley KD (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4:176–184
Šnorek M, Hodyc D, Šedivý V, Ďurišová J, Skoumalová A, Wilhelm J, Neckář J, Kolář F, Herget J (2012) Short-term fasting reduces the extent of myocardial infarction and incidence of reperfusion arrhythmias in rats. Physiol Res 61:567–574
Udaka H, Percival-Smith A, Sinclair BJ (2013) Increased abundance of Frost mRNA during recovery from cold stress is not essential for cold tolerance in adult Drosophila melanogaster. Insect Mol Biol 22:541–550
Vigne P, Tauc M, Frelin C (2009) Strong dietary restrictions protect Drosophila against anoxia/reoxygenation injuries. PLoS One 4:e5422
Acknowledgments
dFOXO, da-GAL4, and Atg flies were kindly provided, respectively, by Cédric Polisello (UMR CNRS 5547, University Paul-Sabatier, Toulouse, France), Guillaume Isabel (UMR CNRS 5169, University Paul-Sabatier, Toulouse, France), and Nadège Minois (Biomedical Sciences Research Complex, University of St Andrews, Scotland). Guillaume Isabel and Hervé Colinet, (UMR CNRS 6553, University Rennes-1, France) were also very helpful in various matters.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Le Bourg, É., Massou, I. Fasting increases survival to cold in FOXO, DIF, autophagy mutants and in other genotypes of Drosophila melanogaster . Biogerontology 16, 411–421 (2015). https://doi.org/10.1007/s10522-015-9557-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10522-015-9557-0