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A mild cold stress that increases resistance to heat lowers FOXO translocation in Drosophila melanogaster

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Abstract

Previous studies have shown that subjecting Drosophila melanogaster flies to a mild stress at young or middle age can increase lifespan and resistance to severe stresses throughout life and that the NF-κB-like transcription factor DIF, the 70 kDa heat-shock proteins, and the Drosophila Forkhead box class O (dFOXO) transcription factor could explain some of these effects. The present study showed that two dFOXO mutants do not survive longer heat if previously subjected to a mild cold stress, contrarily to wild-type flies. This cold pretreatment had nearly no effect on dFOXO nuclear translocation in wild-type males. Heat stress strongly increased dFOXO translocation, but this effect was lowered in cold-pretreated males. Because cold-pretreated wild-type males survived longer heat and had nevertheless a lower dFOXO translocation after this heat stress, one can conclude that dFOXO is required to resist heat but that the cold pretreatment makes that other mechanisms partly substitute to dFOXO translocation.

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References

  • Carter ME, Brunet A (2007) FOXO transcription factors. Curr Biol 17:R113–R114

    Article  CAS  PubMed  Google Scholar 

  • Cognigni P, Bailey AP, Miguel-Aliaga I (2011) Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 13:92–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cypser JR, Johnson TE (2003) Hormesis in Caenorhabditis elegans dauer-defective mutants. Biogerontology 4:203–214

    Article  CAS  PubMed  Google Scholar 

  • Donovan MR, Marr MT 2nd (2016) dFOXO activates large and small heat shock protein genes in response to oxidative stress to maintain proteostasis in Drosophila. J Biol Chem 291:19042–19050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galbadage T, Hartman PS (2008) Repeated temperature fluctuation extends the life span of Caenorhabditis elegans in a daf-16-dependent fashion. Mech Ageing Dev 129:507–514

    Article  CAS  PubMed  Google Scholar 

  • Giannakou ME, Goss M, Partridge L (2008) Role of dFOXO in lifespan extension by dietary restriction in Drosophila melanogaster: not required, but its activity modulates the response. Aging Cell 7:187–198

    Article  CAS  PubMed  Google Scholar 

  • Hazelrigg T, Levis R, Rubin GM (1984) Transformation of white locus DNA in Drosophila: dosage, compensation, zeste interaction, and position effects. Cell 36:469–481

    Article  CAS  PubMed  Google Scholar 

  • Henten AMV, Loeschcke V, Pedersen JG, Leisner JJ, Sarup P (2016) Injuries can prolong lifespan in Drosophila melanogaster males. Biogerontology 17:337–346

    Article  CAS  PubMed  Google Scholar 

  • Jünger MA, Rintelen F, Stocker H, Wasserman JD, Veégh 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Kristensen TN, Sørensen JG, Loeschcke V (2003) Mild heat stress at a young age in Drosophila melanogaster leads to increased Hsp70 synthesis after stress exposure later in life. J Genet 82:89–94

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Le Bourg E (2008) Three mild stresses known to increase longevity in Drosophila melanogaster flies do not increase resistance to oxidative stress. Am J Pharmacol Toxicol 3:137–143

    Article  Google Scholar 

  • Le Bourg E (2009) Hormesis, aging, and longevity. Biochim Biophys Acta 1790:1030–1039

    Article  PubMed  Google Scholar 

  • Le Bourg E (2010) Combined effects of suppressing live yeast and of a cold pretreatment on longevity, aging and resistance to several stresses in Drosophila melanogaster. Biogerontology 11:245–254

    Article  PubMed  Google Scholar 

  • Le Bourg E (2011) A cold stress applied at various ages can increase resistance to heat and fungal infection in aged Drosophila melanogaster flies. Biogerontology 12:185–193

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Le Bourg E (2013) Fasting can protect young and middle-aged Drosophila melanogaster flies against a severe cold stress. Biogerontology 14:513–529

    Article  CAS  PubMed  Google Scholar 

  • Le Bourg E (2016a) Life-time protection against severe heat stress by exposing young Drosophila melanogaster flies to a mild cold stress. Biogerontology 17:409–415

    Article  PubMed  Google Scholar 

  • Le Bourg E (2016b) The somatotropic axis may not modulate ageing and longevity in humans. Biogerontology 17:421–429

    Article  PubMed  Google Scholar 

  • Le Bourg E, Fournier D (2004) Is lifespan extension accompanied by improved antioxidant defences? A study of superoxide dismutase and catalase in Drosophila melanogaster flies that lived in hypergravity at young age. Biogerontology 5:261–266

    Article  PubMed  Google Scholar 

  • Le Bourg E, Massou I (2015) Fasting increases survival to cold in FOXO, DIF, autophagy mutants and in other genotypes of Drosophila melanogaster. Biogerontology 16:411–421

    Article  PubMed  Google Scholar 

  • Le Bourg E, Rattan SIS (eds) (2008) Mild stress and healthy aging. Applying hormesis in aging research and interventions. Springer, Berlin

    Google Scholar 

  • Le Bourg E, Valenti P, Payre F (2002) Lack of hypergravity-associated longevity extension in Drosophila melanogaster flies overexpressing hsp70. Biogerontology 3:355–364

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Maklakov AA, Rowe L, Friberg U (2015) Why organisms age: evolution of senescence under positive pleiotropy? BioEssays 37:802–807

    Article  CAS  PubMed  Google Scholar 

  • Martins R, Lithgow GJ, Link W (2016) Long live FOXO: unraveling the role of FOXO proteins in aging and longevity. Aging Cell 15:196–207

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Puig O, Mattila J (2011) Understanding forkhead box class O function: lessons from Drosophila melanogaster. Antioxid Redox Signal 14:635–647

    Article  CAS  PubMed  Google Scholar 

  • Rattan SIS, Le Bourg E (eds) (2014) Hormesis in health and disease. CRC Press, Boca Raton

    Google Scholar 

  • Slack C, Giannakou ME, Foley A, Goss M, Partridge L (2011) dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10:735–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slaidina M, Delanoue R, Gronke S, Partridge L, Léoopold P (2009) A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev Cell 17:874–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sørensen JG, Kristensen TN, Kristensen KV, Loeschcke V (2007) Sex specific effects of heat induced hormesis in Hsf-deficient Drosophila melanogaster. Exp Gerontol 42:1123–1129

    Article  PubMed  Google Scholar 

  • Zheng X, Yang Z, Yue Z, Alvarez JD, Sehgal A (2007) FOXO and insulin signaling regulate sensitivity of the circadian clock to oxidative stress. Proc Natl Acad Sci USA 104:15899–15904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The dFOXO 21 and dFOXO 25 flies were kindly provided by Hugo Stocker and Igor Vuillez (Institute of Molecular Systems Biology, ETH, Zurich, Switzerland) and the dFOXO Δ94 flies by Julien Colombani (Institut of Biology Valrose, University of Nice-Sophia-Antipoplis, Nice, France). The primary anti-Foxo antibody is a kind gift of Pierre Léopold (Institut of Biology Valrose, University of Nice-Sophia-Antipoplis, Nice, France).

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Correspondence to Eric Le Bourg.

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Polesello, C., Le Bourg, E. A mild cold stress that increases resistance to heat lowers FOXO translocation in Drosophila melanogaster . Biogerontology 18, 791–801 (2017). https://doi.org/10.1007/s10522-017-9722-8

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