Advertisement

Journal of Comparative Physiology B

, Volume 187, Issue 7, pp 899–909 | Cite as

Sex differences in oxidative stress resistance in relation to longevity in Drosophila melanogaster

  • S. Niveditha
  • S. Deepashree
  • S. R. Ramesh
  • T. ShivanandappaEmail author
Original Paper

Abstract

Gender differences in lifespan and aging are known across species. Sex differences in longevity within a species can be useful to understand sex-specific aging. Drosophila melanogaster is a good model to study the problem of sex differences in longevity since females are longer lived than males. There is evidence that stress resistance influences longevity. The objective of this study was to investigate if there is a relationship between sex differences in longevity and oxidative stress resistance in D. melanogaster. We observed a progressive age-dependent decrease in the activity of SOD and catalase, major antioxidant enzymes involved in defense mechanisms against oxidative stress in parallel to the increased ROS levels over time. Longer-lived females showed lower ROS levels and higher antioxidant enzymes than males as a function of age. Using ethanol as a stressor, we have shown differential susceptibility of the sexes to ethanol wherein females exhibited higher resistance to ethanol-induced mortality and locomotor behavior compared to males. Our results show strong correlation between sex differences in oxidative stress resistance, antioxidant defenses and longevity. The study suggests that higher antioxidant defenses in females may confer resistance to oxidative stress, which could be a factor that influences sex-specific aging in D. melanogaster.

Keywords

Longevity Ethanol Aging Free radicals Antioxidant enzymes 

Notes

Acknowledgements

The first and second authors thank Department of Science and Technology, Government of India, for the financial support under INSPIRE fellowship program. Thanks are also due to The Chairperson, Department of Zoology, University of Mysore, Mysuru, for the facilities.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

360_2017_1061_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 KB)

References

  1. Aebi H (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 3rd edn. Verlag, Chemie, Weinheim, pp. 273–286Google Scholar
  2. Andziak B, O’Connor TP, Qi W et al (2006) High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5:463–471CrossRefPubMedGoogle Scholar
  3. Archer CR, Sakaluk SK, Selman C et al (2013) Oxidative stress and the evolution of sex differences in life span and ageing in the decorated cricket, Gryllodes sigillatus. Evol Int J org Evol 67:620–634CrossRefGoogle Scholar
  4. Austad SN, Fischer KE (2016) Sex differences in lifespan. Cell Metab 23:1022–1033CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bainton RJ, Tsai LT, Singh CM et al (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10:187–194CrossRefPubMedGoogle Scholar
  6. Ballard JWO, Melvin RG, Miller JT, Katewa SD (2007) Sex differences in survival and mitochondrial bioenergetics during aging in Drosophila. Aging Cell 6:699–708CrossRefPubMedGoogle Scholar
  7. Barbancho M, Sánchez-Cañete FJ, Dorado G, Pineda M (1987) Relation between tolerance to ethanol and alcohol dehydrogenase (ADH) activity in Drosophila melanogaster: selection, genotype and sex effects. Heredity (Edinb) 58(Pt 3):443–450CrossRefGoogle Scholar
  8. Barja G (2013) Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts. Antioxid Redox Signal 19:1420–1445CrossRefPubMedPubMedCentralGoogle Scholar
  9. Barja G, Herrero A (2000) Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14:312–318PubMedGoogle Scholar
  10. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581PubMedGoogle Scholar
  11. Borrás C, Sastre J, García-Sala D et al (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34:546–552CrossRefPubMedGoogle Scholar
  12. Charlesworth B (1994) Evolution in age-structured populations, 2nd edn. Cambridge University Press, UKCrossRefGoogle Scholar
  13. Chaudhuri A, Bowling K, Funderburk C et al (2007) Interaction of genetic and environmental factors in a Drosophila parkinsonism model. J Neurosci 27:2457–2467CrossRefPubMedGoogle Scholar
  14. Chauhan V, Chauhan A (2016) Effects of methylmercury and alcohol exposure in Drosophila melanogaster: Potential risks in neurodevelopmental disorders. Int J Dev Neurosci 51:36–41CrossRefPubMedGoogle Scholar
  15. Das SK, Vasudevan DM (2007) Alcohol-induced oxidative stress. Life Sci 81:177–187CrossRefPubMedGoogle Scholar
  16. Devineni AV, Heberlein U (2012) Acute ethanol responses in Drosophila are sexually dimorphic. Proc Natl Acad Sci USA 109:21087–21092CrossRefPubMedPubMedCentralGoogle Scholar
  17. Eriksson K, Pikkarainen PH (1968) Differences between the sexes in voluntary alcohol consumption and liver ADH-activity in inbred strains of mice. Metabolism 17:1037–1042CrossRefPubMedGoogle Scholar
  18. Ernsting G, Isaaks JA (1991) Accelerated ageing: a cost of reproduction in the carabid beetle Notiophilus biguttatus F. Funct Ecol 5:299CrossRefGoogle Scholar
  19. Feany MB, Bender WW (2000) A Drosophila model of Parkinson’s disease. Nature 404:394–398CrossRefPubMedGoogle Scholar
  20. Finch CE (1990) Longevity, senescence and the genome. University of Chicago Press, ChicagoGoogle Scholar
  21. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247CrossRefPubMedGoogle Scholar
  22. Gargano JW, Martin I, Bhandari P, Grotewiel MS (2005) Rapid iterative negative geotaxis (RING): a new method for assessing age-related locomotor decline in Drosophila. Exp Gerontol 40:386–395CrossRefPubMedGoogle Scholar
  23. Gibson JB, Lewis N, Adena MA, Wilson SR (1979) Selection for ethanol tolerance in two populations of Drosophila melanogaster segregating alcohol dehydrogenase allozymes. Aust J Biol Sci 32:387–398CrossRefPubMedGoogle Scholar
  24. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300CrossRefPubMedGoogle Scholar
  25. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445CrossRefPubMedGoogle Scholar
  26. Ide T, Tsutsui H, Ohashi N et al (2002) Greater oxidative stress in healthy young men compared with premenopausal women. Arterioscler Thromb Vasc Biol 22:438–442CrossRefPubMedGoogle Scholar
  27. Isaksson C, Sheldon BC, Uller T (2011) The challenges of integrating oxidative stress into life-history biology. Bioscience 61:194–202CrossRefGoogle Scholar
  28. Jahromi SR, Haddadi M, Shivanandappa T, Ramesh SR (2015) Modulatory effect of Decalepis hamiltonii on ethanol-induced toxicity in transgenic Drosophila model of Parkinson’s disease. Neurochem Int 80:1–6CrossRefPubMedGoogle Scholar
  29. Janzen FJ (1995) Experimental evidence for the evolutionary significance of temperature dependent sex determination. Evolution (N Y) 49:864Google Scholar
  30. Johnson TE, de Castro E, Hegi de Castro S et al (2001) Relationship between increased longevity and stress resistance as assessed through gerontogene mutations in Caenorhabditis elegans. Exp Gerontol 36:1609–1617CrossRefPubMedGoogle Scholar
  31. Jones MA, Grotewiel M (2011) Drosophila as a model for age-related impairment in locomotor and other behaviors. Exp Gerontol 46:320–325CrossRefPubMedGoogle Scholar
  32. Kasdallah-Grissa A, Mornagui B, Aouani E et al (2007) Resveratrol, a red wine polyphenol, attenuates ethanol-induced oxidative stress in rat liver. Life Sci 80:1033–1039CrossRefPubMedGoogle Scholar
  33. Kavanagh MW (1987) The efficiency of sound production in two cricket species, Gryllotalpa australis and Teleogryllus commodus (Orthoptera: Grylloidea). J Exp Biol 130:107–119Google Scholar
  34. Kirkwood TBL, Kowald A (2012) The free-radical theory of ageing–older, wiser and still alive: modelling positional effects of the primary targets of ROS reveals new support. Bioessays 34:692–700CrossRefPubMedGoogle Scholar
  35. Ku H-H, Brunk UT, Sohal RS (1993) Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 15:621–627CrossRefPubMedGoogle Scholar
  36. Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764CrossRefPubMedGoogle Scholar
  37. Le Bourg E (2001) Oxidative stress, aging and longevity in Drosophila melanogaster. FEBS Lett 498:183–186CrossRefPubMedGoogle Scholar
  38. LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231CrossRefPubMedGoogle Scholar
  39. Lewis KN, Andziak B, Yang T, Buffenstein R (2013) The naked mole-rat response to oxidative stress: just deal with it. Antioxid Redox Signal 19:1388–1399CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lints FA, Bourgois M, Delalieux A et al (1983) Does the female life span exceed that of the male? A study in Drosophila melanogaster. Gerontology 29:336–352CrossRefPubMedGoogle Scholar
  41. Liochev SI (2015) Reflections on the theories of aging, of oxidative stress, and of science in general. Is it time to abandon the free radical (oxidative stress) theory of aging? Antioxid Redox Signal 23:187–207CrossRefPubMedGoogle Scholar
  42. Logan-Garbisch T, Bortolazzo A, Luu P et al (2014) Developmental ethanol exposure leads to dysregulation of lipid metabolism and oxidative stress in Drosophila. G3 (Bethesda) 5:49–59. doi: 10.1534/g3.114.015040 CrossRefGoogle Scholar
  43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  44. Malherbe Y, Kamping A, van Delden W, van de Zande L (2005) ADH enzyme activity and Adh gene expression in Drosophila melanogaster lines differentially selected for increased alcohol tolerance. J Evol Biol 18:811–819CrossRefPubMedGoogle Scholar
  45. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474CrossRefPubMedGoogle Scholar
  46. McDonald JF, Chambers GK, David J, Ayala FJ (1977) Adaptive response due to changes in gene regulation: a study with Drosophila. Proc Natl Acad Sci USA 74:4562–4566CrossRefPubMedPubMedCentralGoogle Scholar
  47. Migliaccio E, Giorgio M, Mele S et al (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402:309–313CrossRefPubMedGoogle Scholar
  48. Miles DB (2004) The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evol Ecol Res 6:63–75Google Scholar
  49. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92CrossRefPubMedGoogle Scholar
  50. Montooth KL, Siebenthall KT, Clark AG (2006) Membrane lipid physiology and toxin catabolism underlie ethanol and acetic acid tolerance in Drosophila melanogaster. J Exp Biol 209:3837–3850CrossRefPubMedGoogle Scholar
  51. Moore MS, DeZazzo J, Luk AY et al (1998) Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93:997–1007CrossRefPubMedGoogle Scholar
  52. Murakami S, Salmon A, Miller RA (2003) Multiplex stress resistance in cells from long-lived dwarf mice. FASEB J 17:1565–1566PubMedGoogle Scholar
  53. Oka S, Hirai J, Yasukawa T et al (2015) A correlation of reactive oxygen species accumulation by depletion of superoxide dismutases with age-dependent impairment in the nervous system and muscles of Drosophila adults. Biogerontology 16:485–501CrossRefPubMedGoogle Scholar
  54. Okada K, Pitchers WR, Sharma MD et al (2011) Longevity, calling effort, and metabolic rate in two populations of cricket. Behav Ecol Sociobiol 65:1773–1778CrossRefGoogle Scholar
  55. Orr WC, Sohal RS (1994) Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128–1130CrossRefPubMedGoogle Scholar
  56. Pérez VI, Bokov A, Van Remmen H et al (2009) Is the oxidative stress theory of aging dead? Biochim Biophys Acta Gen Subj 1790:1005–1014CrossRefGoogle Scholar
  57. Robert KA, Brunet-Rossinni A, Bronikowski AM (2007) Testing the “free radical theory of aging” hypothesis: physiological differences in long-lived and short-lived colubrid snakes. Aging Cell 6:395–404CrossRefPubMedGoogle Scholar
  58. Rose MR, Vu LN, Park SU, Graves JL (1992) Selection on stress resistance increases longevity in Drosophila melanogaster. Exp Gerontol 27:241–250CrossRefPubMedGoogle Scholar
  59. Sanz A, Fernández-Ayala DJM, Stefanatos RK, Jacobs HT (2010) Mitochondrial ROS production correlates with, but does not directly regulate lifespan in Drosophila. Aging 2:200–223CrossRefPubMedPubMedCentralGoogle Scholar
  60. Service PM, Hutchinson EW, Mackinley MD, Rose MR (1985) Resistance to environmental stress in Drosophila melanogaster selected for postponed senescence. Physiol Zool 58:380–389CrossRefGoogle Scholar
  61. Sohal RS (2002) Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med 33:37–44CrossRefPubMedGoogle Scholar
  62. Sohal RS, Sohal BH, Orr WC (1995) Mitochondrial superoxide and hydrogen peroxide generation, protein oxidative damage, and longevity in different species of flies. Free Radic Biol Med 19:499–504CrossRefPubMedGoogle Scholar
  63. Speakman JR, Selman C (2011) The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 33:255–259CrossRefPubMedGoogle Scholar
  64. Tomás-Zapico C, Alvarez-García O, Sierra V et al (2006) Oxidative damage in the livers of senescence-accelerated mice: a gender-related response. Can J Physiol Pharmacol 84:213–220CrossRefPubMedGoogle Scholar
  65. Tower J, Arbeitman M (2009) The genetics of gender and life span. J Biol 8:38CrossRefPubMedPubMedCentralGoogle Scholar
  66. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 136–179Google Scholar
  67. Vermeulen CJ, Van De Zande L, Bijlsma R (2005) Resistance to oxidative stress induced by paraquat correlates well with both decreased and increased lifespan in Drosophila melanogaster. Biogerontology 6:387–395CrossRefPubMedGoogle Scholar
  68. Viña J, Borrás C, Gambini J et al (2005) Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett 579:2541–2545CrossRefPubMedGoogle Scholar
  69. Warner DA, Andrews RM (2002) Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biol J Linn Soc 76:105–124CrossRefGoogle Scholar
  70. Wolf FW, Rodan AR, Tsai LT-Y, Heberlein U (2002) High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila. J Neurosci 22:11035–11044PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • S. Niveditha
    • 1
  • S. Deepashree
    • 1
  • S. R. Ramesh
    • 1
  • T. Shivanandappa
    • 1
    Email author
  1. 1.Neurobiology Laboratory, Department of ZoologyUniversity of Mysore, ManasagangotriMysuruIndia

Personalised recommendations