SpringerLink
Log in

Effects of calorie restriction on the expression of manganese superoxide dismutase and catalase under oxidative stress conditions in the rotifer Brachionus plicatilis

  • Original Article
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Calorie restriction (CR) in the rotifer Brachionus plicatilis extends its lifespan, as it enhances the expression of antioxidant enzymes such as manganese superoxide dismutase (Mn SOD) and catalase. Here we show that CR also increased the mRNA levels of these antioxidant enzymes upon exposure to oxidative stress. Rotifers cultured under CR showed a higher survival rate than those fed ad libitum (AL) upon exposure to 0.05–0.2 μM juglone, an oxidative stress inducer. The relative mRNA levels of Mn SOD and catalase before exposure to juglone were slightly higher in the CR rotifers than in their AL counterparts, although these differences were not statistically significant. AL rotifers showed no apparent upregulation of the mRNA levels of these antioxidant enzymes upon exposure to 0.025 and 0.05 μM juglone. In contrast, the CR rotifers increased the mRNA levels of Mn SOD and catalase by up to 5.4-fold and 4.2-fold, respectively, resulting in significant differences between their levels in AL and CR rotifers under oxidative stress conditions. Furthermore, the protein level of catalase was clearly higher in CR than in AL rotifers 6 h after exposure to oxidative stress. These results suggest that the upregulation of Mn SOD and catalase genes is involved in CR-induced resistance to oxidative stress in the rotifer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  PubMed  CAS  Google Scholar 

  2. Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337–349

    Article  PubMed  CAS  Google Scholar 

  3. Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, Waskar M, Abdueva D, Skvortsov D, Ford D, Luu A, Badrinath A, Levine RL, Bradley TJ, Tavare S, Tower J (2007) Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 8:R262

    Article  PubMed  Google Scholar 

  4. Sun JT, Folk D, Bradley TJ, Tower J (2002) Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 161:661–672

    PubMed  CAS  Google Scholar 

  5. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, van Remmen H, Wallace DC, Rabinovitch PS (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308:1909–1911

    Article  PubMed  CAS  Google Scholar 

  6. Koubova J, Guarente L (2003) How does calorie restriction work? Genes Dev 17:313–321

    Article  PubMed  CAS  Google Scholar 

  7. Bokov A, Chaudhuri A, Richardson A (2004) The role of oxidative damage and stress in aging. Mech Ageing Dev 125:811–826

    Article  PubMed  CAS  Google Scholar 

  8. Yen K, Patel HB, Lublin AL, Mobbs CV (2009) SOD isoforms play no role in lifespan in ad lib or dietary restricted conditions, but mutational inactivation of SOD-1 reduces life extension by cold. Mech Ageing Dev 130:173–178

    Article  PubMed  CAS  Google Scholar 

  9. Rohrdanz E, Schmuck G, Ohler S, Kahl R (2001) The influence of oxidative stress on catalase and MnSOD gene transcription in astrocytes. Brain Res 900:128–136

    Article  PubMed  CAS  Google Scholar 

  10. Kemp TJ, Causton HC, Clerk A (2003) Changes in gene expression induced by H2O2 in cardiac myocytes. Biochem Biophys Res Commun 307:416–421

    Article  PubMed  CAS  Google Scholar 

  11. Park SK, Tedesco PM, Johnson TE (2009) Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8:258–269

    Article  PubMed  CAS  Google Scholar 

  12. Wheelock CE, Baumgartner TA, Newman JW, Wolfe MF, Tjeerdema RS (2002) Effect of nutritional state on Hsp60 levels in the rotifer Brachionus plicatilis following toxicant exposure. Aquat Toxicol 61:89–93

    Article  PubMed  CAS  Google Scholar 

  13. Yoshinaga T, Kaneko G, Kinoshita S, Tsukamoto K, Watabe S (2003) The molecular mechanisms of life history alterations in a rotifer: a novel approach in population dynamics. Comp Biochem Physiol B 136:715–722

    Article  PubMed  Google Scholar 

  14. Oo AKS, Kaneko G, Hirayama M, Kinoshita S, Watabe S (2010) Identification of genes differentially expressed by calorie restriction in the rotifer (Brachionus plicatilis). J Comp Physiol B 180:105–116

    Article  PubMed  CAS  Google Scholar 

  15. Krall J, Bagley AC, Mullenbach GT, Hallewell RA, Lynch RE (1988) Superoxide mediates the toxicity of paraquat for cultured mammalian cells. J Biol Chem 263:1910–1914

    Google Scholar 

  16. Kaneko G, Yoshinaga T, Yanagawa Y, Ozaki Y, Tsukamoto K, Watabe S (2011) Calorie restriction-induced maternal longevity is transmitted to their daughters in a rotifer. Funct Ecol 25:209–216

    Article  Google Scholar 

  17. Tanaka C, Hashimoto Y, Nakao S, Yoshinaga T (2009) Effect of juglone on the survival time of two Brachionus species (Rotifera): species-specific tolerance against oxidative stress. Fish Sci 75:191–194

    Article  CAS  Google Scholar 

  18. Yoshinaga T, Minegishi Y, Rumengan IFM, Kaneko G, Furukawa S, Yanagawa Y, Tsukamoto K, Watabe S (2004) Molecular phylogeny of the rotifers with two Indonesian Brachionus linages. Coast Mar Sci 29:45–56

    Google Scholar 

  19. Ozaki Y, Kaneko G, Yanagawa Y, Watabe S (2010) Calorie restriction in the rotifer Brachionus plicatilis enhances hypoxia tolerance in association with the increased mRNA levels of glycolytic enzymes. Hydrobiologia 649:267–277

    Article  CAS  Google Scholar 

  20. Kaneko G, Yoshinaga T, Yanagawa Y, Kinoshita S, Tsukamoto K, Watabe S (2005) Molecular characterization of Mn-superoxide dismutase and gene expression studies in dietary restricted Brachionus plicatilis rotifers. Hydrobiologia 546:117–123

    Article  CAS  Google Scholar 

  21. Takabe W, Li RS, Ai LS, Yu F, Berliner JA, Hsiai TK (2010) Oxidized low-density lipoprotein-activated c-Jun NH2-terminal kinase regulates manganese superoxide dismutase ubiquitination. Arterioscler Thromb Vasc Biol 30:436–441

    Article  PubMed  CAS  Google Scholar 

  22. Cao C, Leng YM, Liu X, Yi YP, Li P, Kufe D (2003) Catalase is regulated by ubiquitination and proteosomal degradation. Role of the c-Abl and Arg tyrosine kinases. Biochemistry 42:10348–10353

    Article  PubMed  CAS  Google Scholar 

  23. Snell TW, Joaquim-Justo C (2007) Workshop on rotifers in ecotoxicology. Hydrobiologia 593:227–232

    Article  Google Scholar 

  24. Cochrane BJ, Irby RB, Snell TW (1991) Effects of copper and tributyltin on stress protein abundance in the rotifer Brachionus-plicatilis. Comp Biochem Physiol C 98:385–390

    Article  PubMed  CAS  Google Scholar 

  25. Cochrane BJ, Mattley YD, Snell TW (1994) Polymerase chain-reaction as a tool for develo** stress protein probes. Environ Toxicol Chem 13:1221–1229

    Article  CAS  Google Scholar 

  26. Wheelock CE, Wolfe MF, Olsen H, Tjeerdema RS, Sowby ML (1999) Hsp60-induced tolerance in the rotifer Brachionus plicatilis exposed to multiple environmental contaminants. Arch Environ Contam Toxicol 36:281–287

    Article  PubMed  CAS  Google Scholar 

  27. Roberts MH, Sved DW, Felton SP (1987) Temporal changes in AHH and SOD activities in feral spot from the Elizabeth River, a polluted subestuary. Mar Environ Res 23:89–101

    Google Scholar 

  28. Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol C 100:173–176

    Article  PubMed  CAS  Google Scholar 

  29. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–284

    Article  PubMed  CAS  Google Scholar 

  30. Henderson ST, Johnson TE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11:1975–1980

    Article  PubMed  CAS  Google Scholar 

  31. Huang HJ, Tindall DJ (2007) Dynamic FoxO transcription factors. J Cell Sci 120:2479–2487

    Article  PubMed  CAS  Google Scholar 

  32. Suga K, Mark Welch D, Tanaka Y, Sakakura Y, Hagiwara A (2007) Analysis of expressed sequence tags of the cyclically parthenogenetic rotifer Brachionus plicatilis. PLoS ONE 2:e671

    Article  PubMed  Google Scholar 

  33. Denekamp NY, Thorne MAS, Clark MS, Kube M, Reinhardt R, Lubzens E (2009) Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genomics 10:108

    Article  PubMed  Google Scholar 

  34. Yoshinaga T, Kaneko G, Kinoshita S, Furukawa S, Tsukamoto K, Watabe S (2005) Insulin-like growth factor signaling pathway involved in regulating longevity of rotifers. Hydrobiologia 546:347–352

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We express sincere thanks to Professor A. Hagiwara, Nagasaki University, for providing the Ishikawa strain of Brachionus plicatilis. This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Y. Ozaki was supported by a research fellowships from the Japan Society for the Promotion of Science. M. Kailasam thanks the Department of Biotechnology, Ministry of Science and Technology, Government of India for awarding him a DBT Overseas Associateship.

Author information

Authors and Affiliations

  1. Laboratory of Marine Biochemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, 113-8657, Japan

    Muniyandi Kailasam, Gen Kaneko, Aung Kyaw Swar Oo, Yori Ozaki & Shugo Watabe

  2. Central Institute of Brackishwater Aquaculture, No. 75, Santhome High Road, R. A. Puram, Chennai, 600 028, India

    Muniyandi Kailasam & Arunachalam Rengasamy Thirunavukkarasu

Authors
  1. Muniyandi Kailasam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gen Kaneko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aung Kyaw Swar Oo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yori Ozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arunachalam Rengasamy Thirunavukkarasu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shugo Watabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shugo Watabe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kailasam, M., Kaneko, G., Oo, A.K.S. et al. Effects of calorie restriction on the expression of manganese superoxide dismutase and catalase under oxidative stress conditions in the rotifer Brachionus plicatilis . Fish Sci 77, 403–409 (2011). https://doi.org/10.1007/s12562-011-0334-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-011-0334-y

Keywords

Search

Navigation