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Calorie restriction in the rotifer Brachionus plicatilis enhances hypoxia tolerance in association with the increased mRNA levels of glycolytic enzymes

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Abstract

The rotifer Brachionus plicatilis shows a typical sigmoid growth curve, where calorie restriction (CR) and hypoxia are thought to be introduced at high population density in the stationary phase. CR may induce a shift from aerobic to anaerobic metabolism in this stationary phase, possibly contributing to an increased hypoxia tolerance. This study was undertaken to investigate the effect of CR on hypoxia tolerance at the molecular level. When rotifers were cultured under CR (fed every second day) or fed ad libitum (AL), and subsequently exposed to hypoxia, those in the CR group had a higher survival rate than their AL counterparts. We then cloned cDNAs encoding three glycolytic enzymes, glyceraldehyde 3-phosphate dehydrogenase (GAPDH), enolase (ENO), and phosphoglycerate mutase (PGM) and compared their accumulated mRNA levels between CR and AL rotifers at ages of 1–8 days by quantitative real-time PCR. The CR group showed significantly higher mRNA levels of GAPDH and ENO than their AL counterparts. Furthermore, rotifers in the stationary phase showed higher mRNA levels of these enzymes than those in the exponential growth phase. These results suggest that CR induces anaerobic metabolism, which possibly contributes to population stability under hypoxia in the stationary phase.

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References

  • Castello, L., T. Froio, G. Cavallini, F. Biasi, A. Sapino, G. Leonarduzzi, E. Bergamini, G. Poli & E. Chiarpotto, 2005. Calorie restriction protects against age-related rat aorta sclerosis. FASEB Journal 19: 1863–1865.

    CAS  PubMed  Google Scholar 

  • Denekamp, N. Y., M. A. S. Thorne, M. S. Clark, M. Kube, R. Reinhardt & E. Lubzens, 2009. Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genomics 10: 108.

    Article  PubMed  CAS  Google Scholar 

  • Donati, A., G. Recchia, G. Cavallini & E. Bergamini, 2008. Effect of aging and anti-aging caloric restriction on the endocrine regulation of rat liver autophagy. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 63: 550–555.

    Google Scholar 

  • Enesco, H. E., 1993. Rotifers in aging research: use of rotifers to test various theories of aging. Hydrobiologia 255: 59–70.

    Article  Google Scholar 

  • Esparcia, A., M. R. Miracle & M. Serra, 1989. Brachionus plicatilis tolerance to low oxygen concentrations. Hydrobiologia 186: 331–337.

    Article  Google Scholar 

  • Esparcia, A., M. Serra & M. R. Miracle, 1992. Relationships between oxygen concentration and patterns of energy metabolism in the rotifer Brachionus plicatilis. Comparative Biochemistry and Physiology B – Biochemistry and Molecular Biology 103: 357–362.

    Article  Google Scholar 

  • Finkel, T. & N. J. Holbrook, 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239–247.

    Article  CAS  PubMed  Google Scholar 

  • Gonzales-Pacheco, D. M., W. C. Buss, K. M. Koehler, W. F. Woodside & S. S. Alpert, 1993. Energy restriction reduces metabolic rate in adult male Fisher-344 rats. Journal of Nutrition 123: 90–97.

    CAS  PubMed  Google Scholar 

  • Goodrick, C. L., D. K. Ingram, M. A. Reynolds, J. R. Freeman & N. Cider, 1990. Effects of intermittent feeding upon body weight and lifespan in inbred mice: interaction of genotype and age. Mechanisms of Ageing and Development 55: 69–87.

    Article  CAS  PubMed  Google Scholar 

  • Gorr, T. A., M. Gassmann & P. Wappner, 2006. Sensing and responding to hypoxia via HIF in model invertebrates. Journal of Insect Physiology 52: 349–364.

    Article  CAS  PubMed  Google Scholar 

  • Gracey, A. Y., J. V. Troll, & G. N. Somero, 2001. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proceedings of the National Academy of Sciences of the United States of America 98: 1993-1998.

  • Holt, S. J. & D. L. Riddle, 2003. SAGE surveys C. elegans carbohydrate metabolism: evidence for an anaerobic shift in the long-lived dauer larva. Mechanisms of Ageing and Development 124: 779–800.

    Article  CAS  PubMed  Google Scholar 

  • Houthoofd, K., B. P. Braeckman, I. Lenaerts, K. Brys, A. De Vreese, S. Van Eygn & J. R. Vanfleteren, 2002. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Experimental Gerontology 37: 1359–1369.

    Article  PubMed  Google Scholar 

  • Houthoofd, K., B. P. Braeckman, A. De Vreese, S. Van Eygen, I. Lenaerts, K. Brys, F. Matthijssens & J. R. Vanfleteren, 2004. Caloric restriction, Ins/IGF-1 signalling and longevity in the nematode Caenorhabditis elegans. Belgian Journal of Zoology 134: 79–84.

    Google Scholar 

  • Hulbert, A. J., D. J. Clancy, W. Mair, B. P. Braeckman, D. Gems & L. Partridge, 2004. Metabolic rate is not reduced by dietary-restriction or by lowered insulin/IGF-1 signalling and is not correlated with individual lifespan in Drosophila melanogaster. Experimental Gerontology 39: 1137–1143.

    Article  CAS  PubMed  Google Scholar 

  • Iyer, N. V., L. E. Kotch, F. Agani, S. W. Leung, E. Laughner, R. H. Wenger, M. Gassmann, J. D. Gearhart, A. M. Lawler, A. Y. Yu & G. L. Semenza, 1998. Cellular and developmental control of O-2 homeostasis by hypoxia-inducible factor 1 alpha. Genes & Development 12: 149–162.

    Article  CAS  Google Scholar 

  • Kaneko, G., S. Kinoshita, T. Yoshinaga, K. Tsukamoto & S. Watabe, 2002. Changes in expression patterns of stress protein genes during population growth of the rotifer Brachionus plicatilis. Fisheries Science 68: 1317–1323.

    Article  CAS  Google Scholar 

  • Kaneko, G., T. Yoshinaga, Y. Yanagawa, S. Kinoshita, K. Tsukamoto & S. Watabe, 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 

  • Kizito, Y. S. & A. Nauwerck, 1995. Temporal and vertical distribution of planktonic rotifers in a meromictic crater lake, Lake Nyahirya (western Uganda). Hydrobiologia 313: 303–312.

    Article  Google Scholar 

  • Koizumi, A., M. Tsukada, Y. Wada, H. Masuda & R. Weindruch, 1992. Mitotic activity in mice is suppressed by energy restriction-induced torpor. Journal of Nutrition 122: 1446–1453.

    CAS  PubMed  Google Scholar 

  • Kondoh, H., M. E. Lleonart, J. Gil, J. Wang, P. Degan, G. Peters, D. Martinez, A. Carnero & D. Beach, 2005. Glycolytic enzymes can modulate cellular life span. Cancer Research 65: 177–185.

    CAS  PubMed  Google Scholar 

  • Kondoh, H., M. E. Lleonart, D. Bernard & J. Gil, 2007. Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histology and Histopathology 22: 85–90.

    CAS  PubMed  Google Scholar 

  • Koubova, J. & L. Guarente, 2003. How does calorie restriction work? Genes & Development 17: 313–321.

    Article  CAS  Google Scholar 

  • Lee, C. K., R. G. Klopp, R. Weindruch & T. A. Prolla, 1999. Gene expression profile of aging and its retardation by caloric restriction. Science 285: 1390–1393.

    Article  CAS  PubMed  Google Scholar 

  • Marcial, H. S., A. Hagiwara & T. W. Snell, 2005. Effect of some pesticides on reproduction of rotifer Brachionus plicatilis Müller. Hydrobiologia 546: 569–575.

    Article  CAS  Google Scholar 

  • Masoro, E. J., B. P. Yu & H. A. Bertrand, 1982. Action of food restriction in delaying the aging process. Proceedings of the National Academy of Sciences of the United States of America 79: 4239–4241.

    Article  CAS  PubMed  Google Scholar 

  • Miracle, M. R. & E. Vicente, 1983. Vertical distribution and rotifer concentrations in the chemocline of meromictic lakes. Hydrobiologia 104: 259–267.

    Article  CAS  Google Scholar 

  • Murphy, C. T., S. A. McCarroll, C. I. Bargmann, A. Fraser, R. S. Kamath, J. Ahringer, H. Li & C. Kenyon, 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277–284.

    Article  CAS  PubMed  Google Scholar 

  • Park, H. G., K. W. Lee, S. H. Cho, H. S. Kim & M. M. Jung, 2001. High density culture of the freshwater rotifer, Brachionus calyciflorus. Hydrobiologia 446: 369–374.

    Article  Google Scholar 

  • Rao, G., E. N. Xia, M. J. Nadakavukaren & A. Richardson, 1990. Effect of dietary restriction on the age-dependent changes in the expression of antioxidant enzymes in rat liver. Journal of Nutrition 120: 602–609.

    CAS  PubMed  Google Scholar 

  • Rea, S. & T. E. Johnson, 2003. A metabolic model for life span determination in Caenorhabditis elegans. Developmental Cell 5: 197–203.

    Article  CAS  PubMed  Google Scholar 

  • Semenza, G. L., 1999. Regulation of mammalian O-2 homeostasis by hypoxia-inducible factor 1. Annual Review of Cell and Developmental Biology 15: 551–578.

    Article  CAS  PubMed  Google Scholar 

  • Semsei, I., G. Rao & A. Richardson, 1989. Changes in the expression of superoxide dismutase and catalase as a function of age and dietary restriction. Biochemical and Biophysical Research Communications 164: 620–625.

    Article  CAS  PubMed  Google Scholar 

  • Shen, C., D. Nettleton, M. Jiang, S. K. Kim & J. A. Powell-Coffman, 2005. Roles of the HIF-1 hypoxia-inducible factor during hypoxia response in Caenorhabditis elegans. The Journal of Biological Chemistry 280: 20580–20588.

    Article  CAS  PubMed  Google Scholar 

  • Sohal, R. S. & R. Weindruch, 1996. Oxidative stress, caloric restriction, and aging. Science 273: 59–63.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ton, C., D. Stamatiou & C. Liew, 2003. Gene expression profile of zebrafish exposed to hypoxia during development. Physiological Genomics 13: 97–106.

    CAS  PubMed  Google Scholar 

  • Yoshinaga, T., A. Hagiwara & K. Tsukamoto, 1999. Effect of conditioned media on the asexual reproduction of the monogonont rotifer Brachionus plicatilis O. F. Müller. Hydrobiologia 412: 103–110.

    Article  Google Scholar 

  • Yoshinaga, T., A. Hagiwara & K. Tsukamoto, 2000. Effect of periodical starvation on the life history of Brachionus plicatilis O.F. Müller (Rotifera): a possible strategy for population stability. Journal of Experimental Marine Biology and Ecology 253: 253–260.

    Article  PubMed  Google Scholar 

  • Yoshinaga, T., A. Hagiwara & K. Tsukamoto, 2001. Why do rotifer populations present a typical sigmoid growth curve? Hydrobiologia 446: 99–105.

    Article  Google Scholar 

  • Yoshinaga, T., G. Kaneko, S. Kinoshita, K. Tsukamoto & S. Watabe, 2003. The molecular mechanisms of life history alterations in a rotifer: a novel approach in population dynamics. Comparative Biochemistry and Physiology B-Biochemistry and Molecular Biology 136: 715–722.

    Article  CAS  Google Scholar 

  • Yoshinaga, T., Y. Minegishi, I. F. M. Rumengan, G. Kaneko, S. Furukawa, Y. Yanagawa, K. Tsukamoto & S. Watabe, 2004. Molecular phylogeny of the rotifers with two Indonesian Brachionus lineages. Coastal Marine Science 29: 45–56.

    Google Scholar 

  • Yu, B. P. & H. Y. Chung, 2001. Stress resistance by caloric restriction for longevity. Annals of the New York Academy of Sciences 928: 39–47.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Professor A. Hagiwara, Graduate School of Science and Technology, Nagasaki University, Japan for providing Brachionus plicatilis Ishikawa strain. This work was partly supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Y. O. was supported by Research Fellowships for Young Scientist from the Japan Society for the Promotion of Science.

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  1. Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, 113-8657, Japan

    Yori Ozaki, Gen Kaneko, Yoshiko Yanagawa & Shugo Watabe

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  1. Yori Ozaki
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  2. Gen Kaneko
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  3. Yoshiko Yanagawa
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  4. Shugo Watabe
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Correspondence to Shugo Watabe.

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Handling editor: Darcy J. Lonsdale

Yori Ozaki and Gen Kaneko contributed equally to this work.

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Ozaki, Y., Kaneko, G., Yanagawa, Y. et al. Calorie restriction in the rotifer Brachionus plicatilis enhances hypoxia tolerance in association with the increased mRNA levels of glycolytic enzymes. Hydrobiologia 649, 267–277 (2010). https://doi.org/10.1007/s10750-010-0269-9

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  • DOI: https://doi.org/10.1007/s10750-010-0269-9

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