Skip to main content

Advertisement

SpringerLink
Log in

CTT1 overexpression increases life span of calorie-restricted Saccharomyces cerevisiae deficient in Sod1

  • Research Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Studies using different organisms revealed that reducing calorie intake, without malnutrition, known as calorie restriction (CR), increases life span, but its mechanism is still unkown. Using the yeast Saccharomyces cerevisiae as eukaryotic model, we observed that Cu, Zn-superoxide dismutase (Sod1p) is required to increase longevity, as well as to confer protection against lipid and protein oxidation under CR. Old cells of sod1 strain also presented a premature induction of apoptosis. However, when CTT1 (which codes for cytosolic catalase) was overexpressed, sod1 and WT strains showed similar survival rates. Furthermore, CTT1 overexpression decreased lipid peroxidation and delayed the induction of apoptotic process. Superoxide is rapidly converted to hydrogen peroxide by superoxide dismutase, but it also undergoes spontaneous dismutation albeit at a slower rate. However, the quantity of peroxide produced from superoxide in this way is two-fold higher. Peroxide degradation, catalyzed by catalase, is of vital importance, because in the presence of a reducer transition metal peroxide is reduced to the highly reactive hydroxyl radical, which reacts indiscriminately with most cellular constituents. These findings might explain why overexpression of catalase was able to overcome the deficiency of Sod1p, increasing life span in response to CR.

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

Access this article

Log in via an institution

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

  • Adamis PDB, Panek AD, Eleutherio E (2007) Vacuolar compartmentation of the cadmium-glutathione complex protects Saccharomyces cerevisiae from mutagenesis. Toxicol Lett 173:1–7

    Article  CAS  PubMed  Google Scholar 

  • Aebi H (1964) Catalase in vitro. Methods Enzymol 105:114–118

    Google Scholar 

  • Agarwal S, Sharma S, Agrawal V, Roy N (2005) Caloric restriction augments ROS defense in S. cerevisiae by a Sir2p independent mechanism. Free Radic Res. 39:55–62

    Article  CAS  PubMed  Google Scholar 

  • Bar G (2002) The quantitative measurement of H2O2 generation in isolated mitochondria. J Bioenerg Biomemb. 34:227–233

    Article  Google Scholar 

  • Baur JA (2010) Resveratrol, sirtuins, and the promise of a DR mimetic. Mech Aging Dev. 131:261–269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Botstein D, Fink GR (2011) Yeast: an experimental organism for 21st Century biology. Genetics 189:695–704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carmona-Gutierrez D, Büttner S (2014) The many ways to age for a single yeast cell. Yeast 31(8):289–298

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carter WO, Narayanan PK, Robinson JP (1994) Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J Leukoc Biol 55:253–258

    CAS  PubMed  Google Scholar 

  • Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dalle-Donnea I, Rossib R, Giustarinib D, Milzania A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329:23–38

    Article  Google Scholar 

  • de Moraes LMP, Astolfi-filho S, Oliver SG (1995) Development of yeast strains for the efficient utilisation of starch: evaluation of constructs that express—amylase and glucoamylase separately or as bifunctional fusion proteins. Appl Microbiol Biotechnol 43:1067–1076

    Article  PubMed  Google Scholar 

  • del Valle LG (2011) Oxidative stress in aging: theoretical outcomes and clinical evidences in humans. Biomed Aging Pathol 1:1–7

    Article  Google Scholar 

  • Demir AB, Koc A (2010) Assessment of chronological lifespan dependent molecular damages in yeast lacking mitochondrial antioxidant genes. Biochem Biophys Res Commun 400:106–110

    Article  CAS  PubMed  Google Scholar 

  • Fabrizio P, Longo VD (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2:73–81

    Article  CAS  PubMed  Google Scholar 

  • Fabrizio P, Longo VD (2008) Chronological aging-induced apoptosis in yeast. Biochim Biophys Acta 1783:1280–1285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandes PN, Mannarino SC, Silva CG, Pereira MD, Panek AD, Eleutherio ECA (2007) Oxidative stress response in eukaryotes: effect of glutathione, superoxide dismutase and catalase on adaptation to peroxide and menadione stresses in Saccharomyces cerevisiae. Redox Rep 12:236–244

    Article  CAS  PubMed  Google Scholar 

  • Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15:1583–1606

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425–1435

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gomes DS, Pereira MD, Panek AD, Andrade LR, Eleutherio E (2008) Apoptosis as a mechanism for removal of mutated cells of Saccharomyces cerevisiae: the role of Grx2 under cadmium exposure. Biochim Biophys Acta 1780:160–166

    Article  CAS  PubMed  Google Scholar 

  • Harman D (2006) Free radical theory of aging: an update increasing the functional life span. Ann NY Acad Sci 1067:1–12

    Article  Google Scholar 

  • Harris N, Bachler M, Costa V, Mollapour M, Moradas-Ferreira P, Piper P (2005) Overexpressed Sod1pacts either to reduce or to increase the life spans and stress resistance of yeast, depending on whether it is Cu(2+)-deficient or an active Cu, Zn-superoxide dismutase. Aging Cell 4:41–52

    Article  CAS  PubMed  Google Scholar 

  • Herker E, Jungwirth H, Lehmann KA, Maldener C, Fröhlich KU, Wissing S, Büttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Herrero E, Ros J, Bellí G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780:1217–1235

    Article  CAS  PubMed  Google Scholar 

  • Huberts DEW, González J, Lee SS, Litsios A, Hubmann G, Wit EC, Heinemann EC (2014) Calorie restriction does not elicit a robust extension of replicative lifespan in Saccharomyces cerevisiae. PNAS 111:11727–11731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaeberlein M (2010) Lessons on longevity from budding yeast. Nature 464:513–519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khurana V, Lindquist S (2010) Modelling neurodegeneration in Saccharomyces cerevisiae: why cook with baker’s yeast? Nat Rev 11:436–449

    Article  CAS  Google Scholar 

  • Liu XD, Thiele DJ (1996) Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 10:592–603

    Article  CAS  PubMed  Google Scholar 

  • Longo VD, Gralla EB, Valentine JS (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271:12275–12280

    Article  CAS  PubMed  Google Scholar 

  • Mannarino SC, Amorim MA, Pereira MD, Moradas-Ferreira P, Panek AD, Costa V, Eleutherio EC (2008) Glutathione is necessary to ensure benefits of calorie restriction during aging in Saccharomyces cerevisiae. Mech Aging Dev 129:700–705

    Article  CAS  PubMed  Google Scholar 

  • Mannarino SC, Vilela LF, Brasil AA, Aranha JN, Moradas-Ferreira P, Pereira MD, Costa V, Eleutherio EC (2011) Requirement of glutathione for Sod1 activation during lifespan extension. Yeast 28:19–25

    Article  CAS  PubMed  Google Scholar 

  • Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W, Ingram DK, de Cabo R (2012) Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489:318–321

    Article  CAS  PubMed  Google Scholar 

  • Mecocci P, Polidori MC, Troiano L, Cherubini A, Cecchetti R, Pini G, Straatman M, Monti D, Stahl W, Sies H, Franceschi C, Senin U (2000) Plasma antioxidants and longevity: a study on healthy centenarians. Free Radic Biol Med 28:1243–1248

    Article  CAS  PubMed  Google Scholar 

  • Mesquita A, Weinberger M, Silva A, Sampaio-Marques B, Almeida B, Leão C, Costa V, Rodrigues F, Burhans WC, Ludovico P (2010) Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity. Proc Natl Acad Sci USA 107:15123–15128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miao L, St. Clair DK (2009) Regulation of superoxide dismutase genes: implications in diseases. Free Radic Biol Med 47:344–356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mirisola MG, Braun RJ, Petranovic D (2013) Approaches to study yeast cell aging and death. FEMS Yeast Res 14:109–118

    Article  PubMed  Google Scholar 

  • Ozbay B, Dulger H (2002) Lipid peroxidation and antioxidant enzymes in Turkish population: relation to age, gender, exercise, and smoking. Tohoku J Exp Med 197:119–124

    Article  CAS  PubMed  Google Scholar 

  • Parrella E, Longo VD (2008) The chronological life span of Saccharomyces cerevisiae to study mitochondrial dysfunction and disease. Methods 46(4):256–262

    Article  CAS  PubMed  Google Scholar 

  • Pereira MD, Herdeiro RS, Fernandes PN, Eleutherio E, Panek AD (2003) Targets of oxidative stress in yeast sod mutants. Biochim Biophys Acta 1620:245–251

    Article  CAS  PubMed  Google Scholar 

  • Piper P (2006) Long-lived yeast as a model for aging research. Yeast 23:215–226

    Article  CAS  PubMed  Google Scholar 

  • Poljsak B (2011) Strategies for reducing or preventing the generation of oxidative stress. Oxid Med Cell Longev 2011:194586

    PubMed Central  CAS  PubMed  Google Scholar 

  • Radak Z, Zhao Z, Goto S, Koltai E (2011) Age-associated neurodegeneration and oxidative damage to lipids, proteins and DNA. Mol Asp Med 32:305–315

    Article  CAS  Google Scholar 

  • Reverter-Branchat G, Cabiscol E, Tamarit J, Sorolla MA, Angeles de la Torre M, Ros J (2007) Chronological and replicative life-span extension in Saccharomyces cerevisiae by increased dosage of alcohol dehydrogenase 1. Microbiology 153:3667–3676

    Article  CAS  PubMed  Google Scholar 

  • Ribaric S (2012) Diet and aging. Oxid Med Cell Longev 2012:741468

    Article  PubMed Central  PubMed  Google Scholar 

  • Ristow M, Schmeisser S (2011) Extending life span by increasing oxidative stress. Free Radic Biol Med 51:327–336

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Pousada C, Menezes RA, Pimentel C (2010) The Yap family and its role in stress response. Yeast 27:245–258

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Maniatis T, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sheu SS, Nauduri D, Anders MW (2006) Targeting antioxidants to mitochondria: a new therapeutic direction. Biochim Biophys Acta 1762:256–265

    Article  CAS  PubMed  Google Scholar 

  • Shimokawa I, Chiba T, Yamaza H, Komatsu T (2008) Longevity genes: insights from calorie restriction and genetic longevity models. Mol Cells 30:427–435

    Google Scholar 

  • Srinivasan C, Liba A, Imlay JA, Valentine JS, Gralla EB (2000) Yeast lacking superoxide dismutase(s) show elevated levels of “free iron” as measured by whole cell electron paramagnetic resonance. J Biol Chem 275:29187–29192

    Article  CAS  PubMed  Google Scholar 

  • Steels EL, Learmonth RP, Watson K (1994) Stress tolerance and membrane lipid unsaturation in Saccharomyces cerevisiae grown aerobically or anaerobically. Microbiology 140:569–576

    Article  CAS  PubMed  Google Scholar 

  • Stickland LH (1951) The determination of small quantities of bacteria by means of the Biuret reaction. J Gen Microbiol 5:698–703

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from CAPES and CNPq.

Author information

Authors and Affiliations

  1. Department of Biochemistry, Institute of Chemistry, Federal University of Rio de Janeiro, Avenida Athos da Silveira Ramos 149, Bloco A, Lab 547, Rio de Janeiro, RJ, 21941-909, Brazil

    Germana Rona, Ricardo Herdeiro, Cristiane Juliano Mathias, Marcos Dias Pereira & Elis Eleutherio

  2. Department of Cellular Biology, Institute of Biology, University of Brasília, Brasília, DF, Brazil

    Fernando Araripe Torres

Authors
  1. Germana Rona
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ricardo Herdeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristiane Juliano Mathias
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Araripe Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcos Dias Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elis Eleutherio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Germana Rona.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rona, G., Herdeiro, R., Mathias, C.J. et al. CTT1 overexpression increases life span of calorie-restricted Saccharomyces cerevisiae deficient in Sod1. Biogerontology 16, 343–351 (2015). https://doi.org/10.1007/s10522-015-9550-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-015-9550-7

Keywords

Search

Navigation