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Lead induces oxidative stress and phenotypic markers of apoptosis in Saccharomyces cerevisiae

  • Applied Microbial and Cell Physiology
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Abstract

In the present work, the mode of cell death induced by Pb in Saccharomyces cerevisiae was studied. Yeast cells Pb-exposed, up to 6 h, loss progressively the capacity to proliferate and maintained the membrane integrity evaluated by the fluorescent probes bis(1,3-dibutylbarbituric acid trimethine oxonol) and propidium iodide. Pb-induced death is an active process, requiring the participation of cellular metabolism, since the simultaneous addition of cycloheximide attenuated the loss of cell proliferation capacity. Cells exposed to Pb accumulated intracelullarly reactive oxygen species (ROS), evaluated by 2′,7′-dichlorodihydrofluorescein diacetate. The addition of ascorbic acid (a ROS scavenger) strongly reduced the oxidative stress and impaired the loss of proliferation capacity in Pb-treated cells. Pb-exposed cells displayed nuclear morphological alterations, like chromatin fragmentation, as revealed by diaminophenylindole staining. Together, the data obtained indicate that yeast cells exposition to 1 mmol/l Pb results in severe oxidative stress which can be the trigger of programmed cell death by apoptosis.

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References

  • Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9

    CAS  Google Scholar 

  • Avery SV (2001) Metal toxicity in yeasts and the role of oxidative stress. Adv Appl Microbiol 49:111–142

    Article  CAS  Google Scholar 

  • Balzan R, Sapienza K, Galea DR, Vassallo N, Frey H, Bannister WH (2004) Aspirin commits yeast cells to apoptosis depending on carbon source. Microbiology 150:109–115

    Article  CAS  Google Scholar 

  • Carmona-Gutierrez D, Eisenberg T, Buttner S, Meisinger C, Kroemer G, Madeo F (2010) Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ 17:763–773

    Article  CAS  Google Scholar 

  • Chen C, Wang JL (2007) Response of Saccharomyces cerevisiae to lead ion stress. Appl Microbiol Biotechnol 74:683–687

    Article  CAS  Google Scholar 

  • Dinsdale MG, Lloyd D, Jarvis B (1995) Yeast vitality during cider fermentation: two approaches to the measurement of membrane potential. J Inst Brew 101:453–458

    Google Scholar 

  • Eisenberg T, Carmona-Gutierrez D, Buttner S, Tavernarakis N, Madeo F (2010) Necrosis in yeast. Apoptosis 15:257–268

    Article  Google Scholar 

  • Epps DE, Wolfe ML, Groppi V (1994) Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1, 3-dibutylbarbituric acid)trimethine oxonol (DiBAC4(3)) in model systems and cells. Chem Phys Lipids 69:137–150

    Article  CAS  Google Scholar 

  • Gadd GM (1993) Interaction of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Granot D, Levine A, Dor-Hefetz E (2003) Sugar-induced apoptosis in yeast cells. FEMS Yeast Res 4:7–13

    Article  CAS  Google Scholar 

  • Haugland RP (2005) The handbook—a guide to fluorescent probes and labeling technologies, 10th edn. Invitrogen Corp, Eugene

    Google Scholar 

  • Howlett NG, Avery SV (1997) Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Appl Environ Microbiol 63:2971–2976

    CAS  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527

    Article  CAS  Google Scholar 

  • Liang QL, Zhou B (2007) Copper and manganese induce yeast apoptosis via different pathways. Mol Biol Cell 18:4741–4749

    Article  CAS  Google Scholar 

  • Ludovico P, Sousa MJ, Silva MT, Leao C, Corte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147:2409–2415

    CAS  Google Scholar 

  • Madeo F, Fröhlich E, Fröhlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734

    Article  CAS  Google Scholar 

  • Madeo F, Fröhlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Fröhlich KU (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767

    Article  CAS  Google Scholar 

  • Madeo F, Carmona-Gutierrez D, Ring J, Buettner S, Eisenberg T, Kroemer G (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382:227–231

    Article  CAS  Google Scholar 

  • Nargund AM, Avery SV, Houghton JE (2008) Cadmium induces a heterogeneous and caspase-dependent apoptotic response in Saccharomyces cerevisiae. Apoptosis 13:811–821

    Article  CAS  Google Scholar 

  • Rockenfeller P, Madeo F (2008) Apoptotic death of ageing yeast. Exp Gerontol 43:876–881

    Article  CAS  Google Scholar 

  • Sakamoto F, Ohnuki T, Fujii T, Iefuji H (2010) Response of Saccharomyces cerevisiae to heavy element stress: lead vs. uranium. Geomicrobiol J 27:240–244

    Article  CAS  Google Scholar 

  • Shanmuganathan A, Avery SV, Willetts SA, Houghton JE (2004) Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Lett 556:253–259

    Article  CAS  Google Scholar 

  • Silbergeld EK (2003) Facilitative mechanisms of lead as a carcinogen. Mutat Res 533:121–133

    Article  CAS  Google Scholar 

  • Soares HMVM, Conde PCFL, Almeida AAN, Vasconcelos MTSD (1999) Evaluation of n-substituted aminosulfonic acid pH buffers with a morpholinic ring for cadmium and lead speciation studies by electroanalytical techniques. Anal Chim Acta 394:325–335

    Article  CAS  Google Scholar 

  • Soares EV, Duarte A, Soares H (2000) Study of the suitability of 2-(N-morpholino) ethanesulfonic acid pH buffer for heavy metals accumulation studies using Saccharomyces cerevisiae. Anal Chim Acta 12:59–65

    CAS  Google Scholar 

  • Soares EV, Duarte APSR, Boaventura RA, Soares HMVM (2002) Viability and release of complexing compounds during accumulation of heavy metals by a brewer's yeast. Appl Microbiol Biotechnol 58:836–841

    Article  CAS  Google Scholar 

  • Soares EV, Hebbelinck K, Soares HMVM (2003) Toxic effects caused by heavy metals in the yeast Saccharomyces cerevisiae: a comparative study. Can J Microbiol 49:336–343

    Article  CAS  Google Scholar 

  • Suh JH, Yun JW, Kim DS (1999) Cation (K+, Mg2+, Ca2+) exchange in Pb2+ accumulation by Saccharomyces cerevisiae. Bioprocess Eng 21:383–387

    CAS  Google Scholar 

  • Sumner ER, Shanmuganathan A, Sideri TC, Willetts SA, Houghton JE, Avery SV (2005) Oxidative protein damage causes chromium toxicity in yeast. Microbiology 151:1939–1948

    Article  CAS  Google Scholar 

  • Tarpey MM, Wink DA, Grisham MB (2004) Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286:R431–R444

    Article  CAS  Google Scholar 

  • Van der Heggen M, Martins S, Flores G, Soares EV (2010) Lead toxicity in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 88:1355–1361

    Article  Google Scholar 

  • Yedjou CG, Milner JN, Howard CB, Tchounwou PB (2010) Basic apoptotic mechanisms of lead toxicity in human leukemia (Hl-60) cells. Int J Environ Res Public Health 7:2008–2017

    Article  CAS  Google Scholar 

  • Yu SS, Qin W, Zhuang GQ, Zhang XE, Chen GJ, Liu WF (2009) Monitoring oxidative stress and DNA damage induced by heavy metals in yeast expressing a redox-sensitive green fluorescent protein. Curr Microbiol 58:504–510

    Article  CAS  Google Scholar 

  • Yuan XF, Tang CC (1999) DNA damage and repair in yeast (Saccharomyces cerevisiae) cells exposed to lead. J Environ Sci Health Part A-Toxic/Hazard Subst Environ Eng 34:1117–1128

    Article  Google Scholar 

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Authors and Affiliations

  1. Bioengineering Laboratory, Chemical Engineering Department, Superior Institute of Engineering from Porto Polytechnic Institute, Rua Dr António Bernardino de Almeida, 431, 4200-072, Porto, Portugal

    Jurrian Vanden Bussche & Eduardo V. Soares

  2. Department Industrial Engineering, KaHO St.-Lieven, Gebroeders Desmetstraat 1, 9000, Ghent, Belgium

    Jurrian Vanden Bussche

  3. IBB—Institute for Biotechnology and Bioengineering, Centre for Biological Engineering, Universidade do Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Eduardo V. Soares

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  1. Jurrian Vanden Bussche
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  2. Eduardo V. Soares
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Correspondence to Eduardo V. Soares.

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Bussche, J.V., Soares, E.V. Lead induces oxidative stress and phenotypic markers of apoptosis in Saccharomyces cerevisiae . Appl Microbiol Biotechnol 90, 679–687 (2011). https://doi.org/10.1007/s00253-010-3056-7

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  • DOI: https://doi.org/10.1007/s00253-010-3056-7

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