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Cr-(III)-organic compounds treatment causes genotoxicity and changes in DNA and protein level in Saccharomyces cerevisiae

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Abstract

Natural Cr-(III)-organic species are being known as the part of natural biogeochemical cycle of chromium, but unfortunately, their mechanism of toxicity as well as genotoxic potentiality is still unknown. To evaluate the characteristic toxic effect exerted by natural Cr-(III)-organic species on the cellular macromolecules, changes in DNA and protein level was observed. Besides, Comet assay was applied to measure genotoxic potentiality of Cr-(III)-organic species in the target organism Saccharomyces cerevisiae exposed to Cr-(III)-citrate and Cr-(III)-histidine. It has been observed that both of the Cr-(III)-organic compounds are responsible for diminution in macromolecules concentration. Cr-(III)-citrate showed ladder pattern of DNA fragmentation in support of apoptosis. Two new protein bands appeared in protein profile of the Saccharomyces cerevisiae treated with Cr-(III)-organic compounds. Thus it supports the possibility of the synthesis of stress proteins. Comet assay proved positive correlation between Cr-(III)-organic compounds’ concentration and DNA damage. The Cr-(III)-citrate causes DNA damage at the concentrations ranging from 50 to 150 mg L−1, whereas the DNA damaging capacity of Cr-(III)-histidine was found insignificant, except at highest concentration (150 mg L−1). These results can throw light on the mechanism of the toxic effect as well as genotoxicity exerted by natural Cr-(III)-organic species.

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References

  • Arslan P, Beltrame M, Tomasi A (1987) Intracellular chromium reduction. Biochim Biophys Acta 931:10–15

    Article  CAS  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (2003) Current protocols in molecular biology. Wiley, London

    Google Scholar 

  • Bagchi D, Joshi SS, Bagchi M, Balmoori J, Benner EJ, Kuszynski CA, Stohs SJ (2000) Cadmium- and chromium-induced oxidative stress, DNA damage, and apoptotic cell death in cultured human chronic myelogenous leukemic K562 cells, promyelocytic leukemic HL-60 cells, and normal human peripheral blood mononuclear cells. J Biochem Mol Toxicol 14(1):33–41

    Article  CAS  Google Scholar 

  • Bagchi D, Stohs SJ, Downs BW, Bagchi M, Preuss HG (2002) Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology 180(1):5–22

    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 

  • Barnhart J (1997) Chromium chemistry and implications for environmental fate and toxicity. J Soil Contam 6:561–568

    CAS  Google Scholar 

  • Beaubleu S, Nriagu J, Blowes D, Lawson G (1994) Chromium speciation and distribution in the Great Lakes. Environ Sci Technol 28:730–736

    Article  Google Scholar 

  • Blackwell KJ, Tobin JM, Avery SV (1998) Manganese toxicity towards Saccharomyces cerevisiae: dependence on intracellular and extracellular magnesium conc. Appl Microbiol Biotechnol 49:751–757

    Article  CAS  Google Scholar 

  • Blankenship LJ, Manning FC, Orenstein JM, Patierno SR (1994) Apoptosis is the mode of cell death caused by carcinogenic chromium. Toxicol Appl Pharmacol 126:75–83

    Article  CAS  Google Scholar 

  • Blasco L, Feijoo-Siota L, Veiga-Crespo P, Villa TG (2008) Genetic stabilization of Saccharomyces cerevisiae oenological strains by using benomyl. Int Microbiol 11:127–132

    Google Scholar 

  • Błasiak J, Kowalik J (2000) A comparison of the in vitro genotoxicity of tri- and hexavalent chromium. Mutat Res/Genet Toxicol Environ Mutagen 469(1):135–145

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Casadevall M, Fresco PC, Kortenkamp A (1999) Chromium(VI)-mediated DNA damage: oxidative pathways resulting in the formation of DNA breaks and abasic sites. Chem Biol Interact 123:117–132

    Article  CAS  Google Scholar 

  • Catellas I, Petit A, Zukor DJ, Huk OL (2001) Cytotoxic and apoptotic effects of cobalt and chromium ions on J774 macrophages-implication of caspase-3 in the apoptotic pathway. J Mater Sci Mater Med 12:949–953

    Article  Google Scholar 

  • Chatterjee N, Luo Z (2009a) Effect of two different Cr-(III)-organic compounds exposure to Saccharomyces cerevisiae. Toxicol Environ Chem. doi:10.1080/02772240902830763

  • Chatterjee N, Luo Z, Malghani S, Lian JJ, Zheng W (2009b) Uptake and distribution of chromium in Saccharomyces cerevisiae exposed to Cr-(III)-organic compounds. Chem Speciat Bioavailab (accepted-CSB090275). doi:10.3184/095422909X12554538843778

  • Chen J, Thilly WG (1994) Mutational spectrum of chromium(VI) in human cells. Mutat Res 323:21–27

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Comber S, Gardner M (2003) Chromium redox speciation in natural waters. J Environ Monit 5:410–413

    Article  CAS  Google Scholar 

  • Danadevi K, Roya R, Saleha B, Paramjit G (2004) Genotoxic evaluation of welders occupationally exposed to chromium and nickel using the comet and micronucleus assays. Mutagenesis 19:35–41

    Article  CAS  Google Scholar 

  • Dayan AD, Paine AJ (2001) Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Human Exp Toxicol 20:439–451

    Article  CAS  Google Scholar 

  • Du L, Yu Y, Chen J, Liu Y, Xia Y, Chen Q, Liu X (2007) Arsenic induces caspase- and mitochondria-mediatedapoptosis in Saccharomyces cerevisiae. FEMS Yeast Res 7:860–865

    Article  CAS  Google Scholar 

  • Feng WY, Li B, Liu J, Chai ZF, Zhang PQ, Gao YX, Zhao JJ (2003) Study of chromium-containing proteins in subcellularfractions of rat liver by enriched stable isotopic tracer technique and gel filtration chromatography. Anal Bioanal Chem 375:363–368

    CAS  Google Scholar 

  • Flora SD, Bagnasco M, Serra D, Zanacchi P (1990) Genotoxicity of chromium compounds. A review. Mutat Res 238:99–172

    Google Scholar 

  • Florence TM (1982) The speciation of trace elements in waters. Talanta 29:345–364

    Article  CAS  Google Scholar 

  • Georgieva M, Harata M, Miloshev G (2008) The nuclear actin-related protein Act3p/Arp4 influences yeast cell shape and bulk chromatin organization. J Cell Biochem 104:59–67

    Article  CAS  Google Scholar 

  • Icopini GA, Long DT (2002) Speciation of aqueous chromium by use of solid-phase extractions in the field. Environ Sci Technol 36:2994–2999

    Article  CAS  Google Scholar 

  • James BR, Bartlett RJ (1983) Behavior of chromium in soils: V. Fate of organically complexed Cr(III) added to soil. J Environ Anal 12:169–172

    CAS  Google Scholar 

  • Kaczynski SE, Kieber RJ (1993) Aqueous trivalent chromium photoproduction in natural waters. Environ Sci Technol 27:1572–1576

    Article  CAS  Google Scholar 

  • Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radic Biol Med 32:958–967

    Article  CAS  Google Scholar 

  • Krupa R, Stañczak M, Walter Z (2002) Chromium incorporated in RNA and DNA. Verlag der Zeitschrift für Naturforschung Tübingen 57(c):951–953

  • Ksheminska H, Jaglarz A, Fedorovych D, Babyak L, Yanovych D, Kaszycki P, Koloczek H (2003) Bioremediation of chromium by the yeast Pichia guilliermondii: toxicity and accumulation of Cr(III) and Cr(VI) and the influence of riboflavin on Cr tolerance. Microbiol Res 158:59–67

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Lichtenberg-Frate H, Schmitta M, Gellertb G, Ludwig J (2003) A yeast-based method for the detection of cyto- and genotoxicity. Toxicol In Vitro 17:709–716

    Article  CAS  Google Scholar 

  • Liu S, Medvedovic M, Dixon K (1999) Mutational specificity in a shuttle vector replicating in chromium(VI)-treated mammalian cells. Environ Mol Mutagen 33:313–319

    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, 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 et al (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9(4):911–917

    Article  CAS  Google Scholar 

  • Maines DM (2005) Assessment of cell toxicity. In: Costa LG (ed) Current protocols in toxicology. Wiley, London, pp 174–453

    Google Scholar 

  • Manning FC, Xu J, Patierno SR (1992) Transcriptional inhibition by carcinogenic chromate: relationship to DNA damage. Mol Carcinog 6:270–279

    Article  CAS  Google Scholar 

  • Matsuyama S, Nouraini S, Reed JC (1999) Yeast as a tool for apoptosis research. Curr Opin Microbiol 2:618–623

    Article  CAS  Google Scholar 

  • Mattuck R, Nikolaidis NP (1996) Chromium mobility in freshwater wetlands. J Contam Hydrol 23:213–232

    Article  CAS  Google Scholar 

  • Merk O, Reiser K, Speit G (2000) Analysis of chromate-induced DNA–protein crosslinks with the comet assay. Mutat Res/Genet Toxicol Environ Mutagen 471:71–80

    Article  CAS  Google Scholar 

  • Miloshev G, Mihaylov I, Anachkova B (2002) Application of the single cell gel electrophoresis on yeast cells. Mutat Res/Genet Toxicol Environ Mutagen 513:69–74

    Article  CAS  Google Scholar 

  • Nakayama E, Kuwamoto T, Tsurubo S, Tokoro H, Fujinaga T (1981) Chemical speciation of chromium in sea water. Part 1. Effect of naturally occurring organic materials on the complex formation of chromium(III). Anal Chim Acta 130:289–294

    Article  CAS  Google Scholar 

  • Norseth T (1986) The carcinogenicity of chromium and its salts. Brit J Ind Med 43:649–651

    CAS  Google Scholar 

  • O’Brien TJ, Fornsaglio JL, Ceryak S, Patierno SR (2002) Effects of hexavalent chromium on the survival and cell cycle distribution of DNA repair-deficient S. cerevisiae. DNA Repair 1(8):617–627

    Google Scholar 

  • O’Brien TJ, Ceryak S, Patierno SR (2003) Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat Res/Fundam Mol Mech Mutagen 533:3–36

    Article  Google Scholar 

  • O’Brien TJ, Jiang GH, Chun G, Mandel HG, Westphal CS, Kahen K, Montaser A, States JC, Patierno SR (2006) Incision of trivalent chromium [Cr(III)]-induced DNA damage by Bacillus caldotenax UvrABC endonuclease. Mutat Res/Genet Toxicol Environ Mutagen 610:85–92

    Article  Google Scholar 

  • Olive PL, Banath JP, Durand RE (1990) Detection of etoposide resistance by measuring DNA damage in individual Chinese hamster cells. J Natl Cancer Inst 82(9):779–783

    Article  CAS  Google Scholar 

  • Paš M, Mila R, Drašlar K, Nataša P, Raspor P (2004) Uptake of chromium(III) and chromium(VI) compounds in the yeast cell structure. Biometals 17:25–33

    Article  Google Scholar 

  • Poli P, Buschini A, Restivo FM, Ficarelli A, Cassoni F, Ferrero I, Rossi C (1999) Comet assay application in environmental monitoring: DNA damage in human leukocytes and plant cells in comparison with bacterial and yeast tests. Mutagenesis 14(6):547–556

    Article  CAS  Google Scholar 

  • Puzon GJ, Petersen JN, Roberts AG, Kramer DM, Xun L (2002) A bacterial flavin reductase system reduces chromate to a soluble chromium (III)–NDA+ complex. Biochem Biophys Res Commun 294:76–81

    Article  CAS  Google Scholar 

  • Puzon GJ, Roberts AG, Kramer DM, Xun L (2005) Formation of soluble organo-chromium (III) complexes after chromate reduction in the presence of cellular organics. Environ Sci Technol 39:2811–2817

    Article  CAS  Google Scholar 

  • Puzon GJ, Tokala RK, Zhang H, Yonge D, Peyton BM, Xun L (2008) Mobility and recalcitrance of organo-chromium (III) complexes. Chemosphere 70:2054–2058

    Article  CAS  Google Scholar 

  • Raspor P, Plesničar S, Gazdag Z, Pesti M, Miklavčič M, Lah B, Logar-Marinsek R, Poljša B (2005) Prevention of intracellular oxidation in yeast: the role of vitamin E analogue, Trolox (6-hydroxy-2,5,7,8-tetramethylkroman-2-carboxyl acid). Cell Biol Int 29(1):57–63

    Article  CAS  Google Scholar 

  • Reiter J, Herker E, Madeo F, Schmitt MJ (2005) Viral killer toxins induce caspase-mediated apoptosis in yeast. J Cell Biol 3:353–358

    Article  Google Scholar 

  • Richard FC, Bourg ACM (1991) Aqueous geochemistry of chromium: a review. Water Res 25:807–816

    Article  CAS  Google Scholar 

  • Schmitt M, Gellert G, Ludwig J, Lichtenberg-Frate H (2004) Phenotypic yeast growth analysis for chronic toxicity testing. Ecotoxicol Environ Saf 59:142–150

    Article  CAS  Google Scholar 

  • Severin FF, Hyman AA (2002) Pheromone induces programmed cell death in S. cerevisiae. Curr Biol 12:R233–R235

    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 

  • Shrivastava HY, Nair BU (2000) Protein degradation by peroxide catalyzed by chromium (III): role of coordinated ligand. Biochem Biophys Res Commun 270:749–754

    Article  CAS  Google Scholar 

  • Shrivastava HY, Nair BU (2004) Fluorescence resonance energy transfer from tryptophan to a chromium(III) complex accompanied by non-specific cleavage of albumin: a step forward towards the development of a novel photoprotease. J Inorg Biochem 98:991–994

    Article  CAS  Google Scholar 

  • Singh J, Snow ET (1988) Chromium(III) decreases the fidelity of human DNA polymerase beta. Biochemistry 37:9371–9378

    Article  Google Scholar 

  • Speetjens JK, Collins RA, Vincent JB, Woski SA (1999) The nutritional supplement chromium(III) tris(picolinate) cleaves DNA. Chem Res Toxicol 12:483–487

    Article  CAS  Google Scholar 

  • Srivastava S, Prakash S, Srivastava MM (1999) Chromium mobilization and plant availability—the impact of organic complexing ligands. Plant Soil 212:203–208

    Article  CAS  Google Scholar 

  • Stearns DM, Silveira SM, Wolf KK, Luke AM (2002) Chromium(III) tris(picolinate) is mutagenic at the hypoxanthine (guanine) phosphoribosyltransferase locus in Chinese hamster ovary cells. Mutat Res 513:135–142

    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 

  • Świetlik R (1998) Speciation analysis of chromium in waters. J Environ Stud 7:257–266

    Google Scholar 

  • Tsou TC, Lin RJ, Yang JL (1997) Mutational spectrum induced by chromium(III) in shuttle vectors replicated in human cells: relationship to Cr(III)–DNA interactions. Chem Res Toxicol 10:962–970

    Article  CAS  Google Scholar 

  • Vido K, Spector D, Lagniel G, Lopez S, Toledano M, Labarre J (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J Biol Chem 276:8469–8474

    Article  CAS  Google Scholar 

  • Walsh AR, O’Halloran J (1996) Chromium speciation in the tannery effluent-I. An assessment of techniques and the role of organic Cr-(III) complexes. Wat Res 30:2393–2400

    Article  CAS  Google Scholar 

  • Wang WX, Griscom SB, Fischer NS (1997) Bioavailability of Cr(III) and Cr(VI) to marine mussels from solute and particulate pathways. Environ Sci Technol 31:603–611

    Article  CAS  Google Scholar 

  • Wang J, Mao Z, Zhao X (2004) Response of Saccharomyces cerevisiae to chromium stress. Process Biochem 39:1231–1235

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National High Technology Research and Development programme of China (863 programme) (No. 2007AA06Z337) and the School of Environmental Studies, China University of Geosciences, Wuhan, China. Nivedita Chatterjee is grateful to the Chinese Scholarship Council (CSC) and Ministry of Human Resource Development (MHRD), India, for awarding the research fellowship. The authors would like to thank Dr. Julia Ellis Burnet for her help in editing and correcting this manuscript.

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  1. Key Laboratory of Biogeology and Environmental Geology, Ministry of Education (BGEG), School of Environmental Studies, China University of Geosciences, 388 Lumo Road, Wuhan, Hubei, 430074, China

    Nivedita Chatterjee & Zejiao Luo

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  1. Nivedita Chatterjee
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  2. Zejiao Luo
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Correspondence to Nivedita Chatterjee.

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Chatterjee, N., Luo, Z. Cr-(III)-organic compounds treatment causes genotoxicity and changes in DNA and protein level in Saccharomyces cerevisiae . Ecotoxicology 19, 593–603 (2010). https://doi.org/10.1007/s10646-009-0420-4

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