Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 149, Issue 1, 2009, Pages 90-96

  Rico, Daniel ^a,b   Martín González, Ana ^a   Díaz, Silvia ^a   de Lucas, Pilar ^a   Gutiérrez, Juan Carlos ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b Structural Biology and Biocomputing Programme   (Spain)

Author keywords

Ciliated protozoa; Fluorophores; Heavy metals; Reactive oxygen species

Indexed keywords

CADMIUM; COPPER; FRESH WATER; HEAVY METAL; REACTIVE OXYGEN METABOLITE; ZINC;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPE; HEAVY METAL POISONING; IMAGING SYSTEM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTOZOON; SOIL POLLUTION; TETRAHYMENA; WATER CONTAMINATION;

CILIOPHORA; COLPODA STEINII; METAMORPHA; MYXOZOA; TETRAHYMENA SP.;

EID: 56949092491     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2008.07.016     Document Type: Article

References (71)

1. Aguilar J., Dorronsoro C., Fernández E., Fernández J., García I., Martín F., and Simón M. Soil pollution by a pyrite mine spill in Spain: evolution in time. Environ. Pollut. 132 (2004) 395-401
2. Avery S.V. Metal toxicity in yeast and the role in oxidative stress. Adv. Appl. Microbiol. 49 (2001) 111-142
3. Benov L., Sztejnberg L., and Fridovich I. Critical evaluation of the use of hydroetidine as a measure of superoxide anion radical. Free Rad. Biol. Med. 25 (1998) 826-831
4. Bopp S.K., Abicht H.K., and Knauer K. Copper-induced oxidative stress in rainbow trout gill cells. Aquatic Toxicol. 86 (2008) 197-204
5. Brennan R.J., and Schiestl R.H. Cadmium is an inducer of oxidative stress in yeast. Mutation Res. 356 (1996) 171-178
6. Chang L.W. Toxicology of Metals (1996), CRC Lewis Boca Raton
7. Chimienti F., Jourdan E., Favier A., and Seve M. Zinc resistance impairs sensitivity to oxidative stress in HeLa cells: protection through metallothionein expression. Free Rad. Biol. Med. 31 (2001) 1179-1190
8. Christensen S.T., Chemnitz J., Straarup E.M., Kristiansen K., Wheatley D.N., and Rasmussen L. Stauroporine-induced cell death in Tetrahymena thermophila has mixed characteristics of both apoptotic and autophagic degeneration. Cell Biol. Int. 22 (1998) 591-598
9. Coppellotti O. Sensitivity to copper in a ciliate as possible component of biological monitoring in the lagoon of Venice. Arch. Environ. Contam. Toxicol. 35 (1998) 417-425
10. Crow J.P. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurements of reactive nitrogen and oxygen species. Nitric Oxide 1 (1997) 145-147
11. Cuypers A., Vangronsveld J., and Clijsters H. The chemical behaviour of heavy metals plays a prominent role in the induction of oxidative stress. Free Rad. Res. 31 (1999) S39-43
12. Dayed V.R., Grominsky S., DeWitte-Orr S.J., Sotornik D., Yeung C.R., Lee L.E.J., Lynn D.H., and Bols N.C. Comparing a ciliate and fish cell line for their sensitivity to several classes of toxicants by the novel application of multiwell filter plates to Tetrahymena. Res. Microbiol. 156 (2005) 93-103
13. Delmonte Corrado M.U., Trielli F., Amaroli A., Ognibene M., and Falugi C. Protists as tools for environmental biomonitoring: importance of cholinesterase enzyme activities. In: Burk A.R. (Ed). Water Pollution: New Research (2005), Nova Science Publishers, Hauppauge, NY 181-200
14. Díaz S., Martín-González A., and Gutiérrez J.C. Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. Environ. Int. 32 (2006) 711-717
15. Dini F. Relationship between breeding systems and resistance to mercury in Euplotes crassus (Ciliophora, Hypotrichida). Mar. Ecol. Prog. Ser. 4 (1981) 195-202
16. Dorta D.J., Leite S., DeMarco K.C., Prado I.M.R., Rodrigues T., Mingatto F., Uyemura S.A., Santos A.C., and Curti A. A proponed sequence of events for cadmium-induced mitochondrial impairment. J. Inog. Biochem. 97 (2003) 251-257
17. Fernández-Galiano D. Silver impregnation of ciliated protozoa: procedure yielding good results with the pyridinated silver carbonate method. Trans. Am. Microsc. Soc. 95 (1976) 557-560
18. Formigari A., Irato P., and Santon A. Zinc, antioxidants systems and metallothioneins in metal mediated-apoptosis: biochemical and cytochemical aspects. Comp. Biochem. Physiol. C 146 (2007) 443-459
19. Fujs S., Gazdag Z., Polisak B., Stibili V., Milacic R., Pesti M., Raspor P., and Batic M. The oxidative stress response of the yeast Candida intermedia to copper, zinc, and selenium exposure. J. Basic Microbiol. 45 (2005) 125-135
20. Galán E., González I., and Fernández-Calian J.C. Residual pollution load of soils impacted by Aznalcóllar (Spain) mining spill after clean-up operations. Sci. Total Environ. 286 (2002) 167-179
21. Gallego A., Martín-González A., Ortega R., and Gutiérrez J.C. Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium, zinc and copper on populations of the ciliated protozoan Tetrahymena thermophila. Chemosphere 64 (2007) 647-661
22. Gilron G.L., and Lynn D.H. Ciliated protozoa as test organisms in toxicity assessments. In: Wells P.G. (Ed). Microcale Testing in Aquatic Toxicology (1998), CRC Press, Boca Raton 323-336
23. Gomes A., Fernandes E., and Lima J.L.F.C. Fluorescence probes used for detection of reactive oxygen species. J. Biochem. Biophys. Meths 65 (2005) 45-80
24. Gómez-Mendicute A., and Cajaraville M.P. Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes. Toxicol. In Vitro 17 (2003) 539-546
25. Gutiérrez J.C., and Orias E. Developmental and genetic effects of alcian blue in conjugating Tetrahymena thermophila: doublet formation and macronuclear retention. Cell Differ. 18 (1986) 243-256
26. Gutiérrez J.C., Martín-González A., Díaz S., and Ortega R. Ciliates as potencial source of cellular and molecular biomarkers/biosensors for heavy metal pollution. Eur. J. Protistol. 39 (2003) 461-467
27. Haase H., Wätjen W., and Beyersmann D. Zinc induces apoptosis that can be suppressed by lanthanum in C6 rat glioma cells. J. Biol. Chem. 382 (2001) 1227-1234
28. Halliwell B., and Whiterman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it what do the results mean?. Br. J. Pharmacol. 142 (2004) 231-255
29. Hassoun E.A., and Stohs S.J. Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A1 cell cultures. Toxicology 112 (1996) 219-226
30. Heikens A., Peijnenburg W.J., and Hendriks A.J. Bioaccumulation of heavy metals in terrestrial invertebrates. Environ. Pollut 113 (2001) 385-293
31. Jakubowski W., and Bartosz G. 2,7-Dichlorofluorescein oxidation and reactive oxygen species: what does it measure?. Cell Biol. Int. 10 (2000) 757-760
32. Janssen C.R., and Heijerick D.G. Algal toxicity tests for environmental assessments of metals. Rev. Environ. Contam. Toxicol. 178 (2003) 23-52
33. Kovacs P., Muller W.E., and Csaba W. A lectin-like molecule is discharged from mucocysts of Tetrahymena thermophila in the presence of insulin. J. Eukaryot. Microbiol. 44 (1997) 487-491
34. Kawakami, M., Inagawa, R., Hosokawa, T., Saito, T., Kurasaki, A., in press. Mechanism of apoptosis induced by copper in PC12 cells. Food Chem. Toxicol. doi: 10.1016/j.fct. 2008. 02.014.
35. Krumschnabel G., Manzl C., Berger C., and Hofer B. Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol. Appl. Pharmacol. 209 (2005) 62-73
36. Leonard S.S., Bower J.J., and Shi X. Metal-induced toxicity, carcinogenesis, mechanisms and cellular responses. Mol. Cell Biochem. 255 (2004) 3-10
37. Madoni P., and Romeo M.P. Acute toxicity of heavy metals towards freshwater ciliated protists. Environ. Pollut 141 (2006) 1-7
38. Madoni P., Esteban G., and Gorbi G. Acute toxicity of cadmium, copper, mercury, and zinc to the ciliates from activated sludge plants. Bull. Environ. Contam. Toxicol. 49 (1992) 900-905
39. Martín-González A., Benítez L., and Gutiérrez J.C. Cortical and nuclear events during cell division and resting cyst formation in Colpoda inflata. J. Eukaryot. Microbiol. 38 (1991) 338-344
40. Martín-González A., Díaz S., Jareño C., and Gutiérrez J.C. The use of protists in ecotoxicology: applications and perspectives. Recent Res. Devel. Microbiol. 3 (1999) 93-111
41. Martín-González A., Borniquel S., Diaz S., Ortega R., and Gutiérrez J.C. Ultrastructural alterations in ciliated protozoa under heavy metal exposure. Cell Biol. Int. 29 (2005) 119-126
42. Martín-González A., Diaz S., Borniquel S., Gallego A., and Gutiérrez J.C. Cytotoxicity and bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Res. Microbiol. 157 (2006) 108-118
43. Metha R., Templeton D.M., and O'Brien P.J. Mitochondrial involvement in genetically determined transition metal toxicity II. Copper toxicity. Chem.-Biol. Interact. 163 (2006) 77-85
44. Nicolau A., Mota M., and Lima N. Physiological responses of Tetrahymena pyriformis to copper, zinc, cicloheximide and Triton X-100. FEMS Microbiol. Ecol. 30 (1999) 209-216
45. Nilsson J.R. Tetrahymena in cytotoxicology: with special reference to effects of heavy metals and selected drugs. Eur. J. Protistol. 25 (1989) 2-25
46. Nilsson J.R. Tetrahymena recovering from heavy metal accumulation of gold salt. Acta Protozool. 36 (1997) 111-119
47. Oteiza P.I., Mackenzie G.G., and Verstraeten S.V. Metals in neurodegeneration: involvement of oxidants and antioxidants-sensitive transcription factors. Mol. Asp. Med. 25 (2004) 103-115
48. Piccinni E., Irato P., Coppellotti O., and Guidolin L. Biochemical and ultrastructural data on Tetrahymena pyriformis treated with copper and cadmium. J. Biol. Sci. 88 (1987) 283-293
49. Pinto E., Sigaud-Kutner T.C.S., Leitao M.A.S., Okamoto O.K., Morse D., and Colepicolo P. Heavy Metal-induced Oxidative Stress in Algae. J. Phycol. 39 (2003) 1008-1018
50. Pulido M.D., and Parrish A.R. Metal-induced apoptosis: mechanisms. Mut. Res. 533 (2003) 227-241
51. Ricci N. Protozoa: bioindicators of environmental monitoring and pollution control. In: Rana B.C. (Ed). Pollution and Biomonitoring (1995), Tata McGraw-Hill Publishing Company, New Delhi 240-269
52. Ricci N., Luvera G., Cacciatori M., Banchetti R., and Lueken W. The effects of 2 μM Hg++ on the ethogram of Euplotes vannus (Ciliata, Hypotrichida). Eur. J. Protistol. 33 (1997) 63-71
53. Satir D. Dibucaine-induced synchronous mucocyst secretion in Tetrahymena. Cell Biol. Int. Rep. 1 (1977) 69-73
54. Sauvant M., Pepin D., Bohatier J., Groliere C.A., and Guillot J. Toxicity assessment of 16 inorganic environmental pollutants by six bioassays. Ecotoxicol. Environ. Saf. 37 (1997) 131-140
55. Sauvant M., Pepin D., and Piccinni E. Tetrahymena pyriformis: a tool for toxicological studies. A review. Chemosphere 38 (1999) 1631-1669
56. Schützendübel A., and Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53 (2002) 1352-1365
57. Seebaugh D.R., Goto D., and Wallance W.G. Bioenhancement of cadmium transfer along a multilevel food chain. Mar. Environ. Res. 59 (2005) 473-491
58. Szücs S., Vámosi G., Póka R., Sálváry A., Bádos H., Balázs M., Kappelmayer J., Téth L., Szöllösi J., and Adány H. Single-cell measurement of superoxide anion and hydrogen peroxide production by human neutrophils with digital imaging fluorescence microscopy. Cytometry 33 (1998) 19-31
59. Tate Jr. D.J., Miceli M.V., and Newsome D.A. Zinc protects against oxidative damage in cultured retinal pigment epithelian cells. Free Radical Biol. Med. 26 (1999) 704-713
60. Trielli F., Amaroli A., Sifredi F., Marchi B., Falugi C., and Delmonte Corrado M.U. Effects of xenobiotic compounds on the cell activities of Euplotes crassus, a single-cell eukaryotic test organism for the study of the pollution of marine sediments. Aquat. Toxicol. 83 (2007) 272-283
61. 2+. Chemosphere 62 (2006) 538-544
62. Truong-Tran A.Q., Carter J.C., Ruffin R.E., and Zalewski P.D. The role of zinc in caspase activation and apoptotic cell death. BioMetals 14 (2001) 315-330
63. Valko M., Morris H., and Cronin M.T.D. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12 (2005) 1161-1208
64. Valko M., Izakovic M., Mazur M., Rhodes C.J., and Tester J. Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem. 266 (2004) 37-56
65. Walrand S., Valeix S., Rodriguez C., Ligot P., Chassagne J., and Vasson M.-P. Flow cytometry study of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin. Chim. Acta 331 (2003) 103-110
66. Wang H., and Joseph J.A. Quantifying oxidative stress by dichlorofluorescein assay using microplate reader. Free Radical Biol. Med. 27 (1999) 612-616
67. Wang Y., Fang J., Leonard S.S., and Rao K.M. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radical Biol. Med. 36 (2004) 1434-1443
68. Watanabe M., and Suzuki T. Involvement of reactive oxygen stress in cadmium-induced cellular damage in Euglena gracilis. Comp. Biochem. Physiol. C 131 (2002) 491-500
69. Watanabe M., Henmi K., Ogawa K., and Suzuki T. Cadmium-dependent generation of reactive oxygen species and mitochondrial DNA breaks in photosynthetic and non-photosynthetic strains of Euglena gracilis. Comp. Biochem. Physiol. C 134 (2003) 227-234
70. Wätjen W., and Beyersmann D. Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress. BioMetals 17 (2004) 65-78
71. Xu Z., Bowers N., and Pratt J.R. Variation in morphology, ecology and toxicological responses of Colpoda inflata (Stokes) collected from five biogeographic realms. Eur. J. Protistol. 33 (1997) 136-144