Effects of microcystin-LR on Saccharomyces cerevisiae growth, oxidative stress and apoptosis

Toxicon

Volumn 90, Issue , 2014, Pages 191-198

  Valério, Elisabete ^a,b   Vilares, Arminda ^a   Campos, Alexandre ^b   Pereira, Paulo ^a   Vasconcelos, Vitor ^b,c  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

Antioxidant system; Apoptosis; Growth; Microcystin LR; ROS; Saccharomyces cerevisiae

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MICROCYSTIN LR; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; MICROCYSTIN;

APOPTOSIS; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; FLOW CYTOMETRY; FUNGAL STRAIN; FUNGUS GROWTH; GROWTH CURVE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST CELL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

SACCHAROMYCES CEREVISIAE;

APOPTOSIS; MICROCYSTINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE;

EID: 84906851662     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2014.08.059     Document Type: Article

References (41)

1. C. Bowler, W. Van Camp, M. Van Montagu, D. Inzé, and K. Asada Superoxide dismutase in plants CRC Crit. Rev. Plant Sci. 13 1994 199 218 (Pubitemid 2134136)
2. J.V. Bussche, and E.V. Soares Lead induces oxidative stress and phenotypic markers of apoptosis in Saccharomyces cerevisiae Appl. Microbiol. Biotechnol. 90 2011 679 687
3. A. Campos, and V. Vasconcelos Molecular mechanisms of microcystin toxicity in animal cells Int. J. Mol. Sci. 11 2010 268 287
4. G.A. Codd, L.F. Morrison, and J.S. Metcalf Cyanobacterial toxins: risk management for health protection Toxicol. Appl. Pharmacol. 203 2005 264 272 (Pubitemid 40311873)
5. T. Chen, Q. Wang, J. Cui, W. Yang, Q. Shi, Z. Hua, J. Ji, and P. Shen Induction of apoptosis in mouse liver by Microcystin-LR: a combined transcriptomic, proteomic, and simulation strategy Mol. Cell. Proteomics 4 2005 958 974 (Pubitemid 41309153)
6. H.M. Davey, and P. Hexley Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide Environ. Microbiol. 13 2011 163 171
7. E. Dias, M. Andrade, E. Alverca, P. Pereira, M.C.C. Batoréu, P. Jordan, and M.J. Silva Comparative study of the cytotoxic effect of microcistin-LR and purified extracts from Microcystis aeruginosa on a kidney cell line Toxicon 53 2009 487 495
8. E. Dias, P. Matos, P. Pereira, M.C.C. Batoréu, M.J. Silva, and P. Jordan Microcystin-LR activates the ERK1/2 kinases and stimulates the proliferation of the monkey kidney-derived cell line Vero-E6 Toxicol. in Vitro 24 2010 1689 1695
9. W.X. Ding, and C.N. Ong Role of oxidative stress and mitochondrial changes in cyanobacteria-induced apoptosis and hepatotoxicity FEMS Microbiol. Lett. 10880 2003 1 7 (Pubitemid 36324313)
10. W.-X. Ding, H.-M. Shen, and C.-N. Ong Critical role of reactive oxygen species formation in microcystin-induced cytoskeleton disruption in primary cultured hepatocytes J. Toxicol. Environ. Health A 64 2001 507 519 (Pubitemid 33139650)
11. W.L. Fischer, S. Altheimer, V. Cattori, P.J. Meier, D.R. Dietrich, and B. Hagenbuch Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin Toxicol. Appl. Pharmacol. 203 2005 257 263 (Pubitemid 40311872)
12. L.K. Folkes, K.B. Patel, P. Wardman, and M. Wrona Kinetics of reaction of nitrogen dioxide with dihydrorhodamine and the reaction of the dihydrorhodamine radical with oxygen: implications for quantifying peroxynitrite formation in cells Arch. Biochem. Biophys. 484 2009 122 126
13. F.N. Gil, A.C. Gonçalves, M.J. Jacinto, J.D. Becker, and C.A. Viegas Transcriptional profiling in Saccharomyces cerevisiae relevant for predicting alachlor mechanisms of toxicity Environ. Toxicol. Chem. 30 2011 2506 2518
14. R. Guzmán-Guillén, A.I. Prieto, V.M. Vasconcelos, and A.M. Cameán Cyanobacterium producing cylindrospermopsin cause oxidative stress at environmentally relevant concentrations in sub-chronically exposed tilapia (Oreochromis niloticus) Chemosphere 90 2013 1184 1194
15. A. Huguet, J. Henri, M. Petitpas, K. Hogeveen, and V. Fessard Comparative cytotoxicity, oxidative stress, and cytokine secretion induced by two cyanotoxin variants, Microcystin LR and RR, in human intestinal Caco-2 Cells J. Biochem. Mol. Toxicol. 27 2013 253 258
16. R. Klassen, and F. Meinhardt Induction of DNA damage and apoptosis in Saccharomyces cerevisiae by a yeast killer toxin Cell. Microbiol. 7 2005 393 401 (Pubitemid 40277919)
17. X. Li, Y. Liu, L. Song, and J. Liu Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin-LR Toxicon 42 2003 85 89 (Pubitemid 37297564)
18. V.D. Longo, E.B. Gralla, and J.S. Valentine Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae: mitochondrial production of toxic oxygen species in vivo J. Biol. Chem. 271 1996 12275 12280 (Pubitemid 26160890)
19. O.H. Lowry, N.J. Rosenbrough, A.L. Farr, and R.J. Randall Protein measurement with the folin phenol reagent J. Biol. Chem. 193 1951 265 275
20. P. Ludovico, M.J. Sousa, M.T. Silva, C. Leão, and M. Côrte-Real Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid Microbiology 147 2001 2409 2415 (Pubitemid 32899237)
21. V.I. Lushchak Budding yeast Saccharomyces cerevisiae as a model to study oxidative modification of proteins in eukaryotes Acta Biochim. Pol. 53 2006 679 684 (Pubitemid 46090117)
22. F. Madeo, E. Fröhlich, and K.-U. Fröhlich A yeast mutant showing diagnostic markers of early and late apoptosis J. Cell. Biol. 139 1997 729 734 (Pubitemid 27486568)
23. F. Madeo, E. Fröhlich, M. Ligr, M. Gray, S.J. Sigrist, D.H. Wolf, and K. Fröhlich Oxygen stress: a regulator of apoptosis in yeast J. Cell. Biol. 145 1999 757 767 (Pubitemid 29240853)
24. C.M. McDermott, C.W. Nho, W. Howard, and B. Holton The cyanobacterial toxin, microcystin-LR, can induce apoptosis in a variety of cell types Toxicon 36 1998 1981 1996 (Pubitemid 28532776)
25. F. Meier-Abt, Y. Mokrab, and K. Mizuguchi Organic Anion Transporting Polypeptides of the OATP/SLCO superfamily: identification of new members in nonmammalian species, comparative modeling and a potential transport mode J. Membr. Biol. 208 2005 213 227
26. M. Menacho-Márquez, and J. Murguía Yeast on drugs: Saccharomyces cerevisiae as a tool for anticancer drug research Clin. Transl. Oncol. 9 2007 221 228
27. C. Menezes, E. ValeÍrio, and E. Dias The kidney Vero-E6 cell line: a suitable model to study the toxicity of microcystins Sivakumar Gowder, New Insights into Toxicity and Drug Testing 2013 InTech ISBN: 978-953-51-0946-4
28. Q. Nong, M. Komatsu, K. Izumo, H.P. Indo, B. Xu, K. Aoyama, H.J. Majima, M. Horiuchi, K. Morimoto, and T. Takeuchi Involvement of reactive oxygen species in Microcystin-LR-induced cytogenotoxicity Free Radic. Res. 41 2007 1326 1337 (Pubitemid 350302188)
29. S.R. Pereira, V.M. Vasconcelos, and A. Antunes The phosphoprotein phosphatase family of Ser/Thr phosphatases as principal targets of naturally occurring toxins Crit. Rev. Toxicol. 41 2011 83 110
30. M. Puerto, S. Pichardo, Á. Jos, A.I. Prieto, E. Sevilla, J.E. Frías, and A.M. Cameán Differential oxidative stress responses to pure Microcystin-LR and Microcystin-containing and non-containing cyanobacterial crude extracts on Caco-2 cells Toxicon 55 2010 514 522
31. P. Radha Antioxidant Responses Evoked in vitro and in vivo by Bacopa monnieri Leaf Extracts (Ph.D. thesis) 2010 Avinashilingam Deemed University for Women Coimbatore, India
32. L.A. Rowe, N. Degtyareva, and P.W. Doetsch DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae Free Radic. Biol. Med. 45 2008 1167 1177
33. T.B. Salmon, B.A. Evert, B. Song, and P.W. Doetsch Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae Nucleic Acids Res. 32 2004 3712 3723 (Pubitemid 39161869)
34. M.E. van Apeldoorn, H.P. van Egmond, G.J.A. Speijers, and G.J.I. Bakker Toxins of cyanobacteria Mol. Nutr. Food Res. 51 2007 7 60 (Pubitemid 46144763)
35. M. Vassilakaki, and S. Pflugmacher Oxidative stress response of Synechocystis sp. (PCC 6803) due to exposure to microcystin-LR and cell-free cyanobacterial crude extract containing microcystin-LR J. Appl. Phycol. 20 2008 219 225 (Pubitemid 351693326)
36. WHO Guidelines for drinking water quality third ed. Incorporating the First and Second Addenda vol. 1 2008 World Health Organization Geneva Recommendations
37. C.Y. Yang, W.B. Wang, D.H. Li, and Y.D. Liu Growth and antioxidant system of Escherichia coli in response to Microcystin-RR Bull. Environ. Contam. Toxicol. 81 2008 427 431
38. L. Yin, J. Huang, W. Huang, D. Li, G. Wang, and Y. Liu Microcystin-RR-induced accumulation of reactive oxygen species and alteration of antioxidant systems in tobacco BY-2 cells Toxicon 46 2005 507 512 (Pubitemid 41253368)
39. B. Žegura, A. Straser, and M. Filipic Genotoxicity and potential carcinogenicity of cyanobacterial toxins-a review Mutat. Res./Rev. Mutat. Res. 727 2011 16 41
40. H. Zhang, C. Cai, W. Fang, J. Wang, Y. Zhang, J. Liu, and X. Jia Oxidative damage and apoptosis induced by microcystin-LR in the liver of Rana nigromaculata in vivo Aquat. Toxicol. 140-141 2013 11 18
41. H. Zhang, J. Zhang, Y. Chen, and Y. Zhu Microcystin-RR induces apoptosis in fish lymphocytes by generating reactive oxygen species and causing mitochondrial damage Fish Physiol. Biochem. 34 2008 307 312