Evaluation of Okadaic Acid-Induced Genotoxicity in Human Cells Using the Micronucleus Test and γH2AX Analysis

REFERENCES

• Andrievski , A. and Wilkins , R. C. 2009 . The response of gamma-H2AX in human lymphocytes and lymphocytes subsets measured in whole blood cultures . Int. J. Radiat. Biol , 85 : 369 – 76 .
   PubMed Web of Science ®Google Scholar
• Antonelli , F. , Belli , M. , Cuttone , G. , Dini , V. , Esposito , G. , Simone , G. , Sorrentino , E. and Tabocchini , M. A. 2005 . Induction and repair of DNA double-strand breaks in human cells: dephosphorylation of histone H2AX and its inhibition by calyculin A . Radiat Res , 164 : 514 – 17 .
   PubMed Web of Science ®Google Scholar
• Ao , L. , Liu , J. Y. , Gao , L. H. , Liu , S. X. , Yang , M. S. , Huang , M. H. and Cao , J. 2008 . Differential expression of genes associated with cell proliferation and apoptosis induced by okadaic acid during the transformation process of BALB/c 3T3 cells . Toxicol. In Vitro , 22 : 116 – 27 .
   PubMed Web of Science ®Google Scholar
• Aune , T. and Yndestad , M. 1993 . “ Diarrhetic shellfish poisoning ” . In Algal toxins in seafood and drinking water , Edited by: Falconer , I. R. 87 – 104 . New York : Academic Press .
   Google Scholar
• Avlasevich , S. L. , Bryce , S. M. , Cairns , S. E. and Dertinger , S. D. 2006 . In vitro micronucleus scoring by flow cytometry: Differential staining of micronuclei versus apoptotic and necrotic chromatin enhances assay reliability . Environ. Mol. Mutagen , 47 : 56 – 66 .
   PubMed Web of Science ®Google Scholar
• Bialojan , C. and Takai , A. 1988 . Inhibitory effect of marine sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics . Biochem. J , 256 : 283 – 90 .
   PubMed Web of Science ®Google Scholar
• Cabado , A. G. , Leira , F. , Vieytes , M. R. , Vieites , J. M. and Botana , L. M. 2004 . Cytoskeletal disruption is the key factor that triggers apoptosis in okadaic acid-treated neuroblastoma cells . Arch. Toxicol , 78 : 74 – 85 .
   PubMed Web of Science ®Google Scholar
• Carvalho , P. S. , Moukha , S. , Matias , W. G. and Creppy , E. E. 2006 . Comparative study of domoic acid and okadaic acid induced-chromosomal abnormalities in the Caco-2 cell line . Int. J. Environ. Res. Public Health , 3 : 4 – 10 .
   PubMedGoogle Scholar
• Chin , L. S. , Singh , S. K. , Wang , Q. and Murray , S. F. 2000 . Identification of okadaic-acid-induced genes by mRNA differential display in glioma cells . J. Biomed. Sci , 7 : 152 – 59 .
   PubMed Web of Science ®Google Scholar
• Colognato , R. , Coppedè , F. , Ponti , J. , Sabbioni , E. and Migliore , L. 2007 . Genotoxicity induced by arsenic compounds in peripheral human lymphocytes analysed by cytokinesis-block micronucleus assay . Mutagenesis , 22 : 255 – 61 .
   PubMed Web of Science ®Google Scholar
• Cordier , S. , Monfort , C. , Miossec , L. , Richarson , S. and Belin , C. 2000 . Ecological analysis of digestive cancer mortality related to contamination by diarrhetic shellfish poisoning toxins along the coasts of France . Environ. Res , 84 : 145 – 50 .
   PubMed Web of Science ®Google Scholar
• Creppy , E. E. , Traoré , A. , Baudrimont , I. , Cascante , M. and Carratú , M. R. 2002 . Recent advances in the study of epigenetic effects induced by the phycotoxin okadaic acid . Toxicology , 182 : 433 – 39 .
   Google Scholar
• Davis , M. A. , Chang , S. H. and Trump , B. F. 1996 . Differential sensitivity of normal and H-ras oncogene-transformed rat kidney epithelial cells to okadaic acid-induced apoptosis . Toxicol. Appl. Pharmacol , 141 : 93 – 01 .
   PubMed Web of Science ®Google Scholar
• Dionysiou , D. 2010 . Overview: Harmful algal blooms and natural toxins in fresh and marine waters—Exposure, occurrence, detection, toxicity, control, management and policy . Toxicon , 55 : 907 – 8 .
   PubMed Web of Science ®Google Scholar
• Fenech , M. 2007 . Cytokinesis-block micronucleus cytome assay . Nat Protocol , 2 : 1084 – 1104 .
   PubMed Web of Science ®Google Scholar
• Fernández-Capetillo , O. , Lee , A. , Nussenzweig , M. and Nussenzweig , A. 2004 . H2AX: The histone guardian of the genome . DNA Repair , 3 : 959 – 67 .
   PubMed Web of Science ®Google Scholar
• Fessard , V. , Grosse , Y. , Pfohl-Leszkowicz , A. and Puiseux-Dao , S. 1996 . Okadaic acid treatment induces DNA adduct formation in BHK21 C13 fibroblasts and HESV keratinocytes . Mutat. Res , 361 : 133 – 41 .
   PubMed Web of Science ®Google Scholar
• Franchini , A. , Malagoli , D. and Ottaviani , E. 2010 . Targets and effects of yessotoxin, okadaic acid and palytoxin: A differential review . Mar. Drugs , 8 : 658 – 77 .
   PubMed Web of Science ®Google Scholar
• Fujiki , H. , Suganuma , M. , Suguri , H. , Yoshizawa , S. , Takagi , K. , Uda , N. , Wakamatsu , K. , Yamada , K. , Murata , M. , Yasumoto , T. and Sugimura , T. 1988 . Diarrhetic shellfish toxin, dinophysistoxin-1, is a potent tumor promoter on mouse skin . Jpn. J. Cancer Res , 79 : 1089 – 93 .
   PubMedGoogle Scholar
• Fujiki , H. , Suganuma , M. , Nishiwaki , S. , Yoshizawa , S. , Yatsunami , J. , Matsushima , R. , Furuya , H. , Okabe , S. , Matsunaga , S. and Sugimura , T. 1992 . Specific mechanistic aspects of animal tumor promoters: The okadaic acid pathway . Prog. Clin. Biol. Res , 374 : 337 – 50 .
   PubMedGoogle Scholar
• Ghosh , S. , Paweletz , N. and Schroeter , D. 1992 . Effects of okadaic acid on mitotic HeLa cells . J. Cell Sci , 103 : 117 – 24 .
   PubMed Web of Science ®Google Scholar
• Gotoh , E. , Asakawa , Y. and Kosaka , H. 1995 . Inhibition of protein serine/threonine phosphatases directly induces premature chromosome condensation in mammalian somatic cells . Biomed. Res , 16 : 63 – 68 .
   Web of Science ®Google Scholar
• He , J. , Yamada , K. , Zou , L.-B. and Nabeshima , T. 2001 . Spatial memory deficit and neurodegeneration induced by the direct injection of okadaic acid into the hippocampus in rats . J. Neural. Transm , 108 : 1435 – 43 .
   PubMed Web of Science ®Google Scholar
• Ito , E. , Yasumoto , T. , Takai , A. , Imanishi , S. and Harada , K. 2002 . Investigation of the distribution and excretion of okadaic acid in mice using immunostaining method . Toxicon , 40 : 159 – 65 .
   PubMed Web of Science ®Google Scholar
• Knasmüller , S. , Mersch-Sundermann , V. , Kevekordes , S. , Darroudi , F. , Huber , W. W. , Hoelzl , C. , Bichler , J. and Majer , B. J. 2004 . Use of human-derived liver cell lines for the detection of environmental and dietary genotoxicants, current state of knowledge . Toxicology , 198 : 315 – 28 .
   PubMed Web of Science ®Google Scholar
• Laffon , B. , Pásaro , E. and Méndez , J. 2002 . DNA damage and repair in human leukocytes exposed to styrene-7,8-oxide measured by the comet assay . Toxicol. Lett , 126 : 61 – 68 .
   PubMed Web of Science ®Google Scholar
• Lago , J. , Santaclara , F. , Vieites , J. M. and Cabado , A. G. 2005 . Collapse of mitochondrial membrane potential and caspases activation are early events in okadaic acid-treated Caco-2 cells . Toxicon , 46 : 579 – 86 .
   PubMed Web of Science ®Google Scholar
• Le Hégarat , L. , Puech , L. , Fessard , V. , Poul , J. M. and Dragacci , S. 2003 . Aneugenic potential of okadaic acid revealed by the micronucleus assay combined with the FISH technique in CHO-K1 cells . Mutagenesis , 18 : 293 – 98 .
   PubMed Web of Science ®Google Scholar
• Le Hégarat , L. , Fessard , V. , Poul , J.M. , Dragacci , S. and Sanders , P. 2004 . Marine toxin okadaic acid induces aneuploidy in CHO-K1 cells in presence of rat liver postmitochondrial fraction, revealed by cytokinesis-block micronucleus assay coupled to FISH . Environ. Toxicol. , 19 : 123 – 28 .
   PubMed Web of Science ®Google Scholar
• Le Hégarat , L. , Jacquin , A.G. , Bazin , E. and Fessard , V. 2006 . Genotoxicity of the marine toxin okadaic acid, in human Caco-2 cells and in mice gut cells . Environ. Toxicol. , 21 : 55 – 64 .
   PubMed Web of Science ®Google Scholar
• Lerga , A. , Richard , C. , Delgado , M. D. , Cañelles , M. , Frade , P. , Cuadrado , M. A. and León , J. 1999 . Apoptosis and mitotic arrest are two independent effects of the protein phosphatases inhibitor okadaic acid in K562 leukemia cells . Biochem. Biophys. Res. Commun. , 260 : 256 – 64 .
   PubMed Web of Science ®Google Scholar
• López-Rodas , V. , Maneiro , E. , Martínez , J. , Navarro , M. and Costas , E. 2006 . Harmful algal blooms, red tides and human health: Diarrheic shellfish poisoning and colorectal cancer . Ann. R. Acad. Nac. Farm. , 72 : 391 – 408 .
   Google Scholar
• Matias , W. G. and Creppy , E. E. 1996 . Evidence for an enterohepatic circulation with okadaic acid in mice . Toxic. Subst. Mech. , 15 : 405 – 14 .
   Google Scholar
• Matias , W. G. , Bonini , M. and Creppy , E. E. 1996 . Inhibition of protein synthesis in a cell-free system and Vero cells by okadaic acid, a diarrhetic shellfish toxin . J. Toxicol. Environ. Health , 48 : 309 – 17 .
   PubMed Web of Science ®Google Scholar
• Morimoto , Y. , Ohba , T. , Kobayashi , S. and Haneji , T. 1997 . The protein phosphatase inhibitors okadaic acid and calyculin A induce apoptosis in human osteoblastic cells . Exp. Cell Res. , 230 : 181 – 86 .
   PubMed Web of Science ®Google Scholar
• Nakagama , H. , Kaneko , S. , Shima , H. , Inamori , H. , Fukuda , H. , Kominami , R. , Sugimura , T. and Nagao , M. 1997 . Induction of minisatellite mutation in NIH 3T3 cells by treatment with the tumor promoter okadaic acid . Proc. Natl. Acad. Sci. USA , 94 : 10813 – 16 .
   PubMed Web of Science ®Google Scholar
• Nüsse , M. , Beisker , W. , Kramer , J. , Miller , B. M. , Schreiber , G. A. , Viaggi , S. , Weller , E. M. and Wessels , J. M. 1994 . Measurement of micronuclei by flow cytometry . Methods Cell Biol. , 42 : 149 – 58 .
   PubMed Web of Science ®Google Scholar
• Nüsse , M. and Marx , K. 1997 . Flow cytometric analysis of micronuclei in cell cultures and human lymphocytes: Advantages and disadvantages . Mutat. Res. , 392 : 109 – 15 .
   PubMed Web of Science ®Google Scholar
• Nuydens , R. , de Jong , M. , Van Den Kieboom , G. , Heers , C. , Dispersyn , G. , Cornelissen , F. , Nuyens , R. , Borgers , M. and Geerts , H. 1998 . Okadaic acid-induced apoptosis in neuronal cells: Evidence for an abortive mitotic attempt . J. Neurochem. , 70 : 1124 – 33 .
   PubMed Web of Science ®Google Scholar
• Pérez Machado , G. , González Borroto , J.I. , Castañedo , N. , Creus , A. and Marcos , R. 2004 . In vitro genotoxicity testing of the furylethylene derivative UC-245 in human cells . Mutagenesis , 19 : 75 – 80 .
   PubMed Web of Science ®Google Scholar
• Pilch , D. R. , Sedelnikova , O. A. , Redon , C. , Celeste , A. , Nussenzweig , A. and Bonner , W. M. 2003 . Characteristics of gamma-H2AX foci at DNA double-strand breaks sites . Biochem. Cell Biol. , 81 : 123 – 29 .
   PubMed Web of Science ®Google Scholar
• Redon , C. , Pilch , D. R. and Bonner , W. M. 2006 . Genetic analysis of Saccharomyces cerevisiae H2A serine 129 mutant suggests a functional relationship between H2A and the sister-chromatid cohesion partners Csm3–Tof1 for the repair of topoisomerase I-induced DNA damage . Genetics , 172 : 67 – 76 .
   PubMed Web of Science ®Google Scholar
• Rogakou , E. P. , Pilch , D. R. , Orr , A. H. , Ivanova , V. S. and Bonner , W. M. 1998 . DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139 . J. Biol. Chem. , 273 : 5858 – 68 .
   PubMed Web of Science ®Google Scholar
• Rogers , C. G. , Héroux-Metcalf , C. and Langlois , I. 1994 . Evaluation of cytotoxicity and genotoxicity of okadaic acid, a non-phorbol ester type tumour promoter, in V79 Chinese hamster lung cells . Toxicol. In Vitro. , 8 : 269 – 76 .
   PubMed Web of Science ®Google Scholar
• Roman , D. , Locher , F. , Suter , W. , Cordier , A. and Bobadilla , M. 1998 . Evaluation of a new procedure for the flow cytometric analysis of in vitro, chemically induced micronuclei in V79 cells . Environ. Mol. Mutagen. , 32 : 387 – 96 .
   PubMed Web of Science ®Google Scholar
• Rouse , J. and Jackson , S. P. 2002 . Interfaces between the detection, signaling, and repair of DNA damage . Science , 297 : 547 – 51 .
   PubMed Web of Science ®Google Scholar
• Sakai , A. and Fujiki , H. 1991 . Promotion of BALB/3T3 cell transformation by the okadaic acid class of tumor promoters, okadaic acid and dinophysistoxin-1 . Jpn. J. Cancer Res. , 82 : 518 – 23 .
   PubMedGoogle Scholar
• Schuler , M. , Rupa , D. S. and Eastmond , D. A. 1997 . A critical evaluation of centromeric labeling to distinguish micronuclei induced by chromosomal loss and breakage in vitro . Mutat. Res. , 392 : 81 – 95 .
   PubMed Web of Science ®Google Scholar
• Souid-Mensi , G. , Moukha , S. , Mobio , T.A. , Maaroufi , K. and Creppy , E. E. 2008 . The cytotoxicity and genotoxicity of okadaic acid are cell-line dependent . Toxicon , 51 : 1338 – 44 .
   PubMed Web of Science ®Google Scholar
• Suganuma , M. , Fujiki , H. , Suguiri , H. , Yoshizwa , S. , Hirota , M. , Nakayasu , M. , Ojika , M. , Wakamatsu , K. , Yamada , K. and Sugimura , T. 1988 . Okadaic acid, an additional non-phorbol-12-tetradecanoate-13-acetate type tumor promoter . Proc. Natl. Acad. Sci. USA , 85 : 1768 – 71 .
   PubMed Web of Science ®Google Scholar
• Tanaka , T. , Halicka , D. , Traganos , F. and Darzynkiewicz , Z. 2009 . Cytometric analysis of DNA damage, phosphorylation of histone H2AX as a marker of DNA double-strand breaks (DSBs) . Methods Mol. Biol , 523 : 161 – 68 .
   PubMedGoogle Scholar
• Traoré , A. , Baudrimont , I. , Ambaliou , S. , Dano , S. D. and Creppy , E. E. 2001 . DNA breaks and cell cycle arrest induced by okadaic acid in Caco-2 cells, a human colonic epithelial cell line . Arch. Toxicol , 75 : 110 – 17 .
   PubMed Web of Science ®Google Scholar
• Valdiglesias , V. , Méndez , J. , Pásaro , E. , Cemeli , E. , Anderson , D. and Laffon , B. 2010 . Assessment of okadaic acid effects on cytotoxicity, DNA damage and DNA repair in human cells . Mutat. Res , 689 : 74 – 79 .
   PubMed Web of Science ®Google Scholar
• Valdiglesias , V. , Méndez , J. , Pásaro , E. , Cemeli , E. , Anderson , D. and Laffon , B. 2011a . Induction of oxidative DNA damage by the marine toxin okadaic acid depends on human cell type . Toxicon , 57 : 882 – 888 .
   PubMed Web of Science ®Google Scholar
• Valdiglesias , V. , Laffon , B. , Pásaro , E. and Méndez , J. 2011b . Okadaic acid induces morphological changes, apoptosis and cell cycle alterations in different human cell types . J. Environ. Monit , DOI:10.1039/C0EM00771D
   PubMedGoogle Scholar
• Vale , C. and Botana , L. M. 2008 . Marine toxins and the cytoskeleton, okadaic acid and dinophysistoxins . FEBS J. , 275 : 6060 – 66 .
   PubMed Web of Science ®Google Scholar
• Van Dolah , F. M. and Ramsdell , J. S. 1992 . Okadaic acid inhibits a protein phosphatase activity involved in formation of the mitotic spindle of GH4 rat pituitary cells . J. Cell Physiol , 152 : 190 – 98 .
   PubMed Web of Science ®Google Scholar
• Viaggi , S. , Braselmann , H. and Nüsse , M. 1995 . Flow cytometric analysis of micronuclei in the CD2+/- subpopulation of human lymphocytes enriched by magnetic separation . Int. J. Radiat. Biol , 67 : 193 – 202 .
   PubMed Web of Science ®Google Scholar
• Yasumoto , T. , Oshima , Y. and Yamaguchi , M. 1978 . Occurrence of a new type of shellfish poisoning in the Tohoku District . Nippon Suisan Gakkaishi , 44 : 1249 – 55 .
   Google Scholar
• Zhou , B. B. and Elledge , S. J. 2000 . The DNA damage response: Putting checkpoints in perspective . Nature , 408 : 433 – 39 .
   PubMed Web of Science ®Google Scholar