431
Views
1
CrossRef citations to date
0
Altmetric
Review Articles

Cyanotoxin genotoxicity: a review

, , , , &
Pages 699-712 | Received 30 Jan 2021, Accepted 24 Apr 2021, Published online: 10 May 2021

References

  • Abbas, T., et al., 2020. Recent advancements in the removal of cyanotoxins from water using conventional and modified adsorbents—a contemporary review. Water, 12 (10), 2756.
  • Antoniou, M.G., et al., 2005. Cyanotoxins: new generation of water contaminants. Journal of environmental engineering, 131 (9), 1239–1243.
  • Bazin, E., et al., 2010. Genotoxicity of a freshwater cyanotoxin, cylindrospermopsin, in two human cell lines: Caco‐2 and HepaRG. Environmental and molecular mutagenesis, 51 (3), 251–259.
  • Bazin, E., et al., 2012. Cytotoxic and genotoxic effects of cylindrospermopsin in mice treated by gavage or intraperitoneal injection. Environmental toxicology, 27 (5), 277–284.
  • Boopathi, T., and Ki, J.S., 2014. Impact of environmental factors on the regulation of cyanotoxin production. Toxins, 6 (7), 1951–1978.
  • Bouaïcha, N., and Maatouk, I., 2004. Microcystin-LR and nodularin induce intracellular glutathione alteration, reactive oxygene species production and lipid peroxidation in primary cultured rat hepatocytes. Toxicology letters, 148 (5), 3–63.
  • Bouaïcha, N., et al., 2005. Genotoxic potential of microcystin‐LR and nodularin in vitro in primary cultured rat hepatocytes and in vivo in rat liver. Environmental toxicology: an international journal, 20 (3), 341–347.
  • Bouaïcha, N., et al., 2019. Structural diversity, characterization and toxicology of microcystins. Toxins, 11 (12), 714.
  • Carmichael, W.W., et al., 2001. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental health perspectives, 109 (7), 663–668.
  • Chen, T., et al., 2005a. Effects of microcystin‐LR on patterns of iNOS and cytokine mRNA expression in macrophages in vitro. Environmental toxicology: an international journal, 20 (1), 85–91.
  • Chen, T., et al., 2005b. Induction of apoptosis in mouse liver by microcystin-LR: a combined transcriptomic, proteomic, and simulation strategy. Molecular cellular proteomics, 4 (7), 958–974.
  • Chen, L., et al., 2019. Regulation of microcystin-LR-induced DNA damage by miR-451a in HL7702 cells. Toxins, 11 (3), 164.
  • Chorus, I., and Bartram, M., 2021. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Bury St Edmunds: St Edmundsbury Press.
  • Cirés, S., et al., 2017. Toxicity at the edge of life: a review on cyanobacterial toxins from extreme environments. Marine drugs, 15 (7), 233.
  • De La Cruz, A.A., et al., 2013. A review on cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environmental science: processes & impacts, 15 (11), 1979–2003.
  • De La Cruz, A. A., et al., 2020., Introduction to cyanobacteria and cyanotoxins. In: M. Antoniou, ed. Water treatment for purification from cyanobacteria and cyanotoxins. Hoboken, NJ: John Wiley & Sons, 1–35.
  • Dias, E., et al., 2014. Genotoxicity of microcystin-LR in in vitro and in vivo experimental models. BioMed research international, 2014, 949521.
  • Díez-Quijada, L., et al., 2019a. In vitro mutagenic and genotoxic assessment of a mixture of the cyanotoxins microcystin-lr and cylindrospermopsin. Toxins, 11 (6), 318.
  • Díez-Quijada, L., et al., 2019b. In vivo genotoxicity evaluation of cylindrospermopsin in rats using a combined micronucleus and comet assay. Food and chemical toxicology, 132, 110664.
  • Diez-Quijada Jiménez, L., et al., 2020. A new method for the simultaneous determination of cyanotoxins (Microcystins and Cylindrospermopsin) in mussels using SPE-UPLC-MS/MS. Environmental research, 185, 109284.
  • Díez-Quijada, L., et al., 2020a. Cylindrospermopsin-microcystin-LR combinations may induce genotoxic and histopathological damage in rats. Toxins, 12 (6), 348.
  • Díez-Quijada, L., et al., 2020b. Genotoxic effects of cylindrospermopsin, microcystin-lr and their binary mixture in human hepatocellular carcinoma (HepG2) cell line. Toxins, 12 (12), 778.
  • Dong, L., et al., 2008. Study on DNA-protein crosslinks of certain organs of mice induced by microcystin-LR. Wei sheng yan jiu = Journal of hygiene research, 37 (2), 144–146.
  • Fawell, J.K., et al., 1999. The toxicity of cyanobacterial toxins in the mouse: II anatoxin-a. Human experimental toxicology, 18 (3), 168–173.
  • Feng, N., et al., 2016. Pathway for biodegrading nodularin (NOD) by Sphingopyxis sp. USTB-05. Toxins, 8 (5), 116.
  • Feng, N., et al., 2020. MicroRNA-16 participates in the cell cycle alteration of HepG2 cells induced by MC-LR. Ecotoxicology and environmental safety, 192, 110295.
  • Fessard, V., and Bernard, C., 2003. Cell alterations but no DNA strand breaks induced in vitro by cylindrospermopsin in CHO K1 cells. Environmental toxicology: an international journal, 18 (5), 353–359.
  • Fonseca, A.L., et al., 2014. In vivo genotoxicity of treated water containing the cylindrospermopsin-producer Cylindrospermopsis raciborskii. Journal of water and health, 12 (3), 474–483.
  • Gaudin, J., et al., 2008. In vivo DNA damage induced by the cyanotoxin microcystin-LR: comparison of intra-peritoneal and oral administrations by use of the comet assay. Mutation research/genetic toxicology and environmental mutagenesis, 652 (1), 65–71.
  • Gaudin, J., et al., 2009. In vivo genotoxic potential of microcystin‐LR: A cyanobacterial toxin, investigated both by the unscheduled DNA synthesis (UDS) and the comet assays after intravenous administration. Environmental toxicology: an international journal, 24 (2), 200–209.
  • Gutiérrez-Praena, D., et al., 2019. Cytotoxic and morphological effects of microcystin‐LR, cylindrospermopsin, and their combinations on the human hepatic cell line HepG2. Environmental toxicology, 34 (3), 240–251.
  • Guzmán-Guillén, R., et al., 2013. Cyanobacterium producing cylindrospermopsin cause oxidative stress at environmentally relevant concentrations in sub-chronically exposed tilapia (Oreochromis niloticus). Chemosphere, 90 (3), 1184–1194.
  • Hercog, K., et al., 2017. Genotoxic potential of the binary mixture of cyanotoxins microcystin-LR and cylindrospermopsin. Chemosphere, 189, 319–329.
  • Hercog, K., et al., 2020. Application of advanced HepG2 3D cell model for studying genotoxic activity of cyanobacterial toxin cylindrospermopsin. Environmental pollution, 265, 114965.
  • Herrera, N., et al., 2018. Genotoxicity and cytotoxicity of three microcystin-LR containing cyanobacterial samples from Antioquia, Colombia. Toxicon, 154, 50–59.
  • Huang, P. and Xu, A., 2009. Genotoxic effects of microcystin-LR in mammalian cells. 2009 3rd International Conference on Bioinformatics and Biomedical Engineering, Beijing, China, 1–3.
  • Humpage, A.R., et al., 2005. Cylindrospermopsin genotoxicity and cytotoxicity: role of cytochrome P-450 and oxidative stress. Journal of toxicology and environmental health, part A, 68 (9), 739–753.
  • Humpage, A.R., et al., 2000. Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin. Mutation research/genetic toxicology and environmental mutagenesis, 472 (1–2), 155–161.
  • IARC. 2010. Working Group on the Evaluation of Carcinogenic Risks to Humans, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Ingested Nitrate and Nitrite, and Cyanobacterial Peptide Toxins. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. World Health Organization, International Agency for Research on Cancer. https://doi.org/http://dx.doi.org/10.1002/food.19940380335.
  • Khadairi, M.M., et al., 2017. The biochemical alteration and DNA damage in rats (Rattus rattus) after chronic intraperitoneally injection to purified microcystin-LR from Anabaena circinalis. Asian journal of pharmaceutical and clinical research, 10 (11), 277–283.
  • Kumar, P., et al., 2018. Physico-chemical treatment for the degradation of cyanotoxins with emphasis on drinking water treatment—how far have we come? Journal of environmental chemical engineering, 6 (4), 5369–5388.
  • Lankoff, A., et al., 2002. Protective effect of melatonin against nodularin-induced oxidative stress. Archives of toxicology., 76, 158–165.
  • Lankoff, A., et al., 2004. DNA damage and repair in human peripheral blood lymphocytes following treatment with microcystin-LR. Mutation research/genetic toxicology and environmental mutagenesis, 559 (1–2), 131–142.
  • Lankoff, A., et al., 2006a. Inhibition of nucleotide excision repair (NER) by microcystin-LR in CHO-K1 cells. Toxicon, 48 (8), 957–965.
  • Lankoff, A., et al., 2006b. Nodularin-induced genotoxicity following oxidative DNA damage and aneuploidy in HepG2 cells. Toxicology letters, 164 (3), 239–248.
  • Lankoff, A., et al., 2006c. The repair of gamma-radiation-induced DNA damage is inhibited by microcystin-LR, the PP1 and PP2A phosphatase inhibitor. Mutagenesis, 21 (1), 83–90.
  • Lankoff, A., et al., 2007. No induction of structural chromosomal aberrations in cylindrospermopsin-treated CHO-K1 cells without and with metabolic activation. Toxicon, 50 (8), 1105–1115.
  • Lankoff, A., et al., 2008. Nucleotide excision repair impairment by nodularin in CHO cell lines due to ERCC1/XPF inactivation. Toxicology letters, 179 (2), 101–107.
  • Liu, C., et al., 2020. Toxicity of chlorinated algal-impacted waters: formation of disinfection byproducts vs. reduction of cyanotoxins. Water research, 184, 116145.
  • Liu, W., et al., 2018. Microcystin-LR increases genotoxicity induced by aflatoxin B1 through oxidative stress and DNA base excision repair genes in human hepatic cell lines. Environmental pollution, 233, 455–463.
  • Lone, Y., et al., 2015. An overview of the toxic effect of potential human carcinogen Microcystin-LR on testis. Toxicology reports, 2, 289–296.
  • Maatouk, I., et al., 2004. Detection by 32P-postlabelling of 8-oxo-7, 8-dihydro-2′-deoxyguanosine in DNA as biomarker of microcystin-LR-and nodularin-induced DNA damage in vitro in primary cultured rat hepatocytes and in vivo in rat liver. Mutation research/genetic toxicology and environmental mutagenesis, 564 (1), 9–20.
  • McLellan, N.L., and Manderville, R.A., 2017. Toxic mechanisms of microcystins in mammals. Toxicology research, 6 (4), 391–405.
  • Merel, S., et al., 2013. State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environment international, 59, 303–327.
  • Miao, C., et al., 2016. Microcystin‐LR promotes migration and invasion of colorectal cancer through matrix metalloproteinase‐13 up‐regulation. Molecular carcinogenesis, 55 (5), 514–524.
  • Munoz, M., et al., 2019. Degradation of widespread cyanotoxins with high impact in drinking water (microcystins, cylindrospermopsin, anatoxin-a and saxitoxin) by CWPO. Water research, 163, 114853.
  • Nong, Q., et al., 2007. Involvement of reactive oxygen species in Microcystin-LR-induced cytogenotoxicity. Free radical research, 41 (12), 1326–1337.
  • Obaidat, A., et al., 2012. The expression and function of organic anion transporting polypeptides in normal tissues and in cancer. Annual review of pharmacology and toxicology, 52, 135–151.
  • Ohtani, I., et al., 1992. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. Journal of the American chemical society, 114 (20), 7941–7942.
  • Osswald, J., et al., 2007. Vasconcelos, Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria, anatoxin-a. Environment international, 33 (8), 1070–1089.
  • Palinska, K.A., and Surosz, W., 2014. Taxonomy of cyanobacteria: a contribution to consensus approach. Hydrobiologia, 740 (1), 1–11.
  • Puerto, M., et al., 2018. Mutagenic and genotoxic potential of pure Cylindrospermopsin by a battery of in vitro tests. Food and chemical toxicology, 121, 413–422.
  • Pulz, O., and Gross, W., 2004. Valuable products from biotechnology of microalgae. Applied microbiology and biotechnology, 65 (6), 635–648.
  • Rao, P.L., and Bhattacharya, R., 1996. The cyanobacterial toxin microcystin-LR induced DNA damage in mouse liver in vivo. Toxicology, 114 (1), 29–36.
  • Rao, P.L., et al., 1998. Freshwater cyanobacterium Microcystis aeruginosa (UTEX 2385) induced DNA damage in vivo and in vitro. Environmental toxicology and pharmacology, 5 (1), 1–6.
  • Rao, P.L., et al., 2002. Involvement of caspase and reactive oxygen species in cyanobacterial toxin anatoxin-a-induced cytotoxicity and apoptosis in rat thymocytes and Vero cells. Archives of toxicology, 76 (4), 227–235.
  • Ren, Y., et al., 2019. Microcystin-LR promotes migration via the cooperation between microRNA-221/PTEN and STAT3 signal pathway in colon cancer cell line DLD-1. Ecotoxicology and environmental safety, 167, 107–113.
  • Rücker, J., et al., 2007. Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon, 50 (6), 800–809.
  • Shen, X., et al., 2002. Genotoxicity investigation of a cyanobacterial toxin Cylindrospermopsin. Toxicon, 40 (10), 1499–1501.
  • Shen, X., et al., 2004. Genotoxicity investigation of chlorinated degradation products of a cyanobacterial toxin, Cylindrospermopsin. Xth International Conference on Harmful Algae, St. Pete Beach, Florida, USA, 21–25 October 2002, 133–135.
  • Sierosławska, A., and Rymuszka, A., 2010. Evaluation of genotoxic potential of neurotoxin anatoxin-a with the use of umuC test. Neuroendocrinology letters, 31 (2), 16.
  • Sierosławska, A., and Rymuszka, A., 2013. Assessment of the potential genotoxic and proapoptotic impact of selected cyanotoxins on fish leukocytes. Central European journal of immunology, 2, 190–195.
  • Sierosławska, A., and Rymuszka, A., 2015. Cylindrospermopsin induces oxidative stress and genotoxic effects in the fish CLC cell line. Journal of applied toxicology, 35 (4), 426–433.
  • Singh, J.S., 2016. Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Frontiers in microbiology, 7, 529.
  • Sinha, R.P., and Häder, D.P., 2008. UV-protectants in cyanobacteria. Plant science, 174 (3), 278–289.
  • Sotton, B., et al., 2012. Short-term uptake of microcystin-LR by Coregonus lavaretus: GST activity and genotoxicity. Ecotoxicology, 21 (7), 1788–1796.
  • Štraser, A., et al., 2013. The influence of cylindrospermopsin on oxidative DNA damage and apoptosis induction in HepG2 cells. Chemosphere, 92 (1), 24–30.
  • Sueoka, E., et al., 1997. Expression of the tumor necrosis factorα gene and early response genes by nodularin, a liver tumor promoter, in primary cultured rat hepatocytes. Journal of cancer research and clinical oncology, 123 (8), 413–419.
  • Teneva, I., et al., 2005. Cytotoxicity and apoptotic effects of microcystin-LR and anatoxin-a in mouse lymphocytes. Folia biologica-praha, 51 (3), 62.
  • Tsuji, K., et al., 1997. Stability of microcystins from cyanobacteria—IV. Effect of chlorination on decomposition. Toxicon, 35 (7), 1033–1041.
  • Ueno, Y., et al., 1996. Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis, 17 (6), 1317–1321.
  • Valério, E., et al., 2010. Diversity and impact of prokaryotic toxins on aquatic environments: a review. Toxins, 2 (10), 2359–2410.
  • Wang, L., et al., 2020b. Low-dose microcystin-LR antagonizes aflatoxin B1 induced hepatocarcinogenesis through decreasing cytochrome P450 1A2 expression and aflatoxin B1-DNA adduct generation. Chemosphere, 248, 126036.
  • Wang, X., et al., 2015. Role of nitric oxide in the genotoxic response to chronic microcystin-LR exposure in human–hamster hybrid cells. Journal of environmental sciences, 29, 210–218.
  • Wang, X., et al., 2020a. Genotoxicity of microcystin-LR in mammalian cells: implication from peroxynitrite produced by mitochondria. Ecotoxicology and environmental safety, 195, 110408.
  • Wen, C., et al., 2019. Effects of microcystins-LR on genotoxic responses in human intestinal epithelial cells (NCM460). Journal of toxicology and environmental health, part A, 82 (21), 1113–1119.
  • WHO. 2017. Guidelines for drinking‑water quality fourth edition incorporating the first addendum. https://www.who.int/publications/i/item/9789241549950.
  • WHO. 2020a. Cyanobacterial toxins: cylindrospermopsins Background document for development of WHO Guidelines for drinking-water quality and Guidelines for safe recreational water environments. https://apps.who.int/iris/bitstream/handle/10665/338063/WHO-HEP-ECH-WSH-2020.4-eng.pdf?sequence=1&isAllowed=y
  • WHO. 2020b. Cyanobacterial toxins: anatoxin-a and analogues (No. WHO/HEP/ECH/WSH/2020.1). World Health Organization. Licence: CC BY-NC-SA 3.0 IGO. https://apps.who.int/iris/bitstream/handle/10665/338060/WHO-HEP-ECH-WSH-2020.1-eng.pdf?sequence=1&isAllowed=y
  • Yang, Y., et al., 2021. Four decades of progress in cylindrospermopsin research: the ins and outs of a potent cyanotoxin. Journal of hazardous materials, 406, 124653.
  • Yu, S.Z., 1995. Primary prevention of hepatocellular carcinoma. Journal of gastroenterology and hepatology, 10 (6), 674–682.
  • Žegura, B., et al., 2003. Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon, 41 (1), 41–48.
  • Žegura, B., 2004. The role of reactive oxygen species in microcystin-LR-induced DNA damage. Toxicology, 200 (1), 59–68.
  • Žegura, B., et al., 2006. Alteration of intracellular GSH levels and its role in microcystin-LR-induced DNA damage in human hepatoma HepG2 cells. Mutation research/genetic toxicology and environmental mutagenesis, 611 (1–2), 25–33.
  • Žegura, B., et al., 2008a. Different sensitivities of human colon adenocarcinoma (CaCo-2), astrocytoma (IPDDC-A2) and lymphoblastoid (NCNC) cell lines to microcystin-LR induced reactive oxygen species and DNA damage. Toxicon, 52 (3), 518–525.
  • Žegura, B., et al., 2008b. Patterns of microcystin-LR induced alteration of the expression of genes involved in response to DNA damage and apoptosis. Toxicon, 51 (4), 615–623.
  • Žegura, B., et al., 2011a. Cylindrospermopsin induced DNA damage and alteration in the expression of genes involved in the response to DNA damage, apoptosis and oxidative stress. Toxicon, 58 (6–7), 471–479.
  • Žegura, B., et al., 2011b. Genotoxicity and potential carcinogenicity of cyanobacterial toxins–a review. Mutation research/reviews in mutation research, 727 (1–2), 16–41.
  • Žegura, B., et al., 2011c. Microcystin-LR induced DNA damage in human peripheral blood lymphocytes. Mutation research/genetic toxicology and environmental mutagenesis, 726 (2), 116–122.
  • Žegura, B., 2016. An overview of the mechanisms of microcystin-LR genotoxicity and potential carcinogenicity. Mini reviews in medicinal chemistry, 16 (13), 1042–1062.
  • Zhan, L., et al., 2004. Genotoxicity of microcystin-LR in human lymphoblastoid TK6 cells. Mutation research/genetic toxicology and environmental mutagenesis, 557 (1), 1–6.
  • Zhang, Z., et al., 2012. Effects of microcystin-LR exposure on matrix metalloproteinase-2/-9 expression and cancer cell migration. Ecotoxicology and environmental safety, 77, 88–93.
  • Zhou, L., et al., 2002. Relationship between microcystin in drinking water and colorectal cancer. Biomedical and environmental sciences, 15 (2), 166–171.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.