Abstract
Arsenic (As) is one of the most relevant environmental global single substance toxicants that have long been regarded as a carcinogenic and genotoxic potential. In this respect, we evaluated the cytogenetic effect of arsenic exposure in Nile tilapia (Oreochromis niloticus), in terms of erythrocyte alteration, apoptosis, and induction of micronuclei. Spirulina platensis (SP) is a filamentous cyanobacterium microalgae with potent dietary phytoantioxidant, anti-inflammatory, and anti-cancerous properties supplementation. The protective role of Spirulina as supplementary feeds was studied in Nile tilapia (O. niloticus) against arsenic-induced cytogenotoxicity. Four groups were assigned as control group (no SP or As), As group (exposed to water-born As in the form of NaAsO2 at 7 ppm), SP1 (SP at 7.5 % + As at the same level of exposure), and SP2 (SP at 10 % + As at the same level of exposure). As-treated group had a significant increase in all cytogenetic analyses including erythrocyte alteration, apoptosis, and induction of micronuclei after 2 weeks with continuous increase in response after 3 weeks. The combined treatment of Spirulina at two different concentrations of 7.5 and 10 % had significantly declined the induction of erythrocyte alteration, apoptosis, and micronuclei formation induced by arsenic intoxication.
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Ahmad, S., Kitchin, K. T., & Cullen, W. R. (2000). Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Archives of Biochemistry and Biophysics, 382, 195–202.
Ahmed, K., Akhand, A. A., Hasan, M., Islam, M., & Hasan, A. (2008). Toxicity of arsenic (sodium arsenite) to fresh water spotted snakehead Channa punctatus (Bloch) on cellular death and DNA content. American Eurasian Journal of Agricultural and Environmental Science, 4, 18–22.
Ahmed, M. K., Habibullah-Al-Mamun, M., Hossain, M. A., Arif, M., Parvin, E., Akter, M. S., Khan, M. S., & Islam, M. M. (2011). Assessing the genotoxic potentials of arsenic in tilapia (Oreochromis mossambicus) using alkaline comet assay and micronucleus test. Chemosphere, 84, 143–149.
Akter, M., Ahmed, M., Akhand, A., Ahsan, N., Islam, M., & Khan, M. (2009). Arsenic and mercury induce death of Anabas testudineus (Bloch) involving fragmentation of chromosomal DNA. Terrestrial and Aquatic Environmental Toxicology, 3, 42–47.
Al-Sabti, K., & Metcalfe, C. D. (1995). Fish micronuclei for assessing genotoxicity in water. Mutation Research, Genetic Toxicology, 343, 121–135.
Ayllon, F., & Garcia-Vazquez, E. (2000). Induction of micronuclei and other nuclear abnormalities in European minnow (Phoxinus phoxinus) and mollie (Poecilia latipinna): an assessment of the fish micronucleus test. Mutation Research, Genetic Toxicology and Environmental Mutagenesis, 467, 177–186.
Barbosa, J., Cabral, T., Ferreira, D., Agnez-Lima, L., & Batistuzzo de Medeiros, S. (2010). Genotoxicity assessment in aquatic environment impacted by the presence of heavy metals. Ecotoxicology and Environmental Safety, 73, 320–325.
Bolognesi, C., Perrone, E., Roggieri, P., Pampanin, D. M., & Sciutto, A. (2006). Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquatic Toxicology, 78, S93–S98.
Cantrell, S. M., Joy-Schlezinger, J., Stegeman, J. J., Tillitt, D. E., & Hannink, M. (1998). Correlation of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin-induced apoptotic cell death in the embryonic vasculature with embryotoxicity. Toxicology and Applied Pharmacology, 148, 24–34.
Chen, Q. M., Bartholomew, J. C., Campisi, J., Acosta, M., Reagan, J. D., & Ames, B. N. (1998). Molecular analysis of H2O2-induced senescent-like growth arrest in normal human fibroblasts: p53 and Rb control G1 arrest but not cell replication. Biochemistry Journal, 332, 43–50.
Darzynkiewicz, Z. (1990). Differential staining of DNA and RNA in intact cells and isolated cell nuclei with acridine orange. Methods in Cell Biology, 33, 285–298.
Datta, S., Saha, D. R., Ghosh, D., Majumdar, T., Bhattacharya, S., & Mazumder, S. (2007). Sub-lethal concentration of arsenic interferes with the proliferation of hepatocytes and induces in vivo apoptosis in (Clarias batrachus) L. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 145, 339–349.
Deng, R., & Chow, T. J. (2010). Hypolipidemic, antioxidant, and antiinflammatory activities of microalgae Spirulina. Cardiovascular Therapeutics, 28, e33–e45.
Dural, M., Göksu, M., & Özak, A. A. (2007). Investigation of heavy metal levels in economically important fish species captured from the Tuzla lagoon. Food Chemistry, 102, 415–421.
Frechet, M., Canitrot, Y., Cazaux, C., & Hoffmann, J. S. (2001). DNA polymerase beta imbalance increases apoptosis and mutagenesis induced by oxidative stress. FEBS Letters, 505, 229–232.
Galindo, T. P., & Moreira, L. M. (2009). Evaluation of genotoxicity using the micronucleus assay and nuclear abnormalities in the tropical sea fish Bathygobius soporator (Valenciennes, 1837) (Teleostei, Gobiidae). Genetics and Molecular Biology, 32, 394–398.
Gebel, T. W. (2001). Genotoxicity of arsenical compounds. International Journal of Hygiene and Environmental Health, 203, 249–262.
Grisolia, C. K. (2002). A comparison between mouse and fish micronucleus test using cyclophosphamide, mitomycin C and various pesticides. Mutation Research, Genetic Toxicology and Environmental Mutagenesis, 518, 145–150.
Güroy, B., Şahin, İ., Mantoğlu, S., & Kayalı, S. (2012). Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellow tail cichlid Pseudotropheus acei. Aquaculture International, 20, 869–878.
Hei, T. K., Liu, S. X., & Waldren, C. (1998). Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proceedings of the National Academy of Sciences, 95, 8103–8107.
Hughes, M. F. (2002). Arsenic toxicity and potential mechanisms of action. Toxicology Letters, 133, 1–16.
Hwang, P., & Tsai, Y. (1993). Effects of arsenic on osmoregulation in the tilapia Oreochromis mossambicus reared in seawater. Marine Biology, 117, 551–558.
Iarmarcovai, G., Bonassi, S., Botta, A., Baan, R., & Orsiere, T. (2008). Genetic polymorphisms and micronucleus formation: a review of the literature. Mutation Research, Reviews in Mutation Research, 658, 215–233.
Ibrahem, M. D., Mohamed, M. F., & Ibrahim, M. A. (2013). The role of Spirulina platensis (Arthrospira platensis) in growth and immunity of Nile tilapia (Oreochromis niloticus) and its resistance to bacterial infection. Journal of Agricultural Science, 5, 109–117.
James, R., (2010). Effect of dietary supplementation of spirulina on growth and phosphatase activity in copper-exposed carp (Labeo rohita).
James, R., Sampath, K., Nagarajan, R., Vellaisamy, P., & Manikandan, M. M. (2009). Effect of dietary Spirulina on reduction of copper toxicity and improvement of growth, blood parameters and phosphatases activities in carp, Cirrhinus mrigala (Hamilton, 1822). Indian Journal of Experimental Biology, 47, 754.
Khan, Z., Bhadouria, P., & Bisen, P. (2005). Nutritional and therapeutic potential of Spirulina. Current Pharmaceutical Biotechnology, 6, 373–379.
Kumar, A., Kesari, V. P., & Khan, P. K. (2013). Fish micronucleus assay to assess genotoxic potential of arsenic at its guideline exposure in aquatic environment. BioMetals, 26(2), 337–346.
Lage, C. R., Nayak, A., & Kim, C. H. (2006). Arsenic ecotoxicology and innate immunity. Integrative and Comparative Biology, 46, 1040–1054.
Linjawi, S.A., (2011). Protective effect of spirulina against mitomycin C-induced genotoxic damage in male rats. Journal of American Science 7.
Lushchak, V. I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101, 13–30.
Mathew, B., Sankaranarayanan, R., Nair, P. P., Varghese, C., Somanathan, T., Amma, B. P., Amma, N. S., & Nair, M. K. (1995). Evaluation of chemoprevention of oral cancer with Spirulina fusiformis. Nutrition and Cancer, 24(2), 197–202.
Mekkawy, I. A., Mahmoud, U. M., & Sayed, A. E.-D. H. (2011). Effects of 4-nonylphenol on blood cells of the African catfish (Clarias gariepinus) (Burchell, 1822). Tissue and Cell, 43, 223–229.
Mokhtar, M. B., Aris, A. Z., Munusamy, V., & Praveena, S. M. (2009). Assessment level of heavy metals in Penaeus monodon and Oreochromis spp. in selected aquaculture ponds of high densities development area. European Journal of Scientific Research, 30, 348–360.
Nwani, C., Lakra, W., Nagpure, N., Kumar, R., Kushwaha, B., & Srivastava, S. (2010). Mutagenic and genotoxic effects of carbosulfan in freshwater fish (Channa punctatus) (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Food and Chemical Toxicology, 48, 202–208.
Pascoe, S., & Gatehouse, D. (1986). The use of a simple haematoxylin and eosin staining procedure to demonstrate micronuclei within rodent bone marrow. Mutation Resarch, 164, 237–243.
Ramírez, O. A. B., & García, F. P. (2005). Genotoxic damage in zebra fish (Danio rerio) by arsenic in waters from Zimapan, Hidalgo, Mexico. Mutagenesis, 20, 291–295.
Roy, S., & Bhattacharya, S. (2006). Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotoxicology and Environmental Safety, 65, 218–229.
Sánchez, M., Bernal-Castillo, J., Rozo, C., Rodríguez, I., (2003). Spirulina (Arthrospira): an edible microorganism: a review.
Sawhney, A., & Johal, M. (2000). Erythrocyte alterations induced by malathion in Channa punctatus (Bloch). Bulletin of Environmental Contamination and Toxicology, 64, 398–405.
Sayed, A. H., & Fawzy, M. A. (2014). Effect of dietary supplementation of Spirulina platensis on the growth and haematology of the Catfish Clarias gariepinus. Journal of Advances in Biology, 5, 625–635.
Sayed, A. H., Oda, S., & Mitani, H. (2014). Nuclear and cytoplasmic changes in erythrocytes of p53-deficient medaka fish (Oryzias latipes) after exposure to gamma-radiation. Mutation Research, Genetic Toxicology and Environmental Mutagenesis, 771, 64–70.
Schmidt, W. (1975). The micronucleus test. Mutation Research, 31, 9–15.
Seok, S.-H., Baek, M.-W., Lee, H.-Y., Kim, D.-J., Na, Y.-R., Noh, K.-J., Park, S.-H., Lee, H.-K., Lee, B.-H., & Ryu, D.-Y. (2007). Arsenite-induced apoptosis is prevented by antioxidants in zebrafish liver cell line. Toxicology in Vitro, 21, 870–877.
Sharma, K., Upreti, N., Sharma, S., & Sharma, S. (2012). Protective effect of Spirulina and tamarind fruit pulp diet supplement in fish (Gambusia affinis Baird & Girard) exposed to sublethal concentration of fluoride, aluminum and aluminum fluoride. Indian Journal of Experimental Biology, 50(12), 897–903.
Vuyyuri, S. B., Ishaq, M., Kuppala, D., Grover, P., & Ahuja, Y. (2006). Evaluation of micronucleus frequencies and DNA damage in glass workers exposed to arsenic. Environmental and Molecular Mutagenesis, 47, 562–570.
Wang, Y.-C., Chaung, R.-H., & Tung, L.-C. (2004). Comparison of the cytotoxicity induced by different exposure to sodium arsenite in two fish cell lines. Aquatic Toxicology, 69, 67–79.
Yadav, K. K., & Trivedi, S. P. (2009). Sublethal exposure of heavy metals induces micronuclei in fish, (Channa punctata). Chemosphere, 77, 1495–1500.
Zhang, T., Wang, S., Hong, L., Wang, X., & Qi, Q. (2003). Arsenic trioxide induces apoptosis of rat hepatocellular carcinoma cells in vivo. Journal of Experimental & Clinical Cancer Research, 22, 61–68.
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All experiments were carried out in accordance with the Egyptian laws and University guidelines for the care of experimental animals. The protocol for this work was described in compliance with the guidelines of the ethical committee of Assiut University and Mansoura University.
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Sayed, A.ED.H., Elbaghdady, H.A.M. & Zahran, E. Arsenic-induced genotoxicity in Nile tilapia (Orechromis niloticus); the role of Spirulina platensis extract. Environ Monit Assess 187, 751 (2015). https://doi.org/10.1007/s10661-015-4983-7
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DOI: https://doi.org/10.1007/s10661-015-4983-7