Research Article
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Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells

Year 2022, Volume: 5 Issue: 2, 117 - 128, 01.04.2022

Seda Kuşoğlu Gültekin , Elif Mertoğlu Kamalı , Kaan Yılancıoğlu , Nazlı Arda

https://doi.org/10.3153/AR22011

Abstract

Microcystis aeruginosa, which spreads in five continents in the world and reported in drinking water resources in 257 countries, is a dangerous microalgae for human and animal health due to its toxins. The aim of current study was to evaluate the effects of M. aeruginosa extract and its chromatographically separated fractions on human endothelial cells. In this context, crude extract was prepared from M. aeruginosa cultured in BG-11 medium, and it was fractionated by an optimized HPLC method. Algae extract and its six fractions were then analyzed for their cytotoxic effects on ECV304 using MTT assay. The results revealed that algae extract inhibited ECV304 cells by around 72%, a higher percentage than all fractions. The most toxic fraction was the first fraction, which inhibited the cells by 55%. Other fractions, except the third one, were also toxic with 35-40% inhibition percentages. Third fraction and certain doses of some fractions showed proliferative activity on ECV304 cells. These results showed that the activities of the total extract and its fractions in promoting or inhibiting cell proliferation varied depending on not only the content but also the treatment dose.

Keywords

Microcystis aeruginosa Human endothelial cells ECV304 Cytotoxicity Cell proliferation Algae

Supporting Institution

This study was supported by the Istanbul University Research Foundation, Turkey

Project Number

FYL-2016-21655

Thanks

We would like to thank Prof. Dr. Reyhan Akçaalan Albay for her supply of cyanobacteria and Associate Prof. Dr. Belkıs Atasever Arslan for her supply of ECV304 cell line.

References

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Year 2022, Volume: 5 Issue: 2, 117 - 128, 01.04.2022

Seda Kuşoğlu Gültekin , Elif Mertoğlu Kamalı , Kaan Yılancıoğlu , Nazlı Arda

https://doi.org/10.3153/AR22011

Abstract

Project Number

FYL-2016-21655

References

  • Abdel-Rahman, G., Sultan, Y.Y., Hassoub, M.A., Marrez, D.A. (2020). Cytotoxicity and antibacterial activity of the blue green alga Microcystis aeruginosa extracts against human cancer cell lines and foodborne bacteria. Egyptian Journal of Chemistry, 63(10), 4095-4105. https://doi.org/10.21608/EJCHEM.2020.42714.2862
  • Alverca, E., Andrade, M., Dias, E., Bento, F.S., Batoreu, M.C.C., Jordan, P., Silva, M.J., Pereiraa, P. (2009). Morphological and ultrastructural effects of microcystin-LR from Microcystis aeruginosa extract on a kidney cell line. Toxicon, 54(3), 283-294. https://doi.org/10.1016/j.toxicon.2009.04.014
  • Atasever-Arslan, B., Yilancioglu, K., Kalkan, Z., Timucin, A.C., Gür, H., Isik, F.B., Deniz, E., Erman, B., Cetiner, S. (2016). Screening of new antileukemic agents from essential oils of algae extracts and computational modeling of their interactions with intracellular signaling nodes. European Journal of Pharmaceutical Sciences, 83, 120-131. https://doi.org/10.1016/j.ejps.2015.12.001
  • Babica, P., Kohoutek, J., Bláha, L., Adamovský, O., Maršálek B. (2006). Evaluation of extraction approaches linked to ELISA and HPLC for analyses of microcystin-LR, -RR and -YR in freshwater sediments with different organic material contents. Analytical and Bioanalytical Chemistry, 385, 1545-1551. https://doi.org/10.1007/s00216-006-0545-8
  • Bagu, J.R., Sykes, B.D., Craig, M.M., Holmes, C.F. (1997). A molecular basis for different interactions of marine toxins with protein phosphatase-1. Molecular models for bound motuporin, microcystins, okadaic acid, and calyculin A. Journal of Biological Chemistry, 272, 5087-5097. https://doi.org/10.1074/jbc.272.8.5087
  • Birungi, G., Li, S.F. (2009). Determination of cyanobacterial cyclic peptide hepatotoxins in drinking water using CE. Electrophoresis, 30(15), 2737-2742. https://doi.org/10.1002/elps.200900030
  • Bittner, M., Štern, A., Smutná, M., Hilscherová, K., Žegura, B. (2021). Cytotoxic and genotoxic effects of cyanobacterial and algal extracts-microcystin and retinoic acid content. Toxins (Basel), 13(2), 107-132. https://doi.org/10.3390/toxins13020107.
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  • Campos, A., Vasconcelos, V. (2010). Molecular mechanisms of microcystin toxicity in animal cells. International Journal of Molecular Sciences, 11, 268-287. https://doi.org/10.3390/ijms11010268
  • Carmichael, W.W. (1994). The toxins of cyanobacteria. Scientific American, 270(1), 78-86. https://doi.org/10.1038/scientificamerican0194-78
  • Chen, H., Zhao, J., Li, Y., He, L.X., Huang, Y.J., Shu, W.Q., Cao, J., Liu, W.B., Liu, J.Y. (2018). Gene expression network regulated by DNA methylation and microRNA during microcystin-leucine arginine induced malignant transformation in human hepatocyte L02 cells. Toxicology Letters, 289(1), 42-53. https://doi.org/10.1016/j.toxlet.2018.03.003
  • Chong, M.W.K., Gu, K.D., Lam, P.K.S., Yang, M., Fong, W.F. (2000). Study on the cytotoxicity of microcystin-LR on cultured cells. Chemosphere, 41, 143-147. https://doi.org/10.1016/S0045-6535(99)00402-6
  • Cines, D.B., Pollak, E.S., Buck, C.A., Loscalzo, J., Zimmerman, G.A., McEver, R.P., Pober, J.S., Wick, T.M., Konkle, B.A., Schwartz, B.S., Barnathan, E.S., McCrae, K.R., Hug, B.A., Schmidt, A-M., Stern, D.M. (1998). Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood, 91(10), 3527-3561. https://doi.org/10.1182/blood.V91.10.3527
  • Dias, E., Andrade, M., Alverca, E., Pereira, P., Batore´u, M.C., Jordan, P., Silva, M.J. (2009). Comparative study of the cytotoxic effect of microcistin-LR and purified extracts from Microcystis aeruginosa on a kidney cell line. Toxicon, 53, 487-495. https://doi.org/10.1016/j.toxicon.2009.01.029
  • Entfellner, E., Freil, M., Christiansen, G., Deng, L., Blom, J., Kurmayer, R. (2017). Evolution of anabaenopeptin peptide structural variability in the cyanobacterium Planktot-hrix. Frontier in Microbiology, 8, 1-13. https://doi.org/10.3389/fmicb.2017.00219
  • Faassen, E.J., Lürling, M. (2013). Occurrence of the microcystins MC-LW and MC-LF in dutch surface waters and their contribution to total microcystin toxicity. Marine Drugs, 11(7), 2643-2654. https://doi.org/10.3390/md11072643
  • Foroh, M.O. Mahrouz, D. (2016). The effect of cyanobacteria Nostoc. Sp Isc 113 polysaccharide on the proliferation and adhesion of endothelial cells to repair the vessel, Journal Of Animal Physiology And Development, 9(33), 1-11.
  • Fosse, J.H., Haraldsen, G., Falk, K., Edelmann, R. (2021). Endothelial cells in emerging viral infections. Frontiers in Cardiovascular Medicine, 8, 95. https://doi.org/10.3389/fcvm.2021.619690
  • Gutiérrez-Praena, D., Pichardo, S., Jos, A., Moreno, F.J., Cameán, A.M. (2012). Alterations observed in the endothelial HUVEC cell line exposed to pure cylindrospermopsin. Chemosphere, 89(9), 1151-1160. https://doi.org/10.1016/j.chemosphere.2012.06.023
  • Gutiérrez-Praena, D., Guzmán-Guillén, R., Pichardo, S., Moreno, F.J. (2019). Cytotoxic and morphological effects of microcystin-LR, cylindrospermopsin, and their combinations on the human hepatic cell line HepG2. Environmental Toxicology, 34, 240-251. https://doi.org/10.1002/tox.22679
  • Harke, M.J., Steffen, M.M., Gobler, C.J., Otten, T.G., Wilhelm, S.W., Wood, S.A., Paerl, H.W. (2016). A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis sp. Harmful Algae, 54, 4-20. https://doi.org/10.1016/j.hal.2015.12.007
  • Herrera, N., Herrera, C., Ortíz, I., Orozco, L., Robledo, S., Agudelo, D., Echeverria, F. (2018). Genotoxicity and cytotoxicity of three microcystin-LR containing cyanobacterial samples from Antioquia, Colombia. Toxicon, 154, 50-59. https://doi.org/10.1016/j.toxicon.2018.09.011
  • Karjalainen, M., Engstrom-Ost, J., Korpinen, S., Peltonen, H., Paakkonen, J.P., Ronkkonen, S., Suikkanen, S., Viitasalo, M. (2007). Ecosystem consequences of cyanobacteria in the northern Baltic Sea. Ambio, 36, 195-202. https://doi.org/10.1579/0044-7447
  • Khalid, M.N., Shameel, M., Ahmad, V., Shahzad, S., Leghari, S. (2010). Studies on the bioactivity and phycochemistry of Microcystis aeruginosa (Cyanophycota) from Sindh. Pakistan Journal of Botany, 42, 2635-2646.
  • Kim, S.K., Chojnacka, K. (2015). Marine Algae Extracts Processes, Products, and Applications, Wroclaw: Wiley-VCN, p. 227-346, ISBN: 9783527337088
  • Kotak, B.G., Lam, A.K., Prepas, E.E., Kenefi, S.L., Hrudey, S.E. (1995). Variability of the hepatotoxin, microcystin-LR, in hypereurophic drinking water lakes. Journal Phycology, 31, 248-263. https://doi.org/10.1111/j.0022-3646.1995.00248.x
  • Krüger-Genge, A., Blocki, A., Franke, R.P., Jung, F. (2019). Vascular endothelial cell biology: an update. International Journal of Molecular Sciences, 20(18), 4411-4433. https://doi.org/10.3390/ijms20184411
  • Kurmayer, R. (2011). The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. Journal of Phycology, 47, 200-207. https://doi.org/10.1111/j.1529-8817.2010.00931.x
  • Laude, K., Thuillez, C., Richard, V. (2001). Coronary endothelial dysfunction after ischemia and reperfusion: a new therapeutic target? Brazilian Journal of Medical and Biological Research, 34(1) 1-7. https://doi.org/10.1590/S0100-879X2001000100001
  • Lawton, L.A., Edwards, C., Codd, G.A. (1994). Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst, 11(9), 1525- 1530. https://doi.org/10.1039/AN9941901525
  • Moreno, I.M., Maraver, J., Aguete, E.C., Leao, M., Gago-Martínez, A., Cameán, A.M. (2004). Decomposition of microcystin-LR, microcystin-RR, and microcystin-YR in water samples submitted to in vitro dissolution tests. Journal of Agriculture Food Chemistry, 52(19), 5933-5938. https://doi.org/10.1021/jf0489668
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There are 52 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Research Articles
Authors

Seda Kuşoğlu Gültekin 0000-0003-0674-1582

Elif Mertoğlu Kamalı 0000-0002-3606-4722

Kaan Yılancıoğlu 0000-0003-0740-5580

Nazlı Arda 0000-0002-1043-5652

Project Number FYL-2016-21655
Early Pub Date January 28, 2022
Publication Date April 1, 2022
Submission Date August 17, 2021
Published in Issue Year 2022Volume: 5 Issue: 2

Cite

APA Kuşoğlu Gültekin, S., Mertoğlu Kamalı, E., Yılancıoğlu, K., Arda, N. (2022). Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells. Aquatic Research, 5(2), 117-128. https://doi.org/10.3153/AR22011
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