Research Article
PDF EndNote BibTex Cite

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
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.

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.
  • Bryant, D.A. (1994). Gene nomenclature recommendations for green photosynthetic bacteria and heliobacteria‖. Photosynthesis Research, 41, 27-28. https://doi.org/10.1007/BF02184142
  • 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
  • Paiva, L., Lima, E., Neto, A.I., Baptista, J. (2017). Angiotensin I-converting enzyme (ACE) inhibitory activity, antioxidant properties, phenolic content and amino acid profiles of Fucus spiralis protein hydrolysate fractions. Marine Drugs, 15(10), 311-329. https://doi.org/10.3390/md15100311
  • Pearson, L., Mihali, T., Moffitt, M., Kellmann, R., Neilan, B. (2010). On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 8, 1650-1680. https://doi.org/10.3390/md8051650
  • Pırıldar, S., Sütlüpınar, N., Atasever, B., Erdem-Kuruca, S., Papouskova, B., Šimánek, V. (2010). Chemical constituents of the different parts of Colchicum baytopiorum (Liliaceae) and their cytotoxic activities on K562 and HL60 cell-lines. Pharmaceutical Biology, 48(1), 32-39. https://doi.org/10.3109/13880200903029373
  • Piyathilaka, M.A.P.C., Pathmalal, M.M., Tennekoon, K.H., De Silva, B.G.D.N.K., Samarakoon, S.R., Chanthirika, S. (2015). Microcystin-LR-induced cytotoxicity and apoptosis in human embryonic kidney and human kidney adenocarcinoma cell lines. Microbiology, 161, 819-828. https://doi.org/10.1099/mic.0.000046
  • Plate, K.H., Breier, G., Risau, W. (1994). Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathology, 4, 207-218. https://doi.org/10.1111/j.1750-3639.1994.tb00835.x
  • Rajendran, P., Rengarajan, T., Thangavel, J., Nishigaki, Y., Sakthisekaran, D., Sethi, G., Nishigaki, I. (2013). The vascular endothelium and human diseases. International Journal of Biological Sciences, 9(10), 1057-1069. https://doi.org/10.7150/ijbs.7502
  • Ramanan, S., Tang, J., Velayudhan, A. (2000). Isolation and preparative purification of microcystin variants. Journal of Chromatography A, 883(1-2), 103-112. https://doi.org/10.1016/S0021-9673(00)00378-2
  • Ramos, D.F., Matthiensen, A., Colvara, W., Votto, A.P.S., Trindade, G.S., Silva, P.E.A., Yunes, J.S. (2015). Antimycobacterial and cytotoxicity activity of microcystins. Journal of Venomous Animals and Toxins Including Tropical Diseases, 21(9), 1-7. https://doi.org/10.1186/s40409-015-0009-8
  • Silva-Stenico, M.E., Kaneno, R., Zambuzi, F.A., Vaz, M.G., Alvarenga, D.O., Fiore, M.F. (2013). Natural products from cyanobacteria with antimicrobial and antitumor activity. Current Pharmaceutical Biotechnology, 14(9), 820-828. https://doi.org/10.2174/1389201014666131227114846
  • Singh, S., Kate, B.N., Banerjee, U.C. (2005). Bioactive compounds from cyanobacteria and microalgae: An overview. Critical Reviews in Biotechnology, 25, 73-95. https://doi.org/10.1080/07388550500248498
  • Singhal, A.K., Symons, J.D., Boudina, S., Jaishy, B., Shiu, Y.T. (2010). Role of endothelial cells in myocardial ischemia-reperfusion injury. Vascular Disease Prevention, 7, 1-14. http//: doi: 10.2174/1874120701007010001
  • Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales). Bacterological Reviews, 35, 171-205.
  • Svobodova, H., Jost, P., Stetina, R. (2012). Cytotoxicity and genotoxicity evaluation of antidote HI-6 tested on eight cell lines of human and rodent origin. General Physiology and Biophysics, 31(1), 77-84. https://doi.org/10.4149/gpb_2012_010
  • Tillett, D., Dittmann, E., Erhard, M., Döhren, H., Börner, T., Neila, B. (2000). Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806 an integrated peptide–polyketide synthetase system. Chemistry & Biology, 7(10), 753-764. https://doi.org/10.1016/s1074-5521(00)00021-1
  • Tonk, L., Visser, P.M., Christiansen, G., Dittmann, E., Snelder, E.O., Wiedner, C., Mur, L.R., Huisman, J. (2005). The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Applied and Environmental Microbiology, 71, 5177-5181. https://doi.org/10.1128/AEM.71.9.5177-5181.2005
  • Wang, L., Chen, G., Xiao, G., Han, L., Wang, Q., Hu. T. (2020). Cylindrospermopsin induces abnormal vascular development through impairing cytoskeleton and promoting vascular endothelial cell apoptosis by the Rho/ROCK signaling pathway. Environmental Research, 183, 109236. https://doi.org/10.1016/j.envres.2020.109236
  • Wei, N., Hu, L., Song, L., Gan, N. (2016). Microcystin-bound protein patterns in different cultures of Microcystis aeruginosa and field samples. Toxins, 8(10), 293-310. https://doi.org/10.3390/toxins8100293
  • Welker, M., von Dohren, H. (2006). Cyanobacterial peptides-nature’s own combinatorial biosynthesis. FEMS Microbiology Ecology, 30, 530-563. https://doi.org/10.1111/j.1574-6976.2006.00022.x
  • Yu, H., Clark, K.D., Anderson, J.L. (2015). Rapid and sensitive analysis of microcystins using ionic liquid-based in situ dispersive liquid-liquid microextracton. Journal of Chromatography A, 1406, 10-18. https://doi.org/10.1016/j.chroma.2015.05.075
  • Zegura, B., Sedmak, B., Filipic, M. (2003). Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon, 41(1), 41-48. https://doi.org/10.1016/s0041-0101(02)00207-6
  • Zhong, Q., Sun, F., Wang, W., Xiao, W., Zhao, X., Gu, K. (2017). Water metabolism dysfunction via renin-angiotensin system activation caused by liver damage in mice treated with microcystin-RR. Toxicology Letters, 273(5), 86-96. https://doi.org/10.1016/j.toxlet.2017.03.019

Year 2022, Volume 5, Issue 2, 117 - 128, 01.04.2022
https://doi.org/10.3153/AR22011

Abstract

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.
  • Bryant, D.A. (1994). Gene nomenclature recommendations for green photosynthetic bacteria and heliobacteria‖. Photosynthesis Research, 41, 27-28. https://doi.org/10.1007/BF02184142
  • 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
  • Paiva, L., Lima, E., Neto, A.I., Baptista, J. (2017). Angiotensin I-converting enzyme (ACE) inhibitory activity, antioxidant properties, phenolic content and amino acid profiles of Fucus spiralis protein hydrolysate fractions. Marine Drugs, 15(10), 311-329. https://doi.org/10.3390/md15100311
  • Pearson, L., Mihali, T., Moffitt, M., Kellmann, R., Neilan, B. (2010). On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 8, 1650-1680. https://doi.org/10.3390/md8051650
  • Pırıldar, S., Sütlüpınar, N., Atasever, B., Erdem-Kuruca, S., Papouskova, B., Šimánek, V. (2010). Chemical constituents of the different parts of Colchicum baytopiorum (Liliaceae) and their cytotoxic activities on K562 and HL60 cell-lines. Pharmaceutical Biology, 48(1), 32-39. https://doi.org/10.3109/13880200903029373
  • Piyathilaka, M.A.P.C., Pathmalal, M.M., Tennekoon, K.H., De Silva, B.G.D.N.K., Samarakoon, S.R., Chanthirika, S. (2015). Microcystin-LR-induced cytotoxicity and apoptosis in human embryonic kidney and human kidney adenocarcinoma cell lines. Microbiology, 161, 819-828. https://doi.org/10.1099/mic.0.000046
  • Plate, K.H., Breier, G., Risau, W. (1994). Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathology, 4, 207-218. https://doi.org/10.1111/j.1750-3639.1994.tb00835.x
  • Rajendran, P., Rengarajan, T., Thangavel, J., Nishigaki, Y., Sakthisekaran, D., Sethi, G., Nishigaki, I. (2013). The vascular endothelium and human diseases. International Journal of Biological Sciences, 9(10), 1057-1069. https://doi.org/10.7150/ijbs.7502
  • Ramanan, S., Tang, J., Velayudhan, A. (2000). Isolation and preparative purification of microcystin variants. Journal of Chromatography A, 883(1-2), 103-112. https://doi.org/10.1016/S0021-9673(00)00378-2
  • Ramos, D.F., Matthiensen, A., Colvara, W., Votto, A.P.S., Trindade, G.S., Silva, P.E.A., Yunes, J.S. (2015). Antimycobacterial and cytotoxicity activity of microcystins. Journal of Venomous Animals and Toxins Including Tropical Diseases, 21(9), 1-7. https://doi.org/10.1186/s40409-015-0009-8
  • Silva-Stenico, M.E., Kaneno, R., Zambuzi, F.A., Vaz, M.G., Alvarenga, D.O., Fiore, M.F. (2013). Natural products from cyanobacteria with antimicrobial and antitumor activity. Current Pharmaceutical Biotechnology, 14(9), 820-828. https://doi.org/10.2174/1389201014666131227114846
  • Singh, S., Kate, B.N., Banerjee, U.C. (2005). Bioactive compounds from cyanobacteria and microalgae: An overview. Critical Reviews in Biotechnology, 25, 73-95. https://doi.org/10.1080/07388550500248498
  • Singhal, A.K., Symons, J.D., Boudina, S., Jaishy, B., Shiu, Y.T. (2010). Role of endothelial cells in myocardial ischemia-reperfusion injury. Vascular Disease Prevention, 7, 1-14. http//: doi: 10.2174/1874120701007010001
  • Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales). Bacterological Reviews, 35, 171-205.
  • Svobodova, H., Jost, P., Stetina, R. (2012). Cytotoxicity and genotoxicity evaluation of antidote HI-6 tested on eight cell lines of human and rodent origin. General Physiology and Biophysics, 31(1), 77-84. https://doi.org/10.4149/gpb_2012_010
  • Tillett, D., Dittmann, E., Erhard, M., Döhren, H., Börner, T., Neila, B. (2000). Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806 an integrated peptide–polyketide synthetase system. Chemistry & Biology, 7(10), 753-764. https://doi.org/10.1016/s1074-5521(00)00021-1
  • Tonk, L., Visser, P.M., Christiansen, G., Dittmann, E., Snelder, E.O., Wiedner, C., Mur, L.R., Huisman, J. (2005). The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Applied and Environmental Microbiology, 71, 5177-5181. https://doi.org/10.1128/AEM.71.9.5177-5181.2005
  • Wang, L., Chen, G., Xiao, G., Han, L., Wang, Q., Hu. T. (2020). Cylindrospermopsin induces abnormal vascular development through impairing cytoskeleton and promoting vascular endothelial cell apoptosis by the Rho/ROCK signaling pathway. Environmental Research, 183, 109236. https://doi.org/10.1016/j.envres.2020.109236
  • Wei, N., Hu, L., Song, L., Gan, N. (2016). Microcystin-bound protein patterns in different cultures of Microcystis aeruginosa and field samples. Toxins, 8(10), 293-310. https://doi.org/10.3390/toxins8100293
  • Welker, M., von Dohren, H. (2006). Cyanobacterial peptides-nature’s own combinatorial biosynthesis. FEMS Microbiology Ecology, 30, 530-563. https://doi.org/10.1111/j.1574-6976.2006.00022.x
  • Yu, H., Clark, K.D., Anderson, J.L. (2015). Rapid and sensitive analysis of microcystins using ionic liquid-based in situ dispersive liquid-liquid microextracton. Journal of Chromatography A, 1406, 10-18. https://doi.org/10.1016/j.chroma.2015.05.075
  • Zegura, B., Sedmak, B., Filipic, M. (2003). Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon, 41(1), 41-48. https://doi.org/10.1016/s0041-0101(02)00207-6
  • Zhong, Q., Sun, F., Wang, W., Xiao, W., Zhao, X., Gu, K. (2017). Water metabolism dysfunction via renin-angiotensin system activation caused by liver damage in mice treated with microcystin-RR. Toxicology Letters, 273(5), 86-96. https://doi.org/10.1016/j.toxlet.2017.03.019

Details

Primary Language English
Subjects Marine and Freshwater Biology
Journal Section Research Articles
Authors

Seda KUŞOĞLU GÜLTEKİN>
Üsküdar University, Faculty of Engineering and Natural Sciences, Department of Chemical Engineering
0000-0003-0674-1582
Türkiye


Elif MERTOĞLU KAMALI>
İstanbul University, Institute of Graduate Studies in Sciences, Department of Molecular Biology and Genetics
0000-0002-3606-4722
Türkiye


Kaan YILANCIOĞLU>
Üsküdar University, Faculty of Engineering and Natural Sciences, Department of Molecular Biology and Genetics
0000-0003-0740-5580
Türkiye


Nazlı ARDA> (Primary Author)
Istanbul University, Science Faculty, Molecular Biology and Genetics Department
0000-0002-1043-5652
Türkiye

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.
Early Pub Date January 28, 2022
Publication Date April 1, 2022
Application Date August 17, 2021
Acceptance Date January 21, 2022
Published in Issue Year 2022, Volume 5, Issue 2

Cite

Bibtex @research article { aquatres983789, journal = {Aquatic Research}, eissn = {2618-6365}, address = {Esnaf Mah. Pembe Köşk Sok. Kentplus Kadıköy Sitesi B Blok D435 Kadıköy-İstanbul}, publisher = {Nuray ERKAN ÖZDEN}, year = {2022}, volume = {5}, number = {2}, pages = {117 - 128}, doi = {10.3153/AR22011}, title = {Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells}, key = {cite}, author = {Kuşoğlu Gültekin, Seda and Mertoğlu Kamalı, Elif and Yılancıoğlu, Kaan and Arda, Nazlı} }
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 . DOI: 10.3153/AR22011
MLA Kuşoğlu Gültekin, S. , Mertoğlu Kamalı, E. , Yılancıoğlu, K. , Arda, N. "Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells" . Aquatic Research 5 (2022 ): 117-128 <https://aquatres.scientificwebjournals.com/en/pub/issue/68273/983789>
Chicago Kuşoğlu Gültekin, S. , Mertoğlu Kamalı, E. , Yılancıoğlu, K. , Arda, N. "Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells". Aquatic Research 5 (2022 ): 117-128
RIS TY - JOUR T1 - Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells AU - Seda Kuşoğlu Gültekin , Elif Mertoğlu Kamalı , Kaan Yılancıoğlu , Nazlı Arda Y1 - 2022 PY - 2022 N1 - doi: 10.3153/AR22011 DO - 10.3153/AR22011 T2 - Aquatic Research JF - Journal JO - JOR SP - 117 EP - 128 VL - 5 IS - 2 SN - -2618-6365 M3 - doi: 10.3153/AR22011 UR - https://doi.org/10.3153/AR22011 Y2 - 2022 ER -
EndNote %0 Aquatic Research Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells %A Seda Kuşoğlu Gültekin , Elif Mertoğlu Kamalı , Kaan Yılancıoğlu , Nazlı Arda %T Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells %D 2022 %J Aquatic Research %P -2618-6365 %V 5 %N 2 %R doi: 10.3153/AR22011 %U 10.3153/AR22011
ISNAD Kuşoğlu Gültekin, Seda , Mertoğlu Kamalı, Elif , Yılancıoğlu, Kaan , Arda, Nazlı . "Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells". Aquatic Research 5 / 2 (April 2022): 117-128 . https://doi.org/10.3153/AR22011
AMA Kuşoğlu Gültekin S. , Mertoğlu Kamalı E. , Yılancıoğlu K. , Arda N. Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells. Aquat Res. 2022; 5(2): 117-128.
Vancouver Kuşoğlu Gültekin S. , Mertoğlu Kamalı E. , Yılancıoğlu K. , Arda N. Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells. Aquatic Research. 2022; 5(2): 117-128.
IEEE S. Kuşoğlu Gültekin , E. Mertoğlu Kamalı , K. Yılancıoğlu and N. Arda , "Dose-dependent cytotoxic and proliferative effects of Microcystis aeruginosa extract and its fractions on human endothelial cells", Aquatic Research, vol. 5, no. 2, pp. 117-128, Apr. 2022, doi:10.3153/AR22011

ustresim_2020_dergipark.png

is licensed under a CreativeCommons Attribtion-ShareAlike 4.0 International Licence 14628   13259

Open Access Statement:

This is an open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.