In vitro modulation of intracellular receptor signaling and cytotoxicity induced by extracts of cyanobacteria, complex water blooms and their fractions

Štěpánková, Tereza; Ambrožová, Lenka; Bláha, Luděk; Giesy, John P.; Hilscherová, Klára

doi:10.1016/j.aquatox.2011.08.002

Cited by 32 publications

(14 citation statements)

References 57 publications

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“…Increasing global temperature, nutrient and pollutant enrichment via anthropogenic runoff, drought and flooding lead to eutrophication and outbreak of cyanobacterial blooms 3 4 . The toxic cyanobacterial blooms can produce and release cyanotoxins, the secondary metabolites of cyanobacteria, into water 5 . Among all the cyanobacterial toxins, microcystins (MCs) represent a family of potent hepatotoxins and are considered as the most resistant of cyanotoxins to degradation because of their stable cyclic peptide structure 6 .…”

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confidence: 99%

Sex-dependent effects of microcystin-LR on hypothalamic-pituitary-gonad axis and gametogenesis of adult zebrafish

Liu

Chen

et al. 2016

Sci Rep

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While microcystins (MCs) have been reported to exert reproductive toxicity on fish with a sexdependent effect, the underlying mechanism has been rarely investigated. In the present study, zebrafish were exposed to 1, 5 and 20 μg/L MC-LR for 30 d. The gonad-somatic index declined in all treated males. 17β-estradiol (E 2 ), testosterone (T), 11-keto testosterone (11-KT) and follicle-stimulating hormone (FSH) levels increased in serum from all treated females, while T, FSH and luteinizing hormone (LH) levels changed in all treated males. Histomorphological observation showed that MC-LR exposure evidently retarded oogenesis and spermatogenesis. Transcriptional changes of 22 genes of the hypothalamic-pituitary-gonad (HPG) axis exhibited sex-specific responses, and the relationship between gene transcriptions and gametogenesis was evaluated by principle component analysis (PCA). Major contributors to PC1 (gnrh2, gnrhr3, ar, lhr, hmgra, hmgrb and cyp19a) were positively correlated with the number of post-vitellogenic oocytes, while PC1 (gnrh2, lhβ, erβ, fshr, cyp11a and 17βhsd) were positively correlated with the number of spermatozoa. The protein levels of 17βHSD and CYP19a were affected in both females and males. In conclusion, this study first investigated the sex-dependent effects of microcystins on fish reproduction and revealed some important molecular biomarkers related to gametogenesis in zebrafish suffered from MC-LR.Cyanobacteria are photosynthetic, oxygen producing, gram-negative microorganisms found ubiquitously in nature even at extreme climatic conditions 1,2 . Increasing global temperature, nutrient and pollutant enrichment via anthropogenic runoff, drought and flooding lead to eutrophication and outbreak of cyanobacterial blooms 3,4 . The toxic cyanobacterial blooms can produce and release cyanotoxins, the secondary metabolites of cyanobacteria, into water 5 . Among all the cyanobacterial toxins, microcystins (MCs) represent a family of potent hepatotoxins and are considered as the most resistant of cyanotoxins to degradation because of their stable cyclic peptide structure 6 . To date, over 100 variants of MCs have been isolated, and microcystin-LR (MC-LR), a hydrophobic variant, is considered to be the most commonly occurring and lethal toxin 7 . In fish, MCs accumulate mainly in liver and therefore liver is considered as the first target organ of MCs 8,9 . A provisional safety guideline of 1.0 μg/L MC-LR in drinking water was recommended by the World Health Organization (WHO) 10 . MCs are released from the cyanobacterial cells into the water bodies where fish spends their whole life stage, including growth, reproduction and embryonic development 11 . Gonad has been recognized as the second important target organ of MCs 12 and MCs exert negative effects on the reproductive system of fish [13][14][15] . Lysis of the gonadosomatic tissue in ovary and disruption of spermatogenesis in testis were observed in medaka fish exposed to MC-LR 13. Hou et al. also suggested MC-LR had adverse effects on histologic...

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confidence: 99%

Sex-dependent effects of microcystin-LR on hypothalamic-pituitary-gonad axis and gametogenesis of adult zebrafish

Liu

Chen

et al. 2016

Sci Rep

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“…While the study of estrogenic effects of cyanobacteria has been the subject of several reports, androgen-and glucocorticoid-type effects have not been studied in depth so far. However, the limited data did not support such effects from cyanobacterial extracts [19]. We only included androgen-and glucocorticoid-responsive RGAs in preliminary screenings that need further verification.…”

Section: Discussionmentioning

confidence: 99%

“…It is not entirely clear which of the different compounds present in cyanobacterial blooms exert estrogen activity. The net effect may be the result from the interaction of different cyanobacterial metabolites in the bloom, which constitute in themselves a complex mixture of known and unknown compounds, and/or other substances coexisting in the water [18,19,21].…”

Section: Introductionmentioning

confidence: 99%

“…These studies indicate that cyanobacterial compounds other than MCs are at least Most studies have mainly focused on EDCs of anthropogenic origin without extensively considering those that are naturally-produced in the environment [17,18]. However, it has been reported that cyanobacterial compounds (extracts from blooms and exudates) have ED activity, mainly through activation of the estrogen receptor [19,20]. It is not entirely clear which of the different compounds present in cyanobacterial blooms exert estrogen activity.…”

Section: Introductionmentioning

confidence: 99%

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Investigation of In Vitro Endocrine Activities of Microcystis and Planktothrix Cyanobacterial Strains

Mallia

Ivanova

Eriksen

et al. 2020

Toxins

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Cyanobacteria are cosmopolitan photosynthetic prokaryotes that can form dense accumulations in aquatic environments. They are able to produce many bioactive metabolites, some of which are potentially endocrine disrupting compounds, i.e., compounds that interfere with the hormonal systems of animals and humans. Endocrine disruptors represent potential risks to both environmental and human health, making them a global challenge. The aim of this study was to investigate the potential endocrine disrupting activities with emphasis on estrogenic effects of extracts from cultures of Microcystis or Planktothrix species. We also assessed the possible role of microcystins, some of the most studied cyanobacterial toxins, and thus included both microcystin-producing and non-producing strains. Extracts from 26 cyanobacterial cultures were initially screened in estrogen-, androgen-, and glucocorticoid-responsive reporter-gene assays (RGAs) in order to identify endocrine disruption at the level of nuclear receptor transcriptional activity. Extracts from selected strains were tested repeatedly in the estrogen-responsive RGAs, but the observed estrogen agonist and antagonist activity was minor and similar to that of the cyanobacteria growth medium control. We thus focused on another, non-receptor mediated mechanism of action, and studied the 17β-estradiol (natural estrogen hormone) biotransformation in human liver microsomes in the presence or absence of microcystin-LR (MC-LR), or an extract from the MC-LR producing M. aeruginosa PCC7806 strain. Our results show a modulating effect on the estradiol biotransformation. Thus, while 2-hydroxylation was significantly decreased following co-incubation of 17β-estradiol with MC-LR or M. aeruginosa PCC7806 extract, the relative concentration of estrone was increased.

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“…For the reaction, the primers MAPF (5′-CTAATGGCCGATTGGAAGAA-3′) and MAPR (5′-CAGACTATCCCGTTCCGTTG-3′) [ 61 ] were used in a mixture containing DreamTaq PCR Master Mix (ThermoFisher Scientific ® ) with 1 U of Taq DNA polymerase using a T100™ Thermal Cycler (BioRad) with a thermocycling profile consisting of an initial denaturation step at 94 °C for 3 min, followed by 35 cycles of 20 s at 94 °C, 20 s at 60 °C, and 20 s at 72 °C and a final extension step of 5 min at 72 °C. DNA from the P. agardhii strain CCALA159, that is a microcystin producer [ 62 ], was used has a positive control for the amplification. The PCR reactions were checked for fragment amplification under UV light after electrophoretic analysis performed in 1% w/v agarose gel with GreenSafe Premium™ DNA staining (NZYTech ® ), at 80 V in 0.5× Tris-borate EDTA (TBE) buffer for 45 min.…”

Section: Methodsmentioning

confidence: 99%

Detection of a Planktothrix agardhii Bloom in Portuguese Marine Coastal Waters

Churro

Azevedo²,

Vasconcelos³

et al. 2017

Toxins

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Cyanobacteria blooms are frequent in freshwaters and are responsible for water quality deterioration and human intoxication. Although, not a new phenomenon, concern exists on the increasing persistence, scale, and toxicity of these blooms. There is evidence, in recent years, of the transfer of these toxins from inland to marine waters through freshwater outflow. However, the true impact of these blooms in marine habitats has been overlooked. In the present work, we describe the detection of Planktothrix agardhii, which is a common microcystin producer, in the Portuguese marine coastal waters nearby a river outfall in an area used for shellfish harvesting and recreational activities. P. agardhii was first observed in November of 2016 in seawater samples that are in the scope of the national shellfish monitoring system. This occurrence was followed closely between November and December of 2016 by a weekly sampling of mussels and water from the sea pier and adjacent river mouth with salinity ranging from 35 to 3. High cell densities were found in the water from both sea pier and river outfall, reaching concentrations of 4,960,608 cells·L−1 and 6810.3 × 106 cells·L−1 respectively. Cultures were also established with success from the environment and microplate salinity growth assays showed that the isolates grew at salinity 10. HPLC-PDA analysis of total microcystin content in mussel tissue, water biomass, and P. agardhii cultures did not retrieve a positive result. In addition, microcystin related genes were not detected in the water nor cultures. So, the P. agardhii present in the environment was probably a non-toxic strain. This is, to our knowledge, the first report on a P. agardhii bloom reaching the sea and points to the relevance to also monitoring freshwater harmful phytoplankton and related toxins in seafood harvesting and recreational coastal areas, particularly under the influence of river plumes.

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In vitro modulation of intracellular receptor signaling and cytotoxicity induced by extracts of cyanobacteria, complex water blooms and their fractions

Cited by 32 publications

References 57 publications

Sex-dependent effects of microcystin-LR on hypothalamic-pituitary-gonad axis and gametogenesis of adult zebrafish

Sex-dependent effects of microcystin-LR on hypothalamic-pituitary-gonad axis and gametogenesis of adult zebrafish

Investigation of In Vitro Endocrine Activities of Microcystis and Planktothrix Cyanobacterial Strains

Detection of a Planktothrix agardhii Bloom in Portuguese Marine Coastal Waters

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