Proteomic analysis of anatoxin-a acute toxicity in zebrafish reveals gender specific responses and additional mechanisms of cell stress

Carneiro, Mariana; Gutiérrez-Praena, Daniel; Osório, Hugo; Vasconcelos, Vı́tor; Carvalho, António Paulo; Campos, Alexandre

doi:10.1016/j.ecoenv.2015.05.031

Cited by 21 publications

(17 citation statements)

References 63 publications

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“…In the present study, the neurotoxicological response of medaka fish subjected to anatoxin-a appears comparable to that found in carp (Osswald et al, 2007a) and zebrafish (Carneiro et al, 2015) supporting the evidences for the existence of a similar mechanism of action. Whereas no apparent precursor effect appears when fish are gavaged with sub-acute doses of anatoxin-a, the symptoms observed in the fish exposed to a higher dose denote an all-or-nothing effect, comprising rapid and intense neurotoxic signs, that are compatible with the mechanism of toxic action of anatoxin-a in the nervous system that has been described so far for other vertebrates (Fawell et al, 1999).…”

Section: Discussionsupporting

confidence: 88%

“…Despite the acute neurotoxic effects of anatoxin-a, the consequence of the proliferation of anatoxins-a producing cyanobacterial biofilms on ecosystem health and aquatic organisms remains largely unknown. Despite, toxic benthic cyanobacterial mats have been associated with decreased macro-invertebrate diversity (Aboal et al, 2002), few studies have investigated the genuine toxicological effects of these compounds on aquatic organisms (Carneiro et al, 2015; Osswald et al, 2007b; Anderson et al, 2018). In some experiments performed on fishes, such as carps and goldfish, behaviourial defects such as rapid opercular movement, abnormal swimming (Osswald et al, 2007a) and muscle rigidity (Carmichael et al, 1975) were observed.…”

Section: Introductionmentioning

confidence: 99%

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Toxicity, transfer and depuration of anatoxin-a (cyanobacterial neurotoxin) in medaka fish exposed by single-dose gavage

Marie

Colas

Duval

2019

Preprint

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9The proliferations of cyanobacteria are increasingly prevalent in warm and nutrient-enriched 10 waters and occur in many rivers and water bodies due especially to eutrophication. The aim of 11 this work is to study in female medaka fish the toxicity, the transfer and the depuration of the 12 anatoxin-a, a neurotoxin produced by benthic cyanobacterial biofilms. This work will provide 13 answers regarding acute toxicity induced by single gavage by anatoxin-a and to the risks of 14 exposure by ingestion of contaminated fish flesh, considering that data on these aspects remain 15 particularly limited. 16 17The oral LD 50 of a single dose of (±)-anatoxin-a was determined at 11.50 µg.g -1 . First of all, 18lethal dose (100% from 20 µg.g -1 ) provokes rapid respiratory paralysis (in 1-2 min) of the fish 19 inducing the death by asphyxia. Noticeably, no death nor apparent neurotoxicologic effect 20 occurred during the experimentation period for the 45 fish exposed to a single sub-acute dose 21 of (±)-anatoxin-a corresponding to the no observable adverse effect level (NOAEL = 6.67 µg.g -22 1 ). Subsequently, the toxico-kinetics of the (±)-anatoxin-a was observed in the guts, the livers 23 and the muscles of female medaka fish for 10 days. 24In parallel, a protocol for extraction of anatoxin-a has been optimized beforehand by testing 25 3 different solvents on several matrices, the extraction with 75% methanol + 0.1% formic acid 26 appearing to be the most efficient. Anatoxin-a was quantified by high-resolution qTOF mass 27 spectrometry coupled upstream to a UHPLC chromatographic chain. The toxin could not be 28 detected in the liver after 12 h, and in the gut and muscle after 3 days. The mean clearance rates 29 of (±)-anatoxin-a calculated after 12 h are above 58%, 100% and 90% for the guts, the livers 30 and the muscles, respectively. Non-targeted metabolomics investigations performed on the fish 31 liver indicates that the single sub-acute exposure by gavage induces noticeable metabolome 32 dysregulations, including important phospholipid decreases, with an organism recovery period 33 of above 12-24h. Overall, the medaka fish do not appear to accumulate (±)-anatoxin-a and to 34 largely recover after 24h following a single sub-acute oral liquid exposure at the NOAEL. 35 36

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Section: Discussionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Toxicity, transfer and depuration of anatoxin-a (cyanobacterial neurotoxin) in medaka fish exposed by single-dose gavage

Marie

Colas

Duval

2019

Preprint

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“…In some cases the possible mode of action would unlikely be sensitive to sex-differences. This is the case for example for neurotoxins like anatoxin-a (Carneiro et al 2015) and 4,5-dichloro-2-n-octyl-4-isothiazolin-3-one (DCOIT) (Chen et al 2014), the metalloid arsenic (Carlson et al 2013), or benzo[a]pyrene (B[a]P) (Riva et al 2011). Anatoxin-a exerts its toxic effects by acting as a competitive agonist for acetylcholine receptors affecting signal transmission in neuromuscular junctions.…”

Section: Sex Dependent Effectmentioning

confidence: 99%

Use of proteomics to detect sex-related differences in effects of toxicants: implications for using proteomics in toxicology

Rietjens

Vervoort

Maslowska-Gornicz

et al. 2018

Critical Reviews in Toxicology

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This review provides an overview of results obtained when using proteome analysis for detecting sexbased differences in response to toxicants. It reveals implications to be taken into account when considering the use of proteomics in toxicological studies. It appears that results may differ when studying the same chemical in the same species in different target tissues. Another result of interest is the limited dose-response behavior of differential abundance patterns observed in studies where more than one dose level is tested. It is concluded that use of proteomics to study differences in modes of action of toxic compounds is an active area of research. The examples from use of proteomics to study sexdependent differences also reveal that further studies are needed to provide reliable insight in modes of action, novel biomarkers or even novel therapies. To eventually reach this aim for this and other toxicological endpoints, it is essential to consider background variability, consequences of timing of toxicant administration, dose-response behavior, relevant species and target organ, species and organ variability and the presence of proteoforms.

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“…Development of high‐throughput techniques enabled obtaining the complex expression profiles in living systems. The annotated genome sequence for zebrafish is currently available and many proteomic studies on zebrafish were performed to analyze embryogenic stages , organ systems , or pathological effects of genetic mutations and toxins . A proteome profiling of adult zebrafish organs previously performed by Abramsson et al.…”

mentioning

confidence: 99%

“…The annotated genome sequence for zebrafish is currently available [7] and many proteomic studies on zebrafish were performed to analyze embryogenic stages [8,9], organ systems [10,11], or pathological effects of genetic mutations [12] and toxins [13][14][15]. A proteome profiling of adult zebrafish organs previously performed by Abramsson et al [10] showed high percentage (40%) of brain-specific proteins.…”

mentioning

confidence: 99%

A detailed proteomic profiling of plasma membrane from zebrafish brain

Šmidák

Aradská

Kirchberger

et al. 2016

Proteomics Clinical Apps

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Zebrafish (Danio rerio) is a well-established model organism in developmental biology and disease modeling. In recent years, an increasing amount of studies used zebrafish to analyze the genetic changes underlying various neurological disorders. The brain plasma membrane proteome represents the major subsets of signaling proteins and promising drug targets, but is often understudied due to traditional experimental difficulties including problems with solubility, detergent removal, or low abundance. Here, we report a comprehensive dataset of the proteins identified in the enriched plasma membrane of the zebrafish brain by applying sequential trypsin/chymotrypsin digestion with multidimensional LC-MS/MS. A total number of 97 017 peptide groups corresponding to 9201 proteins were identified. These were annotated in various molecular functions or neurological disorders. The dataset of the current study provides a useful data source for further utilizing zebrafish in basic and clinical neuroscience.

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Proteomic analysis of anatoxin-a acute toxicity in zebrafish reveals gender specific responses and additional mechanisms of cell stress

Cited by 21 publications

References 63 publications

Toxicity, transfer and depuration of anatoxin-a (cyanobacterial neurotoxin) in medaka fish exposed by single-dose gavage

Toxicity, transfer and depuration of anatoxin-a (cyanobacterial neurotoxin) in medaka fish exposed by single-dose gavage

Use of proteomics to detect sex-related differences in effects of toxicants: implications for using proteomics in toxicology

A detailed proteomic profiling of plasma membrane from zebrafish brain

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