Insights into the nature of uranium target proteins within zebrafish gills after chronic and acute waterborne exposures

Bucher, Guillaume; Mounicou, Sandra; Simon, Olivier; Floriani, Magali; Łobiński, Ryszard; Frelon, Sandrine

doi:10.1002/etc.3249

Cited by 17 publications

(7 citation statements)

References 27 publications

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“…Much remains to be discovered regarding biologically relevant uranium–protein interactions. Although recent proteomic and transcriptomic studies have explored effects on protein/transcript abundances in response to uranium, ,,− in vivo protein–uranyl associations were studied in only a handful of cases so far. − Furthermore, although bio-geochemical redox transformations of uranium are intensely studied, information on intracellular redox chemistry of uranium is still limited . It is clearly desirable to expand further metalloproteomic studies as well as to explore uranium redox chemistry with individual proteins and within the cytosol, to better understand uranium metabolic pathways, toxicity, and resistance mechanisms.…”

Section: Discussionsupporting

confidence: 76%

“…To understand cellular effects of uranium, and also to be able to bioengineer bacterial strains with superior tolerance toward and/or accumulation of uranium, it is important to consider intracellular speciation, toxicity pathways, and mechanisms for detoxification. In this context, there has been increasing interest in studying the interactions of uranyl with proteins, either with selected candidates , or in the context of metalloproteomics studies. − In a study on the model uranium accumulator Procambarus clarkii, a freshwater crayfish, uranium was detected in fractions containing low-molecular weight proteins, designated as “MT-like fraction” . “MT” stands for metallothioneins, an important class of mostly intracellular proteins with roles in both heavy metal detoxification and reactive oxygen species scavenging. − They are stress-response metalloproteins, characterized by their small size (usually less than 10 kDa) and high metal and sulfur contents.…”

Section: Introductionmentioning

confidence: 99%

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Unexpected Interactions of the Cyanobacterial Metallothionein SmtA with Uranium

Acharya

Blindauer

2016

Inorg. Chem.

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Molecules for remediating or recovering uranium from contaminated environmental resources are of high current interest, with protein-based ligands coming into focus recently. Metallothioneins either bind or redox-silence a range of heavy metals, conferring protection against metal stress in many organisms. Here, we report that the cyanobacterial metallothionein SmtA competes with carbonate for uranyl binding, leading to formation of heterometallic (UO2)(n)Zn4SmtA species, without thiol oxidation, zinc loss, or compromising secondary or tertiary structure of SmtA. In turn, only metalated and folded SmtA species were found to be capable of uranyl binding. (1)H NMR studies and molecular modeling identified Glu34/Asp38 and Glu12/C-terminus as likely adventitious, but surprisingly strong, bidentate binding sites. While it is unlikely that these interactions correspond to an evolved biological function of this metallothionein, their occurrence may offer new possibilities for designing novel multipurpose bacterial metallothioneins with dual ability to sequester both soft metal ions including Cu(+), Zn(2+), Cd(2+), Hg(2+), and Pb(2+) and hard, high-oxidation state heavy metals such as U(VI). The concomitant protection from the chemical toxicity of uranium may be valuable for the development of bacterial strains for bio-remediation.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Unexpected Interactions of the Cyanobacterial Metallothionein SmtA with Uranium

Acharya

Blindauer

2016

Inorg. Chem.

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“…Plastin is involved in the formation of cross-linked actin filaments, which are also responsible for the structural solidity of certain cells (Shinomiya, 2012). Plastin is a protein known for binding metals including Ca and could therefore be a candidate for binding uranium (U) with a low pH of 5.2 (Bucher et al, 2016). If the alteration in plastin occurs in the presence of U, it may contribute to the structural damage previously observed in gill tissues of zebrafish (Barillet et al, 2010).…”

Section: Local Adaptation Of Shinkaia Crosnierimentioning

confidence: 99%

Population Genetic Structure and Gene Expression Plasticity of the Deep-Sea Vent and Seep Squat Lobster Shinkaia crosnieri

Xiao

Sun

et al. 2020

Front. Mar. Sci.

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“…Long exposure durations at 20 µg L -1 altered the reproduction capacity of Danio (Simon et al, 2014). Molecular effects in Danio ovaries were also observed from a 20 µg L -1 exspoure ((Bucher et al, 2016;Eb-Levadoux et al, 2017;Simon et al, 2018).…”

Section: Accepted Manuscriptmentioning

confidence: 83%

Use of fish otoliths as a temporal biomarker of field uranium exposure

Mounicou

Frelon

Guernic

et al. 2019

Science of The Total Environment

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This study aimed to determine uranium (U) pollution over time using otoliths as a marker of fish U contamination. Experiments were performed in field contamination (~20 μg L−1: encaged fish: 15d, 50d and collected wild fish) and in laboratory exposure conditions (20 and 250 μg L−1, 20d). We reported the U seasonal concentrations in field waterborne exposed roach fish (Rutilus rutilus), in organs and otoliths. Otoliths were analyzed by ICPMS and LA-ICP SF MS of the entire growth zone. Concentrations were measured on transects from nucleus to the edge of otoliths to characterize environmental variations of metal accumulation. Results showed a spatial and temporal variation of U contamination in water (from 51 to 9.4 μg L−1 at the surface of the water column), a high and seasonal accumulation in fish organs, mainly the digestive tract (from 1000 to 30,000 ng g−1, fw), the gills (from 1600 to 3200 ng g−1, fw) and the muscle (from 144 to 1054 ng g−1, fw). U was detected throughout the otolith and accumulation varied over the season from 70 to 350 ng g−1, close to the values measured (310 ng g−1) after high exposure levels in laboratory conditions. U in otoliths of encaged fish showed rapid and high U accumulation from 20 to 150 ng g−1. The U accumulation signal was mainly detected on the edge of the otolith, showing two U accumulation peaks, probably correlated to fish age, i.e. 2 years old. Surprisingly, elemental U and Zn signatures followed the same pattern therefore using the same uptake pathways. Laboratory, caging and field experiments indicated that otoliths were able to quickly accumulate U on the surface even for low levels and to store high levels of U. This study is an encouraging first step in using otoliths as a marker of U exposure. Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.

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Insights into the nature of uranium target proteins within zebrafish gills after chronic and acute waterborne exposures

Cited by 17 publications

References 27 publications

Unexpected Interactions of the Cyanobacterial Metallothionein SmtA with Uranium

Unexpected Interactions of the Cyanobacterial Metallothionein SmtA with Uranium

Population Genetic Structure and Gene Expression Plasticity of the Deep-Sea Vent and Seep Squat Lobster Shinkaia crosnieri

Use of fish otoliths as a temporal biomarker of field uranium exposure

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