Biomphalaria glabrata Metallothionein: Lacking Metal Specificity of the Protein and Missing Gene Upregulation Suggest Metal Sequestration by Exchange Instead of through Selective Binding

Niederwanger, Michael; Calatayud, Sara; Zerbe, Oliver; Atrian, Sı́lvia; Albalat, Ricard; Capdevila, Mercè; Palacios, Òscar; Dallinger, Reinhard

doi:10.3390/ijms18071457

Cited by 16 publications

(26 citation statements)

References 22 publications

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“…MTs expression increases in the response of variety inducers such as metals, interleukins, interferons, tumor necrosis factor alpha and glucocorticoid hormones (Subramanian et al, 2016;Dziegiel et al, 2016;Maret, 2011). MT could resist stress due to metal exposure by non-specific binding through metal exchange reactions in protein binding sites (Niederwanger et al, 2017). Moreover, high constitutive expression levels can also contribute to the tolerance of heat and cold shock by MTs genes (Gonçalves et al, 2016;Baurand et al, 2016;Salice et al, 2017).…”

Section: The Results Of Mt-2a Gene Sequencingmentioning

confidence: 99%

The Identification of Metallothionein Gene in Human Plasma: Molecular analysis of Kadmium and Lead Pollution in Gas Station Environment

Dewi

Yuniastuti

Ahmed³

2018

JPII

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Metallothionein (MTs) is a protein that binds to metals, cysteine-rich and has low molecular weights. Metallothionein binds metals and has some essential cellular functions, such as transportation, storage, and metal detoxification. When metallic lead (Pb) and cadmium (Cd) are absorbed, it will immediately be bounded by metallothionein and transported by the blood to the liver. Metallothionein gene is encoded by MTs. This study aimed to identify the MTs gene in blood of fuel station workers which can further be used as a vulnerability biomarker of the body as a result of exposure to heavy metals like Pb and Cd in humans. This study was a cross-sectional study, conducted for 8 months and took place in Fuel Stations in the city of Semarang. Samples were fuel station workers who met the study criteria, they sought to fulfill as much as 52 samples. Blood of samples was taken approximately 5 ml and then the MT2 gene was analyzed using Polymerase Chain Reaction (PCR). The data were analyzed descriptively. The results showed that 96% of MT2 gene expression had a resemblance to normal human gene sequences by Blast GenBank. MT2 gene expression did not always reflect the accumulation of lead and cadmium in the blood of fuel station workers. The MT2 gene is likely to have a limitation when used as a biomarker for early detection of the heavy metals exposure in humans to determine the susceptibility of heavy metals exposure.

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Section: The Results Of Mt-2a Gene Sequencingmentioning

confidence: 99%

The Identification of Metallothionein Gene in Human Plasma: Molecular analysis of Kadmium and Lead Pollution in Gas Station Environment

Dewi

Yuniastuti

Ahmed³

2018

JPII

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“…We compare two species of gastropods, Arion vulgaris and Biomphalaria glabrata, and their response to Cd exposure. Arion vulgaris possesses an inducible Cd-selective MT (AvMT1) [39], while the second species relies on a non-selective MT that is hardly inducible by Cd exposure [37,40]. We provide evidence that in snails, PCs are ready to take over protection against Cd impact, if the detoxification capacity of MTs becomes deficient due to lacking metal binding selectivity or oversaturation of their binding capacity.…”

Section: Introductionmentioning

confidence: 92%

“…In Table 2, Cys concentrations in MTs or PCs, expressed as molar Cys equivalents theoretically available for Cd 2+ binding, are reported. The data were calculated assuming a binding ratio of Cys: Cd 2+ of 3:1 in the Cd-selective AvMT1 of Arion vulgaris [39], 1.83:1 in the unspecific MT of Biomphalaria glabrata [40], and 2:1 in PCs [44,45]. If we consider that the unspecific MT of Biomphalaria glabrata forms, owing to its non-specific binding features for Cd 2+ , mixed metal complexes involving other metal ions like the divalent Zn 2+ and the monovalent Cu + , too [40], it must be assumed that the real availability of Cys for Cd 2+ binding in this MT may even be lower than that reported in Table 2.…”

Section: Metallothioneins Versus Phytochelatinsmentioning

confidence: 99%

“…The data were calculated assuming a binding ratio of Cys: Cd 2+ of 3:1 in the Cd-selective AvMT1 of Arion vulgaris [39], 1.83:1 in the unspecific MT of Biomphalaria glabrata [40], and 2:1 in PCs [44,45]. If we consider that the unspecific MT of Biomphalaria glabrata forms, owing to its non-specific binding features for Cd 2+ , mixed metal complexes involving other metal ions like the divalent Zn 2+ and the monovalent Cu + , too [40], it must be assumed that the real availability of Cys for Cd 2+ binding in this MT may even be lower than that reported in Table 2. Moreover, the low fraction of total Cd 2+ associated with MT in the midgut gland of Biomphalaria glabrata (see Figure 2B) shows that a considerable amount of the metal pool in this snail is kept apart from MT, and would need, if any, additional mechanisms for its detoxification.…”

Section: Metallothioneins Versus Phytochelatinsmentioning

confidence: 99%

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Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Dvorak

Schnegg

Niederwanger

et al. 2019

IJMS

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Metal detoxification is crucial for animals to cope with environmental exposure. In snails, a pivotal role in protection against cadmium (Cd) is attributed to metallothioneins (MTs). Some gastropod species express, in a lineage-specific manner, Cd-selective MTs devoted exclusively to the binding and detoxification of this single metal, whereas other species of snails possess non-selective MTs, but still show a high tolerance against Cd. An explanation for this may be that invertebrates and in particular snails may also synthetize phytochelatins (PCs), originally known to be produced by plants, to provide protection against metal or metalloid toxicity. Here we demonstrate that despite the fact that similar mechanisms for Cd inactivation exist in snail species through binding of the metal to MTs, the actual detoxification pathways for this metal may follow different traits in a species-specific manner. In particular, this depends on the detoxification capacity of MTs due to their Cd-selective or non-specific binding features. In the terrestrial slug Arion vulgaris, for example, Cd is solely detoxified by a Cd-selective MT isoform (AvMT1). In contrast, the freshwater snail Biomphalaria glabrata activates an additional pathway for metal inactivation by synthesizing phytochelatins, which compensate for the insufficient capacity of its non-selective MT system to detoxify Cd. We hypothesize that in other snails and invertebrate species, too, an alternative inactivation of the metal by PCs may occur, if their MT system is not Cd-selective enough, or its Cd loading capacity is exhausted.

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“…Namely, a high preponderance of lysine (K) over asparagine (N) residues, as observed in the two md-MTs of A. biplicata, was considered to be a typical feature of Cd-selective snail MTs (Table 1) [24,78]. In the MT of Biomphalaria glabrata, for example, the replacement of a lysine by an asparagine residue increased the Cu but not the Cd-binding capability of the respective MT protein [79]. In addition, Cd-selective snail MTs typically exhibit a higher content of charged amino acids, compared to non-metal-specific variants [24] (Table 1).…”

Section: Are Alinda Biplicata Md-mts Involved In CD Detoxification?mentioning

confidence: 99%

Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

Pedrini-Martha

Köll

Dvorak

et al. 2020

IJMS

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Terrestrial snails (Gastropoda) possess Cd-selective metallothioneins (CdMTs) that inactivate Cd2+ with high affinity. Most of these MTs are small Cysteine-rich proteins that bind 6 Cd2+ equivalents within two distinct metal-binding domains, with a binding stoichiometry of 3 Cd2+ ions per domain. Recently, unusually large, so-called multi-domain MTs (md-MTs) were discovered in the terrestrial door snail Alinda biplicata (A.b.). The aim of this study is to evaluate the ability of A.b. to cope with Cd stress and the potential involvement of md-MTs in its detoxification. Snails were exposed to increasing Cd concentrations, and Cd-tissue concentrations were quantified. The gene structure of two md-MTs (9md-MT and 10md-MT) was characterized, and the impact of Cd exposure on MT gene transcription was quantified via qRT PCR. A.b. efficiently accumulates Cd at moderately elevated concentrations in the feed, but avoids food uptake at excessively high Cd levels. The structure and expression of the long md-MT genes of A.b. were characterized. Although both genes are intronless, they are still transcribed, being significantly upregulated upon Cd exposure. Overall, our results contribute new knowledge regarding the metal handling of Alinda biplicata in particular, and the potential role of md-MTs in Cd detoxification of terrestrial snails, in general.

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Biomphalaria glabrata Metallothionein: Lacking Metal Specificity of the Protein and Missing Gene Upregulation Suggest Metal Sequestration by Exchange Instead of through Selective Binding

Cited by 16 publications

References 22 publications

The Identification of Metallothionein Gene in Human Plasma: Molecular analysis of Kadmium and Lead Pollution in Gas Station Environment

The Identification of Metallothionein Gene in Human Plasma: Molecular analysis of Kadmium and Lead Pollution in Gas Station Environment

Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

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