Tributyltin inhibits the oligomycin-sensitive Mg-ATPase activity in Mytilus galloprovincialis digestive gland mitochondria

Ventrella, Vittoria; Nesci, Salvatore; Trombetti, Fabiana; Bandiera, Patrizia; Pirini, Maurizio; Borgatti, Anna; Pagliarani, Alessandra

doi:10.1016/j.cbpc.2010.08.007

Cited by 18 publications

(36 citation statements)

References 49 publications

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“…On this basis, the observed gill oligomycin-sensitive Mg-ATPase activation, in contrast with the enzyme inhibition registered in the digestive gland [6], can be explained on considering other parameters showing a different trend in the gills and in the digestive gland from experimental mussels. On this basis, the observed gill oligomycin-sensitive Mg-ATPase activation, in contrast with the enzyme inhibition registered in the digestive gland [6], can be explained on considering other parameters showing a different trend in the gills and in the digestive gland from experimental mussels.…”

Section: Discussionmentioning

confidence: 87%

“…The other chromatographic conditions were reported previously [6]. The resulting preparation was centrifuged at 600 g for 5 min, and 1.5-ml aliquots of the supernatant were placed in 10-ml auto-SPME sample vials (Supelco) crimped with aluminum caps containing Teflon-lined septa.…”

Section: Organotin Analysesmentioning

confidence: 99%

“…The total Mg-ATPase activity was determined by subtracting from the Pi hydrolyzed by known amounts of mitochondrial protein, the Pi hydrolyzed by the spontaneous nonenzymatic ATP breakdown. Because TBT in vitro added to mussel mitochondria at higher than 1.0 mM significantly increased the oligomycininsensitive Mg-ATPase fraction [6,7], the oligomycin-sensitive and oligomycin-insensitive Mg-ATPases were considered separately. The oligomycin-sensitive Mg-ATPase was measured as the difference between the Pi hydrolyzed in the absence of oligomycin and that hydrolyzed in the presence of 4 mg/ml oligomycin.…”

Section: Assay Of Mg-atpase Activitiesmentioning

confidence: 99%

“…Among the ascertained mitochondrial TBT targets-which span from the inner membrane integrity [4] to the occurrence of protein binding sites, allowing covalent interactions between tin and electron donor atoms such as sulfur-the F 0 F 1 -adenosine triphosphatase (ATPase), the key complex of energy metabolism, has been repeatedly pointed out as TBT susceptible, because severe inhibition of ATPase catalytic activity has been reported in mammalian, yeast, and mussel mitochondria [5][6][7]. Among the ascertained mitochondrial TBT targets-which span from the inner membrane integrity [4] to the occurrence of protein binding sites, allowing covalent interactions between tin and electron donor atoms such as sulfur-the F 0 F 1 -adenosine triphosphatase (ATPase), the key complex of energy metabolism, has been repeatedly pointed out as TBT susceptible, because severe inhibition of ATPase catalytic activity has been reported in mammalian, yeast, and mussel mitochondria [5][6][7].…”

Section: Introductionmentioning

confidence: 99%

“…With the aim of depicting an overall pattern of TBT effects on mussel mitochondria, or at least of obtaining useful data on this subject, the present investigation shares M. galloprovincialis specimens and exposure trials with a parallel work focused on TBT effects on digestive gland mitochondria and detailed in a previously published paper [6]. In our opinion, such a choice may facilitate the comparison between the response of mitochondria from the gills and the digestive gland by preventing possible overlapping differentiating factors.…”

Section: Introductionmentioning

confidence: 99%

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Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Fiorini¹,

Pagliarani²,

Nesci³

et al. 2012

Enviro Toxic and Chemistry

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The use of tributyltin (TBT) as a biocide in antifouling paints leads to a ruinous input of this contaminant in the aquatic environment. Human exposure to TBT mainly occurs through ingestion of contaminated seafood such as filter-feeding mollusks. Tributyltin is known to act as a membrane-active toxicant on several targets, but especially on the mitochondria, and by several mechanisms. The effects of tributyltin on fatty acid composition, on Mg-adenosine triphosphatase (ATPase) activities, and on the membrane physical state were investigated in gill mitochondrial membranes from cultivated mussels Mytilus galloprovincialis exposed to 0.5 µg/L and 1.0 µg/L TBT and unexposed for 120 h. The higher TBT exposure dose induced a decrease in the total and n-3 polyunsaturated fatty acids (PUFAs), especially 22:6 n-3, and an activation of the oligomycin-sensitive Mg-ATPase. Both TBT concentrations decreased mitochondrial membrane polarity detected by Laurdan steady-state fluorescence spectroscopy. These findings may help cast light on the multiple modes of action of this toxicant.

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Section: Discussionmentioning

confidence: 87%

Section: Organotin Analysesmentioning

confidence: 99%

Section: Assay Of Mg-atpase Activitiesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Fiorini¹,

Pagliarani²,

Nesci³

et al. 2012

Enviro Toxic and Chemistry

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Tri‐n‐butyltin binding to a low‐affinity site decreases the F₁F_O‐ATPase sensitivity to oligomycin in mussel mitochondria

Nesci

Ventrella

Trombetti

et al. 2012

Applied Organom Chemis

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In mussel digestive gland mitochondria the environmental pollutant tri‐n‐butyltin (TBT), other than strongly inhibiting ATPase activity at <1.0 μ m, at ≥1.0 μ m concentration was previously found to desensitize F1FO‐ATPase to the antibiotic oligomycin. While F1FO‐ATPase inhibition is widely known as one of the main mitochondrial damages caused by TBT, the enzyme's desensitization to oligomycin was quite unexpected. The possible mechanisms involved are here stepwise approached, aiming at enlightening the molecular mechanism(s) of TBT toxicity and the still poorly investigated oligomycin interaction with FO. The findings strongly suggest that the oligomycin desensitization directly stems from the covalent binding of TBT to monothiols of the F1FO‐ATPase. This binding implies sulfur oxidation, irrespective of the possible formation of radical species in mitochondria, a mechanism which does not seem to be involved here. It is hypothesized that TBT interacts with the enzyme complex in at least two sites distinguished by different affinities: TBT binding to the high‐affinity site would lead to ATPase inhibition, while TBT binding to monothiols in the low‐affinity site could mirror the decrease in F1FO‐ATPase oligomycin sensitivity at ≥1.0 μ m TBT. Experiments carried out on inside‐out submitochondrial particles hint that TBT binding destabilizes the oligomycin‐blocked FO conformation, allowing proton flux recovery within FO, without uncoupling the catalytic function from proton channeling. Copyright © 2012 John Wiley & Sons, Ltd.

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Modulation of the F₁F_O‐ATPase function by butyltin compounds

Nesci

Ventrella

Pagliarani

2013

Applied Organom Chemis

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Among butyltin compounds, tributyltin (TBT), widely exploited in the past in antifouling paints for its biocidal properties, is long known as one of the most harmful sea contaminants. Among the ascertained and universal toxicity mechanisms, TBT targeting F1FO‐ATPase and thus impairing cell bioenergetics, is here reviewed. While TBT effects on F1FO‐ATPase have been investigated for decades, the possible impact of the derivatives dibutyltin (DBT) and monobutyltin (MBT), produced by abiotic and/or biotic dealkylation of TBT and usually considered far less toxic, have been poorly explored up until now. Butyltin effects on F1FO‐ATPase and their underlying action mechanism seem to be tightly structure dependent. Butyltins are membrane‐active toxicants. Owing to its more pronounced lipophilicity TBT targets the transmembrane FO sector, blocks ionic translocation and causes a dose‐dependent loss of sensitivity to FO inhibitors such as oligomycin and N,N′‐dicyclohexylcarbodiimide. DBT strongly inhibits F1FO‐ATPase activity by competing with the Mg+2 cofactor in the F1 catalytic site but is ineffective on the enzyme sensitivity to FO inhibitors. MBT is apparently ineffective. The possible contribution of DBT to the overall butyltin toxicity on membrane systems may not be neglectable since usually TBT coexists with its derivatives in organotin‐exposed animal tissues. Copyright © 2013 John Wiley & Sons, Ltd.

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Tributyltin inhibits the oligomycin-sensitive Mg-ATPase activity in Mytilus galloprovincialis digestive gland mitochondria

Cited by 18 publications

References 49 publications

Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Tri‐n‐butyltin binding to a low‐affinity site decreases the F₁F_O‐ATPase sensitivity to oligomycin in mussel mitochondria

Modulation of the F₁F_O‐ATPase function by butyltin compounds

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Tributyltin inhibits the oligomycin-sensitive Mg-ATPase activity in Mytilus galloprovincialis digestive gland mitochondria

Cited by 18 publications

References 49 publications

Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri‐n‐butyltin

Tri‐n‐butyltin binding to a low‐affinity site decreases the F1FO‐ATPase sensitivity to oligomycin in mussel mitochondria

Modulation of the F1FO‐ATPase function by butyltin compounds

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Tri‐n‐butyltin binding to a low‐affinity site decreases the F₁F_O‐ATPase sensitivity to oligomycin in mussel mitochondria

Modulation of the F₁F_O‐ATPase function by butyltin compounds