The Impact of Nitric Oxide Toxicity on the Evolution of the Glutathione Transferase Superfamily

Bocedi, Alessio; Fabrini, Raffaele; Farrotti, Andrea; Stella, Lorenzo; Ketterman, Albert J.; Pedersen, Jens Z.; Allocati, Nerino; Lau, Peter C. K.; Große, Stephan; Eltis, Lindsay D.; Ruzzini, Antonio C.; Edwards, Thomas E.; Morici, Laura; Grosso, Erica Del; Guidoni, Leonardo; Bovi, Daniele; Bello, Mario Lo; Federici, Giorgio; Parker, Michael W.; Board, Philip G.; Ricci, Giorgio

doi:10.1074/jbc.m113.476135

Cited by 32 publications

(44 citation statements)

References 63 publications

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“…tyrosine, serine, or cysteine that complete the coordination shell of the ferrous ion (27). By testing 39 different GSTs, we also found that the Cys-GSTs, which are close to the ancestral GST protein, have thousands of times lower affinity for DNDGIC than the Tyr-GSTs and Ser-GSTs (23). Thus, protection of the cell against NO by means of GSTs was proposed to recently have been acquired during evolution.…”

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confidence: 82%

“…The peculiar affinities of these two variants toward DNDGIC and their expression and localization inside the cell suggest some possible comments. In fact, GSTA1-1 and GSTA3-3 display the highest affinity, showing 20 times higher affinity for DNDGIC (ϳ8 ϫ 10 Ϫ11 M) than all other Mu and Pi variants (1.5 ϫ 10 Ϫ9 M) (23). The complete loss of activity after the half-of-the-sites binding of DNDGIC seems to be the price that needs to be paid by these GSTs for assuming the role of interceptors toward DNDGIC.…”

Section: Journal Of Biological Chemistry 26741mentioning

confidence: 99%

“…Purified GSTs-Human GSTP1-1, human GSTA1-1, human GSTA2-2, human GSTA3-3, human GSTM2-2, O. volvulus GST2, S. haematobium GST, L. cuprina GSTc, Anopheles dirus GSTD3-3, A. dirus GSTD4-4, A. dirus GSTD5-5, human GSTT2-2, Ochrobactrum anthropi GST, Burkholderia xenovorans GST, Sphingomonas paucimobilis GST, and Proteus mirabilis GST, all except L. cuprina GST (M. W. Parker, personal gift), were expressed and purified as described previously (23).…”

Section: Methodsmentioning

confidence: 99%

“…Thus, protection of the cell against NO by means of GSTs was proposed to recently have been acquired during evolution. Interestingly, Cys-GSTs are the only known GSTs expressed by bacteria, and their low affinity for DNDGIC has been related to the sensitivity of these organisms to nitrosylative stress (23). Notwithstanding the beneficial effects of the DNDGIC sequestration by GSTs, a likely disadvantage is that these enzymes, when saturated reversibly by this complex, become catalytically inactive and lose their ability to conjugate GSH to many other toxins.…”

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confidence: 99%

“…1A) formed sponta-neously when an excess of nitric oxide is produced in the cell (23). By sequestering free iron and NO, this complex may counteract both oxidative and nitrosylative stress.…”

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confidence: 99%

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Evolution of Negative Cooperativity in Glutathione Transferase Enabled Preservation of Enzyme Function

Bocedi¹,

Fabrini²,

Bello³

et al. 2016

Journal of Biological Chemistry

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Edited by Norma AllewellNegative cooperativity in enzyme reactions, in which the first event makes subsequent events less favorable, is sometimes well understood at the molecular level, but its physiological role has often been obscure. Negative cooperativity occurs in human glutathione transferase (GST) GSTP1-1 when it binds and neutralizes a toxic nitric oxide adduct, the dinitrosyl-diglutathionyl iron complex (DNDGIC). However, the generality of this behavior across the divergent GST family and its evolutionary significance were unclear. To investigate, we studied 16 different GSTs, revealing that negative cooperativity is present only in more recently evolved GSTs, indicating evolutionary drift in this direction. In some variants, Hill coefficients were close to 0.5, the highest degree of negative cooperativity commonly observed (although smaller values of n H are theoretically possible). As DNDGIC is also a strong inhibitor of GSTs, we suggest negative cooperativity might have evolved to maintain a residual conjugating activity of GST against toxins even in the presence of high DNDGIC concentrations. Interestingly, two human isoenzymes that play a special protective role, safeguarding DNA from DNDGIC, display a classical half-of-the-sites interaction. Analysis of GST structures identified elements that could play a role in negative cooperativity in GSTs. Beside the well known lock-and-key and clasp motifs, other alternative structural interactions between subunits may be proposed for a few GSTs. Taken together, our findings suggest the evolution of self-preservation of enzyme function as a novel facility emerging from negative cooperativity.

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confidence: 82%

Section: Journal Of Biological Chemistry 26741mentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Evolution of Negative Cooperativity in Glutathione Transferase Enabled Preservation of Enzyme Function

Bocedi¹,

Fabrini²,

Bello³

et al. 2016

Journal of Biological Chemistry

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Two delta class glutathione S‐transferases involved in the detoxification of malathion in Bactrocera dorsalis (Hendel)

Meng

Yuan

et al. 2019

Pest Management Science

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BACKGROUND The oriental fruit fly Bactrocera dorsalis (Hendel), a widespread agricultural pest, has evolved resistance to many insecticides, including organophosphorus compounds. Glutathione S‐transferases (GSTs) are involved in xenobiotic detoxification and insecticide resistance in many insects. However, the role of delta class GSTs in detoxifying malathion in B. dorsalis is unknown. Here, we evaluated the roles of two delta class GSTs in malathion detoxification in this species. RESULTS Two delta class GSTs genes, BdGSTd1 and BdGSTd10, were characterized in B. dorsalis. They were highly expressed in 5‐day‐old adults, as well as in midgut and Malpighian tubules. Upon malathion exposure, the two genes were upregulated by 2.63‐ and 2.85‐fold, respectively. Injection of double‐stranded RNA targeting BdGSTd1 or BdGSTd10 significantly reduced their mRNA levels in adults and also significantly increased adult susceptibility to malathion. The expression of these two GSTs in Escherichia coli helped the host to endure malathion stress at a concentration of 10 µg mL−1 according to a Cell Counting Kit‐8 assay. High‐performance liquid chromatography analyses indicated that malathion could be significantly depleted by the two delta GSTs. The role of BdGSTd10 in malathion sequestration was also discussed. CONCLUSION BdGSTd1 and BdGSTd10 play important roles in the detoxification of malathion in B. dorsalis. © 2019 Society of Chemical Industry

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Erythrocyte Glutathione Transferase as a Biomarker in Kidney Health and Disease

Bocedi

Noce

Fabrini

et al. 2016

Biomarkers in Kidney Disease

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The Impact of Nitric Oxide Toxicity on the Evolution of the Glutathione Transferase Superfamily

Cited by 32 publications

References 63 publications

Evolution of Negative Cooperativity in Glutathione Transferase Enabled Preservation of Enzyme Function

Evolution of Negative Cooperativity in Glutathione Transferase Enabled Preservation of Enzyme Function

Two delta class glutathione S‐transferases involved in the detoxification of malathion in Bactrocera dorsalis (Hendel)

Erythrocyte Glutathione Transferase as a Biomarker in Kidney Health and Disease

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