Philipp Reinert, Seiryo Ogata, Laura Leiskau, Sernur Sena Yildiz, Takaaki Akaike, Uladzimir Barayeu, Marcel Deponte
Hydropersulfides have gained attention as excellent biochemical nucleophiles and membrane-protective radical scavengers. They form perthiyl radicals, which terminate radical chain reactions through self-recombination, yielding polysulfides. It is currently unknown exactly how polysulfides are subsequently reduced. Using stopped-flow kinetic measurements in combination with mass spectrometry, we show that the model class I glutaredoxin from Plasmodium falciparum (PfGrx) rapidly reduces the polysulfides glutathione trisulfide (GS3G) and tetrasulfide (GS4G), yielding glutathionylated PfGrx and the corresponding glutathione hydropersulfide (GSSH) and hydrotrisulfide (GS3H). The second-order rate constants of these reductions ≥107 M-1s-1 are even slightly higher than for glutathione disulfide (GSSG). In contrast, PfGrx was inactive or only moderately active toward cystine or cysteine trisulfide. GSSH and GS3H are further reduced by PfGrx with second-order rate constants on the order of 106-107 M-1s-1, yielding glutathionylated PfGrx and hydrogen sulfide (H2S) or hydrogen disulfide (H2S2), respectively. Thus, glutaredoxins specifically recognize the glutathione moiety of glutathione (hydro)per/polysulfides. Since reduced glutathione (GSH) rapidly reduces glutathionylated glutaredoxins, glutathione (hydro)per/polysulfides are efficiently converted to GSSG and H2S or the corresponding hydrogen polysulfides. As a consequence, the steady-state concentration of glutathione (hydro)per/polysulfides should be tightly controlled in subcellular compartments containing active glutaredoxins and high GSH concentrations.