Plant catalases as NO and H2S targets

Abstract

Catalase is a powerful antioxidant metalloenzyme located in peroxisomes which also plays a central role in signaling processes under physiological and adverse situations. Whereas animals contain a single catalase gene, in plants this enzyme is encoded by a multigene family providing multiple isoenzymes whose number varies depending on the species, and their expression is regulated according to their tissue/organ distribution and the environmental conditions. This enzyme can be modulated by reactive oxygen and nitrogen species (ROS/RNS) as well as by hydrogen sulfide (H₂S). Catalase is the major protein undergoing Tyr-nitration [post-translational modification (PTM) promoted by RNS] during fruit ripening, but the enzyme from diverse sources is also susceptible to undergo other activity-modifying PTMs. Data on S-nitrosation and persulfidation of catalase from different plant origins are given and compared here with results from obese children where S-nitrosation of catalase occurs. The cysteine residues prone to be S-nitrosated in catalase from plants and from bovine liver have been identified. These evidences assign to peroxisomes a crucial statement in the signaling crossroads among relevant molecules (NO and H₂S), since catalase is allocated in these organelles. This review depicts a scenario where the regulation of catalase through PTMs, especially S-nitrosation and persulfidation, is highlighted.

Keywords: Docking; Nitration; Persulfidation; Post-translational modifications; S-nitrosation; Signaling.

Graphical abstract

Fig 1

Analysis of Arabidopsis thaliana catalase activity in the presence of different concentrations of S-nitrosoglutathione (GSNO). Aliquots of Arabidopsis leaf samples were pre-incubated before activity assay at 25 °C for 45 min in the presence of 2 mM GSNO (nitric oxide donor). The catalase specific activity of the untreated samples was 50.1 μmol H₂O₂ · min⁻¹ · mg⁻¹ protein. The remaining catalase activity (expressed as %) after the treatment was plotted. Catalase activity was determined according to Ref. [1]. Results are the mean of at least three biological replicates (with triplicate assays each) ± SEM. ∗Differences in relation to control values were significant at P < 0.05.

Fig. 2

Blind docking of GSNO to Arabidopsis thaliana catalase. Poses of the docking of GSNO on catalase isozymes from A. thaliana near to Cys (sulfur atom in yellow), showing the predicted Kd calculated from the estimated ΔG of the interaction and the distance with the sulfur atom from GSNO. The surface of the protein is colored as a function of the Kyte-Doolittle scale. Colors range from dodger blue to white for the most hydrophilic and to orange-red for the most hydrophobic. Residues involved in the interaction with GSNO are listed on the right side of each image.

Fig. 3

Erythrocyte catalase in healthy and obese children. The enzyme activity (A), protein expression (B) and nitrosation modification (C) were analyzed after an overnight fast in red blood cells of healthy (white bars) and obese (black bars) children. Catalase activity was determined according to Ref. [1]. Values represent means ± SEM. *P < 0.05. SDS was performed in 12% acrylamide gels. Antibodies used were Anti-CAT XP® (Cell Signaling) and Anti-β-actin (Abcam). For detection of nitrosated catalase (catalase-SNO), the biotin-switch method for nitrosthiols groups (SNO) was followed. Data from biotin-switch were quantified by the ImageJ programme.