S-Nitrosation of Arabidopsis thaliana Protein Tyrosine Phosphatase 1 Prevents Its Irreversible Oxidation by Hydrogen Peroxide

Valérie Nicolas-Francès; Jordan Rossi; Claire Rosnoblet; Carole Pichereaux; Siham Hichami; Jeremy Astier; Agnès Klinguer; David Wendehenne; Angélique Besson-Bard

doi:10.3389/fpls.2022.807249

S-Nitrosation of Arabidopsis thaliana Protein Tyrosine Phosphatase 1 Prevents Its Irreversible Oxidation by Hydrogen Peroxide

Front Plant Sci. 2022 Feb 11:13:807249. doi: 10.3389/fpls.2022.807249. eCollection 2022.

Authors

Valérie Nicolas-Francès¹, Jordan Rossi¹, Claire Rosnoblet¹, Carole Pichereaux^{2

3}, Siham Hichami¹, Jeremy Astier¹, Agnès Klinguer¹, David Wendehenne¹, Angélique Besson-Bard¹

Affiliations

¹ Agroécologie, CNRS, INRAE, Institut Agro, Université de Bourgogne, Université Bourgogne Franche-Comté, Dijon, France.
² Fédération de Recherche (FR3450), Agrobiosciences, Interactions et Biodiversité (FRAIB), CNRS, Toulouse, France.
³ Institut de Pharmacologie et de Biologie Structurale (IPBS), Université de Toulouse UPS, CNRS, Toulouse, France.

Abstract

Tyrosine-specific protein tyrosine phosphatases (Tyr-specific PTPases) are key signaling enzymes catalyzing the removal of the phosphate group from phosphorylated tyrosine residues on target proteins. This post-translational modification notably allows the regulation of mitogen-activated protein kinase (MAPK) cascades during defense reactions. Arabidopsis thaliana protein tyrosine phosphatase 1 (AtPTP1), the only Tyr-specific PTPase present in this plant, acts as a repressor of H₂O₂ production and regulates the activity of MPK3/MPK6 MAPKs by direct dephosphorylation. Here, we report that recombinant histidine (His)-AtPTP1 protein activity is directly inhibited by H₂O₂ and nitric oxide (NO) exogenous treatments. The effects of NO are exerted by S-nitrosation, i.e., the formation of a covalent bond between NO and a reduced cysteine residue. This post-translational modification targets the catalytic cysteine C265 and could protect the AtPTP1 protein from its irreversible oxidation by H₂O₂. This mechanism of protection could be a conserved mechanism in plant PTPases.

Keywords: Arabidopsis thaliana; H2O2; S-nitrosation; mitogen-activated protein kinases; nitric oxide; oxidation; post-translational modifications; protein tyrosine phosphatase 1.