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As with all protein tyrosine phosphatases, the activity of PTPN22 is redox regulated, but if or how such regulation can modulate inflammatory pathways in vivo is not known. To determine this, we created a mouse with a cysteine-to-serine mutation at position 129 in PTPN22 (C129S), a residue proposed to alter the redox regulatory properties of PTPN22 by forming a disulfide with the catalytic C227 residue. The C129S mutant mouse showed a stronger T-cell-dependent inflammatory response and development of T-cell-dependent autoimmune arthritis due to enhanced TCR signaling and activation of T cells, an effect neutralized by a mutation in Ncf1, a component of the NOX2 complex. Activity assays with purified proteins suggest that the functional results can be explained by an increased sensitivity to oxidation of the C129S mutated PTPN22 protein. We also observed that the disulfide of native PTPN22 can be directly reduced by the thioredoxin system, while the C129S mutant lacking this disulfide was less amenable to reductive reactivation. In conclusion, we show that PTPN22 functionally interacts with Ncf1 and is regulated by oxidation via the noncatalytic C129 residue and oxidation-prone PTPN22 leads to increased severity in the development of T-cell-dependent autoimmunity.<\/jats:p>","DOI":"10.7554\/elife.74549","type":"journal-article","created":{"date-parts":[[2022,3,24]],"date-time":"2022-03-24T17:15:36Z","timestamp":1648142136000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.74549","source":"Crossref","is-referenced-by-count":26,"title":["Redox regulation of PTPN22 affects the severity of T-cell-dependent autoimmune inflammation"],"prefix":"10.7554","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3732-8838","authenticated-orcid":true,"given":"Jaime","family":"James","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/056d84691","id-type":"ROR","asserted-by":"publisher"}],"name":"Division of Medical Inflammation Research, Department of Medical Biochemistry and Biophysics, 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