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Gene\u2013gene interaction between certain HLA class I risk alleles and variants of the endoplasmic reticulum aminopeptidase ERAP1 controls the risk for common immune-mediated diseases, including psoriasis, ankylosing spondylitis, and Beh\u00e7et disease. The functional mechanisms underlying this statistical association are unknown. In psoriasis, HLA-C*06:02 mediates an autoimmune response against melanocytes by autoantigen presentation. Using various genetically modified cell lines together with an autoreactive psoriatic TCR in a TCR activation assay, we demonstrate in this study that in psoriasis, ERAP1 generates the causative melanocyte autoantigen through trimming N-terminal elongated peptide precursors to the appropriate length for presentation by HLA-C*06:02. An ERAP1 risk haplotype for psoriasis produced the autoantigen much more efficiently and increased HLA-C expression and stimulation of the psoriatic TCR by melanocytes significantly more than a protective haplotype. Compared with the overall HLA class I molecules, cell surface expression of HLA-C decreased significantly more upon ERAP1 knockout. The combined upregulation of ERAP1 and HLA-C on melanocytes in psoriasis lesions emphasizes the pathogenic relevance of their interaction in patients. We conclude that in psoriasis pathogenesis, the increased generation of an ERAP1-dependent autoantigen by an ERAP1 risk haplotype enhances the likelihood that autoantigen presentation by HLA-C*06:02 will exceed the threshold for activation of potentially autoreactive T cells, thereby triggering CD8+ T cell\u2013mediated autoimmune disease. These data identify ERAP1 function as a central checkpoint and promising therapeutic target in psoriasis and possibly other HLA class I\u2013associated diseases with a similar genetic predisposition.<\/jats:p>","DOI":"10.4049\/jimmunol.2100686","type":"journal-article","created":{"date-parts":[[2021,9,27]],"date-time":"2021-09-27T12:21:14Z","timestamp":1632745274000},"page":"2235-2244","source":"Crossref","is-referenced-by-count":59,"title":["ERAP1 Controls the Autoimmune Response against Melanocytes in Psoriasis by Generating the Melanocyte Autoantigen and Regulating Its Amount for HLA-C*06:02 Presentation"],"prefix":"10.1093","volume":"207","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6679-3029","authenticated-orcid":false,"given":"Akiko","family":"Arakawa","sequence":"first","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emma","family":"Reeves","sequence":"additional","affiliation":[{"name":"Centre for Cancer Immunology, University Hospital Southampton , Southampton ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sigrid","family":"Vollmer","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4249-6393","authenticated-orcid":false,"given":"Yukiyasu","family":"Arakawa","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1891-6506","authenticated-orcid":false,"given":"Mengwen","family":"He","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrian","family":"Galinski","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia","family":"St\u00f6hr","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klaus","family":"Dornmair","sequence":"additional","affiliation":[{"name":"Institute of Clinical Neuroimmunology, Biomedical Center and University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edward","family":"James","sequence":"additional","affiliation":[{"name":"Centre for Cancer Immunology, University Hospital Southampton , Southampton ,","place":["United Kingdom"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8857-5495","authenticated-orcid":false,"given":"J\u00f6rg C","family":"Prinz","sequence":"additional","affiliation":[{"name":"Department of Dermatology and Allergy, University Hospital, Ludwig-Maximilian-University Munich , Munich ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,11,1]]},"reference":[{"key":"2025022610322098000_r1","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1038\/ni.3731","article-title":"The multiple pathways to autoimmunity","volume":"18","author":"Theofilopoulos","year":"2017","journal-title":"Nat. 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