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Mitochondrial DNA oxidation propagates autoimmunity by enabling plasmacytoid dendritic cells induce Tfh differentiation

Title: Mitochondrial DNA oxidation propagates autoimmunity by enabling plasmacytoid dendritic cells induce Tfh differentiation
Authors: Karin, Michael; Xian, Hongxu; Ohira, Masafumi; Watari, Kosuke; Brito, Jonathan; Onyuru, Janset; Zuniga, Elina; Hoffman, Hal
Publisher Information: Springer Science and Business Media LLC
Publication Year: 2024
Description: NLRP3 inflammasome activation depends on stress-induced production of oxidized mitochondrial DNA (Ox-mtDNA) fragments that enter the cytoplasm to bind NLRP3 and activate caspase-1. Along with pro-IL-1β processing, caspase-1 generates gasdermin D pores that result in circulatory mtDNA release. Elevated amounts of circulating cell-free (ccf)-mtDNA, which is likely to be oxidized, were documented in the elderly and patients with metabolic and autoimmune disorders and its intra-articular injection elicited arthritis in mice. Investigating whether ccf-mtDNA may promote autoimmunity, we found that induction of sustained Ox-mtDNA release triggered by a prototypical NLRP3 inflammasome activator elicited autoantibody production and glomerulonephritis in mice. Similar autoimmune responses, dependent on plasmacytoid dendritic cells (pDC) and T follicular helper cells (Tfh), were elicited by in-vitro generated Ox-mtDNA but not by non-oxidized mtDNA. Although both mtDNA forms were internalized by pDC and induced interferon-a, only Ox-mtDNA stimulated autocrine IL-1β signaling that induced expression of immunoregulatory and co-stimulatory molecules, including IL-21, that enabled mouse and human pDC convert naïve CD4 + T cells into functional Tfh, supportive of autoantibody production. Highlighting pDC-generated IL-1β as an orchestrator of autoantibody production, these findings suggest that Ox-mtDNA could be a key participant in immune-aging and unravel new therapeutic opportunities.
Document Type: other/unknown material
Language: unknown
DOI: 10.21203/rs.3.rs-5194985/v1
Availability: https://doi.org/10.21203/rs.3.rs-5194985/v1; https://www.researchsquare.com/article/rs-5194985/v1; https://www.researchsquare.com/article/rs-5194985/v1.html
Rights: https://creativecommons.org/licenses/by/4.0/
Accession Number: edsbas.A7DBA110
Database: BASE