Language

English

Publication Date

7-1-2025

Journal

Kidney International

DOI

10.1016/j.kint.2025.03.020

PMID

40268165

Abstract

Introduction: Proteinase 3 (PR3) is a major autoantigen in patients with anti-neutrophil cytoplasmic autoantibody (ANCA)-associated vasculitis (AAV). Here, we performed a proof-of-principle study using ex vivo CRISPR-Cas9 guided gene editing to eliminate the PR3 autoantigen as an alternative to suppressing the autoimmune response to PR3.

Methods: A ribonucleoprotein (RNP) complex of Cas9 protein and a PR3-specific single guide-RNA was transfected into human CD34+ hematopoietic stem and progenitor cells (HSPC) by electroporation. Effects on PR3 protein abundance, neutrophil differentiation, and ANCA-dependent and -independent neutrophil responses were assessed.

Results: Gene editing introduced a frame shift in exon 2 of PRTN3. Consequently, PR3 protein was efficiently reduced in neutrophil-differentiated HSPCs as demonstrated by immunoblotting, ELISA, microscopy, and the complete absence of PR3-specific proteolytic activity. Human neutrophil elastase served as control and was not affected. PR3-deleted (PR3KO)- and PR3 wild-type (PR3WT)-HSPCs showed similar neutrophil differentiation. Importantly, general neutrophil defense functions to non-ANCA receptor-independent and -dependent stimuli were similar in PR3KO- and PR3WT-neutrophils as was constitutive apoptosis. Flow cytometry showed that cell membrane-PR3 was significantly reduced on PR3KO-neutrophils and consequent neutrophil activation to either monoclonal antibodies to PR3 or human PR3-ANCA was attenuated. In contrast, myeloperoxidase-ANCA stimulation was not affected.

Conclusions: We show the feasibility and efficacy of depleting the PR3 autoantigen in human CD34+ HSPCs using CRISPR-Cas9. Depleting the PR3 autoantigen instead of suppressing the autoimmune response to PR3 could potentially lead to drug-free remission, particularly in patients with refractory or relapsing disease.

Keywords

Humans, Myeloblastin, CRISPR-Cas Systems, Autoantigens, Neutrophils, Gene Editing, Anti-Neutrophil Cytoplasmic Antibody-Associated Vasculitis, Hematopoietic Stem Cells, Cell Differentiation, Proof of Concept Study, Antibodies, Antineutrophil Cytoplasmic, RNA, Guide, CRISPR-Cas Systems, Cells, Cultured, Genetic Therapy, Leukocyte Elastase, ANCA vasculitis, CRISPR-Cas9, autoimmunity, gene editing, proteinase 3

Published Open-Access

yes

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