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@ARTICLE{Lakshmi:307321,
author = {K. Lakshmi and A. v. Jutrzenka-Trzebiatowski and L.
Loureiro and K. E. G. Soto and K. Peter and J. M. M. Morales
and S. S. Nirmala and N. Berndt and C. Arndt and Y. Hu and
J.-W. Li and C. Peitzsch and A. Taubenberger and R.
Wehner$^*$ and M. Schmitz$^*$ and K. Hölig and H. Abken and
E. Bonifacio and M. Bornhäuser$^*$ and M. Bachmann$^*$ and
A. Feldmann$^*$ and A. Fuchs$^*$},
title = {{A}utomated {GMP}-compatible production of universal {CAR}
{T}regs for organ-targeted tolerance induction.},
journal = {Journal of translational medicine},
volume = {23},
number = {1},
issn = {1479-5876},
address = {London},
publisher = {BioMed Central},
reportid = {DKFZ-2025-03007},
pages = {1399},
year = {2025},
abstract = {Adoptive transfer of regulatory T cells (Tregs) has
demonstrated safety, feasibility and early signs of efficacy
in promoting immunological tolerance in inflammatory
conditions such as graft-versus-host disease (GvHD).
Chimeric antigen receptor (CAR)-engineered Tregs offer
localized activation and suppression compared to polyclonal
Tregs, but their clinical translation is limited by high
manufacturing costs, lengthy developing times and fixed
single-antigen specificity. To address these limitations, we
employed the universal adapter Reverse CAR (RevCAR) system,
which harbors a peptide epitope lacking intrinsic antigen
specificity but provides flexibility in targeting through
the use of an antigen-specific RevCAR Target Module (RevTM).
As a proof-of-concept, we used a RevTM targeting
carcinoembryonic antigen (CEA), which is highly expressed in
the gastrointestinal (GI) tract, as a potential strategy to
achieve localized immunosuppression in GI acute GvHD.To
support clinical translation, we established an automated,
GMP-compatible, clinical-scale manufacturing process. Tregs
were magnetically enriched from leukapheresis using the
CliniMACS® Plus, followed by high-purity sorting on the
MACSQuant® Tyto®. The sorted cells were virally transduced
and the RevCAR Tregs were expanded on the CliniMACS
Prodigy® to obtain clinically relevant cell numbers. The
harvested products were evaluated for phenotype, stability,
antigen specificity and suppressive function.Across five
manufacturing runs, Tregs (CD4+CD25highCD127lowFOXP3+) with
a median initial purity of $94\%$ were expanded to achieve a
median therapeutic yield of 602 × 106 cells. The final
product maintained a high purity (median: $91.9\%)$ and
exhibited high RevCAR expression (median: $60\%$ RevCAR+).
Mass cytometry analysis revealed that expanded RevCAR Tregs
predominantly exhibited a central memory phenotype with high
expression of functional and homing markers. Under
experimental pro-inflammatory conditions, the cells
maintained stable FOXP3 and Helios expression with minimal
pro-inflammatory cytokine production. Importantly, RevCAR
Tregs showed antigen-specific activation upon target
engagement via the CEA-specific RevTM and robust,
dose-dependent suppression.The study establishes a scalable,
GMP-compatible process for manufacturing pure, stable and
functional universal RevCAR Tregs for clinical applications.
Furthermore, the RevCAR system offers a promising approach
toward an allogenic, off-the-shelf Treg therapy capable of
treating diverse immune-mediated diseases with spatial
precision.},
keywords = {T-Lymphocytes, Regulatory: immunology / T-Lymphocytes,
Regulatory: cytology / Humans / Receptors, Chimeric Antigen:
metabolism / Immune Tolerance: immunology / Automation /
Organ Specificity / Carcinoembryonic Antigen: metabolism /
Carcinoembryonic Antigen: immunology / Graft vs Host
Disease: immunology / Automated expansion (Other) /
Closed-system manufacturing (Other) / Good manufacturing
practice (Other) / Precision immunotherapy (Other) /
Regulatory T cells (Other) / Treg cell therapy (Other) /
Universal adapter CAR (Other) / Receptors, Chimeric Antigen
(NLM Chemicals) / Carcinoembryonic Antigen (NLM Chemicals)},
cin = {DD01},
ddc = {610},
cid = {I:(DE-He78)DD01-20160331},
pnm = {899 - ohne Topic (POF4-899)},
pid = {G:(DE-HGF)POF4-899},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:41408297},
doi = {10.1186/s12967-025-07431-0},
url = {https://inrepo02.dkfz.de/record/307321},
}