From:  Epigenetic and metabolic reprogramming in autoimmune rheumatology: toward immune tolerance reprogramming

 Therapeutic classes, development stage, and translational limitations in tolerance reprogramming.

ModalityTarget pathway (metabolic/epigenetic/cellular)Mechanism of tolerance reprogrammingDisease evidenceStage (preclinical/phase I/phase II/clinical use)Limitations/challengesReferences
AMPK activators (e.g., metformin, AICAR)MetabolicRestore OXPHOS, reduce glycolysis, lower ROS; support Treg survival and mitochondrial fitnessRA, SLE, vasculitis (immunometabolic and clinical data)Clinical use (repurposed); formal tolerance-focused trials mostly phase II /exploratoryIndirect effects; variable efficacy across patients; limited specificity for immune subsets[242, 243]
NAD+ boosters (NR, NMN, nicotinamide)MetabolicIncrease NAD+ → enhance sirtuin activity; promote histone deacetylation; improve mitochondrial quality and regulatory-cell stabilityPreclinical models of arthritis, lupus, and inflammatory agingPreclinical; early human studies in metabolic/aging contextsLimited clinical efficacy in RA; inconsistent effects on Treg function; unclear target engagement[244246]
PPAR-γ agonists (e.g., pioglitazone)MetabolicReprogram lipid metabolism; suppress NF-κB; favor oxidative and anti-inflammatory phenotypes in immune and stromal cellsExperimental arthritis and fibrosis models; limited rheumatic clinical dataClinical use in diabetes; preclinical/early translational in rheumatologySystemic metabolic effects, weight gain, and limited immune-specific targeting[247]
HDAC inhibitorsEpigeneticIncrease histone acetylation at regulatory loci; enhance Treg function; compress inflammatory chromatin accessibilityArthritis and lupus models; small early-phase human dataPreclinical and phase I/IIOff-target epigenetic effects; toxicity with chronic use; limited selectivity[248, 249]
BET inhibitorsEpigeneticDisrupt BRD4/super-enhancer complexes at TNF, IL6, CXCL loci; reduce sustained inflammatory transcriptionPreclinical RA and tissue-inflammation modelsPreclinical; some early oncology trials, limited immune-tolerance trialsHematopoietic toxicity (e.g., thrombocytopenia); off-target transcriptional effects; narrow therapeutic window[146, 158, 250]
EZH2 inhibitorsEpigeneticReduce H3K27me3 at silenced regulatory genes (e.g., SOCS3, CDKN1A); relieve repression of tolerogenic programsB cells and FLS in RA and SLE; strong preclinical rationalePreclinical and early clinical (mainly oncology); rheumatic use exploratoryRisk of global chromatin dysregulation; unclear long-term safety in non-malignant disease[94, 147]
Low-dose DNMT inhibitorsEpigeneticPartially reverse pathological DNA hypermethylation at tolerance genes; re-open FOXP3 and IL10 lociPreclinical models of autoimmunity; conceptual alignment with epigenetic drift dataPreclinical; early clinical experience in oncologyRisk of global hypomethylation; potential oncogenic effects; dose optimization challenges[251, 252]
CAR-TregsCellularAntigen-specific suppression at inflamed sites; stable FOXP3 expression and local IL-10/TGF-β deliveryStrong preclinical efficacy in arthritis, colitis, and transplantation modelsPreclinical; early phase I trials in other immune contextsLimited in vivo persistence; phenotypic instability; high cost and manufacturing complexity[253, 254]
Tolerogenic dendritic cells (tolDCs)CellularPresent self-antigen with low costimulation; induce and expand Tregs; dampen effector primingPhase I/II trials in RA and other autoimmune diseases are showing safety and biological activityPhase I/phase IIVariable durability; scalability challenges; patient-to-patient variability[255, 256]
MSC-based and EV-based therapiesCellular/paracrineDeliver tolerogenic cytokines, metabolites, and miRNAs; remodel immune and stromal metabolic-epigenetic statesEarly trials in RA, SLE, and systemic sclerosis (SSc); preclinical evidence of regulatory reprogrammingPhase I/phase II; some compassionate/controlled clinical useHeterogeneity of preparations; unclear mechanism consistency; regulatory complexity[257, 258]
Nanoparticle-targeted metabolic/epigenetic agentsDelivery/metabolic/epigeneticCell- or tissue-specific delivery of metabolic/epigenetic drugs to synovium or lymphoid organs; limit systemic toxicityRobust preclinical data in arthritis and systemic inflammationPreclinicalLimited tissue penetration; delivery efficiency challenges; manufacturing scalability[259, 260]
Integrated multi-omic/digital-twin–guided regimensSystems/computationalUse epigenomic, transcriptomic, and metabolomic signatures to tailor and adapt tolerance-reprogramming therapies over timeEmerging computational and pilot translational studiesConceptual and early translational; not yet in routine clinical practiceLack of validated clinical biomarkers; high cost; limited clinical integration[261263]

AICAR: 5-aminoimidazole-4-carboxamide ribonucleotide; AMPK: AMP-activated protein kinase; BET: bromodomain and extra-terminal; BRD4: bromodomain-containing protein 4; CAR-Tregs: chimeric antigen receptor regulatory T cells; CDKN1A: cyclin dependent kinase inhibitor 1A; CXCL: C-X-C motif chemokine ligand; DNMT: DNA methyltransferase; EV: extracellular vesicle; FLS: fibroblast-like synoviocytes; FOXP3: forkhead box P3; HDAC: histone deacetylase; IL: interleukin; MSC: mesenchymal stem cell; NMN: nicotinamide mononucleotide; NR: nicotinamide riboside; OXPHOS: oxidative phosphorylation; PPAR-γ: peroxisome proliferator-activated receptor gamma; RA: rheumatoid arthritis; ROS: reactive oxygen species; SOCS3: suppressor of cytokine signaling 3; SLE: systemic lupus erythematosus; TGF-β: transforming growth factor beta; TNF: tumor necrosis factor.