☆ 4.8 Review

Nature vs. nurture: FOXP3, genetics, and tissue environment shape Treg function

FRONTIERS IN IMMUNOLOGY (2022)

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CRISPR/Cas9-mediated demethylation of FOXP3-TSDR toward Treg-characteristic programming of Jurkat T cells

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Summary: Demethylation of FOXP3-TSDR is crucial for the stable differentiation and suppressive function of regulatory T cells. This study demonstrates that transfection of specific plasmids can decrease FOXP3-TSDR methylation and increase FOXP3 mRNA expression in Jurkat cells, potentially enabling the programming of primary T cells into regulatory T cells.

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Immune and Metabolic Effects of Antigen-Specific Immunotherapy Using Multiple β-Cell Peptides in Type 1 Diabetes

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Summary: Type 1 diabetes is caused by a loss of tolerance to pancreatic beta-cell autoantigens and defects in regulatory T-cell function. Immunotherapy with multiple peptides has shown promise in preclinical models and a clinical study demonstrated that it can restore immune tolerance and maintain C-peptide levels in newly diagnosed type 1 diabetes patients. This therapy also resulted in changes in immune responses and regulatory T-cell gene expression.

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CTLA-4 gene mutation and multiple sclerosis: A case report and literature review

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Summary: We reported a case of a patient with multiple disorders, including autoimmune disease, immunodeficiency, enteropathy, organomegaly and lymphocytic infiltration. The patient showed excellent response to abatacept treatment.

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Knockdown of lncRNA HAGLR promotes Treg cell differentiation through increasing the RUNX3 level in dermatomyositis

Wang Yan et al.

Summary: This study suggests that up-regulation of Homeobox D gene cluster antisense growth-associated long noncoding RNA (HAGLR) in dermatomyositis (DM) leads to down-regulation of Forkhead box P3 (Foxp3) and decrease in the proportion of regulatory T (Treg) cells. Meanwhile, the protein levels of Runt-related transcription factor (RUNX3) also decrease. Interfering with HAGLR can restore the expression of Foxp3 and RUNX3, increase the proportion of Treg cells, and alleviate the development of DM.

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microRNA-142 guards against autoimmunity by controlling Treg cell homeostasis and function

Wei-Le Wang et al.

Summary: Research has shown that the absence of miR-142 gene in T-reg cells can lead to systemic autoimmune disorders. The study also revealed that miR-142 deficiency in T-reg cells results in excessive production and signaling of interferon gamma, which can be alleviated by inhibiting interferon gamma.

PLOS BIOLOGY (2022)

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Characterization of chromatin accessibility in psoriasis

Zheng Zhang et al.

Summary: The study systematically analyzed the changes in chromatin accessibility in psoriasis and found that chromatin remodeling significantly contributes to the pathogenesis of the disease. Differences in chromatin accessibility and transcriptional dynamics were also observed in memory Th and Treg cells.

FRONTIERS OF MEDICINE (2022)

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Summary: TCR-T cell therapy is a potential cellular immunotherapy for cancer treatment. However, its efficacy in solid tumors is lower compared to hematological malignancies. This article discusses the barriers and strategies affecting the efficacy of TCR-T cell immunotherapy in solid tumors.

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The FOXP3 full-length isoform controls the lineage-stability of CD4+FOXP3+ regulatory T cells

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Reduction of peripheral regulatory T cells in active rheumatoid arthritis patients with coronary artery disease

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BMC IMMUNOLOGY (2021)

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Exosomes derived from thymic stromal lymphopoietin-treated dendritic cells regulate T helper 17/regulatory T cell differentiation via miR-21/Smad7 axis

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Targeted De-Methylation of the FOXP3-TSDR Is Sufficient to Induce Physiological FOXP3 Expression but Not a Functional Treg Phenotype

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Summary: This study investigated the epigenetic regulation of Treg cells, demonstrating that demethylation of TSDR can induce FOXP3 expression but is not sufficient for stable induction of functional Treg cell phenotype.

FRONTIERS IN IMMUNOLOGY (2021)

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Celiac Disease Causes Epithelial Disruption and Regulatory T Cell Recruitment in the Oral Mucosa

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FRONTIERS IN IMMUNOLOGY (2021)

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Evolving Antibody Therapies for the Treatment of Type 1 Diabetes

Qi Ke et al.

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FRONTIERS IN IMMUNOLOGY (2021)

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Control of Foxp3 induction and maintenance by sequential histone acetylation and DNA demethylation

Jun Li et al.

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CELL REPORTS (2021)

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The microbiota is dispensable for the early stages of peripheral regulatory T cell induction within mesenteric lymph nodes

Carolin Wiechers et al.

Summary: Research shows that the microbiota and their metabolites have a limited impact on the induction of pTreg in mLNs, and do not contribute to the initialization of the Treg-specific epigenetic landscape.

CELLULAR & MOLECULAR IMMUNOLOGY (2021)

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Polyclonal Regulatory T Cell Manufacturing Under cGMP: A Decade of Experience

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FRONTIERS IN IMMUNOLOGY (2021)

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MicroRNA-21 Regulates Diametrically Opposed Biological Functions of Regulatory T Cells

Jijun Sun et al.

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FRONTIERS IN IMMUNOLOGY (2021)

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Co-Expression of FOXP3FL and FOXP3Δ2 Isoforms Is Required for Optimal Treg-Like Cell Phenotypes and Suppressive Function

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Summary: FOXP3 is a crucial transcription factor in regulating immune responses in both mice and humans. In humans, there are two predominant isoforms of FOXP3, full-length and alternatively spliced delta 2, which when co-expressed lead to optimal Treg-like cell function, including downregulation of cytokines and enhanced suppressive function.

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FRONTIERS IN IMMUNOLOGY (2021)

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Distinct Foxp3 enhancer elements coordinate development, maintenance, and function of regulatory T cells

Ryoji Kawakami et al.

Summary: The transcription factor Foxp3 plays crucial roles in Treg cell development and function by controlling Foxp3 transcription. Deletion of CNS0 and CNS3 completely abrogates Treg cell generation and impairs Foxp3 expression stability in residual Treg cells, leading to lethal systemic autoimmunity and inflammation. Hierarchical and coordinated activation of Foxp3 CNS0 and CNS3 initiates and stabilizes Foxp3 gene expression, crucially controlling Treg cell development and self-tolerance.

IMMUNITY (2021)

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A distal Foxp3 enhancer enables interleukin-2 dependent thymic Treg cell lineage commitment for robust immune tolerance

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IL-6 receptor blockade does not slow beta cell loss in new-onset type 1 diabetes

Carla J. Greenbaum et al.

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Strong Expansion of Human Regulatory T Cells for Adoptive Cell Therapy Results in Epigenetic Changes Which May Impact Their Survival and Function

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CAR- and TRuC-redirected regulatory T cells differ in capacity to control adaptive immunity to FVIII

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Single-cell analysis of FOXP3 deficiencies in humans and mice unmasks intrinsic and extrinsic CD4+ T cell perturbations

David Zemmour et al.

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2021)

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TGF-β signaling controls Foxp3 methylation and T reg cell differentiation by modulating Uhrf1 activity

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JOURNAL OF EXPERIMENTAL MEDICINE (2019)

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Long non-coding RNA DQ786243 modulates the induction and function of CD4+ Treg cells through Foxp3-miR-146a-NF-κB axis: Implications for alleviating oral lichen planus

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Article Rheumatology

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Novel small molecule IL-6 inhibitor suppresses autoreactive Th17 development and promotes Treg development

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CLINICAL AND EXPERIMENTAL IMMUNOLOGY (2019)

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Type 1 Diabetes in STAT Protein Family Mutations: Regulating the Th17/Treg Equilibrium and Beyond

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Transcription factor Foxp1 regulates Foxp3 chromatin binding and coordinates regulatory T cell function

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Homeobox protein Hhex negatively regulates Treg cells by inhibiting Foxp3 expression and function

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miRNA142-3p targets Tet2 and impairs Treg differentiation and stability in models of type 1 diabetes

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1,25-Dihydroxyvitamin D3 Ameliorates Collagen-Induced Arthritis via Suppression of Th17 Cells Through miR-124 Mediated Inhibition of IL-6 Signaling

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Bim regulates the survival and suppressive capability of CD8+ FOXP3+ regulatory T cells during murine GVHD

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Peripherally induced regulatory T cells contribute to the control of autoimmune diabetes in the NOD mouse model

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Maresin 1 improves the Treg/Th17 imbalance in rheumatoid arthritis through miR-21

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FRONTIERS IN IMMUNOLOGY (2018)

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JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY (2018)

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A long-lived IL-2 mutein that selectively activates and expands regulatory T cells as a therapy for autoimmune disease

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Thymus-derived Foxp3+ regulatory T cells upregulate RORt expression under inflammatory conditions

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Interleukin 2 modulates thymic-derived regulatory T cell epigenetic landscape

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Serum microRNA Profiles Serve as Novel Biomarkers for Autoimmune Diseases

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Pre-diagnostic genotyping identifies TID subjects with impaired Treg IL-2 signaling and an elevated proportion of FOXP3+IL-17+ cells

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Analyses of a Mutant Foxp3 Allele Reveal BATF as a Critical Transcription Factor in the Differentiation and Accumulation of Tissue Regulatory T Cells

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Flicr, a long noncoding RNA, modulates Foxp3 expression and autoimmunity

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Ash1l and lnc-Smad3 coordinate Smad3 locus accessibility to modulate iTreg polarization and T cell autoimmunity

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Single CD28 stimulation induces stable and polyclonal expansion of human regulatory T cells

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Transcriptional regulation of FOXP3 requires integrated activation of both promoter and CNS regions in tumor-induced CD8+ Treg cells

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The transcription factor Batf3 inhibits the differentiation of regulatory T cells in the periphery

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Different molecular complexes that mediate transcriptional induction and repression by FoxP3

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Proinflammatory cytokine interferon-γ and microbiome-derived metabolites dictate epigenetic switch between forkhead box protein 3 isoforms in coeliac disease

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Foxp3 programs the development and function of CD4+CD25+ regulatory T cells

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Helios Controls a Limited Subset of Regulatory T Cell Functions

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Antigen exposure shapes the ratio between antigen-specific Tregs and conventional T cells in human peripheral blood

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The Chromatin-Modifying Enzyme Ezh2 Is Critical for the Maintenance of Regulatory T Cell Identity after Activation

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Peripherally Induced Tolerance Depends on Peripheral Regulatory T Cells That Require Hopx To Inhibit Intrinsic IL-2 Expression

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Divergent Phenotypes of Human Regulatory T Cells Expressing the Receptors TIGIT and CD226

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Phenotypic Complexity of the Human Regulatory T Cell Compartment Revealed by Mass Cytometry

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Super-enhancers delineate disease-associated regulatory nodes in T cells

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Type 1 diabetes immunotherapy using polyclonal regulatory T cells

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MicroRNA-31 negatively regulates peripherally derived regulatory T-cell generation by repressing retinoic acid-inducible protein 3

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Peripheral blood regulatory T cells in patients with diffuse systemic sclerosis (SSc) before and after autologous hematopoietic SCT: a pilot study

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miR-155 Activates Cytokine Gene Expression in Th17 Cells by Regulating the DNA-Binding Protein Jarid2 to Relieve Polycomb-Mediated Repression

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Decreased expression of microRNA-21 correlates with the imbalance of Th17 and Treg cells in patients with rheumatoid arthritis

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Human IL2RA null mutation mediates immunodeficiency with lymphoproliferation and autoimmunity

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Self-antigen-Driven Activation Induces Instability of Regulatory T Cells during an Inflammatory Autoimmune Response

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Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells

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Uhrf1-dependent H3K23 ubiquitylation couples maintenance DNA methylation and replication

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Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells

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An N-Terminal Mutation of the Foxp3 Transcription Factor Alleviates Arthritis but Exacerbates Diabetes

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Loss of Epigenetic Modification Driven by the Foxp3 Transcription Factor Leads to Regulatory T Cell Insufficiency

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Plasticity of Foxp3+ T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells

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Smad3 binding to the foxp3 enhancer is dispensable for the development of regulatory T cells with the exception of the gut

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IFN-γ Production by Allogeneic Foxp3+ Regulatory T Cells Is Essential for Preventing Experimental Graft-versus-Host Disease

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Type 1 Diabetes-Associated IL2RA Variation Lowers IL-2 Signaling and Contributes to Diminished CD4+CD25+ Regulatory T Cell Function

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CAR/FoxP3-engineered T regulatory cells target the CNS and suppress EAE upon intranasal delivery

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Novel Foxo1-dependent transcriptional programs control Treg cell function

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A multiply redundant genetic switch 'locks in' the transcriptional signature of regulatory T cells

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NATURE IMMUNOLOGY (2012)

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Systematic Localization of Common Disease-Associated Variation in Regulatory DNA

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Anti-CD3 Therapy Promotes Tolerance by Selectively Depleting Pathogenic Cells while Preserving Regulatory T Cells

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IL-2 Controls the Stability of Foxp3 Expression in TGF-β-Induced Foxp3+ T Cells In Vivo

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Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation

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IMMUNITY (2010)

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Transcription factors Foxo3a and Foxo1 couple the E3 ligase Cbl-b to the induction of Foxp3 expression in induced regulatory T cells

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Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate

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Dual function of CTLA-4 in regulatory T cells and conventional T cells to prevent multiorgan autoimmunity

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2010)

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Quantification and phenotype of regulatory T cells in rheumatoid arthritis according to Disease Activity Score-28

Jose Miguel Sempere-Ortells et al.

AUTOIMMUNITY (2009)

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Expansion of Human Regulatory T-Cells From Patients With Type 1 Diabetes

Amy L. Putnam et al.

DIABETES (2009)

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Human natural Treg microRNA signature: Role of microRNA-31 and microRNA-21 in FOXP3 expression

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EUROPEAN JOURNAL OF IMMUNOLOGY (2009)

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Nuclear Factor-κB Modulates Regulatory T Cell Development by Directly Regulating Expression of Foxp3 Transcription Factor

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IMMUNITY (2009)

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In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression

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JOURNAL OF EXPERIMENTAL MEDICINE (2009)

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Induction of Foxp3 demethylation increases regulatory CD4(+)CD25(+) T cells and prevents the occurrence of diabetes in mice

Qanhui Zheng et al.

JOURNAL OF MOLECULAR MEDICINE-JMM (2009)

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Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo

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NATURE IMMUNOLOGY (2009)

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The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation

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NATURE IMMUNOLOGY (2009)

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TGF-p-induced Foxp3+ regulatory T cells rescue scurfy mice

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EUROPEAN JOURNAL OF IMMUNOLOGY (2008)

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DNA methylation controls Foxp3 gene expression

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Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination

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HUMAN IMMUNOLOGY (2008)

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Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction

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IMMUNITY (2008)

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Article Immunology

Molecular antagonism and plasticity of regulatory and inflammatory T cell programs

Xuexian O. Yang et al.

IMMUNITY (2008)

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Article Immunology

CD4+FoxP3+ regulatory T cells confer infectious tolerance in a TGF-β-dependent manner

John Andersson et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2008)

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Article Immunology

Functional suppression by FoxP3(+)CD4(+)CD25(high) regulatory T cells during acute hepatitis C virus infection

Susan Smyk-Pearson et al.

JOURNAL OF INFECTIOUS DISEASES (2008)

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Article Multidisciplinary Sciences

The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA

Jafar Sharif et al.

NATURE (2007)

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Article Multidisciplinary Sciences

UHRF1 plays a role in maintaining DNA methylation in mammalian cells

Magnolia Bostick et al.

SCIENCE (2007)

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Article Immunology

CD8+ T cell-mediated suppression of autoimmunity in a murine lupus model of peptide-induced immune tolerance depends on Foxp3 expression

Ram Pyare Singh et al.

JOURNAL OF IMMUNOLOGY (2007)

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Article Immunology

Cutting edge:: IL-2 is essential for TGF-β-mediated induction of Foxp3+ T regulatory cells

Todd S. Davidson et al.

JOURNAL OF IMMUNOLOGY (2007)

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Article Biochemistry & Molecular Biology

Epigenetic control of the foxp3 locus in regulatory T cells

Stefan Floess et al.

PLOS BIOLOGY (2007)

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Article Biochemistry & Molecular Biology

FOXP3 controls regulatory T cell function through cooperation with NFAT

Yongqing Wu et al.

CELL (2006)

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Article Immunology

Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B1

Dongping Xu et al.

JOURNAL OF IMMUNOLOGY (2006)

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Article Immunology

Therapeutic potential of self-antigen-specific CD4+CD25+ regulatory T cells selected in vitro from a polyclonal repertoire

S Fisson et al.

EUROPEAN JOURNAL OF IMMUNOLOGY (2006)

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Article Immunology

Expansion of functional endogenous antigen-specific CD4+CD25+ regulatory T cells from nonobese diabetic mice

EL Masteller et al.

JOURNAL OF IMMUNOLOGY (2005)

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Article Endocrinology & Metabolism

A single course of anti-CD3 monoclonal antibody hOKT3γ1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes

KC Herold et al.

DIABETES (2005)

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Article Immunology

Regulatory T cell lineage specification by the forkhead transcription factor FoxP3

JD Fontenot et al.

IMMUNITY (2005)

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Article Endocrinology & Metabolism

Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes

S Lindley et al.

DIABETES (2005)

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Article Immunology

In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes

QZ Tang et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2004)

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Article Immunology

Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3

WJ Chen et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2003)

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Article Hematology

Human CD8+CD25+ thymocytes share phenotypic and functional features with CD4+CD25+ re latory thyrnocytes

L Cosmi et al.

BLOOD (2003)

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Article Immunology

Foxp3 programs the development and function of CD4+CD25+ regulatory T cells

JD Fontenot et al.

NATURE IMMUNOLOGY (2003)

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Article Multidisciplinary Sciences

Control of regulatory T cell development by the transcription factor Foxp3

S Hori et al.

SCIENCE (2003)

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Article Immunology

The amount of scurfin protein determines peripheral T cell number and responsiveness

R Khattri et al.

JOURNAL OF IMMUNOLOGY (2001)

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Article Genetics & Heredity

X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy

RS Wildin et al.

NATURE GENETICS (2001)

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Article Genetics & Heredity

Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse

ME Brunkow et al.

NATURE GENETICS (2001)

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Article Genetics & Heredity

The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3

CL Bennett et al.

NATURE GENETICS (2001)

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