Regulatory T cell dysfunction in type 1 diabetes: what's broken and how can we fix it?

Hull, Caroline M.; Peakman, Mark; Tree, Timothy I. M.

doi:10.1007/s00125-017-4377-1

Cited by 196Diabetes and associated disordersT-cell and B-cell ImmunologyPancreatic function and diabetes

Regulatory T cell dysfunction in type 1 diabetes: what's broken and how can we fix it?

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Hull, Caroline M., Peakman, Mark, Tree, Timothy I. M.·2017·Diabetologia

DOI 10.1007/s00125-017-4377-1PMC PMC6448885

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Abstract

Type 1 diabetes is an autoimmune disease characterised by the destruction of insulin producing beta cells in the pancreas. Whilst it remains unclear what the original triggering factors for this destruction are, observations from the natural history of human type 1 diabetes, including incidence rates in twins, suggest that the disease results from a combination of genetic and environmental factors. Whilst many different immune cells have been implicated, including members of the innate and adaptive immune systems, a view has emerged over the past 10 years that beta cell damage is mediated by the combined actions of CD4 + and CD8 + T cells with specificity for islet autoantigens. In health, these potentially pathogenic T cells are held in check by multiple regulatory mechanisms, known collectively as ‘immunological tolerance’. This raises the question as to whether type 1 diabetes develops, at least in part, as a result of a defect in one or more of these control mechanisms. Immunological tolerance includes both central mechanisms (purging of the T cell repertoire of high-affinity autoreactive T cells in the thymus) and peripheral mechanisms, a major component of which is the action of a specialised subpopulation of T cells, known as regulatory T cells (Tregs). In this review, we highlight the evidence suggesting that a reduction in the functional capacity of different Treg populations contributes to disease development in type 1 diabetes. We also address current controversies regarding the putative causes of this defect and discuss strategies to correct it as a means to reduce or prevent islet destruction in a clinical setting.

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The pathogenesis of type 1 diabetes results from a complex interaction between the pancreatic β-cell and innate and adaptive immune systems.
“The pathogenesis of type 1 diabetes results from a complex interaction between the pancreatic β-cell and innate and adaptive immune systems (figure 3).47”
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Anti-thymocyte globulin/G-CSF treatment preserves β cell function in patients with established type 1 diabetes
Haller, M. J., Gitelman, S. E., Gottlieb, P. A., Michels, A. W., Rosenthal, S. M., Shuster, J. J., Zou, B., Brusko, T. M., Hulme, M. A., Wasserfall, C. H., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78492 · Cited by 167 · see citing works
Type I Regulatory T Cells Specific for Desmoglein 3 Are More Frequently Detected in Healthy Individuals than in Patients with Pemphigus Vulgaris
Veldman, C. M., Höhne, A., Dieckmann, D., Schuler, G., & Hertl, M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.10.6468 · Cited by 164 · see citing works
Rapid induction of clinical remission by low-dose interleukin-2 in a patient with refractory SLE
Humrich, J. Y., von Spee-Mayer, C., Siegert, E., Alexander, T., Hiepe, F., Radbruch, A., Burmester, G. R., & Riemekasten, G. (2015) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2014-206506 · Cited by 162 · see citing works
Teplizumab treatment may improve C-peptide responses in participants with type 1 diabetes after the new-onset period: a randomised controlled trial
Herold, K. C., Gitelman, S. E., Willi, S. M., Gottlieb, P. A., Waldron-Lynch, F., Devine, L., Sherr, J. L., Rosenthal, S. M., Adi, S., Jalaludin, M. Y., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2753-4 · Cited by 159 · see citing works
Proinsulin peptide immunotherapy in type 1 diabetes: report of a first-in-man Phase I safety study
Thrower, S., James, L. K., Hall, W., Green, K. M., Arif, S., Allen, J. S., Van-Krinks, C., Lozanoska‐Ochser, B., de Marquesini, L. G. P., Brown, S., et al. (2008) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2008.03814.x · Cited by 153 · see citing works
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Differential effects of rapamycin and retinoic acid on expansion, stability and suppressive qualities of human CD4+CD25+FOXP3+ T regulatory cell subpopulations
Scottà, C., Esposito, M., Fazekasova, H., Fanelli, G. C., Edozie, F. C., Ali, N., Xiao, F., Peakman, M., Afzali, B., Sagoo, P., et al. (2012) · Haematologica · doi:10.3324/haematol.2012.074088 · Cited by 149 · see citing works
Self-citation
Induction of GAD65-specific regulatory T-cells inhibits ongoing autoimmune diabetes in nonobese diabetic mice.
Tisch, R., Liblau, R., Yang, X., Liblau, P., & McDevitt, H. O. (1998) · Diabetes · doi:10.2337/diabetes.47.6.894 · Cited by 147 · see citing works
Phenotypic Complexity of the Human Regulatory T Cell Compartment Revealed by Mass Cytometry
Mason, G. M., Lowe, K., Melchiotti, R., Ellis, R., de Rinaldis, E., Peakman, M., Heck, S., Lombardi, G., & Tree, T. I. M. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500703 · Cited by 147 · see citing works
Self-citation
An autoimmune-associated variant in PTPN2 reveals an impairment of IL-2R signaling in CD4+ T cells
Long, S., Cerosaletti, K. M., Wan, J. Y., Ho, J.-C., Tatum, M., Wei, S., Shilling, H. G., & Buckner, J. H. (2010) · Genes and Immunity · doi:10.1038/gene.2010.54 · Cited by 143 · see citing works
Gliadin-Specific Type 1 Regulatory T Cells from the Intestinal Mucosa of Treated Celiac Patients Inhibit Pathogenic T Cells
Gianfrani, C., Levings, M. K., Sartirana, C., Mazzarella, G., Barba, G., Zanzi, D., Camarca, A., Iaquinto, G., Giardullo, N., Auricchio, S., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.6.4178 · Cited by 141 · see citing works
Human Antigen-Specific Regulatory T Cells Generated by T Cell Receptor Gene Transfer
Brusko, T. M., Koya, R. C., Zhu, S., Lee, M. R., Putnam, A. L., McClymont, S., Nishimura, M. I., Han, S., Chang, L., Atkinson, M. A., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011726 · Cited by 140 · see citing works
T cell receptor reversed polarity recognition of a self-antigen major histocompatibility complex
Beringer, D. X., Kleijwegt, F. S., Wiede, F., van der Slik, A. R., Loh, K. L., Petersen, J., Dudek, N. L., Duinkerken, G., Laban, S., Joosten, A. M., et al. (2015) · Nature Immunology · doi:10.1038/ni.3271 · Cited by 135 · see citing works
Suppressive properties of human CD4+CD25+ regulatory T cells are dependent on CTLA‐4 expression
Birebent, B., Lorho, R., Lechartier, H., de Guibert, S., Alizadeh, M., Vu, N., Beauplet, A., Robillard, N., & Sémana, G. (2004) · European Journal of Immunology · doi:10.1002/eji.200324632 · Cited by 123 · see citing works
Multiple Autoimmune-Associated Variants Confer Decreased IL-2R Signaling in CD4+CD25hi T Cells of Type 1 Diabetic and Multiple Sclerosis Patients
Cerosaletti, K. M., Schneider, A., Schwedhelm, K. V., Frank, I., Tatum, M., Wei, S., Whalen, E., Greenbaum, C. J., Kita, M., Buckner, J. H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083811 · Cited by 119 · see citing works
Inducible reprogramming of human T cells into Treg cells by a conditionally active form of FOXP3
Allan, S., Song-Zhao, G. X., Abraham, T., McMurchy, A. N., & Levings, M. K. (2008) · European Journal of Immunology · doi:10.1002/eji.200838373 · Cited by 116 · see citing works
Interindividual variation in human T regulatory cells
Ferraro, A., D’Alise, A. M., Raj, T., Asinovski, N., Phillips, R., Ergün, A., Replogle, J. M., Bernier, A. V., Laffel, L. M., Stranger, B. E., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1401343111 · Cited by 115 · see citing works
Treg activation defect in type 1 diabetes: correction with TNFR2 agonism
Okubo, Y., Torrey, H., Butterworth, J., Zheng, H., & Faustman, D. L. (2016) · Clinical & Translational Immunology · doi:10.1038/cti.2015.43 · Cited by 111 · see citing works
Antigen-Specific Mediated Suppression of β Cell Autoimmunity by Plasmid DNA Vaccination
Tisch, R., Wang, B., Weaver, D. J., Liu, B., Bui, T., Arthos, J. A., & SERREZE, D. V. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.3.2122 · Cited by 110 · see citing works
Enhanced T cell responses to IL-6 in type 1 diabetes are associated with early clinical disease and increased IL-6 receptor expression
Hundhausen, C., Roth, A., Whalen, E., Chen, J., Schneider, A., Long, S. A., Wei, S., Rawlings, R., Kinsman, M., Evanko, S. P., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad9943 · Cited by 102 · see citing works
Anti-cytokine therapies in T1D: Concepts and strategies
Nepom, G. T., Ehlers, M. R., & Mandrup-Poulsen, T. R. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.02.003 · Cited by 72 · see citing works
At-Risk and Recent-Onset Type 1 Diabetic Subjects Have Increased Apoptosis in the CD4+CD25+high T-Cell Fraction
Glisic-Milosavljevic, S., Waukau, J., Jailwala, P., Jana, S., KHOO, H., Albertz, H., Woodliff, J. E., Koppen, M., Alemzadeh, R., Hagopian, W., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000146 · Cited by 72 · see citing works
Impact of Protective IL-2 Allelic Variants on CD4+Foxp3+ Regulatory T Cell Function In Situ and Resistance to Autoimmune Diabetes in NOD Mice
Sgouroudis, E., Albanese, A., & Piccirillo, C. A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.9.6283 · Cited by 69 · see citing works
A Regulatory T-Cell Gene Signature Is a Specific and Sensitive Biomarker to Identify Children With New-Onset Type 1 Diabetes
Pesenacker, A. M., Wang, A. Y., Singh, A., Gillies, J., Kim, Y., Piccirillo, C. A., Nguyen, D., Haining, W. N., Tebbutt, S. J., Panagiotopoulos, C., et al. (2016) · Diabetes · doi:10.2337/db15-0572 · Cited by 69 · see citing works
Clonal regulatory T cells specific for a red blood cell autoantigen in human autoimmune hemolytic anemia
Ward, F. J., Hall, A. M., Cairns, L. S., Leggat, A. S., Urbaniak, S. J., Vickers, M. A., & Barker, R. N. (2007) · Blood · doi:10.1182/blood-2007-07-101345 · Cited by 66 · see citing works
Islet antigen specific IL-10+ immune responses but not CD4+CD25+FoxP3+ cells at diagnosis predict glycemic control in type 1 diabetes
Sanda, S., Roep, B. O., & von Herrath, M. (2008) · Clinical Immunology · doi:10.1016/j.clim.2007.12.003 · Cited by 65 · see citing works
Autoreactive T cell clones specific for class I and class II HLA antigens isolated from a human chimera.
Roncarolo, M., Yssel, H., Touraine, J. L., Betuel, H., de Vries, J. E., & Spits, H. (1988) · The Journal of Experimental Medicine · doi:10.1084/jem.167.5.1523 · Cited by 63 · see citing works
IL-2 therapy in type 1 diabetes: “Trials” and tribulations
Long, S. A., Buckner, J. H., & Greenbaum, C. J. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.02.005 · Cited by 62 · see citing works
Transfer of Regulatory Properties from Tolerogenic to Proinflammatory Dendritic Cells via Induced Autoreactive Regulatory T Cells
Kleijwegt, F. S., Laban, S., Duinkerken, G., Joosten, A. M., Koeleman, B. P. C., Nikolić, T., & Roep, B. O. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101638 · Cited by 59 · see citing works
Natural Variation in Interleukin-2 Sensitivity Influences Regulatory T-Cell Frequency and Function in Individuals With Long-standing Type 1 Diabetes
Yang, J. H. M., Cutler, A. J., Ferreira, R. C., Reading, J. L., Cooper, N. J., Wallace, C., Pamela, C., Smyth, D. J., Boyce, C. S., Gao, G., et al. (2015) · Diabetes · doi:10.2337/db15-0516 · Cited by 59 · see citing works
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Clinical grade production of IL-10 producing regulatory Tr1 lymphocytes for cell therapy of chronic inflammatory diseases
Brun, V., Bastian, H., Neveu, V., & Foussat, A. (2009) · International Immunopharmacology · doi:10.1016/j.intimp.2009.01.032 · Cited by 58 · see citing works
The IL-2/CD25 Pathway Determines Susceptibility to T1D in Humans and NOD Mice
Dendrou, C. A., & Wicker, L. S. (2008) · Journal of Clinical Immunology · doi:10.1007/s10875-008-9237-9 · Cited by 58 · see citing works
Proinsulin multi-peptide immunotherapy induces antigen-specific regulatory T cells and limits autoimmunity in a humanized model
Gibson, V. B., Nikolić, T., Pearce, V. Q., Demengeot, J., Roep, B. O., & Peakman, M. (2015) · Clinical & Experimental Immunology · doi:10.1111/cei.12687 · Cited by 56 · see citing works
Self-citation
IFN-γ and IL-10 islet-antigen-specific T cell responses in autoantibody-negative first-degree relatives of patients with type 1 diabetes
de Marquesini, L. G. P., Fu, J., Connor, K., Bishop, A. J., McLintock, N. E., Pope, C., Wong, F. S., & Dayan, C. M. (2010) · Diabetologia · doi:10.1007/s00125-010-1739-3 · Cited by 56 · see citing works
Dynamic changes in CD4+ CD25+ high T cell apoptosis after the diagnosis of type 1 diabetes
Glisic-Milosavljevic, S., Wang, T., Koppen, M., Kramer, J., Ehlenbach, S. J., Waukau, J., Jailwala, P., Jana, S., Alemzadeh, R., & Ghosh, S. (2007) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2007.03475.x · Cited by 38 · see citing works
Rationale and study design of the Adaptive study of IL-2 dose on regulatory T cells in type 1 diabetes (DILT1D): a non-randomised, open label, adaptive dose finding trial
Waldron-Lynch, F., Kareclas, P., Kathryn, I., Walker, N. M., Mander, A., Wicker, L. S., Todd, J. A., & Bond, S. J. (2014) · BMJ Open · doi:10.1136/bmjopen-2014-005559 · Cited by 31 · see citing works
Natural variation of H3K27me3 modification in two Arabidopsis accessions and their hybrid
Yang, M., Wang, X., Huang, H., Ren, D., Su, Y., Zhu, P., Zhu, D., Fan, L., Chen, L., He, G., et al. (2015) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12443 · Cited by 24 · see citing works
Isolation of functional autologous collagen-II specific IL-10 producing Tr1 cell clones from rheumatoid arthritis blood
Brun, V., Neveu, V., Pers, Y., Fabre, S., Quatannens, B., Bastian, H., Clerget–Chossat, N., Jørgensen, C., & Foussat, A. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.03.001 · Cited by 24 · see citing works
Protocol of the adaptive study of IL-2 dose frequency on regulatory T cells in type 1 diabetes (DILfrequency): a mechanistic, non-randomised, repeat dose, open-label, response-adaptive study
Truman, L. A., Pękalski, M. Ł., Kareclas, P., Evangelou, M., Walker, N. M., Howlett, J., Mander, A., Kennet, J., Wicker, L. S., Bond, S. J., et al. (2015) · BMJ Open · doi:10.1136/bmjopen-2015-009799 · Cited by 20 · see citing works
Genetic association of HLA DQB1 with CD4+CD25+high T-cell apoptosis in type 1 diabetes
Glišić, S., Klinker, M. W., Waukau, J., Jailwala, P., Jana, S., Basken, J., Wang, T., Alemzadeh, R., Hagopian, W., & Ghosh, S. (2009) · Genes and Immunity · doi:10.1038/gene.2009.14 · Cited by 19 · see citing works
Interaction between Treg Apoptosis Pathways, Treg Function and HLA Risk Evolves during Type 1 Diabetes Pathogenesis
Glišić, S., & Jailwala, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036040 · Cited by 15 · see citing works
Regulatory T cell phenotype and function 4 years after GAD–alum treatment in children with type 1 diabetes
Pihl, M., Åkerman, L., Axelsson, S., Chéramy, M., Hjorth, M., Mallone, R., Ludvigsson, J., & Casas, R. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12078 · Cited by 14 · see citing works
The Type of Responder T-Cell Has a Significant Impact in a Human In Vitro Suppression Assay
Jana, S., Campbell, H., Woodliff, J. E., Waukau, J., Jailwala, P., Ghorai, J. K., Ghosh, S., & Glišić, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015154 · Cited by 11 · see citing works

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Type 1 diabetes
DiMeglio, L. A., Evans-Molina, C., & Oram, R. A. (2018) · The Lancet · doi:10.1016/s0140-6736(18)31320-5 · Cited by 1,561 · see citing works
The heterogeneous pathogenesis of type 1 diabetes mellitus
Ilonen, J., Lempainen, J., & Veijola, R. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0254-y · Cited by 497 · see citing works
Introducing the Endotype Concept to Address the Challenge of Disease Heterogeneity in Type 1 Diabetes
Battaglia, M., Ahmed, S., Anderson, M. S., Atkinson, M. A., Becker, D., Bingley, P. J., Bosi, E., Brusko, T. M., DiMeglio, L. A., Evans-Molina, C., et al. (2020) · Diabetes Care · doi:10.2337/dc19-0880 · Cited by 351 · see citing works
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Current understanding of CTLA-4: from mechanism to autoimmune diseases
Hossen, M. M., Ma, Y., Yin, Z., Xia, Y., Du, J., Huang, J. Y., Huang, J. J., Zou, L., Ye, Z., & Huang, Z. W. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1198365 · Cited by 245 · see citing works
Alterations in microbiota of patients with COVID-19: potential mechanisms and therapeutic interventions
Wang, B., Zhang, L., Wang, Y., Dai, T., Qin, Z., Zhou, F., & Zhang, L. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00986-0 · Cited by 185 · see citing works
A Systematic Review of Phytochemistry, Pharmacology and Pharmacokinetics on Astragali Radix: Implications for Astragali Radix as a Personalized Medicine
Guo, Z., Lou, Y., Kong, M., Luo, Q., Liu, Z., & Wu, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061463 · Cited by 163 · see citing works
The diabetes pandemic and associated infections: suggestions for clinical microbiology
Toniolo, A., Cassani, G., Puggioni, A., Rossi, A., Colombo, A., Onodera, T., & Ferrannini, E. (2018) · Reviews in Medical Microbiology · doi:10.1097/mrm.0000000000000155 · Cited by 152 · see citing works
IL-2-based approaches to Treg enhancement
Harris, F., Berdugo, Y. A., & Tree, T. I. M. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac105 · Cited by 145 · see citing works
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Short-Chain Fatty Acid (SCFA) as a Connecting Link between Microbiota and Gut-Lung Axis─A Potential Therapeutic Intervention to Improve Lung Health
Verma, A., Bhagchandani, T., Rai, A., Nikita, N., Sardarni, U. K., Bhavesh, N. S., Gulati, S., Malik, R., & Tandon, R. (2024) · ACS Omega · doi:10.1021/acsomega.3c05846 · Cited by 123 · see citing works
Regulatory T Cells in Systemic Sclerosis
Frantz, C., Auffray, C., Avouac, J., & Allanore, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02356 · Cited by 110 · see citing works
Mechanisms of human FoxP3+ Treg cell development and function in health and disease
Attias, M., Al-Aubodah, T.-A., & Piccirillo, C. A. (2019) · Clinical & Experimental Immunology · doi:10.1111/cei.13290 · Cited by 103 · see citing works
Emerging Therapeutics for Immune Tolerance: Tolerogenic Vaccines, T cell Therapy, and IL-2 Therapy
Moorman, C. D., Sohn, S. J., & Phee, H. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.657768 · Cited by 102 · see citing works
Pancreatic islet-specific engineered T regs exhibit robust antigen-specific and bystander immune suppression in type 1 diabetes models
Yang, S. J., Singh, A. K., Drow, T., Tappen, T., Honaker, Y., Barahmand-pour-Whitman, F., Linsley, P. S., Cerosaletti, K. M., Mauk, K. E., Xiang, Y., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abn1716 · Cited by 88 · see citing works
Function, Failure, and the Future Potential of Tregs in Type 1 Diabetes
Bettini, M., & Bettini, M. L. (2021) · Diabetes · doi:10.2337/dbi18-0058 · Cited by 81 · see citing works
A phase 2 randomized trial with autologous polyclonal expanded regulatory T cells in children with new-onset type 1 diabetes
Bender, C., WIEDEMAN, A. E., Hu, A. K., Ylescupidez, A., Sietsema, W. K., Herold, K. C., Griffin, K., Gitelman, S. E., Long, S. A., on behalf of the T-Rex Study Group†, et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adn2404 · Cited by 82 · see citing works
Immunological biomarkers for the development and progression of type 1 diabetes
Mathieu, C., Lahesmaa, R., Bonifacio, E. E., Achenbach, P., & Tree, T. I. M. (2018) · Diabetologia · doi:10.1007/s00125-018-4726-8 · Cited by 79 · see citing works
Self-citation
Why Is COVID-19 More Severe in Patients With Diabetes? The Role of Angiotensin-Converting Enzyme 2, Endothelial Dysfunction and the Immunoinflammatory System
Roberts, J., Pritchard, A. L., Treweeke, A. T., Rossi, A. G., Brace, N., Cahill, P. A., MacRury, S. M., Wei, J., & Megson, I. L. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.629933 · Cited by 68 · see citing works
Exercise and Type 1 Diabetes
Lu, X., & Zhao, C. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-1792-1_7 · Cited by 71 · see citing works
Advances in Chemical Composition, Extraction Techniques, Analytical Methods, and Biological Activity of Astragali Radix
Chang, X., Chen, X., Guo, Y., Gong, P., Pei, S., Wang, D., Wang, P., Wang, M., & Chen, F. (2022) · Molecules · doi:10.3390/molecules27031058 · Cited by 64 · see citing works
The β Cell in Diabetes: Integrating Biomarkers With Functional Measures
Kahn, S. E., Chen, Y., Esser, N., Taylor, A. J., van Raalte, D. H., Zraika, S., & Verchere, C. B. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab021 · Cited by 69 · see citing works
Adult-onset autoimmune diabetes
Buzzetti, R., Maddaloni, E., Gaglia, J. L., Leslie, R. D., Wong, F. S., & Boehm, B. O. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00390-6 · Cited by 64 · see citing works
Defining the Threshold IL-2 Signal Required for Induction of Selective Treg Cell Responses Using Engineered IL-2 Muteins
Ghelani, A. P., Bates, D. L., Conner, K. P., Wu, M.-Z., Lu, J., Hu, Y.-L., Li, C.-M., Chaudhry, A., & Sohn, S. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01106 · Cited by 60 · see citing works
Mitochondrial-encoded MOTS-c prevents pancreatic islet destruction in autoimmune diabetes
Kong, B. S., Min, S. H., Lee, C. D., & Cho, Y. M. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109447 · Cited by 62 · see citing works
Targeting the receptor for advanced glycation end products (RAGE) in type 1 diabetes
Bagge, S. L., Fotheringham, A. K., Leung, S. S., & Forbes, J. M. (2020) · Medicinal Research Reviews · doi:10.1002/med.21654 · Cited by 51 · see citing works
Presumption of guilt for T cells in type 1 diabetes: lead culprits or partners in crime depending on age of onset?
Carré, A., Richardson, S. J., Larger, É., & Mallone, R. (2020) · Diabetologia · doi:10.1007/s00125-020-05298-y · Cited by 51 · see citing works
Innate inflammation drives NK cell activation to impair Treg activity
Dean, J. W., Peters, L. D., Fuhrman, C. A., Seay, H. R., Posgai, A. L., Stimpson, S. E., Brusko, M., Perry, D. J., Yeh, W.-I., Newby, B. N., et al. (2020) · Journal of Autoimmunity · doi:10.1016/j.jaut.2020.102417 · Cited by 48 · see citing works
Dipeptidyl peptidase-4(DPP-4) inhibitors: promising new agents for autoimmune diabetes
Wang, X., Zheng, P., Huang, G., Yang, L., & Zhou, Z. (2018) · Clinical and Experimental Medicine · doi:10.1007/s10238-018-0519-0 · Cited by 47 · see citing works
Tolerizing Strategies for the Treatment of Autoimmune Diseases: From ex vivo to in vivo Strategies
Cauwels, A., & Tavernier, J. H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00674 · Cited by 46 · see citing works
Advanced Glycation End Products and Inflammation in Type 1 Diabetes Development
Du, C., Whiddett, R. O., Buckle, I., Chen, C., Forbes, J. M., & Fotheringham, A. K. (2022) · Cells · doi:10.3390/cells11213503 · Cited by 47 · see citing works
Single-cell insights into immune dysregulation in rheumatoid arthritis flare versus drug-free remission
Baker, K. F., McDonald, D., Hulme, G., Hussain, R., Coxhead, J., Swan, D. J., Schulz, A. R., Mei, H. E., MacDonald, L., Pratt, A. G., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45213-2 · Cited by 48 · see citing works
Treg gene signatures predict and measure type 1 diabetes trajectory
Pesenacker, A. M., Chen, V., Gillies, J. K., Speake, C., Marwaha, A., Sun, A. C., Chow, S., Tan, R., Elliott, T. G., Dutz, J. P., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.123879 · Cited by 44 · see citing works
Modeling human T1D-associated autoimmune processes
Maharlooei, M. K., Madley, R., Borsotti, C., Ferreira, L. M. R., Sharp, R. C., Brehm, M. A., Greiner, D. L., Parent, A. V., Anderson, M. S., Sykes, M., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101417 · Cited by 42 · see citing works
Engineered Treg cells: The heir to the throne of immunotherapy
Stucchi, A., Maspes, F., Montee-Rodrigues, E., & Fousteri, G. (2023) · Journal of Autoimmunity · doi:10.1016/j.jaut.2022.102986 · Cited by 43 · see citing works
Role of Polyamines and Hypusine in β Cells and Diabetes Pathogenesis
Kulkarni, A., Anderson, C. M., Mirmira, R. G., & Tersey, S. A. (2022) · Metabolites · doi:10.3390/metabo12040344 · Cited by 39 · see citing works
Chimeric Antigen Receptor (CAR)-Based Cell Therapy for Type 1 Diabetes Mellitus (T1DM); Current Progress and Future Approaches
Mohammadi, V., Maleki, A. J., Nazari, M., Siahmansouri, A., Moradi, A., Elahi, R., & Esmaeilzadeh, A. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10668-1 · Cited by 36 · see citing works
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Authors: Hull, C. M., Peakman, M., & Tree, T. I. M.
Affiliations: Guy's Hospital (GB)
Corresponding author: Hull, Caroline M.
Tree, Timothy I. M.
ORCID: Hull, Caroline M.
Peakman, Mark
Tree, Timothy I. M.
Venue: Diabetologia
Publisher: Springer Science and Business Media LLC
Published: 2017-08-02
Volume: 60
Issue: 10
Pages: 1839-1850
ISSN: 0012-186X (ISSN-L)
1432-0428
DOI: 10.1007/s00125-017-4377-1
PMC: PMC6448885
OpenAlex: W2739639576
Cited by: 194
References: 109
Citations by year: 2026: 11 · 2025: 32 · 2024: 30 · 2023: 17 · 2022: 25 · 2021: 25 · 2020: 21 · 2019: 19 · 2018: 13 · 2017: 1
FWCI: 1.89
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (unspecified)
Locations: Diabetologia (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Research Portal (King's College London) (publishedVersion, cc-by)
Funders: King's College London
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Keywords: type 1 diabetes, regulatory T cells, immune tolerance, beta cell destruction, islet autoantigens, CD4+ T cells, CD8+ T cells, thymic selection, peripheral tolerance, Treg dysfunction, Treg therapy, autoimmunity
MeSH terms: Animals, Diabetes Mellitus, Type 1, Humans, Immune Tolerance, T-Lymphocytes, Regulatory

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Regulatory T cell dysfunction in type 1 diabetes: what's broken and how can we fix it?

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