Circulating β cell‐specific CD8+ T cells restricted by high‐risk HLA class I molecules show antigen experience in children with and at risk of type 1 diabetes
Summary In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by t...
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| Published in | Clinical and experimental immunology Vol. 199; no. 3; pp. 263 - 277 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Oxford University Press
01.03.2020
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0009-9104 1365-2249 1365-2249 |
| DOI | 10.1111/cei.13391 |
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| Abstract | Summary
In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)‐specific and insulin B (InsB)‐specific CD8+ T cells in HLA‐B*3906+ children newly diagnosed with T1D and in high‐risk HLA‐A*2402+ children before the appearance of disease‐specific autoantibodies and before diagnosis of T1D. Antigen‐specific CD8+ T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA‐B*3906+ children with T1D, we observed an increase in PPI5–12‐specific transitional memory CD8+ T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI5–12‐specific CD8+ T cells in HLA‐B*3906+ children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8+ T cells. In longitudinal samples from high‐risk HLA‐A*2402+ children, the percentage of terminal effector cells within the InsB15–24‐specific CD8+ T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA‐B*3906‐restricted autoreactive CD8+ T cells in T1D. Collectively, our results provide evidence that β cell‐reactive CD8+ T cells restricted by disease‐associated HLA class I molecules display an antigen‐experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease.
In this study, we characterised circulating autoreactive CD8+ T cells in children with type 1 diabetes with HLA-B*3906+ and HLA-A*2402+ genotypes which are associated with increased risk and early onset of disease. In HLA-B*3906+ children with newly diagnosed type 1 diabetes, we observed an increase in PPI5–12‐specific transitional memory CD8+ T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI5–12‐specific CD8+ T cells in HLA‐B*3906+ children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8+ T cells. Further, in longitudinal samples from high-risk HLA-A*2402+ children, the percentage of terminal effector cells within the InsB15–24‐specific CD8+ T cell population was increased before diagnosis relative to samples taken before the appearance of autoantibodies. |
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| AbstractList | In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin-producing β cells. The HLA-B*3906 and HLA-A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)-specific and insulin B (InsB)-specific CD8+ T cells in HLA-B*3906+ children newly diagnosed with T1D and in high-risk HLA-A*2402+ children before the appearance of disease-specific autoantibodies and before diagnosis of T1D. Antigen-specific CD8+ T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA-B*3906+ children with T1D, we observed an increase in PPI5-12 -specific transitional memory CD8+ T cells compared to non-diabetic, age- and HLA-matched subjects. Furthermore, PPI5-12 -specific CD8+ T cells in HLA-B*3906+ children with T1D showed a significantly more antigen-experienced phenotype compared to polyclonal CD8+ T cells. In longitudinal samples from high-risk HLA-A*2402+ children, the percentage of terminal effector cells within the InsB15-24 -specific CD8+ T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA-B*3906-restricted autoreactive CD8+ T cells in T1D. Collectively, our results provide evidence that β cell-reactive CD8+ T cells restricted by disease-associated HLA class I molecules display an antigen-experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease.In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin-producing β cells. The HLA-B*3906 and HLA-A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)-specific and insulin B (InsB)-specific CD8+ T cells in HLA-B*3906+ children newly diagnosed with T1D and in high-risk HLA-A*2402+ children before the appearance of disease-specific autoantibodies and before diagnosis of T1D. Antigen-specific CD8+ T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA-B*3906+ children with T1D, we observed an increase in PPI5-12 -specific transitional memory CD8+ T cells compared to non-diabetic, age- and HLA-matched subjects. Furthermore, PPI5-12 -specific CD8+ T cells in HLA-B*3906+ children with T1D showed a significantly more antigen-experienced phenotype compared to polyclonal CD8+ T cells. In longitudinal samples from high-risk HLA-A*2402+ children, the percentage of terminal effector cells within the InsB15-24 -specific CD8+ T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA-B*3906-restricted autoreactive CD8+ T cells in T1D. Collectively, our results provide evidence that β cell-reactive CD8+ T cells restricted by disease-associated HLA class I molecules display an antigen-experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease. In type 1 diabetes (T1D), autoreactive cytotoxic CD8 T cells are implicated in the destruction of insulin-producing β cells. The HLA-B*3906 and HLA-A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8 T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)-specific and insulin B (InsB)-specific CD8 T cells in HLA-B*3906 children newly diagnosed with T1D and in high-risk HLA-A*2402 children before the appearance of disease-specific autoantibodies and before diagnosis of T1D. Antigen-specific CD8 T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA-B*3906 children with T1D, we observed an increase in PPI -specific transitional memory CD8 T cells compared to non-diabetic, age- and HLA-matched subjects. Furthermore, PPI -specific CD8 T cells in HLA-B*3906 children with T1D showed a significantly more antigen-experienced phenotype compared to polyclonal CD8 T cells. In longitudinal samples from high-risk HLA-A*2402 children, the percentage of terminal effector cells within the InsB -specific CD8 T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA-B*3906-restricted autoreactive CD8 T cells in T1D. Collectively, our results provide evidence that β cell-reactive CD8 T cells restricted by disease-associated HLA class I molecules display an antigen-experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease. Summary In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)‐specific and insulin B (InsB)‐specific CD8+ T cells in HLA‐B*3906+ children newly diagnosed with T1D and in high‐risk HLA‐A*2402+ children before the appearance of disease‐specific autoantibodies and before diagnosis of T1D. Antigen‐specific CD8+ T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA‐B*3906+ children with T1D, we observed an increase in PPI5–12‐specific transitional memory CD8+ T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI5–12‐specific CD8+ T cells in HLA‐B*3906+ children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8+ T cells. In longitudinal samples from high‐risk HLA‐A*2402+ children, the percentage of terminal effector cells within the InsB15–24‐specific CD8+ T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA‐B*3906‐restricted autoreactive CD8+ T cells in T1D. Collectively, our results provide evidence that β cell‐reactive CD8+ T cells restricted by disease‐associated HLA class I molecules display an antigen‐experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease. In this study, we characterised circulating autoreactive CD8+ T cells in children with type 1 diabetes with HLA-B*3906+ and HLA-A*2402+ genotypes which are associated with increased risk and early onset of disease. In HLA-B*3906+ children with newly diagnosed type 1 diabetes, we observed an increase in PPI5–12‐specific transitional memory CD8+ T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI5–12‐specific CD8+ T cells in HLA‐B*3906+ children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8+ T cells. Further, in longitudinal samples from high-risk HLA-A*2402+ children, the percentage of terminal effector cells within the InsB15–24‐specific CD8+ T cell population was increased before diagnosis relative to samples taken before the appearance of autoantibodies. In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8+ T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)‐specific and insulin B (InsB)‐specific CD8+ T cells in HLA‐B*3906+ children newly diagnosed with T1D and in high‐risk HLA‐A*2402+ children before the appearance of disease‐specific autoantibodies and before diagnosis of T1D. Antigen‐specific CD8+ T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA‐B*3906+ children with T1D, we observed an increase in PPI5–12‐specific transitional memory CD8+ T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI5–12‐specific CD8+ T cells in HLA‐B*3906+ children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8+ T cells. In longitudinal samples from high‐risk HLA‐A*2402+ children, the percentage of terminal effector cells within the InsB15–24‐specific CD8+ T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA‐B*3906‐restricted autoreactive CD8+ T cells in T1D. Collectively, our results provide evidence that β cell‐reactive CD8+ T cells restricted by disease‐associated HLA class I molecules display an antigen‐experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease. In type 1 diabetes (T1D), autoreactive cytotoxic CD8 + T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402 class I genes confer increased risk and promote early disease onset, suggesting that CD8 + T cells that recognize peptides presented by these class I molecules on pancreatic β cells play a pivotal role in the autoimmune response. We examined the frequency and phenotype of circulating preproinsulin (PPI)‐specific and insulin B (InsB)‐specific CD8 + T cells in HLA‐B*3906 + children newly diagnosed with T1D and in high‐risk HLA‐A*2402 + children before the appearance of disease‐specific autoantibodies and before diagnosis of T1D. Antigen‐specific CD8 + T cells were detected using human leucocyte antigen (HLA) class I tetramers and flow cytometry was used to assess memory status. In HLA‐B*3906 + children with T1D, we observed an increase in PPI 5–12 ‐specific transitional memory CD8 + T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI 5–12 ‐specific CD8 + T cells in HLA‐B*3906 + children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8 + T cells. In longitudinal samples from high‐risk HLA‐A*2402 + children, the percentage of terminal effector cells within the InsB 15–24 ‐specific CD8 + T cells was increased before diagnosis relative to samples taken before the appearance of autoantibodies. This is the first study, to our knowledge, to report HLA‐B*3906 ‐restricted autoreactive CD8 + T cells in T1D. Collectively, our results provide evidence that β cell‐reactive CD8 + T cells restricted by disease‐associated HLA class I molecules display an antigen‐experienced phenotype and acquire enhanced effector function during the period leading to clinical diagnosis, implicating these cells in driving disease. In this study, we characterised circulating autoreactive CD8 + T cells in children with type 1 diabetes with HLA-B*3906 + and HLA-A*2402 + genotypes which are associated with increased risk and early onset of disease. In HLA-B*3906 + children with newly diagnosed type 1 diabetes, we observed an increase in PPI 5–12 ‐specific transitional memory CD8 + T cells compared to non‐diabetic, age‐ and HLA‐matched subjects. Furthermore, PPI 5–12 ‐specific CD8 + T cells in HLA‐B*3906 + children with T1D showed a significantly more antigen‐experienced phenotype compared to polyclonal CD8 + T cells. Further, in longitudinal samples from high-risk HLA-A*2402 + children, the percentage of terminal effector cells within the InsB 15–24 ‐specific CD8 + T cell population was increased before diagnosis relative to samples taken before the appearance of autoantibodies. |
| Author | Dolton, G. Toppari, J. Veijola, R. Eichmann, M. Heck, S. Sewell, A. K. Yeo, L. Knip, M. Baptista, R. Mikk, M.‐L. Kronenberg‐Versteeg, D. Härkönen, T. Pujol‐Autonell, I. Peakman, M. Ilonen, J. |
| AuthorAffiliation | 4 Research Program for Clinical and Molecular Metabolism Faculty of Medicine University of Helsinki Helsinki Finland 3 Division of Infection and Immunity School of Medicine and Systems Immunity Research Institute Cardiff University Cardiff UK 6 Department of Paediatrics University of Turku and Turku University Hospital Turku Finland 11 Folkhälsan Research Centre Helsinki Finland 10 Department of Pediatrics Tampere University Hospital Tampere Finland 2 National Institute of Health Research Biomedical Research Centre at Guy’s and St Thomas’ Hospital and King’s College London London UK 12 Clinical Microbiology Turku University Hospital Turku Finland 13 King’s Health Partners Institute of Diabetes, Endocrinology and Obesity London UK 1 Department of Immunobiology Faculty of Life Sciences and Medicine King’s College London London UK 9 Children’s Hospital University of Helsinki and Helsinki University Hospital Helsinki Finland 5 Immunogenetics Laboratory Institute of Biomedicine University of Turku Tu |
| AuthorAffiliation_xml | – name: 11 Folkhälsan Research Centre Helsinki Finland – name: 7 Institute of Biomedicine Research Centre for Integrative Physiology and Pharmacology University of Turku Turku Finland – name: 2 National Institute of Health Research Biomedical Research Centre at Guy’s and St Thomas’ Hospital and King’s College London London UK – name: 3 Division of Infection and Immunity School of Medicine and Systems Immunity Research Institute Cardiff University Cardiff UK – name: 8 Department of Paediatrics PEDEGO Research Unit Medical Research Centre Oulu University Hospital and University of Oulu Oulu Finland – name: 10 Department of Pediatrics Tampere University Hospital Tampere Finland – name: 5 Immunogenetics Laboratory Institute of Biomedicine University of Turku Turku Finland – name: 1 Department of Immunobiology Faculty of Life Sciences and Medicine King’s College London London UK – name: 13 King’s Health Partners Institute of Diabetes, Endocrinology and Obesity London UK – name: 6 Department of Paediatrics University of Turku and Turku University Hospital Turku Finland – name: 9 Children’s Hospital University of Helsinki and Helsinki University Hospital Helsinki Finland – name: 12 Clinical Microbiology Turku University Hospital Turku Finland – name: 4 Research Program for Clinical and Molecular Metabolism Faculty of Medicine University of Helsinki Helsinki Finland |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31660582$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2019 British Society for Immunology 2019 British Society for Immunology. 2020 British Society for Immunology 2019 The Authors. published by John Wiley & Sons Ltd on behalf of British Society for Immunology |
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| DocumentTitleAlternate | Autoreactive diabetogenic T cells restricted by high‐risk class I HLA |
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| ISSN | 0009-9104 1365-2249 |
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| Issue | 3 |
| Keywords | HLA-A24 HLA-B39 CD8+ T cells type 1 diabetes |
| Language | English |
| License | https://creativecommons.org/licenses/by/4.0 2019 British Society for Immunology. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally to this work. |
| ORCID | 0000-0002-9638-4920 |
| OpenAccessLink | https://proxy.k.utb.cz/login?url=https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcei.13391 |
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| PublicationDate | March 2020 |
| PublicationDateYYYYMMDD | 2020-03-01 |
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| PublicationPlace | England |
| PublicationPlace_xml | – name: England – name: Oxford – name: Hoboken |
| PublicationTitle | Clinical and experimental immunology |
| PublicationTitleAlternate | Clin Exp Immunol |
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| Publisher | Oxford University Press John Wiley and Sons Inc |
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In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and... In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin-producing β cells. The HLA-B*3906 and HLA-A*2402... In type 1 diabetes (T1D), autoreactive cytotoxic CD8 T cells are implicated in the destruction of insulin-producing β cells. The HLA-B*3906 and HLA-A*2402... In type 1 diabetes (T1D), autoreactive cytotoxic CD8+ T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402... In type 1 diabetes (T1D), autoreactive cytotoxic CD8 + T cells are implicated in the destruction of insulin‐producing β cells. The HLA‐B*3906 and HLA‐A*2402... |
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| SubjectTerms | Antigens Autoantibodies Autoimmunity - immunology Beta cells CD8 antigen CD8+ T cells CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Child Child, Preschool Children Cytotoxicity Diabetes Diabetes mellitus (insulin dependent) Diabetes Mellitus, Type 1 - blood Diabetes Mellitus, Type 1 - immunology Diabetes Mellitus, Type 1 - metabolism Diagnosis Effector cells Female Flow cytometry Genotype & phenotype Histocompatibility antigen HLA Histocompatibility Antigens Class I - immunology Histocompatibility Antigens Class I - metabolism HLA-A24 Antigen - immunology HLA-A24 Antigen - metabolism HLA-B Antigens - immunology HLA-B Antigens - metabolism HLA‐A24 HLA‐B39 Humans Immunological memory Infant Insulin Insulin - immunology Insulin - metabolism Insulin-Secreting Cells - immunology Insulin-Secreting Cells - metabolism Lymphocytes Lymphocytes T Male Memory cells Original Pancreas Phenotypes Preproinsulin Protein Precursors - immunology Protein Precursors - metabolism Risk Factors type 1 diabetes |
| Title | Circulating β cell‐specific CD8+ T cells restricted by high‐risk HLA class I molecules show antigen experience in children with and at risk of type 1 diabetes |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcei.13391 https://www.ncbi.nlm.nih.gov/pubmed/31660582 https://www.proquest.com/docview/2352555129 https://www.proquest.com/docview/2310289069 https://pubmed.ncbi.nlm.nih.gov/PMC7008222 |
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