Gestational respiratory infections interacting with offspring HLA and CTLA-4 modifies incident β-cell autoantibodies
β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tes...
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| Published in: | Journal of autoimmunity Vol. 86; pp. 93 - 103 |
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| Main Authors: | , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Elsevier Ltd
01-01-2018
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| Abstract | β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tested if gestational infections and interactions with child's human leukocyte antigen (HLA) and non-HLA genes affected the appearance of the first β-cell autoantibody. Singletons of mothers without diabetes (n = 7472) with T1D-associated HLA-DR-DQ genotypes were prospectively followed quarterly through the first 4 years of life, then semiannually until age 6 years, using standardized autoantibody analyses. Maternal infections during pregnancy were assessed via questionnaire 3–4.5 months post-delivery. Polymorphisms in twelve non-HLA genes associated with the first appearing β-cell autoantibodies were included in a Cox regression analysis. IAA predominated as the first appearing β-cell autoantibody in younger children (n = 226, median age at seroconversion 1.8 years) and GADA (n = 212; 3.2 years) in children aged ≥2 years. Gestational infections were not associated with the first appearing β-cell autoantibodies overall. However, gestational respiratory infections (G-RI) showed a consistent protective influence on IAA (HR 0.64, 95% CI 0.45–0.91) among CTLA4-(AG, GG) children (G-RI*CTLA4 interaction, p = 0.002). The predominant associations of HLA-DR-DQ 4-8/8-4 with IAA and HLA-DR-DQ 3-2/3-2 with GADA were not observed if a G-RI was reported (G-RI*HLA-DR-DQ interaction, p = 0.03). The role of G-RI may depend on offspring HLA and CTLA-4 alleles and supports a bidirectional trigger for IAA or GADA as a first appearing β-cell autoantibody in early life.
•The first β-cell autoantibody to appear in children depends on T1D-associated genes.•IAA as first appears in younger children, GADA-first in children older than 2 years.•Gestational respiratory infections (G-RI) protective of IAA-first among CTLA4-G children.•Strong HLA association with IAA-first and GADA-first not observed if a G-RI reported.•G-RI role in early life depends on offspring HLA and CTLA-4 alleles. |
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| AbstractList | β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tested if gestational infections and interactions with child's human leukocyte antigen (HLA) and non-HLA genes affected the appearance of the first β-cell autoantibody. Singletons of mothers without diabetes (n = 7472) with T1D-associated HLA-DR-DQ genotypes were prospectively followed quarterly through the first 4 years of life, then semiannually until age 6 years, using standardized autoantibody analyses. Maternal infections during pregnancy were assessed via questionnaire 3–4.5 months post-delivery. Polymorphisms in twelve non-HLA genes associated with the first appearing β-cell autoantibodies were included in a Cox regression analysis. IAA predominated as the first appearing β-cell autoantibody in younger children (n = 226, median age at seroconversion 1.8 years) and GADA (n = 212; 3.2 years) in children aged ≥2 years. Gestational infections were not associated with the first appearing β-cell autoantibodies overall. However, gestational respiratory infections (G-RI) showed a consistent protective influence on IAA (HR 0.64, 95% CI 0.45–0.91) among CTLA4-(AG, GG) children (G-RI*CTLA4 interaction, p = 0.002). The predominant associations of HLA-DR-DQ 4-8/8-4 with IAA and HLA-DR-DQ 3-2/3-2 with GADA were not observed if a G-RI was reported (G-RI*HLA-DR-DQ interaction, p = 0.03). The role of G-RI may depend on offspring HLA and CTLA-4 alleles and supports a bidirectional trigger for IAA or GADA as a first appearing β-cell autoantibody in early life.
•The first β-cell autoantibody to appear in children depends on T1D-associated genes.•IAA as first appears in younger children, GADA-first in children older than 2 years.•Gestational respiratory infections (G-RI) protective of IAA-first among CTLA4-G children.•Strong HLA association with IAA-first and GADA-first not observed if a G-RI reported.•G-RI role in early life depends on offspring HLA and CTLA-4 alleles. β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tested if gestational infections and interactions with child’s human leukocyte antigen (HLA) and non-HLA genes affected the appearance of the first β-cell autoantibody. Singletons of mothers without diabetes (n=7472) with T1D-associated HLA-DR-DQ genotypes were prospectively followed quarterly through the first 4 years of life, then semiannually until age 6 years, using standardized autoantibody analyses. Maternal infections during pregnancy were assessed via questionnaire 3–4.5 months post-delivery. Polymorphisms in twelve non-HLA genes associated with the first appearing β-cell autoantibodies were included in a Cox regression analysis. IAA predominated as the first appearing β-cell autoantibody in younger children (n=226, median age at seroconversion 1.8 years) and GADA (n=212; 3.2 years) in children aged ≥2 years. Gestational infections were not associated with the first appearing β-cell autoantibodies overall. However, gestational respiratory infections (G-RI) showed a consistent protective influence on IAA (HR 0.64, 95% CI 0.45–0.91) among CTLA4 -(AG, GG) children (G-RI* CTLA4 interaction, p=0.002). The predominant associations of HLA-DR-DQ 4-8/8-4 with IAA and HLA-DR-DQ 3-2/3-2 with GADA were not observed if a G-RI was reported (G-RI*HLA-DR-DQ interaction, p=0.03). The role of G-RI may depend on offspring HLA and CTLA-4 alleles and supports a bidirectional trigger for IAA or GADA as a first appearing β-cell autoantibody in early life. β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tested if gestational infections and interactions with child's human leukocyte antigen (HLA) and non-HLA genes affected the appearance of the first β-cell autoantibody. Singletons of mothers without diabetes (n = 7472) with T1D-associated HLA-DR-DQ genotypes were prospectively followed quarterly through the first 4 years of life, then semiannually until age 6 years, using standardized autoantibody analyses. Maternal infections during pregnancy were assessed via questionnaire 3-4.5 months post-delivery. Polymorphisms in twelve non-HLA genes associated with the first appearing β-cell autoantibodies were included in a Cox regression analysis. IAA predominated as the first appearing β-cell autoantibody in younger children (n = 226, median age at seroconversion 1.8 years) and GADA (n = 212; 3.2 years) in children aged ≥2 years. Gestational infections were not associated with the first appearing β-cell autoantibodies overall. However, gestational respiratory infections (G-RI) showed a consistent protective influence on IAA (HR 0.64, 95% CI 0.45-0.91) among CTLA4-(AG, GG) children (G-RI*. CTLA4 interaction, p = 0.002). The predominant associations of HLA-DR-DQ 4-8/8-4 with IAA and HLA-DR-DQ 3-2/3-2 with GADA were not observed if a G-RI was reported (G-RI*HLA-DR-DQ interaction, p = 0.03). The role of G-RI may depend on offspring HLA and CTLA-4 alleles and supports a bidirectional trigger for IAA or GADA as a first appearing β-cell autoantibody in early life. β-cell autoantibodies against insulin (IAA), GAD65 (GADA) and IA-2 (IA-2A) precede onset of childhood type 1 diabetes (T1D). Incidence of the first appearing β-cell autoantibodies peaks at a young age and is patterned by T1D-associated genes, suggesting an early environmental influence. Here, we tested if gestational infections and interactions with child's human leukocyte antigen (HLA) and non-HLA genes affected the appearance of the first β-cell autoantibody. Singletons of mothers without diabetes (n = 7472) with T1D-associated HLA-DR-DQ genotypes were prospectively followed quarterly through the first 4 years of life, then semiannually until age 6 years, using standardized autoantibody analyses. Maternal infections during pregnancy were assessed via questionnaire 3-4.5 months post-delivery. Polymorphisms in twelve non-HLA genes associated with the first appearing β-cell autoantibodies were included in a Cox regression analysis. IAA predominated as the first appearing β-cell autoantibody in younger children (n = 226, median age at seroconversion 1.8 years) and GADA (n = 212; 3.2 years) in children aged ≥2 years. Gestational infections were not associated with the first appearing β-cell autoantibodies overall. However, gestational respiratory infections (G-RI) showed a consistent protective influence on IAA (HR 0.64, 95% CI 0.45-0.91) among CTLA4-(AG, GG) children (G-RI*CTLA4 interaction, p = 0.002). The predominant associations of HLA-DR-DQ 4-8/8-4 with IAA and HLA-DR-DQ 3-2/3-2 with GADA were not observed if a G-RI was reported (G-RI*HLA-DR-DQ interaction, p = 0.03). The role of G-RI may depend on offspring HLA and CTLA-4 alleles and supports a bidirectional trigger for IAA or GADA as a first appearing β-cell autoantibody in early life. |
| Author | Bonifacio, Ezio Krischer, Jeffrey P. Hagopian, William A. Lee, Hye-Seung Toppari, Jorma Rewers, Marian J. She, Jin-Xiong Lynch, Kristian F. Haller, Michael J. Ziegler, Anette-G. Hyöty, Heikki Akolkar, Beena Vehik, Kendra Larsson, Helena Elding Lernmark, Åke Törn, Carina Simell, Olli G. |
| AuthorAffiliation | f Center for Biotechnology and Genomic Medicine, Medical College of Georgia, Augusta University, Augusta GA, U.S.A e Barbara Davis Center for Childhood Diabetes, University of Colorado, Aurora CO, U.S.A i Institute of Diabetes Research, Helmholtz Zentrum München, and Klinikum rechts der Isar, Technische Universität München, and Forschergruppe Diabetes e.V., Neuherberg, Germany h Department of Physiology, Institute of Biomedicine, University of Turku, Turku, Finland k Department of Virology, Faculty of Medicine and Lifesciences, University of Tampere, Tampere, Finland c Department of Pediatrics, University of Florida Gainesville, Gainesville, FL l Fimlab Laboratories, Pirkannmaa Hospital District, Tampere, Finland a Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa FL, U.S.A b Department of Clinical Sciences Malmö, Lund University/CRC, Skåne University Hospital SUS, Malmö, Sweden g Department of Pediatrics, Turku University Hospital, Turku, Finland j Na |
| AuthorAffiliation_xml | – name: e Barbara Davis Center for Childhood Diabetes, University of Colorado, Aurora CO, U.S.A – name: h Department of Physiology, Institute of Biomedicine, University of Turku, Turku, Finland – name: j National Institute of Diabetes & Digestive & Kidney Diseases, Bethesda MD, U.S.A – name: d Pacific Northwest Diabetes Research Institute, Seattle WA, U.S.A – name: g Department of Pediatrics, Turku University Hospital, Turku, Finland – name: a Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa FL, U.S.A – name: c Department of Pediatrics, University of Florida Gainesville, Gainesville, FL – name: i Institute of Diabetes Research, Helmholtz Zentrum München, and Klinikum rechts der Isar, Technische Universität München, and Forschergruppe Diabetes e.V., Neuherberg, Germany – name: k Department of Virology, Faculty of Medicine and Lifesciences, University of Tampere, Tampere, Finland – name: l Fimlab Laboratories, Pirkannmaa Hospital District, Tampere, Finland – name: f Center for Biotechnology and Genomic Medicine, Medical College of Georgia, Augusta University, Augusta GA, U.S.A – name: m Center for Regenerative Therapies Dresden, Dresden University of Technology, Dresden, Germany, and the – name: b Department of Clinical Sciences Malmö, Lund University/CRC, Skåne University Hospital SUS, Malmö, Sweden |
| Author_xml | – sequence: 1 givenname: Kristian F. surname: Lynch fullname: Lynch, Kristian F. email: Kristian.Lynch@epi.usf.edu organization: Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, USA – sequence: 2 givenname: Hye-Seung surname: Lee fullname: Lee, Hye-Seung organization: Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, USA – sequence: 3 givenname: Carina surname: Törn fullname: Törn, Carina organization: Department of Clinical Sciences Malmö, Lund University/CRC, Skåne University Hospital SUS, Malmö, Sweden – sequence: 4 givenname: Kendra surname: Vehik fullname: Vehik, Kendra organization: Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, USA – sequence: 5 givenname: Jeffrey P. orcidid: 0000-0003-4526-888X surname: Krischer fullname: Krischer, Jeffrey P. organization: Health Informatics Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, USA – sequence: 6 givenname: Helena Elding orcidid: 0000-0003-3306-1742 surname: Larsson fullname: Larsson, Helena Elding organization: Department of Clinical Sciences Malmö, Lund University/CRC, Skåne University Hospital SUS, Malmö, Sweden – sequence: 7 givenname: Michael J. surname: Haller fullname: Haller, Michael J. organization: Department of Pediatrics, University of Florida Gainesville, Gainesville, FL, USA – sequence: 8 givenname: William A. surname: Hagopian fullname: Hagopian, William A. organization: Pacific Northwest Diabetes Research Institute, Seattle, WA, USA – sequence: 9 givenname: Marian J. surname: Rewers fullname: Rewers, Marian J. organization: Barbara Davis Center for Childhood Diabetes, University of Colorado, Aurora, CO, USA – sequence: 10 givenname: Jin-Xiong surname: She fullname: She, Jin-Xiong organization: Center for Biotechnology and Genomic Medicine, Medical College of Georgia, Augusta University, Augusta, GA, USA – sequence: 11 givenname: Olli G. surname: Simell fullname: Simell, Olli G. organization: Department of Pediatrics, Turku University Hospital, Turku, Finland – sequence: 12 givenname: Jorma orcidid: 0000-0003-2228-334X surname: Toppari fullname: Toppari, Jorma organization: Department of Pediatrics, Turku University Hospital, Turku, Finland – sequence: 13 givenname: Anette-G. surname: Ziegler fullname: Ziegler, Anette-G. organization: Institute of Diabetes Research, Helmholtz Zentrum München, Neuherberg, Germany – sequence: 14 givenname: Beena surname: Akolkar fullname: Akolkar, Beena organization: National Institute of Diabetes & Digestive & Kidney Diseases, Bethesda, MD, USA – sequence: 15 givenname: Heikki surname: Hyöty fullname: Hyöty, Heikki organization: Department of Virology, Faculty of Medicine and Lifesciences, University of Tampere, Tampere, Finland – sequence: 16 givenname: Ezio surname: Bonifacio fullname: Bonifacio, Ezio organization: Center for Regenerative Therapies Dresden, Dresden University of Technology, Dresden, Germany – sequence: 17 givenname: Åke orcidid: 0000-0003-1735-0499 surname: Lernmark fullname: Lernmark, Åke organization: Department of Clinical Sciences Malmö, Lund University/CRC, Skåne University Hospital SUS, Malmö, Sweden |
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| Keywords | Autoimmunity Type 1 diabetes β-cell autoantibodies Autoimmune diabetes Glutamic acid decarboxylase HLA Insulin IA-2 |
| Language | English |
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| SubjectTerms | Autoantibodies - metabolism Autoimmune diabetes Autoimmunity Clinical Medicine CTLA-4 Antigen - metabolism Endocrinology and Diabetes Endokrinologi och diabetes Female Gestational Age Glutamate Decarboxylase - immunology Glutamic acid decarboxylase HLA HLA-DQ Antigens - genetics HLA-DQ Antigens - metabolism HLA-DR Antigens - genetics HLA-DR Antigens - metabolism Humans IA-2 Infant Insulin Insulin - immunology Insulin-Secreting Cells - immunology Klinisk medicin Male Medical and Health Sciences Medicin och hälsovetenskap Polymorphism, Genetic Pregnancy Prenatal Exposure Delayed Effects - epidemiology Prenatal Exposure Delayed Effects - immunology Receptor-Like Protein Tyrosine Phosphatases, Class 8 - immunology Respiratory Tract Infections - epidemiology Respiratory Tract Infections - immunology Type 1 diabetes β-cell autoantibodies |
| Title | Gestational respiratory infections interacting with offspring HLA and CTLA-4 modifies incident β-cell autoantibodies |
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