CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci

Abstract Chronic hyperglycemia is a major risk factor for glomerular or retinal microangiopathy and cardiovascular complications of type 1 diabetes (T1D). At the interface of genetics and environment, dynamic epigenetic changes associated with hyperglycemia may unravel some of the mechanisms contrib...

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Main Authors: Xiaojian Shao, Sophie Le Fur, Warren Cheung, Marie-Pierre Belot, Kevin Perge, Natacha Bouhours-Nouet, Candace Bensignor, Lucie Levaillant, Bing Ge, Tony Kwan, Mark Lathrop, Tomi Pastinen, Pierre Bougnères
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Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-82698-9
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author Xiaojian Shao
Sophie Le Fur
Warren Cheung
Marie-Pierre Belot
Kevin Perge
Natacha Bouhours-Nouet
Candace Bensignor
Lucie Levaillant
Bing Ge
Tony Kwan
Mark Lathrop
Tomi Pastinen
Pierre Bougnères
author_facet Xiaojian Shao
Sophie Le Fur
Warren Cheung
Marie-Pierre Belot
Kevin Perge
Natacha Bouhours-Nouet
Candace Bensignor
Lucie Levaillant
Bing Ge
Tony Kwan
Mark Lathrop
Tomi Pastinen
Pierre Bougnères
author_sort Xiaojian Shao
collection DOAJ
description Abstract Chronic hyperglycemia is a major risk factor for glomerular or retinal microangiopathy and cardiovascular complications of type 1 diabetes (T1D). At the interface of genetics and environment, dynamic epigenetic changes associated with hyperglycemia may unravel some of the mechanisms contributing to these T1D complications. In this study, blood samples were collected from 112 young patients at T1D diagnosis and 3 years later in average. Whole genome-wide bisulfite sequencing was used to measure blood DNA methylation changes of about 28 million CpGs at single base resolution over this time. Chronic hyperglycemia was estimated every 3–4 months by HbA1c measurement. Linear regressions with adjustment to age, sex, treatment duration, blood proportions and batch effects were employed to characterize the relationships between the dynamic changes of DNA methylation and average HbA1c levels. We identified that longitudinal DNA methylation changes at 815 CpGs (with suggestive p-value threshold of 1e-4) were associated with average HbA1c. Most of them (> 98%) were located outside of the promoter regions and were enriched in CpG island shores and multiple immune cell type specific accessible chromatin regions. Among the 36 more strongly associated loci (p-value < 5e-6), 16 were harbouring genes or non-coding sequences involved in angiogenesis regulation, glomerular and retinal vascularization or development, or coronary disease. Our findings support the identification of new genomic sites where CpG methylation associated with hyperglycemia may contribute to long-term complications of T1D, shedding light on potential mechanisms for further exploration.
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spelling doaj-art-8adf201e222e4941bba8b76d3e7c23882025-08-20T03:09:35ZengNature PortfolioScientific Reports2045-23222025-05-0115111210.1038/s41598-024-82698-9CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene lociXiaojian Shao0Sophie Le Fur1Warren Cheung2Marie-Pierre Belot3Kevin Perge4Natacha Bouhours-Nouet5Candace Bensignor6Lucie Levaillant7Bing Ge8Tony Kwan9Mark Lathrop10Tomi Pastinen11Pierre Bougnères12Digital Technologies Research Center, National Research Council CanadaGroupe d’Études Diabète-Obésité-Croissance, Assoc1901Genomic Medicine Center, Children’s Mercy - Kansas City and Children’s Mercy Research InstituteGroupe d’Études Diabète-Obésité-Croissance, Assoc1901Endocrinologie Pédiatrique, Hôpital Mère EnfantEndocrinologie et diabétologie pédiatriques , Hôpital universitaireCHU Dijon Bourgogne, Hôpital d’EnfantsEndocrinologie et diabétologie pédiatriques , Hôpital universitaireDepartment of Human Genetics, McGill University and McGill Genome CenterDepartment of Human Genetics, McGill University and McGill Genome CenterDepartment of Human Genetics, McGill University and McGill Genome CenterGenomic Medicine Center, Children’s Mercy - Kansas City and Children’s Mercy Research InstituteGroupe d’Études Diabète-Obésité-Croissance, Assoc1901Abstract Chronic hyperglycemia is a major risk factor for glomerular or retinal microangiopathy and cardiovascular complications of type 1 diabetes (T1D). At the interface of genetics and environment, dynamic epigenetic changes associated with hyperglycemia may unravel some of the mechanisms contributing to these T1D complications. In this study, blood samples were collected from 112 young patients at T1D diagnosis and 3 years later in average. Whole genome-wide bisulfite sequencing was used to measure blood DNA methylation changes of about 28 million CpGs at single base resolution over this time. Chronic hyperglycemia was estimated every 3–4 months by HbA1c measurement. Linear regressions with adjustment to age, sex, treatment duration, blood proportions and batch effects were employed to characterize the relationships between the dynamic changes of DNA methylation and average HbA1c levels. We identified that longitudinal DNA methylation changes at 815 CpGs (with suggestive p-value threshold of 1e-4) were associated with average HbA1c. Most of them (> 98%) were located outside of the promoter regions and were enriched in CpG island shores and multiple immune cell type specific accessible chromatin regions. Among the 36 more strongly associated loci (p-value < 5e-6), 16 were harbouring genes or non-coding sequences involved in angiogenesis regulation, glomerular and retinal vascularization or development, or coronary disease. Our findings support the identification of new genomic sites where CpG methylation associated with hyperglycemia may contribute to long-term complications of T1D, shedding light on potential mechanisms for further exploration.https://doi.org/10.1038/s41598-024-82698-9CpG methylationHyperglycemiaType 1 diabetes complicationsAngiogenesis
spellingShingle Xiaojian Shao
Sophie Le Fur
Warren Cheung
Marie-Pierre Belot
Kevin Perge
Natacha Bouhours-Nouet
Candace Bensignor
Lucie Levaillant
Bing Ge
Tony Kwan
Mark Lathrop
Tomi Pastinen
Pierre Bougnères
CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
Scientific Reports
CpG methylation
Hyperglycemia
Type 1 diabetes complications
Angiogenesis
title CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
title_full CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
title_fullStr CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
title_full_unstemmed CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
title_short CpG methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
title_sort cpg methylation changes associated with hyperglycemia in type 1 diabetes occur at angiogenic glomerular and retinal gene loci
topic CpG methylation
Hyperglycemia
Type 1 diabetes complications
Angiogenesis
url https://doi.org/10.1038/s41598-024-82698-9
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