A new class of human CpG Island promoters with primate-specific repeats

Abstract A subset of imprinting control regions (ICRs) in the human and mouse possess CpG islands associated with imperfect tandem repeats (TRs) that were shown to be essential for genomic imprinting through genetic studies. To identify whether this feature is also present in non-imprinted CpG islan...

Full description

Saved in:
Bibliographic Details
Main Authors: K. Naga Mohan, Anuhya Anne, Lov Kumar, J. Richard Chaillet
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-11213-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849333613224525824
author K. Naga Mohan
Anuhya Anne
Lov Kumar
J. Richard Chaillet
author_facet K. Naga Mohan
Anuhya Anne
Lov Kumar
J. Richard Chaillet
author_sort K. Naga Mohan
collection DOAJ
description Abstract A subset of imprinting control regions (ICRs) in the human and mouse possess CpG islands associated with imperfect tandem repeats (TRs) that were shown to be essential for genomic imprinting through genetic studies. To identify whether this feature is also present in non-imprinted CpG island promoters, we performed extensive dot plot analyses and identified 342 (326 autosomal and 16 X-chromosomal) human CpG island gene promoters associated with imperfect TRs of ≥ 400 bp, unit lengths 50–150 bp. Most occur as clusters at the human chromosome ends, distinct from the clusters of imprinted genes, and enriched in neurodevelopmental/behavioral disorders, with some showing interindividual variation in methylation levels. A subset of TR-CGIs is highly methylated and remains so during reprogramming to primed iPSCs, but become unmethylated in naïve iPSCs, as in the case of ICRs. Transcript levels correlate with methylation levels for some TR-CGI genes suggesting their gene regulatory potential. Non-TR CGI mouse orthologs of methylated human TR-CGIs are unmethylated in mouse, suggesting the association of TRs with higher methylation levels. Most human TR-CGIs accompanied primate evolution after divergence from mouse TR-CGIs with evidence of recent additions in hominid evolution. In summary, the incorporation of TRs in certain CGI promoters in mammalian evolution results in the unique ability to acquire methylation during human embryonic development and resist reprogramming to a pluripotent stem cell state with an effect on gene expression.
format Article
id doaj-art-1cc785de622844e887dc9f4e2aa7cab5
institution Kabale University
issn 2045-2322
language English
publishDate 2025-07-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-1cc785de622844e887dc9f4e2aa7cab52025-08-20T03:45:48ZengNature PortfolioScientific Reports2045-23222025-07-0115111410.1038/s41598-025-11213-5A new class of human CpG Island promoters with primate-specific repeatsK. Naga Mohan0Anuhya Anne1Lov Kumar2J. Richard Chaillet3Molecular Biology and Genetics laboratory, Department of Biological Sciences, Birla Institute of Technology and Science, Centre for Human Disease Research, Birla Institute of Technology and ScienceMolecular Biology and Genetics laboratory, Department of Biological Sciences, Birla Institute of Technology and Science, Centre for Human Disease Research, Birla Institute of Technology and ScienceDepartment of Computer Engineering, National Institute of TechnologyDepartment of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of MedicineAbstract A subset of imprinting control regions (ICRs) in the human and mouse possess CpG islands associated with imperfect tandem repeats (TRs) that were shown to be essential for genomic imprinting through genetic studies. To identify whether this feature is also present in non-imprinted CpG island promoters, we performed extensive dot plot analyses and identified 342 (326 autosomal and 16 X-chromosomal) human CpG island gene promoters associated with imperfect TRs of ≥ 400 bp, unit lengths 50–150 bp. Most occur as clusters at the human chromosome ends, distinct from the clusters of imprinted genes, and enriched in neurodevelopmental/behavioral disorders, with some showing interindividual variation in methylation levels. A subset of TR-CGIs is highly methylated and remains so during reprogramming to primed iPSCs, but become unmethylated in naïve iPSCs, as in the case of ICRs. Transcript levels correlate with methylation levels for some TR-CGI genes suggesting their gene regulatory potential. Non-TR CGI mouse orthologs of methylated human TR-CGIs are unmethylated in mouse, suggesting the association of TRs with higher methylation levels. Most human TR-CGIs accompanied primate evolution after divergence from mouse TR-CGIs with evidence of recent additions in hominid evolution. In summary, the incorporation of TRs in certain CGI promoters in mammalian evolution results in the unique ability to acquire methylation during human embryonic development and resist reprogramming to a pluripotent stem cell state with an effect on gene expression.https://doi.org/10.1038/s41598-025-11213-5DNA methylationEpigenetic reprogrammingStem cellsCpG IslandHuman evolutionGenome organization
spellingShingle K. Naga Mohan
Anuhya Anne
Lov Kumar
J. Richard Chaillet
A new class of human CpG Island promoters with primate-specific repeats
Scientific Reports
DNA methylation
Epigenetic reprogramming
Stem cells
CpG Island
Human evolution
Genome organization
title A new class of human CpG Island promoters with primate-specific repeats
title_full A new class of human CpG Island promoters with primate-specific repeats
title_fullStr A new class of human CpG Island promoters with primate-specific repeats
title_full_unstemmed A new class of human CpG Island promoters with primate-specific repeats
title_short A new class of human CpG Island promoters with primate-specific repeats
title_sort new class of human cpg island promoters with primate specific repeats
topic DNA methylation
Epigenetic reprogramming
Stem cells
CpG Island
Human evolution
Genome organization
url https://doi.org/10.1038/s41598-025-11213-5
work_keys_str_mv AT knagamohan anewclassofhumancpgislandpromoterswithprimatespecificrepeats
AT anuhyaanne anewclassofhumancpgislandpromoterswithprimatespecificrepeats
AT lovkumar anewclassofhumancpgislandpromoterswithprimatespecificrepeats
AT jrichardchaillet anewclassofhumancpgislandpromoterswithprimatespecificrepeats
AT knagamohan newclassofhumancpgislandpromoterswithprimatespecificrepeats
AT anuhyaanne newclassofhumancpgislandpromoterswithprimatespecificrepeats
AT lovkumar newclassofhumancpgislandpromoterswithprimatespecificrepeats
AT jrichardchaillet newclassofhumancpgislandpromoterswithprimatespecificrepeats