Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1

Ligtenberg, Marjolijn J L; Kuiper, Roland P; Chan, Tsun Leung; Goossens, Monique; Hebeda, Konnie M; Voorendt, Marsha; Lee, Tracy Y H; Bodmer, Danielle; Hoenselaar, Eveline; Hendriks-Cornelissen, Sandra J B; Tsui, Wai Yin; Kong, Chi Kwan; Brunner, Han G; van Kessel, Ad Geurts; Yuen, Siu Tsan; van Krieken, J Han J M; Leung, Suet Yi; Hoogerbrugge, Nicoline

doi:10.1038/ng.283

Cited by 827Genetic factors in colorectal cancerEpigenetics and DNA MethylationDNA Repair Mechanisms

Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1

Ligtenberg, Marjolijn J L, Kuiper, Roland P, Chan, Tsun Leung, Goossens, Monique, Hebeda, Konnie M, Voorendt, Marsha, Lee, Tracy Y H, Bodmer, Danielle +10 more·2009·Nature Genetics

DOI 10.1038/ng.283

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Abstract

Lynch syndrome patients are susceptible to colorectal and endometrial cancers owing to inactivating germline mutations in mismatch repair genes, including MSH2 (ref. 1). Here we describe patients from Dutch and Chinese families with MSH2-deficient tumors carrying heterozygous germline deletions of the last exons of TACSTD1, a gene directly upstream of MSH2 encoding Ep-CAM. Due to these deletions, transcription of TACSTD1 extends into MSH2. The MSH2 promoter in cis with the deletion is methylated in Ep-CAM positive but not in Ep-CAM negative normal tissues, thus revealing a correlation between activity of the mutated TACSTD1 allele and epigenetic inactivation of the corresponding MSH2 allele. Gene silencing by transcriptional read-through of a neighboring gene in either sense, as demonstrated here, or antisense direction, could represent a general mutational mechanism. Depending on the expression pattern of the neighboring gene that lacks its normal polyadenylation signal, this may cause either generalized or mosaic patterns of epigenetic inactivation.

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In these cases, the abnormal DNA methylation of the gene under investigation was linked to a mutation in a neighboring gene that removed the transcription termination signal.
“In these cases, the abnormal DNA methylation of the gene under investigation was linked to a mutation in a neighboring gene that removed the transcription termination signal (Fig. 1b).”
From A critical view on transgenerational epigenetic inheritance in humans (2018) · cites this paper as [16]
Several studies including Guéant et al. have reported the co-segregation of an abnormal DNA methylation pattern (epimutation) with a rare disease in two or more generations of certain families.
“Several studies14–16 including a recent study by Guéant et al.18 in this journal, have reported the co-segregation of an abnormal DNA methylation pattern (called “epimutation”) with a rare disease in two or more generations of certain families.”
From A critical view on transgenerational epigenetic inheritance in humans (2018) · cites this paper as [16]
Most cases of segregation of abnormal DNA methylation patterns in families with rare diseases turned out to be caused by an underlying genetic variant.
“Most cases of segregation of abnormal DNA methylation patterns in families with rare diseases, however, turned out to be caused by an underlying genetic variant14–16 (see below).”
From A critical view on transgenerational epigenetic inheritance in humans (2018) · cites this paper as [16]
As a consequence, transcription from this gene extended into the gene under investigation, causing abnormal promoter methylation and gene silencing.
“As a consequence, transcription from this gene extended into the gene under investigation, causing abnormal promoter methylation and gene silencing.”
From A critical view on transgenerational epigenetic inheritance in humans (2018) · cites this paper as [16]

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Self-citation

Authors: Ligtenberg, M. J. L., Kuiper, R. P., Chan, T. L., Goossens, M., Hebeda, K. M., Voorendt, M., Lee, T. Y. H., Bodmer, D., Hoenselaar, E., Hendriks-Cornelissen, S. J. B., Tsui, W. Y., Kong, C. K., Brunner, H. G., van Kessel, A. G., Yuen, S. T., van Krieken, J. H. J. M., Leung, S. Y., & Hoogerbrugge, N.
Affiliations: Radboud University Medical Center (NL)
Queen Mary Hospital (CN)
Yan Chai Hospital (HK)
Corresponding author: Ligtenberg, Marjolijn J L
Leung, Suet Yi
ORCID: Ligtenberg, Marjolijn J L
Kuiper, Roland P
Chan, Tsun Leung
Hebeda, Konnie M
Tsui, Wai Yin
Kong, Chi Kwan
Brunner, Han G
Yuen, Siu Tsan
Hoogerbrugge, Nicoline
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2008-12-21
Volume: 41
Issue: 1
Pages: 112-117
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/ng.283
OpenAlex: W1972254989
Cited by: 818
References: 25
Citations by year: 2026: 19 · 2025: 34 · 2024: 38 · 2023: 45 · 2022: 34 · 2021: 41 · 2020: 59 · 2019: 44 · 2018: 54 · 2017: 51 · 2016: 56 · 2015: 46 · 2014: 59 · 2013: 71 · 2012: 49
FWCI: 27.68
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Keywords: Lynch syndrome, MSH2, EpCAM, germline deletion, read-through transcription, epigenetic silencing, mismatch repair genes, colorectal cancer, endometrial cancer, polyadenylation signal, gene silencing
MeSH terms: Epithelial Cell Adhesion Molecule, Adolescent, Adult, Alleles, Antigens, Neoplasm, Base Sequence, China, Colorectal Neoplasms, Hereditary Nonpolyposis, Exons, Family, Female, Humans, Male, Middle Aged, Molecular Sequence Data, Netherlands, Pedigree, Promoter Regions, Genetic, Cell Adhesion Molecules, Open Reading Frames, Sequence Deletion, DNA Methylation, Inheritance Patterns, White People, Asian People, MutS Homolog 2 Protein, Microsatellite Instability

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Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1

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