Genetic and epigenetic characteristics of inflammatory bowel disease-associated colorectal cancer
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BACKGROUND & AIMS: Inflammatory bowel disease (IBD) is a chronic, relapsing inflammatory disorder associated with an elevated risk of colorectal cancer (CRC). IBD-associated CRC (IBD-CRC) may represent a distinct pathway of tumorigenesis compared to sporadic CRC (sCRC). Our aim was to comprehensively characterize IBD-associated tumorigenesis integrating multiple high-throughput approaches, and to compare the results with in-house data sets from sCRCs. METHODS: Whole-genome sequencing, single nucleotide polymorphism arrays, RNA sequencing, genome-wide methylation analysis, and immunohistochemistry were performed using fresh-frozen and formalin-fixed tissue samples of tumor and corresponding normal tissues from 31 patients with IBD-CRC. RESULTS: Transcriptome-based tumor subtyping revealed the complete absence of canonical epithelial tumor subtype associated with WNT signaling in IBD-CRCs, dominated instead by mesenchymal stroma-rich subtype. Negative WNT regulators AXIN2 and RNF43 were strongly down-regulated in IBD-CRCs and chromosomal gains at HNF4A, a negative regulator of WNT-induced epithelial-mesenchymal transition (EMT), were less frequent compared to sCRCs. Enrichment of hypomethylation at HNF4α binding sites was detected solely in sCRC genomes. PIGR and OSMR involved in mucosal immunity were dysregulated via epigenetic modifications in IBD-CRCs. Genome-wide analysis showed significant enrichment of noncoding mutations to 5'untranslated region of TP53 in IBD-CRCs. As reported previously, somatic mutations in APC and KRAS were less frequent in IBD-CRCs compared to sCRCs. CONCLUSIONS: Distinct mechanisms of WNT pathway dysregulation skew IBD-CRCs toward mesenchymal tumor subtype, which may affect prognosis and treatment options. Increased OSMR signaling may favor the establishment of mesenchymal tumors in patients with IBD.
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The profile of inflammatory bowel disease-related colorectal cancer mainly falls in the CMS4 group.
“the profile of inflammatory bowel disease–related colorectal cancer mainly falls in the CMS4 group (25).”
From Clinical Challenges of Consensus Molecular Subtype CMS4 Colon Cancer in the Era of Precision Medicine (2024) · cites this paper as [25]
The CMS4 tumor state arises from the progression of a less aggressive state, rather than originating from a distinct carcinogenesis pathway, perhaps with the exception of inflammation-induced colorectal cancer.
“Altogether, several works based on paired tumor regions (11, 19, 30) support the notion that the CMS4 tumor state arises from the progression of a less aggressive state, rather than originating from a distinct carcinogenesis pathway, perhaps with the exception of inflammation-induced colorectal cancer (25).”
From Clinical Challenges of Consensus Molecular Subtype CMS4 Colon Cancer in the Era of Precision Medicine (2024) · cites this paper as [25]
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- Authors
- Rajamäki, K., Taira, A., Katainen, R., Välimäki, N., Kuosmanen, A., Plaketti, R.-M., Seppälä, T. T., Ahtiainen, M., Wirta, E.-V., Vartiainen, E., Sulo, P., Ravantti, J., Lehtipuro, S., Granberg, K. J., Nykter, M., Tanskanen, T., Ristimäki, A., Koskensalo, S., Renkonen-Sinisalo, L., Lepistö, A., Böhm, J., Taipale, J., Mecklin, J.-P., Aavikko, M., Palin, K., & Aaltonen, L. A.
- Affiliations
- University of Helsinki (FI)
- Central Finland Health Care District (FI)
- Tampere University Hospital (FI)
- Tampere University (FI)
- Finnish Cancer Registry (FI)
- Corresponding author
- Rajamäki, Kristiina
- Aaltonen, Lauri A.
- ORCID
- Rajamäki, Kristiina
- Taira, Aurora
- Katainen, Riku
- Välimäki, Niko
- Kuosmanen, Anna
- Seppälä, Toni T.
- Ahtiainen, Maarit
- Wirta, Erkki-Ville
- Vartiainen, Emilia
- Sulo, Päivi
- Ravantti, Janne
- Nykter, Matti
- Tanskanen, Tomas
- Koskensalo, Selja
- Lepistö, Anna
- Böhm, Jan
- Taipale, Jussi
- Mecklin, Jukka-Pekka
- Aavikko, Mervi
- Palin, Kimmo
- Aaltonen, Lauri A.
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2021-08
- Volume
- 161
- Issue
- 2
- Pages
- 592-607
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W3159023541
- Cited by
- 230
- References
- 77
- Citations by year
- 2026: 38 · 2025: 45 · 2024: 45 · 2023: 50 · 2022: 46 · 2021: 5
- FWCI
- 24.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gastroenterology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Jyväskylä University Digital Archive (University of Jyväskylä) (submittedVersion, cc-by-nc-nd)
- Työväentutkimus Vuosikirja (submittedVersion)
- Tampere University Institutional Repository (Tampere University) (submittedVersion, cc-by-nc-nd)
- Funders
- Helsingin Yliopisto
- Emil Aaltosen Säätiö
- Helsingin ja Uudenmaan Sairaanhoitopiiri
- Sigrid Juséliuksen Säätiö
- Suomen Lääketieteen Säätiö
- Instrumentariumin Tiedesäätiö
- Finska Läkaresällskapet
- Syöpäsäätiö
- Suomen Akatemia
- Itä-Suomen Yliopisto
- Jane ja Aatos Erkon Säätiö
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- inflammatory bowel disease-associated colorectal cancer, sporadic colorectal cancer, Wnt signaling, epithelial-mesenchymal transition, HNF4α, DNA methylation, tumor transcriptome, Axin2, RNF43, OSMR, polymeric immunoglobulin receptor, mucosal immunity, APC, KRAS, non-coding mutations, carcinogenesis
- MeSH terms
- Whole Genome Sequencing, Colitis-Associated Neoplasms, Adult, Aged, Aged, 80 and over, Cell Transformation, Neoplastic, DNA Mutational Analysis, Female, Finland, Humans, Male, Middle Aged, Mutation, Neoplasm Staging, Biomarkers, Tumor, Inflammatory Bowel Diseases, Sequence Analysis, RNA, DNA Methylation, Oligonucleotide Array Sequence Analysis, Polymorphism, Single Nucleotide, Gene Expression Profiling, Epigenesis, Genetic, Epigenomics, High-Throughput Nucleotide Sequencing, Tumor Microenvironment, Transcriptome, Neoplasm Grading
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