Characterisation of the Circulating Transcriptomic Landscape in Inflammatory Bowel Disease Provides Evidence for Dysregulation of Multiple Transcription Factors Including NFE2, SPI1, CEBPB, and IRF2
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AIM: To assess the pathobiological and translational importance of whole-blood transcriptomic analysis in inflammatory bowel disease [IBD]. METHODS: We analysed whole-blood expression profiles from paired-end sequencing in a discovery cohort of 590 Europeans recruited across six countries in the IBD Character initiative (newly diagnosed patients with Crohn's disease [CD; n = 156], ulcerative colitis [UC; n = 167], and controls [n = 267]), exploring differential expression [DESeq2], co-expression networks [WGCNA], and transcription factor involvement [EPEE, ChEA, DoRothEA]. Findings were validated by analysis of an independent replication cohort [99 CD, 100 UC, 95 controls]. In the discovery cohort, we also defined baseline expression correlates of future treatment escalation using cross-validated elastic-net and random forest modelling, along with a pragmatic ratio detection procedure. RESULTS: Disease-specific transcriptomes were defined in IBD [8697 transcripts], CD [7152], and UC [8521], with the most highly significant changes in single genes, including CD177 (log2-fold change [LFC] = 4.63, p = 4.05 × 10-118), MCEMP1 [LFC = 2.45, p = 7.37 × 10-109], and S100A12 [LFC = 2.31, p = 2.15 × 10-93]. Significantly over-represented pathways included IL-1 [p = 1.58 × 10-11], IL-4, and IL-13 [p = 8.96 × 10-9]. Highly concordant results were obtained using multiple regulatory activity inference tools applied to the discovery and replication cohorts. These analyses demonstrated central roles in IBD for the transcription factors NFE2, SPI1 [PU.1], CEBPB, and IRF2, all regulators of cytokine signalling, based on a consistent signal across cohorts and transcription factor ranking methods. A number of simple transcriptome-based models were associated with the need for treatment escalation, including the binary CLEC5A/CDH2 expression ratio in UC (hazard ratio = 23.4, 95% confidence interval [CI] 5.3-102.0). CONCLUSIONS: Transcriptomic analysis has allowed for a detailed characterisation of IBD pathobiology, with important potential translational implications.
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These TFs have been previously reported to be associated with IBD in the literature.
“These TFs have been previously reported to be associated with IBD in the literature.”
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- Authors
- Nowak, J. K., Adams, A. T., Kalla, R., Lindstrøm, J. C., Vatn, S., Bergemalm, D., Keita, Å. V., Gomollón, F., Jahnsen, J., Vatn, M. H., Ricanek, P., Ostrowski, J., Walkowiak, J., Halfvarson, J., Satsangi, J., IBD Character Consortium, Andersson, E., Arnott, I. D., Bayes, M., Bonfiglio, F., Boyapati, R. K., Carstens, A., Casén, C., Ciemniejewska, E., D’Amato, M., A. Dahl, F., Detlie, T. E., Drummond, H. E., Ekeland, G. S., Ekman, D., Frengen, A. B., Gullberg, M., Gut, I. G., Gut, M., Heath, S. C., Hjelm, F., Hjortswang, H., Ho, G.-T., Jonkers, D., Kennedy, N. A., Lees, C. W., Lindahl, T., Lindqvist, M., Merkel, A., Modig, E., Moen, A. E. F., Nilsen, H., Nimmo, E. R., Noble, C. L., Nordberg, N., O’Leary, K. R., Ocklind, A., Olbjørn, C., Pettersson, E., Pierik, M., Poncelet, D., Repsilber, D., Sabatel, C., Schoemans, R., Shand, A. G., Söderholm, J. D., Sølvernes, J., Sundell, M., Tannæs, T. M., Törkvist, L., Veillard, A.-C., Ventham, N. T., Wilson, D. C., & You, P.
- Affiliations
- Poznan University of Medical Sciences (PL)
- John Radcliffe Hospital (GB)
- Centre for Inflammation Research (GB)
- University of Oslo (NO)
- Örebro University (SE)
- Linköping University (SE)
- Instituto de Investigación Sanitaria Aragón (ES)
- Akershus University Hospital (NO)
- The Maria Sklodowska-Curie National Research Institute of Oncology (PL)
- Department of Pediatric Gastroenterology and Metabolic Diseases, Poznan University of Medical Sciences , Poznan , Poland
- Corresponding author
- Nowak, Jan K
- Satsangi, Jack
- ORCID
- Nowak, Jan K
- Adams, Alex T
- Kalla, Rahul
- Lindstrøm, Jonas C
- Vatn, Simen
- Bergemalm, Daniel
- Keita, Åsa V
- Gomollón, Fernando
- Jahnsen, Jørgen
- Ricanek, Petr
- Ostrowski, Jerzy
- Halfvarson, Jonas
- Satsangi, Jack
- Arnott, Ian D
- Bonfiglio, Ferdinando
- Boyapati, Ray K
- Carstens, Adam
- D’Amato, Mauro
- Detlie, Trond Espen
- Ekeland, Gunn S
- Frengen, Anna B
- Gullberg, Mats
- Gut, Ivo G
- Heath, Simon C
- Hjortswang, Henrik
- Ho, Gwo-Tzer
- Jonkers, Daisy
- Kennedy, Nicholas A
- Merkel, Angelika
- Moen, Aina E F
- Nilsen, Hilde
- Olbjørn, Christine
- Pierik, Marieke
- Repsilber, Dirk
- Söderholm, Johan D
- Tannæs, Tone M
- Ventham, Nicholas T
- Venue
- Journal of Crohn's and Colitis
- Publisher
- Oxford University Press (OUP)
- Published
- 2022-02-25
- Volume
- 16
- Issue
- 8
- Pages
- 1255-1268
- ISSN
- 1873-9946 (ISSN-L)
- 1876-4479
- PMC
- PMC9426667
- OpenAlex
- W4213430069
- Cited by
- 51
- References
- 65
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 14 · 2023: 13 · 2022: 4 · 2013: 1
- FWCI
- 6.18
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Crohn s and Colitis (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc)
- Funders
- European Union’s Seventh Framework Programme (2858546)
- Polish National Science Centre (2017/25/B/NZ5/02783)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- inflammatory bowel disease, Crohn's disease
- MeSH terms
- Colitis, Ulcerative, Crohn Disease, Humans, Receptors, Cell Surface, Transcription Factors, Inflammatory Bowel Diseases, CCAAT-Enhancer-Binding Protein-beta, Lectins, C-Type, Interferon Regulatory Factor-2, Transcriptome
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