Response to IL-6 trans- and IL-6 classic signalling is determined by the ratio of the IL-6 receptor α to gp130 expression: fusing experimental insights and dynamic modelling
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BACKGROUND: Interleukin-6 is a pleiotropic cytokine with high clinical relevance and an important mediator of cellular communication, orchestrating both pro- and anti-inflammatory processes. Interleukin-6-induced signalling is initiated by binding of IL-6 to the IL-6 receptor α and subsequent binding to the signal transducing receptor subunit gp130. This active receptor complex initiates signalling through the Janus kinase/signal transducer and activator of transcription pathway. Of note, IL-6 receptor α exists in a soluble and a transmembrane form. Binding of IL-6 to membrane-bound IL-6 receptor α induces anti-inflammatory classic signalling, whereas binding of IL-6 to soluble IL-6 receptor α induces pro-inflammatory trans-signalling. Trans-signalling has been described to be markedly stronger than classic signalling. Understanding the molecular mechanisms that drive differences between trans- and classic signalling is important for the design of trans-signalling-specific therapies. These differences will be addressed here using a combination of dynamic mathematical modelling and molecular biology. METHODS: We apply an iterative systems biology approach using set-based modelling and validation approaches combined with quantitative biochemical and cell biological analyses. RESULTS: The combination of experimental analyses and dynamic modelling allows to relate the observed differences between IL-6-induced trans- and classic signalling to cell-type specific differences in the expression and ratios of the individual subunits of the IL-6 receptor complex. Canonical intracellular Jak/STAT signalling is indifferent in IL-6-induced trans- and classic signalling. CONCLUSION: This study contributes to the understanding of molecular mechanisms of IL-6 signal transduction and underlines the power of combined dynamical modelling, model-based validation and biological experiments. The opposing pro- and anti-inflammatory responses initiated by IL-6 trans- and classic signalling depend solely on the expression ratios of the subunits of the entire receptor complex. By pointing out the importance of the receptor expression ratio for the strength of IL-6 signalling this study lays a foundation for future precision medicine approaches that aim to selectively block pro-inflammatory trans-signalling. Furthermore, the derived models can be used for future therapy design.
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Specific inhibition of IL-6 trans-signaling, rather than total inhibition of IL-6 signaling, is sufficient to suppress tumor progression.
“Only the specific inhibition of IL-6 trans-signaling, rather than total inhibition of IL-6 signaling, is sufficient to suppress tumor progression [71, 72].”
From The double-edged effects of IL-6 in liver regeneration, aging, inflammation, and diseases (2024) · cites this paper as [72]
The Discussion (page unavailable) describes selective inhibition of IL-6 trans-signalling while preserving classic signalling, and reports its use in animal models of Crohn’s disease. It does not report that selective inhibition suppresses tumor progression or establish that it is sufficient to do so rather than total IL-6 inhibition. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIL-6 trans-signaling, but not IL-6 classic signaling, is essential to promote HCC carcinogenesis and progression; activation of membrane-bound IL-6R and gp130 in hepatocytes alone seems not sufficient for tumor formation.
“In addition, evidences suggest that IL-6 trans-signaling, but not IL-6 classic signaling, is essential to promote HCC carcinogenesis and progression, and only the activation of membrane-bound IL-6R and gp130 in hepatocytes seems not sufficient for tumor formation [71, 72].”
From The double-edged effects of IL-6 in liver regeneration, aging, inflammation, and diseases (2024) · cites this paper as [72]
The Results section ('IL-6-induced trans-signalling is more potent than classic signalling in human hepatoma cells'; page unavailable) reports stronger STAT3 activation with trans-signalling in HepG2 cells. It does not establish that trans-signalling is essential for HCC carcinogenesis or progression, or that activation of membrane-bound IL-6R and gp130 in hepatocytes is insufficient for tumor formation. The separate proliferation experiments used murine pre-B cells, not a tumor-formation model. (LLM, conf=0.85)
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- Authors
- Reeh, H., Rudolph, N., Billing, U., Christen, H., Streif, S., Bullinger, E., Schliemann-Bullinger, M., Findeisen, R., Schaper, F., Huber, H. J., & Dittrich, A.
- Affiliations
- Otto-von-Guericke-Universität Magdeburg (DE)
- Chemnitz University of Technology (DE)
- Boehringer Ingelheim (Germany) (DE)
- Corresponding author
- Dittrich, Anna
- ORCID
- Venue
- Cell Communication and Signaling
- Published
- 2019-05-17
- Volume
- 17
- Issue
- 1
- Pages
- 46-46
- ISSN
- 1478-811X (ISSN-L)
- PMC
- PMC6525395
- OpenAlex
- W2947098448
- Cited by
- 180
- References
- 62
- Citations by year
- 2026: 25 · 2025: 39 · 2024: 27 · 2023: 29 · 2022: 26 · 2021: 24 · 2020: 9 · 2019: 1
- FWCI
- 6.27
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Cell Communication and Signaling (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Bundesministerium für Bildung und Forschung (031A300A/InTraSig)
- Max-Planck-Gesellschaft (IMPRS ProEng)
- European Regional Development Fund (ERDF CDS)
- Topics
- Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- interleukin-6, IL-6 trans-signalling, IL-6 receptor alpha, gp130, JAK/STAT signaling, cytokine signaling, model-based validation, pro-inflammatory signaling, anti-inflammatory signaling
- MeSH terms
- Animals, Humans, Models, Biological, Signal Transduction, Interleukin-6, Receptors, Interleukin-6, Cytokine Receptor gp130
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