A constitutive interferon-high immunophenotype defines response to immunotherapy in colorectal cancer
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Fewer than 50% of metastatic deficient mismatch repair (dMMR) colorectal cancer (CRC) patients respond to immune checkpoint inhibition (ICI). Identifying and expanding this patient population remains a pressing clinical need. Here, we report that an interferon-high immunophenotype locally enriched in cytotoxic lymphocytes and antigen-presenting macrophages is required for response. This immunophenotype is not exclusive to dMMR CRCs but comprises a subset of MMR proficient (pMMR) CRCs. Single-cell spatial analysis and in vitro cell co-cultures indicate that interferon-producing cytotoxic T cells induce overexpression of antigen presentation in adjacent macrophages and tumor cells, including MHC class II invariant chain CD74. dMMR CRCs expressing high levels of CD74 respond to ICI and a subset of CD74 high pMMR CRC patients show better progression free survival when treated with ICI. Therefore, CD74 abundance can identify the constitutive interferon-high immunophenotype determining clinical benefit in CRC, independently of tumor mutational burden or MMR status.
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Local enrichment of cytotoxic lymphocytes with an interferon-high immunophenotype that induces antigen-presentation in adjacent macrophages and tumour cells is a positive response predictor in subsets of dMMR/MSI-H and pMMR/MSS CRC.
“A novel interesting approach was recently published, identifying local enrichment of cytotoxic lymphocytes with an interferon-high immunophenotype that induces antigen-presentation in adjacent macrophages and tumour cells as a positive response predictor in subsets of dMMR/MSI-H but also pMMR/MSS CRC.108”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [108]
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- Authors
- Acha-Sagredo, A., Andrei, P., Clayton, K., Taggart, E., Antoniotti, C., Woodman, C. A., Afrache, H., Fourny, C., Armero, M., Moinudeen, H. K., Green, M., Bhardwaj, N., Mikolajczak, A., Rodriguez-Lopez, M., Crawford, M., Connick, E., Lim, S., Hobson, P., Linares, J., Ignatova, E., Pelka, D., Smyth, E. C., Diamantis, N., Sosnowska, D., Carullo, M., Ciraci, P., Bergamo, F., Intini, R., Nye, E., Barral, P., Mishto, M., Arnold, J. N., Lonardi, S., Cremolini, C., Fontana, E., Rodriguez-Justo, M., & Ciccarelli, F. D.
- Affiliations
- Queen Mary University of London (GB)
- University of Pisa (IT)
- King's College London (GB)
- The Francis Crick Institute (GB)
- University College London (GB)
- Sarah Cannon Research Institute (GB)
- Churchill Hospital (GB)
- Royal Free London NHS Foundation Trust (GB)
- Istituto Oncologico Veneto (IT)
- Corresponding author
- Ciccarelli, Francesca D.
- ORCID
- Andrei, Pietro
- Clayton, Kalum
- Taggart, Emma
- Antoniotti, Carlotta
- Woodman, Chloé A.
- Green, Mary
- Mikolajczak, Anna
- Lim, Steven
- Hobson, Philip
- Ignatova, Ekaterina
- Smyth, Elizabeth C.
- Diamantis, Nikolaos
- Sosnowska, Dominika
- Carullo, Martina
- Bergamo, Francesca
- Intini, Rossana
- Nye, Emma
- Barral, Patricia
- Mishto, Michele
- Arnold, James N.
- Lonardi, Sara
- Cremolini, Chiara
- Fontana, Elisa
- Ciccarelli, Francesca D.
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2025-02
- Volume
- 43
- Issue
- 2
- Pages
- 292-307.e7
- ISSN
- 1535-6108 (ISSN-L)
- OpenAlex
- W4406547947
- Cited by
- 71
- References
- 76
- Citations by year
- 2026: 46 · 2025: 25
- FWCI
- 29.40
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, cc-by)
- Research Portal (King's College London) (submittedVersion, cc-by-nc)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- The Francis Crick Institute (cc-by)
- Funders
- Medical Research Council (MR/W006820/1, CANCTA-2023/100002)
- European Commission
- Wellcome Trust
- Ministero dell’Istruzione, dell’Università e della Ricerca
- Cancer Research UK (CANCTA-2023/100002, C43634/A25487, C7893/A26233, EDDPJT-Nov21\u2216100010)
- Francis Crick Institute
- National Institute for Health and Care Research
- UCLH Biomedical Research Centre
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- colorectal cancer, immune checkpoint inhibitors, CD74, cytotoxic T lymphocytes, tumor-associated macrophages, antigen presentation, mismatch repair status, immunotherapy response prediction, single-cell spatial analysis, progression-free survival
- MeSH terms
- Immune Checkpoint Inhibitors, Antigens, Differentiation, B-Lymphocyte, Histocompatibility Antigens Class II, Female, Humans, Immunotherapy, Interferons, Macrophages, Male, T-Lymphocytes, Cytotoxic, Colorectal Neoplasms, Immunophenotyping, Antigen Presentation, DNA Mismatch Repair
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