Metastatic recurrence in colorectal cancer arises from residual EMP1+ cells
Open accessAbstract
Around 30-40% of patients with colorectal cancer (CRC) undergoing curative resection of the primary tumour will develop metastases in the subsequent years 1. Therapies to prevent disease relapse remain an unmet medical need. Here we uncover the identity and features of the residual tumour cells responsible for CRC relapse. An analysis of single-cell transcriptomes of samples from patients with CRC revealed that the majority of genes associated with a poor prognosis are expressed by a unique tumour cell population that we named high-relapse cells (HRCs). We established a human-like mouse model of microsatellite-stable CRC that undergoes metastatic relapse after surgical resection of the primary tumour. Residual HRCs occult in mouse livers after primary CRC surgery gave rise to multiple cell types over time, including LGR5+ stem-like tumour cells 2-4, and caused overt metastatic disease. Using Emp1 (encoding epithelial membrane protein 1) as a marker gene for HRCs, we tracked and selectively eliminated this cell population. Genetic ablation of EMP1 high cells prevented metastatic recurrence and mice remained disease-free after surgery. We also found that HRC-rich micrometastases were infiltrated with T cells, yet became progressively immune-excluded during outgrowth. Treatment with neoadjuvant immunotherapy eliminated residual metastatic cells and prevented mice from relapsing after surgery. Together, our findings reveal the cell-state dynamics of residual disease in CRC and anticipate that therapies targeting HRCs may help to avoid metastatic relapse.
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Immune checkpoint blockade particularly facilitates destruction of small tumours and micrometastases, in which PD-L1 positivity and T cell infiltration are higher compared with larger metastases.
“Furthermore, ICB particularly facilitates the destruction of small tumours and micrometastases, in which PD-L1 positivity and T cell infiltration are higher compared with larger metastases.174”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [174]
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“and, indeed, perioperative ICB enabled eradication of micrometastases after resection of the primary tumour in a mouse model of pMMR/MSS CRC.174”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [174]
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- Authors
- Cañellas-Socias, A., Cortina, C., Hernando-Momblona, X., Palomo-Ponce, S., Mulholland, E. J., Turon, G., Mateo, L., Conti, S., Roman, O., Sevillano, M., Slebe, F., Stork, D., Caballé-Mestres, A., Berenguer-Llergo, A., Álvarez-Varela, A., Fenderico, N., Novellasdemunt, L., Jiménez-Gracia, L., Sipka, T., Bardia, L., Lorden, P., Colombelli, J., Heyn, H., Trepat, X., Tejpar, S., Sancho, E., Tauriello, D. V. F., Leedham, S., Attolini, C. S.-O., & Batlle, E.
- Affiliations
- Institute for Research in Biomedicine (ES)
- Centre for Human Genetics (GB)
- Barcelona Institute of Science and Technology (ES)
- Universitat Pompeu Fabra (ES)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- KU Leuven (BE)
- Radboud University Medical Center (NL)
- Corresponding author
- Batlle, Eduard
- ORCID
- Cañellas-Socias, Adrià
- Cortina, Carme
- Palomo-Ponce, Sergio
- Mulholland, Eoghan J.
- Mateo, Lidia
- Conti, Sefora
- Roman, Olga
- Sevillano, Marta
- Slebe, Felipe
- Caballé-Mestres, Adrià
- Berenguer-Llergo, Antonio
- Álvarez-Varela, Adrián
- Fenderico, Nicola
- Novellasdemunt, Laura
- Jiménez-Gracia, Laura
- Sipka, Tamara
- Bardia, Lidia
- Lorden, Patricia
- Colombelli, Julien
- Heyn, Holger
- Trepat, Xavier
- Tejpar, Sabine
- Sancho, Elena
- Tauriello, Daniele V. F.
- Leedham, Simon
- Attolini, Camille Stephan-Otto
- Batlle, Eduard
- Venue
- Nature
- Published
- 2022-11-09
- Volume
- 611
- Issue
- 7936
- Pages
- 603-613
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7616986
- OpenAlex
- W4308620623
- Cited by
- 256
- References
- 86
- Citations by year
- 2026: 63 · 2025: 94 · 2024: 58 · 2023: 39 · 2022: 2
- FWCI
- 20.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- Lirias (KU Leuven) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Wellcome Trust (206314/Z/17/Z, 206314)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Keywords
- colorectal cancer, distant recurrence, EMP1, epithelial membrane protein 1, micrometastases, immune exclusion, T cell infiltration, neoadjuvant immunotherapy, cell state dynamics, surgical resection
- MeSH terms
- Animals, Disease Models, Animal, Humans, Immunotherapy, Neoplasm Metastasis, Neoplasm Proteins, Neoplasm Recurrence, Local, Receptors, Cell Surface, T-Lymphocytes, Colorectal Neoplasms, Lymphocytes, Tumor-Infiltrating, Neoplasm, Residual, Disease Progression, Neoadjuvant Therapy, Mice
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