Single-cell and bulk transcriptome sequencing identifies two epithelial tumor cell states and refines the consensus molecular classification of colorectal cancer
Open accessAbstract
The consensus molecular subtype (CMS) classification of colorectal cancer is based on bulk transcriptomics. The underlying epithelial cell diversity remains unclear. We analyzed 373,058 single-cell transcriptomes from 63 patients, focusing on 49,155 epithelial cells. We identified a pervasive genetic and transcriptomic dichotomy of malignant cells, based on distinct gene expression, DNA copy number and gene regulatory network. We recapitulated these subtypes in bulk transcriptomes from 3,614 patients. The two intrinsic subtypes, iCMS2 and iCMS3, refine CMS. iCMS3 comprises microsatellite unstable (MSI-H) cancers and one-third of microsatellite-stable (MSS) tumors. iCMS3 MSS cancers are transcriptomically more similar to MSI-H cancers than to other MSS cancers. CMS4 cancers had either iCMS2 or iCMS3 epithelium; the latter had the worst prognosis. We defined the intrinsic epithelial axis of colorectal cancer and propose a refined ‘IMF’ classification with five subtypes, combining intrinsic epithelial subtype (I), microsatellite instability status (M) and fibrosis (F).
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The majority of CMS4 tumours can be grouped into one of two major intrinsic CMS (iCMS) subtypes defined by distinct gene expression, DNA copy number and gene regulatory network.
“revealed that the majority CMS4 tumours could be grouped into one of the two major iCMS subtypes, defined by a distinct gene expression, DNA copy number and gene regulatory network.”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [124]
A subset of fibrotic tumours in the iCMS2 and iCMS3 group expresses high levels of fibroblast, endothelial and immune-specific genes.
“Therefore, a subset of fibrotic tumours in the iCMS2 and iCMS3 group is expressing high levels of fibroblast, endothelial and immune-specific genes,”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [124]
iCMS2 and iCMS3 are genetically distinct, but independent of those genetic profiles some tumours develop fibrotic stromal signatures resulting in CMS4-like tumours.
“indicating that iCMS2 and iCMS3 are genetically distinct, but independent of those genetic profiles some tumours develop fibrotic stromal signatures resulting in CMS4-like tumours.”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [124]
Cancer cells from CMS4 colorectal cancer reside in either a fibrotic intrinsic CMS2 (iCMS2) or iCMS3 state according to the type of lesion: TA-type CMS4 correspond to the iCMS2-F class, while SSL-type CMS4 correspond to the iCMS3-F class.
“According to the single-cell study by Joanito and colleagues (14), cancer cells from CMS4 colorectal cancer reside in either a fibrotic intrinsic CMS2 (iCMS2) or iCMS3 state according to the type of lesion: TA-type CMS4 correspond to the iCMS2-F class (F standing for fibrotic), while SSL-type CMS4 correspond to the iCMS3-F class.”
From Clinical Challenges of Consensus Molecular Subtype CMS4 Colon Cancer in the Era of Precision Medicine (2024) · cites this paper as [14]
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Current and emerging concepts for systemic treatment of metastatic colorectal cancer
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- Authors
- Joanito, I., Wirapati, P., Zhao, N., Nawaz, Z., Yeo, G., Lee, F., Eng, C. L. P., Macalinao, D. C., Kahraman, M., Srinivasan, H., Lakshmanan, V., Verbandt, S., Tsantoulis, P., Gunn, N., Venkatesh, P. N., Poh, Z. W., Nahar, R., Oh, H. L. J., Loo, J. M., Chia, S., Cheow, L. F., Cheruba, E., Wong, M. T., Kua, L., Chua, C., Nguyen, A., Golovan, J., Gan, A., Lim, W.-J., Guo, Y. A., Yap, C. K., Tay, B., Hong, Y., Chong, D. Q., Chok, A.-Y., Park, W.-Y., Han, S., Chang, M. H., Seow-En, I., Fu, C., Mathew, R., Toh, E.-L., Hong, L. Z., Skanderup, A. J., DasGupta, R., Ong, C.-A. J., Lim, K. H., Tan, E. K. W., Koo, S.-L., Leow, W. Q., Tejpar, S., Prabhakar, S., & Tan, I. B.
- Affiliations
- Agency for Science, Technology and Research (SG)
- SIB Swiss Institute of Bioinformatics (CH)
- National Cancer Centre Singapore (SG)
- KU Leuven (BE)
- University of Geneva (CH)
- MSD (Singapore) (SG)
- National University of Singapore (SG)
- NantOmics LLC (United States) (US)
- Samsung Medical Center (KR)
- Singapore General Hospital (SG)
- Corresponding author
- Tejpar, Sabine
- Prabhakar, Shyam
- Tan, Iain Beehuat
- ORCID
- Joanito, Ignasius
- Wirapati, Pratyaksha
- Zhao, Nancy
- Nawaz, Zahid
- Yeo, Grace
- Lee, Fiona
- Eng, Christine L. P.
- Macalinao, Dominique Camat
- Srinivasan, Harini
- Lakshmanan, Vairavan
- Verbandt, Sara
- Tsantoulis, Petros
- Venkatesh, Prasanna Nori
- Poh, Zhong Wee
- Loo, Jia Min
- Cheow, Lih Feng
- Cheruba, Elsie
- Kua, Lindsay
- Nguyen, Andy
- Gan, Anna
- Lim, Wan-Jun
- Guo, Yu Amanda
- Tay, Brenda
- Hong, Yourae
- Chong, Dawn Qingqing
- Chok, Aik-Yong
- Park, Woong-Yang
- Han, Shuting
- Seow-En, Isaac
- Fu, Cherylin
- Mathew, Ronnie
- Toh, Ee-Lin
- Hong, Lewis Z.
- Skanderup, Anders Jacobsen
- DasGupta, Ramanuj
- Ong, Chin-Ann Johnny
- Tan, Emile K. W.
- Koo, Si-Lin
- Leow, Wei Qiang
- Tejpar, Sabine
- Prabhakar, Shyam
- Tan, Iain Beehuat
- Venue
- Nature Genetics
- Published
- 2022-06-30
- Volume
- 54
- Issue
- 7
- Pages
- 963-975
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC9279158
- OpenAlex
- W4283716873
- Cited by
- 434
- References
- 74
- Citations by year
- 2026: 100 · 2025: 144 · 2024: 110 · 2023: 63 · 2022: 17
- FWCI
- 27.59
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- IRIS (submittedVersion, cc-by)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- SERVAL (Université de Lausanne) (submittedVersion, cc-by)
- Funders
- Agency for Science, Technology and Research (#H18/01/a0/020)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- colorectal cancer, consensus molecular subtypes, single-cell transcriptomics, PAM50 molecular subtypes, microsatellite instability, DNA copy number alterations, gene regulatory networks, tumor fibrosis, tumor microenvironment, prognosis, molecular classification
- MeSH terms
- Epithelial Cells, Humans, Neoplasms, Glandular and Epithelial, Colorectal Neoplasms, Microsatellite Repeats, Microsatellite Instability, Transcriptome
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