Cited by 677Colorectal Cancer Treatments and StudiesGenetic factors in colorectal cancerColorectal Cancer Surgical Treatments

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From tumour heterogeneity to advances in precision treatment of colorectal cancer

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Punt, Cornelis J. A., Koopman, Miriam, Vermeulen, Louis·2017·Nature Reviews Clinical Oncology

DOI 10.1038/nrclinonc.2016.171

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Abstract

In recent years, the high heterogeneity of colorectal cancer (CRC) has become evident. Hence, biomarkers need to be developed that enable the stratification of patients with CRC into different prognostic subgroups and in relation to response to therapies, according to the distinctive tumour biology. Currently, only RAS-mutation status is used routinely as a negative predictive marker to avoid treatment with anti-EGFR agents in patients with metastatic CRC, and mismatch-repair status can guide the use of adjuvant chemotherapy in patients with early stage colon cancer. Advances in molecular biology over the past decade have enabled a better understanding of the development of CRC, as well as the more-precise use of innovative targeted therapies for this disease, and include three fundamental achievements. First, the availability of large databases to capture and store the genomic landscape of patients with CRC, providing information on the genes that are frequently deregulated in CRC. Second, the possibility of using gene-expression profiling to differentiate the subtypes of CRC into prognostic groups. Third, results from highly sensitive next-generation sequencing analyses have led to an appreciation of the extensive intratumoural heterogeneity of CRC. Herein, we discuss these advances and place them into the clinical context, and present the novel targets and therapeutic opportunities that are on the horizon.

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GraphPath: a graph attention model for molecular stratification with interpretability based on the pathway–pathway interaction network
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“These heterogeneities within the same type of cancer give rise to varying treatment responses and overall prognosis among patients, posing significant challenges in cancer diagnosis and management (Abeshouse et al. 2015, Ateeq et al. 2016, Punt et al. 2017, Buikhuisen et al. 2020).”
Background
Transcriptomic subtyping of gastrointestinal malignancies
de Back, T. R., van Hooff, S. R., Sommeijer, D. W., & Vermeulen, L. (2024) · Trends in cancer · doi:10.1016/j.trecan.2024.06.007 · Cited by 19
Self-citation
Phase I study of safety and efficacy of allogeneic natural killer cell therapy in relapsed/refractory neuroblastomas post autologous hematopoietic stem cell transplantation
Mohseni, R., Sharif, P. M., Behfar, M., Shojaei, S., Shoae‐Hassani, A., Jafari, L., Khosravi, A., Nikfetrat, Z., & Hamidieh, A. A. (2024) · Scientific Reports · doi:10.1038/s41598-024-70958-7 · Cited by 18
De Novo Computational Design for Development of a Peptide Ligand Oriented to VEGFR-3 with High Affinity and Long Circulation
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Long non-coding RNA BCYRN1 exerts an oncogenic role in colorectal cancer by regulating the miR-204-3p/KRAS axis
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Telomere maintenance in interplay with DNA repair in pathogenesis and treatment of colorectal cancer
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Precision Approaches in the Management of Colorectal Cancer: Current Evidence and Latest Advancements towards Individualizing the Treatment
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“Interestingly, inhibition of BRAF has been associated with over-activation of EGFR, which is postulated to cause the attenuated response of vemurafenib observed in in-vitro mCRC [46].”
Background
Discovery of Small-Molecule Inhibitors of the PTK7/β-Catenin Interaction Targeting the Wnt Signaling Pathway in Colorectal Cancer
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The epigenetic modifier HDAC2 and the checkpoint kinase ATM determine the responses of microsatellite instable colorectal cancer cells to 5-fluorouracil
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“In light of the high level of colorectal cancer intra-tumoral heterogeneity (Punt et al. 2017), one Fig.”
Background
Decoding the colorectal cancer ecosystem emphasizes the cooperative role of cancer cells, TAMs and CAFsin tumor progression
Shen, R., Li, P., Zhang, B., Feng, L., & Cheng, S. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03661-8 · Cited by 16
“However, satisfactory clinical outcomes have not been achieved due to tremendous intratumoral heterogeneity [2].”
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CD44-targeted nanoparticles for co-delivery of docetaxel and an Akt inhibitor against colorectal cancer
González‐Valdivieso, J., Vallejo, R., Rodríguez‐Rojo, S., Santos, M., Schneider, J., Arias, F. J., & Girotti, A. (2023) · Biomaterials Advances · doi:10.1016/j.bioadv.2023.213595 · Cited by 16
KIF18A improves migration and invasion of colorectal cancer (CRC) cells through inhibiting PTEN signaling
Liu, Y., Sun, M., Zhang, B., & Zhao, W. (2023) · Aging · doi:10.18632/aging.205027 · Cited by 16
Detection of Intratumor Heterogeneity in Modern Pathology: A Multisite Tumor Sampling Perspective
Cortés, J. M., Petris, G. D., & Lopez, J. I. (2017) · Frontiers in Medicine · doi:10.3389/fmed.2017.00025 · Cited by 16
“Finally, CRC was proven to be a molecularly complex and highly heterogeneous disease at inter- and intratumor levels (41).”
Background
Integrating Microbiome Network: Establishing Linkages Between Plants, Microbes and Human Health
Krishna, S. B. N., Dubey, A., Malla, M. A., Kothari, R., Upadhyaya, C. P., Adam, J. K., & Kumar, A. (2019) · The Open Microbiology Journal · doi:10.2174/1874285801913020330 · Cited by 17
Identification of an Immune Gene Signature Based on Tumor Microenvironment Characteristics in Colon Adenocarcinoma
Chen, Y., & Zhao, J. (2021) · Cell Transplantation · doi:10.1177/09636897211001314 · Cited by 16
“The following steps were conducted in processing the 499 RNA-Seq read count samples: (1) remove the samples with an overall survival (OS) <30 days; (2) remove normal tissue samples; (3) convert read counts to transcripts per million (TPM) with the annotation information of GENCODE v22 [in terms of data distribution, t…”
Method
The circulating soluble form of the CD40 costimulatory immune checkpoint receptor and liver metastasis risk in rectal cancer
Meltzer, S., Torgunrud, A., Abrahamsson, H., Solbakken, A. M., Flatmark, K., Dueland, S., Bakke, K. M., Bousquet, P. A., Negård, A., Johansen, C., et al. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01377-y · Cited by 17
Nanotechnology as a Delivery Tool for Precision Cancer Therapies
Sharma, B., Crist, R. M., & Adiseshaiah, P. P. (2017) · The AAPS Journal · doi:10.1208/s12248-017-0152-y · Cited by 16
Image-based consensus molecular subtype classification (imCMS) of colorectal cancer using deep learningPreprint
Sirinukunwattana, K., Domingo, E., Richman, S., Redmond, K., Blake, A., Verrill, C., Leedham, S., Chatzipli, A., Hardy, C. W., Whalley, C., et al. (2019) · bioRxiv · doi:10.1101/645143 · Cited by 15
Prognostic value of primary tumor location in colorectal cancer: an updated meta-analysis
Gholamalizadeh, H., Zafari, N., Velayati, M., Fiuji, H., Maftooh, M., Ghorbani, E., Hassanian, S. M., Khazaei, M., Ferns, G. A., Nazari, E., et al. (2023) · Clinical and Experimental Medicine · doi:10.1007/s10238-023-01120-2 · Cited by 15
CT-based radiomics nomogram for the preoperative prediction of microsatellite instability and clinical outcomes in colorectal cancer: a multicentre study
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Chromatin Remodeling in Patient‐Derived Colorectal Cancer Models
Xiang, K., Wang, E., Mantyh, J. B., Rupprecht, G., Negrete, M., Sanati, G., Hsu, C., Randon, P. M., Dohlman, A. B., Kretzschmar, K., et al. (2024) · Advanced Science · doi:10.1002/advs.202303379 · Cited by 15
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Method
Increased IFRD1 Expression in Human Colon Cancers Predicts Reduced Patient Survival
Lewis, M. A., Sharabash, N. M., Miao, Z., Lyons, L. N., Piccirillo, J. F., Kallogjeri, D., Schootman, M., Mutch, M. G., Yan, Y., Levin, M. S., et al. (2017) · Digestive Diseases and Sciences · doi:10.1007/s10620-017-4819-0 · Cited by 17
“Changes in the tumor landscape which may involve global modulation of gene expression have been suggested to play a role in these processes [4].”
Integrative analysis from multi‐centre studies identifies a function‐derived personalized multi‐gene signature of outcome in colorectal cancer
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Prognostic Factors of Colorectal Cancer: A Comparative Study on Patients With or Without Liver Metastasis
Peng, H., Liu, G., Bao, Y., Zhang, X., Zhou, L., Huang, C., Song, Z., Cao, S., Dang, S., Zhang, J., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.626190 · Cited by 15
“The intratumoral heterogeneity of CRC was shown to be much less than other cancers such as lung cancer (15, 16), making it more difficult to identify differentially mutated genes.”
Background
AA-NAT, MT1 and MT2 Correlates with Cancer Stem-Like Cell Markers in Colorectal Cancer: Study of the Influence of Stage and p53 Status of Tumors
Casado, J., Iñigo-Chaves, A., Jiménez-Ruiz, S. M., Ríos‐Arrabal, S., Carazo, Á., González‐Puga, C., Núñez, M. I., Ruiz‐Extremera, A., Salmerón, J., & León, J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061251 · Cited by 15
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“To properly address postoperative surveillance and treatment, it is fruitful to explore prognostic biomarkers to characterize the heterogeneity of CRCs [2, 5, 6].”
BackgroundInfluential
Targeted Quantitative Profiling of GTP-Binding Proteins in Cancer Cells Using Isotope-Coded GTP Probes
Cai, R., Huang, M., & Wang, Y. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b03727 · Cited by 15
A RAS-Independent Biomarker Panel to Reliably Predict Response to MEK Inhibition in Colorectal Cancer
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Background
The role of miRNA-128 in the development and progression of gastrointestinal and urogenital cancer
Al‐Awsi, G. R. L., Jasim, S. A., Mustafa, Y. F., Alhachami, F. R., Ziyadullaev, S., Kandeel, M. K., Abulkassim, R., Sivaraman, R., Hameed, N. M., Romero‐Parra, R. M., et al. (2022) · Future Oncology · doi:10.2217/fon-2022-0574 · Cited by 14
High-throughput proteomics profiling-derived signature associated with chemotherapy response and survival for stage II/III colorectal cancer
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“Currently, the selection of patients is suboptimal, which leads to either over-or undertreatment 3 .”
Host-microbiota interactions contributing to the heterogeneous tumor microenvironment in colorectal cancer
Li, X., Wu, D., Li, Q., Gu, J., Gao, W., Zhu, X., Yin, W., Zhu, R., Zhu, L., & Jiao, N. (2023) · Physiological Genomics · doi:10.1152/physiolgenomics.00103.2023 · Cited by 15
A consensus molecular subtypes classification strategy for clinical colorectal cancer tissues
de Back, T. R., Wu, T., Schafrat, P. J. M., ten Hoorn, S., Tan, M., He, L., van Hooff, S. R., Köster, J., Nijman, L. E., Vink, G. R., et al. (2024) · Life Science Alliance · doi:10.26508/lsa.202402730 · Cited by 19
“The authors use comparisons for fresh frozen RNA data as their benchmark, indicating that in some cases their new classifier improves classification accuracy.”
Self-citation
Bifunctional Nanoassembly Enables Metabolism-Driven Microfluidic Blood Screening Guided by MRI Localization for Cancer Monitoring
Luan, X., Gao, Y., Pan, Y., Huang, Z., Zeng, F., He, G., He, B., Ye, D., & Song, Y. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.4c05427 · Cited by 14
Death Domain-Associated Protein Promotes Colon Cancer Metastasis through Direct Interaction with ZEB1
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An innovative radiomics approach to predict response to chemotherapy of liver metastases based on CT images
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Violacein negatively modulates the colorectal cancer survival and epithelial–mesenchymal transition
Oliveira, P. F. D. S., Faria, A. V. D. S., Clerici, S. P., Akagi, E. M., Carvalho, H. F., Justo, G. Z., Durán, N., & Ferreira‐Halder, C. V. (2022) · Journal of Cellular Biochemistry · doi:10.1002/jcb.30295 · Cited by 14
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BackgroundInfluential
CDX2 as a Predictive Biomarker Involved in Immunotherapy Response Suppresses Metastasis through EMT in Colorectal Cancer
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Authors: Punt, C. J. A., Koopman, M., & Vermeulen, L.
Affiliations: Amsterdam UMC Location University of Amsterdam (NL)
University Medical Center Utrecht (NL)
Corresponding author: Punt, Cornelis J. A.
ORCID: Punt, Cornelis J. A.
Koopman, Miriam
Vermeulen, Louis
Venue: Nature Reviews Clinical Oncology
Publisher: Springer Science and Business Media LLC
Published: 2016-12-06
Volume: 14
Issue: 4
Pages: 235-246
ISSN: 1759-4774 (ISSN-L)
1759-4782
DOI: 10.1038/nrclinonc.2016.171
OpenAlex: W2560375214
Cited by: 654
References: 177
Citations by year: 2026: 38 · 2025: 41 · 2024: 87 · 2023: 79 · 2022: 88 · 2021: 96 · 2020: 83 · 2019: 57 · 2018: 56 · 2017: 28
FWCI: 4.73
Type: journal article
Language: en
Open access: green
pure.amsterdamumc.nl
Licence: other-oa
www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Clinical Oncology (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Utrecht University Repository (Utrecht University) (submittedVersion)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Maag Lever Darm Stichting (MLDS-CDG 14-03)
H2020 European Research Council (638193)
Topics: Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
Keywords: colorectal cancer, intratumoral heterogeneity, precision medicine, targeted therapy, gene expression profiling, tumor subtypes, prognostic factors, predictive biomarkers, RAS mutations, DNA mismatch repair, anti-EGFR therapy, adjuvant chemotherapy, next-generation sequencing
MeSH terms: Antineoplastic Combined Chemotherapy Protocols, Forecasting, Humans, Immunotherapy, Neoplasm Metastasis, Neoplasm Proteins, Neoplasm Staging, Prognosis, Quality of Health Care, Colorectal Neoplasms, Treatment Outcome, Genetic Heterogeneity, Therapies, Investigational, Proto-Oncogene Proteins B-raf, DNA Mismatch Repair, Early Detection of Cancer, Precision Medicine, Molecular Targeted Therapy

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From tumour heterogeneity to advances in precision treatment of colorectal cancer

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