From tumour heterogeneity to advances in precision treatment of colorectal cancer

Punt, Cornelis J. A.; Koopman, Miriam; Vermeulen, Louis

doi:10.1038/nrclinonc.2016.171

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

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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5-FU/LV is useful in palliative therapy for mCRC, but the development of effective doublet combination therapy regimens, including FOLFOX and FOLFIRI, resulted in significant survival advantages.
“5-FU/LV is useful in palliative therapy for mCRC, but the development of effective doublet combination therapy regimens, including FOLFOX (folinic acid (leucovorin), 5-FU, oxaliplatin) and FOLFIRI (leucovorin, 5-FU, irinotecan) [10], resulted in significant survival advantages.”
From Recent Advances in Therapeutic Strategies to Improve Colorectal Cancer Treatment (2024) · cites this paper as [10]

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Increased Detection Sensitivity for KRAS Mutations Enhances the Prediction of Anti-EGFR Monoclonal Antibody Resistance in Metastatic Colorectal Cancer
Molinari, F., Felicioni, L., Buscarino, M., De Dosso, S., Buttitta, F., Malatesta, S., Movilia, A., Luoni, M., Boldorini, R., Alabiso, O., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-3137 · Cited by 159 · see citing works
Porcupine inhibitor suppresses paracrine Wnt-driven growth of Rnf43;Znrf3 -mutant neoplasia
Koo, B., van Es, J. H., van den Born, M., & Clevers, H. C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508113112 · Cited by 157 · see citing works
Clinical Relevance of KRAS -Mutated Subclones Detected with Picodroplet Digital PCR in Advanced Colorectal Cancer Treated with Anti-EGFR Therapy
Laurent‐Puig, P., Pekin, D., Normand, C., Kotsopoulos, S. K., Nizard, P., Perez‐Toralla, K., Rowell, R. K., Olson, J., Srinivasan, P., Corre, D. L., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-0983 · Cited by 156 · see citing works
Heterogeneity of KRAS, NRAS, BRAF and PIK3CA mutations in metastatic colorectal cancer and potential effects on therapy in the CAPRI GOIM trial
Normanno, N., Rachiglio, A. M., Lambiase, M., Martinelli, E., Fenizia, F., Esposito, C., Roma, C., Troiani, T., Rizzi, D., Tatangelo, F., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv176 · Cited by 149 · see citing works
MET signaling in colon cancer stem-like cells blunts the therapeutic response to EGFR inhibitors.
Luraghi, P., Reato, G., Cipriano, E., Sassi, F., Orzan, F., Bigatto, V., De Bacco, F., Menietti, E., Han, M., Rideout, W. M., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2340-t · Cited by 146 · see citing works
Exploiting Temporal Collateral Sensitivity in Tumor Clonal Evolution
Zhao, B., Sedlak, J. C., Srinivas, R. R., Creixell, P., Pritchard, J. R., Tidor, B., Lauffenburger, D. A., & Hemann, M. T. (2016) · Cell · doi:10.1016/j.cell.2016.01.045 · Cited by 142 · see citing works
Analysis of Molecular Alterations in Left- and Right-Sided Colorectal Carcinomas Reveals Distinct Pathways of Carcinogenesis
Sugai, T., Habano, W., Jiao, Y., Tsukahara, M., Takeda, Y., Otsuka, K., & Nakamura, S. (2006) · Journal of Molecular Diagnostics · doi:10.2353/jmoldx.2006.050052 · Cited by 138 · see citing works
Biomarker-driven phase 2 study of MK-2206 and selumetinib (AZD6244, ARRY-142886) in patients with colorectal cancer
Do, K. T., Speranza, G., Bishop, R. J., Khin, S. A., Rubinstein, L., Kinders, R. J., Datiles, M. B., Eugeni, M. A., Lam, M. H., Doyle, L. A., et al. (2015) · Investigational New Drugs · doi:10.1007/s10637-015-0212-z · Cited by 133 · see citing works
Resection of the primary tumour versus no resection prior to systemic therapy in patients with colon cancer and synchronous unresectable metastases (UICC stage IV): SYNCHRONOUS - a randomised controlled multicentre trial (ISRCTN30964555)
Rahbari, N. N., Lordick, F., Fink, C., Bork, U., Stange, A., Jäger, D., Luntz, S. P., Englert, S., Rossion, I., Koch, M., et al. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-142 · Cited by 126 · see citing works
Circulating Free DNA as Biomarker and Source for Mutation Detection in Metastatic Colorectal Cancer
Spindler, K.-L. G., Pallisgaard, N., Andersen, R. F., Brandslund, I., & Jakobsen, A. K. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0108247 · Cited by 123 · see citing works
Independent Validation of a Prognostic Genomic Signature (ColoPrint) for Patients With Stage II Colon Cancer
Maak, M., Simón, I., Nitsche, U., Roepman, P., Snel, M. H. J., Glas, A. M., Schuster, T., Keller, G., Zeestraten, E. C. M., Goossens, I., et al. (2013) · Annals of Surgery · doi:10.1097/sla.0b013e31827c1180 · Cited by 120 · see citing works
Decreased mitochondrial priming determines chemoresistance of colon cancer stem cells
Çolak, S., Zimberlin, C. D., Fessler, E., Hogdal, L. J., Prasetyanti, P. R., Grandela, C., Letai, A. G., & Medema, J. P. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.37 · Cited by 119 · see citing works
Clinical activity of FOLFIRI plus cetuximab according to extended gene mutation status by next-generation sequencing: findings from the CAPRI-GOIM trial.
Ciardiello, F., Normanno, N., Maiello, E., Martinelli, E., Troiani, T., Pisconti, S., Giuliani, F., Barone, C., Cartenì, G., Rachiglio, A. M., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu230 · Cited by 116 · see citing works
DNA Copy-Number Alterations Underlie Gene Expression Differences between Microsatellite Stable and Unstable Colorectal Cancers
Jorissen, R. N., Lipton, L. R., Gibbs, P., Chapman, M., Desai, J., Jones, I. T., Yeatman, T. J., East, P., Tomlinson, I. P. M., Verspaget, H. W., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1431 · Cited by 114 · see citing works
Prognostic value of KRAS mutations in stage III colon cancer: post hoc analysis of the PETACC8 phase III trial dataset
Blons, H., Emile, J. F., Le Malicot, K., Julié, C., Zaanan, A., Tabernero, J., Mini, E., Folprecht, G., Van Laethem, J. L., Thaler, J., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu464 · Cited by 108 · see citing works
Role of First-Line Anti–Epidermal Growth Factor Receptor Therapy Compared With Anti–Vascular Endothelial Growth Factor Therapy in Advanced Colorectal Cancer: A Meta-Analysis of Randomized Clinical Trials
Khattak, M. A., Martin, H. L., Davidson, A., & Phillips, M. R. (2015) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2014.12.011 · Cited by 99 · see citing works
Association between KRAS mutation and lung metastasis in advanced colorectal cancer
Pereira, A. A. L., Rego, J. F. M., Morris, V, Overman, M. J., Eng, C., Garrett, C. R., Boutin, A. T., Ferrarotto, R., Lee, M., Jiang, Z.-Q., et al. (2015) · British Journal of Cancer · doi:10.1038/bjc.2014.619 · Cited by 94 · see citing works
Should the Benefit of Adjuvant Chemotherapy in Colon Cancer Be Re-Evaluated?
Påhlman, L. A., Hohenberger, W., Matzel, K. E., Sugihara, K., Quirke, P., & Glimelius, B. L. G. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2015.65.3048 · Cited by 91 · see citing works
A review on the use of molecular markers of cytotoxic therapy for colorectal cancer, what have we learned?
Koopman, M., Venderbosch, S., Nagtegaal, I. D., van Krieken, J. H., & Punt, C. J. A. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2009.04.023 · Cited by 89 · see citing works
Self-citation
The CAIRO4 study: the role of surgery of the primary tumour with few or absent symptoms in patients with synchronous unresectable metastases of colorectal cancer – a randomized phase III study of the Dutch Colorectal Cancer Group (DCCG)
Boer, J. ’. L. , Mol, L., Verhoef, C. K., de Haan, A. F. J., Yilmaz, M., Punt, C. J. A., de Wilt, J. H. W., & Koopman, M. (2014) · BMC Cancer · doi:10.1186/1471-2407-14-741 · Cited by 88 · see citing works
Self-citation
A Vulnerability of a Subset of Colon Cancers with Potential Clinical Utility
Vecchione, L., Gambino, V., Raaijmakers, J. A., Schlicker, A., Fumagalli, A., Russo, M., Villanueva, A., Beerling, E., Bartolini, A., Mollevı́, D. G., et al. (2016) · Cell · doi:10.1016/j.cell.2016.02.059 · Cited by 87 · see citing works
Prognostic gene expression signature associated with two molecularly distinct subtypes of colorectal cancer
Oh, S. C., Park, Y., Park, E. S., Lim, J. Y., Kim, S. M., Kim, S.-B., Kim, J. S., Kim, S. C., Chu, I., Smith, J. J., et al. (2011) · Gut · doi:10.1136/gutjnl-2011-300812 · Cited by 84 · see citing works
Cerebral Hemorrhage, Warfarin, and Intravenous tPA
Alberts, M. J. (2012) · JAMA · doi:10.1001/jama.2012.7265 · Cited by 83 · see citing works
Treatment strategies in colorectal cancer patients with initially unresectable liver-only metastases, a study protocol of the randomised phase 3 CAIRO5 study of the Dutch Colorectal Cancer Group (DCCG)
Huiskens, J., van Gulik, T. M., van Lienden, K. P., Engelbrecht, M. R. W., Meijer, G. A., van Grieken, N. C. T., Schriek, J., Keijser, A., Mol, L., Molenaar, I. Q., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1323-9 · Cited by 75 · see citing works
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Reconciliation of classification systems defining molecular subtypes of colorectal cancer
Sadanandam, A., Wang, X., Melo, F. D. S. E., Gray, J. W., Vermeulen, L., Hanahan, D., & Medema, J. P. (2014) · Cell Cycle · doi:10.4161/cc.27769 · Cited by 74 · see citing works
Self-citation
Phase I Expansion and Pharmacodynamic Study of the Oral MEK Inhibitor RO4987655 (CH4987655) in Selected Patients with Advanced Cancer with RAS–RAF Mutations
Zimmer, L., Barlesi, F., Martinez-Garcia, M., Dieras, V., Schellens, J. H. M., Spano, J.-P., Middleton, M. R., Calvo, E., Paz-Ares, L., Larkin, J., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-0341 · Cited by 71 · see citing works
RandomizEd controlled trial for pre-operAtive dose-escaLation BOOST in locally advanced rectal cancer (RECTAL BOOST study): study protocol for a randomized controlled trial
Burbach, J. M., Verkooijen, H. M., Intven, M., Kleijnen, J.-P., Bosman, M. E., Raaymakers, B. W., van Grevenstein, W. M. U., Koopman, M., Seravalli, E., van Asselen, B., et al. (2015) · Trials · doi:10.1186/s13063-015-0586-4 · Cited by 69 · see citing works
Self-citation
A robust genomic signature for the detection of colorectal cancer patients with microsatellite instability phenotype and high mutation frequency
Tian, S., Roepman, P., Popovici, V. C., Michaut, M., Majewski, I. J., Salazar, R., Santos, C., Rosenberg, R., Nitsche, U., Mesker, W. E., et al. (2012) · The Journal of Pathology · doi:10.1002/path.4092 · Cited by 62 · see citing works
Cancer-initiating cells derived from human rectal adenocarcinoma tissues carry mesenchymal phenotypes and resist drug therapies
Fan, C., Chen, T., Shang, Y.-N., Gu, Y.-Z., Zhang, S. L., Lu, R., OuYang, S.-R., Zhou, X., Li, Y., Wt, M., et al. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.337 · Cited by 62 · see citing works
Defective mismatch repair and benefit from bevacizumab for colon cancer: findings from NSABP C-08.
Pogue-Geile, K., Yothers, G., Taniyama, Y., Tanaka, N., Gavin, P., Colangelo, L., Blackmon, N., Lipchik, C., Kim, S. R., Sharif, S., et al. (2013) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djt140 · Cited by 61 · see citing works
RSPO fusion transcripts in colorectal cancer in Japanese population
Shinmura, K., Kahyo, T., Kato, H., Igarashi, H., Matsuura, S., Nakamura, S., Kurachi, K., Nakamura, T., Ogawa, H., Funai, K., et al. (2014) · Molecular Biology Reports · doi:10.1007/s11033-014-3409-x · Cited by 60 · see citing works
Biomarker discovery for colon cancer using a 761 gene RT-PCR assay
Clark-Langone, K. M., Wu, J. Y., Sangli, C., Chen, A., Snable, J. L., Nguyen, A., Hackett, J. R., Baker, J. B., Yothers, G., Kim, C., et al. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-279 · Cited by 55 · see citing works
Histological and Molecular Evaluation of Patient-Derived Colorectal Cancer Explants
Uronis, J. M., Osada, T., McCall, S. J., Yang, X. Y., Mantyh, C. R., Morse, M. A., Lyerly, H. K., Clary, B. M., & Hsu, D. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038422 · Cited by 52 · see citing works
ERCC1, defective mismatch repair status as predictive biomarkers of survival for stage III colon cancer patients receiving oxaliplatin-based adjuvant chemotherapy
LI, P.-J., Fang, Y. J., Li, F., Ou, Q.-J., Chen, G., & Ma, G. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.83 · Cited by 51 · see citing works
A Review of Excision Repair Cross-complementation Group 1 in Colorectal Cancer
Bohanes, P. O., LaBonte, M. J., & Lenz, H. (2011) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2011.03.024 · Cited by 51 · see citing works
Phase I study of the selective BRAFV600 inhibitor encorafenib (LGX818) combined with cetuximab and with or without the α-specific PI3K inhibitor BYL719 in patients with advanced BRAF-mutant colorectal cancer.
van Geel, R. M. J. M., Élez, E., Bendell, J. C., Faris, J. E., Lolkema, M. P., Eskens, F. A. L. M., Spreafico, A., Kavan, P., Delord, J., Schüler, M., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2014.32.15_suppl.3514 · Cited by 44 · see citing works
The role of primary tumor resection in colorectal cancer patients with asymptomatic, synchronous unresectable metastasis: Study protocol for a randomized controlled trial
Kim, C. W., Baek, J., Choi, G., Yu, C. S., Kang, S. B., Park, W. C., Lee, B. H., Kim, H. R., Oh, J. H., Kim, J. H., et al. (2016) · Trials · doi:10.1186/s13063-016-1164-0 · Cited by 40 · see citing works
Molecular markers to predict outcome to antiangiogenic therapies in colorectal cancer: Current evidence and future perspectives
Custodio, A., Barriuso, J., de Castro, J., Martínez-Marín, V., Moreno, V., Rodrı́guez-Salas, N., & Feliú, J. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.02.004 · Cited by 38 · see citing works
Dissecting cancer heterogeneity – An unsupervised classification approach
Wang, X., Markowetz, F. M., Melo, F. D. S. E., Medema, J. P., & Vermeulen, L. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.08.014 · Cited by 33 · see citing works
Self-citation
MAVERICC, a phase 2 study of mFOLFOX6-bevacizumab (BV) vs FOLFIRI-BV with biomarker stratification as first-line (1L) chemotherapy (CT) in patients (pts) with metastatic colorectal cancer (mCRC).
Lenz, H., Lee, F.-C., Yau, L., Koh, H. A., Knost, J. A., Mitchell, E. P., Bosanac, I., Mancao, C., & Parikh, A. R. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.4_suppl.493 · Cited by 30 · see citing works
LBA-07 Updated Results of the MEK inhibitor trametinib (T), BRAF inhibitor dabrafenib (D), and anti-EGFR antibody panitumumab (P) in patients (pts) with BRAF V600E mutated (BRAFm) metastatic colorectal cancer (mCRC)
Cutsem, E. V., Atreya, C. E., André, T., Bendell, J. C., Schellens, J. H. M., Gordon, M. S., McRee, A. J., Yoshino, T., Muro, K., O'Dwyer, P. J., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv262.07 · Cited by 23 · see citing works
The PARSC trial, a prospective study for the assessment of recurrence risk in stage II colon cancer patients using ColoPrint.
Salazar, R., Marshall, J. L., Capdevila, J., Glimelius, B. L. G., de Waard, J. W. D., van der Hoeven, J. J. M., Klaase, J. M., Bibeau, F., Bachleitner‐Hofmann, T., Midgley, R. A., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2012.30.15_suppl.tps10632 · Cited by 20 · see citing works
Human colonic fibroblasts regulate stemness and chemotherapy resistance of colon cancer stem cells
Çolak, S., & Medema, J. P. (2014) · Cell Cycle · doi:10.4161/15384101.2014.973321 · Cited by 19 · see citing works
LBA-08 Results of a phase 1b study of the selective BRAF V600 inhibitor encorafenib in combination with cetuximab alone or cetuximab + alpelisib for treatment of patients with advanced BRAF-mutant metastatic colorectal cancer
Élez, E., Schellens, J. H. M., van Geel, R. M. J. M., Bendell, J. C., Spreafico, A., Schüler, M., Yoshino, T., Delord, J., Yamada, Y., Lolkema, M. P., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv262.08 · Cited by 15 · see citing works
Prognostic value of BRAF V600E and KRAS exon 2 mutations in microsatellite stable (MSS), stage III colon cancers (CC) from patients (pts) treated with adjuvant FOLFOX+/- cetuximab: A pooled analysis of 3934 pts from the PETACC8 and N0147 trials.
Taı̈eb, J., Malicot, K. L., Penault-Llorca, F. M., Bouché, O., Shi, Q., Thibodeau, S. N., Tabernero, J. M., Mini, E., Goldberg, R. M., Folprecht, G., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2015.33.15_suppl.3507 · Cited by 14 · see citing works
Final Results from Quasar2, a Multicentre, International Randomised Phase III Trial of Capecitabine (Cap) +/- Bevacizumab (Bev) in the Adjuvant Setting of Stage Ii/Iii Colorectal Cancer (Crc)
Midgley, R. S., Love, S., Tomlinson, I. P. M., Johnstone, E. C., Scudder, C., Pearson, S., Julier, P., Domingo, E., Church, D. N., Pezzella, F., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu438.10 · Cited by 9 · see citing works
The PARSC trial, a prospective study for the assessment of recurrence risk in stage II colon cancer (CC) patients using ColoPrint.
Salazar, R., Rosenberg, R., Holzik, M. L., Marshall, J., van der Hoeven, J. J. M., Glimelius, B. L. G., Bibeau, F., Stork‐Sloots, L., Bender, R. A., & Capdevila, J. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2011.29.15_suppl.tps167 · Cited by 1 · see citing works

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Current understanding of the human microbiome
Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., & Knight, R. (2018) · Nature Medicine · doi:10.1038/nm.4517 · Cited by 2,609 · see citing works
5-fluorouracil and other fluoropyrimidines in colorectal cancer: Past, present and future
Vodenkova, S., Buchler, T., Cervena, K., Veskrnova, V., Vodicka, P., & Vymetalkova, V. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107447 · Cited by 956 · see citing works
Patient-derived organoids can predict response to chemotherapy in metastatic colorectal cancer patients
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Genome doubling shapes the evolution and prognosis of advanced cancers
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Clinical management of metastatic colorectal cancer in the era of precision medicine
Ciardiello, F., Ciardiello, D., Martini, G., Napolitano, S., Tabernero, J. M., & Cervantes, A. M. R. (2022) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21728 · Cited by 537 · see citing works
The MAPK and AMPK signalings: interplay and implication in targeted cancer therapy
Yuan, J., Dong, X., Yap, J., & Hu, J. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00949-4 · Cited by 500 · see citing works
Host–microbiota maladaptation in colorectal cancer
Janney, A., Powrie, F., & Mann, E. H. (2020) · Nature · doi:10.1038/s41586-020-2729-3 · Cited by 445 · see citing works
New insights into the role of <scp>EMT</scp> in tumor immune escape
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“While the majority of colon carcinomas and corresponding cell lines appear more Epi on average, some tumors do exhibit Mes-like phenotypes likely corresponding to the newly established Mes molecular subtype (Punt et al., 2017).”
Background
m6A-induced lncRNA RP11 triggers the dissemination of colorectal cancer cells via upregulation of Zeb1
Wu, Y., Yang, X., Chen, Z., Tian, L., Jiang, G., Chen, F., Li, J., An, P., Lu, L., Luo, N., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1014-2 · Cited by 390 · see citing works
Integrated Omics of Metastatic Colorectal Cancer
Li, C., Sun, Y.-D., Yu, G.-Y., Cui, J.-R., Lou, Z., Zhang, H., Huang, Y., Bai, C.-G., Deng, L.-L., Liu, P., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.08.002 · Cited by 297 · see citing works
Image-based consensus molecular subtype (imCMS) classification of colorectal cancer using deep learning
Sirinukunwattana, K., Domingo, E., Richman, S. D., Redmond, K. L., Blake, A., Verrill, C., Leedham, S. J., Chatzipli, A., Hardy, C., Whalley, C. M., et al. (2021) · Gut · doi:10.1136/gutjnl-2019-319866 · Cited by 264 · see citing works
Prognostic and Predictive Molecular Biomarkers for Colorectal Cancer: Updates and Challenges
Koncina, E., Haan, S., Rauh, S., & Letellier, E. (2020) · Cancers · doi:10.3390/cancers12020319 · Cited by 261 · see citing works
“This mutation is typically mutually exclusive with other RAS mutations [40,69].”
Background
Impact of Consensus Molecular Subtype on Survival in Patients With Metastatic Colorectal Cancer: Results From CALGB/SWOG 80405 (Alliance)
Lenz, H.-J., Ou, F.-S., Venook, A. P., Hochster, H. S., Niedzwiecki, D., Goldberg, R. M., Mayer, R. J., Bertagnolli, M. M., Blanke, C. D., Zemla, T., et al. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.18.02258 · Cited by 246 · see citing works
“These insights have the potential to help treating physicians to use an individual’s tumor molecular makeup to predict likely sensitivity and resistance to targeted therapies.(9,10) ASSOCIATED CONTENT See accompanying Editorial on page 1847 Appendix Data Supplements Author affiliations and support information (if appl…”
Background
Droplet-based digital PCR and next generation sequencing for monitoring circulating tumor DNA: a cancer diagnostic perspective
Postel, M., Roosen, A., Laurent‐Puig, P., Taly, V., & Renault, S. (2017) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2018.1400384 · Cited by 255 · see citing works
“Third, presence of multiple tumor sites also complicates the characterization of the patient pathology [14].”
Background
Implementing anti-epidermal growth factor receptor (EGFR) therapy in metastatic colorectal cancer: challenges and future perspectives
Martinelli, E., Ciardiello, D., Martini, G., Troiani, T., Cardone, C., Vitiello, P. P., Normanno, N., Rachiglio, A. M., Maiello, E., Latiano, T., et al. (2020) · Annals of Oncology · doi:10.1016/j.annonc.2019.10.007 · Cited by 225 · see citing works
“Intratumor genetic heterogeneity refers to the concept that in a single tumor, different cancer cell clones, carrying different molecular alterations, coexist.(30) Recently, greater attention has been focused on the issue of tumor heterogeneity, since the presence of cancer cell clones with different mutations could c…”
Background
Clinical value of consensus molecular subtypes in colorectal cancer: a systematic review and meta-analysis
ten Hoorn, S., de Back, T. R., Sommeijer, D. W., & Vermeulen, L. (2022) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djab106 · Cited by 203 · see citing works
“CRC is a highly heterogeneous disease with respect to clinical and biological features, resulting in striking differences in disease progression and treatment response (2).”
BackgroundSelf-citation
Integrative analysis from multi-center studies identities a consensus machine learning-derived lncRNA signature for stage II/III colorectal cancer
Liu, Z., Guo, C., Dang, Q., Wang, L., Liu, L., Weng, S., Xu, H., Lu, T., Sun, Z., & Han, X. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103750 · Cited by 185 · see citing works
Overcoming Resistance to Natural Killer Cell Based Immunotherapies for Solid Tumors
Nayyar, G., Chu, Y., & Cairo, M. S. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00051 · Cited by 177 · see citing works
“This heterogeneity could be due to differences in evolution of these tumors caused by varying gene profile signature, different mutations and involvement of different cell signaling pathways (2, 3).”
Background
Colorectal Cancers: An Update on Their Molecular Pathology
Inamura, K. (2018) · Cancers · doi:10.3390/cancers10010026 · Cited by 176 · see citing works
Gold nanorods together with HSP inhibitor-VER-155008 micelles for colon cancer mild-temperature photothermal therapy
Tang, X., Tan, L., Shi, K., Peng, J., Xiao, Y., Li, W., Chen, L., Yang, Q., & Qian, Z. (2018) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2018.05.011 · Cited by 147 · see citing works
Genetic and epigenetic alterations of colorectal cancer
Hong, S. N. (2018) · Intestinal Research · doi:10.5217/ir.2018.16.3.327 · Cited by 144 · see citing works
“In human MSI-H CRC and cancer cell lines with MSI-H, APC , KRAS , and TP53 have been found to be mutated.(20,21) MSI-H tumors have been found in about 15% of sporadic CRCs.”
Background
Role of Epithelial to Mesenchymal Transition in Colorectal Cancer
Lu, J., Kornmann, M., & Traub, B. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914815 · Cited by 148 · see citing works
“[3,9,18,28,32,63–65].”
Molecular subtypes in cancers of the gastrointestinal tract
Bijlsma, M. F., Sadanandam, A., Tan, P. B. O., & Vermeulen, L. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.33 · Cited by 130 · see citing works
Self-citation
DDX39B drives colorectal cancer progression by promoting the stability and nuclear translocation of PKM2
Zhao, G., Yuan, H., Qin, L., Zhang, J., Guo, Y., Feng, T., Gu, R. C., Ou, D., Li, S., Li, K., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01096-7 · Cited by 127 · see citing works
Lactate controls cancer stemness and plasticity through epigenetic regulation
Nguyen, N. B., Gevers, S., Kok, R. N. U., Burgering, L. M., Neikes, H. K., Akkerman, N., Betjes, M. A., Ludikhuize, M. C., Gulersonmez, C. M. C., Stigter, E. C. A., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.01.002 · Cited by 129 · see citing works
SOX12 promotes colorectal cancer cell proliferation and metastasis by regulating asparagine synthesis
Du, F., Chen, J., Liu, H., Cai, Y., Cao, T., Han, W., Yi, X., Qian, M., Tian, D., Nie, Y., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1481-9 · Cited by 117 · see citing works
Integration of transcriptomics, proteomics, and metabolomics data to reveal HER2-associated metabolic heterogeneity in gastric cancer with response to immunotherapy and neoadjuvant chemotherapy
Yuan, Q., Deng, D., Chen, P., Ren, J., Wei, T., Wu, Z., Zhang, B., Li, S., Yin, P., & Shang, D. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.951137 · Cited by 117 · see citing works
“The response of patients to chemotherapy and immunotherapy and their prognosis are intimately associated with tumour heterogeneity (7, 8).”
Background
Co-cultures of colon cancer cells and cancer-associated fibroblasts recapitulate the aggressive features of mesenchymal-like colon cancer
Strating, E., Verhagen, M. P., Wensink, G. E., Dünnebach, E., Wijler, L. A., Aranguren, I., la Cruz, A. S. D., Peters, N. A., Hageman, J. H., van der Net, M. C., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1053920 · Cited by 120 · see citing works
“Some of this information has been used to devise more personalized strategies of (targeted) anti-cancer treatment (8, 9).”
Method
Integrated approaches for precision oncology in colorectal cancer: The more you know, the better
Andrei, P., Battuello, P., Grasso, G., Rovera, E., Tesio, N., & Bardelli, A. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.04.007 · Cited by 113 · see citing works
Mapping the spreading routes of lymphatic metastases in human colorectal cancer
Zhang, C., Zhang, L., Xu, T., Xue, R., Yu, L., Zhu, Y.-L., Wu, Y., Zhang, Q., Li, D., Shen, S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15886-6 · Cited by 112 · see citing works
Targeting cholesterol biosynthesis promotes anti-tumor immunity by inhibiting long noncoding RNA SNHG29-mediated YAP activation
Ni, W., Mo, H., Liu, Y., Xu, Y., Qin, C., Zhou, Y., Li, Y., Li, Y., Zhou, A., Yao, S., et al. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.05.012 · Cited by 110 · see citing works
Piperlongumine, a piper alkaloid targets Ras/PI3K/Akt/mTOR signaling axis to inhibit tumor cell growth and proliferation in DMH/DSS induced experimental colon cancer
Kumar, S., & Agnihotri, N. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.10.182 · Cited by 109 · see citing works
Prognostic Cancer Gene Expression Signatures: Current Status and Challenges
Qian, Y., Daza, J., Itzel, T., Betge, J., Zhan, T., Marmé, F., & Teufel, A. (2021) · Cells · doi:10.3390/cells10030648 · Cited by 107 · see citing works
“However, the selection of patients is currently suboptimal due to a lack of established biomarkers (except for mismatch repair deficiency), leading to either over- or undertreatment [45].”
Background
CCNA2 acts as a novel biomarker in regulating the growth and apoptosis of colorectal cancer
Gan, Y., Li, Y., Li, T., Shu, G., & Yin, G. (2018) · Cancer Management and Research · doi:10.2147/cmar.s176833 · Cited by 108 · see citing works
“Due to the high heterogeneity of CRC, researchers are exploring biomarkers that could indicate the specific cancer subtype and prognosis of CRC in recent decades.(20) Until now, several biomarkers have been discovered in a wide range of cancers.”
Background
Review of 5-FU resistance mechanisms in colorectal cancer: clinical significance of attenuated on-target effects
Gmeiner, W. H., & Okechukwu, C. C. (2023) · Cancer Drug Resistance · doi:10.20517/cdr.2022.136 · Cited by 108 · see citing works
DDX17 induces epithelial-mesenchymal transition and metastasis through the miR-149-3p/CYBRD1 pathway in colorectal cancer
Zhao, G., Wang, Q., Zhang, Y., Gu, R. C., Liu, M., Li, Q., Zhang, J., Yuan, H., Feng, T., Ou, D., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-022-05508-y · Cited by 103 · see citing works
“Accumulating evidence has indicated that CRC is a highly heterogeneous disease characterized by extensively dysregulated gene expression and mutational burdens [5, 6].”
Background
Targeting autophagy enhances apatinib-induced apoptosis via endoplasmic reticulum stress for human colorectal cancer
Cheng, X., Feng, H., Wu, H., Jin, Z., Shen, X., Kuang, J., Huo, Z., Chen, X., Gao, H., Ye, F., et al. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.05.046 · Cited by 102 · see citing works
Characterization of a p53/miR-34a/CSF1R/STAT3 Feedback Loop in Colorectal Cancer
Shi, X., Kaller, M., Rokavec, M., Kirchner, T., Horst, D. A., & Hermeking, H. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.04.002 · Cited by 101 · see citing works
“More than 50% of colorectal cancer (CRC) patients will develop liver metastases, leading to ineffective chemotherapy and increased mortality.(2,3) Epithelialmesenchymal transition (EMT) of primary tumor cells is one of the first steps of the metastatic cascade.”
Background
Integration of microbiology, molecular pathology, and epidemiology: a new paradigm to explore the pathogenesis of microbiome‐driven neoplasms
Hamada, T., Nowak, J. A., Milner, D. A., Song, M., & Ogino, S. (2019) · The Journal of Pathology · doi:10.1002/path.5236 · Cited by 100 · see citing works
Therapeutic potential of FLANC, a novel primate-specific long non-coding RNA in colorectal cancer
Pichler, M., Rodriguez‐Aguayo, C., Nam, S. Y., Dragomir, M. P., Bayraktar, R., Anfossi, S., Knutsen, E., Ivan, C., Fuentes‐Mattei, E., Lee, S. K., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-318903 · Cited by 95 · see citing works
MYC-Activated LncRNA MNX1-AS1 Promotes the Progression of Colorectal Cancer by Stabilizing YB1
Wu, Q., Luo, X.-J., Liu, J., Lu, Y., Wang, Y., Qi, J., Liu, Z., Huang, Q., Liu, Z.-K., Lu, J.-B., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-3747 · Cited by 96 · see citing works
“Recently, molecular stratification has been implemented in clinical practice to identify subgroups who may benefit from novel treatments, especially among patients with metastatic colorectal cancer who lack treatment options (1, 2, 4).”
Background
Peritoneal Metastases From Colorectal Cancer: Defining and Addressing the Challenges
Kranenburg, O., der Speeten, K. V., & de Hingh, I. H. J. T. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.650098 · Cited by 95 · see citing works
“The most effective regimens have prolonged median overall survival to more than 2 years (65).”
Background
Mutant p53 drives cancer chemotherapy resistance due to loss of function on activating transcription of PUMA
Huang, Y., Liu, N., Liu, J., Liu, Y., Zhang, C., Long, S., Luo, G., Zhang, L., & Zhang, Y. (2019) · Cell Cycle · doi:10.1080/15384101.2019.1688951 · Cited by 94 · see citing works
“P53 mutations found in 50% of the tumors left the growth out of control, promoting malignant development of the tumor [39,40], and were likely to be a clinical indicator of tumor [41,42].”
Background
A novel long noncoding RNA SP100-AS1 induces radioresistance of colorectal cancer via sponging miR-622 and stabilizing ATG3
Zhou, Y., Shao, Y., Hu, W., Zhang, J., Shi, Y., Kong, X., & Jiang, J. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-01049-1 · Cited by 93 · see citing works
Supramolecular Nanofibers of Curcumin for Highly Amplified Radiosensitization of Colorectal Cancers to Ionizing Radiation
Xu, H., Wang, T., Yang, C., Li, X., Liu, G., Yang, Z., Singh, P. K., Krishnan, S., & Ding, D. (2018) · Advanced Functional Materials · doi:10.1002/adfm.201707140 · Cited by 93 · see citing works
cRGD-decorated biodegradable polytyrosine nanoparticles for robust encapsulation and targeted delivery of doxorubicin to colorectal cancer in vivo
Gu, X., Wei, Y., Fan, Q., Sun, H., Cheng, R., Zhong, Z., & Deng, C. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.03.005 · Cited by 92 · see citing works
“Colorectal cancer remains one of the leading causes of cancer-related death worldwide [1,2].”
Background
Exploring and modelling colon cancer inter-tumour heterogeneity: opportunities and challenges
Buikhuisen, J. Y., Torang, A., & Medema, J. P. (2020) · Oncogenesis · doi:10.1038/s41389-020-00250-6 · Cited by 92 · see citing works
“Administration of chemotherapy to stage III patients increases overall survival, but the bene ﬁ t for high-risk stage II patients has been called into question 9,10 .”
BackgroundInfluential
Co-targeting of EGFR and autophagy signaling is an emerging treatment strategy in metastatic colorectal cancer
Koustas, E., Karamouzis, M. V., Mihailidou, C., Schizas, D., & Papavassiliou, A. G. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.03.023 · Cited by 79 · see citing works
Heterogeneous pathway activation and drug response modelled in colorectal-tumor-derived 3D cultures
Schumacher, D., Andrieux, G., Boehnke, K., Keil, M., Silvestri, A., Silvestrov, M., Keilholz, U., Haybaeck, J., Erdmann, G., Sachse, C., et al. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008076 · Cited by 80 · see citing works
“Mutations in RAS gene family members or BRAF turn out to be negative predictors for anti-receptor tyrosine kinase therapies [5], while at least a subset of RAS wild-type tumors shows a therapeutic response [6].”
Background
In silico development and clinical validation of novel 8 gene signature based on lipid metabolism related genes in colon adenocarcinoma
Jiang, C., Liu, Y., Wen, S., Xu, C., & Gu, L. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105644 · Cited by 80 · see citing works
Molecular subtype identification and prognosis stratification by a metabolism-related gene expression signature in colorectal cancer
Lin, D., Fan, W., Zhang, R., Zhao, E., Li, P., Zhou, W., Peng, J., & Li, L. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-02952-w · Cited by 80 · see citing works
“However, the relapse and death risks may vary vastly even in patients with the same clinicopathological features due to the high level of molecular heterogeneity [4, 5].”
Background
Molecular profiling of neuroendocrine tumours to predict response and toxicity to peptide receptor radionuclide therapy
Bodei, L., Schöder, H. M., Baum, R. P., Herrmann, K., Strosberg, J., Caplin, M. E., Öberg, K., & Modlin, I. M. (2020) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30323-5 · Cited by 79 · see citing works
Recent Advances in Therapeutic Strategies to Improve Colorectal Cancer Treatment
Gmeiner, W. H. (2024) · Cancers · doi:10.3390/cancers16051029 · Cited by 78 · see citing works
“5-FU/LV is useful in palliative therapy for mCRC, but the development of effective doublet combination therapy regimens, including FOLFOX (folinic acid (leucovorin), 5-FU, oxaliplatin) and FOLFIRI (leucovorin, 5-FU, irinotecan) [10], resulted in significant survival advantages.”
Background
Microenvironment-triggered multimodal precision diagnostics
Hao, L., Rohani, N., Zhao, R. T., Pulver, E. M., Mak, H. H., Kelada, O. J., Ko, H., Fleming, H. E., Gertler, F. B., & Bhatia, S. N. (2021) · Nature Materials · doi:10.1038/s41563-021-01042-y · Cited by 76 · see citing works
Patient-derived mini-colons enable long-term modeling of tumor–microenvironment complexity
Lorenzo‐Martín, L. F., Broguière, N., Langer, J., Tillard, L., Nikolaev, M., Coukos, G., Homicskó, K., & Lütolf, M. P. (2024) · Nature Biotechnology · doi:10.1038/s41587-024-02301-4 · Cited by 74 · see citing works
“Despite these efforts, ex vivo modeling of CRC has shown relatively limited translational success in the clinical scenario so far 6,7 , indicating that the nature of current in vitro systems is still overly simplistic 4,8,9 .”
Autophagy mediates glucose starvation-induced glioblastoma cell quiescence and chemoresistance through coordinating cell metabolism, cell cycle, and survival
Wang, L. Y., Shang, Z., Zhou, Y., Hu, X., Chen, Y., Fan, Y., Wei, X., Wu, L. L., Liang, Q., Zhang, J., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0242-x · Cited by 73 · see citing works
Bioinspired protein corona strategy enhanced biocompatibility of Ag-Hybrid hollow Au nanoshells for surface-enhanced Raman scattering imaging and on-demand activation tumor-phototherapy
He, J., Wei, Q., Wang, S., Hua, S., & Zhou, M. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120734 · Cited by 71 · see citing works
Ribosome Biogenesis Alterations in Colorectal Cancer
Nait-Slimane, S., Marcel, V., Fenouil, T., Catez, F., Saurin, J., Bouvet, P., Diaz, J., & Mertani, H. C. (2020) · Cells · doi:10.3390/cells9112361 · Cited by 68 · see citing works
“Among the genetic mutations, the Kirsten rat sarcoma 2 viral oncogene homolog (KRAS) gene mutated in 40% and the BRAF gene mutated in 10% of CRC patients are useful predictive markers for metastatic disease [2,18,19].”
Background
Advances in colon cancer research: in vitro and animal models
Lannagan, T. R. M., Jackstadt, R., Leedham, S. J., & Sansom, O. J. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.12.003 · Cited by 71 · see citing works
“While the use of EGFR inhibitor depends on the mutation status of KRAS and BRAF [5], VEGFR inhibitors are routinely applied for stage IV patients [6].”
Background
Macromolecular Poly(N‐isopropylacrylamide) (PNIPAM) in Cancer Treatment and Beyond
Throat, S., & Bhattacharya, S. (2024) · Advances in Polymer Technology · doi:10.1155/2024/1444990 · Cited by 68 · see citing works
Prognostic role of carcinoembryonic antigen and carbohydrate antigen 19-9 in metastatic colorectal cancer: a BRAF-mutant subset with high CA 19-9 level and poor outcome
Thomsen, M., Skovlund, E., Sørbye, H., Bolstad, N., Nustad, K., Glimelius, B. L. G., Pfeiffer, P., Kure, E. H., Johansen, J. S., Tveit, K. M., et al. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0115-9 · Cited by 68 · see citing works
“1 162 (29) 155 (28) 145 (29) 10 (20) 126 (29) 119 (29)”
High‐risk Stage III colon cancer patients identified by a novel five‐gene mutational signature are characterized by upregulation of IL‐23A and gut bacterial translocation of the tumor microenvironment
Ge, W., Hu, H., Cai, W., Xu, J., Hu, W., Weng, X., Qin, X., Huang, Y., Han, W., Hu, Y., et al. (2019) · International Journal of Cancer · doi:10.1002/ijc.32775 · Cited by 67 · see citing works
“Single genetic characteristics, such as DNA mismatch repair (MMR) deficiency status, RAS-mutation or BRAFmutation, have been proposed as prognostic biomarkers.(1,5) Somatic mutational profiling based molecular signatures have been developed to detecting patients at a high risk of recurrence.”
Background
The effect of miRNA and autophagy on colorectal cancer
Long, J., He, Q., Yin, Y., Lei, X., Li, Z., & Zhu, W. (2020) · Cell Proliferation · doi:10.1111/cpr.12900 · Cited by 66 · see citing works
HSP90-dependent PUS7 overexpression facilitates the metastasis of colorectal cancer cells by regulating LASP1 abundance
Song, D., Guo, M. Z., Xu, S., Xiaotian, S., Bai, B., Li, Z., Chen, J., An, Y., Nie, Y., Wu, K., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01951-5 · Cited by 65 · see citing works
“and advanced metastatic CRC remains incurable [3, 5].”
Conversion strategies with chemotherapy plus targeted agents for colorectal cancer liver-only metastases: A systematic review
Bolhuis, K., Kos, M., van Oijen, M. G. H., Swijnenburg, R., & Punt, C. J. A. (2020) · European Journal of Cancer · doi:10.1016/j.ejca.2020.09.037 · Cited by 63 · see citing works
Self-citation
Tumor PDCD1LG2 (PD-L2) Expression and the Lymphocytic Reaction to Colorectal Cancer
Masugi, Y., Nishihara, R., Hamada, T., Song, M., da Silva, A., Kosumi, K., Gu, M., Shi, Y. X., Li, W., Liu, L., et al. (2017) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0122 · Cited by 61 · see citing works
A Phase Ib/II Study of WNT974 + Encorafenib + Cetuximab in Patients With BRAFV600E-MutantKRASWild-Type Metastatic Colorectal Cancer
Tabernero, J. M., Cutsem, E. V., Garralda, E., Tai, D. W.-M., de Braud, F., Geva, R., van Bussel, M. T. J., Dotti, K. F., Élez, E., Miguel, M. J. D., et al. (2023) · The Oncologist · doi:10.1093/oncolo/oyad007 · Cited by 60 · see citing works
TIME (Tumor Immunity in the MicroEnvironment) classification based on tumor CD274 (PD-L1) expression status and tumor-infiltrating lymphocytes in colorectal carcinomas
Hamada, T., Soong, T. R., Masugi, Y., Kosumi, K., Nowak, J. A., da Silva, A., Mu, X. J., Twombly, T. S., Koh, H., Yang, J., et al. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1442999 · Cited by 58 · see citing works
DNA methylation and chromatin modifiers in colorectal cancer
Vymetalkova, V. P., Vodička, P., Vodenková, S., Alonso, S., & Schneider‐Stock, R. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.04.002 · Cited by 58 · see citing works
The Promise of Circulating Tumor DNA (ctDNA) in the Management of Early-Stage Colon Cancer: A Critical Review
Chakrabarti, S., Xie, H., Urrutia, R. A., & Mahipal, A. (2020) · Cancers · doi:10.3390/cancers12102808 · Cited by 57 · see citing works
“Furthermore, tumor sequencing might not detect all relevant mutations because of intratumor heterogeneity [42] and may not capture subsequently emerging mutations as a result of treatment [43].”
Background
Chimeric antigen receptor T cells in solid tumors: a war against the tumor microenvironment
Zhao, Z., Xiao, X., Saw, P. E., Wu, W., Huang, H., Chen, J., & Nie, Y. (2019) · Science China Life Sciences · doi:10.1007/s11427-019-9665-8 · Cited by 56 · see citing works
5-ALA mediated photodynamic therapy with combined treatment improves anti-tumor efficacy of immunotherapy through boosting immunogenic cell death
Sun, Z., Zhao, M., Wang, W., Hong, L., Wu, Z., Luo, G., Lu, S., Tang, Y., Li, J., Wang, J., et al. (2023) · Cancer Letters · doi:10.1016/j.canlet.2022.216032 · Cited by 57 · see citing works
Immune Resistance and EGFR Antagonists in Colorectal Cancer
Giordano, G., Remo, A., Porrás, A., & Pancione, M. (2019) · Cancers · doi:10.3390/cancers11081089 · Cited by 55 · see citing works
“In fact, the inhibition of VEGFR2 in xenograft assays resistant to EGFR blockade was able to reduce tumor growth [4,14,23].”
Background
New insights into the epigenetics of inflammatory rheumatic diseases
Ballestar, E., & Li, T. (2017) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2017.147 · Cited by 54 · see citing works
Tumor-associated macrophages (TAMs) depend on MMP1 for their cancer-promoting role
Yu, J., Xu, Z., Guo, J., Yang, K., Zheng, J., & Sun, X. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00730-7 · Cited by 53 · see citing works
“Although great progress has been achieved in early detection and multimodality treatment of CRC [2, 3], most advanced CRC patients have a poor prognosis.”
Background
Integrated multi-omics characterization of KRAS mutant colorectal cancer
Chong, W., Zhu, X., Ren, H., Ye, C., Xu, K., Wang, Z., Jia, S., Shang, L., Li, L., & Chen, H. (2022) · Theranostics · doi:10.7150/thno.73089 · Cited by 53 · see citing works
“CRC is widely considered a heterogeneous disease, with multiple gene alterations and numerous pathways involved in its pathogenesis [2].”
Background
Enhanced anti-cancer activity of andrographis with oligomeric proanthocyanidins through activation of metabolic and ferroptosis pathways in colorectal cancer
Shimura, T., Sharma, P., Sharma, G. G., Banwait, J. K., & Goel, A. (2021) · Scientific Reports · doi:10.1038/s41598-021-87283-y · Cited by 52 · see citing works
Stemness Refines the Classification of Colorectal Cancer With Stratified Prognosis, Multi-Omics Landscape, Potential Mechanisms, and Treatment Options
Liu, Z., Xu, H., Weng, S., Ren, Y., & Han, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.828330 · Cited by 52 · see citing works
“Mounting evidence have established the links between cancer stemness and intratumoral heterogeneity across cancer (2, 9, 10, 18), and a theory believes cancer stemness is the origin of intratumoral heterogeneity and plasticity (19).”
BackgroundMethod
Patient-derived organoids as a platform for drug screening in metastatic colorectal cancer
He, X., Jiang, Y. J., Zhang, L., Li, Y., Hu, X., Hua, G., Cai, S., Mo, S., & Peng, J. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1190637 · Cited by 52 · see citing works
Role of COL6A3 in colorectal cancer
Liu, W., Li, L., Ye, H., Tao, H., & He, H. (2018) · Oncology Reports · doi:10.3892/or.2018.6331 · Cited by 52 · see citing works
“The application of NGS has led to the identification of several mutated genes in CRC that predict survival outcomes (2,27).”
Background
T‐cell immunoglobulin and ITIM domain, as a potential immune checkpoint target for immunotherapy of colorectal cancer
Fathi, M., Pustokhina, I., Kuznetsov, S. V., Khayrullin, M., Hojjat‐Farsangi, M., Karpisheh, V., Jalili, A., & Jadidi‐Niaragh, F. (2021) · IUBMB Life · doi:10.1002/iub.2461 · Cited by 52 · see citing works
“Similarly, liver metastases in many CRC patients with unsuccessful treatment result in higher mortality.(14,15) Mounting studies have demonstrated the role of the tumor microenvironment in cancer treatments, particularly checkpoint inhibitor-based immunotherapy.”
Background
Chemistry of Fluorinated Pyrimidines in the Era of Personalized Medicine
Gmeiner, W. H. (2020) · Molecules · doi:10.3390/molecules25153438 · Cited by 51 · see citing works
“FPs cont nue to be he most widely used drugs for CRC treatment and are h ghly relevant for cancer treatment in the era of personalized medicine [99].”
Background
Not Everyone Fits the Mold: Intratumor and Intertumor Heterogeneity and Innovative Cancer Drug Design and Development
Dzobo, K., Senthebane, D. A., Thomford, N. E., Rowe, A., Dandara, C., & Parker, M. I. (2018) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2017.0174 · Cited by 51 · see citing works
“Currently, biomarkers obtained using cancer cells are obtained from the primary tumor direct targeted therapy (Punt et al., 2017; Turner and Reis-Filho, 2012; Zhang et al., 2016a).”
Novel digital signatures of tissue phenotypes for predicting distant metastasis in colorectal cancer
Sirinukunwattana, K., Snead, D. R. J., Epstein, D. B. A., Aftab, Z., Mujeeb, I., Tsang, Y. W., Cree, I. A., & Rajpoot, N. (2018) · Scientific Reports · doi:10.1038/s41598-018-31799-3 · Cited by 52 · see citing works
Histopathological growth patterns of colorectal liver metastasis exhibit little heterogeneity and can be determined with a high diagnostic accuracy
Höppener, D. J., Nierop, P. M. H., Herpel, E., Rahbari, N. N., Doukas, M., Vermeulen, P., Grünhagen, D. J., & Verhoef, C. K. (2019) · Clinical & Experimental Metastasis · doi:10.1007/s10585-019-09975-0 · Cited by 51 · see citing works
DPP3/CDK1 contributes to the progression of colorectal cancer through regulating cell proliferation, cell apoptosis, and cell migration
Tong, Y., Huang, Y., Zhang, Y., Zeng, X., Yan, M., Xia, Z., & Lai, D. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03796-4 · Cited by 51 · see citing works
BRAF Mutations as Actionable Targets: A Paradigm Shift in the Management of Colorectal Cancer and Novel Avenues
Şahin, İ. H., & Klostergaard, J. (2021) · JCO Oncology Practice · doi:10.1200/op.21.00160 · Cited by 53 · see citing works
Detection and clinical significance of circulating tumor cells in colorectal cancer
Jiang, M., Jin, S., Han, J., Li, T., Shi, J., Zhong, Q., Li, W., Tang, W., Huang, Q., & Zong, H. (2021) · Biomarker Research · doi:10.1186/s40364-021-00326-4 · Cited by 51 · see citing works
“Early detection and precision treatment are keys to improving the prognosis of CRC patients [3].”
Background
Forkhead box K2 promotes human colorectal cancer metastasis by upregulating ZEB1 and EGFR
Du, F., Qiao, C., Li, X., Chen, Z., Liu, H., Wu, S., Hu, S., Qiu, Z., Qian, M., Tian, D., et al. (2019) · Theranostics · doi:10.7150/thno.31716 · Cited by 50 · see citing works
“which have improved the survival rate of CRC at the early stage, knowledge of the underlying molecular mechanisms and therapeutics for advanced metastatic CRC are lacking [2, 3].”
Background
Patient‐derived organoids as a preclinical platform for precision medicine in colorectal cancer
Cho, Y., Min, D., Kim, H., An, Y., Kim, S., Youk, J., Chun, J., Im, J. P., Song, S., Ju, Y. S., et al. (2021) · Molecular Oncology · doi:10.1002/1878-0261.13144 · Cited by 49 · see citing works
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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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