Cited by 540Colorectal Cancer Treatments and StudiesLung Cancer Treatments and MutationsHER2/EGFR in Cancer Research

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PTEN loss of expression predicts cetuximab efficacy in metastatic colorectal cancer patients

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Frattini, M, Saletti, P, Romagnani, E, Martin, V, Molinari, F, Ghisletta, M, Camponovo, A, Etienne, L L, Cavalli, F, Mazzucchelli, L·2007·British Journal of Cancer

DOI 10.1038/sj.bjc.6604009PMC PMC2360431

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Abstract

To evaluate whether the epidermal growth factor receptor (EGFR), K-Ras and PTEN, all members of the EGFR signalling pathway, may affect the clinical response in cetuximab-treated metastatic colorectal cancer (mCRC) patients. Twenty-seven cetuximab-treated mCRC patients were evaluated for drug response and investigated for EGFR protein expression and gene status, K-Ras mutational status and PTEN protein expression. Ten patients achieved a partial response (PR) to cetuximab-based therapy. All 27 patients showed EGFR protein overexpression. Epidermal growth factor receptor gene amplification was observed in eight out of 27 (30%) and chromosome 7 marked polysomy in 16 (59%) patients. Partial response was observed in six out of eight patients with EGFR gene amplification, four out of 16 with marked polysomy and none out of three with eusomy (P<0.05). The K-Ras wild-type sequence was observed in 17 patients, and nine of them experienced a PR. Conversely, K-Ras was mutated in 10 cases, of which one patient experienced a PR (P<0.05). The PTEN protein was normally expressed in 16 patients, and 10 of them achieved a PR. In contrast, no benefit was documented in 11 patients with loss of PTEN activity (P<0.001). Patients with EGFR gene amplification or chromosome 7 marked polysomy respond to cetuximab. In addition to K-Ras mutations, we demonstrate for the first time that the loss of PTEN protein expression is associated with nonresponsiveness to cetuximab.

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Basic Science Review: Nitric Oxide—Releasing Prosthetic Materials
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Inhibition of EGFR, HER2, and HER3 signalling in patients with colorectal cancer wild-type for BRAF, PIK3CA, KRAS , and NRAS (FOCUS4-D): a phase 2–3 randomised trial
Adams, R., Brown, E. R., Brown, L. C., Butler, R., Falk, S. J., Fisher, D. J., Kaplan, R. S., Quirke, P., Richman, S. D., Samuel, L. M., et al. (2017) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(17)30394-1 · Cited by 56
Sorafenib and irinotecan (NEXIRI) as second- or later-line treatment for patients with metastatic colorectal cancer and KRAS-mutated tumours: a multicentre Phase I/II trial
Samalin, E., Bouché, O., Thézenas, S., François, É., Adenis, A., Bennouna, J., Taı̈eb, J., Desseigne, F., Seitz, J. F., Conroy, T., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2013.813 · Cited by 55
“Expression of EGFR, HER2, PTEN, NF-kB and cyclin D1 was evaluated by immunohistochemistry on 3-mm tissue sections of paraffin-embedded specimens as previously performed in previous studies (Chung et al, 2005; Frattini et al, 2007; Scartozzi et al, 2007; Cascinu et al, 2008; Loupakis et al, 2009).”
Method
Prognostic and predictive value of TOPK stratified by KRAS and BRAF gene alterations in sporadic, hereditary and metastatic colorectal cancer patients
Zlobec, I., Molinari, F., Kovac, M., Bihl, M., Altermatt, H. J., Diebold, J., Frick, H., Germer, M., Horcic, M., Montani, M., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605452 · Cited by 54
“Clinical data including patient age at diagnosis, tumour location and follow-up were retrieved from patient records.”
MethodSelf-citation
Human umbilical cord blood mesenchymal stem cell-derived extracellular matrix prohibits metastatic cancer cell MDA-MB-231 proliferation
Sun, B., Yu, K., Bhandari, D. R., Jung, J., Kang, S., & Kang, K. (2010) · Cancer Letters · doi:10.1016/j.canlet.2010.04.007 · Cited by 54
“PTEN levels in cancer cells are critical for cancer promotion [22,23].”
Background
Spatially aware graph neural networks and cross-level molecular profile prediction in colon cancer histopathology: a retrospective multi-cohort study
Ding, K., Zhou, M., Wang, H., Zhang, S., & Metaxas, D. (2022) · The Lancet Digital Health · doi:10.1016/s2589-7500(22)00168-6 · Cited by 53
Profilin‐1 overexpression inhibits proliferation of MDA‐MB‐231 breast cancer cells partly through p27kip1 upregulation
Zou, L., Ding, Z., & Roy, P. S. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22058 · Cited by 53
“Cancer cells with reduced PTEN expression and therefore having hyperactivated AKT signaling are resistant to chemotherapy and conversely, PTEN overexpression increases apoptotic susceptibility of cancer cells to chemotherapeutics (Yan et al., 2006; Frattini et al., 2007; Jiang et al., 2007).”
Background
Tumor budding predicts response to anti-EGFR therapies in metastatic colorectal cancer patients
Zlobec, I. (2010) · World Journal of Gastroenterology · doi:10.3748/wjg.v16.i38.4823 · Cited by 52
PTEN expression controls cellular response to cetuximab by mediating PI3K/AKT and RAS/RAF/MAPK downstream signaling in KRAS wild-type, hormone refractory prostate cancer cells
Merlin (2009) · Oncology Reports · doi:10.3892/or_00000278 · Cited by 53
Advances in targeted and immunobased therapies for colorectal cancer in the genomic era
Seow, H. F., Yip, W. K., & Fifis, T. (2016) · OncoTargets and Therapy · doi:10.2147/ott.s95101 · Cited by 54
ERK and MDM2 prey on FOXO3a
Yang, W., Dolloff, N. G., & El‐Deiry, W. S. (2008) · Nature Cell Biology · doi:10.1038/ncb0208-125 · Cited by 50
Trastuzumab Sensitizes Ovarian Cancer Cells to EGFR-targeted Therapeutics
Wilken, J. A., Webster, K. T., & Maihle, N. J. (2010) · Journal of Ovarian Research · doi:10.1186/1757-2215-3-7 · Cited by 50
“In these studies, K-Ras mutation status has proven to be a clinically useful negative indicator of responsiveness to cetuximab [26-29], but in no case is there a single accurate positive predictor of responsiveness to this new drug, including analysis of expression of cetuximab's target i.”
Background
The PI3K/Akt/mTOR axis in colorectal cancer: Oncogenic alterations, non‐coding RNAs, therapeutic opportunities, and the emerging role of nanoparticles
Sanaei, M., Khorasani, A. B. S., Pourbagheri‐Sigaroodi, A., Shahrokh, S., Zali, M. R., & Bashash, D. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30655 · Cited by 57
“…loss of PTEN expression in metastatic CRC patients could be predictive for the outcome of combined therapy using both cetux- imab and irinotecan (Frattini et al., 2007; Loupakis et al., 2009); suggesting that it would be beneficial to identify PTEN status in metastatic CRC patients before…”
Background
Additional value of EGFR downstream signaling phosphoprotein expression to KRAS status for response to anti‐EGFR antibodies in colorectal cancer
Perkins, G., Lièvre, A., Ramacci, C., Méatchi, T., de Reyniès, A., Emile, J., Boige, V., Tomasic, G., Bachet, J., Bibeau, F., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25152 · Cited by 54
“Recently, the loss of PTEN expression, a key negative regulator of PI3K/AKT pathway has also been shown linked to resistance to cetuximab or panitumumab.(13) This result is consistent with the association between resistance to anti-EGFR therapies and the high expression of pP70S6K, the terminal effector of the PI3K/AK…”
Result
PTEN expression is consistent in colorectal cancer primaries and metastases and associates with patient survival
Atreya, C. E., Sangale, Z., Xu, N., Matli, M. R., Tikishvili, E., Welbourn, W., Stone, S., Shokat, K. M., & Warren, R. S. (2013) · Cancer Medicine · doi:10.1002/cam4.97 · Cited by 52
Prognostic but not predictive role of platelet‐derived growth factor receptors in patients with recurrent glioblastoma
Paulsson, J., Lindh, M. B., Jarvius, M., Puputti, M., Nistér, M., Nupponen, N. N., Paulus, W., Söderberg, O., Dresemann, G. P., von Deimling, A., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25528 · Cited by 49
Biomarkers of Resistance to Epidermal Growth Factor Receptor Monoclonal Antibodies in Patients with Metastatic Colorectal Cancer
Banck, M. S., & Grothey, A. F. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0188 · Cited by 47
EGFR gene copy number assessment from areas with highest EGFR expression predicts response to anti-EGFR therapy in colorectal cancer
Ålgars, A., Lintunen, M., Carpén, O., Ristamäki, R., & Sundström, J. T. T. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.223 · Cited by 53
Therapeutic modulation of k-ras signaling in colorectal cancer
Krens, L. L., Baas, J. M., Gelderblom, H. A. J., & Guchelaar, H. (2010) · Drug Discovery Today · doi:10.1016/j.drudis.2010.05.012 · Cited by 46
Clinical, laboratory and molecular factors predicting chemotherapy efficacy and toxicity in colorectal cancer
Chua, W. M., Kho, P. S., Moore, M. M., Charles, K. A., & Clarke, S. J. (2010) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2010.07.012 · Cited by 45
“[202] 27 patients treated with cetuximab± irinotecan; first and”
Background
Combined therapies for cancer: a review of EGFR-targeted monotherapy and combination treatment with other drugs
Zahorowska, B., Crowe, P. J., & Yang, J. (2009) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-009-0622-4 · Cited by 47
“For example, PTEN status likewise aVects the EGFR-targeted treatment response (Frattini et al. 2007).”
Background
Association between KRAS codon 13 mutations and clinical response to anti-EGFR treatment in patients with metastatic colorectal cancer: results from a meta-analysis
Chen, J., Ye, Y., Sun, H., & Shi, G. (2012) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-012-2005-9 · Cited by 48
An overview of the epidermal growth factor receptor fluorescence in situ hybridisation challenge in tumour pathology
Martin, V., Mazzucchelli, L., & Frattini, M. (2008) · Journal of Clinical Pathology · doi:10.1136/jcp.2008.059592 · Cited by 46
“16–19 33 However, it is becoming evident that, in this context, alterations occurring at the EGFR downstream pathways (ie, K-ras, PTEN) might also play a relevant role in the prediction of the efficacy of EGFR targeted therapies.(17) 30”
BackgroundMethodSelf-citation
The human epidermal growth factor receptor (EGFR) gene in European patients with advanced colorectal cancer harbors infrequent mutations in its tyrosine kinase domain
Metzger, B., Chambeau, L., Begon, D. Y., Faber, C., Kayser, J., Berchem, G., Pauly, M., Boniver, J., Delvenne, P., Dicato, M. A., et al. (2011) · BMC Medical Genetics · doi:10.1186/1471-2350-12-144 · Cited by 48
“34 to 12% .[10-13, 15, 18-20] Hence, our cohort may be representative of the disease.”
Background
Experimental results and related clinical implications of PET detection of epidermal growth factor receptor (EGFr) in cancer
Pantaleo, M. A., Nannini, M., Maleddu, A., Fanti, S., Nanni, C., Boschi, S., Lodi, F., Nicoletti, G., Landuzzi, L., Lollini, P., et al. (2008) · Annals of Oncology · doi:10.1093/annonc/mdn625 · Cited by 45
“In a small series, the loss of PTEN protein expression in at least 50% of tumour cells by IHC seemed to be associated with nonresponsiveness to cetuximab: 62% of patients with intact protein expression had an objective response to cetuximabbased therapy, whereas 0% of patients with loss of PTEN protein expression had…”
Background
A pan-HER approach for cancer therapy: background, current status and future development
Huang, Z., Brdlik, C. M., Jin, P., & Shepard, H. M. (2008) · Expert Opinion on Biological Therapy · doi:10.1517/14712590802630427 · Cited by 45
“KRAS mutation and loss of the phosphatase and tensin homolog (PTEN) tumor suppressor gene, which activates signaling downstream of HER receptors, has been demonstrated to contribute to the primary resistance to cetuximab and panitumumab [58] .”
Background
Meta-analysis comparing the efficacy of anti-EGFR monoclonal antibody therapy between KRAS G13D and other KRAS mutant metastatic colorectal cancer tumours
Rowland, A., Dias, M. M., Wiese, M. D., Kichenadasse, G., McKinnon, R. A., Karapetis, C. S., & Sorich, M. J. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2015.11.025 · Cited by 46
Targeted therapy in advanced metastatic colorectal cancer: Current concepts and perspectives
Hohla, F. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i20.6102 · Cited by 45
JQ1 suppresses tumor growth via PTEN/PI3K/AKT pathway in endometrial cancer
Qiu, H., Li, J., Clark, L. H., Jackson, A. L., Zhang, L., Guo, H., Kilgore, J. E., Gehrig, P. A., Zhou, C., & Bae-Jump, V. L. (2016) · Oncotarget · doi:10.18632/oncotarget.11631 · Cited by 45
Retracted
Genetic and Epigenetic Biomarkers of Colorectal Cancer
Choong, M. K., & Tsafnat, G. (2011) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2011.04.020 · Cited by 45
A comprehensive analysis of phosphatase and tensin homolog deleted on chromosome 10 (PTEN) loss in colorectal cancer
Lin, P.-C., Lin, J.-K., Lin, H., Lan, Y., Lin, C., Yang, S.-H., Chen, W.-S., Liang, W.-Y., Jiang, J., & Chang, S. (2015) · World Journal of Surgical Oncology · doi:10.1186/s12957-015-0601-y · Cited by 44
“3 %) of CRCs and is consistent with other reports, which have indicated that 20–40 % of CRCs are negative for PTEN expression [25, 26].”
Result
Analgesic-antitumor peptide induces apoptosis and inhibits the proliferation of SW480 human colon cancer cells
Gu, Y., Liu, S., Ju, W.-Z., Li, C., & Cao, P. (2012) · Oncology Letters · doi:10.3892/ol.2012.1049 · Cited by 44
“Loss of PTEN expression is present in 20-40% of CRC tumors assessed by immunohistochemistry (31-33).”
The Role of PTEN in Tumor Angiogenesis
Rodriguez, S., & Huynh‐Do, U. (2011) · Journal of Oncology · doi:10.1155/2012/141236 · Cited by 44
Clinical Biomarkers in Oncology
Roock, W. D., Biesmans, B., Schutter, J. D., & Tejpar, S. (2009) · Molecular Diagnosis & Therapy · doi:10.1007/bf03256319 · Cited by 44
Predictive role of multiple gene alterations in response to cetuximab in metastatic colorectal cancer: A single center study
Ulivi, P., Capelli, L., Valgiusti, M., Zoli, W., Scarpi, E., Chiadini, E., Rosetti, P., Bravaccini, S., Calistri, D., Saragoni, L., et al. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-87 · Cited by 45
“We did not obtain significant results on PTEN alterations, in accordance with some studies [21,27] but in contrast to others in which a correlation was observed between the lack of PTEN expression and response to CTX [19,37].”
Result
EGFR FISH in colorectal cancer: what is the current reality?
Moroni, M., Bianchi, A. S., Veronese, S. M., & Siena, S. (2008) · The Lancet Oncology · doi:10.1016/s1470-2045(08)70109-8 · Cited by 45
Beyond KRAS: Predictive factors of the efficacy of anti-EGFR monoclonal antibodies in the treatment of metastatic colorectal cancer
Stefano, A. D. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i29.9732 · Cited by 45
Molecular Testing in Colorectal Cancer
Shi, C., & Washington, K. M. (2012) · American Journal of Clinical Pathology · doi:10.1309/ajcpi83dinulujni · Cited by 43
Molecular Predictors of Response to Chemotherapy in Colorectal Cancer
Dienstmann, R., Vilar, E., & Tabernero, J. M. (2011) · The Cancer Journal · doi:10.1097/ppo.0b013e318212f844 · Cited by 43
“Loss of PTEN expression is present in 20% to 40% of CRC tumors assessed by IHC.36,43,44 It has been suggested that loss of PTEN expression, 118 www.journalppo.com * 2011 Lippincott Williams & Wilkins Copyright © 2011 Lippincott Williams & Wilkins.”
Background
New Strategies in Colorectal Cancer: Biomarkers of Response to Epidermal Growth Factor Receptor Monoclonal Antibodies and Potential Therapeutic Targets in Phosphoinositide 3-Kinase and Mitogen-Activated Protein Kinase Pathways
Dasari, A. N., & Messersmith, W. A. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-2283 · Cited by 42
Colorectal Cancer: From Genetic Landscape to Targeted Therapy
Bali, M. E., Bakkach, J., & Mechita, M. B. (2021) · Journal of Oncology · doi:10.1155/2021/9918116 · Cited by 43
Role of HGF–MET Signaling in Primary and Acquired Resistance to Targeted Therapies in Cancer
Corte, C. M. D., Fasano, M., Papaccio, F., Ciardiello, F., & Morgillo, F. (2014) · Biomedicines · doi:10.3390/biomedicines2040345 · Cited by 41
“(PTEN) expression [57].”
Hepatocyte Growth Factor Induces Resistance to Anti-Epidermal Growth Factor Receptor Antibody in Lung Cancer
Yamada, T., Takeuchi, S., Kita, K., Bando, H., Nakamura, T., Matsumoto, K., & Yano, S. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e3182398e69 · Cited by 44
Loss of PTEN expression as a predictor of resistance to anti-EGFR monoclonal therapy in metastatic colorectal cancer: evidence from retrospective studies
Wang, Z., Gao, Q., & Fang, J. (2012) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-012-1886-y · Cited by 43
“Frattini [12], Italy Retrospective 27 11/27 (40.”
Background
A growing family: Adding mutated Erbb4 as a novel cancer target
Rudloff, U., & Samuels, Y. (2010) · Cell Cycle · doi:10.4161/cc.9.8.11239 · Cited by 40
PTEN Overexpression Cooperates With Lithium to Reduce the Malignancy and to Increase Cell Death by Apoptosis via PI3K/Akt Suppression in Colorectal Cancer Cells
de Araújo, W. M., Robbs, B. K., Bastos, L. G., de Souza, W. F., Vidal, F. C. B., Viola, J. P. B., & Morgado‐Díaz, J. A. (2015) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25294 · Cited by 41
“In CRC patients, downregulation of PTEN and/or the presence of mutated PI3K induces resistance to treatment with cetuximab, an EGFR-targeting antibody; similar results have been observed in CRC cell lines [Frattini et al., 2007; Jhawer et al., 2008].”
Result
Systematic review of pharmacogenetic testing for predicting clinical benefit to anti-EGFR therapy in metastatic colorectal cancer.
Lin, J. S., Webber, E. M., Senger, C. A., Holmes, R. S., & Whitlock, E. P. (2011) · PubMed · Cited by 40
Role of Biologics in First-Line Treatment of Colorectal Cancer
Mahipal, A., & Grothey, A. F. (2016) · Journal of Oncology Practice · doi:10.1200/jop.2016.018382 · Cited by 42
Mechanisms of resistance to EGFR inhibitors in head and neck cancer
Cooper, J. B., & Cohen, E. E. W. (2009) · Head & Neck · doi:10.1002/hed.21109 · Cited by 39
“mCRC.(77) PTEN expression has also been associated with sensitivity to chemotherapeutics by indirectly suppressing the expression of bcl-2 (by decreasing PI3K/Akt signaling), an inhibitor of apoptosis.”
Background
Advances in the Treatment of Metastatic Colorectal Cancer
Kurkjian, C. D., & Kummar, S. (2009) · American Journal of Therapeutics · doi:10.1097/mjt.0b013e3181907ed9 · Cited by 41

Authors: Frattini, M., Saletti, P., Romagnani, E., Martin, V, Molinari, F., Ghisletta, M., Camponovo, A., Etienne, L. L., Cavalli, F., & Mazzucchelli, L.
Affiliations: Istituto Cantonale di Patologia (CH)
Ospedale San Giovanni Bellinzona (CH)
Corresponding author: Frattini, M
ORCID: Frattini, M
Cavalli, F
Venue: British Journal of Cancer
Publisher: Springer Science and Business Media LLC
Published: 2007-10
Volume: 97
Issue: 8
Pages: 1139-1145
ISSN: 0007-0920 (ISSN-L)
1532-1827
DOI: 10.1038/sj.bjc.6604009
PMC: PMC2360431
OpenAlex: W2100589633
Cited by: 540
References: 31
Citations by year: 2026: 3 · 2025: 3 · 2024: 9 · 2023: 7 · 2022: 8 · 2021: 14 · 2020: 16 · 2019: 14 · 2018: 9 · 2017: 15 · 2016: 20 · 2015: 30 · 2014: 38 · 2013: 38 · 2012: 63
FWCI: 33.57
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
www.springer.com/tdm (unspecified)
Locations: British Journal of Cancer (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Oncosuisse
Topics: Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Health Sciences › Medicine › Oncology › HER2/EGFR in Cancer Research
Keywords: PTEN loss, cetuximab, metastatic colorectal cancer, EGFR overexpression, EGFR amplification, KRAS mutation, chromosome 7 polysomy, drug response prediction, predictive biomarkers
MeSH terms: Cetuximab, Adult, Aged, Algorithms, Antibodies, Monoclonal, Antineoplastic Agents, Chromosomes, Human, Pair 7, Female, Gene Amplification, Humans, Immunohistochemistry, Male, Middle Aged, Proto-Oncogene Proteins, Biomarkers, Tumor, Colorectal Neoplasms, Gene Expression, Proto-Oncogene Proteins p21(ras), In Situ Hybridization, Fluorescence, ras Proteins, Drug Resistance, Neoplasm, PTEN Phosphohydrolase, Antibodies, Monoclonal, Humanized, ErbB Receptors

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PTEN loss of expression predicts cetuximab efficacy in metastatic colorectal cancer patients

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