Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR

Inhibition of activated BRAF has been ineffective in colon cancers with the mutation; here, this is shown to be due to the feedback activation of the epidermal growth factor receptor (EGFR) in response to BRAF inhibition. Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (...

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Vydáno v:Nature (London) Ročník 483; číslo 7387; s. 100 - 103
Hlavní autoři: Prahallad, Anirudh, Sun, Chong, Huang, Sidong, Di Nicolantonio, Federica, Salazar, Ramon, Zecchin, Davide, Beijersbergen, Roderick L., Bardelli, Alberto, Bernards, René
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 01.03.2012
Nature Publishing Group
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ISSN:0028-0836, 1476-4687, 1476-4687
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Abstract Inhibition of activated BRAF has been ineffective in colon cancers with the mutation; here, this is shown to be due to the feedback activation of the epidermal growth factor receptor (EGFR) in response to BRAF inhibition. Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma 1 . However, colon cancer patients harbouring the same BRAF ( V600E ) oncogenic lesion have poor prognosis and show only a very limited response to this drug 2 , 3 , 4 . To investigate the cause of the limited therapeutic effect of PLX4032 in BRAF ( V600E ) mutant colon tumours, here we performed an RNA-interference-based genetic screen in human cells to search for kinases whose knockdown synergizes with BRAF(V600E) inhibition. We report that blockade of the epidermal growth factor receptor (EGFR) shows strong synergy with BRAF(V600E) inhibition. We find in multiple BRAF ( V600E ) mutant colon cancers that inhibition of EGFR by the antibody drug cetuximab or the small-molecule drugs gefitinib or erlotinib is strongly synergistic with BRAF(V600E) inhibition, both in vitro and in vivo . Mechanistically, we find that BRAF(V600E) inhibition causes a rapid feedback activation of EGFR, which supports continued proliferation in the presence of BRAF(V600E) inhibition. Melanoma cells express low levels of EGFR and are therefore not subject to this feedback activation. Consistent with this, we find that ectopic expression of EGFR in melanoma cells is sufficient to cause resistance to PLX4032. Our data suggest that BRAF ( V600E ) mutant colon cancers (approximately 8–10% of all colon cancers 2 , 3 , 5 ), for which there are currently no targeted treatment options available, might benefit from combination therapy consisting of BRAF and EGFR inhibitors.
AbstractList Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma. However, colon cancer patients harbouring the same BRAF(V600E) oncogenic lesion have poor prognosis and show only a very limited response to this drug. To investigate the cause of the limited therapeutic effect of PLX4032 in BRAF(V600E) mutant colon tumours, here we performed an RNA-interference-based genetic screen in human cells to search for kinases whose knockdown synergizes with BRAF(V600E) inhibition. We report that blockade of the epidermal growth factor receptor (EGFR) shows strong synergy with BRAF(V600E) inhibition. We find in multiple BRAF(V600E) mutant colon cancers that inhibition of EGFR by the antibody drug cetuximab or the small-molecule drugs gefitinib or erlotinib is strongly synergistic with BRAF(V600E) inhibition, both in vitro and in vivo. Mechanistically, we find that BRAF(V600E) inhibition causes a rapid feedback activation of EGFR, which supports continued proliferation in the presence of BRAF(V600E) inhibition. Melanoma cells express low levels of EGFR and are therefore not subject to this feedback activation. Consistent with this, we find that ectopic expression of EGFR in melanoma cells is sufficient to cause resistance to PLX4032. Our data suggest that BRAF(V600E) mutant colon cancers (approximately 8-10% of all colon cancers), for which there are currently no targeted treatment options available, might benefit from combination therapy consisting of BRAF and EGFR inhibitors.Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma. However, colon cancer patients harbouring the same BRAF(V600E) oncogenic lesion have poor prognosis and show only a very limited response to this drug. To investigate the cause of the limited therapeutic effect of PLX4032 in BRAF(V600E) mutant colon tumours, here we performed an RNA-interference-based genetic screen in human cells to search for kinases whose knockdown synergizes with BRAF(V600E) inhibition. We report that blockade of the epidermal growth factor receptor (EGFR) shows strong synergy with BRAF(V600E) inhibition. We find in multiple BRAF(V600E) mutant colon cancers that inhibition of EGFR by the antibody drug cetuximab or the small-molecule drugs gefitinib or erlotinib is strongly synergistic with BRAF(V600E) inhibition, both in vitro and in vivo. Mechanistically, we find that BRAF(V600E) inhibition causes a rapid feedback activation of EGFR, which supports continued proliferation in the presence of BRAF(V600E) inhibition. Melanoma cells express low levels of EGFR and are therefore not subject to this feedback activation. Consistent with this, we find that ectopic expression of EGFR in melanoma cells is sufficient to cause resistance to PLX4032. Our data suggest that BRAF(V600E) mutant colon cancers (approximately 8-10% of all colon cancers), for which there are currently no targeted treatment options available, might benefit from combination therapy consisting of BRAF and EGFR inhibitors.
[...] Cdc25A can bind to and dephosphorylate EGFR16. [...] treatment of WiDr cells with PLX4032 inhibited phosphorylation ofCDC25C at Thr 48 (Fig. 2f), which has been shown to be required for its phosphatase activity15.\n At first glance, it would seem counterintuitive to consider treating a BRAF mutant colon cancer with an EGFR inhibitor, as multiple clinical studies in colon cancer have shown that EGFR inhibition is without clinical benefit when either KRAS or BRAF is mutated downstream of EGFR7,13,14.
Inhibition of activated BRAF has been ineffective in colon cancers with the mutation; here, this is shown to be due to the feedback activation of the epidermal growth factor receptor (EGFR) in response to BRAF inhibition. Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma 1 . However, colon cancer patients harbouring the same BRAF ( V600E ) oncogenic lesion have poor prognosis and show only a very limited response to this drug 2 , 3 , 4 . To investigate the cause of the limited therapeutic effect of PLX4032 in BRAF ( V600E ) mutant colon tumours, here we performed an RNA-interference-based genetic screen in human cells to search for kinases whose knockdown synergizes with BRAF(V600E) inhibition. We report that blockade of the epidermal growth factor receptor (EGFR) shows strong synergy with BRAF(V600E) inhibition. We find in multiple BRAF ( V600E ) mutant colon cancers that inhibition of EGFR by the antibody drug cetuximab or the small-molecule drugs gefitinib or erlotinib is strongly synergistic with BRAF(V600E) inhibition, both in vitro and in vivo . Mechanistically, we find that BRAF(V600E) inhibition causes a rapid feedback activation of EGFR, which supports continued proliferation in the presence of BRAF(V600E) inhibition. Melanoma cells express low levels of EGFR and are therefore not subject to this feedback activation. Consistent with this, we find that ectopic expression of EGFR in melanoma cells is sufficient to cause resistance to PLX4032. Our data suggest that BRAF ( V600E ) mutant colon cancers (approximately 8–10% of all colon cancers 2 , 3 , 5 ), for which there are currently no targeted treatment options available, might benefit from combination therapy consisting of BRAF and EGFR inhibitors.
Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma. However, colon cancer patients harbouring the same BRAF(V600E) oncogenic lesion have poor prognosis and show only a very limited response to this drug. To investigate the cause of the limited therapeutic effect of PLX4032 in BRAF(V600E) mutant colon tumours, here we performed an RNA-interference-based genetic screen in human cells to search for kinases whose knockdown synergizes with BRAF(V600E) inhibition. We report that blockade of the epidermal growth factor receptor (EGFR) shows strong synergy with BRAF(V600E) inhibition. We find in multiple BRAF(V600E) mutant colon cancers that inhibition of EGFR by the antibody drug cetuximab or the small-molecule drugs gefitinib or erlotinib is strongly synergistic with BRAF(V600E) inhibition, both in vitro and in vivo. Mechanistically, we find that BRAF(V600E) inhibition causes a rapid feedback activation of EGFR, which supports continued proliferation in the presence of BRAF(V600E) inhibition. Melanoma cells express low levels of EGFR and are therefore not subject to this feedback activation. Consistent with this, we find that ectopic expression of EGFR in melanoma cells is sufficient to cause resistance to PLX4032. Our data suggest that BRAF(V600E) mutant colon cancers (approximately 8-10% of all colon cancers), for which there are currently no targeted treatment options available, might benefit from combination therapy consisting of BRAF and EGFR inhibitors.
Author Di Nicolantonio, Federica
Bardelli, Alberto
Zecchin, Davide
Beijersbergen, Roderick L.
Sun, Chong
Huang, Sidong
Salazar, Ramon
Prahallad, Anirudh
Bernards, René
Author_xml – sequence: 1
  givenname: Anirudh
  surname: Prahallad
  fullname: Prahallad, Anirudh
  organization: Division of Molecular Carcinogenesis, Center for Biomedical Genetics and Cancer Genomics Centre, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
– sequence: 2
  givenname: Chong
  surname: Sun
  fullname: Sun, Chong
  organization: Division of Molecular Carcinogenesis, Center for Biomedical Genetics and Cancer Genomics Centre, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
– sequence: 3
  givenname: Sidong
  surname: Huang
  fullname: Huang, Sidong
  organization: Division of Molecular Carcinogenesis, Center for Biomedical Genetics and Cancer Genomics Centre, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
– sequence: 4
  givenname: Federica
  surname: Di Nicolantonio
  fullname: Di Nicolantonio, Federica
  organization: Laboratory of Molecular Genetics, Institute for Cancer Research and Treatment, University of Torino, Medical School, Str prov 142 Km 3.95, 10060 Candiolo, Torino, Italy, FIRC-IFOM Institute for Molecular Oncology, Via Adamello 16, 20100 Milan, Italy
– sequence: 5
  givenname: Ramon
  surname: Salazar
  fullname: Salazar, Ramon
  organization: IDIBELL, Institut Català d’Oncologia L’Hospitalet de Llobregat, Gran Via s/n, km 2, 7 08907 L’Hospitalet-Barcelona, Spain
– sequence: 6
  givenname: Davide
  surname: Zecchin
  fullname: Zecchin, Davide
  organization: Laboratory of Molecular Genetics, Institute for Cancer Research and Treatment, University of Torino, Medical School, Str prov 142 Km 3.95, 10060 Candiolo, Torino, Italy
– sequence: 7
  givenname: Roderick L.
  surname: Beijersbergen
  fullname: Beijersbergen, Roderick L.
  organization: Division of Molecular Carcinogenesis, Center for Biomedical Genetics and Cancer Genomics Centre, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
– sequence: 8
  givenname: Alberto
  surname: Bardelli
  fullname: Bardelli, Alberto
  organization: Laboratory of Molecular Genetics, Institute for Cancer Research and Treatment, University of Torino, Medical School, Str prov 142 Km 3.95, 10060 Candiolo, Torino, Italy, FIRC-IFOM Institute for Molecular Oncology, Via Adamello 16, 20100 Milan, Italy
– sequence: 9
  givenname: René
  surname: Bernards
  fullname: Bernards, René
  email: r.bernards@nki.nl
  organization: Division of Molecular Carcinogenesis, Center for Biomedical Genetics and Cancer Genomics Centre, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
BackLink http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25539125$$DView record in Pascal Francis
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Keywords Antineoplastic agent
Epidermal growth factor receptor
BRAF Gene
Colon cancer
Cancerology
Established cell line
Genetics
Intestinal disease
Protooncogene
Human
Rodentia
Enzyme inhibitor
Malignant tumor
In vitro
Colonic disease
In vivo
Vertebrata
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Mammalia
Treatment
Mouse
Animal
C-Onc gene
Digestive diseases
Cancer
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Snippet Inhibition of activated BRAF has been ineffective in colon cancers with the mutation; here, this is shown to be due to the feedback activation of the epidermal...
Inhibition of the BRAF(V600E) oncoprotein by the small-molecule drug PLX4032 (vemurafenib) is highly effective in the treatment of melanoma. However, colon...
[...] Cdc25A can bind to and dephosphorylate EGFR16. [...] treatment of WiDr cells with PLX4032 inhibited phosphorylation ofCDC25C at Thr 48 (Fig. 2f), which...
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SubjectTerms 631/208/737
692/699/67/1504/1885/1393
692/700/565/1436
692/700/565/1436/1437
Animals
Antibodies, Monoclonal - pharmacology
Antibodies, Monoclonal, Humanized
Antineoplastic agents
Antineoplastic Agents - pharmacology
Antineoplastic Agents - therapeutic use
Apoptosis - drug effects
Biological and medical sciences
Cell Line, Tumor
Cell Proliferation - drug effects
Cetuximab
Chemotherapy
Colorectal Neoplasms - drug therapy
Colorectal Neoplasms - enzymology
Colorectal Neoplasms - genetics
Colorectal Neoplasms - pathology
Drug Resistance, Neoplasm - drug effects
Drug Synergism
Enzyme Activation - drug effects
Erlotinib Hydrochloride
Feedback, Physiological - drug effects
Female
Gastroenterology. Liver. Pancreas. Abdomen
HEK293 Cells
Humanities and Social Sciences
Humans
Indoles - pharmacology
Indoles - therapeutic use
Kinases
letter
Library collections
Medical sciences
Melanoma - drug therapy
Melanoma - metabolism
Mice
multidisciplinary
Pharmacology. Drug treatments
Phosphorylation
Protein Kinase Inhibitors - pharmacology
Protein Kinase Inhibitors - therapeutic use
Proteins
Proto-Oncogene Proteins B-raf - antagonists & inhibitors
Proto-Oncogene Proteins B-raf - chemistry
Proto-Oncogene Proteins B-raf - genetics
Proto-Oncogene Proteins B-raf - metabolism
Quinazolines - pharmacology
Quinazolines - therapeutic use
Receptor, Epidermal Growth Factor - agonists
Receptor, Epidermal Growth Factor - antagonists & inhibitors
Receptor, Epidermal Growth Factor - metabolism
RNA Interference
Science
Science (multidisciplinary)
Stomach. Duodenum. Small intestine. Colon. Rectum. Anus
Studies
Sulfonamides - pharmacology
Sulfonamides - therapeutic use
Tumors
Xenograft Model Antitumor Assays
Title Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR
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