Inhibition of DDR1‐BCR signalling by nilotinib as a new therapeutic strategy for metastatic colorectal cancer
The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models...
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| Vydáno v: | EMBO molecular medicine Ročník 10; číslo 4; s. 1 - n/a |
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| Médium: | Journal Article |
| Jazyk: | angličtina |
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London
Nature Publishing Group UK
01.04.2018
Wiley Open Access John Wiley and Sons Inc Springer Nature |
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| ISSN: | 1757-4676, 1757-4684, 1757-4684 |
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| Abstract | The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion
in vitro
and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS‐independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1‐mediated BCR phosphorylation on Tyr177, which is important for maintaining β‐catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient‐derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC.
Synopsis
The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC.
DDR1 tyrosine kinase activity promotes colorectal cancer cell invasion and metastatic properties in nude mice.
BCR is a central substrate of DDR1.
DDR1 activation maintains a high level of β‐catenin transcriptional activity necessary for cell invasion and metastatic progression.
DDR1 pharmacological inhibition by nilotinib inhibits colorectal cancer cell invasion and metastatic properties in nude mice.
Nilotinib may be of clinical interest for treatment of metastatic colorectal cancer.
Graphical Abstract
The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC. |
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| AbstractList | The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS‐independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1‐mediated BCR phosphorylation on Tyr177, which is important for maintaining β‐catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient‐derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS‐independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1‐mediated BCR phosphorylation on Tyr177, which is important for maintaining β‐catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient‐derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. Synopsis The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC. DDR1 tyrosine kinase activity promotes colorectal cancer cell invasion and metastatic properties in nude mice. BCR is a central substrate of DDR1. DDR1 activation maintains a high level of β‐catenin transcriptional activity necessary for cell invasion and metastatic progression. DDR1 pharmacological inhibition by nilotinib inhibits colorectal cancer cell invasion and metastatic properties in nude mice. Nilotinib may be of clinical interest for treatment of metastatic colorectal cancer. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS‐independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1‐mediated BCR phosphorylation on Tyr177, which is important for maintaining β‐catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient‐derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. Synopsis The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC. DDR1 tyrosine kinase activity promotes colorectal cancer cell invasion and metastatic properties in nude mice. BCR is a central substrate of DDR1. DDR1 activation maintains a high level of β‐catenin transcriptional activity necessary for cell invasion and metastatic progression. DDR1 pharmacological inhibition by nilotinib inhibits colorectal cancer cell invasion and metastatic properties in nude mice. Nilotinib may be of clinical interest for treatment of metastatic colorectal cancer. Graphical Abstract The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Targeting the receptor for collagens DDR1 by nilotinib inhibits mCRC cells properties and paves the way to a new therapeutic strategy for mCRC. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS-independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1-mediated BCR phosphorylation on Tyr177, which is important for maintaining β-catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient-derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS-independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1mediated BCR phosphorylation on Tyr177, which is important for maintaining b-catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient-derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. Abstract The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS‐independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1‐mediated BCR phosphorylation on Tyr177, which is important for maintaining β‐catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient‐derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS-independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1-mediated BCR phosphorylation on Tyr177, which is important for maintaining β-catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient-derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC.The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic myeloid leukaemia, strongly inhibits human CRC cell invasion in vitro and reduces their metastatic potential in intrasplenic tumour mouse models. Nilotinib acts by inhibiting the kinase activity of DDR1, a receptor tyrosine kinase for collagens, which we identified as a RAS-independent inducer of CRC metastasis. Using quantitative phosphoproteomics, we identified BCR as a new DDR1 substrate and demonstrated that nilotinib prevents DDR1-mediated BCR phosphorylation on Tyr177, which is important for maintaining β-catenin transcriptional activity necessary for tumour cell invasion. DDR1 kinase inhibition also reduced the invasion of patient-derived metastatic and circulating CRC cell lines. Collectively, our results indicate that the targeting DDR1 kinase activity with nilotinib may be beneficial for patients with mCRC. |
| Author | Martineau, Pierre Canterel‐Thouennon, Lucile Otandault, Amaëlle Tosti, Priscillia Roche, Serge El Messaoudi, Safia Grillet, Fanny Mollevi, Caroline Le Guet, Jordy Leroy, Cédric Lafitte, Marie Busson, Muriel Thierry, Alain R Simon, Valérie Pannequin, Julie Robert, Bruno Sirvent, Audrey Jeitany, Maya Bonenfant, Debora |
| AuthorAffiliation | 5 IGF CNRS INSERM University Montpellier Montpellier France 2 Novartis Institutes for Biomedical Research, Postfach Basel Switzerland 4 IRCM INSERM University Montpellier Montpellier France 3 Actelion Pharmaceuticals Ltd Allschwil Switzerland 1 CRBM CNRS University Montpellier Montpellier France |
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| Keywords | targeted therapy colorectal cancer invasion collagen receptor tyrosine kinase Digestive System Pharmacology & Drug Discovery tyrosine kinase Subject Categories Cancer |
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| Publisher | Nature Publishing Group UK Wiley Open Access John Wiley and Sons Inc Springer Nature |
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SgK269/PEAK1 in a basal breast cancer signaling pathway publication-title: Cancer Res – volume: 7 start-page: 10765 year: 2016 article-title: TOM1L1 drives membrane delivery of MT1‐MMP to promote ERBB2‐induced breast cancer cell invasion publication-title: Nat Commun – volume: 17 start-page: 867 year: 2011 end-page: 874 article-title: Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs publication-title: Nat Med – volume: 21 start-page: 1350 year: 2015 end-page: 1356 article-title: The consensus molecular subtypes of colorectal cancer publication-title: Nat Med – volume: 7 start-page: 55 year: 2016 article-title: Discoidin domain receptors: potential actors and targets in cancer publication-title: Front Pharm – volume: 29 start-page: 1303 year: 2010 end-page: 1315 article-title: Src family tyrosine kinases‐driven colon cancer cell invasion is induced by Csk membrane delocalization publication-title: Oncogene – volume: 499 start-page: 166 year: 2013 end-page: 171 article-title: Temporal regulation of EGF signalling networks by the scaffold protein Shc1 publication-title: Nature – volume: 66 start-page: 3992 year: 2006 end-page: 3995 article-title: KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer publication-title: Cancer Res – volume: 23 start-page: 94 year: 2005 end-page: 101 article-title: Immunoaffinity profiling of tyrosine phosphorylation in cancer cells publication-title: Nat Biotechnol – volume: 76 start-page: 68 year: 2017 end-page: 75 article-title: Molecular subtypes of metastatic colorectal cancer are associated with patient response to irinotecan‐based therapies publication-title: Eur J Cancer – volume: 166 start-page: 47 year: 2016 end-page: 62 article-title: Multi‐organ site metastatic reactivation mediated by non‐canonical discoidin domain receptor 1 signaling publication-title: Cell – volume: 210 start-page: 1331 year: 2013 end-page: 1350 article-title: AP4 is a mediator of epithelial‐mesenchymal transition and metastasis in colorectal cancer publication-title: J Exp Med – volume: 59 start-page: 2163 year: 2014 end-page: 2172 article-title: MiR‐199a‐5p loss up‐regulated DDR1 aggravated colorectal cancer by activating epithelial‐to‐mesenchymal transition related signaling publication-title: Dig Dis Sci – volume: 17 start-page: 79 year: 2017 end-page: 92 article-title: Consensus molecular subtypes and the evolution of precision medicine in colorectal cancer publication-title: Nat Rev Can – volume: 110 start-page: 4055 year: 2007 end-page: 4063 article-title: Chemical proteomic profiles of the BCR‐ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets publication-title: Blood – volume: 66 start-page: 1802 year: 2017 end-page: 1810 article-title: Circulating tumour cells from patients with colorectal cancer have cancer stem cell hallmarks in culture publication-title: Gut – volume: 4 start-page: 1269 year: 2014 end-page: 1280 article-title: Resistance to anti‐EGFR therapy in colorectal cancer: from heterogeneity to convergent evolution publication-title: Cancer Discov – volume: 207 start-page: 517 year: 2014 end-page: 533 article-title: Discoidin domain receptor 1 controls linear invadosome formation via a Cdc42‐Tuba pathway publication-title: J Cell Biol – volume: 14 start-page: 1169 year: 2016 end-page: 1180 article-title: Tead and AP1 coordinate transcription and motility publication-title: Cell Rep – volume: 6 start-page: 1095 year: 2005 end-page: 1100 article-title: Bcr is a negative regulator of the Wnt signalling pathway publication-title: EMBO Rep – volume: 19 start-page: 125 year: 2011 end-page: 137 article-title: Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling publication-title: Cancer Cell – volume: 7 start-page: 345 year: 2007 end-page: 356 article-title: Second generation inhibitors of BCR‐ABL for the treatment of imatinib‐resistant chronic myeloid leukaemia publication-title: Nat Rev Cancer – volume: 18 start-page: 1774 year: 2017 end-page: 1790 article-title: Discoidin domain receptor 1 mediates myosin‐dependent collagen contraction publication-title: Cell Rep – volume: 344 start-page: 1031 year: 2001 end-page: 1037 article-title: Efficacy and safety of a specific inhibitor of the BCR‐ABL tyrosine kinase in chronic myeloid leukemia publication-title: N Engl J Med – volume: 15 start-page: 232 year: 2015 end-page: 244 article-title: Contribution of phosphoproteomics in understanding SRC signaling in normal and tumor cells publication-title: Proteomics – volume: 310 start-page: 39 year: 2014 end-page: 87 article-title: Discoidin domain receptor functions in physiological and pathological conditions publication-title: Int Rev Cell Mol Biol – volume: 26 start-page: 374 year: 2008 end-page: 379 article-title: KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab publication-title: J Clin Oncol – volume: 25 start-page: 773 year: 2007 end-page: 780 article-title: Gene expression signature in advanced colorectal cancer patients select drugs and response for the use of leucovorin, fluorouracil, and irinotecan publication-title: J Clin Oncol – volume: 24 start-page: 410 year: 2013 end-page: 421 article-title: Origins of metastatic traits publication-title: Cancer Cell – volume: 7 start-page: 281ra244 year: 2015 article-title: An EphB‐Abl signaling pathway is associated with intestinal tumor initiation and growth publication-title: Sci Transl Med – volume: 1 start-page: 13 year: 1997 end-page: 23 article-title: The discoidin domain receptor tyrosine kinases are activated by collagen publication-title: Mol Cell – volume: 5 start-page: 198 year: 2015 end-page: 211 article-title: Promotion of colorectal cancer invasion and metastasis through activation of NOTCH‐DAB1‐ABL‐RHOGEF protein TRIO publication-title: Cancer Discov – volume: 107 start-page: 10920 year: 2010 end-page: 10925 article-title: Pseudopodium‐enriched atypical kinase 1 regulates the cytoskeleton and cancer progression publication-title: Proc Natl Acad Sci USA – volume: 7 start-page: 129 year: 2005 end-page: 141 article-title: Characterization of AMN107, a selective inhibitor of native and mutant Bcr‐Abl publication-title: Cancer Cell – volume: 96 start-page: 3343 year: 2000 end-page: 3356 article-title: The molecular biology of chronic myeloid leukemia publication-title: Blood – volume: 6 start-page: 319 year: 2013 end-page: 328 article-title: Circulating cell‐free DNA from colorectal cancer patients may reveal high KRAS or BRAF mutation load publication-title: Transl Oncol – volume: 18 start-page: 969 year: 2012 end-page: 980 article-title: Inhibition of collagen receptor discoidin domain receptor‐1 (DDR1) reduces cell survival, homing, and colonization in lung cancer bone metastasis publication-title: Clin Can Res – volume: 22 start-page: 270 year: 2016 end-page: 277 article-title: Combined inhibition of DDR1 and Notch signaling is a therapeutic strategy for KRAS‐driven lung adenocarcinoma publication-title: Nat Med – volume: 20 start-page: 430 year: 2014 end-page: 435 article-title: Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA publication-title: Nat Med – volume: 185 start-page: 399 year: 2015 end-page: 408 article-title: mTOR and PDGF pathway blockade inhibits liver metastasis of colorectal cancer by modulating the tumor microenvironment publication-title: Am J Pathol – volume: 2 start-page: 357 year: 2012 end-page: 371 article-title: Oncogenic signaling by tyrosine kinases of the SRC family in advanced colorectal cancer publication-title: Am J Can Res |
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| Snippet | The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for chronic... Abstract The clinical management of metastatic colorectal cancer (mCRC) faces major challenges. Here, we show that nilotinib, a clinically approved drug for... |
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| SubjectTerms | Animals Cellular Biology collagen receptor colorectal cancer Colorectal Neoplasms - metabolism Colorectal Neoplasms - pathology Discoidin Domain Receptor 1 - genetics Discoidin Domain Receptor 1 - metabolism EMBO03 EMBO12 EMBO28 HCT116 Cells HEK293 Cells Humans invasion Life Sciences Mice Phosphoproteins - metabolism Protein-Tyrosine Kinases - genetics Protein-Tyrosine Kinases - metabolism Proto-Oncogene Proteins c-bcr - genetics Proto-Oncogene Proteins c-bcr - metabolism Pyrimidines - pharmacology Receptors, Collagen - genetics Receptors, Collagen - metabolism Research Article Signal Transduction - drug effects Signal Transduction - genetics targeted therapy tyrosine kinase |
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| Title | Inhibition of DDR1‐BCR signalling by nilotinib as a new therapeutic strategy for metastatic colorectal cancer |
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