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Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer

Bladder cancer is one of the most common and aggressive cancers and, regardless of the treatment, often recurs and metastasizes. Thus, a better understanding of the mechanisms regulating urothelial tumorigenesis is critical for the design and implementation of rational therapeutic strategies. We pre...

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Autores principales: Buraschi, Simone, Morcavallo, Alaide, Neill, Thomas, Stefanello, Manuela, Palladino, Chiara, Xu, Shi-Qiong, Belfiore, Antonino, Iozzo, Renato V., Morrione, Andrea
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7852334/
https://www.ncbi.nlm.nih.gov/pubmed/33543020
http://dx.doi.org/10.1016/j.mbplus.2020.100022
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author Buraschi, Simone
Morcavallo, Alaide
Neill, Thomas
Stefanello, Manuela
Palladino, Chiara
Xu, Shi-Qiong
Belfiore, Antonino
Iozzo, Renato V.
Morrione, Andrea
author_facet Buraschi, Simone
Morcavallo, Alaide
Neill, Thomas
Stefanello, Manuela
Palladino, Chiara
Xu, Shi-Qiong
Belfiore, Antonino
Iozzo, Renato V.
Morrione, Andrea
author_sort Buraschi, Simone
collection PubMed
description Bladder cancer is one of the most common and aggressive cancers and, regardless of the treatment, often recurs and metastasizes. Thus, a better understanding of the mechanisms regulating urothelial tumorigenesis is critical for the design and implementation of rational therapeutic strategies. We previously discovered that the IGF-IR axis is critical for bladder cancer cell motility and invasion, suggesting a possible role in bladder cancer progression. However, IGF-IR depletion in metastatic bladder cancer cells only partially inhibited anchorage-independent growth. Significantly, metastatic bladder cancer cells have decreased IGF-IR levels but overexpressed the insulin receptor isoform A (IR-A), suggesting that the latter may play a more prevalent role than the IGF-IR in bladder tumor progression. The collagen receptor DDR1 cross-talks with both the IGF-IR and IR in breast cancer, and previous data suggest a role of DDR1 in bladder cancer. Here, we show that DDR1 is expressed in invasive and metastatic, but not in papillary, non-invasive bladder cancer cells. DDR1 is phosphorylated upon stimulation with IGF-I, IGF-II, and insulin, co-precipitates with the IGF-IR, and the IR-A and transient DDR1 depletion severely inhibits IGF-I-induced motility. We further demonstrate that DDR1 interacts with Pyk2 and non-muscle myosin IIA in ligands-dependent fashion, suggesting that it may link the IGF-IR and IR-A to the regulation of F-actin cytoskeleton dynamics. Similarly to the IGF-IR, DDR1 is upregulated in bladder cancer tissues compared to healthy tissue controls. Thus, our findings provide the first characterization of the molecular cross-talk between DDR1 and the IGF-I system and could lead to the identification of novel targets for therapeutic intervention in bladder cancer. Moreover, the expression profiles of IGF-IR, IR-A, DDR1, and downstream effectors could serve as a novel biomarker signature with diagnostic and prognostic significance.
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spelling pubmed-78523342021-02-03 Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer Buraschi, Simone Morcavallo, Alaide Neill, Thomas Stefanello, Manuela Palladino, Chiara Xu, Shi-Qiong Belfiore, Antonino Iozzo, Renato V. Morrione, Andrea Matrix Biol Plus Article Bladder cancer is one of the most common and aggressive cancers and, regardless of the treatment, often recurs and metastasizes. Thus, a better understanding of the mechanisms regulating urothelial tumorigenesis is critical for the design and implementation of rational therapeutic strategies. We previously discovered that the IGF-IR axis is critical for bladder cancer cell motility and invasion, suggesting a possible role in bladder cancer progression. However, IGF-IR depletion in metastatic bladder cancer cells only partially inhibited anchorage-independent growth. Significantly, metastatic bladder cancer cells have decreased IGF-IR levels but overexpressed the insulin receptor isoform A (IR-A), suggesting that the latter may play a more prevalent role than the IGF-IR in bladder tumor progression. The collagen receptor DDR1 cross-talks with both the IGF-IR and IR in breast cancer, and previous data suggest a role of DDR1 in bladder cancer. Here, we show that DDR1 is expressed in invasive and metastatic, but not in papillary, non-invasive bladder cancer cells. DDR1 is phosphorylated upon stimulation with IGF-I, IGF-II, and insulin, co-precipitates with the IGF-IR, and the IR-A and transient DDR1 depletion severely inhibits IGF-I-induced motility. We further demonstrate that DDR1 interacts with Pyk2 and non-muscle myosin IIA in ligands-dependent fashion, suggesting that it may link the IGF-IR and IR-A to the regulation of F-actin cytoskeleton dynamics. Similarly to the IGF-IR, DDR1 is upregulated in bladder cancer tissues compared to healthy tissue controls. Thus, our findings provide the first characterization of the molecular cross-talk between DDR1 and the IGF-I system and could lead to the identification of novel targets for therapeutic intervention in bladder cancer. Moreover, the expression profiles of IGF-IR, IR-A, DDR1, and downstream effectors could serve as a novel biomarker signature with diagnostic and prognostic significance. Elsevier 2020-01-17 /pmc/articles/PMC7852334/ /pubmed/33543020 http://dx.doi.org/10.1016/j.mbplus.2020.100022 Text en © 2020 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Buraschi, Simone
Morcavallo, Alaide
Neill, Thomas
Stefanello, Manuela
Palladino, Chiara
Xu, Shi-Qiong
Belfiore, Antonino
Iozzo, Renato V.
Morrione, Andrea
Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title_full Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title_fullStr Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title_full_unstemmed Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title_short Discoidin Domain Receptor 1 functionally interacts with the IGF-I system in bladder cancer
title_sort discoidin domain receptor 1 functionally interacts with the igf-i system in bladder cancer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7852334/
https://www.ncbi.nlm.nih.gov/pubmed/33543020
http://dx.doi.org/10.1016/j.mbplus.2020.100022
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