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Inhibition of Discoidin Domain Receptor 1 Reduces Collagen-mediated Tumorigenicity in Pancreatic Ductal Adenocarcinoma
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Abstract
The extracellular matrix (ECM), a principal component of pancreatic ductal adenocarcinoma (PDA), is rich in fibrillar collagens that facilitate tumor cell survival and chemoresistance. Discoidin domain receptor 1 (DDR1) is a receptor tyrosine kinase that specifically binds fibrillar collagens and has been implicated in promoting cell proliferation, migration, adhesion, ECM remodeling, and response to growth factors. We found that collagen-induced activation of DDR1 stimulated protumorigenic signaling through protein tyrosine kinase 2 (PYK2) and pseudopodium-enriched atypical kinase 1 (PEAK1) in pancreatic cancer cells. Pharmacologic inhibition of DDR1 with an ATP-competitive orally available small-molecule kinase inhibitor (7rh) abrogated collagen-induced DDR1 signaling in pancreatic tumor cells and consequently reduced colony formation and migration. Furthermore, the inhibition of DDR1 with 7rh showed striking efficacy in combination with chemotherapy in orthotopic xenografts and autochthonous pancreatic tumors where it significantly reduced DDR1 activation and downstream signaling, reduced primary tumor burden, and improved chemoresponse. These data demonstrate that targeting collagen signaling in conjunction with conventional cytotoxic chemotherapy has the potential to improve outcome for pancreatic cancer patients. Mol Cancer Ther; 16(11); 2473–85. ©2017 AACR.
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PDAC cells produce low tonic levels of a distinct oncogenic homo-trimeric collagen that binds α3β1 integrin, mediating immune suppression and reprogramming the tumor-associated microbiome.
“PDAC cells produce “tonic” (low) levels of a distinct oncogenic homo-trimeric collagen that binds to α3β1 integrin, thereby mediating immune suppression and reprogramming the tumor-associated microbiome167”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [167]
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Metadata
- Authors
- Aguilera, K. Y., Huang, H., Du, W., Hagopian, M. M., Wang, Z., Hinz, S., Hwang, T. H., Wang, H., Fleming, J. B., Castrillon, D. H., Ren, X., Ding, K., & Brekken, R. A.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Jinan University (CN)
- The University of Texas MD Anderson Cancer Center (US)
- 6Department of Clinical Science, UT Southwestern Medical Center, Dallas, Texas.
- Corresponding author
- Brekken, Rolf A.
- ORCID
- Venue
- Molecular Cancer Therapeutics
- Published
- 2017-11-01
- Volume
- 16
- Issue
- 11
- Pages
- 2473-2485
- ISSN
- 1535-7163 (ISSN-L)
- 1538-8514
- PMC
- PMC5669827
- OpenAlex
- W2751614779
- Cited by
- 118
- References
- 61
- Citations by year
- 2026: 6 · 2025: 12 · 2024: 17 · 2023: 12 · 2022: 15 · 2021: 16 · 2020: 15 · 2019: 15 · 2018: 9 · 2017: 1
- FWCI
- 4.82
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Molecular Cancer Therapeutics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (R01CA118240, U54 CA210181, F31 CA168350)
- CPRIT (RP160211)
- National Science Fund (#81425021)
- Guangdong province (#2016A050502041)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- DDR1, pancreatic ductal adenocarcinoma, collagen signaling, extracellular matrix, Pyk2, PEAK1, kinase inhibitors, chemosensitization, tumor cell migration, tumor cell proliferation, combination chemotherapy
- MeSH terms
- Discoidin Domain Receptor 1, Adenocarcinoma, Animals, Cell Adhesion, Cell Movement, Collagen, Humans, Protein-Tyrosine Kinases, Signal Transduction, Carcinoma, Pancreatic Ductal, Xenograft Model Antitumor Assays, Cell Proliferation, Mice, Focal Adhesion Kinase 1, Small Molecule Libraries, Carcinogenesis
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