Multitasking discoidin domain receptors are involved in several and specific hallmarks of cancer

References

• Hanahan D, Weinberg RA. The hallmarks of cancer. Cell [Internet]. 2000;100:57–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10647931. doi:10.1016/S0092-8674(00)81683-9.
   Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell [Internet]. 2011;144:646–74. doi:10.1016/j.cell.2011.02.013.
   Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med [Internet]. 2013;19:1423–37. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24202395. doi:10.1038/nm.3394.
   PubMed Web of Science ®Google Scholar
• Ramaswamy S, Ross KN, Lander ES, et al. A molecular signature of metastasis in primary solid tumors. Nat Genet [Internet]. 2003;33:49–54. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12469122. doi:10.1038/ng1060.
   PubMed Web of Science ®Google Scholar
• Levental KR, Yu H, Kass L, et al. Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling. Cell [Internet]. 2009;139:891–906. doi:10.1016/j.cell.2009.10.027.
   Google Scholar
• Alves F, Vogel W, Mossie K, et al. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene [Internet]. 1995;10:609–618. Available from: http://europepmc.org/abstract/MED/7845687
   PubMed Web of Science ®Google Scholar
• Leitinger B. Discoidin domain receptor functions in physiological and pathological conditions [Internet]. 1st ed. Elsevier Inc.; 2014. doi:10.1016/B978-0-12-800180-6.00002-5
   Google Scholar
• Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 2010;141:1117–34. doi:10.1016/j.cell.2010.06.011.
   PubMed Web of Science ®Google Scholar
• Noordeen NA, Carafoli F, Hohenester E, et al. A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1. J Biol Chem. 2006;281:22744–51. doi:10.1074/jbc.M603233200.
   PubMed Web of Science ®Google Scholar
• Mihai C, Chotani M, Elton TS, et al. Mapping of DDR1 Distribution and Oligomerization on the Cell Surface by FRET Microscopy. J Mol Biol [Internet]. 2009;385:432–45. doi:10.1016/j.jmb.2008.10.067.
   PubMed Web of Science ®Google Scholar
• Xu H, Abe T, Liu JKH, et al. Normal activation of discoidin domain receptor 1 mutants with disulfide cross-links, insertions, or deletions in the extracellular juxtamembrane region: Mechanistic implications. J Biol Chem. 2014;289:13565–74. doi:10.1074/jbc.M113.536144.
   PubMed Web of Science ®Google Scholar
• Carafoli F, Hohenester E. Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim Biophys Acta – Proteins Proteomics [Internet]. 2013;1834:2187–97. doi:10.1016/j.bbapap.2012.10.014.
   PubMed Web of Science ®Google Scholar
• Leitinger B. Transmembrane collagen receptors. Annu Rev Cell Dev Biol [Internet]. 2011;27:265–90. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21568710. doi:10.1146/annurev-cellbio-092910-154013.
   PubMed Web of Science ®Google Scholar
• Shrivastava A, Radziejewski C, Campbell E, et al. An Orphan Receptor Tyrosine Kinase Family Whose Members Serve as Nonintegrin Collagen Receptors. Mol Cell. 1997;1:25–34. doi:10.1016/S1097-2765(00)80004-0.
   PubMed Web of Science ®Google Scholar
• Vogel W, Gish GD, Alves F, et al. The Discoidin Domain Receptor Tyrosine Kinases Are Activated by Collagen. Mol Cell [Internet]. 1997;1:13–23. Available from: http://dx.doi.org/10.1016/S1097-2765(00)80003-9%5Cnhttp://www.sciencedirect.com/science/article/pii/S1097276500800039%5Cnhttp://www.sciencedirect.com/science?_ob=MImg&_imagekey=B6WSR-4194JBT-3-K&_cdi=7053&_user=9799020&_pii=S1097276500800039&_origin=&_cov. doi:10.1016/S1097-2765(00)80003-9.
   PubMed Web of Science ®Google Scholar
• Leitinger B. Molecular analysis of collagen binding by the human discoidin domain receptors, DDR1 and DDR2. Identification of collagen binding sites in DDR2. J Biol Chem. 2003;278:16761–9. doi:10.1074/jbc.M301370200.
   PubMed Web of Science ®Google Scholar
• Xu H, Raynal N, Stathopoulos S, et al. Collagen binding specificity of the discoidin domain receptors: Binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol [Internet]. 2011;30:16–26. doi:10.1016/j.matbio.2010.10.004.
   PubMed Web of Science ®Google Scholar
• Konitsiotis AD, Raynal N, Bihan D, et al. Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J Biol Chem. 2008;283:6861–8. doi:10.1074/jbc.M709290200.
   PubMed Web of Science ®Google Scholar
• Leitinger B, Steplewski A, Fertala A. The D2 period of collagen II contains a specific binding site for the human discoidin domain receptor, DDR2. J Mol Biol. 2004;344:993–1003. doi:10.1016/j.jmb.2004.09.089.
   PubMed Web of Science ®Google Scholar
• Leitinger B, Kwan APL. The discoidin domain receptor DDR2 is a receptor for type X collagen. Matrix Biol. 2006;25:355–64. doi:10.1016/j.matbio.2006.05.006.
   PubMed Web of Science ®Google Scholar
• Yang K, Kim JH, Kim HJ, et al. Tyrosine 740 phosphorylation of discoidin domain receptor 2 by Src stimulates intramolecular autophosphorylation and Shc signaling complex formation. J Biol Chem. 2005;280:39058–66. doi:10.1074/jbc.M506921200.
   PubMed Web of Science ®Google Scholar
• Lu KK, Trcka D, Bendeck MP. Collagen stimulates discoidin domain receptor 1-mediated migration of smooth muscle cells through Src. Cardiovasc Pathol [Internet]. 2011;20:71–6. doi:10.1016/j.carpath.2009.12.006.
   PubMed Web of Science ®Google Scholar
• Ikeda K, Wang LH, Torres R, et al. Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J Biol Chem. 2002;277:19206–12. doi:10.1074/jbc.M201078200.
   PubMed Web of Science ®Google Scholar
• Juskaite V, Corcoran DS, Leitinger B. Collagen induces activation of DDR1 through lateral dimer association and phosphorylation between dimers. Elife [Internet]. 2017;6:e25716. Available from: http://elifesciences.org/lookup/doi/10.7554/eLife.25716
   PubMed Web of Science ®Google Scholar
• Valiathan RR, Marco M, Leitinger B, et al. Discoidin domain receptor tyrosine kinases: New players in cancer progression. Cancer Metastasis Rev. 2012;31:295–321. doi:10.1007/s10555-012-9346-z.
   PubMed Web of Science ®Google Scholar
• Rammal H, Saby C, Magnien K, et al. Discoidin domain receptors: Potential actors and targets in cancer. Front Pharmacol. 2016;7:1–13.
   PubMed Web of Science ®Google Scholar
• Payne LS, Huang PH. Discoidin Domain Receptor 2 Signaling Networks and Therapy in Lung Cancer. J Thorac Oncol [Internet]. 2014;9:900–4. doi:10.1097/JTO.0000000000000164.
   PubMed Web of Science ®Google Scholar
• Coelho NM, Arora PD, van Putten S, et al. Discoidin Domain Receptor 1 Mediates Myosin-Dependent Collagen Contraction. Cell Rep [Internet]. 2017;18:1774–90. doi:10.1016/j.celrep.2017.01.061.
   PubMed Web of Science ®Google Scholar
• Juin A, Billottet C, Moreau V, et al. Physiological type I collagen organization induces the formation of a novel class of linear invadosomes. Mol Biol Cell [Internet]. 2012;23:297–309. doi:10.1091/mbc.E11-07-0594.
   PubMed Web of Science ®Google Scholar
• Juin A, Di Martino J, Leitinger B, et al. Discoidin domain receptor 1 controls linear invadosome formation via a Cdc42-Tuba pathway. J Cell Biol. 2014;207:517–33. doi:10.1083/jcb.201404079.
   PubMed Web of Science ®Google Scholar
• Hidalgo-Carcedo C, Hooper S, Chaudhry SI, et al. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat Cell Biol [Internet]. 2011;13:49–58. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3018349&tool = pmcentrez&rendertype = abstract. doi:10.1038/ncb2133.
   PubMed Web of Science ®Google Scholar
• Huang Y, Arora P, McCulloch CA, et al. The collagen receptor DDR1 regulates cell spreading and motility by associating with myosin IIA. J Cell Sci [Internet]. 2009;122:1637–46. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19401332%5Cnhttp://jcs.biologists.org/cgi/content/abstract/122/10/1637. doi:10.1242/jcs.046219.
   PubMed Web of Science ®Google Scholar
• Nemoto T, Ohashi K, Akashi T, et al. Overexpression of protein tyrosine kinases in human esophageal cancer. Pathobiology. 1997;65:195–203. doi:10.1159/000164123.
   PubMed Web of Science ®Google Scholar
• Xie R, Wang X, Qi G, et al. DDR1 enhances invasion and metastasis of gastric cancer via epithelial-mesenchymal transition. Tumor Biol [Internet]. 2016;37:12049–59. doi:10.1007/s13277-016-5070-6.
   Google Scholar
• Yamanaka R, Arao T, Yajima N, et al. Identification of expressed genes characterizing long-term survival in malignant glioma patients. Oncogene. 2006;25:5994–6002. doi:10.1038/sj.onc.1209585.
   PubMed Web of Science ®Google Scholar
• Malaguarnera R, Nicolosi ML, Sacco A, et al. Novel cross-talk between IGF-IR and DDR1 regulates IGF-IR trafficking, signaling and biological responses. Oncotarget. 2015;6:16084–105. doi:10.18632/oncotarget.3177.
   PubMedGoogle Scholar
• Xiao Q, Jiang Y, Liu Q, et al. Minor Type IV Collagen α 5 Chain Promotes Cancer Progression through Discoidin Domain Receptor-1. PLoS Genet. 2015;11:e1005249. doi:10.1371/journal.pgen.1005249.
   Web of Science ®Google Scholar
• Assent D, Bourgot I, Hennuy B, et al. A Membrane-Type-1 Matrix Metalloproteinase (MT1-MMP) – Discoidin Domain Receptor 1 Axis Regulates Collagen- Induced Apoptosis in Breast Cancer Cells. PLoS One. 2015;10:e0116006. doi:10.1371/journal.pone.0116006.
   PubMedGoogle Scholar
• Rudra-ganguly N, Lowe C, Mattie M, et al. Discoidin Domain Receptor 1 Contributes to Tumorigenesis through Modulation of TGFBI Expression. PLoS One. 2014;9:1–11. doi:10.1371/journal.pone.0111515.
   Web of Science ®Google Scholar
• Wang Z, Sun X, Bao Y, et al. E2F1 silencing inhibits migration and invasion of osteosarcoma cells via regulating DDR1 expression. Int J Oncol. 2017;51:1639–50. doi:10.3892/ijo.2017.4165.
   PubMed Web of Science ®Google Scholar
• Xie X, Rui W, He W, et al. Discoidin domain receptor 1 activity drives an aggressive phenotype in gastric carcinoma. Am J Transl Res [Internet]. 2017;9:2500–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28143619%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = PMC5286810%0Ahttp://bmccancer.biomedcentral.com/articles/10.1186/s12885-017-3051-9
   PubMed Web of Science ®Google Scholar
• Hammerman PS, Sos ML, Ramos AH, et al. Mutations in the DDR2 Kinase Gene identify a Novel therapeutic target in squamous cell lung cancer. Cancer Discov. 2011;1:78–89. doi:10.1158/2159-8274.CD-11-0005.
   PubMed Web of Science ®Google Scholar
• Azemikhah M, Ashtiani HA, Aghaei M, et al. Evaluation of discoidin domain receptor-2 (DDR2) expression level in normal, benign, and malignant human prostate tissues. Res Pharm Sci. 2015;10:356–63.
   PubMed Web of Science ®Google Scholar
• Badiola I, Villacé P, Basaldua I, et al. Downregulation of discoidin domain receptor 2 in A375 human melanoma cells reduces its experimental liver metastasis ability. Oncol Rep. 2011;26:971–8.
   PubMed Web of Science ®Google Scholar
• Saby C, Buache E, Brassart-Pasco S, et al. Type I collagen aging impairs discoidin domain receptor 2-mediated tumor cell growth suppression. Oncotarget [Internet]. 2016;7:24908–27. Available from: http://www.oncotarget.com/abstract/8795
   PubMedGoogle Scholar
• Iwai L., Payne L., Luczynski M., et al. Phosphoproteomics of collagen receptor networks reveals SHP-2 phosphorylation downstream of wild-type DDR2 and its lung cancer mutants. Biochem J. 2013;454:501–13. doi:10.1042/BJ20121750.
   PubMed Web of Science ®Google Scholar
• Wall SJ, Werner E, Werb Z, et al. Discoidin Domain Receptor 2 Mediates Tumor Cell Cycle Arrest Induced by Fibrillar Collagen. J Biol Chem. 2005;280:40187–94. doi:10.1074/jbc.M508226200.
   PubMed Web of Science ®Google Scholar
• Day E, Waters B, Spiegel K, et al. Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol [Internet]. 2008;599:44–53. doi:10.1016/j.ejphar.2008.10.014.
   PubMed Web of Science ®Google Scholar
• Davies H, Hunter C, Smith R, et al. Somatic mutations of the protein kinase gene family in human lung cancer. Cancer Res. 2005;65:7591–5. doi:10.1158/0008-5472.CAN-05-1855.
   PubMed Web of Science ®Google Scholar
• Ding L, Getz G, Wheeler DA, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature [Internet]. 2008;455:1069–75. doi:10.1038/nature07423.
   Google Scholar
• Loriaux MM, Levine RL, Tyner JW, et al. High-throughput sequence analysis of the tyrosine kinome in acute myeloid leukemia High-throughput sequence analysis of the tyrosine kinome in acute myeloid leukemia. Blood. 2008;111:4788–96. doi:10.1182/blood-2007-07-101394.
   PubMed Web of Science ®Google Scholar
• Rudd ML, Mohamed H, Price JC, et al. Mutational analysis of the tyrosine kinome in serous and clear cell endometrial cancer uncovers rare somatic mutations in TNK2 and DDR1. BMC Cancer [Internet]. 2014;14:884. Available from: http://bmccancer.biomedcentral.com/articles/10.1186/1471-2407-14-884. doi:10.1186/1471-2407-14-884.
   PubMed Web of Science ®Google Scholar
• Ongusaha PP, Kim J il, Fang L, et al. p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J. 2003;22:1289–301. doi:10.1093/emboj/cdg129.
   PubMed Web of Science ®Google Scholar
• Das S, Ongusaha PP, Yang YS, et al. Discoidin domain receptor 1 receptor tyrosine kinase induces cyclooxygenase-2 and promotes chemoresistance through nuclear factor-kappaB pathway activation. Cancer Res. 2006;66:8123–30. doi:10.1158/0008-5472.CAN-06-1215.
   PubMed Web of Science ®Google Scholar
• Cader FZ, Vockerodt M, Bose S, et al. The EBV oncogene LMP1 protects lymphoma cells from cell death through the collagen-mediated activation of DDR1. Blood. 2017;122:4237–46. doi:10.1182/blood-2013-04-499004.
   Google Scholar
• Deng Y, Zhao F, Hui L, et al. Suppressing miR-199a-3p by promoter methylation contributes to tumor aggressiveness and cisplatin resistance of ovarian cancer through promoting DDR1 expression. J Ovarian Res. 2017;1:1–11.
   Google Scholar
• Aljohani H, Koncar RF, Zarzour A, Park BS, Lee SH, Bahassi El M. ROS1 amplification mediates resistance to gefitinib in glioblastoma cells. Oncotarget. 2015;6:20388–95. doi:10.18632/oncotarget.3981.
   Google Scholar
• Ambrogio C, Gómez-López G, Falcone M, et al. Combined inhibition of DDR1 and Notch signaling is a therapeutic strategy for KRAS-driven lung adenocarcinoma. Nat Med. 2016;22:270–7. doi:10.1038/nm.4041.
   PubMed Web of Science ®Google Scholar
• Ambrogio C, Nadal E, Villanueva A, et al. KRAS-driven lung adenocarcinoma: combined DDR1/Notch inhibition as an effective therapy. ESMO Open [Internet]. 2016;1:e000076. doi:10.1136/esmoopen-2016-000076.
   PubMed Web of Science ®Google Scholar
• Beauchamp EM, Woods BA, Dulak AM, et al. Acquired Resistance to Dasatinib in Lung Cancer Cell Lines Conferred by DDR2 Gatekeeper Mutation and NF1 Loss. Mol Cancer Ther. 2014;13:475–83. doi:10.1158/1535-7163.MCT-13-0817.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Zitvogel L, Sautès–Fridman C, et al. The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol [Internet]. 2017;5–8. Available from: http://www.nature.com/doifinder/10.1038/nrclinonc.2017.101
   Web of Science ®Google Scholar
• Kamohara H, Yamashiro S, Galligan C, et al. Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J. 2001;15:2724–6. doi:10.1096/fj.01-0359fje.
   PubMed Web of Science ®Google Scholar
• Hachehouche LN, Chetoui N, Aoudjit F. Implication of discoidin domain receptor 1 in T cell migration in three-dimensional collagen. Mol Immunol [Internet]. 2010;47:1866–9. doi:10.1016/j.molimm.2010.02.023.
   PubMed Web of Science ®Google Scholar
• Chetoui N, El azreq M-A, Boisvert M, et al. Discoidin domain receptor 1 expression in activated T cells is regulated by the ERK MAP kinase signaling pathway. J Cell Biochem [Internet]. 2011;112:3666–74. doi:10.1002/jcb.23300.
   PubMed Web of Science ®Google Scholar
• Kadiri M, El Azreq M-A, Berrazouane S, et al. Human Th17 Migration in Three-Dimensional Collagen Involves p38 MAPK. J Cell Biochem. 2017;118:2819–27. doi:10.1002/jcb.25932.
   PubMed Web of Science ®Google Scholar
• El Azreq M, Kadiri M, Boisvert M, et al. Discoidin domain receptor 1 promotes Th17 cell migration by activating the RhoA / ROCK / MAPK / ERK signaling pathway. Oncotarget. 2016;7:44975–44990. doi:10.18632/oncotarget.10455.
   PubMedGoogle Scholar
• Afonso P V, Mccann CP, Kapnick SM, et al. Discoidin domain receptor 2 regulates neutrophil chemotaxis in 3D collagen matrices. Blood. 2013;121:1644–51. doi:10.1182/blood-2012-08-451575.
   PubMed Web of Science ®Google Scholar
• Lee Y, Moon W, Kim D. Discoidin domain receptor 2 is involved in the activation of bone marrow-derived dendritic cells caused by type I collagen. Biochem Biophys Res Commun. 2007;352:244–50. doi:10.1016/j.bbrc.2006.11.010.
   PubMed Web of Science ®Google Scholar
• Poudel B, Yoon D, Lee J, et al. Collagen I enhances functional activities of human monocyte-derived dendritic cells via discoidin domain receptor 2. Cell Immunol [Internet]. 2012;278:95–102. doi:10.1016/j.cellimm.2012.07.004.
   PubMed Web of Science ®Google Scholar
• Rafii S, Lyden D, Benezra R, et al. Vascular and haematopoietic stem cells: Novel targets for anti-angiogenesis therapy? Nat Rev Cancer. 2002;2:826–35. doi:10.1038/nrc925.
   PubMed Web of Science ®Google Scholar
• Seano G, Chiaverina G, Gagliardi PA, et al. Endothelial podosome rosettes regulate vascular branching in tumour angiogenesis. Nat Cell Biol. 2014;16:931–8. doi:10.1038/ncb3036.
   PubMed Web of Science ®Google Scholar
• Seano G, Daubon T, Génot E, et al. Podosomes as novel players in endothelial biology. Eur J Cell Biol [Internet]. 2014;93:405–12. doi:10.1016/j.ejcb.2014.07.009.
   PubMed Web of Science ®Google Scholar
• Tatin F, Varon C, Genot E, et al. A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci [Internet]. 2006;119:769–81. doi:10.1242/jcs.02787.
   PubMed Web of Science ®Google Scholar
• Hou G, Vogel W, Bendeck MP. The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest [Internet]. 2001;107:727–35. Available from: http://www.jci.org/articles/view/10720. doi:10.1172/JCI10720.
   PubMed Web of Science ®Google Scholar
• Zhang S, Bu X, Zhao H, et al. A host deficiency of discoidin domain receptor 2 (DDR2) inhibits both tumour angiogenesis and metastasis. J Pathol. 2014;232:436–48. doi:10.1002/path.4311.
   PubMed Web of Science ®Google Scholar
• Katanasaka Y, Asai T, Naitou H, et al. Proteomic Characterization of Angiogenic Endothelial Cells Stimulated with Cancer Cell-Conditioned Medium. Biol Pharm Bull. 2007;30:2300–7. doi:10.1248/bpb.30.2300.
   PubMed Web of Science ®Google Scholar
• Chen SC, Wang BW, Wang DL, et al. Hypoxia induces discoidin domain receptor-2 expression via the p38 pathway in vascular smooth muscle cells to increase their migration. Biochem Biophys Res Commun. 2008;374:662–7. doi:10.1016/j.bbrc.2008.07.092.
   PubMed Web of Science ®Google Scholar
• Zhu T, Zhu J, Bu X, et al. The anti-angiogenic role of discoidin domain receptor 2 (DDR2) in laser-induced choroidal neovascularization. J Mol Med. 2015;2:187–98. doi:10.1007/s00109-014-1213-7.
   Google Scholar
• Badiola I, Olaso E, Crende O, et al. Discoidin domain receptor 2 deficiency predisposes hepatic tissue to colon carcinoma metastasis. Gut. 2012;61:1465–72. doi:10.1136/gutjnl-2011-300810.
   PubMed Web of Science ®Google Scholar
• Augustin HG, Young Koh G, Thurston G, et al. Control of vascular morphogenesis and homeostasis through the angiopoietin – Tie system. Nat Rev Mol Cell Biol. 2009;10:165–77. doi:10.1038/nrm2639.
   PubMed Web of Science ®Google Scholar
• Olaso E, Labrador J-P, Wang L, et al. Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem [Internet]. 2002;277:3606–13. Available from: http://www.jbc.org/content/277/5/3606.long. doi:10.1074/jbc.M107571200.
   PubMed Web of Science ®Google Scholar
• Majkowska I, Shitomi Y, Ito N, et al. Discoidin domain receptor 2 mediates collagen-induced activation of membrane-type 1 matrix metalloproteinase in human fibroblasts. J Biol Chem. 2017;292:6633–43. doi:10.1074/jbc.M116.770057.
   PubMed Web of Science ®Google Scholar
• Yang SH, Baek HA, Lee HJ, et al. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung carcinomas SUN. Oncol Rep. 2010;24:311–9.
   PubMed Web of Science ®Google Scholar
• Valencia K, Ormazábal C, Zandueta C, et al. Inhibition of collagen receptor discoidin domain receptor-1 (DDR1) reduces cell survival, homing, and colonization in lung cancer bone metastasis. Clin Cancer Res. 2012;18:969–80. doi:10.1158/1078-0432.CCR-11-1686.
   PubMed Web of Science ®Google Scholar
• Barker KT, Martindale JE, Mitchell PJ, et al. Expression patterns of the novel receptor-like tyrosine kinase, DDR, in human breast tumours. Oncogene. 1995;10:569–75.
   PubMed Web of Science ®Google Scholar
• Shen Q, Cicinnati VR, Zhang X, et al. Role of microRNA-199a-5p and discoidin domain receptor 1 in human hepatocellular carcinoma invasion. Mol Cancer [Internet]. 2010;9:227. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 2939569&tool = pmcentrez&rendertype = abstract. doi:10.1186/1476-4598-9-227.
   PubMed Web of Science ®Google Scholar
• Shimada K, Nakamura M, Ishida E, et al. Prostate cancer antigen-1 contributes to cell survival and invasion though discoidin receptor 1 in human prostate cancer. Cancer Sci. 2008;99:39–45.
   PubMed Web of Science ®Google Scholar
• Gao H, Chakraborty G, Zhang Z, et al. Multi-organ Site Metastatic Reactivation Mediated by Non- canonical Discoidin Domain Receptor 1 Signaling. Cell. 2016;166:47–62. doi:10.1016/j.cell.2016.06.009.
   PubMed Web of Science ®Google Scholar
• Thiery JP, Acloque H, Huang RYJ, et al. Epithelial-Mesenchymal Transitions in Development and Disease. Cell. 2009;139:871–90. doi:10.1016/j.cell.2009.11.007.
   PubMed Web of Science ®Google Scholar
• Nieto MA. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol [Internet]. 2011;27:347–76. Available from: http://www.annualreviews.org/doi/pdf/10.1146/annurev-cellbio-092910-154036. doi:10.1146/annurev-cellbio-092910-154036.
   PubMed Web of Science ®Google Scholar
• Koh M, Woo Y, Valiathan RR, et al. Discoidin domain receptor 1 is a novel transcriptional target of ZEB1 in breast epithelial cells undergoing H-Ras-induced epithelial to mesenchymal transition. Int J Cancer. 2015;136:508–20. doi:10.1002/ijc.29154.
   PubMed Web of Science ®Google Scholar
• Taube JH, Herschkowitz JI, Komurov K, et al. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci [Internet]. 2010;107:15449–54. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1015095107%5Cnpapers2://publication/doi/10.1073/pnas.1015095107. doi:10.1073/pnas.1004900107.
   PubMed Web of Science ®Google Scholar
• Chung VY, Tan TZ, Huang R, et al. Loss of discoidin domain receptor 1 (DDR1) via CpG methylation during EMT in epithelial ovarian cancer. Gene [Internet]. 2017;635:9–15. doi:10.1016/j.gene.2017.09.001.
   Google Scholar
• Shintani Y, Fukumoto Y, Chaika N, et al. Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor. J Cell Biol. 2008;180:1277–89. doi:10.1083/jcb.200708137.
   PubMed Web of Science ®Google Scholar
• Song J, Chen X, Bai J, et al. Discoidin domain receptor 1 (DDR1), a promising biomarker, induces epithelial to mesenchymal transition in renal cancer cells. Tumor Biol [Internet]. 2016;37:11509–21. doi:10.1007/s13277-016-5021-2.
   PubMedGoogle Scholar
• Wang C, Yeh Y, Tang M-J. DDR1 / E-cadherin complex regulates the activation of DDR1 and cell spreading. Am J Physiol Cell Physiol [Internet]. 2009;297:419–29. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19474292. doi:10.1152/ajpcell.00101.2009.
   PubMed Web of Science ®Google Scholar
• Miao L, Zhu S, Wang Y, et al. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung cancer and promotes cell invasion via epithelial-to-mesenchymal transition. Med Oncol. 2013;30:626. doi:10.1007/s12032-013-0626-4.
   PubMed Web of Science ®Google Scholar
• Hu Y, Liu J, Jiang B, et al. MiR-199a-5p Loss Up-Regulated DDR1 Aggravated Colorectal Cancer by Activating Epithelial-to-Mesenchymal Transition Related Signaling. Dig Dis Sci. 2014;59:2163–72. doi:10.1007/s10620-014-3136-0.
   PubMed Web of Science ®Google Scholar
• Yoshida D, Teramoto A. Enhancement of pituitary adenoma cell invasion and adhesion is mediated by discoidin domain receptor-1. J Neurooncol. 2007;82:29–40. doi:10.1007/s11060-006-9246-6.
   PubMed Web of Science ®Google Scholar
• Park HS, Kim KR, Lee HJ, et al. Overexpression of discoidin domain receptor 1 increases the migration and invasion of hepatocellular carcinoma cells in association with matrix metalloproteinase. Oncol Rep. 2007;18:1435–41.
   PubMed Web of Science ®Google Scholar
• Hansen C, Greengard P, Nairn AC, et al. Phosphorylation of DARPP-32 regulates breast cancer cell migration downstream of the receptor tyrosine kinase DDR1. Exp Cell Res. 2006;312:4011–8. doi:10.1016/j.yexcr.2006.09.003.
   PubMed Web of Science ®Google Scholar
• Song S, Shackel NA, Wang XM, et al. Discoidin Domain Receptor 1. Am J Pathol [Internet]. 2011;178:1134–44. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0002944010002051. doi:10.1016/j.ajpath.2010.11.068.
   PubMed Web of Science ®Google Scholar
• Ezzoukhry Z, Henriet E, Piquet L, et al. TGF-β1 promotes linear invadosome formation in hepatocellular carcinoma cells, through DDR1 up-regulation and collagen I cross-linking. Eur J Cell Biol [Internet]. 2016;95:503–12. doi:10.1016/j.ejcb.2016.09.003.
   PubMed Web of Science ®Google Scholar
• Ram R, Lorente G, Nikolich K, et al. Discoidin domain receptor-1a (DDR1a) promotes glioma cell invasion and adhesion in association with matrix metalloproteinase-2. J Neurooncol. 2006;76:239–48. doi:10.1007/s11060-005-6874-1.
   PubMed Web of Science ®Google Scholar
• Huang H, Svoboda RA, Lazenby AJ, et al. Up-Regulation of N-Cadherin by Collagen I-activated discoidin domain receptor 1 in pancreatic cancer requires the adaptor molecule Shc. J Biol Chem. 2016;291:23208–23. doi:10.1074/jbc.M116.740605.
   PubMed Web of Science ®Google Scholar
• Xu J, Lu W, Zhang S, et al. Overexpression of DDR2 contributes to cell invasion and migration in head and neck squamous cell carcinoma. Cancer Biol Ther [Internet]. 2014;15:612–22. Available from: http://www.tandfonline.com/doi/abs/10.4161/cbt.28181. doi:10.4161/cbt.28181.
   PubMed Web of Science ®Google Scholar
• von Mässenhausen A, Sanders C, Brägelmann J, Konantz M, et al. Targeting DDR2 in head and neck squamous cell carcinoma with dasatinib. Int J Cancer. 2016;139:2359–69. doi:10.1002/ijc.30279.
   PubMed Web of Science ®Google Scholar
• Chua H, Yeh T, Wang Y, et al. Upregulation of discoidin domain receptor 2 in nasopharyngeal carcinoma. Head Neck. 2008;30:427–36.
   Web of Science ®Google Scholar
• Zhang K, Corsa CA, Ponik SM, et al. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat Cell Biol [Internet]. 2013;15:677–87. doi:10.1038/ncb2743.
   PubMed Web of Science ®Google Scholar
• Ren T, Zhang W, Liu X, et al. Discoidin domain receptor 2 (DDR2) promotes breast cancer cell metastasis and the mechanism implicates epithelial-mesenchymal transition programme under hypoxia. J Pathol. 2014;234:526–37. doi:10.1002/path.4415.
   PubMed Web of Science ®Google Scholar
• Toy KA, Valiathan RR, Núñez F, et al. Tyrosine kinase discoidin domain receptors DDR1 and DDR2 are coordinately deregulated in triple-negative breast cancer. Breast Cancer Res Treat. 2015;150:9–18. doi:10.1007/s10549-015-3285-7.
   PubMed Web of Science ®Google Scholar
• Park J-W, Lee Y-S, Kim JS, et al. Downregulation of discoidin domain receptor 2 decreases tumor growth of hepatocellular carcinoma. J Cancer Res Clin Oncol [Internet]. 2015;1973–83. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25842034. doi:10.1007/s00432-015-1967-5.
   PubMed Web of Science ®Google Scholar
• Xie B, Lin W, Ye J, et al. DDR2 facilitates hepatocellular carcinoma invasion and metastasis via activating ERK signaling and stabilizing SNAIL1. J Exp Clin cancer Res [Internet]. 2015;34:101. Available from: http://jeccr.biomedcentral.com/articles/10.1186/s13046-015-0218-6. doi:10.1186/s13046-015-0218-6.
   PubMed Web of Science ®Google Scholar
• Wang YG, Xu L, Jia RR, et al. DDR2 Induces Gastric Cancer Cell Activities via Activating mTORC2 Signaling and Is Associated with Clinicopathological Characteristics of Gastric Cancer. Dig Dis Sci. 2016;61:2272–83. doi:10.1007/s10620-016-4116-3.
   PubMed Web of Science ®Google Scholar
• Kurashige J, Hasegawa T, Niida A, et al. Integrated Molecular Profiling of Human Gastric Cancer Identifies DDR2 as a Potential Regulator of Peritoneal Dissemination. Sci Rep. 2016;6:1–11. doi:10.1038/srep22371.
   PubMed Web of Science ®Google Scholar
• Li D, Yang Z, Liu Z, et al. DDR2 and IFITM1 Are Prognostic Markers in Gallbladder Squamous Cell/Adenosquamous Carcinomas and Adenocarcinomas. Pathol Oncol Res. 2017;1–11. doi:10.1007/s12253-017-0314-3. [Epub ahead of print]
   Google Scholar
• Tsai M-C, Li W-M, Huang C-N, et al. DDR2 overexpression in urothelial carcinoma indicates an unfavorable prognosis: a large cohort study. Oncotarget. 2016;7:78918–31. doi:10.18632/oncotarget.12912.
   PubMedGoogle Scholar
• Sasaki S, Ueda M, Iguchi T, et al. DDR2 Expression Is Associated with a High Frequency of Peritoneal Dissemination and Poor Prognosis in Colorectal Cancer. Anticancer Res [Internet]. 2017;37:2587–91. Available from: http://ar.iiarjournals.org/content/37/5/2587.abstract. doi:10.21873/anticanres.11603.
   PubMed Web of Science ®Google Scholar
• Fan Y, Xu Z, Fan J, et al. Prognostic significance of discoidin domain receptor 2 (DDR2) expression in ovarian cancer. Am J Transl Res. 2016;8:2845–50.
   PubMed Web of Science ®Google Scholar
• Gonzalez ME, Martin E, Anwar T, et al. Mesenchymal stem cell induced DDR2 mediates stromal-breast cancer interactions and metastasis growth. Cell Rep. 2017;18:1215–28. doi:10.1016/j.celrep.2016.12.079.
   PubMed Web of Science ®Google Scholar
• Badiola I, Villacé P, Basaldua I, et al. Downregulation of discoidin domain receptor 2 in A375 human melanoma cells reduces its experimental liver metastasis ability. Oncol Rep. 2011;26:971–8.
   PubMed Web of Science ®Google Scholar
• Poudel B, Lee YM, Kim DK. DDR2 inhibition reduces migration and invasion of murine metastatic melanoma cells by suppressing MMP2/9 expression through ERK/NF-κB pathway. Acta Biochim Biophys Sin (Shanghai). 2015;47:292–8. doi:10.1093/abbs/gmv005.
   PubMed Web of Science ®Google Scholar
• Yan Z, Jin S, Wei Z, et al. Discoidin domain receptor 2 facilitates prostate cancer bone metastasis via regulating parathyroid hormone-related protein. Biochim Biophys Acta – Mol Basis Dis [Internet]. 2014;1842:1350–63. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0925443914001057. doi:10.1016/j.bbadis.2014.04.018.
   PubMed Web of Science ®Google Scholar
• Badiola I, Olaso E, Crende O, et al. Discoidin domain receptor 2 deficiency predisposes hepatic tissue to colon carcinoma metastasis. Gut [Internet]. 2012;61:1465–72. Available from: http://gut.bmj.com/lookup/doi/10.1136/gutjnl-2011-300810. doi:10.1136/gutjnl-2011-300810.
   PubMed Web of Science ®Google Scholar
• Corsa CAS, Brenot A, Grither WR, et al. The Action of Discoidin Domain Receptor 2 in Basal Tumor Cells and Stromal Cancer-Associated Fibroblasts Is Critical for Breast Cancer Metastasis. Cell Rep [Internet]. 2016;15:2510–23. doi:10.1016/j.celrep.2016.05.033.
   PubMed Web of Science ®Google Scholar
• Canning P, Tan L, Chu K, et al. Structural mechanisms determining inhibition of the collagen receptor DDR1 by selective and multi-targeted type II kinase inhibitors. J Mol Biol [Internet]. 2014;426:2457–70. doi:10.1016/j.jmb.2014.04.014.
   PubMed Web of Science ®Google Scholar
• Jeitany M, Leroy C, Tosti P, et al. Inhibition of DDR 1 -BCR signalling by nilotinib as a new therapeutic strategy for metastatic colorectal cancer. EMBO Mol Med. 2018;10:1–16.
   PubMed Web of Science ®Google Scholar
• Hedberg ML, Goh G, Chiosea SI, et al. Genetic landscape of metastatic and recurrent head and neck squamous cell carcinoma. J Clin Invest. 2015;126:169–80. doi:10.1172/JCI82066.
   PubMed Web of Science ®Google Scholar
• Xu C, Buczkowski KA, Zhang Y, et al. NSCLC Driven by DDR2 Mutation Is Sensitive to Dasatinib and JQ1 Combination Therapy. Mol Cancer Ther [Internet]. 2015;14:2382–9. Available from: http://mct.aacrjournals.org/cgi/doi/10.1158/1535-7163.MCT-15-0077. doi:10.1158/1535-7163.MCT-15-0077.
   PubMed Web of Science ®Google Scholar
• Pitini V, Arrigo C, Di Mirto C, et al. Response to dasatinib in a patient with SQCC of the lung harboring a discoid-receptor-2 and synchronous chronic myelogenous leukemia. Lung Cancer [Internet]. 2013;82:171–2. doi:10.1016/j.lungcan.2013.07.004.
   PubMed Web of Science ®Google Scholar
• Li Y, Lu X, Ren X, et al. Small molecule discoidin domain receptor kinase inhibitors and potential medical applications. J Med Chem. 2015;58:3287–301. doi:10.1021/jm5012319.
   PubMed Web of Science ®Google Scholar
• Gao M, Duan L, Luo J, et al. Discovery and optimization of 3-(2-(Pyrazolo[1,5- a]pyrimidin-6-yl) ethynyl)benzamides as novel selective and orally bioavailable discoidin domain receptor 1 (DDR1) inhibitors. J Med Chem. 2013;56:3281–95. doi:10.1021/jm301824k.
   PubMed Web of Science ®Google Scholar
• Kim H-G, Tan L, Weisberg EL, et al. Discovery of a Potent and Selective DDR1 Receptor Tyrosine Kinase Inhibitor. ACS Chem Biol [Internet]. 2013;8:2145–50. Available from: http://pubs.acs.org/doi/abs/10.1021/cb400430t. doi:10.1021/cb400430t.
   PubMed Web of Science ®Google Scholar
• Elkamhawy A, Park J-E, Cho N-C, et al. Discovery of a broad spectrum antiproliferative agent with selectivity for DDR1 kinase: cell line-based assay, kinase panel, molecular docking, and toxicity studies. J Enzyme Inhib Med Chem. 2016;31:158–66. doi:10.3109/14756366.2015.1004057.
   PubMed Web of Science ®Google Scholar
• Aguilera KY, Huang H, Du W, et al. Inhibition of Discoidin Domain Receptor 1 Reduces Collagen-mediated Tumorigenicity in Pancreatic Ductal Adenocarcinoma. Mol Cancer Ther [Internet]. 2017;16:2473–85. Available from: http://mct.aacrjournals.org/lookup/doi/10.1158/1535-7163.MCT-16-0834. doi:10.1158/1535-7163.MCT-16-0834.
   PubMed Web of Science ®Google Scholar
• Lu Q, Chen W, Peng J, et al. Antitumor activity of 7RH, a discoidin domain receptor?1 inhibitor, alone or in combination with dasatinib exhibits antitumor effects in nasopharyngeal carcinoma cells. Oncol Lett [Internet]. 2016;3598–608. Available from: http://www.spandidos-publications.com/10.3892/ol.2016.5088. doi:10.3892/ol.2016.5088.
   PubMed Web of Science ®Google Scholar
• Hur H, Ham I-H, Lee D, et al. Discoidin domain receptor 1 activity drives an aggressive phenotype in gastric carcinoma. BMC Cancer. 2017;17:87. doi:10.1186/s12885-017-3051-9.
   PubMed Web of Science ®Google Scholar
• Siddiqui K, Kim GW, Lee DH, et al. Actinomycin D identified as an inhibitor of discoidin domain receptor 2 interaction with collagen through an insect cell based screening of a drug compound library. Biol Pharm Bull. 2009;32:136–41. doi:10.1248/bpb.32.136.
   PubMed Web of Science ®Google Scholar
• Kim D, Ko P, You E, et al. The intracellular juxtamembrane domain of discoidin domain receptor 2 (DDR2) is essential for receptor activation and DDR2-mediated cancer progression. Int J Cancer. 2014;135:2547–57. doi:10.1002/ijc.28901.
   PubMed Web of Science ®Google Scholar
• Kim D, Yeom JH, Lee B, et al. Inhibition of discoidin domain receptor 2-mediated lung cancer cells progression by gold nanoparticle-aptamer-assisted delivery of peptides containing transmembrane-juxtamembrane 1/2 domain. Biochem Biophys Res Commun [Internet]. 2015;464:392–5. doi:10.1016/j.bbrc.2015.06.044.
   PubMed Web of Science ®Google Scholar
• Terai H, Tan L, Beauchamp EM, et al. Characterization of DDR2 Inhibitors for the Treatment of DDR2 Mutated Nonsmall Cell Lung Cancer. ACS Chem Biol. 2015;10:2687–96. doi:10.1021/acschembio.5b00655.
   PubMed Web of Science ®Google Scholar