[en] During tumour dissemination, invading breast carcinoma cells become confronted with a reactive stroma, a type I collagen-rich environment endowed with anti-proliferative and pro-apoptotic properties. To develop metastatic capabilities, tumour cells must acquire the capacity to cope with this novel microenvironment. How cells interact with and respond to their microenvironment during cancer dissemination remains poorly understood. To address the impact of type I collagen on the fate of tumour cells, human breast carcinoma MCF-7 cells were cultured within three-dimensional type I collagen gels (3D COL1). Using this experimental model, we have previously demonstrated that membrane type-1 matrix metalloproteinase (MT1-MMP), a proteinase overexpressed in many aggressive tumours, promotes tumour progression by circumventing the collagen-induced up-regulation of BIK, a pro-apoptotic tumour suppressor, and hence apoptosis. Here we performed a transcriptomic analysis to decipher the molecular mechanisms regulating 3D COL1-induced apoptosis in human breast cancer cells. Control and MT1-MMP expressing MCF-7 cells were cultured on two-dimensional plastic plates or within 3D COL1 and a global transcriptional time-course analysis was performed. Shifting the cells from plastic plates to 3D COL1 activated a complex reprogramming of genes implicated in various biological processes. Bioinformatic analysis revealed a 3D COL1-mediated alteration of key cellular functions including apoptosis, cell proliferation, RNA processing and cytoskeleton remodelling. By using a panel of pharmacological inhibitors, we identified discoidin domain receptor 1 (DDR1), a receptor tyrosine kinase specifically activated by collagen, as the initiator of 3D COL1-induced apoptosis. Our data support the concept that MT1-MMP contributes to the inactivation of the DDR1-BIK signalling axis through the cleavage of collagen fibres and/or the alteration of DDR1 receptor signalling unit, without triggering a drastic remodelling of the transcriptome of MCF-7 cells.
Disciplines :
Oncology
Author, co-author :
Assent, Delphine
Bourgot, Isabelle ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Hennuy, Benoît ; Université de Liège - ULiège > GIGA-Research
Geurts, Pierre ; Université de Liège - ULiège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Algorith. des syst. en interaction avec le monde physique
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique
Maquoi, Erik ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Language :
English
Title :
A Membrane-Type-1 Matrix Metalloproteinase (MT1-MMP) - Discoidin Domain Receptor 1 Axis Regulates Collagen-Induced Apoptosis in Breast Cancer Cells.
Publication date :
2015
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Geiger B, Bershadsky A, Pankov R, Yamada KM (2001) Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2: 793-805. PMID: 11715046
Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21: 309-322. doi: 10.1016/j.ccr.2012.02.022 PMID: 22439926
Harunaga JS, Yamada KM (2011) Cell-matrix adhesions in 3D. Matrix Biol 30: 363-368. doi: 10. 1016/j.matbio.2011.06.001 PMID: 21723391
Pampaloni F, Reynaud EG, Stelzer EH (2007) The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 8: 839-845. PMID: 17684528
Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130: 601-610. PMID: 17719539
Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374. PMID: 12724734
Poincloux R, Lizarraga F, Chavrier P (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122: 3015-3024. doi: 10.1242/jcs.034561 PMID: 19692588
Rowe RG, Weiss SJ (2008) Breaching the basement membrane: who, when and how? Trends Cell Biol 18: 560-574. doi: 10.1016/j.tcb.2008.08.007 PMID: 18848450
Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, et al. (2010) Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 70: 5706-5716. doi: 10. 1158/0008-5472.CAN-09-2356 PMID: 20570886
Bissell MJ, Rizki A, Mian IS (2003) Tissue architecture: the ultimate regulator of breast epithelial function. Curr Opin Cell Biol 15: 753-762. PMID: 14644202
Noel A, Kebers F, Maquoi E, Foidart JM (1999) Cell-cell and cell-matrix interactions during breast cancer progression. Curr Top Pathol 93: 183-193. PMID: 10339911
Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401. PMID: 16572188
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100: 57-70. PMID: 10647931
Liotta LA, Kohn EC (2001) The microenvironment of the tumour-host interface. Nature 411: 375-379.PMID: 11357145
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674. doi: 10.1016/j.cell.2011.02.013 PMID: 21376230
Sabeh F, Li XY, Saunders TL, Rowe RG, Weiss SJ (2009) Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 284: 23001-23011. doi: 10.1074/jbc.M109.002808 PMID: 19542530
Sodek KL, Brown TJ, Ringuette MJ (2008) Collagen I but not Matrigel matrices provide an MMP-dependent barrier to ovarian cancer cell penetration. BMC Cancer 8: 223. doi: 10.1186/1471-2407-8-223 PMID: 18681958
Henriet P, Zhong ZD, Brooks PC, Weinberg KI, DeClerck YA (2000) Contact with fibrillar collagen inhibits melanoma cell proliferation by up-regulating p27KIP1. Proc Natl Acad Sci U S A 97: 10026-10031. PMID: 10944199
Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ (2000) Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 149: 1309-1323. PMID: 10851027
Mizushima H, Wang X, Miyamoto S, Mekada E (2009) Integrin signal masks growth-promotion activity of HB-EGF in monolayer cell cultures. J Cell Sci 122: 4277-4286. doi: 10.1242/jcs.054551 PMID: 19887590
Bao W, Stromblad S (2004) Integrin alphav-mediated inactivation of p53 controls a MEK1-dependent melanoma cell survival pathway in three-dimensional collagen. J Cell Biol 167: 745-756. PMID: 15557124
Fujisaki H, Hattori S (2002) Keratinocyte apoptosis on type I collagen gel caused by lack of laminin 5/ 10/11 deposition and Akt signaling. Exp Cell Res 280: 255-269. PMID: 12413891
Montgomery AM, Reisfeld RA, Cheresh DA (1994) Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen. Proc Natl Acad Sci U S A 91: 8856-8860. PMID: 7522323
Birkedal-Hansen H (1987) Catabolism and turnover of collagens: collagenases. Methods Enzymol 144: 140-171. PMID: 3041177
Perumal S, Antipova O, Orgel JP (2008) Collagen fibril architecture, domain organization, and triplehelical conformation govern its proteolysis. Proc Natl Acad Sci U S A 105: 2824-2829. doi: 10.1073/ pnas.0710588105 PMID: 18287018
Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69: 562-573. PMID: 16405877
Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141: 52-67. doi: 10.1016/j.cell.2010.03.015 PMID: 20371345
Noel A, Gutierrez-Fernandez A, Sounni NE, Behrendt N, Maquoi E, et al. (2012) New and paradoxical roles of matrix metalloproteinases in the tumor microenvironment. Front Pharmacol 3: 140. doi: 10. 3389/fphar.2012.00140 PMID: 22822400
Noel A, Jost M, Maquoi E (2008) Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol 19: 52-60. PMID: 17625931
Lopez-Otin C, Hunter T (2010) The regulatory crosstalk between kinases and proteases in cancer. Nat Rev Cancer 10: 278-292. doi: 10.1038/nrc2823 PMID: 20300104
Rodriguez D, Morrison CJ, Overall CM (2010) Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim Biophys Acta 1803: 39-54. doi: 10.1016/j.bbamcr.2009.09.015 PMID: 19800373
Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, et al. (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272: 2446-2451. PMID: 8999957
Barbolina MV, Stack MS (2008) Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Semin Cell Dev Biol 19: 24-33. PMID: 17702616
Figueira RC, Gomes LR, Neto JS, Silva FC, Silva ID, et al. (2009) Correlation between MMPs and their inhibitors in breast cancer tumor tissue specimens and in cell lines with different metastatic potential. BMC Cancer 9: 20. doi: 10.1186/1471-2407-9-20 PMID: 19144199
Okada A, Bellocq JP, Rouyer N, Chenard MP, Rio MC, et al. (1995) Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc Natl Acad Sci U S A 92: 2730-2734. PMID: 7708715
McGowan PM, Duffy MJ (2008) Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database. Ann Oncol 19: 1566-1572. doi: 10.1093/annonc/ mdn180 PMID: 18503039
Maquoi E, Assent D, Detilleux J, Pequeux C, Foidart JM, et al. (2012) MT1-MMP protects breast carcinoma cells against type I collagen-induced apoptosis. Oncogene 31: 480-493. doi: 10.1038/onc. 2011.249 PMID: 21706048
Kim HG, Tan L, Weisberg EL, Liu F, Canning P, et al. (2013) Discovery of a potent and selective DDR1 receptor tyrosine kinase inhibitor. ACS Chem Biol 8: 2145-2150. doi: 10.1021/cb400430t PMID: 23899692
Lin SM, Du P, Huber W, Kibbe WA (2008) Model-based variance-stabilizing transformation for Illumina microarray data. Nucleic Acids Res 36: e11. doi: 10.1093/nar/gkm1075 PMID: 18178591
Kallio MA, Tuimala JT, Hupponen T, Klemela P, Gentile M, et al. (2011) Chipster: user-friendly analysis software for microarray and other high-throughput data. BMC Genomics 12: 507. doi: 10.1186/ 1471-2164-12-507 PMID: 21999641
Barbosa-Morais NL, Dunning MJ, Samarajiwa SA, Darot JF, Ritchie ME, et al. (2010) A re-annotation pipeline for Illumina BeadArrays: improving the interpretation of gene expression data. Nucleic Acids Res 38: e17. doi: 10.1093/nar/gkp942 PMID: 19923232
Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378. PMID: 12613259
Maquoi E, Frankenne F, Baramova E, Munaut C, Sounni NE, et al. (2000) Membrane type 1 matrix metalloproteinase-associated degradation of tissue inhibitor of metalloproteinase 2 in human tumor cell lines. J Biol Chem 275: 11368-11378. PMID: 10753951
Kleinman HK, Martin GR (2005) Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol 15: 378-386. PMID: 15975825
Emanuele MJ, Ciccia A, Elia AE, Elledge SJ (2011) Proliferating cell nuclear antigen (PCNA)-associated KIAA0101/PAF15 protein is a cell cycle-regulated anaphase-promoting complex/cyclosome substrate. Proc Natl Acad Sci U S A 108: 9845-9850. doi: 10.1073/pnas.1106136108 PMID: 21628590
Belyantseva IA, Perrin BJ, Sonnemann KJ, Zhu M, Stepanyan R, et al. (2009) Gamma-actin is required for cytoskeletal maintenance but not development. Proc Natl Acad Sci U S A 106: 9703-9708. doi: 10.1073/pnas.0900221106 PMID: 19497859
Huang XF, Han J, Hu XT, He C (2012) Mechanisms involved in biological behavior changes associated with Angptl4 expression in colon cancer cell lines. Oncol Rep 27: 1541-1547. doi: 10.3892/or. 2012.1672 PMID: 22307217
Bhamidipati A, Lewis SA, Cowan NJ (2000) ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. J Cell Biol 149: 1087-1096. PMID: 10831612
Sun J, Zhang D, Bae DH, Sahni S, Jansson P, et al. (2013) Metastasis suppressor, NDRG1, mediates its activity through signaling pathways and molecular motors. Carcinogenesis 34: 1943-1954. doi: 10.1093/carcin/bgt163 PMID: 23671130
Schofield AV, Bernard O (2013) Rho-associated coiled-coil kinase (ROCK) signaling and disease. Crit Rev Biochem Mol Biol 48: 301-316. doi: 10.3109/10409238.2013.786671 PMID: 23601011
Millerot-Serrurot E, Guilbert M, Fourre N, Witkowski W, Said G, et al. (2010) 3D collagen type I matrix inhibits the antimigratory effect of doxorubicin. Cancer Cell Int 10: 26. doi: 10.1186/1475-2867-10-26 PMID: 20707917
Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG (1993) hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62: 289-321. PMID: 8352591
Han SP, Tang YH, Smith R (2010) Functional diversity of the hnRNPs: past, present and perspectives. Biochem J 430: 379-392. doi: 10.1042/BJ20100396 PMID: 20795951
Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, et al. (2012) Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 1: 167-178. PMID: 22574288
Chen ZY, Cai L, Zhu J, Chen M, Chen J, et al. (2011) Fyn requires HnRNPA2B1 and Sam68 to synergistically regulate apoptosis in pancreatic cancer. Carcinogenesis 32: 1419-1426. doi: 10.1093/ carcin/bgr088 PMID: 21642356
Chen LC, Chung IC, Hsueh C, Tsang NM, Chi LM, et al. (2010) The antiapoptotic protein, FLIP, is regulated by heterogeneous nuclear ribonucleoprotein K and correlates with poor overall survival of nasopharyngeal carcinoma patients. Cell Death Differ 17: 1463-1473. doi: 10.1038/cdd.2010.24 PMID: 20224598
Rauch J, O'Neill E, Mack B, Matthias C, Munz M, et al. (2010) Heterogeneous nuclear ribonucleoprotein H blocks MST2-mediated apoptosis in cancer cells by regulating A-Raf transcription. Cancer Res 70: 1679-1688. doi: 10.1158/0008-5472.CAN-09-2740 PMID: 20145135
Xu N, Chen CY, Shyu AB (2001) Versatile role for hnRNP D isoforms in the differential regulation of cytoplasmic mRNA turnover. Mol Cell Biol 21: 6960-6971. PMID: 11564879
Marko M, Leichter M, Patrinou-Georgoula M, Guialis A (2010) hnRNP M interacts with PSF and p54 (nrb) and co-localizes within defined nuclear structures. Exp Cell Res 316: 390-400. doi: 10.1016/j. yexcr.2009.10.021 PMID: 19874820
Wahl MC, Will CL, Luhrmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701-718. doi: 10.1016/j.cell.2009.02.009 PMID: 19239890
Chen M, Manley JL (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10: 741-754. doi: 10.1038/nrm2777 PMID: 19773805
Jaskiewicz L, FilipowiczW(2008) Role of Dicer in posttranscriptional RNA silencing. Curr Top Microbiol Immunol 320: 77-97. PMID: 18268840
Semenza GL (2009) Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 24: 97-106. doi: 10.1152/physiol.00045.2008 PMID: 19364912
Cui H, Grosso S, Schelter F, Mari B, Kruger A (2012) On the Pro-Metastatic Stress Response to Cancer Therapies: Evidence for a Positive Co-Operation between TIMP-1, HIF-1alpha, and miR-210. Front Pharmacol 3: 134. doi: 10.3389/fphar.2012.00134 PMID: 22807917
Sakamoto T, Niiya D, Seiki M (2011) Targeting the Warburg effect that arises in tumor cells expressing membrane type-1 matrix metalloproteinase. J Biol Chem 286: 14691-14704. doi: 10.1074/jbc.M110. M188714 PMID: 21372132
Sakamoto T, Weng JS, Hara T, Yoshino S, Kozuka-Hata H, et al. (2014) Hypoxia-Inducible Factor 1 Regulation through Cross Talk between mTOR and MT1-MMP. Mol Cell Biol 34: 30-42. doi: 10. 1128/MCB.01169-13 PMID: 24164895
Zhu P, Tan MJ, Huang RL, Tan CK, Chong HC, et al. (2011) Angiopoietin-like 4 protein elevates the prosurvival intracellular O2(-):H2O2 ratio and confers anoikis resistance to tumors. Cancer Cell 19: 401-415. doi: 10.1016/j.ccr.2011.01.018 PMID: 21397862
Padua D, Zhang XH, Wang Q, Nadal C, Gerald WL, et al. (2008) TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133: 66-77. doi: 10.1016/j.cell.2008.01.046 PMID: 18394990
McDonald PC, Winum JY, Supuran CT, Dedhar S (2012) Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 3: 84-97. PMID: 22289741
Ureshino H, Murakami Y, Watari K, Izumi H, Kawahara A, et al. (2012) N-myc downstream regulated gene 1 (NDRG1) promotes metastasis of human scirrhous gastric cancer cells through epithelial mesenchymal transition. PLoS One 7: e41312. doi: 10.1371/journal.pone.0041312 PMID: 22844455
Cheng J, Xie HY, Xu X, Wu J, Wei X, et al. (2011) NDRG1 as a biomarker for metastasis, recurrence and of poor prognosis in hepatocellular carcinoma. Cancer Lett 310: 35-45. doi: 10.1016/j.canlet. 2011.06.001 PMID: 21763068
Wang Q, Li LH, Gao GD, Wang G, Qu L, et al. (2013) HIF-1alpha up-regulates NDRG1 expression through binding to NDRG1 promoter, leading to proliferation of lung cancer A549 cells. Mol Biol Rep 40: 3723-3729. doi: 10.1007/s11033-012-2448-4 PMID: 23526365
Liao SH, Zhao XY, Han YH, Zhang J, Wang LS, et al. (2009) Proteomics-based identification of two novel direct targets of hypoxia-inducible factor-1 and their potential roles in migration/invasion of cancer cells. Proteomics 9: 3901-3912. doi: 10.1002/pmic.200800922 PMID: 19637235
Tracy K, Macleod KF (2007) Regulation of mitochondrial integrity, autophagy and cell survival by BNIP3. Autophagy 3: 616-619. PMID: 17786027
Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, et al. (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283: 10892-10903. doi: 10. 1074/jbc.M800102200 PMID: 18281291
Vijayalingam S, Pillai SG, Rashmi R, Subramanian T, Sagartz JE, et al. (2010) Overexpression of BH3-Only Protein BNIP3 Leads to Enhanced Tumor Growth. Genes Cancer 1: 964-971. doi: 10. 1177/1947601910386110 PMID: 21779475
Germain M, Mathai JP, Shore GC (2002) BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J Biol Chem 277: 18053-18060. PMID: 11884414
Jawdekar GW, Henry RW (2008) Transcriptional regulation of human small nuclear RNA genes. Biochim Biophys Acta 1779: 295-305. doi: 10.1016/j.bbagrm.2008.04.001 PMID: 18442490
O'Reilly D, Dienstbier M, Cowley SA, Vazquez P, Drozdz M, et al. (2013) Differentially expressed, variant U1 snRNAs regulate gene expression in human cells. Genome Res 23: 281-291. doi: 10.1101/ gr.142968.112 PMID: 23070852
Biencowe BJ (2002) Transcription: surprising role for an elusive small nuclear RNA. Current Biology 12: R147-149. PMID: 11864590
Prasanth KV, Camiolo M, Chan G, Tripathi V, Denis L, et al. (2010) Nuclear organization and dynamics of 7SK RNA in regulating gene expression. Mol Biol Cell 21: 4184-4196. doi: 10.1091/mbc.E10-02-0105 PMID: 20881057
Kubow KE, Horwitz AR (2011) Reducing background fluorescence reveals adhesions in 3D matrices. Nat Cell Biol 13: 3-5; author reply 5-7. doi: 10.1038/ncb0111-3 PMID: 21173800
Mori H, Tomari T, Koshikawa N, Kajita M, Itoh Y, et al. (2002) CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J 21: 3949-3959. PMID: 12145196
Fu HL, Sohail A, Valiathan RR, Wasinski BD, Kumarasiri M, et al. (2013) Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. J Biol Chem 288: 12114-12129. doi: 10.1074/jbc.M112.409599 PMID: 23519472
Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, et al. (2001) SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J Pharmacol Exp Ther 296: 312-321. PMID: 11160612
Uehara Y, Murakami Y, Mizuno S, Kawai S (1988) Inhibition of transforming activity of tyrosine kinase oncogenes by herbimycin A. Virology 164: 294-298. PMID: 2452516
Sen B, Johnson FM (2011) Regulation of SRC family kinases in human cancers. J Signal Transduct 2011: 865819. doi: 10.1155/2011/865819 PMID: 21776389
Brandvold KR, Steffey ME, Fox CC, Soellner MB (2012) Development of a highly selective c-Src kinase inhibitor. ACS Chem Biol 7: 1393-1398. doi: 10.1021/cb300172e PMID: 22594480
Day E, Waters B, Spiegel K, Alnadaf T, Manley PW, et al. (2008) Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol 599: 44-53. doi: 10.1016/j.ejphar.2008.10.014 PMID: 18938156
Montero JC, Seoane S, Ocana A, Pandiella A (2011) Inhibition of SRC family kinases and receptor tyrosine kinases by dasatinib: possible combinations in solid tumors. Clin Cancer Res 17: 5546-5552. doi: 10.1158/1078-0432.CCR-10-2616 PMID: 21670084
Valiathan RR, Marco M, Leitinger B, Kleer CG, Fridman R (2012) Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev 31: 295-321. doi: 10.1007/ s10555-012-9346-z PMID: 22366781
Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1: 13-23. PMID: 9659899
Cader FZ, Vockerodt M, Bose S, Nagy E, Brundler MA, et al. (2013) The EBV oncogene LMP1 protects lymphoma cells from cell death through the collagen-mediated activation of DDR1. Blood 122: 4237-4245. doi: 10.1182/blood-2013-04-499004 PMID: 24136166
Kim HG, Hwang SY, Aaronson SA, Mandinova A, Lee SW (2011) DDR1 receptor tyrosine kinase promotes prosurvival pathway through Notch1 activation. J Biol Chem 286: 17672-17681. doi: 10.1074/ jbc.M111.236612 PMID: 21398698
Ongusaha PP, Kim JI, Fang L, Wong TW, Yancopoulos GD, et al. (2003) p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J 22: 1289-1301. PMID: 12628922
Bonnomet A, Brysse A, Tachsidis A, Waltham M, Thompson EW, et al. (2010) Epithelial-to-mesenchymal transitions and circulating tumor cells. J Mammary Gland Biol Neoplasia 15: 261-273. doi: 10.1007/s10911-010-9174-0 PMID: 20449641
Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, et al. (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 107: 15449-15454. doi: 10.1073/pnas. 1004900107 PMID: 20713713
Gilles C, Polette M, Seiki M, Birembaut P, Thompson EW (1997) Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab Invest 76: 651-660. PMID: 9166284
Vogel W, Brakebusch C, Fassler R, Alves F, Ruggiero F, et al. (2000) Discoidin domain receptor 1 is activated independently of beta(1) integrin. J Biol Chem 275: 5779-5784. PMID: 10681566
