DDR1 and MT1-MMP Expression Levels Are Determinant for Triggering BIK-Mediated Apoptosis by 3D Type I Collagen Matrix in Invasive Basal-Like Breast Carcinoma Cells.
DDR1 and MT1-MMP Expression Levels Are Determinant for Triggering BIK-Mediated Apoptosis by 3D Type I Collagen Matrix in Invasive Basal-Like Breast Carcinoma Cells - 2019.pdf
DDR1; MT1-MMP; apoptosis; breast carcinoma; type I collagen
Abstract :
[en] Type I collagen is the major adhesive component in breast interstitial stroma, which represents the first barrier against tumor cell invasion after basement-membrane degradation. Among cellular receptors, type I collagen is able to activate discoidin domain receptors DDR1 and DDR2. We have previously shown that in 3D collagen matrix, DDR1 plays a key role as it promotes cell growth suppression and apoptosis through the upregulation of the pro-apoptotic mediator BIK in noninvasive luminal-like breast carcinoma cells. We have also shown that MT1-MMP is able to rescue these cells and protect them against the effects induced by collagen/DDR1/BIK axis. Our data suggested that the protective effect of MT1-MMP might be mediated through the degradation of type I collagen and/or DDR1 cleavage. Decreased DDR1 expression has been associated with the epithelial to mesenchymal transition process in breast cancer, and its overexpression in aggressive basal-like breast cancer cells reduces their invasiveness in 3D cultures and in vivo. In the present work, we propose to study the role of MT1-MMP in the resistance against collagen-induced apoptosis in basal-like breast carcinoma MDA-MB-231 cells. We aimed to investigate whether MT1-MMP depletion is able to restore apoptosis mediated by collagen/DDR1/BIK axis and to verify if such depletion is able to restore full-length DDR1 expression and phosphorylation. ShRNA strategy against MT1-MMP mRNA was able to partially restore full length DDR1 expression and phosphorylation. This was accompanied by a decrease in cell growth and an upregulation of BIK expression. This suggested that MT1-MMP expression in basal-like breast carcinoma cells, in addition to a low basal level of DDR1 expression, protects these cells against collagen-induced apoptosis via DDR1 cleavage. Since DDR1 was moderately expressed in MDA-MB-231 cells, we then investigated whether overexpression of DDR1 could be able to increase its ability to suppress cell growth and to induce apoptosis. Data showed that overexpression of DDR1 induced a decrease in cell growth and an increase in BIK expression, suggesting that moderate expression level of full length DDR1 in basal-like breast carcinoma provides them with a capacity to resist to collagen-induced cell growth suppression and apoptosis. Finally, the combined overexpression of DDR1 and depletion of MT1-MMP in MDA-MB-231 cells synergistically increased collagen-induced cell growth suppression and apoptosis to a level similar to that observed in luminal breast carcinoma. Taken together, our data suggest that during the acquisition of mesenchymal features, the low level of DDR1 expression should be considered as an important biomarker in the prognosis of basal-like breast carcinoma, conferring them a high rate of cell growth and resistance to BIK-mediated apoptosis induced by the stromal collagen.
Disciplines :
Oncology
Author, co-author :
Saby, Charles
Collin, Guillaume
Sinane, Maha
Buache, Emilie
Van Gulick, Laurence
Saltel, Frederic
Maquoi, Erik ✱; Université de Liège - ULiège > Cancer-Tumours and development biology
Morjani, Hamid ✱
✱ These authors have contributed equally to this work.
Language :
English
Title :
DDR1 and MT1-MMP Expression Levels Are Determinant for Triggering BIK-Mediated Apoptosis by 3D Type I Collagen Matrix in Invasive Basal-Like Breast Carcinoma Cells.
Aït-Belkacem, D., Guilbert, M., Roche, M., Duboisset, J., Ferrand, P., Sockalingum, G., et al. (2012). Microscopic structural study of collagen aging in isolated fibrils using polarized second harmonic generation. J. Biomed. Opt. 17, 080506-080501. doi: 10.1117/1.JBO.17.8.080506
Albrechtsen, R., Kveiborg, M., Stautz, D., Vikeså, J., Noer, J. B., Kotzsh, A., et al. (2013). ADAM12 redistributes and activates MMP-14, resulting in gelatin degradation, reduced apoptosis and increased tumor growth. J. Cell Sci. 126, 4707-4720. doi: 10.1242/jcs.129510
Amar, S., Smith, L., and Fields, G. B. (2017). Matrix metalloproteinase collagenolysis in health and disease. Biochim. Biophys. Acta, Mol. Cell Res. 1864, 1940-1951. doi: 10.1016/j.bbamcr.2017.04.015
Assent, D., Bourgot, I., Hennuy, B., Geurts, P., Noël, A., Foidart, J. M., et al. (2015). A membrane-type-1 matrix metalloproteinase (MT1-MMP)-discoidin domain receptor 1 axis regulates collagen-induced apoptosis in breast cancer cells. PLoS One 10:e0116006. doi: 10.1371/journal.pone.0116006
Beauchamp, E. M., Woods, B. A., Dulak, A. M., Tan, L., Xu, C., Gray, N. S., et al. (2014). Acquired resistance to dasatinib in lung cancer cell lines conferred by DDR2 gatekeeper mutation and NF1 loss. Mol. Cancer Ther. 13, 475-482. doi: 10.1158/1535-7163.MCT-13-0817
Bonnans, C., Chou, J., and Werb, Z. (2014). Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15, 786-801. doi: 10.1038/nrm3904
Borza, C. M., and Pozzi, A. (2013). Discoidin domain receptors in disease. Matrix Biol. 34, 185-192. doi: 10.1016/j.matbio.2013.12.002
Buache, E., Thai, R., Wendling, C., Alpy, F., Page, A., Chenard, M. P., et al. (2014). Functional relationship between matrix metalloproteinase-11 and matrix metalloproteinase-14. Cancer Med. 3, 1197-1210. doi: 10.1002/cam4.290
Carafoli, F., and Hohenester, E. (2013). Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim. Biophys. Acta 1834, 2187-2194. doi: 10.1016/j.bbapap.2012.10.014
Castro-Castro, A., Marchesin, V., Monteiro, P., Lodillinsky, C., Rossé, C., and Chavrier, P. (2016). Cellular and molecular mechanisms of MT1-MMP-dependent cancer cell invasion. Annu. Rev. Cell Dev. Biol. 32, 555-576. doi: 10.1146/annurev-cellbio-111315-125227
Chung, V. Y., Tan, T. Z., Huang, R. L., Lai, H. C., and Huang, R. Y. (2017). Loss of discoidin domain receptor 1 (DDR1) via CpG methylation during EMT in epithelial ovarian cancer. Gene 635, 9-15. doi: 10.1016/j.gene.2017.09.001
Ciriello, G., Gatza, M. L., Beck, A. H., Wilkerson, M. D., Rhie, S. K., Pastore, A., et al. (2015). Comprehensive molecular portraits of invasive lobular breast cancer. Cell 163, 506-519. doi: 10.1016/j.cell.2015.09.033
Croissant, C., Tuariihionoa, A., Bacou, M., Souleyreau, W., Sala, M., Henriet, E., et al. (2018). DDR1 and DDR2 physical interaction leads to signaling interconnection but with possible distinct functions. Cell Adhes. Migr. 12, 324-334. doi: 10.1080/19336918.2018.1460012
Di Martino, J., Henriet, E., Ezzoukhry, Z., Goetz, J. G., Moreau, V., and Saltel, F. (2016). The microenvironment controls invadosome plasticity. J. Cell Sci. 129, 1759-1768. doi: 10.1242/jcs.182329
Egeblad, M., Rasch, M. G., and Weaver, V. M. (2010). Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22, 697-706. doi: 10.1016/j.ceb.2010.08.015
Ford, C. E., Lau, S. K., Zhu, C. Q., Andersson, T., Tsao, M. S., and Vogel, W. F. (2007). Expression and mutation analysis of the discoidin domain receptors 1 and 2 in non-small cell lung carcinoma. Br. J. Cancer 96, 808-814. doi: 10.1038/sj.bjc.6603614
Fu, H. L., Sohail, A., Valiathan, R. R., Wasinski, B. D., Kumarasiri, M., Mahasenan, K. V., et al. (2013a). Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. J. Biol. Chem. 288, 12114-12129. doi: 10.1074/jbc.M112.409599
Fu, H. L., Valiathan, R. R., Arkwright, R., Sohail, A., Mihai, C., Kumarasiri, M., et al. (2013b). Discoidin domain receptors: unique receptor tyrosine kinases in collagen-mediated signaling. J. Biol. Chem. 288, 7430-7437. doi: 10.1074/jbc.R112.444158
Garnotel, R., Rittie, L., Poitevin, S., Monboisse, J. C., Nguyen, P., Potron, G., et al. (2000). Human blood monocytes interact with type I collagen through alpha x beta 2 integrin (CD11c-CD18, gp150-95). J. Immunol. 164, 5928-5934. doi: 10.4049/jimmunol.164.11.5928
Györffy, B., Lanczky, A., Eklund, A. C., Denkert, C., Budczies, J., Li, Q., et al. (2010). An online survival analysis tool to rapidly assess the effect of 22, 277 genes on breast cancer prognosis using microarray data of 1, 809 patients. Breast Cancer Res. Treat. 123, 725-731.
Henriet, E., Sala, M., Abou Hammoud, A., Tuariihionoa, A., Di Martino, J., Ros, M., et al. (2018). Multitasking discoidin domain receptors are involved in several and specific hallmarks of cancer. Cell Adhes. Migr. 12, 363-377. doi: 10.1080/19336918.2018.1465156
Humphries, J. D., Byron, A., and Humphries, M. J. (2006). Integrin ligands at a glance. J. Cell Sci. 19(Pt 119), 3901-3903. doi: 10.1242/jcs.03098
Iwai, L. K., Payne, L. S., Luczynski, M. T., Chang, F., Xu, H., Clinton, R. W., et al. (2013). Phosphoproteomics of collagen receptor networks reveals SHP-2 phosphorylation downstream of wild-type DDR2 and its lung cancer mutants. Biochem. J. 454, 501-513. doi: 10.1042/BJ20121750
Jeitany, M., Leroy, C., Tosti, P., Lafitte, M., Le Guet, J., Simon, V., et al. (2018). Inhibition of DDR1-BCR signalling by nilotinib as a new therapeutic strategy for metastatic colorectal cancer. EMBO Mol. Med. 10:e7918. doi: 10.15252/emmm.201707918
Jézéquel, P., Campone, M., Gouraud, W., Guerin-Charbonnel, C., Leux, C., Ricolleau, G., et al. (2012). Bc-GenExMiner: an easy-to-use online platform for gene prognostic analyses in breast cancer. Breast Cancer Res. Treat. 131, 765-775. doi: 10.1007/s10549-011-1457-7
Juin, A., Di Martino, J., Leitinger, B., Henriet, E., Gary, A. S., Paysan, L., et al. (2014). Discoidin domain receptor 1 controls linear invadosome formation via a Cdc42-tuba pathway. J. Cell Biol. 207, 517-533. doi: 10.1083/jcb.201404079
Koh, M., Woo, Y., Valiathan, R. R., Jung, H. Y., Park, S. Y., Kim, Y. N., et al. (2015). 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 136, E508-E520. doi: 10.1002/ijc.29154
Lacroix, M., Toillon, R. A., and Leclercq, G. (2006). p53 and breast cancer, an update. Endocr. Relat. Cancer 13, 293-325. doi: 10.1677/erc.1.01172
Leitinger, B. (2014). Discoidin domain receptor functions in physiological and pathological conditions. Int. Rev. Cell Mol. Biol. 310, 39-87. doi: 10.1016/B978-0-12-800180-6.00002-5
Maquoi, E., Assent, D., Detilleux, J., Pequeux, C., Foidart, J. M., and Noël, A. (2012). MT1-MMP protects breast carcinoma cells against type I collagen-induced apoptosis. Oncogene 31, 480-493. doi: 10.1038/onc.2011.249
Moreau, V., and Saltel, F. (2015). Type I collagen fibrils and discoidin domain receptor 1 set invadosomes straight. Mol. Cell Oncol. 2:e1004963. doi: 10.1080/23723556.2015.1004963
Mouw, J. K., Ou, G., and Weaver, V. M. (2014). Extracellular matrix assembly: a multiscale deconstruction. Nat. Rev. Mol. Cell Biol. 15, 771-785. doi: 10.1038/nrm3902
Muller, P. A., and Vousden, K. H. (2014). Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 25, 304-317. doi: 10.1016/j.ccr.2014.01.021
Ongusaha, P. P., Kim, J. I., Fang, L., Wong, T. W., Yancopoulos, G. D., Aaronson, S. A., 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. doi: 10.1093/emboj/cdg129
Pickup, M. W., Mouw, J. K., and Weaver, V. M. (2014). The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 15, 1243-1253. doi: 10.15252/embr.201439246
Poincloux, R., Lizárraga, F., and Chavrier, P. (2009). Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 17(Pt 122), 3015-3024. doi: 10.1242/jcs.034561
Quail, D. F., and Joyce, J. A. (2013). Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 19, 1423-1437. doi: 10.1038/nm.3394
Rammal, H., Saby, C., Magnien, K., Van-Gulick, L., Garnotel, R., Buache, E., et al. (2016). Discoidin domain receptors: potential actors and targets in cancer. Front. Pharmacol. 7:55. doi: 10.3389/fphar.2016.00055
Saby, C., Buache, E., Brassart-Pasco, S., El Btaouri, H., Courageot, M. P., Van Gulick, L., et al. (2016). Type I collagen aging impairs discoidin domain receptor 2-mediated tumor cell growth suppression. Oncotarget 7, 24908-24927. doi: 10.18632/oncotarget.8795
Saby, C., Rammal, H., Magnien, K., Buache, E., Brassart-Pasco, S., Van-Gulick, L., et al. (2018). Age-related modifications of type I collagen impair DDR1-induced apoptosis in non-invasive breast carcinoma cells. Cell Adhes. Migr. 12, 335-347. doi: 10.1080/19336918.2018.1472182
Sakuma, S., Saya, H., Tada, M., Nakao, M., Fujiwara, T., Roth, J. A., et al. (1996). Receptor protein tyrosine kinase DDR is up-regulated by p53 protein. FEBS Lett. 398, 165-169. doi: 10.1016/S0014-5793(96)01234-3
Takai, K., Drain, A. P., Lawson, D. A., Littlepage, L. E., Karpuj, M., Kessenbrock, K., et al. (2018). Discoidin domain receptor 1 (DDR1) ablation promotes tissue fibrosis and hypoxia to induce aggressive basal-like breast cancers. Genes Dev. 32, 244-257. doi: 10.1101/gad.301366.117
Terashima, M., Togashi, Y., Sato, K., Mizuuchi, H., Sakai, K., Suda, K., et al. (2016). Functional analyses of mutations in receptor tyrosine kinase genes in non-small cell lung cancer: double-edged sword of DDR2. Clin. Cancer Res. 22, 3663-3671. doi: 10.1158/1078-0432.CCR-15-2093
Toy, K. A., Valiathan, R. R., Núñez, F., Kidwell, K. M., Gonzalez, M. E., Fridman, R., et al. (2015). Tyrosine kinase discoidin domain receptors DDR1 and DDR2 are coordinately deregulated in triple-negative breast cancer. Breast Cancer Res. Treat. 150, 9-18. doi: 10.1007/s10549-015-3285-7
Valiathan, R. R., Marco, M., Leitinger, B., Kleer, C. G., and 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
Vogel, W., Gish, G. D., Alves, F., and Pawson, T. (1997). The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13-23. doi: 10.1016/S1097-2765(00)80003-9
Wall, S. J., Werner, E., Werb, Z., and DeClerck, Y. A. (2005). Discoidin domain receptor 2 mediates tumor cell cycle arrest induced by fibrillar collagen. J. Biol. Chem. 280, 40187-40194. doi: 10.1074/jbc.M508226200
