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Cited by 77

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CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer

Macpherson, Iain R, Rainero, Elena, Mitchell, Louise E, van den Berghe, Peter VE, Speirs, Claire, Dozynkiewicz, Marta A, Chaudhary, Suman, Kalna, Gabriela, Edwards, Joanne, Timpson, Paul, Norman, Jim C·2014·Journal of Cell Science
DOI 10.1242/jcs.135947
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Abstract

Chloride intracellular channel 3 (CLIC3) drives invasiveness of pancreatic and ovarian cancer by acting in concert with Rab25 to regulate recycling of α5β1 from late endosomes to the plasma membrane. Here we show that in two estrogen receptor (ER)-negative breast cancer cell lines CLIC3 has little influence on integrin recycling, but controls trafficking of the pro-invasive matrix metalloprotease, MT1-MMP. In MDA-MB-231 cells MT1-MMP and CLIC3 are localised primarily to late endosomal/lysosomal compartments located above the plane of adhesion and near the nucleus. MT1-MMP is transferred from these late endosomes to sites of cell-matrix adhesion in a CLIC3-dependent fashion. Correspondingly, CLIC3-knockdown opposes MT1-MMP-dependent invasive processes. These include the disruption of the basement membrane as acini formed from MCF10DCIS.com cells acquire invasive characteristics in 3D culture, and the invasion of MDA-MB-231 cells into Matrigel or organotypic plugs of type I collagen. Consistent with this, expression of CLIC3 predicts poor prognosis in ER-negative breast cancer. The identification of MT1-MMP as a cargo of a CLIC3-regulated pathway that drives invasion highlights the importance of late endosomal sorting and trafficking in breast cancer.

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  • Rab27a

    Bahadoran, P., Aberdam, E., Mantoux, F., Buscà, R., Bille, K., Yalman, N., de Saint-Basile, G., Casaroli-Marano, R., Ortonne, J.-P., & Ballotti, R. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.4.843 · Cited by 221

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Research works printed but not linked: 43

  1. Amornphimoltham, 2013, Rab25 regulates invasion and metastasis in head and neck cancer., Clin. Cancer Res., 19, 1375, 10.1158/1078-0432.CCR-12-2858 · DOI
  2. Behbod, 2009, An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ., Breast Cancer Res., 11, R66, 10.1186/bcr2358 · DOI
  3. Bravo-Cordero, 2007, MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway., EMBO J., 26, 1499, 10.1038/sj.emboj.7601606 · DOI
  4. Cheng, 2004, The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers., Nat. Med., 10, 1251, 10.1038/nm1125 · DOI
  5. Cheng, 2006, Loss of RAB25 expression in breast cancer., Int. J. Cancer, 118, 2957, 10.1002/ijc.21739 · DOI
  6. Cheng, 2010, Tumor suppressor function of Rab25 in triple-negative breast cancer., Int. J. Cancer, 126, 2799, 10.1002/ijc.24900 · DOI
  7. Debnath, 2003, Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures., Methods, 30, 256, 10.1016/S1046-2023(03)00032-X · DOI
  8. Desmedt, 2007, Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series., Clin. Cancer Res., 13, 3207, 10.1158/1078-0432.CCR-06-2765 · DOI
  9. Dozynkiewicz, 2012, Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression., Dev. Cell, 22, 131, 10.1016/j.devcel.2011.11.008 · DOI
  10. Frittoli, 2011, Secretory and endo/exocytic trafficking in invadopodia formation: the MT1-MMP paradigm., Eur. J. Cell Biol., 90, 108, 10.1016/j.ejcb.2010.04.007 · DOI
  11. Glück, 2012, TP53 genomics predict higher clinical and pathologic tumor response in operable early-stage breast cancer treated with docetaxel-capecitabine ± trastuzumab., Breast Cancer Res. Treat., 132, 781, 10.1007/s10549-011-1412-7 · DOI
  12. Hennigan, 1994, Fos-transformation activates genes associated with invasion., Oncogene, 9, 3591
  13. Hotary, 2006, A cancer cell metalloprotease triad regulates the basement membrane transmigration program., Genes Dev., 20, 2673, 10.1101/gad.1451806 · DOI
  14. Hu, 2008, Regulation of in situ to invasive breast carcinoma transition., Cancer Cell, 13, 394, 10.1016/j.ccr.2008.03.007 · DOI
  15. Jedeszko, 2009, Fibroblast hepatocyte growth factor promotes invasion of human mammary ductal carcinoma in situ., Cancer Res., 69, 9148, 10.1158/0008-5472.CAN-09-1043 · DOI · Paper page
  16. Li, 2008, Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase., Mol. Biol. Cell, 19, 3221, 10.1091/mbc.E08-01-0016 · DOI
  17. McGowan, 2008, Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database., Ann. Oncol., 19, 1566, 10.1093/annonc/mdn180 · DOI
  18. Ménasché, 2000, Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome., Nat. Genet., 25, 173, 10.1038/76024 · DOI
  19. Miller, 2000, MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ., J. Natl. Cancer Inst., 92, 1185, 10.1093/jnci/92.14.1185A · DOI
  20. Monteiro, 2013, Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia., J. Cell Biol., 203, 1063, 10.1083/jcb.201306162 · DOI
  21. Nam, 2010, Loss of Rab25 promotes the development of intestinal neoplasia in mice and is associated with human colorectal adenocarcinomas., J. Clin. Invest., 120, 840, 10.1172/JCI40728 · DOI
  22. Ohotski, 2012, Expression of sphingosine 1-phosphate receptor 4 and sphingosine kinase 1 is associated with outcome in oestrogen receptor-negative breast cancer., Br. J. Cancer, 106, 1453, 10.1038/bjc.2012.98 · DOI
  23. Ostrowski, 2010, Rab27a and Rab27b control different steps of the exosome secretion pathway., Nat. Cell Biol., 12, 19, 10.1038/ncb2000 · DOI
  24. Packard, 2009, Direct visualization of protease activity on cells migrating in three-dimensions., Matrix Biol., 28, 3, 10.1016/j.matbio.2008.10.001 · DOI
  25. Perentes, 2011, Cancer cell-associated MT1-MMP promotes blood vessel invasion and distant metastasis in triple-negative mammary tumors., Cancer Res., 71, 4527, 10.1158/0008-5472.CAN-10-4376 · DOI
  26. Poincloux, 2009, Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia., J. Cell Sci., 122, 3015, 10.1242/jcs.034561 · DOI
  27. Remacle, 2003, Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface., J. Cell Sci., 116, 3905, 10.1242/jcs.00710 · DOI
  28. Remacle, 2005, The transmembrane domain is essential for the microtubular trafficking of membrane type-1 matrix metalloproteinase (MT1-MMP)., J. Cell Sci., 118, 4975, 10.1242/jcs.02610 · DOI
  29. Rhodes, 2004, ONCOMINE: a cancer microarray database and integrated data-mining platform., Neoplasia, 6, 1, 10.1016/S1476-5586(04)80047-2 · DOI
  30. Roberts, 2001, PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading., Curr. Biol., 11, 1392, 10.1016/S0960-9822(01)00442-0 · DOI
  31. Sabeh, 2004, Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP., J. Cell Biol., 167, 769, 10.1083/jcb.200408028 · DOI
  32. So, 2013, Targeting CD44-STAT3 signaling by Gemini vitamin D analog leads to inhibition of invasion in basal-like breast cancer., PLoS ONE, 8, e54020, 10.1371/journal.pone.0054020 · DOI
  33. Steffen, 2008, MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7., Curr. Biol., 18, 926, 10.1016/j.cub.2008.05.044 · DOI
  34. Szabova, 2008, MT1-MMP is required for efficient tumor dissemination in experimental metastatic disease., Oncogene, 27, 3274, 10.1038/sj.onc.1210982 · DOI
  35. Têtu, 2006, The influence of MMP-14, TIMP-2 and MMP-2 expression on breast cancer prognosis., Breast Cancer Res., 8, R28, 10.1186/bcr1503 · DOI
  36. Timpson, 2011, Organotypic collagen I assay: a malleable platform to assess cell behaviour in a 3-dimensional context., J. Vis. Exp., 56, e3089
  37. Tong, 2012, Rab25 is a tumor suppressor gene with antiangiogenic and anti-invasive activities in esophageal squamous cell carcinoma., Cancer Res., 72, 6024, 10.1158/0008-5472.CAN-12-1269 · DOI
  38. Uekita, 2001, Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity., J. Cell Biol., 155, 1345, 10.1083/jcb.200108112 · DOI
  39. Ueno, 1997, Expression and tissue localization of membrane-types 1, 2, and 3 matrix metalloproteinases in human invasive breast carcinomas., Cancer Res., 57, 2055
  40. Wang, 2004, Co-recycling of MT1-MMP and MT3-MMP through the trans-Golgi network. Identification of DKV582 as a recycling signal., J. Biol. Chem., 279, 9331, 10.1074/jbc.M312369200 · DOI
  41. Williams, 2011, Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration., J. Biol. Chem., 286, 43405, 10.1074/jbc.M111.297069 · DOI
  42. Wolf, 2007, Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion., Nat. Cell Biol., 9, 893, 10.1038/ncb1616 · DOI
  43. Yu, 2012, N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods., J. Cell Biol., 199, 527, 10.1083/jcb.201203025 · DOI

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Metadata

Authors
Macpherson, I. R., Rainero, E., Mitchell, L. E., van den Berghe, P. V., Speirs, C., Dozynkiewicz, M. A., Chaudhary, S., Kalna, G., Edwards, J., Timpson, P., & Norman, J. C.
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2014-01-01
ISSN
  • 1477-9137
  • 0021-9533
DOI
10.1242/jcs.135947
Cited by
77
References
1
Language
en

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