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Coronin 1C promotes triple-negative breast cancer invasiveness through regulation of MT1-MMP traffic and invadopodia function

Oncogene volume 37, pages 6425–6441 (2018)Cite this article

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Abstract

Membrane type 1-matrix metalloproteinase (MT1-MMP), a membrane-tethered protease, is key for matrix breakdown during cancer invasion and metastasis. Assembly of branched actin networks by the Arp2/3 complex is required for MT1-MMP traffic and formation of matrix-degradative invadopodia. Contrasting with the well-established role of actin filament branching factor cortactin in invadopodia function during cancer cell invasion, the contribution of coronin-family debranching factors to invadopodia-based matrix remodeling is not known. Here, we investigated the contribution of coronin 1C to the invasive potential of breast cancer cells. We report that expression of coronin 1C is elevated in invasive human breast cancers, correlates positively with MT1-MMP expression in relation with increased metastatic risk and is a new independent prognostic factor in breast cancer. We provide evidence that, akin to cortactin, coronin 1C is required for invadopodia formation and matrix degradation by breast cancer cells lines and for 3D collagen invasion by multicellular spheroids. Using intravital imaging of orthotopic human breast tumor xenografts, we find that coronin 1C accumulates in structures forming in association with collagen fibrils in the tumor microenvironment. Moreover, we establish the role of coronin 1C in the regulation of positioning and trafficking of MT1-MMP-positive endolysosomes. These results identify coronin 1C as a novel player of the multi-faceted mechanism responsible for invadopodia formation, MT1-MMP surface exposure and invasiveness in breast cancer cells.

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References

  1. Rowe RG, Weiss SJ. Breaching the basement membrane: who, when and how? Trends Cell Biol. 2008;18:560–74.

    Article  CAS  Google Scholar 

  2. Lodillinsky C, Infante E, Guichard A, Chaligne R, Fuhrmann L, Cyrta J, et al. p63/MT1-MMP axis is required for in situ to invasive transition in basal-like breast cancer. Oncogene. 2016;35:344–57.

    Article  CAS  Google Scholar 

  3. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 2006;20:2673–86.

    Article  CAS  Google Scholar 

  4. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol. 2007;9:893–904.

    Article  CAS  Google Scholar 

  5. Linder S, Wiesner C, Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol. 2011;27:185–211.

    Article  CAS  Google Scholar 

  6. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 2006;66:3034–43.

    Article  CAS  Google Scholar 

  7. Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, Rottner K, et al. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol. 2008;18:926–31.

    Article  CAS  Google Scholar 

  8. Monteiro P, Rosse C, Castro-Castro A, Irondelle M, Lagoutte E, Paul-Gilloteaux P, et al. Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol. 2013;203:1063–79.

    Article  CAS  Google Scholar 

  9. Gligorijevic B, Bergman A, Condeelis J. Multiparametric classification links tumor microenvironments with tumor cell phenotype. PLoS Biol. 2014;12:e1001995.

    Article  Google Scholar 

  10. Leong HS, Robertson AE, Stoletov K, Leith SJ, Chin CA, Chien AE, et al. Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 2014;8:1558–70.

    Article  CAS  Google Scholar 

  11. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol. 2005;168:441–52.

    Article  CAS  Google Scholar 

  12. Ayala I, Baldassarre M, Giacchetti G, Caldieri G, Tete S, Luini A, et al. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci. 2008;121:369–78.

    Article  CAS  Google Scholar 

  13. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, et al. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol. 2001;11:370–4.

    Article  CAS  Google Scholar 

  14. Siton O, Ideses Y, Albeck S, Unger T, Bershadsky AD, Gov NS, et al. Cortactin releases the brakes in actin- based motility by enhancing WASP-VCA detachment from Arp2/3 branches. Curr Biol. 2011;21:2092–7.

    Article  CAS  Google Scholar 

  15. Cai L, Makhov AM, Schafer DA, Bear JE. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell. 2008;134:828–42.

    Article  CAS  Google Scholar 

  16. Chan KT, Creed SJ, Bear JE. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol. 2011;21:481–8.

    Article  CAS  Google Scholar 

  17. Abella JV, Galloni C, Pernier J, Barry DJ, Kjaer S, Carlier MF, et al. Isoform diversity in the Arp2/3 complex determines actin filament dynamics. Nat Cell Biol. 2016;18:76–86.

    Article  CAS  Google Scholar 

  18. Humphries CL, Balcer HI, D’Agostino JL, Winsor B, Drubin DG, Barnes G, et al. Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. J Cell Biol. 2002;159:993–1004.

    Article  CAS  Google Scholar 

  19. Foger N, Rangell L, Danilenko DM, Chan AC. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science. 2006;313:839–42.

    Article  Google Scholar 

  20. Clark ES, Weaver AM. A new role for cortactin in invadopodia: regulation of protease secretion. Eur J Cell Biol. 2008;87:581–90.

    Article  CAS  Google Scholar 

  21. Clark ES, Brown B, Whigham AS, Kochaishvili A, Yarbrough WG, Weaver AM. Aggressiveness of HNSCC tumors depends on expression levels of cortactin, a gene in the 11q13 amplicon. Oncogene. 2009;28:431–44.

    Article  CAS  Google Scholar 

  22. Mader CC, Oser M, Magalhaes MA, Bravo-Cordero JJ, Condeelis J, Koleske AJ, et al. An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res. 2011;71:1730–41.

    Article  CAS  Google Scholar 

  23. Rosse C, Lodillinsky C, Fuhrmann L, Nourieh M, Monteiro P, Irondelle M, et al. Control of MT1-MMP transport by atypical PKC during breast-cancer progression. Proc Natl Acad Sci USA. 2014;111:E1872–1879.

    Article  CAS  Google Scholar 

  24. Molinie N, Gautreau A. The Arp2/3 regulatory system and its deregulation in cancer. Physiol Rev. 2018;98:215–38.

    Article  Google Scholar 

  25. Wu L, Peng CW, Hou JX, Zhang YH, Chen C, Chen LD, et al. Coronin-1C is a novel biomarker for hepatocellular carcinoma invasive progression identified by proteomics analysis and clinical validation. J Exp Clin Cancer Res. 2010;29:17.

    Article  Google Scholar 

  26. Ren G, Tian Q, An Y, Feng B, Lu Y, Liang J, et al. Coronin 3 promotes gastric cancer metastasis via the up-regulation of MMP-9 and cathepsin K. Mol Cancer [Electron Resour]. 2012;11:67.

    Article  CAS  Google Scholar 

  27. Liu C, Zhang S, Wang Q, Zhang X. Tumor suppressor miR-1 inhibits tumor growth and metastasis by simultaneously targeting multiple genes. Oncotarget. 2017;8:42043–60.

    PubMed  PubMed Central  Google Scholar 

  28. Thal D, Xavier CP, Rosentreter A, Linder S, Friedrichs B, Waha A, et al. Expression of coronin-3 (coronin-1C) in diffuse gliomas is related to malignancy. J Pathol. 2008;214:415–24.

    Article  CAS  Google Scholar 

  29. Ziemann A, Hess S, Bhuwania R, Linder S, Kloppenburg P, Noegel AA, et al. CRN2 enhances the invasiveness of glioblastoma cells. Neuro Oncol. 2013;15:548–61.

    Article  CAS  Google Scholar 

  30. Hoshino D, Kirkbride KC, Costello K, Clark ES, Sinha S, Grega-Larson N, et al. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep. 2013;5:1159–68.

    Article  CAS  Google Scholar 

  31. Macpherson IR, Rainero E, Mitchell LE, van den Berghe PV, Speirs C, Dozynkiewicz MA, et al. CLIC3 controls recycling of late endosomal MT1-MMP and dictates invasion and metastasis in breast cancer. J Cell Sci. 2014;127:3893–901.

    Article  CAS  Google Scholar 

  32. Marchesin V, Castro-Castro A, Lodillinsky C, Castagnino A, Cyrta J, Bonsang-Kitzis H, et al. ARF6-JIP3/4 regulate endosomal tubules for MT1-MMP exocytosis in cancer invasion. J Cell Biol. 2015;211:339–58.

    Article  CAS  Google Scholar 

  33. Castro-Castro A, Marchesin V, Monteiro P, Lodillinsky C, Rosse C, Chavrier P. Cellular and molecular mechanisms of MT1-MMP-dependent cancer cell invasion. Annu Rev Cell Dev Biol. 2016;32:555–76.

    Article  CAS  Google Scholar 

  34. Gomez TS, Billadeau DD. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell. 2009;17:699–711.

    Article  CAS  Google Scholar 

  35. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell. 2009;17:712–23.

    Article  CAS  Google Scholar 

  36. Holtta-Vuori M, Vainio S, Kauppi M, Van Eck M, Jokitalo E, Ikonen E. Endosomal actin remodeling by coronin-1A controls lipoprotein uptake and degradation in macrophages. Circ Res. 2012;110:450–5.

    Article  Google Scholar 

  37. Kirkbride KC, Hong NH, French CL, Clark ES, Jerome WG, Weaver AM. Regulation of late endosomal/lysosomal maturation and trafficking by cortactin affects Golgi morphology. Cytoskelet (Hoboken). 2012;69:625–43.

    Article  CAS  Google Scholar 

  38. Sinha S, Hoshino D, Hong NH, Kirkbride KC, Grega-Larson NE, Seiki M, et al. Cortactin promotes exosome secretion by controlling branched actin dynamics. J Cell Biol. 2016;214:197–213.

    Article  CAS  Google Scholar 

  39. Smith SE, Mellor P, Ward AK, Kendall S, McDonald M, Vizeacoumar FS, et al. Molecular characterization of breast cancer cell lines through multiple omic approaches. Breast Cancer Res. 2017;19:65.

    Article  Google Scholar 

  40. Juin A, Billottet C, Moreau V, Destaing O, Albiges-Rizo C, Rosenbaum J, et al. Physiological type I collagen organization induces the formation of a novel class of linear invadosomes. Mol Biol Cell. 2012;23:297–309.

    Article  CAS  Google Scholar 

  41. Chan KT, Roadcap DW, Holoweckyj N, Bear JE. Coronin 1C harbours a second actin-binding site that confers co-operative binding to F-actin. Biochem J. 2012;444:89–96.

    Article  CAS  Google Scholar 

  42. Cai L, Makhov AM, Bear JE. F-actin binding is essential for coronin 1B function in vivo. J Cell Sci. 2007;120:1779–90.

    Article  CAS  Google Scholar 

  43. Behbod F, Kittrell FS, LaMarca H, Edwards D, Kerbawy S, Heestand JC, et al. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res. 2009;11:R66.

    Article  Google Scholar 

  44. Mukherjee S, Maxfield FR. Lipid and cholesterol trafficking in NPC. Biochim Biophys Acta. 2004;1685:28–37.

    Article  CAS  Google Scholar 

  45. Liscum L, Faust JR. The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J Biol Chem. 1989;264:11796–806.

    CAS  PubMed  Google Scholar 

  46. Wang J, Tsouko E, Jonsson P, Bergh J, Hartman J, Aydogdu E, et al. miR-206 inhibits cell migration through direct targeting of the actin-binding protein coronin 1C in triple-negative breast cancer. Mol Oncol. 2014;8:1690–702.

    Article  CAS  Google Scholar 

  47. McGowan PM, Duffy MJ. Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database. Ann Oncol. 2008;19:1566–72.

    Article  CAS  Google Scholar 

  48. Perentes JY, Kirkpatrick ND, Nagano S, Smith EY, Shaver CM, Sgroi D, et al. Cancer cell-associated MT1-MMP promotes blood vessel invasion and distant metastasis in triple-negative mammary tumors. Cancer Res. 2011;71:4527–38.

    Article  CAS  Google Scholar 

  49. Rosentreter A, Hofmann A, Xavier CP, Stumpf M, Noegel AA, Clemen CS. Coronin 3 involvement in F-actin-dependent processes at the cell cortex. Exp Cell Res. 2007;313:878–95.

    Article  CAS  Google Scholar 

  50. Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, et al. N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol. 2012;199:527–44.

    Article  CAS  Google Scholar 

  51. Cai L, Marshall TW, Uetrecht AC, Schafer DA, Bear JE. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell. 2007;128:915–29.

    Article  CAS  Google Scholar 

  52. Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, Ohno-Machado L, et al. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell. 2011;19:372–86.

    Article  CAS  Google Scholar 

  53. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, et al. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell. 2010;143:761–73.

    Article  CAS  Google Scholar 

  54. Gomez TS, Gorman JA, de Narvajas AA, Koenig AO, Billadeau DD. Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lysosomal networks. Mol Biol Cell. 2012;23:3215–28.

    Article  CAS  Google Scholar 

  55. Hong NH, Qi A, Weaver AM. PI(3,5)P2 controls endosomal branched actin dynamics by regulating cortactin-actin interactions. J Cell Biol. 2015;210:753–69.

    Article  CAS  Google Scholar 

  56. Willett R, Martina JA, Zewe JP, Wills R, Hammond GRV, Puertollano R. TFEB regulates lysosomal positioning by modulating TMEM55B expression and JIP4 recruitment to lysosomes. Nat Commun. 2017;8:1580.

    Article  Google Scholar 

  57. Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, et al. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol. 2008;181:985–98.

    Article  CAS  Google Scholar 

  58. Marchesin V, Montagnac G, Chavrier P. ARF6 promotes the formation of Rac1 and WAVE-dependent ventral F-actin rosettes in breast cancer cells in response to epidermal growth factor. PLoS One. 2015;10:e0121747.

    Article  Google Scholar 

  59. Sibarita JB. Deconvolution microscopy. Adv Biochem Eng Biotechnol. 2005;95:201–43.

    PubMed  Google Scholar 

  60. Lamprecht MR, Sabatini DM, Carpenter AE. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques. 2007;42:71–75.

    Article  CAS  Google Scholar 

  61. Castro-Castro A, Janke C, Montagnac G, Paul-Gilloteaux P, Chavrier P. ATAT1/MEC-17 acetyltransferase and HDAC6 deacetylase control a balance of acetylation of alpha-tubulin and cortactin and regulate MT1-MMP trafficking and breast tumor cell invasion. Eur J Cell Biol. 2012;91:950–60.

    Article  CAS  Google Scholar 

  62. Hurbain I, Romao M, Bergam P, Heiligenstein X, Raposo G. Analyzing lysosome-related organelles by electron microscopy. Methods Mol Biol. 2017;1594:43–71.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors greatly acknowledge the Breast Cancer Study Group and patients of Institut Curie for breast tumor samples. They thank the Cell and Tissue Imaging facility (PICT-IBiSA) and Nikon Imaging Centre, Institut Curie, member of the French National Research Infrastructure France-BioImaging (ANR10-INBS-04) for help with image acquisition and Dr Jakko van Rheenen for help with the mammary window and intravital imaging. AC was supported by a grant from Worldwide Cancer Research (Grant 16-1235 to PC), ACC by an EMBO Long Term postdoctoral fellowship and a grant from ‘Institut National du Cancer’ (INCA_6521 to PC), AG by INVADE grant from ITMO Cancer (Call Systems Biology 2012) to PC, SAG by a grant from INCa (INCa PLBIO14-161 to PC). and AAN and CSC by a grant from the German Research Foundation (DFG NO 113/22-2). The intravital imaging was supported by the Fondation pour la Recherche Médicale (FRM N° DGE20111123020), the Cancerople-IdF (n°2012-2-EML-04-IC-1), InCA (Cancer National Institute, n° 2011-1-LABEL-IC-4) and SiRIC (INCa-DGOS- 4654). This work was supported by grants from ‘Institut National du Cancer’ (INCa PLBIO14-161 and INCA_6521), Worldwide Cancer Research (Grant 16-1235) and ‘Equipe labellisée 2015’ from ‘Ligue Nationale contre le Cancer’ to PC.

Author contributions

AC carried out invadopodia formation and collagen degradation assays with the help of AZM and characterized the effects of CORO1C depletion on endolysosomal morphology and position. ACC who initiated the study, generated the cell lines stably expressing GFPCORO1C constructs and analyzed CORO1B and -1C expression in lysates of breast cancer cell lines provided by TD. LF and AVS generated the breast cancer TMA, performed CORO1C IHC labeling, and scored the breast tumor TMA for CORO1C expression with the help of CEK. SV and IB generated the invasive breast cancer cohort and performed RT-qPCR and multivariate analyses. MI performed multicellular spheroid invasion assays, analyzed the phenotype of cells silenced for cortactin, and performed intravital imaging. AG, CL, and SAG carried out mammary gland injections and analyzed tumor xenografts. MR and GR performed electron microscopy analyses. JEB, AAN, and CSC provided essential reagents. PC supervised the study and wrote the manuscript with contribution of all authors.

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Author notes

  1. These authors contributed equally: Alessia Castagnino and Antonio Castro-Castro.

Authors and Affiliations

  1. Institut Curie, PSL Research University, CNRS UMR144, Membrane and Cytoskeleton Dynamics group, 26 rue d’Ulm, F-75005, Paris, France

    Alessia Castagnino, Antonio Castro-Castro, Marie Irondelle, Alan Guichard, Catalina Lodillinsky, Sonia Agüera-González, Anna Zagryazhskaya-Masson & Philippe Chavrier

  2. Institut Curie, PSL Research University, Cell and Tissue Imaging Facility (PICT-IBiSA), 26 rue d’Ulm, F-75005, Paris, France

    Marie Irondelle

  3. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Oncología A. H. Roffo. Área de Investigación. San Martin 5481, Buenos Aires, C1417DTB, Argentina

    Catalina Lodillinsky

  4. Member of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Catalina Lodillinsky

  5. Institut Curie, PSL Research University, Pathology-Genetics-Immunology Department, 26 rue d’Ulm, F-75005, Paris, France

    Laetitia Fuhrmann, Carole El Kesrouani & Anne Vincent-Salomon

  6. Department of Genetics, Institut Curie, PSL Research University, Pharmacogenomic Unit, 26 rue d’Ulm, F-75005, Paris, France

    Sophie Vacher & Ivan Bièche

  7. Institut Curie, PSL Research University, CNRS UMR144, Biogenesis and Functions of Lysosome-Related Organelles group, 26 rue d’Ulm, F-75005, Paris, France

    Maryse Romao & Graça Raposo

  8. Center for Biochemistry, Institute of Biochemistry I, Medical Faculty, University of Cologne, Joseph-Stelzmann-Str. 52, 50931, Cologne, Germany

    Angelika A. Noegel & Christoph S. Clemen

  9. Institut Curie, PSL Research University, Translational Research Department, Breast Cancer Biology Group, Paris, France

    Thierry Dubois

  10. UNC Lineberger Comprehensive Cancer Center and the Department of Cell Biology and Physiology, The University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    James E. Bear

  11. Department of Neurology, Heimer Institute for Muscle Research, University Hospital Bergmannsheil, Ruhr-University Bochum, Bürkle-de-la-Camp-Platz 1, 44789, Bochum, Germany

    Christoph S. Clemen

  12. EA7331, Paris Descartes University, Sorbonne Paris Cité, Faculty of Pharmaceutical and Biological Sciences, 4 avenue de l’observatoire, F-75006, Paris, France

    Ivan Bièche

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  1. Alessia Castagnino
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Correspondence to Philippe Chavrier.

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Castagnino, A., Castro-Castro, A., Irondelle, M. et al. Coronin 1C promotes triple-negative breast cancer invasiveness through regulation of MT1-MMP traffic and invadopodia function. Oncogene 37, 6425–6441 (2018). https://doi.org/10.1038/s41388-018-0422-x

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