Epha2 cleavage by MT1-MMP triggers single cancer cell invasion via homotypic cell repulsion

Journal of Cell Biology

Volumn 201, Issue 3, 2013, Pages 467-484

  Sugiyama, Nami ^a   Gucciardo, Erika ^a   Tatti, Olga ^a   Varjosalo, Markku ^b,c   Hyytiäinen, Marko ^a   Gstaiger, Matthias ^b   Lehti, Kaisa ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR A2; FIBRONECTIN; MATRIX METALLOPROTEINASE 14; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CARCINOMA CELL; CELL DISRUPTION; CELL INVASION; CELL JUNCTION; CELL SURFACE; CONTROLLED STUDY; FEMALE; HOMOTYPIC CELL REPULSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL SHAPE; COLLAGEN; FEMALE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYMPHATIC METASTASIS; MATRIX METALLOPROTEINASE 14; MICE; MICE, SCID; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTOR, EPHA2; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SINGLE-CELL ANALYSIS; TIME-LAPSE IMAGING; TISSUE ARRAY ANALYSIS;

EID: 84877626308     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201205176     Document Type: Article

References (52)

1. Alexander, S., and P. Friedl. 2012. Cancer invasion and resistance: intercon-nected processes of disease progression and therapy failure. Trends Mol. Med. 18:13-26. http://dx.doi.org/10.1016/j.molmed.2011.11.003
2. Astin, J.W., J. Batson, S. Kadir, J. Charlet, R.A. Persad, D. Gillatt, J.D. Oxley, and C.D. Nobes. 2010. Competition amongst Eph receptors regulates contact inhibition of locomotion and invasiveness in prostate cancer cells. Nat. Cell Biol. 12:1194-1204. http://dx.doi.org/10.1038/ncb2122
3. Barbolina, M.V., B.P. Adley, E.V. Ariztia, Y. Liu, and M.S. Stack. 2007. Microenvironmental regulation of membrane type 1 matrix metallopro-teinase activity in ovarian carcinoma cells via collagen-induced EGR1 expression. J. Biol. Chem. 282:4924-4931. http://dx.doi.org/10.1074/ jbc.M608428200
4. Blobel, C.P. 2005. ADAMs: key components in EGFR signalling and de-velopment. Nat. Rev. Mol. Cell Biol. 6:32-43. http://dx.doi.org/10.1038/nrm1548
5. Brantley-Sieders, D.M. 2012. Clinical relevance of Ephs and ephrins in cancer: lessons from breast, colorectal, and lung cancer profiling. Semin. Cell Dev. Biol. 23:102-108. http://dx.doi.org/10.1016/j.semcdb.2011.10.014
6. Brantley-Sieders, D.M., A. Jiang, K. Sarma, A. Badu-Nkansah, D.L. Walter, Y. Shyr, and J. Chen. 2011. Eph/ephrin profiling in human breast can-cer reveals significant associations between expression level and clini-cal outcome. PLoS ONE. 6:e24426. http://dx.doi.org/10.1371/journal.pone.0024426
7. Chan, K.M., H.L. Wong, G. Jin, B. Liu, R. Cao, Y. Cao, K. Lehti, K. Tryggvason, and Z. Zhou. 2012. MT1-MMP inactivates ADAM9 to regulate FGFR2 signaling and calvarial osteogenesis. Dev. Cell. 22:1176-1190. http:// dx.doi.org/10.1016/j.devcel.2012.04.014
8. Egeblad, M., M.G. Rasch, and V.M. Weaver. 2010. Dynamic interplay be-tween the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22:697-706. http://dx.doi.org/10.1016/j.ceb.2010.08.015
9. Faoro, L., P.A. Singleton, G.M. Cervantes, F.E. Lennon, N.W. Choong, R. Kanteti, B.D. Ferguson, A.N. Husain, M.S. Tretiakova, N. Ramnath, et al. 2010. EphA2 mutation in lung squamous cell carcinoma promotes increased cell survival, cell invasion, focal adhesions, and mammalian target of rapamycin activation. J. Biol. Chem. 285:18575-18585. http:// dx.doi.org/10.1074/jbc.M109.075085
10. Friedl, P., and K. Wolf. 2010. Plasticity of cell migration: a multiscale tun-ing model. J. Cell Biol. 188:11-19. http://dx.doi.org/10.1083/jcb.200909003
11. Giampieri, S., C. Manning, S. Hooper, L. Jones, C.S. Hill, and E. Sahai. 2009. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell Biol. 11:1287-1296. http://dx.doi.org/10.1038/ncb1973
12. Giampieri, S., S. Pinner, and E. Sahai. 2010. Intravital imaging illuminates transforming growth factor beta signaling switches during metasta-sis. Cancer Res. 70:3435-3439. http://dx.doi.org/10.1158/0008-5472. CAN-10-0466
13. Harunaga, J.S., and K.M. Yamada. 2011. Cell-matrix adhesions in 3D. Matrix Biol. 30:363-368. http://dx.doi.org/10.1016/j.matbio.2011.06.001
14. Himanen, J.P., N. Saha, and D.B. Nikolov. 2007. Cell-cell signaling via Eph receptors and ephrins. Curr. Opin. Cell Biol. 19:534-542. http://dx.doi.org/10.1016/j.ceb.2007.08.004
15. Himanen, J.P., L. Yermekbayeva, P.W. Janes, J.R. Walker, K. Xu, L. Atapattu, K.R. Rajashankar, A. Mensinga, M. Lackmann, D.B. Nikolov, and S. Dhe-Paganon. 2010. Architecture of Eph receptor clusters. Proc. Natl. Acad. Sci. USA. 107:10860-10865. http://dx.doi.org/10.1073/pnas.1004148107
16. Hiramoto-Yamaki, N., S. Takeuchi, S. Ueda, K. Harada, S. Fujimoto, M. Negishi, and H. Katoh. 2010. Ephexin4 and EphA2 mediate cell migration through a RhoG-dependent mechanism. J. Cell Biol. 190:461-477. http://dx.doi.org/10.1083/jcb.201005141
17. Hotary, K.B., E.D. Allen, P.C. Brooks, N.S. Datta, M.W. Long, and S.J. Weiss. 2003. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell. 114:33-45. http://dx.doi.org/10.1016/S0092-8674(03)00513-0
18. Itoh, Y., and M. Seiki. 2006. MT1-MMP: a potent modifier of pericellu-lar microenvironment. J. Cell. Physiol. 206:1-8. http://dx.doi.org/ 10.1002/jcp.20431
19. Janes, P.W., N. Saha, W.A. Barton, M.V. Kolev, S.H. Wimmer-Kleikamp, E. Nievergall, C.P. Blobel, J.P. Himanen, M. Lackmann, and D.B. Nikolov. 2005. Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell. 123:291-304. http://dx.doi.org/10.1016/j.cell.2005.08.014
20. Janes, P.W., E. Nievergall, and M. Lackmann. 2012. Concepts and conse-quences of Eph receptor clustering. Semin. Cell Dev. Biol. 23:43-50. http://dx.doi.org/10.1016/j.semcdb.2012.01.001
21. Lehti, K., J. Lohi, M.M. Juntunen, D. Pei, and J. Keski-Oja. 2002. Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J. Biol. Chem. 277:8440-8448. http://dx.doi.org/10.1074/jbc.M109128200
22. Lehti, K., E. Allen, H. Birkedal-Hansen, K. Holmbeck, Y. Miyake, T.H. Chun, and S.J. Weiss. 2005. An MT1-MMP-PDGF receptor-beta axis regulates mural cell investment of the microvasculature. Genes Dev. 19:979-991. http://dx.doi.org/10.1101/gad.1294605
23. Lehti, K., N.F. Rose, S. Valavaara, S.J. Weiss, and J. Keski-Oja. 2009. MT1-MMP promotes vascular smooth muscle dedifferentiation through LRP1 pro-cessing. J. Cell Sci. 122:126-135. http://dx.doi.org/10.1242/jcs.035279
24. Li, X.Y., I. Ota, I. Yana, F. Sabeh, and S.J. Weiss. 2008. Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol. Biol. Cell. 19:3221-3233. http:// dx.doi.org/10.1091/mbc.E08-01-0016
25. Macrae, M., R.M. Neve, P. Rodriguez-Viciana, C. Haqq, J. Yeh, C. Chen, J.W. Gray, and F. McCormick. 2005. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell. 8:111-118. http://dx.doi.org/10.1016/j.ccr.2005.07.005
26. Margaryan, N.V., L. Strizzi, D.E. Abbott, E.A. Seftor, M.S. Rao, M.J. Hendrix, and A.R. Hess. 2009. EphA2 as a promoter of melanoma tumorigenicity. Cancer Biol. Ther. 8:279-288. http://dx.doi.org/10.4161/cbt.8.3.7485
27. Miao, H., and B. Wang. 2012. EphA receptor signaling-complexity and emerging themes. Semin. Cell Dev. Biol. 23:16-25. http://dx.doi.org/10.1016/j.semcdb.2011.10.013
28. Miao, H., D.Q. Li, A. Mukherjee, H. Guo, A. Petty, J. Cutter, J.P. Basilion, J. Sedor, J. Wu, D. Danielpour, et al. 2009. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and inva-sion via a reciprocal regulatory loop with Akt. Cancer Cell. 16:9-20. http://dx.doi.org/10.1016/j.ccr.2009.04.009
29. Miura, K., J.M. Nam, C. Kojima, N. Mochizuki, and H. Sabe. 2009. EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol. Biol. Cell. 20:1949-1959. http://dx.doi.org/10.1091/mbc.E08-06-0549
30. Neve, R.M., K. Chin, J. Fridlyand, J. Yeh, F.L. Baehner, T. Fevr, L. Clark, N. Bayani, J.P. Coppe, F. Tong, et al. 2006. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 10:515-527. http://dx.doi.org/10.1016/j.ccr.2006.10.008
31. Nievergall, E., M. Lackmann, and P.W. Janes. 2012. Eph-dependent cell-cell adhesion and segregation in development and cancer. Cell. Mol. Life Sci. 69:1813-1842. http://dx.doi.org/10.1007/s00018-011-0900-6
32. Nyalendo, C., M. Michaud, E. Beaulieu, C. Roghi, G. Murphy, D. Gingras, and R. Béliveau. 2007. Src-dependent phosphorylation of membrane type I matrix metalloproteinase on cytoplasmic tyrosine 573: role in endothelial and tumor cell migration. J. Biol. Chem. 282:15690-15699. http://dx.doi.org/10.1074/jbc.M608045200
33. Okada, A., J.P. Bellocq, N. Rouyer, M.P. Chenard, M.C. Rio, P. Chambon, and P. Basset. 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. USA. 92:2730-2734. http://dx.doi.org/10.1073/pnas.92.7.2730
34. Ota, I., X.Y. Li, Y. Hu, and S.J. Weiss. 2009. Induction of a MT1-MMP and MT2-MMP-dependent basement membrane transmigration program in cancer cells by Snail1. Proc. Natl. Acad. Sci. USA. 106:20318-20323. http://dx.doi.org/10.1073/pnas.0910962106
35. Paddock, S.W., and G.A. Dunn. 1986. Analysing collisions between fibroblasts and fibrosarcoma cells: fibrosarcoma cells show an active invasionary response. J. Cell Sci. 81:163-187.
36. Parri, M., M.L. Taddei, F. Bianchini, L. Calorini, and P. Chiarugi. 2009. EphA2 reexpression prompts invasion of melanoma cells shifting from mes-enchymal to amoeboid-like motility style. Cancer Res. 69:2072-2081. http://dx.doi.org/10.1158/0008-5472.CAN-08-1845
37. Pasquale, E.B. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6:462-475. http://dx.doi.org/10.1038/nrm1662
38. Pasquale, E.B. 2008. Eph-ephrin bidirectional signaling in physiology and dis-ease. Cell. 133:38-52. http://dx.doi.org/10.1016/j.cell.2008.03.011
39. Sabeh, F., R. Shimizu-Hirota, and S.J. Weiss. 2009. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoe-boid movement revisited. J. Cell Biol. 185:11-19. http://dx.doi.org/ 10.1083/jcb.200807195
40. Sanz-Moreno, V., and C.J. Marshall. 2010. The plasticity of cytoskeletal dynam-ics underlying neoplastic cell migration. Curr. Opin. Cell Biol. 22:690-696. http://dx.doi.org/10.1016/j.ceb.2010.08.020
41. Seiradake, E., K. Harlos, G. Sutton, A.R. Aricescu, and E.Y. Jones. 2010. An extracellular steric seeding mechanism for Eph-ephrin signaling plat-form assembly. Nat. Struct. Mol. Biol. 17:398-402. http://dx.doi.org/ 10.1038/nsmb.1782
42. Sugiyama, N., M. Varjosalo, P. Meller, J. Lohi, K.M. Chan, Z. Zhou, K. Alitalo, J. Taipale, J. Keski-Oja, and K. Lehti. 2010a. FGF receptor-4 (FGFR4) polymorphism acts as an activity switch of a membrane type 1 matrix metalloproteinase-FGFR4 complex. Proc. Natl. Acad. Sci. USA. 107:15786-15791. http://dx.doi.org/10.1073/pnas.0914459107
43. Sugiyama, N., M. Varjosalo, P. Meller, J. Lohi, M. Hyytiäinen, S. Kilpinen, O. Kallioniemi, S. Ingvarsen, L.H. Engelholm, J. Taipale, et al. 2010b. Fibroblast growth factor receptor 4 regulates tumor invasion by coupling fi-broblast growth factor signaling to extracellular matrix degradation. Cancer Res. 70:7851-7861. http://dx.doi.org/10.1158/0008-5472.CAN-10-1223
44. Szabova, L., S.S. Yamada, H. Birkedal-Hansen, and K. Holmbeck. 2005. Expression pattern of four membrane-type matrix metalloproteinases in the normal and diseased mouse mammary gland. J. Cell. Physiol. 205:123-132. http://dx.doi.org/10.1002/jcp.20385
45. Taddei, M.L., M. Parri, A. Angelucci, F. Bianchini, C. Marconi, E. Giannoni, G. Raugei, M. Bologna, L. Calorini, and P. Chiarugi. 2011. EphA2 induces metastatic growth regulating amoeboid motility and clonogenic potential in prostate carcinoma cells. Mol. Cancer Res. 9:149-160. http://dx.doi.org/10.1158/1541-7786.MCR-10-0298
46. Tatti, O., P. Vehviläinen, K. Lehti, and J. Keski-Oja. 2008. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteo-lytic processing of LTBP-1. Exp. Cell Res. 314:2501-2514. http://dx.doi.org/10.1016/j.yexcr.2008.05.018
47. Varjosalo, M., M. Björklund, F. Cheng, H. Syvänen, T. Kivioja, S. Kilpinen, Z. Sun, O. Kallioniemi, H.G. Stunnenberg, W.W. He, et al. 2008. Application of active and kinase-deficient kinome collection for identification of ki-nases regulating hedgehog signaling. Cell. 133:537-548. http://dx.doi.org/10.1016/j.cell.2008.02.047
48. Wolf, K., and P. Friedl. 2011. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21:736-744. http:// dx.doi.org/10.1016/j.tcb.2011.09.006
49. Wykosky, J., and W. Debinski. 2008. The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting. Mol. Cancer Res. 6:1795-1806. http://dx.doi.org/10.1158/1541-7786.MCR-08-0244
50. Wykosky, J., D.M. Gibo, C. Stanton, and W. Debinski. 2005. EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol. Cancer Res. 3:541-551. http://dx.doi.org/10.1158/1541-7786.MCR-05-0056
51. Yilmaz, M., and G. Christofori. 2010. Mechanisms of motility in metastasizing cells. Mol. Cancer Res. 8:629-642. http://dx.doi.org/10.1158/1541-7786. MCR-10-0139
52. Zantek, N.D., M. Azimi, M. Fedor-Chaiken, B. Wang, R. Brackenbury, and M.S. Kinch. 1999. E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ. 10:629-638.