Vimentin intermediate filament and plectin provide a scaffold for invadopodia, facilitating cancer cell invasion and extravasation for metastasis

European Journal of Cell Biology

Volumn 93, Issue 4, 2014, Pages 157-169

  Sutoh Yoneyama, Mihoko ^a   Hatakeyama, Shingo ^a   Habuchi, Tomonori ^b   Inoue, Takamitsu ^b   Nakamura, Toshiya ^c   Funyu, Tomihisa ^d   Wiche, Gerhard ^e   Ohyama, Chikara ^a   Tsuboi, Shigeru ^a,d  

^a HIROSAKI UNIVERSITY   (Japan)

^b AKITA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HIROSAKI UNIVERSITY   (Japan)

^d Oyokyo Kidney Research Institute   (Japan)

^e UNIVERSITY OF VIENNA   (Austria)

Author keywords

Cancer cell extravasation; Invadopodium; Invadosome; Invasion; Plectin; Vimentin

Indexed keywords

PLECTIN; VIMENTIN; ACTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER CANCER CELL LINE; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; DEGRADATION; DNA MICROARRAY; EXTRACELLULAR MATRIX; EXTRAVASATION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BLADDER TUMOR; CELL MOTION; CYTOSKELETON; GENETICS; INTERMEDIATE FILAMENT; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; SECONDARY; TUMOR CELL LINE; TUMOR INVASION;

ACTINS; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CYTOSKELETON; GENE EXPRESSION PROFILING; HUMANS; INTERMEDIATE FILAMENTS; LUNG NEOPLASMS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; PLECTIN; URINARY BLADDER NEOPLASMS; VIMENTIN;

EID: 84902319614     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2014.03.002     Document Type: Article

References (58)

1. Amin M.B. Histological variants of urothelial carcinoma: diagnostic, therapeutic and prognostic implications. Mod. Pathol. 2009, 22(Suppl. 2):S96-S118.
2. Ayala I., Baldassarre M., Giacchetti G., Caldieri G., Tete S., Luini A., Buccione R. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J. Cell Sci. 2008, 121:369-378.
3. Bausch D., Thomas S., Mino-Kenudson M., Fernandez-del C.C., Bauer T.W., Williams M., Warshaw A.L., Thayer S.P., Kelly K.A. Plectin-1 as a novel biomarker for pancreatic cancer. Clin. Cancer Res. 2011, 17:302-309.
4. Blouw B., Seals D.F., Pass I., Diaz B., Courtneidge S.A. A role for the podosome/invadopodia scaffold protein Tks5 in tumor growth in vivo. Eur. J. Cell Biol. 2008, 87:555-567.
5. Brown M.J., Hallam J.A., Liu Y., Yamada K.M., Shaw S. Cutting edge: integration of human T lymphocyte cytoskeleton by the cytolinker plectin. J. Immunol. 2001, 167:641-645.
6. Buccione R., Caldieri G., Ayala I. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev. 2009, 28:137-149.
7. Burgstaller G., Gregor M., Winter L., Wiche G. Keeping the vimentin network under control: cell-matrix adhesion-associated plectin 1f affects cell shape and polarity of fibroblasts. Mol. Biol. Cell 2010, 21:3362-3375.
8. Carman C.V., Sage P.T., Sciuto T.E., de la Fuente M.A., Geha R.S., Ochs H.D., Dvorak H.F., Dvorak A.M., Springer T.A. Transcellular diapedesis is initiated by invasive podosomes. Immunity 2007, 26:784-797.
9. Carman C.V., Springer T.A. Trans-cellular migration: cell-cell contacts get intimate. Curr. Opin. Cell Biol. 2008, 20:533-540.
10. Chang L., Barlan K., Chou Y.H., Grin B., Lakonishok M., Serpinskaya A.S., Shumaker D.K., Herrmann H., Gelfand V.I., Goldman R.D. The dynamic properties of intermediate filaments during organelle transport. J. Cell Sci. 2009, 122:2914-2923.
11. Clark E.A., Golub T.R., Lander E.S., Hynes R.O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 2000, 406:532-535.
12. Drake J.M., Strohbehn G., Bair T.B., Moreland J.G., Henry M.D. ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol. Biol. Cell 2009, 20:2207-2217.
13. Eckert M.A., Lwin T.M., Chang A.T., Kim J., Danis E., Ohno-Machado L., Yang J. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 2011, 19:372-386.
14. Even-Ram S., Yamada K.M. Cell migration in 3D matrix. Curr. Opin. Cell Biol. 2005, 17:524-532.
15. Favre B., Schneider Y., Lingasamy P., Bouameur J.E., Begre N., Gontier Y., Steiner-Champliaud M.F., Frias M.A., Borradori L., Fontao L. Plectin interacts with the rod domain of type III intermediate filament proteins desmin and vimentin. Eur. J. Cell Biol. 2011, 90:390-400.
16. Garcia-Alvarez B., Bobkov A., Sonnenberg A., de Pereda J.M. Structural and functional analysis of the actin binding domain of plectin suggests alternative mechanisms for binding to F-actin and integrin beta4. Structure 2003, 11:615-625.
17. Garcia E., Jones G.E., Machesky L.M., Anton I.M. WIP: WASP-interacting proteins at invadopodia and podosomes. Eur. J. Cell Biol. 2012, 91:869-877.
18. Geerts D., Fontao L., Nievers M.G., Schaapveld R.Q., Purkis P.E., Wheeler G.N., Lane E.B., Leigh I.M., Sonnenberg A. Binding of integrin alpha6beta4 to plectin prevents plectin association with F-actin but does not interfere with intermediate filament binding. J. Cell Biol. 1999, 147:417-434.
19. Gligorijevic B., Wyckoff J., Yamaguchi H., Wang Y., Roussos E.T., Condeelis J. N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. J. Cell Sci. 2012, 125:724-734.
20. Gupta G.P., Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
21. Hatakeyama S., Yamamoto H., Ohyama C. Tumor formation assays. Methods Enzymol. 2010, 479:397-411.
22. Hay E.D. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 2005, 233:706-720.
23. Hisazumi H., Uchibayashi T., Katoh M., Kobayashi T., Nakajima K., Naitoh K., Misaki T., Kuroda K. Anticancer drug sensitivity in vitro in the bladder cancer cell line, KK-47 and prophylactic use of carbazilquinone and urokinase in bladder cancer. Urol. Res. 1981, 9:231-235.
24. Hugo H., Ackland M.L., Blick T., Lawrence M.G., Clements J.A., Williams E.D., Thompson E.W. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J. Cell Physiol. 2007, 213:374-383.
25. Ivaska J., Pallari H.M., Nevo J., Eriksson J.E. Novel functions of vimentin in cell adhesion, migration, and signaling. Exp. Cell Res. 2007, 313:2050-2062.
26. Jaffe A.B., Hall A. Rho GTPases in transformation and metastasis. Adv. Cancer Res. 2002, 84:57-80.
27. Katada K., Tomonaga T., Satoh M., Matsushita K., Tonoike Y., Kodera Y., Hanazawa T., Nomura F., Okamoto Y. Plectin promotes migration and invasion of cancer cells and is a novel prognostic marker for head and neck squamous cell carcinoma. J. Proteomics 2012, 75:1803-1815.
28. Kayajima T., Shirahama T., Yanase I., Ohi Y. Characterization of a new cell line established from a human urinary-bladder cancer, with special reference to metastatic ability to the lung. Jpn. J. Urol. Surg. 1989, 2:577-580.
29. Kidd M.E., Shumaker D.K., Ridge K.M. The role of vimentin intermediate filaments in the progression of lung cancer. Am. J. Respir. Cell Mol. Biol. 2014, 50:1-6.
30. Kokkinos M.I., Wafai R., Wong M.K., Newgreen D.F., Thompson E.W., Waltham M. Vimentin and epithelial-mesenchymal transition in human breast cancer - observations in vitro and in vivo. Cells Tissues Organs 2007, 185:191-203.
31. Koster J., van Wilpe S., Kuikman I., Litjens S.H., Sonnenberg A. Role of binding of plectin to the integrin beta4 subunit in the assembly of hemidesmosomes. Mol. Biol. Cell 2004, 15:1211-1223.
32. Kubota Y., Nakada T., Yanai H., Kakizaki H., Sasagawa I., Watanabe M. Electropermeabilization in bladder cancer chemotherapy. Cancer Chemother. Pharmacol. 1996, 39:67-70.
33. Kural C., Serpinskaya A.S., Chou Y.H., Goldman R.D., Gelfand V.I., Selvin P.R. Tracking melanosomes inside a cell to study molecular motors and their interaction. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5378-5382.
34. Lang S.H., Hyde C., Reid I.N., Hitchcock I.S., Hart C.A., Bryden A.A., Villette J.M., Stower M.J., Maitland N.J. Enhanced expression of vimentin in motile prostate cell lines and in poorly differentiated and metastatic prostate carcinoma. Prostate 2002, 52:253-263.
35. Linder S. Invadosomes at a glance. J. Cell Sci. 2009, 122:3009-3013.
36. Linder S., Nelson D., Weiss M., Aepfelbacher M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9648-9653.
37. Litjens S.H., de Pereda J.M., Sonnenberg A. Current insights into the formation and breakdown of hemidesmosomes. Trends Cell Biol. 2006, 16:376-383.
38. McInroy L., Määttä A. Plectin regulates invasiveness of SW480 colon carcinoma cells and is targeted to podosome-like adhesions in an isoform-specific manner. Exp. Cell Res. 2011, 317:2468-2478.
39. McLean W.H., Pulkkinen L., Smith F.J., Rugg E.L., Lane E.B., Bullrich F., Burgeson R.E., Amano S., Hudson D.L., Owaribe K., McGrath J.A., McMillan J.R., Eady R.A., Leigh I.M., Christiano A.M., Uitto J. Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organization. Genes Dev. 1996, 10:1724-1735.
40. Mendez M.G., Kojima S., Goldman R.D. Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J. 2010, 24:1838-1851.
41. Murphy D.A., Courtneidge S.A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 2011, 12:413-426.
42. Oser M., Yamaguchi H., Mader C.C., Bravo-Cordero J.J., Arias M., Chen X., Desmarais V., van Rheenen J., Koleske A.J., Condeelis J. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 2009, 186:571-587.
43. Quintavalle M., Elia L., Condorelli G., Courtneidge S.A. MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J. Cell Biol. 2010, 189:13-22.
44. Rezniczek G.A., Abrahamsberg C., Fuchs P., Spazierer D., Wiche G. Plectin 5'-transcript diversity: short alternative sequences determine stability of gene products, initiation of translation and subcellular localization of isoforms. Hum. Mol. Genet. 2003, 12:3181-3194.
45. Satelli A., Li S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell. Mol. Life Sci. 2011, 68:3033-3046.
46. Schoumacher M., Goldman R.D., Louvard D., Vignjevic D.M. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 2010, 189:541-556.
47. Seals D.F., Azucena E.F., Pass I., Tesfay L., Gordon R., Woodrow M., Resau J.H., Courtneidge S.A. The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 2005, 7:155-165.
48. Smith S.C., Nicholson B., Nitz M., Frierson H.F., Smolkin M., Hampton G., El-Rifai W., Theodorescu D. Profiling bladder cancer organ site-specific metastasis identifies LAMC2 as a novel biomarker of hematogenous dissemination. Am. J. Pathol. 2009, 174:371-379.
49. Sugiyama N., Yoneyama M.S., Hatakeyama S., Yamamoto H., Okamoto A., Koie T., Saitoh H., Yamaya K., Funyu T., Inoue T., Habuchi T., Ohyama C., Tsuboi S. In vivo selection of high-metastatic subline of bladder cancer cell and its characterization. Oncol. Res. 2013, 20:289-295.
50. Sutoh M., Hashimoto Y., Yoneyama T., Yamamoto H., Hatakeyama S., Koie T., Okamoto A., Yamaya K., Saitoh H., Funyu T., Nakamura T., Sato T., Ohyama C., Tsuboi S. Invadopodia formation by bladder tumor cells. Oncol. Res. 2010, 19:85-92.
51. Takkunen M., Grenman R., Hukkanen M., Korhonen M., Garcia de Herreros A., Virtanen I. Snail-dependent and -independent epithelial-mesenchymal transition in oral squamous carcinoma cells. J. Histochem. Cytochem. 2006, 54:1263-1275.
52. Tokui N., Yoneyama M.S., Hatakeyama S., Yamamoto H., Koie T., Saitoh H., Yamaya K., Funyu T., Nakamura T., Ohyama C., Tsuboi S. Extravasation during bladder cancer metastasis requires cortactinmediated invadopodia formation. Mol. Med. Rep. 2014, 9:1142-1146.
53. Tsuboi S., Sutoh M., Hatakeyama S., Hiraoka N., Habuchi T., Horikawa Y., Hashimoto Y., Yoneyama T., Mori K., Koie T., Nakamura T., Saitoh H., Yamaya K., Funyu T., Fukuda M., Ohyama C. A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans. EMBO J. 2011, 30:3173-3185.
54. Weaver A.M. Cortactin in tumor invasiveness. Cancer Lett. 2008, 265:157-166.
55. Whipple R.A., Balzer E.M., Cho E.H., Matrone M.A., Yoon J.R., Martin S.S. Vimentin filaments support extension of tubulin-based microtentacles in detached breast tumor cells. Cancer Res. 2008, 68:5678-5688.
56. Wiche G., Winter L. Plectin isoforms as organizers of intermediate filament cytoarchitecture. Bioarchitecture 2011, 1:14-20.
57. Winter L., Wiche G. The many faces of plectin and plectinopathies: pathology and mechanisms. Acta Neuropathol. (Berl.) 2013, 125:77-93.
58. Yamamoto H., Sutoh M., Hatakeyama S., Hashimoto Y., Yoneyama T., Koie T., Saitoh H., Yamaya K., Funyu T., Nakamura T., Ohyama C., Tsuboi S. Requirement for FBP17 in invadopodia formation by invasive bladder tumor cells. J. Urol. 2011, 185:1930-1938.