Intermediate filaments and the regulation of focal adhesion

Current Opinion in Cell Biology

Volumn 32, Issue , 2015, Pages 13-20

  Leube, Rudolf E ^a   Moch, Marcin ^a   Windoffer, Reinhard ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; EXTRACELLULAR MATRIX; FOCAL ADHESION; INTERMEDIATE FILAMENT; MESENCHYME CELL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; CYTOSKELETON; HUMAN; METABOLISM;

ANIMALS; CELL ADHESION; CYTOSKELETON; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HUMANS; INTERMEDIATE FILAMENTS;

EID: 84908128597     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.09.011     Document Type: Review

References (67)

1. Gardel M.L., Schneider I.C., Aratyn-Schaus Y., Waterman C.M. Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol 2010, 26:315-333.
2. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2010, 11:633-643.
3. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nat Cell Biol 2007, 9:858-867.
4. Felkl M., Tomas K., Smid M., Mattes J., Windoffer R., Leube R.E. Monitoring the cytoskeletal EGF response in live gastric carcinoma cells. PLoS One 2012, 7:e45280.
5. 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.
6. Capetanaki Y., Bloch R.J., Kouloumenta A., Mavroidis M., Psarras S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp Cell Res 2007, 313:2063-2076.
7. Pavenstadt H., Kriz W., Kretzler M. Cell biology of the glomerular podocyte. Physiol Rev 2003, 83:253-307.
8. Gad A., Lach S., Crimaldi L., Gimona M. Plectin deposition at podosome rings requires myosin contractility. Cell Motil Cytoskeleton 2008, 65:614-625.
9. Olbrich L., Foehring D., Happel P., Brand-Saberi B., Theiss C. Fast rearrangement of the neuronal growth cone's actin cytoskeleton following VEGF stimulation. Histochem Cell Biol 2013, 139:431-445.
10. Correia I., Chu D., Chou Y.H., Goldman R.D., Matsudaira P. Integrating the actin and vimentin cytoskeletons. Adhesion-dependent formation of fimbrin-vimentin complexes in macrophages. J Cell Biol 1999, 146:831-842.
11. 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.
12. 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.
13. Kreis S., Schonfeld H.J., Melchior C., Steiner B., Kieffer N. The intermediate filament protein vimentin binds specifically to a recombinant integrin alpha2/beta1 cytoplasmic tail complex and co-localizes with native alpha2/beta1 in endothelial cell focal adhesions. Exp Cell Res 2005, 305:110-121.
14. 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.
15. Ivaska J., Vuoriluoto K., Huovinen T., Izawa I., Inagaki M., Parker P.J. PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J 2005, 24:3834-3845.
16. Kim H., McCulloch C.A. Filamin A mediates interactions between cytoskeletal proteins that control cell adhesion. FEBS Lett 2011, 585:18-22.
17. Kim H., Nakamura F., Lee W., Shifrin Y., Arora P., McCulloch C.A. Filamin A is required for vimentin-mediated cell adhesion and spreading. Am J Physiol Cell Physiol 2010, 298:C221-C236.
18. Kim H., Nakamura F., Lee W., Hong C., Perez-Sala D., McCulloch C.A. Regulation of cell adhesion to collagen via beta1 integrins is dependent on interactions of filamin A with vimentin and protein kinase C epsilon. Exp Cell Res 2010, 316:1829-1844.
19. Khanamiryan L., Li Z., Paulin D., Xue Z. Self-assembly incompetence of synemin is related to the property of its head and rod domains. Biochemistry 2008, 47:9531-9539.
20. Uyama N., Zhao L., Van Rossen E., Hirako Y., Reynaert H., Adams D.H., Xue Z., Li Z., Robson R., Pekny M., et al. Hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions. Gut 2006, 55:1276-1289.
21. Sun N., Critchley D.R., Paulin D., Li Z., Robson R.M. Identification of a repeated domain within mammalian alpha-synemin that interacts directly with talin. Exp Cell Res 2008, 314:1839-1849.
22. Sun N., Critchley D.R., Paulin D., Li Z., Robson R.M. Human alpha-synemin interacts directly with vinculin and metavinculin. Biochem J 2008, 409:657-667.
23. Hijikata T., Nakamura A., Isokawa K., Imamura M., Yuasa K., Ishikawa R., Kohama K., Takeda S., Yorifuji H. Plectin 1 links intermediate filaments to costameric sarcolemma through beta-synemin, alpha-dystrobrevin and actin. J Cell Sci 2008, 121:2062-2074.
24. Bellin R.M., Sernett S.W., Becker B., Ip W., Huiatt T.W., Robson R.M. Molecular characteristics and interactions of the intermediate filament protein synemin, Interactions with alpha-actinin may anchor synemin-containing heterofilaments. J Biol Chem 1999, 274:29493-29499.
25. Sun N., Huiatt T.W., Paulin D., Li Z., Robson R.M. Synemin interacts with the LIM domain protein zyxin and is essential for cell adhesion and migration. Exp Cell Res 2010, 316:491-505.
26. Mizuno Y., Thompson T.G., Guyon J.R., Lidov H.G., Brosius M., Imamura M., Ozawa E., Watkins S.C., Kunkel L.M. Desmuslin, an intermediate filament protein that interacts with alpha-dystrobrevin and desmin. Proc Natl Acad Sci U S A 2001, 98:6156-6161.
27. Bhosle R.C., Michele D.E., Campbell K.P., Li Z., Robson R.M. Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem Biophys Res Commun 2006, 346:768-777.
28. Pan Y., Jing R., Pitre A., Williams B.J., Skalli O. Intermediate filament protein synemin contributes to the migratory properties of astrocytoma cells by influencing the dynamics of the actin cytoskeleton. FASEB J 2008, 22:3196-3206.
29. Bouameur J.E., Favre B., Fontao L., Lingasamy P., Begre N., Borradori L. Interaction of plectin with keratins 5 and 14: dependence on several plectin domains and keratin quaternary structure. J Invest Dermatol 2014, 10.1038/jid.2014.255.
30. Steinbock F.A., Nikolic B., Coulombe P.A., Fuchs E., Traub P., Wiche G. Dose-dependent linkage, assembly inhibition and disassembly of vimentin and cytokeratin 5/14 filaments through plectin's intermediate filament-binding domain. J Cell Sci 2000, 113(Pt 3):483-491.
31. Windoffer R., Kolsch A., Woll S., Leube R.E. Focal adhesions are hotspots for keratin filament precursor formation. J Cell Biol 2006, 173:341-348.
32. Moch M., Herberich G., Aach T., Leube R.E., Windoffer R. Measuring the regulation of keratin filament network dynamics. Proc Natl Acad Sci U S A 2013, 110:10664-10669.
33. Snider N.T., Omary M.B. Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat Rev Mol Cell Biol 2014, 15:163-177.
34. Rotty J.D., Coulombe P.A. A wound-induced keratin inhibits Src activity during keratinocyte migration and tissue repair. J Cell Biol 2012, 197:381-389.
35. Kroger C., Loschke F., Schwarz N., Windoffer R., Leube R.E., Magin T.M. Keratins control intercellular adhesion involving PKC-alpha-mediated desmoplakin phosphorylation. J Cell Biol 2013, 201:681-692.
36. Fogh B.S., Multhaupt H.A., Couchman J.R. Protein kinase C, focal adhesions and the regulation of cell migration. J Histochem Cytochem 2014, 62:172-184.
37. Bordeleau F., Galarneau L., Gilbert S., Loranger A., Marceau N. Keratin 8/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells. Mol Biol Cell 2010, 21:1698-1713.
38. Dave J.M., Kang H., Abbey C.A., Maxwell S.A., Bayless K.J. Proteomic profiling of endothelial invasion revealed receptor for activated C kinase 1 (RACK1) complexed with vimentin to regulate focal adhesion kinase (FAK). J Biol Chem 2013, 288:30720-30733.
39. Osmanagic-Myers S., Gregor M., Walko G., Burgstaller G., Reipert S., Wiche G. Plectin-controlled keratin cytoarchitecture affects MAP kinases involved in cellular stress response and migration. J Cell Biol 2006, 174:557-568.
40. Osmanagic-Myers S., Wiche G. Plectin-RACK1 (receptor for activated C kinase 1) scaffolding: a novel mechanism to regulate protein kinase C activity. J Biol Chem 2004, 279:18701-18710.
41. Robert A., Herrmann H., Davidson M.W., Gelfand V.I. Microtubule-dependent transport of vimentin filament precursors is regulated by actin and by the concerted action of Rho- and p21-activated kinases. FASEB J 2014, 28:2879-2890.
42. Izawa I., Inagaki M. Regulatory mechanisms and functions of intermediate filaments: a study using site- and phosphorylation state-specific antibodies. Cancer Sci 2006, 97:167-174.
43. Chung B.M., Rotty J.D., Coulombe P.A. Networking galore: intermediate filaments and cell migration. Curr Opin Cell Biol 2013, 25:600-612.
44. Brown M.C., Cary L.A., Jamieson J.S., Cooper J.A., Turner C.E. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol Biol Cell 2005, 16:4316-4328.
45. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005, 6:56-68.
46. Lai I.R., Chu P.Y., Lin H.S., Liou J.Y., Jan Y.J., Lee J.C., Shen T.L. Phosphorylation of focal adhesion kinase at Tyr397 in gastric carcinomas and its clinical significance. Am J Pathol 2010, 177:1629-1637.
47. Deng X., Li Q., Hoff J., Novak M., Yang H., Jin H., Erfani S.F., Sharma C., Zhou P., Rabinovitz I., et al. Integrin-associated CD151 drives ErbB2-evoked mammary tumor onset and metastasis. Neoplasia 2012, 14:678-689.
48. Faure E., Garrouste F., Parat F., Monferran S., Leloup L., Pommier G., Kovacic H., Lehmann M. P2Y2 receptor inhibits EGF-induced MAPK pathway to stabilise keratinocyte hemidesmosomes. J Cell Sci 2012, 125:4264-4277.
49. Boudreau A., Tanner K., Wang D., Geyer F.C., Reis-Filho J.S., Bissell M.J. 14-3-3sigma stabilizes a complex of soluble actin and intermediate filament to enable breast tumor invasion. Proc Natl Acad Sci U S A 2013, 110:E3937-E3944.
50. Eckes B., Colucci-Guyon E., Smola H., Nodder S., Babinet C., Krieg T., Martin P. Impaired wound healing in embryonic and adult mice lacking vimentin. J Cell Sci 2000, 113(Pt 13):2455-2462.
51. Eckes B., Dogic D., Colucci-Guyon E., Wang N., Maniotis A., Ingber D., Merckling A., Langa F., Aumailley M., Delouvee A., et al. Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J Cell Sci 1998, 111(Pt 13):1897-1907.
52. Morley S.M., D'Alessandro M., Sexton C., Rugg E.L., Navsaria H., Shemanko C.S., Huber M., Hohl D., Heagerty A.I., Leigh I.M., et al. Generation and characterization of epidermolysis bullosa simplex cell lines: scratch assays show faster migration with disruptive keratin mutations. Br J Dermatol 2003, 149:46-58.
53. Seltmann K., Roth W., Kroger C., Loschke F., Lederer M., Huttelmaier S., Magin T.M. Keratins mediate localization of hemidesmosomes and repress cell motility. J Invest Dermatol 2013, 133:181-190.
54. Tsuruta D., Jones J.C. The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J Cell Sci 2003, 116(Pt 24):4977-4984.
55. Gregor M., Osmanagic-Myers S., Burgstaller G., Wolfram M., Fischer I., Walko G., Resch G.P., Jorgl A., Herrmann H., Wiche G. Mechanosensing through focal adhesion-anchored intermediate filaments. FASEB J 2014, 28:715-729.
56. Menko A.S., Bleaken B.M., Libowitz A.A., Zhang L., Stepp M.A., Walker J.L. A central role for vimentin in regulating repair function during healing of the lens epithelium. Mol Biol Cell 2014, 25:776-790.
57. Helfand B.T., Mendez M.G., Murthy S.N., Shumaker D.K., Grin B., Mahammad S., Aebi U., Wedig T., Wu Y.I., Hahn K.M., et al. Vimentin organization modulates the formation of lamellipodia. Mol Biol Cell 2011, 22:1274-1289.
58. Beil M., Micoulet A., von Wichert G., Paschke S., Walther P., Omary M.B., Van Veldhoven P.P., Gern U., Wolff-Hieber E., Eggermann J., et al. Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells. Nat Cell Biol 2003, 5:803-811.
59. Tsuruta D., Hashimoto T., Hamill K.J., Jones J.C. Hemidesmosomes and focal contact proteins: functions and cross-talk in keratinocytes, bullous diseases and wound healing. J Dermatol Sci 2011, 62:1-7.
60. Rabinovitz I., Toker A., Mercurio A.M. Protein kinase C-dependent mobilization of the alpha6beta4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J Cell Biol 1999, 146:1147-1160.
61. Hamill K.J., Hopkinson S.B., DeBiase P., Jones J.C. BPAG1e maintains keratinocyte polarity through beta4 integrin-mediated modulation of Rac1 and cofilin activities. Mol Biol Cell 2009, 20:2954-2962.
62. Galarneau L., Loranger A., Gilbert S., Marceau N. Keratins modulate hepatic cell adhesion, size and G1/S transition. Exp Cell Res 2007, 313:179-194.
63. Kleeberger W., Bova G.S., Nielsen M.E., Herawi M., Chuang A.Y., Epstein J.I., Berman D.M. Roles for the stem cell associated intermediate filament Nestin in prostate cancer migration and metastasis. Cancer Res 2007, 67:9199-9206.
64. Hyder C.L., Lazaro G., Pylvanainen J.W., Roberts M.W., Qvarnstrom S.M., Eriksson J.E. Nestin regulates prostate cancer cell invasion by influencing the localisation and functions of FAK and integrins. J Cell Sci 2014, 127:2161-2173.
65. Kolotuev I., Hyenne V., Schwab Y., Rodriguez D., Labouesse M. A pathway for unicellular tube extension depending on the lymphatic vessel determinant Prox1 and on osmoregulation. Nat Cell Biol 2013, 15:157-168.
66. Planko L., Bohse K., Hohfeld J., Betz R.C., Hanneken S., Eigelshoven S., Kruse R., Nothen M.M., Magin T.M. Identification of a keratin-associated protein with a putative role in vesicle transport. Eur J Cell Biol 2007, 86:827-839.
67. Akita Y., Kawasaki H., Imajoh-Ohmi S., Fukuda H., Ohno S., Hirano H., Ono Y., Yonekawa H. Protein kinase C epsilon phosphorylates keratin 8 at Ser8 and Ser23 in GH4C1 cells stimulated by thyrotropin-releasing hormone. FEBS J 2007, 274:3270-3285.