Regulation of cell adhesion to collagen via β1 integrins is dependent on interactions of filamin A with vimentin and protein kinase C epsilon

Experimental Cell Research

Volumn 316, Issue 11, 2010, Pages 1829-1844

  Kim, Hugh ^a   Nakamura, Fumihiko ^b   Lee, Wilson ^a   Hong, Claire ^a   Pérez Sala, Dolores ^c   McCulloch, Christopher A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Actin; Cell adhesion; Cell guidance; Intermediate filaments

Indexed keywords

BETA1 INTEGRIN; COLLAGEN; FILAMIN A; MUTANT PROTEIN; PROTEIN KINASE C EPSILON; VIMENTIN;

ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL SPREADING; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

MAMMALIA;

EID: 77953230270     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.02.007     Document Type: Article

References (66)

1. Li S., Guan J.L., Chien S. Biochemistry and biomechanics of cell motility. Annu. Rev. Biomed. Eng. 2005, 7:105-150.
2. Defilippi P., Olivo C., Venturino M., Dolce L., Silengo L., Tarone G. Actin cytoskeleton organization in response to integrin-mediated adhesion. Microsc. Res. Tech. 1999, 47:67-78.
3. Vicente-Manzanares M., Choi C.K., Horwitz A.R. Integrins in cell migration-the actin connection. J. Cell. Sci. 2009, 122:199-206.
4. Serrels B., Serrels A., Brunton V.G., Holt M., McLean G.W., Gray C.H., Jones G.E., Frame M.C. Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 2007, 9:1046-1056.
5. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
6. Price L.S., Leng J., Schwartz M.A., Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 1998, 9:1863-1871.
7. Zimerman B., Volberg T., Geiger B. Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil. Cytoskelet. 2004, 58:143-159.
8. 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, 116:4977-4984.
9. 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.
10. McInroy L., Maatta A. Down-regulation of vimentin expression inhibits carcinoma cell migration and adhesion. Biochem. Biophys. Res. Commun. 2007, 360:109-114.
11. Eckes B., Dogic D., Colucci-Guyon E., Wang N., Maniotis A., Ingber D., Merckling A., Langa F., Aumailley M., Delouvee A., Koteliansky V., Babinet C., Krieg T. Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J. Cell. Sci. 1998, 111(Pt. 13):1897-1907.
12. Rizki A., Mott J.D., Bissell M.J. Polo-like kinase 1 is involved in invasion through extracellular matrix. Cancer Res. 2007, 67:11106-11110.
13. Arocena M. Effect of acrylamide on the cytoskeleton and apoptosis of bovine lens epithelial cells. Cell Biol. Int. 2006, 30:1007-1012.
14. Chang L., Goldman R.D. Intermediate filaments mediate cytoskeletal crosstalk. Nat. Rev. Mol. Cell Biol. 2004, 5:601-613.
15. Kasas S., Wang X., Hirling H., Marsault R., Huni B., Yersin A., Regazzi R., Grenningloh G., Riederer B., Forro L., Dietler G., Catsicas S. Superficial and deep changes of cellular mechanical properties following cytoskeleton disassembly. Cell Motil. Cytoskelet. 2005, 62:124-132.
16. Seifert G.J., Lawson D., Wiche G. Immunolocalization of the intermediate filament-associated protein plectin at focal contacts and actin stress fibers. Eur. J. Cell Biol. 1992, 59:138-147.
17. Svitkina T.M., Verkhovsky A.B., Borisy G.G. Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J. Cell Biol. 1996, 135:991-1007.
18. Spurny R., Gregor M., Castanon M.J., Wiche G. Plectin deficiency affects precursor formation and dynamics of vimentin networks. Exp. Cell Res. 2008, 314:3570-3580.
19. Yang Y., Dowling J., Yu Q.C., Kouklis P., Cleveland D.W., Fuchs E. An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 1996, 86:655-665.
20. 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.
21. Brown K.D., Binder L.I. Identification of the intermediate filament-associated protein gyronemin as filamin. Implications for a novel mechanism of cytoskeletal interaction. J. Cell. Sci. 1992, 102(Pt. 1):19-30.
22. Kim H., Nakamura F., Lee W., Shifrin Y., Arora P., McCulloch C. Filamin A is required for vimentin-mediated cell adhesion and spreading. Am. J. Physiol. Cell Physiol. 2010, 298:C221-C236.
23. Cunningham C.C., Gorlin J.B., Kwiatkowski D.J., Hartwig J.H., Janmey P.A., Byers H.R., Stossel T.P. Actin-binding protein requirement for cortical stability and efficient locomotion. Science (New York, N.Y 1992, 255:325-327.
24. Gardel M.L., Nakamura F., Hartwig J.H., Crocker J.C., Stossel T.P., Weitz D.A. Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1762-1767.
25. Kasza K.E., Nakamura F., Hu S., Kollmannsberger P., Bonakdar N., Fabry B., Stossel T.P., Wang N., Weitz D.A. Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys. J. 2009, 96:4326-4335.
26. Glogauer M., Arora P., Chou D., Janmey P.A., Downey G.P., McCulloch C.A. The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J. Biol. Chem. 1998, 273:1689-1698.
27. Kim H., Sengupta A., Glogauer M., McCulloch C.A. Filamin A regulates cell spreading and survival via beta1 integrins. Exp. Cell Res. 2008, 314:834-846.
28. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2001, 2:138-145.
29. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., Stossel T.P. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2122-2128.
30. Bellanger J.M., Astier C., Sardet C., Ohta Y., Stossel T.P., Debant A. The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat. Cell Biol. 2000, 2:888-892.
31. Vadlamudi R.K., Li F., Adam L., Nguyen D., Ohta Y., Stossel T.P., Kumar R. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 2002, 4:681-690.
32. Loo D.T., Kanner S.B., Aruffo A. Filamin binds to the cytoplasmic domain of the beta1-integrin. Identification of amino acids responsible for this interaction. J. Biol. Chem. 1998, 273:23304-23312.
33. Kiema T., Lad Y., Jiang P., Oxley C.L., Baldassarre M., Wegener K.L., Campbell I.D., Ylanne J., Calderwood D.A. The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 2006, 21:337-347.
34. Meyer S.C., Sanan D.A., Fox J.E. Role of actin-binding protein in insertion of adhesion receptors into the membrane. J. Biol. Chem. 1998, 273:3013-3020.
35. Popowicz G.M., Schleicher M., Noegel A.A., Holak T.A. Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci. 2006, 31:411-419.
36. Nieminen M., Henttinen T., Merinen M., Marttila-Ichihara F., Eriksson J.E., Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat. Cell Biol. 2006, 8:156-162.
37. 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.
38. Jia Z., Barbier L., Stuart H., Amraei M., Pelech S., Dennis J.W., Metalnikov P., O'Donnell P., Nabi I.R. Tumor cell pseudopodial protrusions. Localized signaling domains coordinating cytoskeleton remodeling, cell adhesion, glycolysis, RNA translocation, and protein translation. J. Biol. Chem. 2005, 280:30564-30573.
39. Jackson W.M., Jaasma M.J., Tang R.Y., Keaveny T.M. Mechanical loading by fluid shear is sufficient to alter the cytoskeletal composition of osteoblastic cells. Am. J. Physiol. Cell Physiol. 2008, 295:C1007-C1015.
40. Meng X., Yuan Y., Maestas A., Shen Z. Recovery from DNA damage-induced G2 arrest requires actin-binding protein filamin-A/actin-binding protein 280. J. Biol. Chem. 2004, 279:6098-6105.
41. Chong S.A., Lee W., Arora P.D., Laschinger C., Young E.W., Simmons C.A., Manolson M., Sodek J., McCulloch C.A. Methylglyoxal inhibits the binding step of collagen phagocytosis. J. Biol. Chem. 2007, 282:8510-8520.
42. Glogauer M., Arora P., Yao G., Sokholov I., Ferrier J., McCulloch C.A. Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell. Sci. 1997, 110(Pt. 1):11-21.
43. Lee W., Sodek J., McCulloch C.A. Role of integrins in regulation of collagen phagocytosis by human fibroblasts. J. Cell. Physiol. 1996, 168:695-704.
44. Knowles G.C., McKeown M., Sodek J., McCulloch C.A. Mechanism of collagen phagocytosis by human gingival fibroblasts: importance of collagen structure in cell recognition and internalization. J. Cell. Sci. 1991, 98(Pt. 4):551-558.
45. Segal G., Lee W., Arora P.D., McKee M., Downey G., McCulloch C.A. Involvement of actin filaments and integrins in the binding step in collagen phagocytosis by human fibroblasts. J. Cell. Sci. 2001, 114:119-129.
46. Zhao X.H., Laschinger C., Arora P., Szaszi K., Kapus A., McCulloch C.A. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J. Cell. Sci. 2007, 120:1801-1809.
47. Batista da Silva A.P., Lee W., Bajenova E., McCulloch C.A., Ellen R.P. The major outer sheath protein of Treponema denticola inhibits the binding step of collagen phagocytosis in fibroblasts. Cell. Microbiol. 2004, 6:485-498.
48. Phares D.J., Holt J.K., Smedley G.T., Flagan R.C. The wall shear stress produced by the normal impingement of a jet on a flat surface. J. Fluid Mech. 2000, 418:351-375.
49. Nakamura F., Osborn E., Janmey P.A., Stossel T.P. Comparison of filamin A-induced cross-linking and Arp2/3 complex-mediated branching on the mechanics of actin filaments. J. Biol. Chem. 2002, 277:9148-9154.
50. Nakamura F., Osborn T.M., Hartemink C.A., Hartwig J.H., Stossel T.P. Structural basis of filamin A functions. J. Cell Biol. 2007, 179:1011-1025.
51. Nakamura F., Pudas R., Heikkinen O., Permi P., Kilpelainen I., Munday A.D., Hartwig J.H., Stossel T.P., Ylanne J. The structure of the GPIb-filamin A complex. Blood 2006, 107:1925-1932.
52. Stamatakis K., Sanchez-Gomez F.J., Perez-Sala D. Identification of novel protein targets for modification by 15-deoxy-Delta12,14-prostaglandin J2 in mesangial cells reveals multiple interactions with the cytoskeleton. J. Am. Soc. Nephrol. 2006, 17:89-98.
53. Fortin S., Le Mercier M., Camby I., Spiegl-Kreinecker S., Berger W., Lefranc F., Kiss R. Galectin-1 is implicated in the protein kinase C epsilon/vimentin-controlled trafficking of integrin-beta1 in glioblastoma cells. Brain Pathol. 2008, 20:36-49.
54. Prahlad V., Yoon M., Moir R.D., Vale R.D., Goldman R.D. Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 1998, 143:159-170.
55. Ando S., Tanabe K., Gonda Y., Sato C., Inagaki M. Domain- and sequence-specific phosphorylation of vimentin induces disassembly of the filament structure. Biochemistry 1989, 28:2974-2979.
56. 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.
57. Ogawara M., Inagaki N., Tsujimura K., Takai Y., Sekimata M., Ha M.H., Imajoh-Ohmi S., Hirai S., Ohno S., Sugiura H., et al. Differential targeting of protein kinase C and CaM kinase II signalings to vimentin. J. Cell Biol. 1995, 131:1055-1066.
58. Yasui Y., Goto H., Matsui S., Manser E., Lim L., Nagata K., Inagaki M. Protein kinases required for segregation of vimentin filaments in mitotic process. Oncogene 2001, 20:2868-2876.
59. Calderwood D.A., Huttenlocher A., Kiosses W.B., Rose D.M., Woodside D.G., Schwartz M.A., Ginsberg M.H. Increased filamin binding to beta-integrin cytoplasmic domains inhibits cell migration. Nat. Cell Biol. 2001, 3:1060-1068.
60. Green K.J., Geiger B., Jones J.C., Talian J.C., Goldman R.D. The relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes. J. Cell Biol. 1987, 104:1389-1402.
61. Eriksson J.E., He T., Trejo-Skalli A.V., Harmala-Brasken A.S., Hellman J., Chou Y.H., Goldman R.D. Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell. Sci. 2004, 117:919-932.
62. Inagaki M., Nishi Y., Nishizawa K., Matsuyama M., Sato C. Site-specific phosphorylation induces disassembly of vimentin filaments in vitro. Nature 1987, 328:649-652.
63. Skalski M., Coppolino M.G. SNARE-mediated trafficking of alpha5beta1 integrin is required for spreading in CHO cells. Biochem. Biophys. Res. Commun. 2005, 335:1199-1210.
64. Dunphy J.L., Moravec R., Ly K., Lasell T.K., Melancon P., Casanova J.E. The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr. Biol. 2006, 16:315-320.
65. Jovic M., Naslavsky N., Rapaport D., Horowitz M., Caplan S. EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell. Sci. 2007, 120:802-814.
66. Tigges U., Koch B., Wissing J., Jockusch B.M., Ziegler W.H. The F-actin cross-linking and focal adhesion protein filamin A is a ligand and in vivo substrate for protein kinase C alpha. J. Biol. Chem. 2003, 278:23561-23569.