A helping hand: How vinculin contributes to cell-matrix and cell-cell force transfer

Cell Adhesion and Migration

Volumn 8, Issue 6, 2014, Pages 550-557

  Dumbauld, David W ^a,b   García, Andrés J ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Adherens junction; Adhesion strength; Focal adhesion; Mechanosensing; Traction force; Vinculin

Indexed keywords

ALPHA CATENIN; BETA CATENIN; INTEGRIN; TALIN; VINCULIN; ACTIN; PROTEIN BINDING;

ACTIN FILAMENT; BINDING AFFINITY; CELL ADHESION; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL STRUCTURE; CELL TRANSFER; EXTRACELLULAR MATRIX; FOCAL ADHESION; FORCE; HUMAN; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; NOTE; PROTEIN FUNCTION; PROTEIN INTERACTION; METABOLISM; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTINS; ADHERENS JUNCTIONS; CELL ADHESION; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HUMANS; INTEGRINS; PROTEIN BINDING; TALIN; VINCULIN;

EID: 84921922050     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.29139     Document Type: Note

References (56)

1. Geiger B, Yamada KM. Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol 2011; 3: 3; PMID:21441590; http://dx.doi.org/10.1101/cshperspect.a005033
2. Gallant ND, Michael KE, García AJ. Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol Biol Cell 2005; 16:4329-40; PMID:16000373; http://dx.doi.org/10.1091/mbc.E05-02-0170
3. Dumbauld DW, Lee TT, Singh A, Scrimgeour J, Gersbach CA, Zamir EA, Fu J, Chen CS, Curtis JE, Craig SW, et al. How vinculin regulates force transmission. Proc Natl Acad Sci U S A 2013; 110:9788-93; PMID:23716647; http://dx.doi.org/10.1073/pnas.1216209110
4. Dumbauld DW, Shin H, Gallant ND, Michael KE, Radhakrishna H, García AJ. Contractility modulates cell adhesion strengthening through focal adhesion kinase and assembly of vinculin-containing focal adhesions. J Cell Physiol 2010; 223:746-56; PMID:20205236
5. Dumbauld DW, Michael KE, Hanks SK, García AJ. Focal adhesion kinase-dependent regulation of adhesive forces involves vinculin recruitment to focal adhesions. Biol Cell 2010; 102:203-13; PMID:19883375; http://dx.doi.org/10.1042/BC20090104
6. Michael KE, Dumbauld DW, Burns KL, Hanks SK, García AJ. Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. Mol Biol Cell 2009; 20:2508-19; PMID:19297531; http://dx.doi.org/10.1091/mbc.E08-01-0076
7. Galbraith CG, Yamada KM, Sheetz MP. The relationship between force and focal complex development. J Cell Biol 2002; 159:695-705; PMID:12446745; http://dx.doi.org/10.1083/jcb.200204153
8. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 2001; 3:466-72; PMID:11331874; http://dx.doi.org/10.1038/35074532
9. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J Cell Biol 2010; 188:877-90; PMID:20308429; http://dx.doi.org/10.1083/jcb.200906012
10. Janostiak R, Brabek J, Auernheimer V, Tatarova Z, Lautscham LA, Dey T, Gemperle J, Merkel R, Goldmann WH, Fabry B, et al. CAS directly interacts with vinculin to control mechanosensing and focal adhesion dynamics. Cell Mol Life Sci 2014; 71:727-44; PMID:23974298
11. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 2010; 466:263-6; PMID:20613844; http://dx.doi.org/10.1038/nature09198
12. Bakolitsa C, Cohen DM, Bankston LA, Bobkov AA, Cadwell GW, Jennings L, Critchley DR, Craig SW, Liddington RC. Structural basis for vinculin activation at sites of cell adhesion. Nature 2004; 430:583-6; PMID:15195105; http://dx.doi.org/10.1038/nature02610
13. Chen H, Choudhury DM, Craig SW. Coincidence of actin filaments and talin is required to activate vinculin. J Biol Chem 2006; 281:40389-98; PMID:17074767; http://dx.doi.org/10.1074/jbc.M607324200
14. Cohen DM, Chen H, Johnson RP, Choudhury B, Craig SW. Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J Biol Chem 2005; 280:17109-17; PMID:15728584; http://dx.doi.org/10.1074/jbc.M414704200
15. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. Stretching single talin rod molecules activates vinculin binding. Science 2009; 323:638-41; PMID:19179532; http://dx.doi.org/10.1126/science.1162912
16. Hirata H, Tatsumi H, Lim CT, Sokabe M. Force-dependent vinculin binding to talin in live cells: a crucial step in anchoring the actin cytoskeleton to focal adhesions. Am J Physiol Cell Physiol 2014; 306:C607-20; PMID:24452377; http://dx.doi.org/10.1152/ajpcell.00122.2013
17. Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J Cell Biol 2007; 179:1043-57; PMID:18056416; http://dx.doi.org/10.1083/jcb.200703036
18. Xu W, Coll JL, Adamson ED. Rescue of the mutant phenotype by reexpression of full-length vinculin in null F9 cells; effects on cell locomotion by domain deleted vinculin. J Cell Sci 1998; 111:1535-44; PMID:9580561
19. Goldmann WH. The coupling of vinculin to the cytoskeleton is not essential for mechano-chemical signaling in F9 cells. Cell Biol Int 2002; 26:279-86; PMID:11991656; http://dx.doi.org/10.1006/cbir.2001.0854
20. Alenghat FJ, Fabry B, Tsai KY, Goldmann WH, Ingber DE. Analysis of cell mechanics in single vinculin-deficient cells using a magnetic tweezer. Biochem Biophys Res Commun 2000; 277:93-9; PMID:11027646; http://dx.doi.org/10.1006/bbrc.2000.3636
21. Holle AW, Tang X, Vijayraghavan D, Vincent LG, Fuhrmann A, Choi YS, del Álamo JC, Engler AJ. In situ mechanotransduction via vinculin regulates stem cell differentiation. Stem Cells 2013; 31:2467-77; PMID:23897765; http://dx.doi.org/10.1002/stem.1490
22. Vasile VC, Edwards WD, Ommen SR, Ackerman MJ. Obstructive hypertrophic cardiomyopathy is associated with reduced expression of vinculin in the intercalated disc. Biochem Biophys Res Commun 2006; 349:709-15; PMID:16949038; http://dx.doi.org/10.1016/j.bbrc.2006.08.106
23. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 2001; 153:1175-86; PMID:11402062; http://dx.doi.org/10.1083/jcb.153.6.1175
24. Ciobanasu C, Faivre B, Le Clainche C. Actomyosin-dependent formation of the mechanosensitive talin-vinculin complex reinforces actin anchoring. Nat Commun 2014; 5: 3095; PMID:24452080; http://dx.doi.org/10.1038/ncomms4095
25. Chang CW, Kumar S. Vinculin tension distributions of individual stress fibers within cell-matrix adhesions. J Cell Sci 2013; 126:3021-30; PMID:23687380; http://dx.doi.org/10.1242/jcs.119032
26. Chen H, Cohen DM, Choudhury DM, Kioka N, Craig SW. Spatial distribution and functional significance of activated vinculin in living cells. J Cell Biol 2005; 169:459-70; PMID:15883197; http://dx.doi.org/10.1083/jcb.200410100
27. Tan TW, Pfau B, Jones D, Meyer T. Stimulation of primary osteoblasts with ATP induces transient vinculin clustering at sites of high intracellular traction force. J Mol Histol 2014; 45:81-9; PMID:23933795; http://dx.doi.org/10.1007/s10735-013-9530-7
28. Thievessen I, Thompson PM, Berlemont S, Plevock KM, Plotnikov SV, Zemljic-Harpf A, Ross RS, Davidson MW, Danuser G, Campbell SL, et al. Vinculinactin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J Cell Biol 2013; 202:163-77; PMID:23836933; http://dx.doi.org/10.1083/jcb.201303129
29. Janssen ME, Kim E, Liu H, Fujimoto LM, Bobkov A, Volkmann N, Hanein D. Three-dimensional structure of vinculin bound to actin filaments. Mol Cell 2006; 21:271-81; PMID:16427016; http://dx.doi.org/10.1016/j.molcel.2005.11.020
30. Tolbert CE, Burridge K, Campbell SL. Vinculin regulation of F-actin bundle formation: what does it mean for the cell? Cell Adh Migr 2013; 7:219-25; PMID:23307141; http://dx.doi.org/10.4161/cam.23184
31. Shen K, Tolbert CE, Guilluy C, Swaminathan VS, Berginski ME, Burridge K, Superfine R, Campbell SL. The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties. J Biol Chem 2011; 286:45103-15; PMID:22052910; http://dx.doi.org/10.1074/jbc.M111.244293
32. Lavelin I, Wolfenson H, Patla I, Henis YI, Medalia O, Volberg T, Livne A, Kam Z, Geiger B. Differential effect of actomyosin relaxation on the dynamic properties of focal adhesion proteins. PLoS One 2013; 8: e73549; PMID:24039980; http://dx.doi.org/10.1371/journal.pone.0073549
33. Carisey A, Tsang R, Greiner AM, Nijenhuis N, Heath N, Nazgiewicz A, Kemkemer R, Derby B, Spatz J, Ballestrem C. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr Biol 2013; 23:271-81; PMID:23375895; http://dx.doi.org/10.1016/j.cub.2013.01.009
34. Wolfenson H, Bershadsky A, Henis YI, Geiger B. Actomyosin-generated tension controls the molecular kinetics of focal adhesions. J Cell Sci 2011; 124:1425-32; PMID:21486952; http://dx.doi.org/10.1242/jcs.077388
35. Janoštiak R, Brábek J, Auernheimer V, Tatárová Z, Lautscham LA, Dey T, Gemperle J, Merkel R, Goldmann WH, Fabry B, et al. CAS directly interacts with vinculin to control mechanosensing and focal adhesion dynamics. Cell Mol Life Sci 2014; 71:727-44; PMID:23974298; http://dx.doi.org/10.1007/s00018-013-1450-x
36. Ciobanasu C, Faivre B, Le Clainche C. Actomyosin-dependent formation of the mechanosensitive talin-vinculin complex reinforces actin anchoring. Nat Commun 2014; 5: 3095; PMID:24452080; http://dx.doi.org/10.1038/ncomms4095
37. Yao M, Goult BT, Chen H, Cong P, Sheetz MP, Yan J. Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci Rep 2014; 4: 4610; PMID:24714394; http://dx.doi.org/10.1038/srep04610
38. Zhang Z, Izaguirre G, Lin SY, Lee HY, Schaefer E, Haimovich B. The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by SRC kinases, affects cell spreading. Mol Biol Cell 2004; 15:4234-47; PMID:15229287; http://dx.doi.org/10.1091/mbc.E04-03-0264
39. Diez G, Kollmannsberger P, Mierke CT, Koch TM, Vali H, Fabry B, Goldmann WH. Anchorage of vinculin to lipid membranes influences cell mechanical properties. Biophys J 2009; 97:3105-12; PMID:20006947; http://dx.doi.org/10.1016/j.bpj.2009.09.039
40. Möhl C, Kirchgessner N, Schäfer C, Küpper K, Born S, Diez G, Goldmann WH, Merkel R, Hoffmann B. Becoming stable and strong: the interplay between vinculin exchange dynamics and adhesion strength during adhesion site maturation. Cell Motil Cytoskeleton 2009; 66:350-64; PMID:19422016; http://dx.doi.org/10.1002/cm.20375
41. Huang Y, Day RN, Gunst SJ. Vinculin phosphorylation at Tyr1065 regulates vinculin conformation and tension development in airway smooth muscle tissues. J Biol Chem 2014; 289:3677-88; PMID:24338477; http://dx.doi.org/10.1074/jbc.M113.508077
42. Cohen DM, Chen H, Johnson RP, Choudhury B, Craig SW. Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J Biol Chem 2005; 280:17109-17; PMID:15728584; http://dx.doi.org/10.1074/jbc.M414704200
43. Has C, Herz C, Zimina E, Qu HY, He Y, Zhang ZG, Wen TT, Gache Y, Aumailley M, Bruckner-Tuderman L. Kindlin-1 Is required for RhoGTPase-mediated lamellipodia formation in keratinocytes. Am J Pathol 2009; 175:1442-52; PMID:19762715; http://dx.doi.org/10.2353/ajpath.2009.090203
44. Gomez GA, McLachlan RW, Yap AS. Productive tension: force-sensing and homeostasis of cell-cell junctions. Trends Cell Biol 2011; 21:499-505; PMID:21763139; http://dx.doi.org/10.1016/j.tcb.2011.05.006
45. Leckband DE, le Duc Q, Wang N, de Rooij J. Mechanotransduction at cadherin-mediated adhesions. Curr Opin Cell Biol 2011; 23:523-30; PMID:21890337; http://dx.doi.org/10.1016/j.ceb.2011.08.003
46. Huveneers S, de Rooij J. Mechanosensitive systems at the cadherin-F-actin interface. J Cell Sci 2013; 126:403-13; PMID:23524998; http://dx.doi.org/10.1242/jcs.109447
47. Yonemura S. Cadherin-actin interactions at adherens junctions. Curr Opin Cell Biol 2011; 23:515-22; PMID:21807490; http://dx.doi.org/10.1016/j.ceb.2011.07.001
48. Yonemura S. A mechanism of mechanotransduction at the cell-cell interface: emergence of α-catenin as the center of a force-balancing mechanism for morphogenesis in multicellular organisms. Bioessays 2011; 33:732-6; PMID:21826690; http://dx.doi.org/10.1002/bies.201100064
49. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 2010; 12:533-42; PMID:20453849; http://dx.doi.org/10.1038/ncb2055
50. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, de Rooij J. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 2010; 189:1107-15; PMID:20584916; http://dx.doi.org/10.1083/jcb.201001149
51. Sumida GM, Tomita TM, Shih W, Yamada S. Myosin II activity dependent and independent vinculin recruitment to the sites of E-cadherin-mediated cell-cell adhesion. BMC Cell Biol 2011; 12: 48; PMID:22054176; http://dx.doi.org/10.1186/1471-2121-12-48
52. Peng X, Maiers JL, Choudhury D, Craig SW, DeMali KA. α-Catenin uses a novel mechanism to activate vinculin. J Biol Chem 2012; 287:7728-37; PMID:22235119; http://dx.doi.org/10.1074/jbc.M111.297481
53. Twiss F, Le Duc Q, Van Der Horst S, Tabdili H, Van Der Krogt G, Wang N, Rehmann H, Huveneers S, Leckband DE, De Rooij J. Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol Open 2012; 1:1128-40; PMID:23213393; http://dx.doi.org/10.1242/bio.20122428
54. Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, Rehmann H, de Rooij J. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 2012; 196:641-52; PMID:22391038; http://dx.doi.org/10.1083/jcb.201108120
55. Thomas WA, Boscher C, Chu YS, Cuvelier D, Martinez-Rico C, Seddiki R, Heysch J, Ladoux B, Thiery JP, Mege RM, et al. α-Catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength. J Biol Chem 2013; 288:4957-69; PMID:23266828; http://dx.doi.org/10.1074/jbc.M112.403774
56. Dufour S, Mège RM, Thiery JP. α-catenin, vinculin, and F-actin in strengthening E-cadherin cell-cell adhesions and mechanosensing. Cell Adh Migr 2013; 7:345-50; PMID:23739176; http://dx.doi.org/10.4161/cam.25139