The FAK-Arp2/3 interaction promotes leading edge advance and haptosensing by coupling nascent adhesions to lamellipodia actin

Molecular Biology of the Cell

Volumn 27, Issue 7, 2016, Pages 1085-1100

  Swaminathan, Vinay ^a   Fischer, R S ^a   Waterman, Clare M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; ENHANCED GREEN FLUORESCENT PROTEIN; F ACTIN; FOCAL ADHESION KINASE; ACTIN; FOCAL ADHESION KINASE 1; INTEGRIN; PROTEIN BINDING; PTK2 PROTEIN, MOUSE;

ACTIN POLYMERIZATION; ADHERENT CELL; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; FOCAL ADHESION; HAPTOSENSING; HISTOGRAM; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LAMELLIPODIUM; MOUSE; NASCENT INTEGRIN ADHESION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; TURNOVER TIME; WESTERN BLOTTING; ANIMAL; CELL MOTION; FIBROBLAST; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PSEUDOPODIUM;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; CELL MOVEMENT; EXTRACELLULAR MATRIX; FIBROBLASTS; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; INTEGRINS; MICE; PHOSPHORYLATION; PROTEIN BINDING; PSEUDOPODIA;

EID: 84962361595     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-08-0590     Document Type: Article

References (48)

1. Alexandrova AY, Arnold K, Schaub S, Vasiliev JM, Meister JJ, Bershadsky AD, Verkhovsky AB (2008). Comparative dynamics of retrograde actin flow and focal adhesions: Formation of nascent adhesions triggers transition from fast to slow flow. PLoS One 3, e3234.
2. Bachir AI, Zareno J, Moissoglu K, Plow EF, Gratton E, Horwitz AR (2014). Integrin-associated complexes form hierarchically with variable stoichiometry in nascent adhesions. Curr Biol 24, 1845-1853.
3. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, et al. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
4. Bolte S, Cordelieres FP (2006). A guided tour into subcellular colocalisation analysis in light microscopy. J Microsc 224, 13-232.
5. Burnette DT, Manley S, Sengupta P, Sougrat R, Davidson MW, Kachar B, Lippincott-Schwartz J (2011). A role for actin arcs in the leading-edge advance of migrating cells. Nat Cell Biol 13, 371-381.
6. Chan KT, Bennin DA, Huttenlocher A (2010). Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). J Biol Chem 285, 11418-11426.
7. Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, Horwitz AR (2008). Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat Cell Biol 10, 1039-1050.
8. Choi CK, Zareno J, Digman MA, Gratton E, Horwitz AR (2011). Cross-correlated fluctuation analysis reveals phosphorylation-regulated paxillin-fak complexes in nascent adhesions. Biophys J 100, 583-592.
9. Cooper LA, Shen T-L, Guan J-L (2003). Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol Cell Biol 23, 8030-8041.
10. Ezratty EJ, Partridge MA, Gundersen GG (2005). Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7, 581-590.
11. Frame MC, Patel H, Serrels B, Lietha D, Eck MJ (2010). The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 11, 802-814.
12. Giannone G, Dubin-Thaler BJ, Döbereiner HG, Kieffer N, Bresnick AR, Sheetz MP (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
13. Gupton SL, Waterman-Storer CM (2006). Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361-1374.
14. Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Rondé P (2005). Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 118, 4415-4425.
15. Higgs HN, Pollard TD (2001). Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70, 649-676.
16. Hoffmann JE, Fermin Y, Stricker RL, Ickstadt K, Zamir E (2014). Symmetric exchange of multi-protein building blocks between stationary focal adhesions and the cytosol. Elife 2014, 1-18.
17. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
18. Iskratsch T, Yu CH, Mathur A, Liu S, Stévenin V, Dwyer J, Hone J, Ehler E, Sheetz M (2013). FHOD1 is needed for directed forces and adhesion maturation during cell spreading and migration. Dev Cell 27, 545-559.
19. Kholodenko BN (2006). Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7, 165-176.
20. Lauffenburger DA, Horwitz AF (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
21. Lawson C, Lim ST, Uryu S, Chen XL, Calderwood DA, Schlaepfer DD (2012). FAK promotes recruitment of talin to nascent adhesions to control cell motility. J Cell Biol 196, 223-232.
22. Lietha D, Cai X, Ceccarelli DFJ, Li Y, Schaller MD, Eck MJ (2007). Structural basis for the autoinhibition of focal adhesion kinase. Cell 129, 1177-1 187.
23. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn KM, Danuser G (2009). Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103.
24. Mitra SK, Hanson DA, Schlaepfer DD (2005). Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6, 56-68.
25. Mullins RD, Heuser JA, Pollard TD (1998). The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95, 6181-6186.
26. Nolen BJ, Tomasevic N, Russell A, Pierce DW, Jia Z, McCormick CD, Hartman J, Sakowicz R, Pollard TD (2009). Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034.
27. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF, Parsons JT, Beggs HE, Stanley ER, Bouton AH (2007). Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 179, 1275-1287.
28. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537-540.
29. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM (2010). Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J Cell Biol 188, 877-890.
30. Plotnikov SV, Pasapera AM, Sabass B, Waterman CM (2012). Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527.
31. Pollard TD, Borisy GG (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
32. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004). Two distinct actin networks drive the protrusion of migrating cells. Science 305, 1782-1786.
33. Renkawitz J, Schumann K, Weber M, Lämmermann T, Pflicke H, Piel M, Polleux J, Spatz JP, Sixt M (2009). Adaptive force transmission in amoeboid cell migration. Nat Cell Biol 11, 1438-1443.
34. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
35. Schaller MD (2010). Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123, 1007-1013.
36. Schneider IC, Hays CK, Waterman CM (2009). Epidermal growth factorinduced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion. Mol Biol Cell 20, 3155-3167.
37. Serrels B, Serrels A, Brunton VG, Holt M, McLean GW, Gray CH, Jones GE, Frame MC (2007). Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol 9, 1046-1056.
38. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, Cooper B, Kath JC, Roberts WG, et al. (2007). Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282, 14845-14852.
39. Thievessen I, Thompson PM, Berlemont S, Plevock KM, Plotnikov SV, Zemljic-Harpf A, Ross RS, Davidson MW, Danuser G, Campbell SL, et al. (2013). Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J Cell Biol 202, 163-177.
40. Tilghman RW, Slack-Davis JK, Sergina N, Martin KH, Iwanicki M, Hershey ED, Beggs HE, Reichardt LF, Parsons JT (2005). Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J Cell Sci 118, 2613-2623.
41. Tomar A, Lawson C, Ghassemian M, Schlaepfer DD (2012). Cortactin as a target for FAK in the regulation of focal adhesion dynamics. PLoS One 7, e44041.
42. Vallotton P, Ponti A, Waterman-Storer CM, Salmon ED, Danuser G (2003). Recovery, visualization, and analysis of actin and tubulin polymer flow in live cells: a fluorescent speckle microscopy study. Biophys J 85, 1289-1306.
43. Wang HB, Dembo M, Hanks SK, Wang Y (2001). Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci USA 98, 11295-11300.
44. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF (2004). FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6, 154-161.
45. Welch MD, Mallavarapu A, Rosenblatt J, Mitchison TJ (1997). Actin dynamics in vivo. Curr Opin Cell Biol 9, 54-61.
46. Wu C, Haynes EM, Asokan SB, Simon JM, Sharpless NE, Baldwin AS, Davis IJ, Johnson GL, Bear JE (2013). Loss of Arp2/3 induces an NF-kB-dependent, nonautonomous effect on chemotactic signaling. J Cell Biol 203, 907-916.
47. Wu X, Suetsugu S, Cooper LA, Takenawa T, Guan J-L (2004). Focal adhesion kinase regulation of N-WASP subcellular localization and function. J Biol Chem 279, 9565-9576.
48. Zaidel-Bar R, Milo R, Kam Z, Geiger B (2007). A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120, 137-148.