Cortactin as a Target for FAK in the Regulation of Focal Adhesion Dynamics

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Tomar, Alok ^a,c   Lawson, Christine ^a   Ghassemian, Majid ^b   Schlaepfer, David D ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTACTIN; FOCAL ADHESION KINASE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; PHENYLALANINE; TYROSINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; C TERMINAL PROLINE RICH DOMAIN 2; C TERMINAL PROLINE RICH DOMAIN 3; CELL MOTILITY; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; FOCAL ADHESION; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL ADHESION; CELL MOVEMENT; CORTACTIN; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE KNOCKDOWN TECHNIQUES; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PHENYLALANINE; PHOSPHORYLATION; PHOSPHOTYROSINE; PROLINE-RICH PROTEIN DOMAINS; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84865579696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044041     Document Type: Article

References (59)

1. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.
2. Parsons JT, Horwitz AR, Schwartz MA, (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11: 633-643.
3. Hu K, Ji L, Applegate KT, Danuser G, Waterman-Storer CM, (2007) Differential transmission of actin motion within focal adhesions. Science 315: 111-115.
4. Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM, (2010) Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol 26: 315-333.
5. Ren G, Crampton MS, Yap AS, (2009) Cortactin: Coordinating adhesion and the actin cytoskeleton at cellular protrusions. Cell Motil Cytoskeleton 66: 865-873.
6. Kirkbride KC, Sung BH, Sinha S, Weaver AM, (2011) Cortactin: a multifunctional regulator of cellular invasiveness. Cell Adh Migr 5: 187-198.
7. Lua BL, Low BC, (2005) Cortactin phosphorylation as a switch for actin cytoskeletal network and cell dynamics control. FEBS Lett 579: 577-585.
8. Lai FP, Szczodrak M, Oelkers JM, Ladwein M, Acconcia F, et al. (2009) Cortactin promotes migration and platelet-derived growth factor-induced actin reorganization by signaling to Rho-GTPases. Mol Biol Cell 20: 3209-3223.
9. Kruchten AE, Krueger EW, Wang Y, McNiven MA, (2008) Distinct phospho-forms of cortactin differentially regulate actin polymerization and focal adhesions. Am J Physiol Cell Physiol 295: C1113-1122.
10. Ammer AG, Weed SA, (2008) Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 65: 687-707.
11. Lapetina S, Mader CC, Machida K, Mayer BJ, Koleske AJ, (2009) Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion. J Cell Biol 185: 503-519.
12. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, et al. (2009) Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 186: 571-587.
13. Lawson C, Lim ST, Uryu S, Chen XL, Calderwood DA, et al. (2012) FAK promotes recruitment of talin to nascent adhesions to control cell motility. J Cell Biol 196: 223-232.
14. Polte TR, Hanks SK, (1995) Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc Natl Acad Sci USA 92: 10678-10682.
15. Schaller MD, (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123: 1007-1013.
16. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, et al. (2004) FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6: 154-161.
17. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, et al. (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282: 14845-14852.
18. Lim ST, Chen XL, Tomar A, Miller NL, Yoo J, et al. (2010) Knock-in mutation reveals an essential role for focal adhesion kinase activity in blood vessel morphogenesis and cell motility-polarity but not cell proliferation. J Biol Chem 285: 21526-21536.
19. Tomar A, Schlaepfer DD, (2009) Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21: 676-683.
20. Wu L, Bernard-Trifilo JA, Lim Y, Lim ST, Mitra SK, et al. (2008) Distinct FAK-Src activation events promote α5β1 and α4β1 integrin-stimulated neuroblastoma cell motility. Oncogene 27: 1439-1448.
21. Holinstat M, Knezevic N, Broman M, Samarel AM, Malik AB, et al. (2006) Suppression of RhoA activity by focal adhesion kinase-induced activation of p190RhoGAP: role in regulation of endothelial permeability. J Biol Chem 281: 2296-2305.
22. Defilippi P, Di Stefano P, Cabodi S, (2006) p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol 16: 257-263.
23. 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.
24. Wu X, Suetsugu S, Cooper LA, Takenawa T, Guan JL, (2004) Focal adhesion kinase regulation of N-WASP subcellular localization and function. J Biol Chem 279: 9565-9576.
25. Izaguirre G, Aguirre L, Hu YP, Lee HY, Schlaepfer DD, et al. (2001) The cytoskeletal/non-muscle isoform of α-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. J Biol Chem 276: 28676-28685.
26. Mitra SK, Schlaepfer DD, (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18: 516-523.
27. Cary LA, Han DC, Polte TR, Hanks SK, Guan J-L, (1998) Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 140: 211-221.
28. Sieg DJ, Hauck CR, Schlaepfer DD, (1999) Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 112: 2677-2691.
29. Pylayeva Y, Gillen KM, Gerald W, Beggs HE, Reichardt LF, et al. (2009) Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J Clin Invest 119: 252-266.
30. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P, Defilippi P, (2010) Integrin signalling adaptors: not only figurants in the cancer story. Nat Rev Cancer 10: 858-870.
31. Meenderink LM, Ryzhova LM, Donato DM, Gochberg DF, Kaverina I, et al. (2010) P130Cas Src-binding and substrate domains have distinct roles in sustaining focal adhesion disassembly and promoting cell migration. PLoS One 5: e13412.
32. Wang Y, McNiven MA, (2012) Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J Cell Biol 196: 375-385.
33. Hildebrand JD, Taylor JM, Parsons JT, (1996) An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol Cell Biol 16: 3169-3178.
34. Ren XR, Du QS, Huang YZ, Ao SZ, Mei L, et al. (2001) Regulation of CDC42 GTPase by proline-rich tyrosine kinase 2 interacting with PSGAP, a novel pleckstrin homology and Src homology 3 domain containing rhoGAP protein. J Cell Biol 152: 971-984.
35. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, et al. (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 118: 2189-2200.
36. Tegtmeyer N, Wittelsberger R, Hartig R, Wessler S, Martinez-Quiles N, et al. (2011) Serine phosphorylation of cortactin controls focal adhesion kinase activity and cell scattering induced by Helicobacter pylori. Cell Host Microbe 9: 520-531.
37. Eke I, Deuse Y, Hehlgans S, Gurtner K, Krause M, et al. (2012) β1 Integrin/FAK/cortactin signaling is essential for human head and neck cancer resistance to radiotherapy. J Clin Invest 122: 1529-1540.
38. Wang W, Liu Y, Liao K, (2011) Tyrosine phosphorylation of cortactin by the FAK-Src complex at focal adhesions regulates cell motility. BMC Cell Biology 12: 49.
39. Meiler E, Nieto-Pelegrin E, Martinez-Quiles N, (2012) Cortactin tyrosine phosphorylation promotes its deacetylation and inhibits cell spreading. PLoS One 7: e33662.
40. Corsi JM, Houbron C, Billuart P, Brunet I, Bouvree K, et al. (2009) Autophosphorylation-independent and dependent functions of Focal Adhesion Kinase during development. J Biol Chem 284: 34769-34776.
41. Tomar A, Lim ST, Lim Y, Schlaepfer DD, (2009) A FAK-p120RasGAP-p190RhoGAP complex regulates polarity in migrating cells. J Cell Sci 122: 1852-1862.
42. Hauck CR, Hunter T, Schlaepfer DD, (2001) The v-Src SH3 domain facilitates a cell adhesion-independent association with focal adhesion kinase. J Biol Chem 276: 17653-17662.
43. Berginski ME, Vitriol EA, Hahn KM, Gomez SM, (2011) High-resolution quantification of focal adhesion spatiotemporal dynamics in living cells. PLoS One 6: e22025.
44. Polte TR, Hanks SK, (1997) Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130Cas) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. Requirements for Src kinase activity and FAK proline-rich motifs. J Biol Chem 272: 5501-5509.
45. Schlaepfer DD, Hauck CR, Sieg DJ, (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478.
46. Boyle SN, Michaud GA, Schweitzer B, Predki PF, Koleske AJ, (2007) A critical role for cortactin phosphorylation by Abl-family kinases in PDGF-induced dorsal-wave formation. Curr Biol 17: 445-451.
47. Wu H, Parsons JT, (1993) Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J Cell Biol 120: 1417-1426.
48. Carragher NO, Westhoff MA, Fincham VJ, Schaller MD, Frame MC, (2003) A Novel Role for FAK as a Protease-Targeting Adaptor Protein. Regulation by p42 ERK and Src. Curr Biol 13: 1442-1450.
49. 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.
50. 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.
51. Iwanicki MP, Vomastek T, Tilghman RW, Martin KH, Banerjee J, et al. (2008) FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J Cell Sci 121: 895-905.
52. Serrels B, Serrels A, Brunton VG, Holt M, McLean GW, et al. (2007) Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol 9: 1046-1056.
53. Huang C, Ni Y, Wang T, Gao Y, Haudenschild CC, et al. (1997) Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J Biol Chem 272: 13911-13915.
54. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS, (2004) Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24: 5269-5280.
55. Okamura H, Resh MD, (1995) p80/85 cortactin associates with the Src SH2 domain and colocalizes with v-Src in transformed cells. J Biol Chem 270: 26613-26618.
56. Schlaepfer DD, Hou S, Lim ST, Tomar A, Yu H, et al. (2007) Tumor necrosis factor-α stimulates focal adhesion kinase activity required for mitogen-activated kinase-associated interleukin 6 expression. J Biol Chem 282: 17450-17459.
57. Lim ST, Chen XL, Lim Y, Hanson DA, Vo TT, et al. (2008) Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol Cell 29: 9-22.
58. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, et al. (2008) PyK2 and FAK connections to p190RhoGEF regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 180: 187-203.
59. Shevchenko A, Wilm M, Vorm O, Mann M, (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.