Mechanism of Focal Adhesion Kinase Mechanosensing

PLoS Computational Biology

Volumn 11, Issue 11, 2015, Pages

  Zhou, Jing ^a   Aponte Santamaría, Camilo ^a   Sturm, Sebastian ^b   Bullerjahn, Jakob Tómas ^b   Bronowska, Agnieszka ^a   Gräter, Frauke ^a,c  

^a HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; BINDING SITES; ENZYMES; MECHANICAL STABILITY; SIGNALING;

BINDING-SITES; BIOCHEMICAL NETWORK; CELLULAR PROCESS; CYTOSKELETONS; FOCAL ADHESION KINASE; FOCAL ADHESIONS; MECHANOSENSING; MECHANOSENSORS; NETWORK SIMULATION; TENSILE FORCES;

MOLECULAR DYNAMICS;

EZRIN; FOCAL ADHESION KINASE; MOESIN; N TERMINAL THREE LOBED 4.1 EZRIN RADIXIN MOESIN; PHOSPHATE; PHOSPHOINOSITIDE PHOSPHATIDYLINSOSITOL 4,5 BIS PHOSPHATE; RADIXIN; RAS PROTEIN; TYROSINE; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN;

ALPHA HELIX; ARTICLE; BINDING SITE; BIOMECHANICS; CELL NUCLEUS; CYTOSKELETON; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME STABILITY; FOCAL ADHESION; FORCE; MECHANOTRANSDUCTION; MEMBRANE BIOLOGY; MOLECULAR DYNAMICS; PROTEIN DOMAIN; PROTEIN TARGETING; SIMULATION; BIOLOGICAL MODEL; BIOLOGY; CHEMISTRY; METABOLISM; PHYSIOLOGY;

COMPUTATIONAL BIOLOGY; CYTOSKELETAL PROTEINS; CYTOSKELETON; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION;

EID: 84949194880     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004593     Document Type: Article

References (63)

1. Vogel V, Sheetz M, Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol. 2006 Apr;7(4):265–275. doi: 10.1038/nrm1890 16607289
2. Schiller HB, Fässler R, Mechanosensitivity and compositional dynamics of cell-matrix adhesions. EMBO Rep. 2013 Jun;14(6):509–519. doi: 10.1038/embor.2013.49 23681438
3. Oakes PW, Gardel ML, Stressing the limits of focal adhesion mechanosensitivity. Curr Opin Cell Biol. 2014 Oct;30:68–73. doi: 10.1016/j.ceb.2014.06.003 24998185
4. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, et al. Nanoscale architecture of integrin-based cell adhesions. Nature. 2010 Nov;468(7323):580–584. doi: 10.1038/nature09621 21107430
5. Zhu J, Luo BH, Xiao T, Zhang C, Nishida N, Springer TA, Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell. 2008 Dec;32(6):849–861. doi: 10.1016/j.molcel.2008.11.018 19111664
6. 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 Jan;323(5914):638–641. doi: 10.1126/science.1162912 19179532
7. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, et al. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell. 2006 Dec;127(5):1015–1026. doi: 10.1016/j.cell.2006.09.044 17129785
8. Schaller MD, Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci. 2010 Apr;123(Pt 7):1007–1013. doi: 10.1242/jcs.045112 20332118
9. Zhao J, Guan JL, Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 2009 Jun;28(1–2):35–49. doi: 10.1007/s10555-008-9165-4 19169797
10. Vadali K, Cai X, Schaller MD, Focal adhesion kinase: an essential kinase in the regulation of cardiovascular functions. IUBMB Life. 2007 Nov;59(11):709–716. doi: 10.1080/15216540701694245 17968709
11. Schlaepfer DD, Mitra SK, Ilic D, Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta. 2004 Jul;1692(2–3):77–102. doi: 10.1016/j.bbamcr.2004.04.008 15246681
12. Calalb MB, Polte TR, Hanks SK, Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol. 1995 Feb;15(2):954–963. doi: 10.1128/MCB.15.2.954 7529876
13. Cooper LA, Shen TL, Guan JL, Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol Cell Biol. 2003 Nov;23(22):8030–8041. doi: 10.1128/MCB.23.22.8030-8041.2003 14585964
14. Lietha D, Cai X, Ceccarelli DFJ, Li Y, Schaller MD, Eck MJ, Structural basis for the autoinhibition of focal adhesion kinase. Cell. 2007 Jun;129(6):1177–1187. doi: 10.1016/j.cell.2007.05.041 17574028
15. Schaller MD, Paxillin: a focal adhesion-associated adaptor protein. Oncogene. 2001 Oct;20(44):6459–6472. doi: 10.1038/sj.onc.1204786 11607845
16. Chen SY, Chen HC, Direct interaction of focal adhesion kinase (FAK) with Met is required for FAK to promote hepatocyte growth factor-induced cell invasion. Mol Cell Biol. 2006 Jul;26(13):5155–5167. doi: 10.1128/MCB.02186-05 16782899
17. Plaza-Menacho I, Morandi A, Mologni L, Boender P, Gambacorti-Passerini C, Magee AI, et al. Focal adhesion kinase (FAK) binds RET kinase via its FERM domain, priming a direct and reciprocal RET-FAK transactivation mechanism. J Biol Chem. 2011 May;286(19):17292–17302. doi: 10.1074/jbc.M110.168500 21454698
18. Goñi GM, Epifano C, Boskovic J, Camacho-Artacho M, Zhou J, Bronowska A, et al. Phosphatidylinositol 4,5-bisphosphate triggers activation of focal adhesion kinase by inducing clustering and conformational changes. Proc Natl Acad Sci U S A. 2014 Aug;111(31):E3177–E3186. doi: 10.1073/pnas.1317022111 25049397
19. Cai X, Lietha D, Ceccarelli DF, Karginov AV, Rajfur Z, Jacobson K, et al. Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol Cell Biol. 2008 Jan;28(1):201–214. doi: 10.1128/MCB.01324-07 17967873
20. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, Voronov S, et al. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature. 2002 Nov;420(6911):85–89. doi: 10.1038/nature01147 12422219
21. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA, Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature. 2002 Nov;420(6911):89–93. doi: 10.1038/nature01082 12422220
22. McLaughlin S, Murray D, Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 2005 Dec;438(7068):605–611. doi: 10.1038/nature04398 16319880
23. van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI, Hubrich BE, et al. Membrane protein sequestering by ionic protein-lipid interactions. Nature. 2011 Nov;479(7374):552–555. doi: 10.1038/nature10545 22020284
24. Ellenbroek WG, Wang YH, Christian DA, Discher DE, Janmey PA, Liu AJ, Divalent cation-dependent formation of electrostatic PIP2 clusters in lipid monolayers. Biophys J. 2011 Nov;101(9):2178–2184. doi: 10.1016/j.bpj.2011.09.039 22067156
25. Carvalho K, Ramos L, Roy C, Picart C, Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: characterization and functionality. Biophys J. 2008 Nov;95(9):4348–4360. doi: 10.1529/biophysj.107.126912 18502807
26. Giannone G, Rondé P, Gaire M, Beaudouin J, Haiech J, Ellenberg J, et al. Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J Biol Chem. 2004 Jul;279(27):28715–28723. doi: 10.1074/jbc.M404054200 15102844
27. Tomakidi P, Schulz S, Proksch S, Weber W, Steinberg T, Focal adhesion kinase (FAK) perspectives in mechanobiology: implications for cell behaviour. Cell Tissue Res. 2014 Sep;357(3):515–526. doi: 10.1007/s00441-014-1945-2 24988914
28. Li S, Kim M, Hu YL, Jalali S, Schlaepfer DD, Hunter T, et al. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J Biol Chem. 1997 Nov;272(48):30455–30462. doi: 10.1074/jbc.272.48.30455 9374537
29. Li S, Butler P, Wang Y, Hu Y, Han DC, Usami S, et al. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc Natl Acad Sci U S A. 2002 Mar;99(6):3546–3551. doi: 10.1073/pnas.052018099 11891289
30. Wang HB, Dembo M, Hanks SK, Wang Y, Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci U S A. 2001 Sep;98(20):11295–11300. doi: 10.1073/pnas.201201198 11572981
31. Polacheck WJ, German AE, Mammoto A, Ingber DE, Kamm RD, Mechanotransduction of fluid stresses governs 3D cell migration. Proc Natl Acad Sci U S A. 2014 Feb;111(7):2447–2452. doi: 10.1073/pnas.1316848111 24550267
32. Chaturvedi LS, Marsh HM, Basson MD, Src and focal adhesion kinase mediate mechanical strain-induced proliferation and ERK1/2 phosphorylation in human H441 pulmonary epithelial cells. Am J Physiol Cell Physiol. 2007 May;292(5):C1701–C1713. doi: 10.1152/ajpcell.00529.2006 17215324
33. Seong J, Tajik A, Sun J, Guan JL, Humphries MJ, Craig SE, et al. Distinct biophysical mechanisms of focal adhesion kinase mechanoactivation by different extracellular matrix proteins. Proc Natl Acad Sci U S A. 2013 Nov;110(48):19372–19377. doi: 10.1073/pnas.1307405110 24222685
34. von Castelmur E, Strümpfer J, Franke B, Bogomolovas J, Barbieri S, Qadota H, et al. Identification of an N-terminal inhibitory extension as the primary mechanosensory regulator of twitchin kinase. Proc Natl Acad Sci U S A. 2012 Aug;109(34):13608–13613. doi: 10.1073/pnas.1200697109 22869697
35. Gräter F, Shen J, Jiang H, Gautel M, Grubmüller H, Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys J. 2005 Feb;88(2):790–804. doi: 10.1529/biophysj.104.052423 15531631
36. Puchner EM, Alexandrovich A, Kho AL, Hensen U, Schäfer LV, Brandmeier B, et al. Mechanoenzymatics of titin kinase. Proc Natl Acad Sci U S A. 2008 Sep;105(36):13385–13390. doi: 10.1073/pnas.0805034105 18765796
37. Mofrad MRK, Golji J, Abdul Rahim NA, Kamm RD, Force-induced unfolding of the focal adhesion targeting domain and the influence of paxillin binding. Mech Chem Biosyst. 2004 Dec;1(4):253–265. 16783922
38. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics. 2013 Apr;29(7):845–854. doi: 10.1093/bioinformatics/btt055 23407358
39. Grubmüller H, Heymann B, Tavan P, Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 1996 Feb;271(5251):997–999. doi: 10.1126/science.271.5251.997
40. Sotomayor M, Schulten K, Single-molecule experiments in vitro and in silico. Science. 2007 May;316(5828):1144–1148. doi: 10.1126/science.1137591 17525328
41. Kadaré G, Gervasi N, Brami-Cherrier K, Blockus H, Messari SE, Arold ST, et al. Conformational dynamics of the focal adhesion targeting domain control specific functions of focal adhesion kinase in cells. J Biol Chem. 2015 Jan;290(1):478–491. doi: 10.1074/jbc.M114.593632
42. Brami-Cherrier K, Gervasi N, Arsenieva D, Walkiewicz K, Boutterin MC, Ortega A, et al. FAK dimerization controls its kinase-dependent functions at focal adhesions. EMBO J. 2014 Feb;33(4):356–370. doi: 10.1002/embj.201386399 24480479
43. Krivobokova T, Briones R, Hub JS, Munk A, de Groot BL, Partial least-squares functional mode analysis: application to the membrane proteins AQP1, Aqy1, and CLC-ec1. Biophys J. 2012 Aug;103(4):786–796. doi: 10.1016/j.bpj.2012.07.022 22947940
44. Hummer G, Szabo A, Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J. 2003 Jul;85(1):5–15. doi: 10.1016/S0006-3495(03)74449-X 12829459
45. Bullerjahn JT, Sturm S, Kroy K, Theory of rapid force spectroscopy. Nat Commun. 2014;5:4463. doi: 10.1038/ncomms5463 25079911
46. Nguyen DH, Webb DJ, Catling AD, Song Q, Dhakephalkar A, Weber MJ, et al. Urokinase-type plasminogen activator stimulates the Ras/Extracellular signal-regulated kinase (ERK) signaling pathway and MCF-7 cell migration by a mechanism that requires focal adhesion kinase, Src, and Shc. Rapid dissociation of GRB2/Sps-Shc complex is associated with the transient phosphorylation of ERK in urokinase-treated cells. J Biol Chem. 2000 Jun;275(25):19382–19388. Available from: http://dx.doi.org/10.1074/jbc.M909575199. 10777511
47. Schlaepfer DD, Jones KC, Hunter T, Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol Cell Biol. 1998 May;18(5):2571–2585. doi: 10.1128/MCB.18.5.2571 9566877
48. Kholodenko BN, Demin OV, Moehren G, Hoek JB, Quantification of short term signaling by the epidermal growth factor receptor. J Biol Chem. 1999 Oct;274(42):30169–30181. doi: 10.1074/jbc.274.42.30169 10514507
49. Hatakeyama M, Kimura S, Naka T, Kawasaki T, Yumoto N, Ichikawa M, et al. A computational model on the modulation of mitogen-activated protein kinase (MAPK) and Akt pathways in heregulin-induced ErbB signalling. Biochem J. 2003 Jul;373(Pt 2):451–463. doi: 10.1042/BJ20021824 12691603
50. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, Simus N, et al. COPASI–a COmplex PAthway SImulator. Bioinformatics. 2006 Dec;22(24):3067–3074. doi: 10.1093/bioinformatics/btl485 17032683
51. James DJ, Khodthong C, Kowalchyk JA, Martin TFJ, Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol. 2008 Jul;182(2):355–366. doi: 10.1083/jcb.200801056 18644890
52. Costescu BI, Gräter F, Time-resolved force distribution analysis. BMC Biophys. 2013;6(1):5. doi: 10.1186/2046-1682-6-5 24499624
53. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE, Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 1997 May;276(5315):1109–1112. doi: 10.1126/science.276.5315.1109 9148804
54. Lee SE, Kamm RD, Mofrad MRK, Force-induced activation of talin and its possible role in focal adhesion mechanotransduction. J Biomech. 2007;40(9):2096–2106. doi: 10.1016/j.jbiomech.2007.04.006 17544431
55. Hytönen VP, Vogel V, How force might activate talin’s vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput Biol. 2008 Feb;4(2):e24. doi: 10.1371/journal.pcbi.0040024 18282082
56. Golji J, Mofrad MRK, A molecular dynamics investigation of vinculin activation. Biophys J. 2010 Aug;99(4):1073–1081. doi: 10.1016/j.bpj.2010.05.024 20712990
57. Toutant M, Costa A, Studler JM, Kadaré G, Carnaud M, Girault JA, Alternative splicing controls the mechanisms of FAK autophosphorylation. Mol Cell Biol. 2002 Nov;22(22):7731–7743. doi: 10.1128/MCB.22.22.7731-7743.2002 12391143
58. Rief M, Pascual J, Saraste M, Gaub HE, Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol. 1999 Feb;286(2):553–561. doi: 10.1006/jmbi.1998.2466 9973570
59. Ritt M, Guan JL, Sivaramakrishnan S, Visualizing and manipulating focal adhesion kinase regulation in live cells. J Biol Chem. 2013 Mar;288(13):8875–8886. doi: 10.1074/jbc.M112.421164 23393139
60. Bisswanger H, Enzyme Kinetics: Section 2.1–2.5. Wiley-VCH Verlag GmbH & Co. KGaA; 2008. p. 59–124. Available from: http://dx.doi.org/10.1002/9783527622023.ch2a.
61. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature. 2010 Jul;466(7303):263–266. doi: 10.1038/nature09198 20613844
62. Wang X, Ha T, Defining single molecular forces required to activate integrin and notch signaling. Science. 2013 May;340(6135):991–994. doi: 10.1126/science.1231041 23704575
63. Humphrey W, Dalke A, Schulten K, VMD: visual molecular dynamics. J Mol Graph. 1996 Feb;14(1):33–8, 27–8. doi: 10.1016/0263-7855(96)00018-5 8744570