Modulation of focal adhesion constituents and their down-stream events by EGF: On the cross-talk of integrins and growth factor receptors

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 10, 2015, Pages 2183-2198

  Eberwein, Philipp ^a   Laird, Dougal ^a   Schulz, Simon ^a   Reinhard, Thomas ^a   Steinberg, Thorsten ^a   Tomakidi, Pascal ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cell motility; Epidermal growth factor; Focal adhesions; Growth factor receptors; Integrins; Mechanotransduction; Zyxin

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; GROWTH FACTOR RECEPTOR; HERBIMYCIN A; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN TYROSINE KINASE; TYROSINE; ZYXIN; EGFR PROTEIN, HUMAN; FOCAL ADHESION KINASE 1; GFR PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PTK2 PROTEIN, HUMAN;

ARTICLE; CELL MOTILITY; CONTROLLED STUDY; FLUORESCENCE IMAGING; FOCAL ADHESION; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; TRANSFORMED CELL LINE;

CELL LINE, TRANSFORMED; EPIDERMAL GROWTH FACTOR; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTEGRINS; KERATINOCYTES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84938100073     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.06.004     Document Type: Article

References (67)

1. Burridge K., Chrzanowska-Wodnicka M. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 1996, 12:463-518.
2. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 2010, 11:633-643.
3. Zaidel-Bar R., Ballestrem C., Kam Z., Geiger B. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 2003, 116:4605-4613.
4. Hirata H., Tatsumi H., Sokabe M. Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J. Cell Sci. 2008, 121:2795-2804.
5. Balanis N., Carlin C.R. Mutual cross-talk between fibronectin integrins and the EGF receptor: molecular basis and biological significance. Cell Logist. 2012, 2:46-51.
6. Ciobanasu C., Faivre B., Le Clainche C. Actin dynamics associated with focal adhesions. Int. J. Cell Biol. 2012, 2012:941292.
7. Oakes P.W., Gardel M.L. Stressing the limits of focal adhesion mechanosensitivity. Curr. Opin. Cell Biol. 2014, 30:68-73.
8. Cukierman E., Pankov R., Stevens D.R., Yamada K.M. Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712.
9. Geiger B., Spatz J.P., Bershadsky A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10:21-33.
10. Wells A. EGF receptor. Int. J. Biochem. Cell Biol. 1999, 31:637-643.
11. Dikic I. Mechanisms controlling EGF receptor endocytosis and degradation. Biochem. Soc. Trans. 2003, 31:1178-1181.
12. Chen P., Xie H., Sekar M.C., Gupta K., Wells A. Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J. Cell Biol. 1994, 127:847-857.
13. Schoeberl B., Eichler-Jonsson C., Gilles E.D., Muller G. Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat. Biotechnol. 2002, 20:370-375.
14. Xie H., Pallero M.A., Gupta K., Chang P., Ware M.F., Witke W., Kwiatkowski D.J., Lauffenburger D.A., Murphy-Ullrich J.E., Wells A. EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLC gamma signaling pathway. J. Cell Sci. 1998, 111(5):615-624.
15. Wu X., Reddy D.S. Integrins as receptor targets for neurological disorders. Pharmacol. Ther. 2012, 134:68-81.
16. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell Biol. 2000, 2:E231-E236.
17. Parsons J.T., Parsons S.J. Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr. Opin. Cell Biol. 1997, 9:187-192.
18. Moro L., Dolce L., Cabodi S., Bergatto E., Boeri Erba E., Smeriglio M., Turco E., Retta S.F., Giuffrida M.G., Venturino M., Godovac-Zimmermann J., Conti A., Schaefer E., Beguinot L., Tacchetti C., Gaggini P., Silengo L., Tarone G., Defilippi P. Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J. Biol. Chem. 2002, 277:9405-9414.
19. Comoglio P.M., Boccaccio C., Trusolino L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr. Opin. Cell Biol. 2003, 15:565-571.
20. Sato K. Cellular functions regulated by phosphorylation of EGFR on Tyr845. Int. J. Mol. Sci. 2013, 14:10761-10790.
21. Miyamoto S., Teramoto H., Gutkind J.S., Yamada K.M. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J. Cell Biol. 1996, 135:1633-1642.
22. Hauck C.R., Hsia D.A., Schlaepfer D.D. Focal adhesion kinase facilitates platelet-derived growth factor-BB-stimulated ERK2 activation required for chemotaxis migration of vascular smooth muscle cells. J. Biol. Chem. 2000, 275:41092-41099.
23. Sieg D.J., Hauck C.R., Ilic D., Klingbeil C.K., Schaefer E., Damsky C.H., Schlaepfer D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2000, 2:249-256.
24. Yamada K.M., Even-Ram S. Integrin regulation of growth factor receptors. Nat. Cell Biol. 2002, 4:E75-E76.
25. Playford M.P., Schaller M.D. The interplay between Src and integrins in normal and tumor biology. Oncogene 2004, 23:7928-7946.
26. Ivaska J., Heino J. Interplay between cell adhesion and growth factor receptors: from the plasma membrane to the endosomes. Cell Tissue Res. 2010, 339:111-120.
27. Balanis N., Yoshigi M., Wendt M.K., Schiemann W.P., Carlin C.R. beta3 integrin-EGF receptor cross-talk activates p190RhoGAP in mouse mammary gland epithelial cells. Mol. Biol. Cell 2011, 22:4288-4301.
28. Schulz S., Steinberg T., Beck D., Tomakidi P., Accardi R., Tommasino M., Reinhard T., Eberwein P. Generation and evaluation of a human corneal model cell system for ophthalmologic issues using the HPV16 E6/E7 oncogenes as uniform immortalization platform. Differentiation 2013, 85:161-172.
29. Moers K., Steinberg T., Schlunck G., Reinhard T., Tomakidi P., Eberwein P. Substrate elasticity as biomechanical modulator of tissue homeostatic parameters in corneal keratinocytes. Exp. Cell Res. 2013, 319:1889-1901.
30. Burgess A., Vigneron S., Brioudes E., Labbé J.-C., Lorca T., Castro A. Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc. Natl. Acad. Sci. 2010, 107:12564-12569.
31. Guo L., Kozlosky C.J., Ericsson L.H., Daniel T.O., Cerretti D.P., Johnson R.S. Studies of ligand-induced site-specific phosphorylation of epidermal growth factor receptor. J. Am. Soc. Mass Spectrom. 2003, 14:1022-1031.
32. Carpenter G., Cohen S. Epidermal growth factor. J. Biol. Chem. 1990, 265:7709-7712.
33. Sato K., Sato A., Aoto M., Fukami Y. c-Src phosphorylates epidermal growth factor receptor on tyrosine 845. Biochem. Biophys. Res. Commun. 1995, 215:1078-1087.
34. Biscardi J.S., Maa M.C., Tice D.A., Cox M.E., Leu T.H., Parsons S.J. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 1999, 274:8335-8343.
35. Tice D.A., Biscardi J.S., Nickles A.L., Parsons S.J. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1415-1420.
36. Sato K., Sato A., Aoto M., Fukami Y. Site-specific association of c-Src with epidermal growth factor receptor in A431 cells. Biochem. Biophys. Res. Commun. 1995, 210:844-851.
37. Eberwein P., Steinberg T., Schulz S., Zimmermann D., Accardi R., Beck D., Reinhard T., Tomakidi P. Expression of keratinocyte biomarkers is governed by environmental biomechanics. Eur. J. Cell Biol. 2011, 90:1029-1040.
38. Schulz S., Beck D., Laird D., Steinberg T., Tomakidi P., Reinhard T., Eberwein P. Natural corneal cell-based microenvironment as prerequisite for balanced 3D corneal epithelial morphogenesis: a promising animal experiment-abandoning tool in ophthalmology. Tissue Eng. Part C Methods 2014, 20:297-307.
39. Schwartz M.A., Ginsberg M.H. Networks and crosstalk: integrin signalling spreads. Nat. Cell Biol. 2002, 4:E65-E68.
40. Guo W., Giancotti F.G. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 2004, 5:816-826.
41. Frame M.C., Patel H., Serrels B., Lietha D., Eck M.J. The FERM domain: organizing the structure and function of FAK. Nat. Rev. Mol. Cell Biol. 2010, 11:802-814.
42. Wu L., Bernard-Trifilo J.A., Lim Y., Lim S.T., Mitra S.K., Uryu S., Chen M., Pallen C.J., Cheung N.K., Mikolon D., Mielgo A., Stupack D.G., Schlaepfer D.D. Distinct FAK-Src activation events promote alpha5beta1 and alpha4beta1 integrin-stimulated neuroblastoma cell motility. Oncogene 2008, 27:1439-1448.
43. Miranti C.K., Brugge J.S. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 2002, 4:E83-E90.
44. Brunton V.G., Frame M.C. Src and focal adhesion kinase as therapeutic targets in cancer. Curr. Opin. Pharmacol. 2008, 8:427-432.
45. McKay M.M., Morrison D.K. Integrating signals from RTKs to ERK/MAPK. Oncogene 2007, 26:3113-3121.
46. Tomar A., Lim S.T., Lim Y., Schlaepfer D.D. A FAK-p120RasGAP-p190RhoGAP complex regulates polarity in migrating cells. J. Cell Sci. 2009, 122:1852-1862.
47. Tatosyan A.G., Mizenina O.A. Kinases of the Src family: structure and functions. Biochemistry 2000, 65:49-58.
48. Haskell M.D., Nickles A.L., Agati J.M., Su L., Dukes B.D., Parsons S.J. Phosphorylation of p190 on Tyr1105 by c-Src is necessary but not sufficient for EGF-induced actin disassembly in C3H10T1/2 fibroblasts. J. Cell Sci. 2001, 114:1699-1708.
49. Zebda N., Dubrovskyi O., Birukov K.G. Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc. Res. 2012, 83:71-81.
50. Sulzmaier F.J., Jean C., Schlaepfer D.D. FAK in cancer: mechanistic findings and clinical applications. Nat. Rev. Cancer 2014, 14:598-610.
51. 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, 357:515-526.
52. Haas M., Wang H., Tian J., Xie Z. Src-mediated inter-receptor cross-talk between the Na+/K+-ATPase and the epidermal growth factor receptor relays the signal from ouabain to mitogen-activated protein kinases. J. Biol. Chem. 2002, 277:18694-18702.
53. Murakami Y., Fukazawa H., Mizuno S., Uehara Y. Effect of herbimycin A on tyrosine kinase receptors and platelet derived growth factor (PDGF)-induced signal transduction. Biol. Pharm. Bull. 1998, 21:1030-1035.
54. Murakami Y., Fukazawa H., Mizuno S., Uehara Y. Conversion of epidermal growth factor (EGF) into a stimulatory ligand for A431-cell growth by herbimycin A by decreasing the level of expression of EGF receptor. Biochem. J. 1994, 301(Pt 1):57-62.
55. Cao Y., Baig M.R., Hamm L.L., Wu K., Simon E.E. Growth factors stimulate kidney proximal tubule cell migration independent of augmented tyrosine phosphorylation of focal adhesion kinase. Biochem. Biophys. Res. Commun. 2005, 328:560-566.
56. Rice D.C., Dobrian A.D., Schriver S.D., Prewitt R.L. Src autophosphorylation is an early event in pressure-mediated signaling pathways in isolated resistance arteries. Hypertension 2002, 39:502-507.
57. Weng Y.I., Shukla S.D. Angiotensin II activation of focal adhesion kinase and pp60c-Src in relation to mitogen-activated protein kinases in hepatocytes. Biochim. Biophys. Acta 2002, 1589:285-297.
58. Huang Y., Chang Y. Epidermal growth factor receptor (EGFR) phosphorylation, signaling and trafficking in prostate cancer. Prostate Cancer from Bench to Bedside 2011, In Tech. P.E. Spiess (Ed.).
59. Mori S., Tanaka K., Kanaki H., Nakao M., Anan T., Yokote K., Tamura K., Saito Y. Identification of an ubiquitin-ligation system for the epidermal-growth-factor receptor-herbimycin A induces in vitro ubiquitination in rabbit-reticulocyte lysate. Eur. J. Biochem. 1997, 247:1190-1196.
60. Arias-Salgado E.G., Lizano S., Sarkar S., Brugge J.S., Ginsberg M.H., Shattil S.J. Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13298-13302.
61. Michael K.E., Dumbauld D.W., Burns K.L., Hanks S.K., García A.J. Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. Mol. Biol. Cell 2009, 20:2508-2519.
62. Yamanaka I., Koizumi M., Baba T., Yamashita S., Suzuki T., Kudo R. Epidermal growth factor increased the expression of alpha2beta1-integrin and modulated integrin-mediated signaling in human cervical adenocarcinoma cells. Exp. Cell Res. 2003, 286:165-174.
63. Chan A.Y., Raft S., Bailly M., Wyckoff J.B., Segall J.E., Condeelis J.S. EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. J. Cell Sci. 1998, 111(Pt 2):199-211.
64. Schneider I.C., Hays C.K., Waterman C.M. Epidermal growth factor-induced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion. Mol. Biol. Cell 2009, 20:3155-3167.
65. Bernards A., Settleman J. GAP control: regulating the regulators of small GTPases. Trends Cell Biol. 2004, 14:377-385.
66. Hu K.Q., Settleman J. Tandem SH2 binding sites mediate the RasGAP-RhoGAP interaction: a conformational mechanism for SH3 domain regulation. EMBO J. 1997, 16:473-483.
67. Hernandez S.E., Settleman J., Koleske A.J. Adhesion-dependent regulation of p190RhoGAP in the developing brain by the Abl-related gene tyrosine kinase. Curr. Biol. 2004, 14:691-696.