A biosensor generated via high-throughput screening quantifies cell edge Src dynamics

Nature Chemical Biology

Volumn 7, Issue 7, 2011, Pages 437-444

  Gulyani, Akash ^a   Vitriol, Eric ^a   Allen, Richard ^a   Wu, Jianrong ^a   Gremyachinskiy, Dmitriy ^a   Lewis, Steven ^a   Dewar, Brian ^a   Graves, Lee M ^a   Kay, Brian K ^b   Kuhlman, Brian ^a   Elston, Tim ^a   Hahn, Klaus M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; PROTEIN TYROSINE KINASE; SCAFFOLD PROTEIN;

ANIMAL CELL; ARTICLE; BIOSENSOR; EMBRYO; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SENSITIVITY ANALYSIS;

EID: 79959379424     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.585     Document Type: Article

References (50)

1. Nalbant, P., Hodgson, L., Kraynov, V., Toutchkine, A. & Hahn, K.M. Activation of endogenous Cdc42 visualized in living cells. Science 305, 1615-1619 (2004). (Pubitemid 39296355)
2. Toutchkine, A., Kraynov, V. & Hahn, K. Solvent-sensitive dyes to report protein conformational changes in living cells. J. Am. Chem. Soc. 125, 4132-4145 (2003). (Pubitemid 36512308)
3. Toutchkine, A., Nguyen, D.V. & Hahn, K.M. Merocyanine dyes with improved photostability. Org. Lett. 9, 2775-2777 (2007).
4. Toutchkine, A., Nguyen, D.V. & Hahn, K.M. Simple one-pot preparation of water-soluble, cysteine-reactive cyanine and merocyanine dyes for biological imaging. Bioconjug. Chem. 18, 1344-1348 (2007). (Pubitemid 47122659)
5. Koide, A., Bailey, C.W., Huang, X. & Koide, S. The fibronectin type III domain as a scaffold for novel binding proteins. J. Mol. Biol. 284, 1141-1151 (1998). (Pubitemid 28558562)
6. Karatan, E. et al. Molecular recognition properties of FN3 monobodies that bind the Src SH3 domain. Chem. Biol. 11, 835-844 (2004). (Pubitemid 38836899)
7. Koide, A., Abbatiello, S., Rothgery, L. & Koide, S. Probing protein conformational changes in living cells by using designer binding proteins: application to the estrogen receptor. Proc. Natl. Acad. Sci. USA 99, 1253-1258 (2002). (Pubitemid 34136479)
8. Sidhu, S.S. & Koide, S. Phage display for engineering and analyzing protein interaction interfaces. Curr. Opin. Struct. Biol. 17, 481-487 (2007). (Pubitemid 47451773)
9. Parsons, S.J. & Parsons, J.T. Src family kinases, key regulators of signal transduction. Oncogene 23, 7906-7909 (2004). (Pubitemid 39468849)
10. Thomas, S.M. & Brugge, J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13, 513-609 (1997). (Pubitemid 28034534)
11. Playford, M.P. & Schaller, M.D. The interplay between Src and integrins in normal and tumor biology. Oncogene 23, 7928-7946 (2004). (Pubitemid 39468852)
12. Bromann, P.A., Korkaya, H. & Courtneidge, S.A. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23, 7957-7968 (2004). (Pubitemid 39468854)
13. Ouyang, M., Sun, J., Chien, S. & Wang, Y. Determination of hierarchical relationship of Src and Rac at subcellular locations with FRET biosensors. Proc. Natl. Acad. Sci. USA 105, 14353-14358 (2008).
14. Wang, Y. et al. Visualizing the mechanical activation of Src. Nature 434, 1040-1045 (2005). (Pubitemid 40586054)
15. Ting, A.Y., Kain, K.H., Klemke, R.L. & Tsien, R.Y. Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells. Proc. Natl. Acad. Sci. USA 98, 15003-15008 (2001). (Pubitemid 34013959)
16. Cowan-Jacob, S.W. et al. The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure 13, 861-871 (2005). (Pubitemid 40804389)
17. Gardner, O.S., Dewar, B.J., Earp, H.S., Samet, J.M. & Graves, L.M. Dependence of peroxisome proliferator-activated receptor ligand-induced mitogen-activated protein kinase signaling on epidermal growth factor receptor transactivation. J. Biol. Chem. 278, 46261-46269 (2003). (Pubitemid 37452196)
18. Dewar, B.J. et al. Capacitative calcium entry contributes to the differential transactivation of the epidermal growth factor receptor in response to thiazolidinediones. Mol. Pharmacol. 72, 1146-1156 (2007). (Pubitemid 350012589)
19. Rizzo, M.A., Springer, G.H., Granada, B. & Piston, D.W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449 (2004). (Pubitemid 38451376)
20. Fosbrink, M., Aye-Han, N.N., Cheong, R., Levchenko, A. & Zhang, J. Visualization of JNK activity dynamics with a genetically encoded fluorescent biosensor. Proc. Natl. Acad. Sci. USA 107, 5459-5464 (2010).
21. Pertz, O., Hodgson, L., Klemke, R.L. & Hahn, K.M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072 (2006).
22. Glick, D., Barth, S. & Macleod, K.F. Autophagy: cellular and molecular mechanisms. J. Pathol. 221, 3-12 (2010).
23. Reis, R.C., Sorgine, M.H. & Coelho-Sampaio, T. A novel methodology for the investigation of intracellular proteolytic processing in intact cells. Eur. J. Cell Biol. 75, 192-197 (1998). (Pubitemid 28138183)
24. Panchuk-Voloshina, N. et al. Alexa dyes, a series of new fluorescent dyes that yield exceptionally bright, photostable conjugates. J. Histochem. Cytochem. 47, 1179-1188 (1999). (Pubitemid 29418323)
25. Hodgson, L., Shen, F. & Hahn, K. Biosensors for characterizing the dynamics of rho family GTPases in living cells. Curr. Protoc. Cell Biol. 46, 14.11.1-14.11.26 (2010).
26. Bright, G.R., Fisher, G.W., Rogowska, J. & Taylor, D.L. Fluorescence ratio imaging microscopy. Methods Cell Biol. 30, 157-192 (1989).
27. Buccione, R., Orth, J.D. & McNiven, M.A. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5, 647-657 (2004). (Pubitemid 39025065)
28. Veracini, L. et al. Two functionally distinct pools of Src kinases for PDGF receptor signalling. Biochem. Soc. Trans. 33, 1313-1315 (2005). (Pubitemid 41779675)
29. Veracini, L. et al. Two distinct pools of Src family tyrosine kinases regulate PDGF-induced DNA synthesis and actin dorsal ruffles. J. Cell Sci. 119, 2921-2934 (2006). (Pubitemid 44177870)
30. Sandilands E., Brunton V.G., Frame M.C. The membrane targeting and spatial activation of Src Yes and Fyn is influenced by palmitoylation and distinct RhoB/RhoD endosome requirements. J. Cell Sci. 120, 2555-2564 (2007). (Pubitemid 47323864)
31. Sandilands, E. et al. RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev. Cell 7, 855-869 (2004). (Pubitemid 39654730)
32. Cary, L.A., Klinghoffer, R.A., Sachsenmaier, C. & Cooper, J.A. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22, 2427-2440 (2002). (Pubitemid 34262966)
33. Fincham, V.J. & Frame, M.C. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 17, 81-92 (1998). (Pubitemid 28041050)
34. Frame M.C., Fincham V.J., Carragher N.O. & Wyke J.A. v-Srcs hold over actin and cell adhesions. Nat. Rev. Mol. Cell Biol. 3, 233-245 (2002). (Pubitemid 34619259)
35. Machacek, M. & Danuser, G. Morphodynamic profiling of protrusion phenotypes. Biophys. J. 90, 1439-1452 (2006).
36. Machacek, M. et al. Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103 (2009).
37. Renard, M. et al. Knowledge-based design of reagentless fluorescent biosensors from recombinant antibodies. J. Mol. Biol. 318, 429-442 (2002). (Pubitemid 34734837)
38. Koide, A., Jordan, M.R., Horner, S.R., Batori, V. & Koide, S. Stabilization of a fibronectin type III domain by the removal of unfavorable electrostatic interactions on the protein surface. Biochemistry 40, 10326-10333 (2001). (Pubitemid 32800140)
39. Kraynov, V.S. et al. Localized Rac activation dynamics visualized in living cells. Science 290, 333-337 (2000).
40. Martinez-Quiles, N., Ho, H.Y., Kirschner, M.W., Ramesh, N. & Geha, R.S. 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 (2004). (Pubitemid 38738162)
41. Cory, G.O., Garg, R., Cramer, R. & Ridley, A.J. Phosphorylation of tyrosine 291 enhances the ability of WASp to stimulate actin polymerization and filopodium formation. Wiskott-Aldrich Syndrome protein. J. Biol. Chem. 277, 45115-45121 (2002). (Pubitemid 36159113)
42. Suetsugu, S. et al. Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev. Cell 3, 645-658 (2002). (Pubitemid 35339483)
43. Plattner, R., Kadlec, L., DeMali, K.A., Kazlauskas, A. & Pendergast, A.M. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13, 2400-2411 (1999). (Pubitemid 29453611)
44. Sini, P., Cannas, A., Koleske, A.J., Di Fiore, P.P. & Scita, G. Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nat. Cell Biol. 6, 268-274 (2004). (Pubitemid 38344366)
45. Yang, L., Kowalski, J.R., Zhan, X., Thomas, S.M. & Luscinskas, F.W. Endothelial cell cortactin phosphorylation by Src contributes to polymorphonuclear leukocyte transmigration in vitro. Circ. Res. 98, 394-402 (2006).
46. Bouton, A.H., Riggins, R.B. & Bruce-Staskal, P.J. Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene 20, 6448-6458 (2001). (Pubitemid 32977850)
47. Polte, T.R. & Hanks, S.K. Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130(Cas)) 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 (1997). (Pubitemid 27102371)
48. DerMardirossian, C., Rocklin, G., Seo, J.Y. & Bokoch, G.M. Phosphorylation of RhoGDI by Src regulates Rho GTPase binding and cytosol-membrane cycling. Mol. Biol. Cell 17, 4760-4768 (2006). (Pubitemid 44665745)
49. Timpson, P., Jones, G.E., Frame, M.C. & Brunton, V.G. Coordination of cell polarization and migration by the Rho family GTPases requires Src tyrosine kinase activity. Curr. Biol. 11, 1836-1846 (2001). (Pubitemid 33136523)
50. Rossman, K.L., Der, C.J. & Sondek, J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180 (2005). (Pubitemid 40215811)