Knowledge-based design of a biosensor to quantify localized ERK activation in living cells

Chemistry and Biology

Volumn 20, Issue 6, 2013, Pages 847-856

  Kummer, Lutz ^a   Hsu, Chia Wen ^b   Dagliyan, Onur ^b   MacNevin, Christopher ^b   Kaufholz, Melanie ^c   Zimmermann, Bastian ^c   Dokholyan, Nikolay V ^b   Hahn, Klaus M ^b   Plückthun, Andreas ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

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

^c Biaffin GmbH and CoKG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; DESIGNED ANKYRIN REPEAT PROTEIN; MEROCYANINE; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOSENSOR; CELL ACTIVATION; CELL NUCLEUS; CELL STIMULATION; CONFORMATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; FLUORESCENCE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALS; BIOSENSING TECHNIQUES; BUTADIENES; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MUSCLE PROTEINS; MUTAGENESIS, SITE-DIRECTED; NIH 3T3 CELLS; NITRILES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PYRIMIDINONES; SUBSTRATE SPECIFICITY;

EID: 84879376222     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.04.016     Document Type: Article

References (52)

1. H.K. Binz, M.T. Stumpp, P. Forrer, P. Amstutz, and A. Plückthun Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins J. Mol. Biol. 332 2003 489 503
2. H.K. Binz, P. Amstutz, A. Kohl, M.T. Stumpp, C. Briand, P. Forrer, M.G. Grütter, and A. Plückthun High-affinity binders selected from designed ankyrin repeat protein libraries Nat. Biotechnol. 22 2004 575 582
3. H.K. Binz, P. Amstutz, and A. Plückthun Engineering novel binding proteins from nonimmunoglobulin domains Nat. Biotechnol. 23 2005 1257 1268
4. Y.L. Boersma, and A. Plückthun DARPins and other repeat protein scaffolds: advances in engineering and applications Curr. Opin. Biotechnol. 22 2011 849 857
5. E. Brient-Litzler, A. Plückthun, and H. Bedouelle Knowledge-based design of reagentless fluorescent biosensors from a designed ankyrin repeat protein Protein Eng. Des. Sel. 23 2010 229 241
6. G.R. Bright, G.W. Fisher, J. Rogowska, and D.L. Taylor Fluorescence ratio imaging microscopy Methods Cell Biol. 30 1989 157 192
7. B.J. Canagarajah, A. Khokhlatchev, M.H. Cobb, and E.J. Goldsmith Activation mechanism of the MAP kinase ERK2 by dual phosphorylation Cell 90 1997 859 869
8. R.H. Chen, C. Sarnecki, and J. Blenis Nuclear localization and regulation of erk- and rsk-encoded protein kinases Mol. Cell. Biol. 12 1992 915 927
9. Z. Chen, T.B. Gibson, F. Robinson, L. Silvestro, G. Pearson, B. Xu, A. Wright, C. Vanderbilt, and M.H. Cobb MAP kinases Chem. Rev. 101 2001 2449 2476
10. S. Cowley, H. Paterson, P. Kemp, and C.J. Marshall Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells Cell 77 1994 841 852
11. O. Dagliyan, E.A. Proctor, K.M. D'Auria, F. Ding, and N.V. Dokholyan Structural and dynamic determinants of protein-peptide recognition Structure 19 2011 1837 1845
12. F. Ding, D. Tsao, H. Nie, and N.V. Dokholyan Ab initio folding of proteins with all-atom discrete molecular dynamics Structure 16 2008 1010 1018
13. F. Ding, S. Yin, and N.V. Dokholyan Rapid flexible docking using a stochastic rotamer library of ligands J. Chem. Inf. Model. 50 2010 1623 1632
14. N.V. Dokholyan, S.V. Buldyrev, H.E. Stanley, and E.I. Shakhnovich Discrete molecular dynamics studies of the folding of a protein-like model Fold. Des. 3 1998 577 587
15. M.F. Favata, K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, W.S. Feeser, D.E. Van Dyk, W.J. Pitts, R.A. Earl, and F. Hobbs Identification of a novel inhibitor of mitogen-activated protein kinase kinase J. Biol. Chem. 273 1998 18623 18632
16. A. Fujioka, K. Terai, R.E. Itoh, K. Aoki, T. Nakamura, S. Kuroda, E. Nishida, and M. Matsuda Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes J. Biol. Chem. 281 2006 8917 8926
17. L. Gervais, and E. Delamarche Toward one-step point-of-care immunodiagnostics using capillary-driven microfluidics and PDMS substrates Lab Chip 9 2009 3330 3337
18. F.A. Gonzalez, A. Seth, D.L. Raden, D.S. Bowman, F.S. Fay, and R.J. Davis Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus J. Cell Biol. 122 1993 1089 1101
19. H.M. Green, and J. Alberola-Ila Development of ERK activity sensor, an in vitro, FRET-based sensor of extracellular regulated kinase activity BMC Chem. Biol. 5 2005 1
20. A. Gulyani, E. Vitriol, R. Allen, J. Wu, D. Gremyachinskiy, S. Lewis, B. Dewar, L.M. Graves, B.K. Kay, and B. Kuhlman A biosensor generated via high-throughput screening quantifies cell edge Src dynamics Nat. Chem. Biol. 7 2011 437 444
21. C.D. Harvey, A.G. Ehrhardt, C. Cellurale, H. Zhong, R. Yasuda, R.J. Davis, and K. Svoboda A genetically encoded fluorescent sensor of ERK activity Proc. Natl. Acad. Sci. USA 105 2008 19264 19269
22. L. Hodgson, P. Nalbant, F. Shen, and K. Hahn Imaging and photobleach correction of Mero-CBD, sensor of endogenous Cdc42 activation Methods Enzymol. 406 2006 140 156
23. L. Hodgson, O. Pertz, and K.M. Hahn Design and optimization of genetically encoded fluorescent biosensors: GTPase biosensors Methods Cell Biol. 85 2008 63 81
24. L. Hodgson, F. Shen, and K. Hahn Biosensors for characterizing the dynamics of Rho family GTPases in living cells Curr. Protoc. Cell Biol. 46 2010 14.11.1 14.11.26
25. M. Kawe, P. Forrer, P. Amstutz, and A. Plückthun Isolation of intracellular proteinase inhibitors derived from designed ankyrin repeat proteins by genetic screening J. Biol. Chem. 281 2006 40252 40263
26. V.S. Kraynov, C. Chamberlain, G.M. Bokoch, M.A. Schwartz, S. Slabaugh, and K.M. Hahn Localized Rac activation dynamics visualized in living cells Science 290 2000 333 337
27. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
28. L. Kummer, P. Parizek, P. Rube, B. Millgramm, A. Prinz, P.R. Mittl, M. Kaufholz, B. Zimmermann, F.W. Herberg, and A. Plückthun Structural and functional analysis of phosphorylation-specific binders of the kinase ERK from designed ankyrin repeat protein libraries Proc. Natl. Acad. Sci. USA 109 2012 E2248 E2257
29. A. Leaver-Fay, M. Tyka, S.M. Lewis, O.F. Lange, J. Thompson, R. Jacak, K. Kaufman, P.D. Renfrew, C.A. Smith, and W. Sheffler ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules Methods Enzymol. 487 2011 545 574
30. P. Lenormand, C. Sardet, G. Pagès, G. L'Allemain, A. Brunet, and J. Pouysségur Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts J. Cell Biol. 122 1993 1079 1088
31. C.J. MacNevin, D. Gremyachinskiy, C.W. Hsu, L. Li, M. Rougie, T.T. Davis, and K.M. Hahn Environment-sensing merocyanine dyes for live cell imaging applications Bioconjug. Chem. 24 2013 215 223
32. C.J. Marshall Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation Cell 80 1995 179 185
33. P.L. McNeil, and E. Warder Glass beads load macromolecules into living cells J. Cell Sci. 88 1987 669 678
34. F.F. Miranda, E. Brient-Litzler, N. Zidane, F. Pecorari, and H. Bedouelle Reagentless fluorescent biosensors from artificial families of antigen binding proteins Biosens. Bioelectron. 26 2011 4184 4190
35. L.K. Mosavi, T.J. Cammett, D.C. Desrosiers, and Z.Y. Peng The ankyrin repeat as molecular architecture for protein recognition Protein Sci. 13 2004 1435 1448
36. P. Nalbant, L. Hodgson, V. Kraynov, A. Toutchkine, and K.M. Hahn Activation of endogenous Cdc42 visualized in living cells Science 305 2004 1615 1619
37. A.W. Nguyen, and P.S. Daugherty Evolutionary optimization of fluorescent proteins for intracellular FRET Nat. Biotechnol. 23 2005 355 360
38. P. Parizek, L. Kummer, P. Rube, A. Prinz, F.W. Herberg, and A. Plückthun Designed ankyrin repeat proteins (DARPins) as novel isoform-specific intracellular inhibitors of c-Jun N-terminal kinases ACS Chem. Biol. 7 2012 1356 1366
39. G. Pearson, F. Robinson, T. Beers Gibson, B.E. Xu, M. Karandikar, K. Berman, and M.H. Cobb Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions Endocr. Rev. 22 2001 153 183
40. O. Pertz, L. Hodgson, R.L. Klemke, and K.M. Hahn Spatiotemporal dynamics of RhoA activity in migrating cells Nature 440 2006 1069 1072
41. R. Roskoski Jr. ERK1/2 MAP kinases: structure, function, and regulation Pharmacol. Res. 66 2012 105 143
42. J. Sambrook, and D.W. Russell Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
43. M. Sato, Y. Kawai, and Y. Umezawa Genetically encoded fluorescent indicators to visualize protein phosphorylation by extracellular signal-regulated kinase in single living cells Anal. Chem. 79 2007 2570 2575
44. D. Steiner, P. Forrer, and A. Plückthun Efficient selection of DARPins with sub-nanomolar affinities using SRP phage display J. Mol. Biol. 382 2008 1211 1227
45. A. Toutchkine, V. Kraynov, and K. Hahn Solvent-sensitive dyes to report protein conformational changes in living cells J. Am. Chem. Soc. 125 2003 4132 4145
46. A. Toutchkine, D.V. Nguyen, and K.M. Hahn Merocyanine dyes with improved photostability Org. Lett. 9 2007 2775 2777
47. A. Toutchkine, D.V. Nguyen, and K.M. Hahn Simple one-pot preparation of water-soluble, cysteine-reactive cyanine and merocyanine dyes for biological imaging Bioconjug. Chem. 18 2007 1344 1348
48. C.M. Welch, H. Elliott, G. Danuser, and K.M. Hahn Imaging the coordination of multiple signalling activities in living cells Nat. Rev. Mol. Cell Biol. 12 2011 749 756
49. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, and A. McCoy Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
50. S. Yin, L. Biedermannova, J. Vondrasek, and N.V. Dokholyan MedusaScore: an accurate force field-based scoring function for virtual drug screening J. Chem. Inf. Model. 48 2008 1656 1662
51. C. Zahnd, F. Pecorari, N. Straumann, E. Wyler, and A. Plückthun Selection and characterization of Her2 binding-designed ankyrin repeat proteins J. Biol. Chem. 281 2006 35167 35175
52. J. Zhao, X. Yuan, M. Frödin, and I. Grummt ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth Mol. Cell 11 2003 405 413