Simple synthetic protein scaffolds can create adjustable artificial MAPK circuits in yeast and mammalian cells

Science Signaling

Volumn 8, Issue 383, 2015, Pages

  Ryu, Jihoon ^a   Park, Sang Hyun ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHOSPHATASE; PROTEIN KINASE C; SCAFFOLD PROTEIN; SYNTHETIC PEPTIDE; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; MAMMAL CELL; MATING; NONHUMAN; OSMOREGULATION; PDZ DOMAIN; PLASTICITY; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; YEAST CELL; ANIMAL; CELL LINE; GENETICS; METABOLISM; RAT; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; MAMMALIA;

ANIMALS; CELL LINE; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; PDZ DOMAINS; RATS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84937819453     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aab3397     Document Type: Article

References (50)

1. M. B. Elowitz, S. Leibler, A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338 (2000).
2. T. S. Moon, C. Lou, A. Tamsir, B. C. Stanton, C. A. Voigt, Genetic programs constructed from layered logic gates in single cells. Nature 491, 249-253 (2012).
3. F. Posas, H. Saito, Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: Scaffold role of Pbs2p MAPKK. Science 276, 1702-1705 (1997).
4. T. Pawson, J. D. Scott, Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080 (1997).
5. W. Kolch, Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837 (2005).
6. J. G. Zalatan, S. M. Coyle, S. Rajan, S. S. Sidhu, W. A. Lim, Conformational control of the Ste5 scaffold protein insulates against MAP kinase misactivation. Science 337, 1218-1222 (2012).
7. S. C. Strickfaden, M. J. Winters, G. Ben-Ari, R. E. Lamson, M. Tyers, P. M. Pryciak, A mechanism for cell-cycle regulat ion of MAP kinase signaling in a yeast differentiation pathway. Cell 128, 519-531 (2007).
8. A. Zeke, M. Lukacs, W. A. Lim, A. Remenyi, Scaffolds: Interaction platforms for cellular signalling circuits. Trends Cell Biol. 19, 364-374 (2009).
9. W. A. Lim, Designing customized cell signalling circuits. Nat. Rev. Mol. Cell Biol. 11, 393-403 (2010).
10. C. J. Bashor, N. C. Helman, S. Yan, W. A. Lim, Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science 319, 1539-1543 (2008).
11. J. E. Ferrell Jr., What do scaffold proteins really do? Sci. STKE 2000, pe1 (2000).
12. M. J. Winters, R. E. Lamson, H. Nakanishi, A. M. Neiman, P. M. Pryciak, A membrane binding domain in the ste5 scaffold synergizes with Gbg binding to control localization and signaling in pheromone response. Mol. Cell 20, 21-32 (2005).
13. K. Y. Choi, B. Satterberg, D. M. Lyons, E. A. Elion, Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78, 499-512 (1994).
14. C. Inouye, N. Dhillon, J. Thorner, Ste5 RING-H2 domain: Role in Ste4-promoted oligomerization for yeast pheromone signaling. Science 278, 103-106 (1997).
15. S. K. Mahanty, Y. Wang, F. W. Farley, E. A. Elion, Nuclear shuttling of yeast scaffold Ste5 is required for its recruitment to the plasma membran e and activation of the mating MAPK cascade. Cell 98, 501-512 (1999).
16. L. S. Garrenton S. L. Young J. Thorner, Function of the MAPK scaffold protein, Ste5, requires a cryptic PH domain, Genes Dev. 20, 1946-1958(2006).
17. R. P. Bhattacharyya, A. Remenyi, M. C. Good, C. J. Bashor, A. M. Falick, W. A. Lim, The Ste5 scaffold allosterically modulates signaling output of the yeast m ating pathway. Science 311, 822-826 (2006).
18. M. Good, G. Tang, J. Singleton, A. Remenyi, W. A. Lim, The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136, 1085-1097 (2009).
19. S. H. Park, A. Zarrinpar, W. A. Lim, Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299, 1061-1064 (2003).
20. J. Moon, S. H. Park, Reassembly of JIP1 scaffold complex in JNK MAP kinase pathway using heterologous protein interactions. PLOS One 9, e96797 (2014).
21. J. E. Dueber, G. C. Wu, G. R. Malmirchegini, T. S. Moon, C. J. P etzold, A. V. Ullal, K. L. Prather, J. D. Keasling, Synthetic protein scaffolds provide modular control over metabolic flux. Nat. Biotechnol. 27, 753-759 (2009).
22. P. M. Pryciak, F. A. Huntress, Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gbg complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12, 2684-2697 (1998).
23. K. Harris, R. E. La mson, B. Nelson, T. R. Hughes, M. J. Marton, C. J. Roberts, C. Boone, P. M. Pryciak, Role of scaffolds in MAP kinase pathway specificity revealed by custom design of pathway-dedicated signaling proteins. Curr. Biol. 11, 1815-1824 (2001).
24. W. Cho, Building signaling complexes at the membrane. Sci. STKE 2006, pe7 (2006).
25. M. Ptashne, A. Gann, Imposing specificity by localization: Mechanism and evolvability. Curr. Biol. 8, R897 (1998).
26. S. M. Coyle, J. Flores, W. A. Lim, Exploitation of latent allostery enables the evolution of new modes of MAP kinase regulation. Cell 154, 875-887 (2013).
27. R. P. Bhattacharyya, A. Remenyi, B. J. Yeh, W. A. Lim, Domains, motifs, and scaffolds: The role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 75, 655-680 (2006).
28. E. C. O'Shaughnessy, S. Palani, J. J. Collins, C. A. Sarkar, Tunable signal processing in synthetic MAP kinase cascades. Cell 144, 119-131 (2011).
29. B. Z. Harris, B. J. Hillier, W. A. Lim, Energetic determinants of internal motif recognition by PDZ domains. Biochemistry 40, 5921-5930 (2001).
30. C. N. Chi, A. Bach, M. Gottschalk, A. S. Kristensen, K. Stromgaard, P. Jemth, Deciphering the kinetic binding mechanism of dimeric ligands using a potent plasmastable dimeric inhibitor of postsynaptic density protein-95 as an example. J. Biol. Chem. 285, 28252-28260 (2010).
31. J. Trueheart, J. D. Boeke, G. R. Fink, Two genes required for cell fusion during yeast conjugation: Evidence for a pheromone-induced surface protein. Mol. Cell. Biol. 7, 2316-2328 (1987).
32. F. Drogen, S. M. O'Rourke, V. M. Stucke, M. Jaquenoud, A. M. Neiman, M. Peter, Phosphorylation of the MEKK Ste11p by the PAK-like kinase Ste20p is required for MAP kinase signaling in vivo. Curr. Biol. 10, 630-639 ( 2000).
33. J. E. Reneke, K. J. Blumer, W. E. Courchesne, J. Thorner, The carboxy-terminal segment of the yeast a-factor receptor is a regulatory domain. Cell 55, 221-234 (1988).
34. A. Remenyi, M. C. Good, R. P. Bhattacharyya, W. A. Lim, The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol. Cell 20, 951-962 (2005).
35. M. C. Good, J. G. Zalatan, W. A. Lim, Scaffold proteins: Hubs for controlling the flow of cellular information. Science 332, 680-686 (2011).
36. S. R. Salama, K. B. Hendricks, J. Thorner, G1 cyclin degradation: The PEST motif of yeast Cln2 is necessary, but not sufficient, for rapid protein turnover. Mol. Cell. Biol. 14, 7953-7966 (1994).
37. X. L. Zhan R. J. Des chenes K. L. Guan. Differential regulation of FUS3 MAP kinase by tyrosine-specific phosphatases PTP2/PTP3 and dual-specificity phosphatase MSG5 in Saccharomyces cerevisiae.Genes Dev. 11 1690-1702 1997
38. K. Doi, A. Gartner, G. Ammerer, B. Errede, H. Shinkawa, K. Sugimoto, K. Matsumoto, MSG5, a novel protein phosphatase promotes adaptation to pheromone response in S. cerevisiae. EMBO J. 13, 61-70 (1 994).
39. X. L. Zhan, K. L. Guan, A specific protein-protein interaction accounts for the in vivo substrate selectivity of Ptp3 towards the Fus3 MAP kinase. Genes Dev. 13, 2811-2827 (1999).
40. A. Levskaya, O. D. Weiner, W. A. Lim, C. A. Voigt, Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461, 997-1001 (2009).
41. A. S. Sely unin, S. E. Sutton, B. A. Weigele, L. E. Reddick, R. C. Orchard, S. M. Bresson, D. R. Tomchick, N. M. Alto, The assembly of a GTPase-kinase signalling complex by a bacterial catalytic scaffold. Nature 469, 1 07-111 (2011).
42. X. Yu, Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, X. F. Yu, Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302, 1056-1060 (2003).
43. F. Pincet, Membrane recruitment of scaffold proteins drives specific signaling. PLOS One 2, e977 (2007).
44. W. R. Burack, A. S. Shaw, Signal transduction: Hanging on a scaffold. Curr. Opin. Cell Biol. 12, 211-216 (2000).
45. W. R. Whitaker, S. A. Davis, A. P. Arkin, J. E. Dueber, Engineering robust control of two-component system phosphotransfer using modular scaffolds. Proc. Natl. Acad. Sci. U.S.A. 109, 18090-18095 (2012).
46. T. Rajakulendran, M. Sahmi, M. Lefrancois, F. Sicheri, M. Therrien, A dimerizationdependent mechanism drives RAF catalytic activation. Nature 461, 542-545 (2009).
47. N. D ard, M. Peter, Scaffold proteins in MAP kinase signaling: More than simple passive activating platforms. BioEssays 28, 146-156 (2006).
48. S. Schneider, M. Buchert, O. Georgiev, B. Catimel, M. Halford, S. A. Stacker, T. Baechi, K. Moelling, C. M. Hovens, Mutagenesis and selection of PDZ domains that bind new protein targets. Nat. Biotechnol. 17, 170-175 (1999).
49. J. Reina, E. Lacroix, S. D. Hobson, G. Fernandez-Ballester, V. Rybin, M. S. Schwab, L. Serrano, C. Gonzalez, Computer-aided design of a PDZ domain to recognize new target sequences. Nat. Struct. Biol. 9, 621-627 (2002).
50. G. F. Sprague Jr., Assay of yeast mating reaction. Methods Enzymol. 194, 77-93 (1991).