Conversion of graded phosphorylation into switch-like nuclear translocation via autoregulatory mechanisms in ERK signalling

Nature Communications

Volumn 7, Issue , 2016, Pages

  Shindo, Yuki ^a,b   Iwamoto, Kazunari ^b   Mouri, Kazunari ^c   Hibino, Kayo ^b,c   Tomita, Masaru ^d   Kosako, Hidetaka ^e   Sako, Yasushi ^c   Takahashi, Koichi ^b,d  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c RIKEN   (Japan)

^d KEIO UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOPORIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

CELLS AND CELL COMPONENTS; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; GENE EXPRESSION; INHIBITOR; MAMMAL; METABOLISM; NUMERICAL MODEL; TRANSLOCATION;

ANIMAL CELL; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IN VITRO STUDY; KINETICS; MATHEMATICAL MODEL; NONHUMAN; PC12 CELL LINE; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL NUCLEUS; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; RNA INTERFERENCE;

MAMMALIA;

ANIMALS; CELL NUCLEUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PC12 CELLS; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RNA INTERFERENCE;

EID: 84955606068     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10485     Document Type: Article

References (50)

1. Chang, L. & Karin, M. Mammalian MAP kinase signalling cascades. Nature 410, 37-40 (2001).
2. Qi, M. & Elion, E. A. MAP kinase pathways. J. Cell Sci. 118, 3569-3572 (2005).
3. Huang, C. Y. & Ferrell, J. E. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl Acad. Sci. USA 93, 10078-10083 (1996).
4. Kholodenko, B. N. Negative feedback and ultrasensitivity can bring about oscillations in the mitogen-activated protein kinase cascades. Eur. J. Biochem. 267, 1583-1588 (2000).
5. Markevich, N. I., Hoek, J. B. & Kholodenko, B. N. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 164, 353-359 (2004).
6. Qiao, L., Nachbar, R. B., Kevrekidis, I. G. & Shvartsman, S. Y. Bistability and oscillations in the Huang-Ferrell model of MAPK signaling. PLoS Comput. Biol. 3, 1819-1826 (2007).
7. Ferrell, J. E. & Machleder, E. M. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 280, 895-898 (1998).
8. Xiong, W. & Ferrell, J. E. A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426, 460-465 (2003).
9. Whitehurst, A., Cobb, M. H. & White, M. A. Stimulus-coupled spatial restriction of extracellular signal-regulated kinase 1/2 activity contributes to the specificity of signal-response. Mol. Cell Biol. 24, 10145-10150 (2004).
10. MacKeigan, J. P., Murphy, L. O., Dimitri, C. A. & Blenis, J. Graded mitogenactivated protein kinase activity precedes switch-like c-Fos induction in mammalian cells. Mol. Cell Biol. 25, 4676-4682 (2005).
11. Santos, S. D. M., Verveer, P. J. & Bastiaens, P. I. H. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9, 324-330 (2007).
12. Perrett, R. M. et al. Signaling to extracellular signal-regulated kinase from ErbB1 kinase and protein kinase C: feedback, heterogeneity, and gating. J. Biol. Chem. 288, 21001-21014 (2013).
13. Caunt, C. J. & McArdle, C. A. ERK phosphorylation and nuclear accumulation: insights from single-cell imaging. Biochem. Soc. Trans. 40, 224-229 (2012).
14. Brunet, A. et al. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18, 664-674 (1999).
15. Plotnikov, A. et al. The nuclear translocation of ERK1/2 as an anticancer target. Nat. Commun. 6, 6685 (2015).
16. Caunt, C. J. & McArdle, C. A. Stimulus-induced uncoupling of extracellular signal-regulated kinase phosphorylation from nuclear localization is dependent on docking domain interactions. J. Cell Sci. 123, 4310-4320 (2010).
17. Ahmed, S. et al. Data-driven modeling reconciles kinetics of ERK phosphorylation, localization, and activity states. Mol. Syst. Biol. 10, 1-14 (2014).
18. Wente, S. R. & Rout, M. P. The Nuclear Pore Complex and Nuclear Transport. Cold Spring Harb. Perspect. Biol. 2, a000562 (2010).
19. Patel, S. S., Belmont, B. J., Sante, J. M. & Rexach, M. F. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129, 83-96 (2007).
20. Frey, S. & Görlich, D. A Saturated FG-Repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130, 512-523 (2007).
21. Lee, T. et al. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol. Cell 14, 43-55 (2004).
22. Matsubayashi, Y., Fukuda, M. & Nishida, E. Evidence for existence of a nuclear pore complex-mediated, cytosol-independent pathway of nuclear translocation of ERK MAP kinase in permeabilized cells. J. Biol. Chem. 276, 41755-41760 (2001).
23. Whitehurst, A. W. et al. ERK2 enters the nucleus by a carrier-independent mechanism. Proc. Natl Acad. Sci. USA 99, 7496-7501 (2002).
24. Lorenzen, J. A. et al. Nuclear import of activated D-ERK by DIM-7, an importin family member encoded by the gene moleskin. Development 128, 1403-1414 (2001).
25. Plotnikov, A., Chuderland, D., Karamansha, Y., Livnah, O. & Seger, R. Nuclear extracellular signal-regulated kinase 1 and 2 translocation is mediated by casein kinase 2 and accelerated by autophosphorylation. Mol. Cell Biol. 31, 3515-3530 (2011).
26. Vomastek, T. et al. Extracellular signal-regulated kinase 2 (ERK2) phosphorylation sites and docking domain on the nuclear pore complex protein Tpr cooperatively regulate ERK2-Tpr interaction. Mol. Cell Biol. 28, 6954-6966 (2008).
27. Kosako, H. et al. Phosphoproteomics reveals new ERK MAP kinase targets and links ERK to nucleoporin-mediated nuclear transport. Nat. Struct. Mol. Biol. 16, 1026-1035 (2009).
28. Carlson, S. M. et al. Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3. Sci. Signal. 4, rs11 (2011).
29. Czubryt, M. P., Austria, J. A. & Pierce, G. N. Hydrogen peroxide inhibition of nuclear protein import is mediated by the mitogen-activated protein kinase, ERK2. J. Cell Biol. 148, 7-16 (2000).
30. Aoki, K., Yamada, M., Kunida, K., Yasuda, S. & Matsuda, M. Processive phosphorylation of ERK MAP kinase in mammalian cells. Proc. Natl Acad. Sci. USA 108, 12675-12680 (2011).
31. Horgan, A. M. & Stork, P. J. Examining the mechanism of Erk nuclear translocation using green fluorescent protein. Exp. Cell Res. 285, 208-220 (2003).
32. Ferrell, J. E. & Ha, S. H. Ultrasensitivity part I: Michaelian responses and zero-order ultrasensitivity. Trends Biochem. Sci. 39, 496-503 (2014).
33. Costa, M. et al. Dynamic regulation of ERK2 nuclear translocation and mobility in living cells. J. Cell Sci. 119, 4952-4963 (2006).
34. Cohen-Saidon, C., Cohen, A. A., Sigal, A., Liron, Y. & Alon, U. Dynamics and variability of ERK2 response to EGF in individual living cells. Mol. Cell 36, 885-893 (2009).
35. Cheong, R., Rhee, A., Wang, C. J., Nemenman, I. & Levchenko, A. Information transduction capacity of noisy biochemical signaling networks. Science 334, 354-358 (2011).
36. Vaudry, D., Stork, P. J. S., Lazarovici, P. & Eiden, L. E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649 (2002).
37. Ohori, M. et al. Identification of a selective ERK inhibitor and structural determination of the inhibitor-ERK2 complex. Biochem. Biophys. Res. Commun. 336, 357-363 (2005).
38. Kamioka, Y., Yasuda, S., Fujita, Y., Aoki, K. & Matsuda, M. Multiple decisive phosphorylation sites for the negative feedback regulation of SOS1 via ERK. J. Biol. Chem. 285, 33540-33548 (2010).
39. Yoon, S. & Seger, R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24, 21-44 (2006).
40. Kim, E. K. & Choi, E.-J. Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta 1802, 396-405 (2010).
41. Aoki, K. et al. Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Mol. Cell 52, 529-540 (2013).
42. Michailovici, I. et al. Nuclear to cytoplasmic shuttling of ERK promotes differentiation of muscle stem/progenitor cells. Development 141, 2611-2620 (2014).
43. Chuderland, D., Konson, A. & Seger, R. Identification and characterization of a general nuclear translocation signal in signaling proteins. Mol. Cell 31, 850-861 (2008).
44. Fukuda, M., Gotoh, Y. & Nishida, E. Interaction of MAP kinase with MAP kinase kinase: its possible role in the control of nucleocytoplasmic transport of MAP kinase. EMBO J. 16, 1901-1908 (1997).
45. Formstecher, E. et al. PEA-15 Mediates Cytoplasmic Sequestration of ERK MAP Kinase. Dev. Cell 1, 239-250 (2001).
46. Torii, S., Kusakabe, M., Yamamoto, T., Maekawa, M. & Nishida, E. Sef is a spatial regulator for Ras/MAP kinase signaling. Dev. Cell 7, 33-44 (2004).
47. Kimura, H. & Cook, P. R. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153, 1341-1353 (2001).
48. Kanda, T., Sullivan, K. F. & Wahl, G. M. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385 (1998).
49. Takahashi, M., Shibata, T., Yanagida, T. & Sako, Y. A protein switch with tunable steepness reconstructed in Escherichia coli cells with eukaryotic signaling proteins. Biochem. Biophys. Res. Commun. 421, 731-735 (2012).
50. Ohsugi, M. et al. Kid-mediated chromosome compaction ensures proper nuclear envelope formation. Cell 132, 771-782 (2008).