MAP kinase modules: The excursion model and the steps that count

Biophysical Journal

Volumn 107, Issue 9, 2014, Pages 2006-2015

  Piala, Alexander T ^a   Humphreys, John M ^a   Goldsmith, Elizabeth J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION;

ANIMALS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION;

EID: 84908592829     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.09.024     Document Type: Review

References (74)

1. W.J. Malaisse Insulin secretion: multifactorial regulation for a single process of release. The Minkowski award lecture delivered on September 7, 1972 before the European Association for the Study of Diabetes at Madrid, Spain Diabetologia 9 1973 167 173
2. M. Janicot, and M.D. Lane Activation of glucose uptake by insulin and insulin-like growth factor I in Xenopus oocytes Proc. Natl. Acad. Sci. USA 86 1989 2642 2646
3. L.B. Ray, and T.W. Sturgill Rapid stimulation by insulin of a serine/threonine kinase in 3T3-L1 adipocytes that phosphorylates microtubule-associated protein 2 in vitro Proc. Natl. Acad. Sci. USA 84 1987 1502 1506
4. J. Blenis, J.G. Spivack, and R.L. Erikson Phorbol ester, serum, and Rous sarcoma virus transforming gene product induce similar phosphorylations of ribosomal protein S6 Proc. Natl. Acad. Sci. USA 81 1984 6408 6412
5. T.G. Boulton, and G.D. Yancopoulos M.H. Cobb An insulin-stimulated protein kinase similar to yeast kinases involved in cell cycle control Science 249 1990 64 67
6. R. Seger, and D. Seger E.G. Krebs Human T-cell mitogen-activated protein kinase kinases are related to yeast signal transduction kinases J. Biol. Chem. 267 1992 25628 25631
7. R. Seger, and N.G. Ahn E.G. Krebs Purification and characterization of mitogen-activated protein kinase activator(s) from epidermal growth factor-stimulated A431 cells J. Biol. Chem. 267 1992 14373 14381
8. C.F. Zheng, and K.L. Guan Cloning and characterization of two distinct human extracellular signal-regulated kinase activator kinases, MEK1 and MEK2 J. Biol. Chem. 268 1993 11435 11439
9. Z. Chen, and T.B. Gibson M.H. Cobb MAP kinases Chem. Rev. 101 2001 2449 2476
10. Y. Keshet, and R. Seger The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions Methods Mol. Biol. 661 2010 3 38
11. N.G. Ahn, and R. Seger E.G. Krebs Multiple components in an epidermal growth factor-stimulated protein kinase cascade. In vitro activation of a myelin basic protein/microtubule-associated protein 2 kinase J. Biol. Chem. 266 1991 4220 4227
12. C.Y. Huang, and J.E. Ferrell Jr. Ultrasensitivity in the mitogen-activated protein kinase cascade Proc. Natl. Acad. Sci. USA 93 1996 10078 10083
13. M. Raman, W. Chen, and M.H. Cobb Differential regulation and properties of MAPKs Oncogene 26 2007 3100 3112
14. S.J. Mansour, and W.T. Matten N.G. Ahn Transformation of mammalian cells by constitutively active MAP kinase kinase Science 265 1994 966 970
15. P.A. Lochhead, and G. Sibbet V. Cleghon Activation-loop autophosphorylation is mediated by a novel transitional intermediate form of DYRKs Cell 121 2005 925 936
16. J.M. Humphreys, and A.T. Piala E.J. Goldsmith Precisely ordered phosphorylation reactions in the p38 mitogen-activated protein (MAP) kinase cascade J. Biol. Chem. 288 2013 23322 23330
17. J.E. Ferrell Jr. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs Trends Biochem. Sci. 21 1996 460 466
18. A.S. Futran, and A.J. Link S.Y. Shvartsman ERK as a model for systems biology of enzyme kinetics in cells Curr. Biol. 23 2013 R972 R979
19. S.Y. Shvartsman, M. Coppey, and A.M. Berezhkovskii MAPK signaling in equations and embryos Fly (Austin) 3 2009 62 67
20. C. Salazar, and T. Höfer Multisite protein phosphorylation - from molecular mechanisms to kinetic models FEBS J. 276 2009 3177 3198
21. N. Blüthgen, and S. Legewie Robustness of signal transduction pathways Cell. Mol. Life Sci. 70 2013 2259 2269
22. N. Dekel, and I. Sherizly Induction of maturation in rat follicle-enclosed oocyte by forskolin FEBS Lett. 151 1983 153 155
23. J.E. Ferrell Jr., and E.M. Machleder The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes Science 280 1998 895 898
24. C.P. Bagowski, and J. Besser J.E. Ferrell Jr. The JNK cascade as a biochemical switch in mammalian cells: ultrasensitive and all-or-none responses Curr. Biol. 13 2003 315 320
25. E.C. O'Shaughnessy, and S. Palani C.A. Sarkar Tunable signal processing in synthetic MAP kinase cascades Cell 144 2011 119 131
26. A. Whitehurst, M.H. Cobb, and M.A. White Stimulus-coupled spatial restriction of extracellular signal-regulated kinase 1/2 activity contributes to the specificity of signal-response pathways Mol. Cell. Biol. 24 2004 10145 10150
27. J.P. MacKeigan, and L.O. Murphy J. Blenis Graded mitogen-activated protein kinase activity precedes switch-like c-Fos induction in mammalian cells Mol. Cell. Biol. 25 2005 4676 4682
28. S. Yamada, T. Taketomi, and A. Yoshimura Model analysis of difference between EGF pathway and FGF pathway Biochem. Biophys. Res. Commun. 314 2004 1113 1120
29. S. Sasagawa, and Y. Ozaki S. Kuroda Prediction and validation of the distinct dynamics of transient and sustained ERK activation Nat. Cell Biol. 7 2005 365 373
30. B. Schoeberl, and C. Eichler-Jonsson G. Müller Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors Nat. Biotechnol. 20 2002 370 375
31. A. Fujioka, and K. Terai M. Matsuda Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes J. Biol. Chem. 281 2006 8917 8926
32. T.A. Haystead, and P. Dent T.W. Sturgill Ordered phosphorylation of p42mapk by MAP kinase kinase FEBS Lett. 306 1992 17 22
33. J.E. Ferrell Jr., and R.R. Bhatt Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase J. Biol. Chem. 272 1997 19008 19016
34. D.J. Robbins, and E. Zhen M.H. Cobb Regulation and properties of extracellular signal-regulated protein kinases 1, 2, and 3 J. Am. Soc. Nephrol. 4 1993 1104 1110
35. W.R. Burack, and T.W. Sturgill The activating dual phosphorylation of MAPK by MEK is nonprocessive Biochemistry 36 1997 5929 5933
36. K. Aoki, and M. Yamada M. Matsuda Processive phosphorylation of ERK MAP kinase in mammalian cells Proc. Natl. Acad. Sci. USA 108 2011 12675 12680
37. Y.Y. Zhang, and Z.Q. Mei Z.X. Wang Enzymatic activity and substrate specificity of mitogen-activated protein kinase p38α in different phosphorylation states J. Biol. Chem. 283 2008 26591 26601
38. B. Zhou, and Z.X. Wang Z.Y. Zhang The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases J. Biol. Chem. 277 2002 31818 31825
39. M. Bell, and R. Capone D. Engelberg Isolation of hyperactive mutants of the MAPK p38/Hog1 that are independent of MAPK kinase activation J. Biol. Chem. 276 2001 25351 25358
40. M. Bell, and D. Engelberg Phosphorylation of Tyr-176 of the yeast MAPK Hog1/p38 is not vital for Hog1 biological activity J. Biol. Chem. 278 2003 14603 14606
41. M. Avitzour, and R. Diskin O. Livnah Intrinsically active variants of all human p38 isoforms FEBS J. 274 2007 963 975
42. K.A. Resing, and S.J. Mansour N.G. Ahn Determination of v-Mos-catalyzed phosphorylation sites and autophosphorylation sites on MAP kinase kinase by ESI/MS Biochemistry 34 1995 2610 2620
43. Y. Zhao, and Z.Y. Zhang The mechanism of dephosphorylation of extracellular signal-regulated kinase 2 by mitogen-activated protein kinase phosphatase 3 J. Biol. Chem. 276 2001 32382 32391
44. A. Farooq, and M.M. Zhou Structure and regulation of MAPK phosphatases Cell. Signal. 16 2004 769 779
45. C. Salazar, and T. Höfer Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions FEBS J. 274 2007 1046 1061
46. M.L. Sohaskey, and J.E. Ferrell Jr. Distinct, constitutively active MAPK phosphatases function in Xenopus oocytes: implications for p42 MAPK regulation in vivo Mol. Biol. Cell 10 1999 3729 3743
47. T. Zhou, and M. Raman E.J. Goldsmith Crystal structure of the TAO2 kinase domain: activation and specificity of a Ste20p MAP3K Structure 12 2004 1891 1900
48. D.R. Knighton, and J.H. Zheng J.M. Sowadski Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase Science 253 1991 414 420
49. J.F. Ohren, and H. Chen C.A. Hasemann Structures of human MAP kinase kinase 1 (MEK1) and MEK2 describe novel noncompetitive kinase inhibition Nat. Struct. Mol. Biol. 11 2004 1192 1197
50. X. Min, and R. Akella E.J. Goldsmith The structure of the MAP2K MEK6 reveals an autoinhibitory dimer Structure 17 2009 96 104
51. T. Matsumoto, and T. Kinoshita T. Tada Crystal structures of MKK4 kinase domain reveal that substrate peptide binds to an allosteric site and induces an auto-inhibition state Biochem. Biophys. Res. Commun. 400 2010 369 373
52. S.R. Hubbard Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog EMBO J. 16 1997 5572 5581
53. A.D. Sharrocks, S.H. Yang, and A. Galanis Docking domains and substrate-specificity determination for MAP kinases Trends Biochem. Sci. 25 2000 448 453
54. T. Kallunki, and B. Su M. Karin JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation Genes Dev. 8 1994 2996 3007
55. T. Tanoue, and E. Nishida Molecular recognitions in the MAP kinase cascades Cell. Signal. 15 2003 455 462
56. A.J. Bardwell, E. Frankson, and L. Bardwell Selectivity of docking sites in MAPK kinases J. Biol. Chem. 284 2009 13165 13173
57. L. Bardwell Mechanisms of MAPK signaling specificity Biochem. Soc. Trans. 34 2006 837 841
58. Y.Y. Zhang, J.W. Wu, and Z.X. Wang A distinct interaction mode revealed by the crystal structure of p38α with the MAPK binding domain of MKP5 Sci. Signal. 4 2011 ra88
59. E.J. Goldsmith Three-dimensional docking in the MAPK p38α Sci. Signal. 4 2011 pe47
60. T. Zhou, and L. Sun E.J. Goldsmith Docking interactions induce exposure of activation loop in the MAP kinase ERK2 Structure 14 2006 1011 1019
61. R. Akella, and X. Min E.J. Goldsmith The third conformation of p38α MAP kinase observed in phosphorylated p38α and in solution Structure 18 2010 1571 1578
62. C.I. Chang, and B.E. Xu E.J. Goldsmith Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b Mol. Cell 9 2002 1241 1249
63. Y.S. Heo, and S.K. Kim C.H. Yang Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125 EMBO J. 23 2004 2185 2195
64. A. Goldbeter, and D.E. Koshland Jr. An amplified sensitivity arising from covalent modification in biological systems Proc. Natl. Acad. Sci. USA 78 1981 6840 6844
65. A. Goldbeter, and D.E. Koshland Jr. Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects J. Biol. Chem. 259 1984 14441 14447
66. N.I. Markevich, J.B. Hoek, and B.N. Kholodenko Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades J. Cell Biol. 164 2004 353 359
67. S. Legewie, and B. Schoeberl H. Herzel Competing docking interactions can bring about bistability in the MAPK cascade Biophys. J. 93 2007 2279 2288
68. J. Gunawardena Multisite protein phosphorylation makes a good threshold but can be a poor switch Proc. Natl. Acad. Sci. USA 102 2005 14617 14622
69. C. Richardson, and D.R. Alessi The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signaling pathway J. Cell Sci. 121 2008 3293 3304
70. N.B. Trunnell, and A.C. Poon J.E. Ferrell Jr. Ultrasensitivity in the regulation of Cdc25C by Cdk1 Mol. Cell 41 2011 263 274
71. R. Dajani, and E. Fraser L.H. Pearl Crystal structure of glycogen synthase kinase 3 β: structural basis for phosphate-primed substrate specificity and autoinhibition Cell 105 2001 721 732
72. S.Y. Kim, and J.E. Ferrell Jr. Substrate competition as a source of ultrasensitivity in the inactivation of Wee1 Cell 128 2007 1133 1145
73. P. Kuzmic DYNAFIT - a software package for enzymology Methods Enzymol. 467 2009 247 280
74. U.S. Bhalla Sigaling in small subcellular voumes II. Stochastic and diffusion effects on synaptic network properties Biophys. J. 87 2004 745 753