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How MAP kinase modules function as robust, yet adaptable, circuits

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Pages 2379-2390 | Received 17 Apr 2014, Accepted 23 May 2014, Published online: 19 Jun 2014

References

  • Kimura M, Ohta T. On some principles governing molecular evolution. Proc Natl Acad Sci U S A 1974; 71:2848 - 52; http://dx.doi.org/10.1073/pnas.71.7.2848; PMID: 4527913
  • Kirschner M, Gerhart J. Evolvability. Proc Natl Acad Sci U S A 1998; 95:8420 - 7; http://dx.doi.org/10.1073/pnas.95.15.8420; PMID: 9671692
  • Gerhart J. 1998 Warkany lecture: signaling pathways in development. Teratology 1999; 60:226 - 39; http://dx.doi.org/10.1002/(SICI)1096-9926(199910)60:4<226::AID-TERA7>3.0.CO;2-W; PMID: 10508976
  • Gerhart J, Kirschner M. The theory of facilitated variation. Proc Natl Acad Sci U S A 2007; 104:Suppl 1 8582 - 9; http://dx.doi.org/10.1073/pnas.0701035104; PMID: 17494755
  • Qi M, Elion EA. MAP kinase pathways. J Cell Sci 2005; 118:3569 - 72; http://dx.doi.org/10.1242/jcs.02470; PMID: 16105880
  • Keshet Y, Seger R. The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions. Methods Mol Biol 2010; 661:3 - 38; http://dx.doi.org/10.1007/978-1-60761-795-2_1; PMID: 20811974
  • Ferrell JE Jr.. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem Sci 1996; 21:460 - 6; http://dx.doi.org/10.1016/S0968-0004(96)20026-X; PMID: 9009826
  • Kholodenko BN, Birtwistle MR. Four-dimensional dynamics of MAPK information processing systems. Wiley Interdiscip Rev Syst Biol Med 2009; 1:28 - 44; http://dx.doi.org/10.1002/wsbm.16; PMID: 20182652
  • Brown GC, Hoek JB, Kholodenko BN. Why do protein kinase cascades have more than one level?. Trends Biochem Sci 1997; 22:288; http://dx.doi.org/10.1016/S0968-0004(97)82216-5; PMID: 9270298
  • Huang CY, Ferrell JE Jr.. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A 1996; 93:10078 - 83; http://dx.doi.org/10.1073/pnas.93.19.10078; PMID: 8816754
  • Burack WR, Sturgill TW. The activating dual phosphorylation of MAPK by MEK is nonprocessive. Biochemistry 1997; 36:5929 - 33; http://dx.doi.org/10.1021/bi970535d; PMID: 9166761
  • Ferrell JE Jr.. How responses get more switch-like as you move down a protein kinase cascade. Trends Biochem Sci 1997; 22:288 - 9; http://dx.doi.org/10.1016/S0968-0004(97)82217-7; PMID: 9270299
  • Kitano H. Biological robustness. Nat Rev Genet 2004; 5:826 - 37; http://dx.doi.org/10.1038/nrg1471; PMID: 15520792
  • Kitano H. Towards a theory of biological robustness. Mol Syst Biol 2007; 3:137; http://dx.doi.org/10.1038/msb4100179; PMID: 17882156
  • Ferrell JE Jr., Machleder EM. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 1998; 280:895 - 8; http://dx.doi.org/10.1126/science.280.5365.895; PMID: 9572732
  • O’Shaughnessy EC, Palani S, Collins JJ, Sarkar CA. Tunable signal processing in synthetic MAP kinase cascades. Cell 2011; 144:119 - 31; http://dx.doi.org/10.1016/j.cell.2010.12.014; PMID: 21215374
  • Harding AS, Hancock JF. Using plasma membrane nanoclusters to build better signaling circuits. Trends Cell Biol 2008; 18:364 - 71; http://dx.doi.org/10.1016/j.tcb.2008.05.006; PMID: 18620858
  • Shin SY, Rath O, Choo SM, Fee F, McFerran B, Kolch W, Cho KH. Positive- and negative-feedback regulations coordinate the dynamic behavior of the Ras-Raf-MEK-ERK signal transduction pathway. J Cell Sci 2009; 122:425 - 35; http://dx.doi.org/10.1242/jcs.036319; PMID: 19158341
  • Bagowski CP, Ferrell JE Jr.. Bistability in the JNK cascade. Curr Biol 2001; 11:1176 - 82; http://dx.doi.org/10.1016/S0960-9822(01)00330-X; PMID: 11516948
  • Santos SD, Verveer PJ, Bastiaens PI. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat Cell Biol 2007; 9:324 - 30; http://dx.doi.org/10.1038/ncb1543; PMID: 17310240
  • Xiong W, Ferrell JE Jr.. A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision. Nature 2003; 426:460 - 5; http://dx.doi.org/10.1038/nature02089; PMID: 14647386
  • Ferrell JE Jr.. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 2002; 14:140 - 8; http://dx.doi.org/10.1016/S0955-0674(02)00314-9; PMID: 11891111
  • Aoki K, Yamada M, Kunida K, Yasuda S, Matsuda M. Processive phosphorylation of ERK MAP kinase in mammalian cells. Proc Natl Acad Sci U S A 2011; 108:12675 - 80; http://dx.doi.org/10.1073/pnas.1104030108; PMID: 21768338
  • Levchenko A, Bruck J, Sternberg PW. Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci U S A 2000; 97:5818 - 23; http://dx.doi.org/10.1073/pnas.97.11.5818; PMID: 10823939
  • Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?. Proc Natl Acad Sci U S A 2004; 101:15386 - 91; http://dx.doi.org/10.1073/pnas.0403984101; PMID: 15494441
  • Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 1999; 79:143 - 80; PMID: 9922370
  • Manning G, Plowman GD, Hunter T, Sudarsanam S. Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 2002; 27:514 - 20; http://dx.doi.org/10.1016/S0968-0004(02)02179-5; PMID: 12368087
  • Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298:1912 - 34; http://dx.doi.org/10.1126/science.1075762; PMID: 12471243
  • Kyriakis JM, Avruch J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev 2012; 92:689 - 737; http://dx.doi.org/10.1152/physrev.00028.2011; PMID: 22535895
  • Blank JL, Gerwins P, Elliott EM, Sather S, Johnson GL. Molecular cloning of mitogen-activated protein/ERK kinase kinases (MEKK) 2 and 3. Regulation of sequential phosphorylation pathways involving mitogen-activated protein kinase and c-Jun kinase. J Biol Chem 1996; 271:5361 - 8; http://dx.doi.org/10.1074/jbc.271.10.5361; PMID: 8621389
  • Deacon K, Blank JL. MEK kinase 3 directly activates MKK6 and MKK7, specific activators of the p38 and c-Jun NH2-terminal kinases. J Biol Chem 1999; 274:16604 - 10; http://dx.doi.org/10.1074/jbc.274.23.16604; PMID: 10347227
  • Nakamura K, Johnson GL. PB1 domains of MEKK2 and MEKK3 interact with the MEK5 PB1 domain for activation of the ERK5 pathway. J Biol Chem 2003; 278:36989 - 92; http://dx.doi.org/10.1074/jbc.C300313200; PMID: 12912994
  • Salmeron A, Ahmad TB, Carlile GW, Pappin D, Narsimhan RP, Ley SC. Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncoprotein, a novel MAP kinase kinase kinase. EMBO J 1996; 15:817 - 26; PMID: 8631303
  • Gotoh I, Adachi M, Nishida E. Identification and characterization of a novel MAP kinase kinase kinase, MLTK. J Biol Chem 2001; 276:4276 - 86; http://dx.doi.org/10.1074/jbc.M008595200; PMID: 11042189
  • Chiariello M, Marinissen MJ, Gutkind JS. Multiple mitogen-activated protein kinase signaling pathways connect the cot oncoprotein to the c-jun promoter and to cellular transformation. Mol Cell Biol 2000; 20:1747 - 58; http://dx.doi.org/10.1128/MCB.20.5.1747-1758.2000; PMID: 10669751
  • Bardwell L, Cook JG, Chang EC, Cairns BR, Thorner J. Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol Cell Biol 1996; 16:3637 - 50; PMID: 8668180
  • Bardwell L, Thorner J. A conserved motif at the amino termini of MEKs might mediate high-affinity interaction with the cognate MAPKs. Trends Biochem Sci 1996; 21:373 - 4; http://dx.doi.org/10.1016/0968-0004(96)30032-7; PMID: 8918190
  • Fukuda M, Gotoh I, Gotoh Y, Nishida E. Cytoplasmic localization of mitogen-activated protein kinase kinase directed by its NH2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J Biol Chem 1996; 271:20024 - 8; http://dx.doi.org/10.1074/jbc.271.33.20024; PMID: 8702720
  • 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 1997; 16:1901 - 8; http://dx.doi.org/10.1093/emboj/16.8.1901; PMID: 9155016
  • Bardwell AJ, Frankson E, Bardwell L. Selectivity of docking sites in MAPK kinases. J Biol Chem 2009; 284:13165 - 73; http://dx.doi.org/10.1074/jbc.M900080200; PMID: 19196711
  • Seger R, Seger D, Lozeman FJ, Ahn NG, Graves LM, Campbell JS, Ericsson L, Harrylock M, Jensen AM, Krebs EG. Human T-cell mitogen-activated protein kinase kinases are related to yeast signal transduction kinases. J Biol Chem 1992; 267:25628 - 31; PMID: 1281467
  • Kato Y, Kravchenko VV, Tapping RI, Han J, Ulevitch RJ, Lee JD. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J 1997; 16:7054 - 66; http://dx.doi.org/10.1093/emboj/16.23.7054; PMID: 9384584
  • Zheng CF, Guan KL. Properties of MEKs, the kinases that phosphorylate and activate the extracellular signal-regulated kinases. J Biol Chem 1993; 268:23933 - 9; PMID: 8226933
  • Raingeaud J, Whitmarsh AJ, Barrett T, Dérijard B, Davis RJ. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol 1996; 16:1247 - 55; PMID: 8622669
  • Lu X, Nemoto S, Lin A. Identification of c-Jun NH2-terminal protein kinase (JNK)-activating kinase 2 as an activator of JNK but not p38. J Biol Chem 1997; 272:24751 - 4; http://dx.doi.org/10.1074/jbc.272.40.24751; PMID: 9312068
  • Tournier C, Whitmarsh AJ, Cavanagh J, Barrett T, Davis RJ. Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc Natl Acad Sci U S A 1997; 94:7337 - 42; http://dx.doi.org/10.1073/pnas.94.14.7337; PMID: 9207092
  • Sánchez I, Hughes RT, Mayer BJ, Yee K, Woodgett JR, Avruch J, Kyriakis JM, Zon LI. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 1994; 372:794 - 8; http://dx.doi.org/10.1038/372794a0; PMID: 7997269
  • Dérijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ, Davis RJ. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 1995; 267:682 - 5; http://dx.doi.org/10.1126/science.7839144; PMID: 7839144
  • Yoon S, Seger R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 2006; 24:21 - 44; http://dx.doi.org/10.1080/02699050500284218; PMID: 16393692
  • Murphy LO, MacKeigan JP, Blenis J. A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol Cell Biol 2004; 24:144 - 53; http://dx.doi.org/10.1128/MCB.24.1.144-153.2004; PMID: 14673150
  • Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J. Molecular interpretation of ERK signal duration by immediate early gene products. Nat Cell Biol 2002; 4:556 - 64; PMID: 12134156
  • Lin J, Harding A, Giurisato E, Shaw AS. KSR1 modulates the sensitivity of mitogen-activated protein kinase pathway activation in T cells without altering fundamental system outputs. Mol Cell Biol 2009; 29:2082 - 91; http://dx.doi.org/10.1128/MCB.01634-08; PMID: 19188442
  • Malleshaiah MK, Shahrezaei V, Swain PS, Michnick SW. The scaffold protein Ste5 directly controls a switch-like mating decision in yeast. Nature 2010; 465:101 - 5; http://dx.doi.org/10.1038/nature08946; PMID: 20400943
  • Burack WR, Shaw AS. Signal transduction: hanging on a scaffold. Curr Opin Cell Biol 2000; 12:211 - 6; http://dx.doi.org/10.1016/S0955-0674(99)00078-2; PMID: 10712921
  • Ferrell JE Jr.. What do scaffold proteins really do?. Sci STKE 2000; 2000:pe1; http://dx.doi.org/10.1126/stke.2000.52.pe1; PMID: 11752612
  • Tian T, Harding A, Inder K, Plowman S, Parton RG, Hancock JF. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol 2007; 9:905 - 14; http://dx.doi.org/10.1038/ncb1615; PMID: 17618274
  • Takahashi S, Pryciak PM. Membrane localization of scaffold proteins promotes graded signaling in the yeast MAP kinase cascade. Curr Biol 2008; 18:1184 - 91; PMID: 18722124
  • Giurisato E, Lin J, Harding A, Cerutti E, Cella M, Lewis RE, Colonna M, Shaw AS. The mitogen-activated protein kinase scaffold KSR1 is required for recruitment of extracellular signal-regulated kinase to the immunological synapse. Mol Cell Biol 2009; 29:1554 - 64; http://dx.doi.org/10.1128/MCB.01421-08; PMID: 19139278
  • Bhattacharyya RP, Reményi A, Good MC, Bashor CJ, Falick AM, Lim WA. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 2006; 311:822 - 6; http://dx.doi.org/10.1126/science.1120941; PMID: 16424299
  • Brennan DF, Dar AC, Hertz NT, Chao WC, Burlingame AL, Shokat KM, Barford D. A Raf-induced allosteric transition of KSR stimulates phosphorylation of MEK. Nature 2011; 472:366 - 9; http://dx.doi.org/10.1038/nature09860; PMID: 21441910
  • Morrison DK, Davis RJ. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 2003; 19:91 - 118; http://dx.doi.org/10.1146/annurev.cellbio.19.111401.091942; PMID: 14570565
  • Good MC, Zalatan JG, Lim WA. Scaffold proteins: hubs for controlling the flow of cellular information. Science 2011; 332:680 - 6; http://dx.doi.org/10.1126/science.1198701; PMID: 21551057
  • Li GW, Xie XS. Central dogma at the single-molecule level in living cells. Nature 2011; 475:308 - 15; http://dx.doi.org/10.1038/nature10315; PMID: 21776076
  • Feinerman O, Veiga J, Dorfman JR, Germain RN, Altan-Bonnet G. Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 2008; 321:1081 - 4; http://dx.doi.org/10.1126/science.1158013; PMID: 18719282
  • Cohen AA, Geva-Zatorsky N, Eden E, Frenkel-Morgenstern M, Issaeva I, Sigal A, Milo R, Cohen-Saidon C, Liron Y, Kam Z, et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008; 322:1511 - 6; http://dx.doi.org/10.1126/science.1160165; PMID: 19023046
  • Csete M, Doyle J. Bow ties, metabolism and disease. Trends Biotechnol 2004; 22:446 - 50; http://dx.doi.org/10.1016/j.tibtech.2004.07.007; PMID: 15331224
  • Oda K, Matsuoka Y, Funahashi A, Kitano H. A comprehensive pathway map of epidermal growth factor receptor signaling. Mol Syst Biol 2005; 1:0010; http://dx.doi.org/10.1038/msb4100014; PMID: 16729045
  • Wang LS, Leebens-Mack J, Kerr Wall P, Beckmann K, dePamphilis CW, Warnow T. The impact of multiple protein sequence alignment on phylogenetic estimation. IEEE/ACM Trans Comput Biol Bioinform 2011; 8:1108 - 19; http://dx.doi.org/10.1109/TCBB.2009.68; PMID: 21566256
  • Hanks SK, Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 1995; 9:576 - 96; PMID: 7768349
  • Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001; 17:754 - 5; http://dx.doi.org/10.1093/bioinformatics/17.8.754; PMID: 11524383
  • Drummond AJAB, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, et al. Geneious v5.6. Available from http://wwwgeneiouscom 2012.
  • Michaelis L, Menten ML, Johnson KA, Goody RS. The original Michaelis constant: translation of the 1913 Michaelis-Menten paper. Biochemistry 2011; 50:8264 - 9; http://dx.doi.org/10.1021/bi201284u; PMID: 21888353
  • Koshland DE Jr., Goldbeter A, Stock JB. Amplification and adaptation in regulatory and sensory systems. Science 1982; 217:220 - 5; http://dx.doi.org/10.1126/science.7089556; PMID: 7089556

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