Osmostress Induces Autophosphorylation of Hog1 via a C-Terminal Regulatory Region That Is Conserved in p38α

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Maayan, Inbal ^a   Beenstock, Jonah ^a   Marbach, Irit ^a   Tabachnick, Shira ^a   Livnah, Oded ^a   Engelberg, David ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; PROTEIN HOG1; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL CELL; NONHUMAN; ONCOTIC PRESSURE; OSMOTIC STRESS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; MAP KINASE KINASE 6; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 14; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, GENETIC; MUTATION; OSMOTIC PRESSURE; PHOSPHORYLATION; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84866285560     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044749     Document Type: Article

References (49)

1. Huse M, Kuriyan J, (2002) The conformational plasticity of protein kinases. Cell 109: 275-282.
2. Lochhead PA, (2009) Protein kinase activation loop autophosphorylation in cis: overcoming a Catch-22 situation. Sci Signal 2: pe4.
3. Nolen B, Taylor S, Ghosh G, (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15: 661-675.
4. Chou MM, Hou W, Johnson J, Graham LK, Lee MH, et al. (1998) Regulation of protein kinase C zeta by PI 3-kinase and PDK1. Curr Biol 8: 1069-1077.
5. Belham C, Wu S, Avruch J, (1999) Intracellular signalling: PDK1-a kinase at the hub of things. Curr Biol 9: R93-96.
6. Sclafani RA, (1996) Cyclin dependent kinase activating kinases. Curr Opin Cell Biol 8: 788-794.
7. Kyriakis JM, Avruch J, (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869.
8. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22: 153-183.
9. Marshall CJ, (1994) MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Genet Dev 4: 82-89.
10. Lewis T S, Shapiro PS, Ahn NG, (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74: 49-139.
11. Anderson NG, Maller JL, Tonks NK, Sturgill TW, (1990) Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature 343: 651-653.
12. Ahn NG, Seger R, Bratlien RL, Diltz CD, Tonks NK, et al. (1991) 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: 4220-4227.
13. Gartner A, Nasmyth K, Ammerer G, (1992) Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1. Genes Dev 6: 1280-1292.
14. Robbins DJ, Zhen E, Owaki H, Vanderbilt CA, Ebert D, et al. (1993) Regulation and properties of extracellular signal-regulated protein kinase 1 and 2 in vitro. J Biol Chem 268: 5097-5106.
15. Bell M, Engelberg D, (2003) Phosphorylation of Tyr-176 of the yeast MAPK Hog1/p38 is not vital for Hog1 biological activity. J Biol Chem 278: 14603-14606.
16. Askari N, Beenstock J, Livnah O, Engelberg D, (2009) p38alpha is active in vitro and in vivo when monophosphorylated at threonine 180. Biochemistry 48: 2497-2504.
17. Yao Z, Dolginov Y, Hanoch T, Yung Y, Ridner G, et al. (2000) Detection of partially phosphorylated forms of ERK by monoclonal antibodies reveals spatial regulation of ERK activity by phosphatases. FEBS Lett 468: 37-42.
18. Zhang YY, Mei ZQ, Wu JW, Wang ZX, (2008) Enzymatic activity and substrate specificity of mitogen-activated protein kinase p38alpha in different phosphorylation states. J Biol Chem 283: 26591-26601.
19. Zhou B, Zhang ZY, (2002) The activity of the extracellular signal-regulated kinase 2 is regulated by differential phosphorylation in the activation loop. J Biol Chem 277: 13889-13899.
20. Salvador JM, Mittelstadt PR, Guszczynski T, Copeland TD, Yamaguchi H, et al. (2005) Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat Immunol 6: 390-395.
21. Ge B, Gram H, Di Padova F, Huang B, New L, et al. (2002) MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha. Science 295: 1291-1294.
22. Bell M, Capone R, Pashtan I, Levitzki A, Engelberg D (2001) Isolation of hyperactive mutants of the MAPK p38/Hog1 that are independent of MAPK kinase activation. J Biol Chem 276, 25351-25358.
23. Avitzour M, Diskin R, Raboy B, Askari N, Engelberg D, et al. (2007) Intrinsically active variants of all human p38 isoforms. Febs J 274: 963-975.
24. Diskin R, Askari N, Capone R, Engelberg D, Livnah O, (2004) Active mutants of the human p38alpha mitogen-activated protein kinase. J Biol Chem 279: 47040-47049.
25. Askari N, Diskin R, Avitzour M, Capone R, Livnah O, et al. (2007) Hyperactive variants of p38alpha induce, whereas hyperactive variants of p38gamma suppress, activating protein 1-mediated transcription. J Biol Chem 282: 91-99.
26. Levin-Salomon V, Kogan K, Ahn NG, Livnah O, Engelberg D, (2008) Isolation of intrinsically active (MEK-independent) variants of the ERK family of mitogen-activated protein (MAP) kinases. J Biol Chem 283: 34500-34510.
27. Levin-Salomon V, Maayan I, Avrahami-Moyal L, Marbach I, Livnah O, et al. (2009) When expressed in yeast, mammalian mitogen-activated protein kinases lose proper regulation and become spontaneously phosphorylated. Biochem J 417: 331-340.
28. Brewster JL, de Valoir T, Dwyer ND, Winter E, Gustin MC, (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
29. Galcheva-Gargova Z, Derijard B, Wu IH Davis RJ, (1994) An osmosensing signal transduction pathway in mammalian cells. Science 265: 806-808.
30. Hohmann S, (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
31. Clotet J, Posas F, (2007) Control of cell cycle in response to osmostress: lessons from yeast. Methods Enzymol 428: 63-76.
32. Maayan I, Engelberg D, (2009) The yeast MAPK Hog1 is not essential for immediate survival under osmostress. FEBS Lett 583: 2015-2020.
33. Hohmann S, Krantz M, Nordlander B, (2007) Yeast osmoregulation. Methods Enzymol 428: 29-45.
34. Gustin MC, Albertyn J, Alexander M, Davenport K, (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264-1300.
35. de Nadal E, Alepuz PM, Posas F, (2002) Dealing with osmostress through MAP kinase activation. EMBO Rep 3: 735-740.
36. Chen RE, Thorner J, (2007) Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773: 1311-1140.
37. Westfall PJ, Patterson JC, Chen RE, Thorner J, (2008) Stress resistance and signal fidelity independent of nuclear MAPK function. Proc Natl Acad Sci U S A 105: 12212-12217.
38. Saito H, Tatebayashi K, (2004) Regulation of the osmoregulatory HOG MAPK cascade in yeast. J Biochem 136: 267-272.
39. Yaakov G, Bell M, Hohmann S, Engelberg D, (2003) Combination of two activating mutations in one HOG1 gene forms hyperactive enzymes that induce growth arrest. Mol Cell Biol 23: 4826-4840.
40. Friedmann Y, Shriki A, Bennett ER, Golos S, Diskin R, et al. (2006) JX401, A p38alpha inhibitor containing a 4-benzylpiperidine motif, identified via a novel screening system in yeast. Mol Pharmacol 70: 1395-1405.
41. Murakami Y, Tatebayashi K, Saito H, (2008) Two adjacent docking sites in the yeast Hog1 mitogen-activated protein (MAP) kinase differentially interact with the Pbs2 MAP kinase kinase and the Ptp2 protein tyrosine phosphatase. Mol Cell Biol 28: 2481-2494.
42. Wilson C, Heberle-Bors E, Vicente O, (1997) A conserved notif at the carboxy terminus of MAP kinases. J Mol Evol 44: 683-685.
43. Chang CI, Xu BE, Akella R, Cobb MH, Goldsmith EJ, (2002) Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b. Mol Cell 9: 1241-1249.
44. Diskin R, Lebendiker M, Engelberg D, Livnah O, (2007) Structures of p38alpha active mutants reveal conformational changes in L16 loop that induce autophosphorylation and activation. J Mol Biol 365: 66-76.
45. Seger R, Ahn NG, Boulton TG, Yancopoulos GD, Panayotatos N, et al. (1991) Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: implications for their mechanism of activation. Proc Natl Acad Sci U S A 88: 6142-6146.
46. Macia J, Regot S, Peeters T, Conde N, Sole R, et al. (2009) Dynamic signaling in the Hog1 MAPK pathway relies on high basal signal transduction. Sci Signal 2: ra13.
47. Maeda T, Wurgler-Murphy SM, Saito H, (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
48. Knebel A, Rahmsdorf HJ, Ullrich A, Herrlich P, (1996) Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. Embo J 15: 5314-5325.
49. Nitta RT, Chu AH, Wong AJ, (2008) Constitutive activity of JNK2 alpha2 is dependent on a unique mechanism of MAPK activation. J Biol Chem 283: 34935-34945.