CHIP-dependent termination of MEKK2 regulates temporal ERK activation required for proper hyperosmotic response

EMBO Journal

Volumn 29, Issue 15, 2010, Pages 2501-2514

  Maruyama, Takeshi ^a,b   Kadowaki, Hisae ^a   Okamoto, Noriaki ^a   Nagai, Atsushi ^a   Naguro, Isao ^a   Matsuzawa, Atsushi ^a   Shibuya, Hiroshi ^b   Tanaka, Keiji ^c   Murata, Shigeo ^a   Takeda, Kohsuke ^a   Nishitoh, Hideki ^a   Ichijo, Hidenori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

CHIP; hyperosmotic stress; MEKK2; ubiquitinproteasomal degradation

Indexed keywords

AQUAPORIN 1; AQUAPORIN 5; HEAT SHOCK COGNATE PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 2; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEPLETION; EMBRYO; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HYPEROSMOLALITY; HYPEROSMOTIC STRESS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; AQUAPORINS; CELLS, CULTURED; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE KINASE KINASE 2; MAP KINASE KINASE KINASES; MICE; MICE, KNOCKOUT; OSMOTIC PRESSURE; PROTEIN BINDING; RATS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 77955421222     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.141     Document Type: Article

References (48)

1. Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, Asai K (2003) Hyperosmolar mannitol simulates expression of aquaporins 4 and 9 through a p38 mitogen-activated protein kinase-dependent pathway in rat astrocytes. J Biol Chem 278: 44525-44534
2. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 19: 4535-4545
3. Blank JL, Gerwins P, Elliott EM, Sather S, Johnson GL (1996) 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 271: 5361-5368
4. Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21: 932-939
5. Brewster JL, De Valoir T, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763
6. Burg MB, Ferraris JD, Dmitrieva NI (2007) Cellular response to hyperosmotic stresses. Physiol Rev 87: 1441-1474
7. Cardozo CP, Michaud C, Ost MC, Fliss AE, Yang E, Patterson C, Hall SJ, Caplan AJ (2003) C-terminal Hsp-interacting protein slows androgen receptor synthesis and reduces its rate of degradation. Arch Biochem Biophys 410: 134-140
8. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40
9. Cheng J, Yu L, Zhang D, Huang Q, Spencer D, Su B (2005a) Dimerization through the catalytic domain is essential for MEKK2 activation. J Biol Chem 280: 13477-13482
10. Cheng J, Zhang D, Kim K, Zhao Y, Su B (2005b) Mip1, an MEKK2-interacting protein, controls MEKK2 dimerization and activation. Mol Cell Biol 25: 5955-5964
11. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Hohfeld J, Patterson C (2001) The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 3: 93-96
12. Guo Z, Clydesdale G, Cheng J, Kim K, Gan L, McConkey DJ, Ullrich SE, Zhuang Y, Su B (2002) Disruption of Mekk2 in mice reveals an unexpected role for MEKK2 in modulating T-cell receptor signal transduction. Mol Cell Biol 22: 5761-5768
13. Hammaker DR, Boyle DL, Chabaud-Riou M, Firestein GS (2004) Regulation of c-Jun N-terminal kinase by MEKK-2 and mitogenactivated protein kinase kinase kinases in rheumatoid arthritis. J Immunol 172: 1612-1618
14. Hoffert JD, Leitch V, Agre P, King LS (2000) Hypertonic induction of aquaporin-5 expression through an ERK-dependent pathway. J Biol Chem 275: 9070-9077
15. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372
16. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21: 737-748
17. Hunter T (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell 28: 730-738
18. Jiang J, Ballinger CA, Wu Y, Dai Q, Cyr DM, Hohfeld J, Patterson C (2001) CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J Biol Chem 276: 42938-42944
19. Kesavan K, Lobel-Rice K, Sun W, Lapadat R, Webb S, Johnson GL, Garrington TP (2004) MEKK2 regulates the coordinate activation of ERK5 and JNK in response to FGF-2 in fibroblasts. J Cell Physiol 199: 140-148
20. Kuivinen E, Hoffman BL, Hoffman PA, Carlin CR (1993) Structurally related class I and class II receptor protein tyrosine kinases are down-regulated by the same E3 protein coded for by human group C adenoviruses. J Cell Biol 120: 1271-1279
21. Lu Z, Xu S, Joazeiro C, Cobb MH, Hunter T (2002) The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol Cell 9: 945-956
22. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185
23. Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3: 100-105
24. Murata S, Chiba T, Tanaka K (2003) CHIP: a quality-control E3 ligase collaborating with molecular chaperones. Int J Biochem Cell Biol 35: 572-578
25. Murata S, Minami Y, Minami M, Chiba T, Tanaka K (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2: 1133-1138
26. Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nat Cell Biol 4: 556-564
27. Nakamura K, Johnson GL (2003) PB1 domains of MEKK2 and MEKK3 interact with the MEK5 PB1 domain for activation of the ERK5 pathway. J Biol Chem 278: 36989-36992
28. Nakamura K, Johnson GL (2007) Noncanonical function of MEKK2 and MEK5 PB1 domains for coordinated extracellular signalregulated kinase 5 and c-Jun N-terminal kinase signaling. Mol Cell Biol 27: 4566-4577
29. Nakamura K, Uhlik MT, Johnson NL, Hahn KM, Johnson GL (2006) PB1 domain-dependent signaling complex is required for extracellular signal-regulated kinase 5 activation. Mol Cell Biol 26: 2065-2079
30. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, Noguchi T, Matsuzawa A, Takeda K, Ichijo H (2008) ALSlinked mutant SOD1 induces ER stress-and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22: 1451-1464
31. Qui MS, Green SH (1992) PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 9: 705-717
32. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596-2606
33. Sasagawa S, Ozaki Y, Fujita K, Kuroda S (2005) Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat Cell Biol 7: 365-373
34. Schaefer BC, Ware MF, Marrack P, Fanger GR, Kappler JW, Johnson GL, Monks CR (1999) Live cell fluorescence imaging of T cell MEKK2: redistribution and activation in response to antigen stimulation of the T cell receptor. Immunity 11: 411-421
35. Shimura H, Schwartz D, Gygi SP, Kosik KS (2004) CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 279: 4869-4876
36. Su B, Cheng J, Yang J, Guo Z (2001) MEKK2 is required for T-cell receptor signals in JNK activation and interleukin-2 gene expression. J Biol Chem 276: 14784-14790
37. Sun W, Wei X, Kesavan K, Garrington TP, Fan R, Mei J, Anderson SM, Gelfand EW, Johnson GL (2003) MEK kinase 2 and the adaptor protein Lad regulate extracellular signal-regulated kinase 5 activation by epidermal growth factor via Src. Mol Cell Biol 23: 2298-2308
38. Tsai TT, Guttapalli A, Agrawal A, Albert TJ, Shapiro IM, Risbud MV (2007) MEK/ERK signaling controls osmoregulation of nucleus pulposus cells of the intervertebral disc by transactivation of TonEBP/OREBP. J Bone Miner Res 22: 965-974
39. Uhlik MT, Abell AN, Johnson NL, Sun W, Cuevas BD, Lobel-Rice KE, Horne EA, Dell'Acqua ML, Johnson GL (2003) Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat Cell Biol 5: 1104-1110
40. Umenishi F, Verkman AS, Gropper MA (1996) Quantitative analysis of aquaporin mRNA expression in rat tissues by RNase protection assay. DNA Cell Biol 15: 475-480
41. Urushitani M, Kurisu J, Tateno M, Hatakeyama S, Nakayama K, Kato S, Takahashi R (2004) CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J Neurochem 90: 231-244
42. Werlen G, Hausmann B, Palmer E (2000) A motif in the alphabeta Tcell receptor controls positive selection by modulating ERK activity. Nature 406: 422-426
43. Wiederkehr T, Bukau B, Buchberger A (2002) Protein turnover: a CHIP programmed for proteolysis. Curr Biol 12: R26-R28
44. Wu SJ, Liu FH, Hu SM,Wang C (2001) Different combinations of the heat-shock cognate protein 70 (hsc70) C-terminal functional groups are utilized to interact with distinct tetratricopeptide repeat-containing proteins. Biochem J 359(Part 2): 419-426
45. Xu W, Marcu M, Yuan X, Mimnaugh E, Patterson C, Neckers L (2002) Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc Natl Acad Sci USA 99: 12847-12852
46. Yamashita M, Ying SX, Zhang GM, Li C, Cheng SY, Deng CX, Zhang YE (2005) Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121: 101-113
47. Zhang D, Facchinetti V, Wang X, Huang Q, Qin J, Su B (2006) Identification of MEKK2/3 serine phosphorylation site targeted by the Toll-like receptor and stress pathways. EMBO J 25: 97-107
48. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, Prodromou C, Pearl LH (2005) Chaperoned ubiquitylation\crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 20: 525-538