ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL

EMBO Journal

Volumn 26, Issue 12, 2007, Pages 2856-2867

  Ewings, Katherine E ^a   Hadfield Moorhouse, Kathryn ^a   Wiggins, Ceri M ^a   Wickenden, Julie A ^a   Balmanno, Kathryn ^a   Gilley, Rebecca ^a   Degenhardt, Kurt ^b   White, Eileen ^b   Cook, Simon J ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Apoptosis; Bcl xL; Bim; ERK1 2; Mcl 1

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1;

ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DISSOCIATION; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

APOPTOSIS REGULATORY PROTEINS; BCL-X PROTEIN; CELL LINE; CULTURE MEDIA, SERUM-FREE; HUMANS; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 34250892541     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601723     Document Type: Article

References (44)

1. Akiyama T, Bouillet P, Miyazaki T, Kadono Y, Chikuda H, Hikita A, Seto H, Okada T, Inaba T, Sanjay A, Baron R, Kawaguchi H, Oda H, Nakamura K, Strasser A, Tanaka S (2003) Regulation of osteoclast apoptosis by ubiquitylation of proapoptotic BH3-only Bcl-2 family member Bim. EMBO J 24: 6653-6664
2. Austin M, Cook SJ (2005) Increased expression of Mcl-1 is required for protection against serum starvation in PTEN null mouse embryonic fibroblasts, but repression of Bim is favored in human glioblastomas. J Biol Chem 280: 33280-33288
3. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286: 1358-1362
4. Boughan PK, Argent RH, Body-Malapel M, Park J-H, Ewings KE, Bowie AG, Ong SJ, Cook SJ, Sorensen OE, Manzo BA, Klein NJ, Nunez G, Atherton JC, Bajaj-Elliott M (2006) Nucleotide-binding oligomerisation domain-1 (NOD-1) and epidermal growth factor receptor (EGFR): critical regulators of β-defensins during H. pylori infection. J Biol Chem 281: 11637-11648
5. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F, Adams JM, Strasser A (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286: 1735-1738
6. Chalmers CJ, Balmanno K, Hadfield K, Ley R, Cook SJ (2003) Thrombin inhibits Bim expression and prevents serum-withdrawal-induced apoptosis via protease-activated receptor 1. Biochem J 375: 99-109
7. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403
8. Chipuk JE, Green DR (2005) Do inducers of apoptosis trigger caspase-independent cell death? Nat Rev Mo Cell Biol 6: 268-275
9. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2: 647-656
10. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241
11. Datta SR, Katsov A, Hu L, Petros A, Fesik SW, Yaffe MB, Greenberg ME (2000) 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol Cell 6: 41-51
12. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ (2000) Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 10: 1201-1204
13. Domina AM, Vrana JA, Gregory MA, Hann SR, Craig RW (2004) MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23: 5301-5315
14. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208
15. Gilley J, Coffer PJ, Ham J (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 162: 613-622
16. Gomez-Bougie P, Bataille R, Amiot M (2005) Endogenous association of Bim BH3-only protein with Mcl-1, Bcl-xL and Bcl-2 on mitochondria in human B cells. Eur J Immunol 35: 971-976
17. Griffiths GJ, Corfe BM, Savory P, Leech S, Esposti MD, Hickman JA, Dive C (2001) Cellular damage signals promote sequential changes at the N-terminus and BH-1 domain of the pro-apoptotic protein Bak. Oncogene 20: 7668-7676
18. Harris CA, Johnson Jr EM (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J Biol Chem 276: 37754-37760
19. Hinds MG, Smits C, Fredericks-Short R, Risk JM, Bailey M, Huang DC, Day CL (2006) Bim, Bad and Bmf: intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ 14: 128-136
20. Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100: 2432-2437
21. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ (2003) Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 278: 18811-18816
22. Ley R, Ewings KE, Hadfield K, Cook SJ (2005b) Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ 12: 1008-1014
23. Ley R, Ewings KE, Hadfield K, Howes E, Balmanno K, Cook SJ (2004) Extracellular signal-regulated kinases 1/2 are serum-stimulated 'Bim(EL) kinases' that bind to the BH3-only protein BimEL causing its phosphorylation and turnover. J Biol Chem 279: 8837-8847
24. EL. J Biol Chem 280: 17657-17663
25. Lizcano JM, Morrice N, Cohen P (2000) Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem J 349: 547-557
26. Luciano F, Jacquel A, Colosetti P, Herrant M, Cagnol S, Pages G, Auberger P (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22: 6785-6793
27. Makin GW, Corfe BM, Griffiths GJ, Thistlethwaite A, Hickman JA, Dive C (2001) Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/complexes occur regardless of cell fate. EMBO J 20: 6306-6315
28. Marani M, Hancock D, Lopes R, Tenev T, Downward J, Lemoine NR (2004) Role of Bim in the survival pathway induced by Raf in epithelial cells. Oncogene 23: 2431-2441
29. Marani M, Tenev T, Hancock D, Downward J, Lemoine NR (2002) Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol 22: 3577-3589
30. Nakano K, Vousden KH (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7: 683-694
31. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S, Huang DC (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J 17: 384-395
32. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3: 287-296
33. Puthalakath H, Strasser A (2002) Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 9: 505-512
34. Ranger AM, Zha J, Harada H, Datta SR, Danial NN, Gilmore AP, Kutok JL, Le Beau MM, Greenberg ME, Korsmeyer SJ (2003) Bad-deficient mice develop diffuse large B cell lymphoma. Proc Natl Acd Sci USA 100: 9324-9329
35. Reginato MJ, Mills KR, Becker EB, Lynch DK, Bonni A, Muthuswamy SK, Brugge JS (2005) Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol Cell Biol 25: 4591-4601
36. Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J, Muthuswamy SK, Brugge JS (2003) Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol 5: 733-740
37. Scheid MP, Schubert KM, Duronio V (1999) Regulation of Bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase. J Biol Chem 274: 31108-31113
38. Tan TT, Degenhardt K, Nelson DA, Beaudoin B, Nieves-Neira W, Bouillet P, Villunger A, Adams JM, White E (2005) Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Cancer Cell 7: 227-238
39. Wang P, Gilmore AP, Streuli CH (2004) Bim is an apoptosis sensor that responds to loss of survival signals delivered by epidermal growth factor but not those provided by integrins. J Biol Chem 279: 41280-41285
40. Weston CR, Balmanno K, Chalmers C, Hadfield K, Molton SA, Ley R, Wagner EF, Cook SJ (2003) Activation of ERK1/2 by ΔRaf-1:ER* represses Bim expression independently of the JNK or PI3K pathways. Oncogene 22: 1281-1293
41. Whitfield J, Neame SJ, Paquet L, Bernard O, Ham J (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29: 629-643
42. Willis SN, Adams JM (2005) Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 17: 617-625
43. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, Strasser A, Kluck RM, Adams JM, Huang DC (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859
44. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87: 619-628