Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1

Maurer, Ulrich; Charvet, Céline; Wagman, Allan; Dejardin, Emmanuel; Green, Douglas

doi:10.1016/j.molcel.2006.02.009

Article (Scientific journals)

Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1

Maurer, Ulrich; Charvet, Céline; Wagman, Allan et al.

2006 • In Molecular Cell, 21 (6), p. 749-760

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https://hdl.handle.net/2268/103039

DOI
10.1016/j.molcel.2006.02.009

PubMed
16543145

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Keywords :

apoptosis, Mcl-1

Abstract :

[en] We investigated the role of glycogen synthase kinase-3 (GSK-3), which is inactivated by AKT, for its role in the regulation of apoptosis. Upon IL-3 withdrawal, protein levels of MCL-1 decreased but were sustained by pharmacological inhibition of GSK-3, which prevented cytochrome c release and apoptosis. MCL-1 was phosphorylated by GSK-3 at a conserved GSK-3 phosphorylation site (S159). S159 phosphorylation of MCL-1 was induced by IL-3 withdrawal or PI3K inhibition and prevented by AKT or inhibition of GSK-3, and it led to increased ubiquitinylation and degradation of MCLA. A phosphorylation-site mutant (MCL-1(S159A)), expressed in IL-3-dependent cells, showed enhanced stability upon IL-3 withdrawal and conferred increased protection from apoptosis compared to wild-type MCL-1. The results demonstrate that the control of MCLA stability by GSK-3 is an important mechanism for the regulation of apoptosis by growth factors, PI3K, and AKT.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Maurer, Ulrich

Charvet, Céline

Wagman, Allan

Dejardin, Emmanuel ; Université de Liège - ULiège > Virologie - Immunologie

Green, Douglas

Language :

English

Title :

Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1

Publication date :

17 March 2006

Journal title :

Molecular Cell

ISSN :

1097-2765

eISSN :

1097-4164

Publisher :

Cell Press, Cambridge, United Kingdom

Volume :

Issue :

Pages :

749-760

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 November 2011

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Bibliography

J.T. Barata, A. Silva, J.G. Brandao, L.M. Nadler, A.A. Cardoso, and V.A. Boussiotis Activation of PI3K is indispensable for interleukin 7-mediated viability, proliferation, glucose use, and growth of T cell acute lymphoblastic leukemia cells J. Exp. Med. 200 2004 659 669
G.N. Bijur, P. De Sarno, and R.S. Jope Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium J. Biol. Chem. 275 2000 7583 7590
P. Bouillet, D. Metcalf, D.C. Huang, D.M. Tarlinton, T.W. Kay, F. Kontgen, J.M. Adams, and A. Strasser Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity Science 286 1999 1735 1738
A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, L.S. Hu, M.J. Anderson, K.C. Arden, J. Blenis, and M.E. Greenberg Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868
M.H. Cardone, N. Roy, H.R. Stennicke, G.S. Salvesen, T.F. Franke, E. Stanbridge, S. Frisch, and J.C. Reed Regulation of cell death protease caspase-9 by phosphorylation Science 282 1998 1318 1321
D. Chen, N. Kon, M. Li, W. Zhang, J. Qin, and W. Gu ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor Cell 121 2005 1071 1083
E.H. Cheng, M.C. Wei, S. Weiler, R.A. Flavell, T.W. Mak, T. Lindsten, and S.J. Korsmeyer BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis Mol. Cell 8 2001 705 711
P. Cohen, and S. Frame The renaissance of GSK3 Nat. Rev. Mol. Cell Biol. 2 2001 769 776
M.K. Collins, J. Marvel, P. Malde, and A. Lopez-Rivas Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents J. Exp. Med. 176 1992 1043 1051
D.A. Cross, D.R. Alessi, P. Cohen, M. Andjelkovich, and B.A. Hemmings Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 378 1995 785 789
D.A. Cross, A.A. Culbert, K.A. Chalmers, L. Facci, S.D. Skaper, and A.D. Reith Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death J. Neurochem. 77 2001 94 102
R.J. Crowder, and R.S. Freeman Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal J. Biol. Chem. 275 2000 34266 34271
S.R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M.E. Greenberg Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241
L. del Peso, M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt Science 278 1997 687 689
J.A. Diehl, M. Cheng, M.F. Roussel, and C.J. Sherr Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization Genes Dev. 12 1998 3499 3511
P.F. Dijkers, R.H. Medema, J.W. Lammers, L. Koenderman, and P.J. Coffer Expression of the proapoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1 Curr. Biol. 10 2000 1201 1204
A.M. Domina, J.A. Vrana, M.A. Gregory, S.R. Hann, and R.W. Craig 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 2004 5301 5315
J. Downward PI 3-kinase, Akt and cell survival Semin. Cell Dev. Biol. 15 2004 177 182
N.M. Droin, M.J. Pinkoski, E. Dejardin, and D.R. Green Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses Mol. Cell. Biol. 23 2003 7638 7647
A.L. Edinger, and C.B. Thompson Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake Mol. Biol. Cell 13 2002 2276 2288
H. Eldar-Finkelman, and E.G. Krebs Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action Proc. Natl. Acad. Sci. USA 94 1997 9660 9664
N. Embi, D.B. Rylatt, and P. Cohen Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase Eur. J. Biochem. 107 1980 519 527
C.J. Fiol, A.M. Mahrenholz, Y. Wang, R.W. Roeske, and P.J. Roach Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3 J. Biol. Chem. 262 1987 14042 14048
C.J. Fox, P.S. Hammerman, R.M. Cinalli, S.R. Master, L.A. Chodosh, and C.B. Thompson The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor Genes Dev. 17 2003 1841 1854
S. Frame, P. Cohen, and R.M. Biondi A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation Mol. Cell 7 2001 1321 1327
J.C. Goldstein, C. Munoz-Pinedo, J.E. Ricci, S.R. Adams, A. Kelekar, M. Schuler, R.Y. Tsien, and D.R. Green Cytochrome c is released in a single step during apoptosis Cell Death Differ. 12 2005 453 462
K. Gottlob, N. Majewski, S. Kennedy, E. Kandel, R.B. Robey, and N. Hay Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase Genes Dev. 15 2001 1406 1418
D.R. Green Apoptotic pathways: ten minutes to dead Cell 121 2005 671 674
J. Han, L.A. Goldstein, B.R. Gastman, C.J. Froelich, X.M. Yin, and H. Rabinowich Degradation of Mcl-1 by granzyme B: implications for Bim-mediated mitochondrial apoptotic events J. Biol. Chem. 279 2004 22020 22029
M. Herrant, A. Jacquel, S. Marchetti, N. Belhacene, P. Colosetti, F. Luciano, and P. Auberger Cleavage of Mcl-1 by caspases impaired its ability to counteract Bim-induced apoptosis Oncogene 23 2004 7863 7873
M. Hetman, J.E. Cavanaugh, D. Kimelman, and Z. Xia Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal J. Neurosci. 20 2000 2567 2574
K.P. Hoeflich, J. Luo, E.A. Rubie, M.S. Tsao, O. Jin, and J.R. Woodgett Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation Nature 406 2000 86 90
H.M. Huang, C.J. Huang, and J.J. Yen Mcl-1 is a common target of stem cell factor and interleukin-5 for apoptosis prevention activity via MEK/MAPK and PI-3K/Akt pathways Blood 96 2000 1764 1771
M. Jourdan, J.L. Veyrune, J.D. Vos, N. Redal, G. Couderc, and B. Klein A major role for Mcl-1 antiapoptotic protein in the IL-6-induced survival of human myeloma cells Oncogene 22 2003 2950 2959
S.G. Kennedy, E.S. Kandel, T.K. Cross, and N. Hay Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria Mol. Cell. Biol. 19 1999 5800 5810
R.M. Kluck, L.M. Ellerby, H.M. Ellerby, S. Naiem, M.P. Yaffe, E. Margoliash, D. Bredesen, A.G. Mauk, F. Sherman, and D.D. Newmeyer Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation J. Biol. Chem. 275 2000 16127 16133
T. Kuwana, L. Bouchier-Hayes, J.E. Chipuk, C. Bonzon, B.A. Sullivan, D.R. Green, and D.D. Newmeyer BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly Mol. Cell 17 2005 525 535
S. Le Gouill, K. Podar, M. Amiot, T. Hideshima, D. Chauhan, K. Ishitsuka, S. Kumar, N. Raje, P.G. Richardson, J.L. Harousseau, and K.C. Anderson VEGF induces Mcl-1 up-regulation and protects multiple myeloma cells against apoptosis Blood 104 2004 2886 2892
A. Letai, M.C. Bassik, L.D. Walensky, M.D. Sorcinelli, S. Weiler, and S.J. Korsmeyer Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics Cancer Cell 2 2002 183 192
R. Ley, K. Balmanno, K. Hadfield, C. Weston, and S.J. Cook Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim J. Biol. Chem. 278 2003 18811 18816
H. Liu, H.W. Peng, Y.S. Cheng, H.S. Yuan, and H.F. Yang-Yen Stabilization and enhancement of the antiapoptotic activity of mcl-1 by TCTP Mol. Cell. Biol. 25 2005 3117 3126
F. Luciano, A. Jacquel, P. Colosetti, M. Herrant, S. Cagnol, G. Pages, and P. Auberger Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function Oncogene 22 2003 6785 6793
M. Mori, D.L. Burgess, L.A. Gefrides, P.J. Foreman, J.T. Opferman, S.J. Korsmeyer, E.A. Cavalheiro, M.G. Naffah-Mazzacoratti, and J.L. Noebels Expression of apoptosis inhibitor protein Mcl1 linked to neuroprotection in CNS neurons Cell Death Differ. 11 2004 1223 1233
D. Nijhawan, M. Fang, E. Traer, Q. Zhong, W. Gao, F. Du, and X. Wang Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation Genes Dev. 17 2003 1475 1486
J.T. Opferman, A. Letai, C. Beard, M.D. Sorcinelli, C.C. Ong, and S.J. Korsmeyer Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1 Nature 426 2003 671 676
J.T. Opferman, H. Iwasaki, C.C. Ong, H. Suh, S. Mizuno, K. Akashi, and S.J. Korsmeyer Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells Science 307 2005 1101 1104
M. Pap, and G.M. Cooper Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway J. Biol. Chem. 273 1998 19929 19932
A. Petlickovski, L. Laurenti, X. Li, S. Marietti, P. Chiusolo, S. Sica, G. Leone, and D.G. Efremov Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells Blood 105 2005 4820 4827
D.R. Plas, S. Talapatra, A.L. Edinger, J.C. Rathmell, and C.B. Thompson Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology J. Biol. Chem. 276 2001 12041 12048
J.C. Rathmell, M.G. Vander Heiden, M.H. Harris, K.A. Frauwirth, and C.B. Thompson In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability Mol. Cell 6 2000 683 692
D.B. Ring, K.W. Johnson, E.J. Henriksen, J.M. Nuss, D. Goff, T.R. Kinnick, S.T. Ma, J.W. Reeder, I. Samuels, and T. Slabiak Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo Diabetes 52 2003 588 595
J.A. Romashkova, and S.S. Makarov NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling Nature 401 1999 86 90
R. Sears, G. Leone, J. DeGregori, and J.R. Nevins Ras enhances Myc protein stability Mol. Cell 3 1999 169 179
R. Sears, F. Nuckolls, E. Haura, Y. Taya, K. Tamai, and J.R. Nevins Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability Genes Dev. 14 2000 2501 2514
A. Shimamura, B.A. Ballif, S.A. Richards, and J. Blenis Rsk1 mediates a MEK-MAP kinase cell survival signal Curr. Biol. 10 2000 127 135
T.C. Somervaille, D.C. Linch, and A. Khwaja Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax Blood 98 2001 1374 1381
J. Song, S. Salek-Ardakani, P.R. Rogers, M. Cheng, L. Van Parijs, and M. Croft The costimulation-regulated duration of PKB activation controls T cell longevity Nat. Immunol. 5 2004 150 158
Z. Songyang, D. Baltimore, L.C. Cantley, D.R. Kaplan, and T.F. Franke Interleukin 3-dependent survival by the Akt protein kinase Proc. Natl. Acad. Sci. USA 94 1997 11345 11350
E.D. Tang, G. Nunez, F.G. Barr, and K.L. Guan Negative regulation of the forkhead transcription factor FKHR by Akt J. Biol. Chem. 274 1999 16741 16746
P. Viatour, E. Dejardin, M. Warnier, F. Lair, E. Claudio, F. Bureau, J.C. Marine, M.P. Merville, U. Maurer, and D. Green GSK3-mediated BCL-3 phosphorylation modulates its degradation and its oncogenicity Mol. Cell 16 2004 35 45
A. von Gise, P. Lorenz, C. Wellbrock, B. Hemmings, F. Berberich-Siebelt, U.R. Rapp, and J. Troppmair Apoptosis suppression by Raf-1 and MEK1 requires MEK- and phosphatidylinositol 3-kinase-dependent signals Mol. Cell. Biol. 21 2001 2324 2336
A.S. Wagman, K.W. Johnson, and D.E. Bussiere Discovery and development of GSK3 inhibitors for the treatment of type 2 diabetes Curr. Pharm. Des. 10 2004 1105 1137
J.M. Wang, J.R. Chao, W. Chen, M.L. Kuo, J.J. Yen, and H.F. Yang-Yen The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signaling pathway through a transcription factor complex containing CREB Mol. Cell. Biol. 19 1999 6195 6206
N.J. Waterhouse, J.C. Goldstein, R.M. Kluck, D.D. Newmeyer, and D.R. Green The (Holey) study of mitochondria in apoptosis Methods Cell Biol. 66 2001 365 391
M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 2001 727 730
M. Welcker, J. Singer, K.R. Loeb, J. Grim, A. Bloecher, M. Gurien-West, B.E. Clurman, and J.M. Roberts Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation Mol. Cell 12 2003 381 392
S.N. Willis, L. Chen, G. Dewson, A. Wei, E. Naik, J.I. Fletcher, J.M. Adams, and D.C. Huang Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins Genes Dev. 19 2005 1294 1305
C. Yost, M. Torres, J.R. Miller, E. Huang, D. Kimelman, and R.T. Moon The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3 Genes Dev. 10 1996 1443 1454
J.Y. Yu, J. Taylor, S.L. DeRuiter, A.B. Vojtek, and D.L. Turner Simultaneous inhibition of GSK3alpha and GSK3beta using hairpin siRNA expression vectors Mol. Ther. 7 2003 228 236
Q. Zhong, W. Gao, F. Du, and X. Wang Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis Cell 121 2005 1085 1095