Prevention of cytokine withdrawal-induced apoptosis by Mcl-1 requires interaction between Mcl-1 and Bim

Biochemistry and Cell Biology

Volumn 88, Issue 5, 2010, Pages 809-818

  Jamil, Sarwat ^a   Wei Wang, Shih ^a   Bondy, Lise ^a   Mojtabavi, Shadi ^a   Duronio, Vincent ^a  

^a VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Apoptosis; Phosphorylation; Protein half life; Protein protein interaction

Indexed keywords

ANTI-APOPTOTIC EFFECTS; APOPTOSIS; APOPTOTIC; BCL-2 FAMILY; BONE MARROW; CYTOKINES; GLUTAMIC ACID; GROWTH FACTOR; HEMOPOIETIC CELLS; INDUCED APOPTOSIS; MITOCHONDRIAL PATHWAYS; NORMAL GROWTH; PROTEIN-PROTEIN INTERACTION; STARVED CONDITIONS; WILD TYPES;

AMINO ACIDS; CELL DEATH; PHOSPHORYLATION;

PROTEINS;

ALANINE; BIM PROTEIN; CYTOKINE; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3; PROLINE; PROTEIN MCL 1; SERINE; THREONINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; GROWTH; HEMATOPOIETIC CELL; MACROPHAGE; MOUSE; MUTANT; MUTATION; NONHUMAN; PLAGUE; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SURVIVAL; WASTE; WILD TYPE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; BONE MARROW; CELLS, CULTURED; CYTOKINES; IMMUNOPRECIPITATION; MACROPHAGES; MEMBRANE PROTEINS; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS;

EID: 78649273276     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O10-004     Document Type: Article

References (41)

1. Adams, J.M., and Cory, S. 1998. The Bcl-2 protein family: arbiters of cell survival. Science, 281(5381): 1322-1326. doi: 10.1126/ science. 281.5381.1322. PMID:9735050.
2. Adams, J.M., and Cory, S. 2001. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 26(1): 61-66. doi:10.1016/S0968-0004(00) 01740-0. PMID: 11165519.
3. Behzad, H., Jamil, S., Denny, T.A., and Duronio, V. 2007. Cytokine-mediated FOXO3a phosphorylation suppresses FasL expression in hemopoietic cell lines: investigations of the role of Fas in apoptosis due to cytokine starvation. Cytokine, 38(2): 74-83. doi:10.1016/j.cyto.2007.05.004. PMID: 17604640.
4. Chao, J.R., Wang, J.M., Lee, S.F., Peng, H.W., Lin, Y.H., Chou, CH., et al. 1998. mci-1 is an immediate-early gene activated by the granulocyte- macrophage colony-stimulating factor (GMCSF) signaling pathway and is one component of the GM-CSF viability response. Mol. Cell. Biol. 18(8): 4883-4898. PMID: 9671497.
5. Chen, L., Willis, S.N., Wei, A., Smith, BJ., Fletcher, J.L., Hinds, M.G., et al. 2005. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell, 17(3): 393-403. doi:10.1016/j.molcel. 2004.12.030. PMID: 15694340.
6. Czabotar, P.E., Lee, E.F., van Delft, M.F., Day, C.L., Smith, B.J., Huang, D.C., et al. 2007. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc. Natl. Acad. Sci. U.S.A. 104(15): 6217-6222. doi:10.1073/pnas.0701297104. PMID: 17389404.
7. Danial, N.N., and Korsmeyer, S.J. 2004. Cell death: critical control points. Cell, 116(2): 205-219. doi:10.1016/S0092-8674(04) 00046-7. PMID: 14744432.
8. Dijkers, P.F., Medema, R.H., Lammers, J.W., Koenderman, L., and Coffer, P.J. 2000. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-Ll. Cum Biol. 10(19): 1201-1204. doi:10.1016/S09609822(00)00728-4. PMID: 11050388.
9. Dijkers, P.F., Birkenkamp, K.U., Lam, E.W., Thomas, N.S., Lammers, J.W., Koenderman, L., and Coffer, P.J. 2002. FKHR-L1 can act as a critical effector of cell death induced by cytokine withdrawal: protein kinase B-enhanced cell survival through maintenance of mitochondrial integrity. J. Cell Biol. 156(3): 531-542. doi: 10.1083/jcb.200108084. PMID: 11815629.
10. Ding, Q., He, X., Hsu, J.M., Xia, W., Chen, C.T., Li, L.Y., et al. 2007. Degradation of Mcl-1 by β-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chernosensitization. Mol. Cell. Biol. 27(11): 4006-4017. doi:10.1128/MCB. 00620-06. PMID: 17387146.
11. Domina, A.M., Vrana, J.A., Gregory, M.A., Hann, S.R., and Craig, R.W. 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(31): 5301-5315. doi:10.1038/sj.onc.l.207692. PMID: 15241487.
12. Franke, T.F., Hornik, C.P., Segev, L., Shostak, G.A., and Sugimoto, C. 2003. PI3K/A.kt and apoptosis: size matters. Oncogene, 22(56): 8983-8998. doi:10.1038/sj.onc. 1207115. PMID: 14663477.
13. Germain, M., and Duronio, V. 2007. The N terminus of the antiapoptotic BCL-2 homologue MCL-1 regulates its localization and function. J. Biol. Chem. 282(44): 32233-32242. doi:10. 1074/jbc.M706408200. PMID:17823113.
14. Horton, R.M. 1995. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3(2): 9399. doi:10.1007/BF02789105.
15. Huang, D.C.S., and Strasser, A. 2000. BH3-only proteins-essential initiators of apoptotic cell death. Cell, 103(6): 839-842. doi :10.1016/S0092-8674(00)00187-2. PMID: 11136969.
16. Hundal, R.S., Gómez-Muñoz, A., Kong, J.Y., SaIh, B.S., Marotta, A., Duronio, V., and Steinbrecher, U.P. 2003. Oxidized low density lipoprotein inhibits macrophage apoptosis by blocking ceramide generation, thereby maintaining protein kinase B activation and Bcl-XL levels. J. Biol. Chem. 278(27): 24399-24408. doi:10.1074/jbc.M209179200. PMID: 12750385.
17. Inoshita, S., Takeda, K., Hatai, T., Terada, Y., Sano, M., Hata, J., et al. 2002. Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J. Biol. Chem. 277(46): 43730-43734. doi: 10.1074/jbc.M207951200. PMID: 12223490.
18. Jamil, S., Sobouti, R., Hojabrpour, P., Raj, M., Kast, J., and Duronio, V. 2005. A proteolytic fragment of Mcl-1. exhibits nuclear localization and regulates cell growth by interaction with Cdk1. Biochem. J. 387(Pt 3): 659-667. doi:10.1042/BJ20041596. PMID: 15554878.
19. Jamil, S., Mojtabavi, S., Hojabrpour, P., Cheah, S., and Duronio, V. 2008. An essential role for MCL-1 in ATR-mediated CHK1 phosphorylation. Mol. Biol, Cell, 19(8): 3212-3220. doi: 10. 1091/mbc,E07-11-1171.
20. Korsmeyer, S.J. 1999. BCL-2 gene family and the regulation of programmed cell death, Cancer Res. 59(7Suppl): 16938-1700s. PMID: 10197582.
21. Kozopas, K.M., Yang, T., Buchan, H.L., Zhou, P., and Craig, R.W. 1993. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. U.S.A. 90(8): 3516-3520. doi:10.1073/pnas.90.8.3516. PMID:7682708.
22. Kuure, S., Popsueva, A., Jakobson, M., Sainio, K., and Sariola, H. 2007. Glycogen synthase kinase-3 inactivation and stabilization of β-catenin induce nephron differentiation in isolated mouse and rat kidney mesenchymes, J. Am, Soc. Nephrol. 18(4): 1130-1139. doi :10.1681/ASN.2006111206, PMID: 17329570.
23. Lei, K., and Davis, R.J, 2003. JNK phosphorylation of Bim-related members of the Bcl.2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. U.S.A. 100(5): 2432-2437. doi: 10.1073/ pnas.0438011100. PMID: 12591950.
24. Martens, J.S., Reiner, N.E., Herrera-Velit, P., and Steinbrecher, U.P. 1998, Phosphatidylinositol 3-kinase is involved in the induction of macrophage growth by oxidized low density lipoprotein. J, Biol. Chem. 273(9): 4915-4920. doi:10,1074/jbc.273.9. 4915. PMID:9478935.
25. Maurer, U., Charvet, C., Wagman, A.S., Dejardin, E., and Green, D.R. 2006. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permcabilization and apoptosis by destabilisation of MCL-1. Mol. Cell, 21(6): 749-760. doi:10.1016/j. molcel.2006.02.009. PMID: 16543145.
26. Mei, Y., Du, W., Yang, Y., and Wu, M. 2005. Puma*Mcl-1 interaction is not sufficient to prevent rapid degradation of Mcl-1 Oncogene, 24(48): 7224-7237. doi : 10.1038/sj.onc. 1208873. PMID: 16007132.
27. Muchmore, S.W., Sattler, M., Liang, H., Meadows, R.P., Harlan, J.E., Yoon, H.S., et al. 1996. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature, 381(6580): 335-341, doi:10.1038/381335a0, PMID:8692274.
28. Nijhawan, D., Fang, M., Traer, E., Zhong, Q., Gao, W., Du, F., and Wang, X. 2003, Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation, Genes Dev. 17(12): 1475-1486. doi: 10.1101/gad. 1093903. PMID: 12783855.
29. Novak, A., and Dedhar, S. 1999. Signaling through β-catenin and Lef/Tcf. Cell. Mol. Life Sci. 56(5-6): 523-537. doi:1.0.1007/ S000180050449. PMID:11212302.
30. Opferman, J.T., Iwasaki, H., Ong, C.C., Suh, H., Mizuno, S., Akashi, K., and Korsmeyer, S.J. 2005, Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science. 307(5712): 1101-1104. doi:10.1126/science. 1106114. PMID: 15718471.
31. Puthalakath, H., Huang, D.C., O'Reilly, L.A., King, S.M., and 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(3): 287-296, doi: 10.1016/S10972765(00)80456-6, PMID: 10198631.
32. Schubert, K.M., and Duronio, V. 2001. Distinct roles for extracellular-signal-regulated protein kinase (ERK) mitogen-activated protein kinases and phosphatidylinositol 3-kinase in the regulation of Mcl-1 synthesis. Biochem. J. 356(Pt 2): 473-480. doi: 10.1042/0264-6021:3560473. PMID: 11368774.
33. Vaux, D.L., Haecker, G., and Strasser, A. 1994. An evolutionary perspective on apoptosis, Cell, 76(5): 777-779. doi:10.1016/ 0092-8674(94)90350-6. PMID:8124715.
34. Vilimek, D., and Duronio, V. 2006. Cytokine-stimulated phosphorylation of GSK-3 is primarily dependent upon PKCs, not PKB. Biochem. Cell Biol. 84(1): 20-29. doi: 10.1139/005-154. PMID: 16462886.
35. Worr, M.R., Acoca, S., Liu, Z., Germain, M., Watson, M., Blanchette, M., et al. 2005, BH3-ligand regulates access of MCl-1 to its E3 ligase. FEBS Lett. 579(25): 5603-5608. PMID:16213503.
36. Wei, M.C., Zong, W.X., Cheng, E.H., Lindsten, T., Panoutsakopoulou, V., Ross, A.J., et al. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science, 292(5517): 727-730. doi: 10.1126/science. 1059108. PMID: 11326099.
37. Yang-Yen, H.F. 2006. Mcl-1: a highly regulated cell death and survival controller. J. Biomed. Sci. 13(2): 201-204. doi: 10.1007/ si 1373-005-9064-4. PMID: 16456709.
38. Zha, J., Harada, H., Yang, E., Jockei, J., and Korsmeyer, S.J. 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(4): 619-628. doi: 10.1016/S0092-8674(00)81382-3. PMID: 8929531.
39. Zhong, Q., Gao, W., Du, F., and Wang, X. 2005. Mule/ARF-BPl, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell, 121(7): 1085-1095. doi:10.1016/j.cell. 2005.06.009. PMID: 15989957.
40. Zhou, P., Qian, L.P., Kozopas, K.M., and Craig, R.W. 1997. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood, 89(2): 630-643. PMID:9002967.
41. Zimmermann, K.C., and Green, D.R. 2001, How cells die: apoptosis pathways. J. Allergy Clin. Immunol, 108(4 Suppl.): S99-S103. doi: 10.1067/mai.2001,117819. PMID: 11586274.