Ubiquitin-independent degradation of antiapoptotic MCL-1

Molecular and Cellular Biology

Volumn 30, Issue 12, 2010, Pages 3099-3110

  Stewart, Daniel P ^a   Koss, Brian ^a   Bathina, Madhavi ^a   Perciavalle, Rhonda M ^a,b   Bisanz, Kristen ^a,c   Opferman, Joseph T ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; PROTEASOME; PROTEIN MCL 1; UBIQUITIN; UBIQUITIN ACTIVATING ENZYME E1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRESS; WILD TYPE;

ALLELES; ANIMALS; APOPTOSIS; CELL LINE; CYCLOHEXIMIDE; EMBRYO, MAMMALIAN; FIBROBLASTS; HALF-LIFE; HEMATOPOIETIC SYSTEM; HUMANS; LEUPEPTINS; MICE; MUTANT PROTEINS; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-BCL-2; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

MURINAE;

EID: 77953378973     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01266-09     Document Type: Article

References (72)

1. Adhikary, S., F. Marinoni, A. Hock, E. Hulleman, N. Popov, R. Beier, S. Bernard, M. Quarto, M. Capra, S. Goettig, U. Kogel, M. Scheffner, K. Helin, and M. Eilers. 2005. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123:409-421.
2. Akgul, C., D. A. Moulding, M. R. White, and S. W. Edwards. 2000. In vivo localisation and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins. FEBS Lett. 478:72-76.
3. Al-Hakim, A. K., A. Zagorska, L. Chapman, M. Deak, M. Peggie, and D. R. Alessi. 2008. Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem. J. 411:249-260.
4. Arbour, N., J. L. Vanderluit, J. N. Le Grand, A. Jahani-Asl, V. A. Ruzhynsky, E. C. Cheung, M. A. Kelly, A. E. MacKenzie, D. S. Park, J. T. Opferman, and R. S. Slack. 2008. Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J. Neurosci. 28:6068-6078.
5. Asher, G., N. Reuven, and Y. Shaul. 2006. 20S proteasomes and protein degradation "by default". Bioessays 28:844-849.
6. Baugh, J. M., E. G. Viktorova, and E. V. Pilipenko. 2009. Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J. Mol. Biol. 386:814-827.
7. Bhatia, N., S. Thiyagarajan, I. Elcheva, M. Saleem, A. Dlugosz, H. Mukhtar, and V. S. Spiegelman. 2006. Gli2 is targeted for ubiquitination and degradation by beta-TrCP ubiquitin ligase. J. Biol. Chem. 281:19320-19326.
8. Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309:127-130.
9. Chen, D., N. Kon, M. Li, W. Zhang, J. Qin, and W. Gu. 2005. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 121:1071-1083.
10. Chen, X., L. F. Barton, Y. Chi, B. E. Clurman, and J. M. Roberts. 2007. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol. Cell 26:843-852.
11. Chiu, Y. H., Q. Sun, and Z. J. Chen. 2007. E1-L2 activates both ubiquitin and FAT10. Mol. Cell 27:1014-1023.
12. Chowdary, D. R., J. J. Dermody, K. K. Jha, and H. L. Ozer. 1994. Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol. Cell. Biol. 14:1997-2003.
13. Ciechanover, A., and R. Ben-Saadon. 2004. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 14:103-106.
14. Clohessy, J. G., J. Zhuang, and H. J. Brady. 2004. Characterisation of Mcl-1 cleavage during apoptosis of haematopoietic cells. Br. J. Haematol. 125:655-665.
15. Czabotar, P. E., E. F. Lee, M. F. van Delft, C. L. Day, B. J. Smith, D. C. Huang, W. D. Fairlie, M. G. Hinds, and P. M. Colman. 2007. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc. Natl. Acad. Sci. U. S. A. 104:6217-6222.
16. Danial, N. N., and S. J. Korsmeyer. 2004. Cell death: critical control points. Cell 116:205-219.
17. Day, C. L., L. Chen, S. J. Richardson, P. J. Harrison, D. C. Huang, and M. G. Hinds. 2005. Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands. J. Biol. Chem. 280:4738-4744.
18. De Biasio, A., J. A. Vrana, P. Zhou, L. Qian, C. K. Bieszczad, K. E. Braley, A. M. Domina, S. J. Weintraub, J. M. Neveu, W. S. Lane, and R. W. Craig. 2007. N-terminal truncation of antiapoptotic MCL1, but not G2/M-induced phosphorylation, is associated with stabilization and abundant expression in tumor cells. J. Biol. Chem. 282:23919-23936.
19. Dehan, E., F. Bassermann, D. Guardavaccaro, G. Vasiliver-Shamis, M. Cohen, K. N. Lowes, M. Dustin, D. C. Huang, J. Taunton, and M. Pagano. 2009. βTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol. Cell 33:109-116.
20. Derouet, M., L. Thomas, A. Cross, R. J. Moots, and S. W. Edwards. 2004. Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J. Biol. Chem. 279:26915-26921.
21. Ding, Q., X. He, J. M. Hsu, W. Xia, C. T. Chen, L. Y. Li, D. F. Lee, J. C. Liu, Q. Zhong, X. Wang, and M. C. Hung. 2007. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol. Cell. Biol. 27:4006-4017.
22. Domina, A. M., J. H. Smith, and R. W. Craig. 2000. Myeloid cell leukemia 1 is phosphorylated through two distinct pathways, one associated with extracellular signal-regulated kinase activation and the other with G2/M accumulation or protein phosphatase 1/2A inhibition. J. Biol. Chem. 275: 21688-21694.
23. Domina, A. M., J. A. Vrana, M. A. Gregory, S. R. Hann, and R. W. Craig. 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.
24. Dupont, S., A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M. J. Stinchfield, S. Soligo, L. Morsut, M. Inui, S. Moro, N. Modena, F. Argenton, S. J. Newfeld, and S. Piccolo. 2009. FAM/ USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136:123-135.
25. Dzhagalov, I., A. St. John, and Y. W. He. 2007. The antiapoptotic protein Mcl-1 is essential for the survival of neutrophils but not macrophages. Blood 109:1620-1626.
26. Hall, J. R., E. Kow, K. R. Nevis, C. K. Lu, K. S. Luce, Q. Zhong, and J. G. Cook. 2007. Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol. Biol. Cell 18:3340-3350.
27. Han, J., L. A. Goldstein, B. R. Gastman, C. J. Froelich, X. M. Yin, and H. Rabinowich. 2004. Degradation of Mcl-1 by granzyme B: implications for Bim-mediated mitochondrial apoptotic events. J. Biol. Chem. 279:22020-22029.
28. Hart, M., J. P. Concordet, I. Lassot, I. Albert, R. del los Santos, H. Durand, C. Perret, B. Rubinfeld, F. Margottin, R. Benarous, and P. Polakis. 1999. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr. Biol. 9:207-210.
29. Herrant, M., A. Jacquel, S. Marchetti, N. Belhacene, P. Colosetti, F. Luciano, and P. Auberger. 2004. Cleavage of Mcl-1 by caspases impaired its ability to counteract Bim-induced apoptosis. Oncogene 23:7863-7873.
30. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
31. Jariel-Encontre, I., G. Bossis, and M. Piechaczyk. 2008. Ubiquitin-independent degradation of proteins by the proteasome. Biochim. Biophys. Acta 1786:153-177.
32. Jin, J., X. Li, S. P. Gygi, and J. W. Harper. 2007. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447:1135-1138.
33. Kojima, S., A. Hyakutake, N. Koshikawa, A. Nakagawara, and K. Takenaga. 2010. MCL-1V, a novel mouse antiapoptotic MCL-1 variant, generated by RNA splicing at a non-canonical splicing pair. Biochem. Biophys. Res. Commun. 391:492-497.
34. Kozopas, K. M., T. Yang, H. L. Buchan, P. Zhou, and R. W. Craig. 1993. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. U. S. A. 90:3516-3520.
35. Kriwacki, R. W., L. Hengst, L. Tennant, S. I. Reed, and P. E. Wright. 1996. Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc. Natl. Acad. Sci. U. S. A. 93:11504-11509.
36. Li, X., L. Amazit, W. Long, D. M. Lonard, J. J. Monaco, and B. W. O'Malley. 2007. Ubiquitin- and ATP-independent proteolytic turnover of p21 by the REGgamma-proteasome pathway. Mol. Cell 26:831-842.
37. Liu, C. W., M. J. Corboy, G. N. DeMartino, and P. J. Thomas. 2003. Endoproteolytic activity of the proteasome. Science 299:408-411.
38. Liu, C. W., X. Li, D. Thompson, K. Wooding, T. L. Chang, Z. Tang, H. Yu, P. J. Thomas, and G. N. DeMartino. 2006. ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol. Cell 24:39-50.
39. Liu, H., H. W. Peng, Y. S. Cheng, H. S. Yuan, and H. F. Yang-Yen. 2005. Stabilization and enhancement of the antiapoptotic activity of Mcl-1 by TCTP. Mol. Cell. Biol. 25:3117-3126.
40. Liu, Z., R. Oughtred, and S. S. Wing. 2005. Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol. Cell. Biol. 25:2819-2831.
41. Maurer, U., C. Charvet, A. S. Wagman, E. Dejardin, and D. R. Green. 2006. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 21:749-760.
42. Mei, Y., W. Du, Y. Yang, and M. Wu. 2005. Puma(*)Mcl-1 interaction is not sufficient to prevent rapid degradation of Mcl-1. Oncogene 24:7224-7237.
43. Morel, C., S. M. Carlson, F. M. White, and R. J. Davis. 2009. Mcl-1 integrates the opposing actions of signaling pathways that mediate survival and apoptosis. Mol. Cell. Biol. 29:3845-3852.
44. Mouchantaf, R., B. A. Azakir, P. S. McPherson, S. M. Millard, S. A. Wood, and A. Angers. 2006. The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X. J. Biol. Chem. 281:38738-38747.
45. Murakami, Y., S. Matsufuji, T. Kameji, S. Hayashi, K. Igarashi, T. Tamura, K. Tanaka, and A. Ichihara. 1992. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360:597-599.
46. Nagai, H., T. Noguchi, K. Homma, K. Katagiri, K. Takeda, A. Matsuzawa, and H. Ichijo. 2009. Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol. Cell 36:805-818.
47. Nathan, J. A., S. Sengupta, S. A. Wood, A. Admon, G. Markson, C. Sanderson, and P. J. Lehner. 2008. The ubiquitin E3 ligase MARCH7 is differentially regulated by the deubiquitylating enzymes USP7 and USP9X. Traffic 9:1130-1145.
48. Nijhawan, D., M. Fang, E. Traer, Q. Zhong, W. Gao, F. Du, and X. Wang. 2003. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 17:1475-1486.
49. Nishimoto, T., T. Takahashi, and C. Basilico. 1980. A temperature-sensitive mutation affecting S-phase progression can lead to accumulation of cells with a G2 DNA content. Somatic Cell Genet. 6:465-476. (Pubitemid 10072995)
50. Opferman, J. T., H. Iwasaki, C. C. Ong, H. Suh, S. Mizuno, K. Akashi, and S. J. Korsmeyer. 2005. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307:1101-1104.
51. Opferman, J. T., A. Letai, C. Beard, M. D. Sorcinelli, C. C. Ong, and S. J. Korsmeyer. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426:671-676.
52. Pelzer, C., I. Kassner, K. Matentzoglu, R. K. Singh, H. P. Wollscheid, M. Scheffner, G. Schmidtke, and M. Groettrup. 2007. UBE1L2, a novel E1 enzyme specific for ubiquitin. J. Biol. Chem. 282:23010-23014.
53. Reischl, S., K. Vanselow, P. O. Westermark, N. Thierfelder, B. Maier, H. Herzel, and A. Kramer. 2007. Beta-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J. Biol. Rhythms 22:375-386.
54. Rinkenberger, J. L., S. Horning, B. Klocke, K. Roth, and S. J. Korsmeyer. 2000. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14:23-27.
55. Rosenberg-Hasson, Y., Z. Bercovich, A. Ciechanover, and C. Kahana. 1989. Degradation of ornithine decarboxylase in mammalian cells is ATP dependent but ubiquitin independent. Eur. J. Biochem. 185:469-474.
56. Schrader, E. K., K. G. Harstad, and A. Matouschek. 2009. Targeting proteins for degradation. Nat. Chem. Biol. 5:815-822.
57. Schwickart, M., X. Huang, J. R. Lill, J. Liu, R. Ferrando, D. M. French, H. Maecker, K. O'Rourke, F. Bazan, J. Eastham-Anderson, P. Yue, D. Dornan, D. C. Huang, and V. M. Dixit. 2010. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463:103-107.
58. Steimer, D. A., K. Boyd, O. Takeuchi, J. K. Fisher, G. P. Zambetti, and J. T. Opferman. 2009. Selective roles for antiapoptotic MCL-1 during granulocyte development and macrophage effector function. Blood 113:2805-2815.
59. Tait, S. W., E. de Vries, C. Maas, A. M. Keller, C. S. D'Santos, and J. Borst. 2007. Apoptosis induction by Bid requires unconventional ubiquitination and degradation of its N-terminal fragment. J. Cell Biol. 179:1453-1466.
60. +-free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26 S proteasomes without ubiquitination. J. Biol. Chem. 275:20295-20301.
61. Touitou, R., J. Richardson, S. Bose, M. Nakanishi, J. Rivett, and M. J. Allday. 2001. A degradation signal located in the C-terminus of p21WAF1/ CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. EMBO J. 20:2367-2375.
62. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
63. Tsvetkov, P., N. Reuven, C. Prives, and Y. Shaul. 2009. Susceptibility of p53 unstructured N terminus to 20 S proteasomal degradation programs the stress response. J. Biol. Chem. 284:26234-26242.
64. Wang, X., R. A. Herr, W. J. Chua, L. Lybarger, E. J. Wiertz, and T. H. Hansen. 2007. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J. Cell Biol. 177:613-624.
65. Warr, M. R., S. Acoca, Z. Liu, M. Germain, M. Watson, M. Blanchette, S. S. Wing, and G. C. Shore. 2005. BH3-ligand regulates access of MCL-1 to its E3 ligase. FEBS Lett. 579:5603-5608.
66. Warr, M. R., and G. C. Shore. 2008. Unique biology of Mcl-1: therapeutic opportunities in cancer. Curr. Mol. Med. 8:138-147.
67. Willis, S. N., L. Chen, G. Dewson, A. Wei, E. Naik, J. I. Fletcher, J. M. Adams, and D. C. Huang. 2005. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19:1294-1305.
68. Winston, J. T., P. Strack, P. Beer-Romero, C. Y. Chu, S. J. Elledge, and J. W. Harper. 1999. The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and betacatenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev. 13:270-283.
69. Yang, T., K. M. Kozopas, and R. W. Craig. 1995. The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J. Cell Biol. 128:1173-1184.
70. Yaron, A., A. Hatzubai, M. Davis, I. Lavon, S. Amit, A. M. Manning, J. S. Andersen, M. Mann, F. Mercurio, and Y. Ben-Neriah. 1998. Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature 396: 590-594.
71. Zhao, Y., B. J. Altman, J. L. Coloff, C. E. Herman, S. R. Jacobs, H. L. Wieman, J. A. Wofford, L. N. Dimascio, O. Ilkayeva, A. Kelekar, T. Reya, and J. C. Rathmell. 2007. Glycogen synthase kinase 3α and 3β mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1. Mol. Cell. Biol. 27:4328-4339.
72. Zhong, Q., W. Gao, F. Du, and X. Wang. 2005. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121:1085-1095.