Ubiquitin-Independent Degradation of Antiapoptotic MCL-1

REFERENCES

• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Asher, G., N. Reuven, and Y. Shaul. 2006. 20S proteasomes and protein degradation “by default”. Bioessays 28:844–849.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309:127–130.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Chiu, Y. H., Q. Sun, and Z. J. Chen. 2007. E1-L2 activates both ubiquitin and FAT10. Mol. Cell 27:1014–1023.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ciechanover, A., and R. Ben-Saadon. 2004. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 14:103–106.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Danial, N. N., and S. J. Korsmeyer. 2004. Cell death: critical control points. Cell 116:205–219.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–479.
   PubMed Web of Science ®Google Scholar
• Jariel-Encontre, I., G. Bossis, and M. Piechaczyk. 2008. Ubiquitin-independent degradation of proteins by the proteasome. Biochim. Biophys. Acta 1786:153–177.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Liu, C. W., M. J. Corboy, G. N. DeMartino, and P. J. Thomas. 2003. Endoproteolytic activity of the proteasome. Science 299:408–411.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Schrader, E. K., K. G. Harstad, and A. Matouschek. 2009. Targeting proteins for degradation. Nat. Chem. Biol. 5:815–822.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Tarcsa, E., G. Szymanska, S. Lecker, C. M. O'Connor, and A. L. Goldberg. 2000. Ca2+-free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26 S proteasomes without ubiquitination. J. Biol. Chem. 275:20295–20301.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Warr, M. R., and G. C. Shore. 2008. Unique biology of Mcl-1: therapeutic opportunities in cancer. Curr. Mol. Med. 8:138–147.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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 beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev. 13:270–283.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar