Emerging regulatory mechanisms in ubiquitindependent cell cycle control

Journal of Cell Science

Volumn 125, Issue 2, 2012, Pages 255-263

  Mocciaro, Annamaria ^a   Rape, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anaphase promoting complex; Lysine 11; SCF; Ubiquitin

Indexed keywords

AURORA B KINASE; CELL CYCLE PROTEIN 20; CULLIN; CYCLIN B1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLINE; F BOX PROTEIN; GUANOSINE TRIPHOSPHATASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE GAMMA; NEDD8 PROTEIN; POLO LIKE KINASE; PROTEIN MAD2; PROTEIN P97; RAN PROTEIN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME E2;

ANAPHASE; AUTOPHOSPHORYLATION; CARCINOGENESIS; CATALYSIS; CELL ACTIVATION; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIVISION; CELL MANIPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHROMOSOME; DEGRADATION; DNA REPLICATION; GENETIC LINKAGE; GENOME; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MOLECULAR INTERACTION; NONHUMAN; NOTE; PRIORITY JOURNAL; PROGENY; PROMETAPHASE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; UBIQUITINATION; YEAST;

CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; HUMANS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EUKARYOTA;

EID: 84858127817     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.091199     Document Type: Note

References (109)

1. Abbas, T. and Dutta, A. (2011). CRL4Cdt2: master coordinator of cell cycle progression and genome stability. Cell Cycle 10, 241-249.
2. Abbas, T., Sivaprasad, U., Terai, K., Amador, V., Pagano, M. and Dutta, A. (2008). PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev. 22, 2496-2506.
3. Abbas, T., Shibata, E., Park, J., Jha, S., Karnani, N. and Dutta, A. (2010). CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 40, 9-21.
4. Arias, E. E. and Walter, J. C. (2006). PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84-90.
5. Baboshina, O. V. and Haas, A. L. (1996). Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5. J. Biol. Chem. 271, 2823-2831.
6. Bashir, T., Dorrello, N. V., Amador, V., Guardavaccaro, D. and Pagano, M. (2004). Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428, 190-193.
7. Bennett, E. J., Shaler, T. A., Woodman, B., Ryu, K. Y., Zaitseva, T. S., Becker, C. H., Bates, G. P., Schulman, H. and Kopito, R. R. (2007). Global changes to the ubiquitin system in Huntington's disease. Nature 448, 704-708.
8. Bennett, E. J., Rush, J., Gygi, S. P. and Harper, J. W. (2010). Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 143, 951-965.
9. Carroll, C. W. and Morgan, D. O. (2002). The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nat. Cell Biol. 4, 880-887.
10. Ceccarelli, D. F., Tang, X., Pelletier, B., Orlicky, S., Xie, W., Plantevin, V., Neculai, D., Chou, Y. C., Ogunjimi, A., Al-Hakim, A. et al. (2011). An allosteric inhibitor of the human cdc34 ubiquitin-conjugating enzyme. Cell 145, 1075-1087.
11. Centore, R. C., Havens, C. G., Manning, A. L., Li, J. M., Flynn, R. L., Tse, A., Jin, J., Dyson, N. J., Walter, J. C. and Zou, L. (2010). CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 40, 22-33.
12. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K. and Varshavsky, A. (1989). A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583.
13. Cunha-Ferreira, I., Rodrigues-Martins, A., Bento, I., Riparbelli, M., Zhang, W., Laue, E., Callaini, G., Glover, D. M. and Bettencourt-Dias, M. (2009). The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr. Biol. 19, 43-49.
14. D'Angiolella, V., Donato, V., Vijayakumar, S., Saraf, A., Florens, L., Washburn, M. P., Dynlacht, B. and Pagano, M. (2010). SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 466, 138-142.
15. da Fonseca, P. C., Kong, E. H., Zhang, Z., Schreiber, A., Williams, M. A., Morris, E. P. and Barford, D. (2011). Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470, 274-278.
16. Deshaies, R. J. and Joazeiro, C. A. (2009). RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
17. Duda, D. M., Borg, L. A., Scott, D. C., Hunt, H. W., Hammel, M. and Schulman, B. A. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006.
18. Ganem, N. J., Godinho, S. A. and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282.
19. Garnett, M. J., Mansfeld, J., Godwin, C., Matsusaka, T., Wu, J., Russell, P., Pines, J. and Venkitaraman. A. R. (2009). UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nat. Cell Biol. 11, 1363-1369.
20. Gerlach, B., Cordier, S. M., Schmukle, A. C., Emmerich, C. H., Rieser, E., Haas, T. L., Webb, A. I., Rickard, J. A., Anderton, H., Wong, W. W. et al. (2011). Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596.
21. Glotzer, M., Murray, A. W. and Kirschner, M. W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138.
22. Guderian, G., Westendorf, J., Uldschmid, A. and Nigg, E. A. (2010). Plk4 transautophosphorylation regulates centriole number by controlling betaTrCP-mediated degradation. J. Cell Sci. 123, 2163-2169.
23. Havens, C. G. and Walter, J. C. (2009). Docking of a specialized PIP Box onto chromatinbound PCNA creates a degron for the ubiquitin ligase CRL4Cdt2. Mol. Cell 35, 93-104.
24. Havens, C. G. and Walter, J. C. (2011). Mechanism of CRL4Cdt2, a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 25, 1568-1582.
25. Hetfeld, B. K., Helfrich, A., Kapelari, B., Scheel, H., Hofmann, K., Guterman, A., Glickman, M., Schade, R., Kloetzel, P. M. and Dubiel, W. (2005). The zinc finger of the CSN-associated deubiquitinating enzyme USP15 is essential to rescue the E3 ligase Rbx1. Curr. Biol. 15, 1217-1221.
26. Holland, A. J., Lan, W., Niessen, S., Hoover, H. and Cleveland, D. W. (2010). Polo-like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol. 188, 191-198.
27. Hsu, J. Y., Reimann, J. D., Sorensen, C. S., Lukas, J. and Jackson, P. K. (2002). E2Fdependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1). Nat. Cell Biol. 4, 358-366.
28. Huang, X., Summers, M. K., Pham, V., Lill, J. R., Liu, J., Lee, G., Kirkpatrick, D. S., Jackson, P. K., Fang, G. and Dixit, V. M. (2011). Deubiquitinase USP37 is activated by CDK2 to antagonize APC(CDH1) and promote S phase entry. Mol. Cell 42, 511-523.
29. Ikeda, F., Deribe, Y. L., Skanland, S. S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S. J., Goswami, P., Nagy, V., Terzic, J. et al. (2011). SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 471, 637-641.
30. Inuzuka, H., Shaik, S., Onoyama, I., Gao, D., Tseng, A., Maser, R. S., Zhai, B., Wan, L., Gutierrez, A., Lau, A. W. et al. (2011). SCF(FBW7) regulates cellular apoptosis by targeting MCL1 for ubiquitylation and destruction. Nature 471, 104-109.
31. Jin, L., Williamson, A., Banerjee, S., Philipp, I. and Rape, M. (2008). Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 133, 653-665.
32. Jorgensen, S., Eskildsen, M., Fugger, K., Hansen, L., Larsen, M. S., Kousholt, A. N., Syljuasen, R. G., Trelle, M. B., Jensen, O. N., Helin, K. et al. (2011). SET8 is degraded via PCNA-coupled CRL4(CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 192, 43-54.
33. Jung, C. R., Hwang, K. S., Yoo, J., Cho, W. K., Kim, J. M., Kim, W. H. and Im, D. S. (2006). E2-EPF UCP targets pVHL for degradation and associates with tumor growth and metastasis. Nat. Med. 12, 809-816.
34. Kaiser, S. E., Riley, B. E., Shaler, T. A., Trevino, R. S., Becker, C. H., Schulman, H. and Kopito, R. R. (2011). Protein standard absolute quantification (PSAQ) method for the measurement of cellular ubiquitin pools. Nat. Methods 8, 691-696.
35. Kalab, P. and Heald, R. (2008). The RanGTP gradient-a GPS for the mitotic spindle. J. Cell Sci. 121, 1577-1586.
36. Kim, S. H. and Michael, W. M. (2008). Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell 32, 757-766.
37. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y. D. and Nigg, E. A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
38. Lee, J. E., Sweredoski, M. J., Graham, R. L., Kolawa, N. J., Smith, G. T., Hess, S. and Deshaies, R. J. (2011). The steady-state repertoire of human SCF ubiquitin ligase complexes does not require ongoing Nedd8 conjugation. Mol. Cell. Proteomics 10, M110 006460.
39. Liakopoulos, D., Doenges, G., Matuschewski, K. and Jentsch, S. (1998). A novel protein modification pathway related to the ubiquitin system. EMBO J. 17, 2208-2214.
40. Listovsky, T., Oren, Y. S., Yudkovsky, Y., Mahbubani, H. M., Weiss, A. M., Lebendiker, M. and Brandeis, M. (2004). Mammalian Cdh1/Fzr mediates its own degradation. EMBO J. 23, 1619-1626.
41. Liu, J., Furukawa, M., Matsumoto, T. and Xiong, Y. (2002). NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 10, 1511-1518.
42. Maerki, S., Olma, M. H., Staubli, T., Steigemann, P., Gerlich, D. W., Quadroni, M., Sumara, I. and Peter, M. (2009). The Cul3-KLHL21 E3 ubiquitin ligase targets aurora B to midzone microtubules in anaphase and is required for cytokinesis. J. Cell Biol. 187, 791-800.
43. Mathe, E., Kraft, C., Giet, R., Deak, P., Peters, J. M. and Glover, D. M. (2004). The E2-C vihar is required for the correct spatiotemporal proteolysis of cyclin B and itself undergoes cyclical degradation. Curr. Biol. 14, 1723-1733.
44. Matsumoto, M. L., Wickliffe, K. E., Dong, K. C., Yu, C., Bosanac, I., Bustos, D., Phu, L., Kirkpatrick, D. S., Hymowitz, S. G., Rape, M. et al. (2010). K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 39, 477-484.
45. Miniowitz-Shemtov, S., Teichner, A., Sitry-Shevah, D. and Hershko, A. (2010). ATP is required for the release of the anaphase-promoting complex/cyclosome from inhibition by the mitotic checkpoint. Proc. Natl. Acad. Sci. USA 107, 5351-5356.
46. Mukhopadhyay, D. and Riezman, H. (2007). Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205.
47. Murray, A. W., Solomon, M. J. and Kirschner, M. W. (1989). The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280-286.
48. Musacchio, A. and Salmon, E. D. (2007). The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393.
49. Neumann, B., Walter, T., Heriche, J. K., Bulkescher, J., Erfle, H., Conrad, C., Rogers, P., Poser, I., Held, M., Liebel, U. et al. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727.
50. Nilsson, J., Yekezare, M., Minshull, J. and Pines, J. (2008). The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 10, 1411-1420.
51. Oda, H., Hubner, M. R., Beck, D. B., Vermeulen, M., Hurwitz, J., Spector, D. L. and Reinberg, D. (2010). Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 40, 364-376.
52. Orlicky, S., Tang, X., Neduva, V., Elowe, N., Brown, E. D., Sicheri, F. and Tyers, M. (2010). An allosteric inhibitor of substrate recognition by the SCF(Cdc4) ubiquitin ligase. Nat. Biotechnol. 28, 733-737.
53. Palframan, W. J., Meehl, J. B., Jaspersen, S. L., Winey, M. and Murray, A. W. (2006). Anaphase inactivation of the spindle checkpoint. Science 313, 680-684.
54. Passmore, L. A., McCormack, E. A., Au, S. W., Paul, A., Willison, K. R., Harper, J. W. and Barford, D. (2003). Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 22, 786-796.
55. Petroski, M. D. and Deshaies, R. J. (2005a). Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20.
56. Petroski, M. D. and Deshaies, R. J. (2005b). Mechanism of lysine 48-linked ubiquitinchain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 123, 1107-1120.
57. Pfleger, C. M. and Kirschner, M. W. (2000). The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14, 655-665.
58. Puklowski, A., Homsi, Y., Keller, D., May, M., Chauhan, S., Kossatz, U., Grunwald, V., Kubicka, S., Pich, A., Manns, M. P. et al. (2011). The SCF-FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat. Cell Biol. 13, 1004-1009.
59. Qi, W. and Yu, H. (2007). KEN-box-dependent degradation of the Bub1 spindle checkpoint kinase by the anaphase-promoting complex/cyclosome. J. Biol. Chem. 282, 3672-3679.
60. Rahighi, S., Ikeda, F., Kawasaki, M., Akutsu, M., Suzuki, N., Kato, R., Kensche, T., Uejima, T., Bloor, S., Komander, D. et al. (2009). Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 136, 1098-1109.
61. Ramadan, K., Bruderer, R., Spiga, F. M., Popp, O., Baur, T., Gotta, M. and Meyer, H. H. (2007). Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450, 1258-1262.
62. Rape, M. and Kirschner, M. W. (2004). Autonomous regulation of the anaphasepromoting complex couples mitosis to S-phase entry. Nature 432, 588-595.
63. Reddy, S. K., Rape, M., Margansky, W. A. and Kirschner, M. W. (2007). Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446, 921-925.
64. Rodrigo-Brenni, M. C. and Morgan, D. O. (2007). Sequential E2s drive polyubiquitin chain assembly on APC targets. Cell 130, 127-139.
65. Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. and Rogers, S. L. (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184, 225-239.
66. Rotin, D. and Kumar, S. (2009). Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398-409.
67. Saha, A. and Deshaies, R. J. (2008). Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell 32, 21-31.
68. Schreiber, A., Stengel, F., Zhang, Z., Enchev, R. I., Kong, E. H., Morris, E. P., Robinson, C. V., da Fonseca, P. C. and Barford, D. (2011). Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 470, 227-232.
69. Schulman, B. A. and Harper, J. W. (2009). Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 10, 319-331.
70. Schwickart, M., Huang, X., Lill, J. R., Liu, J., Ferrando, R., French, D. M., Maecker, H., O'Rourke, K., Bazan, F., Eastham-Anderson, J. et al. (2010). Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463, 103-107.
71. Scott, D. C., Monda, J. K., Grace, C. R., Duda, D. M., Kriwacki, R. W., Kurz, T. and Schulman, B. A. (2010). A dual E3 mechanism for Rub1 ligation to Cdc53. Mol. Cell 39, 784-796.
72. Senga, T., Sivaprasad, U., Zhu, W., Park, J. H., Arias, E. E., Walter, J. C. and Dutta, A. (2006). PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated Nterminal ubiquitination. J. Biol. Chem. 281, 6246-6252.
73. Shibutani, S. T., de la Cruz, A. F. A., Tran, V., Turbyfill, W. J., 3rd, Reis, T., Edgar, B. A. and Duronio, R. J. (2008). Intrinsic negative cell cycle regulation provided by PIP box- and Cul4Cdt2-mediated destruction of E2f1 during S phase. Dev. Cell 15, 890-900.
74. Sloper-Mould, K. E., Jemc, J. C., Pickart, C. M. and Hicke, L. (2001). Distinct functional surface regions on ubiquitin. J. Biol. Chem. 276, 30483-30489.
75. Song, E. J., Werner, S, L., Neubauer, J., Stegmeier, F., Aspden, J., Rio, D., Harper, J, W., Elledge, S. J., Kirschner, M. W. and Rape, M. (2010). The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24, 1434-1447.
76. Song, L. and Rape, M. (2010). Regulated degradation of spindle assembly factors by the anaphase-promoting complex. Mol. Cell 38, 369-382.
77. Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S. et al. (2009). An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736.
78. Sowa, M. E., Bennett, E. J., Gygi, S. P. and Harper, J. W. (2009). Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403.
79. Stegmeier, F., Rape, M., Draviam, V. M., Nalepa, G., Sowa, M. E., Ang, X. L., McDonald, E. R., 3rd, Li, M. Z., Hannon, G. J., Sorger, P. K. et al. (2007). Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446, 876-881.
80. Stewart, S. and Fang, G. (2005a). Anaphase-promoting complex/cyclosome controls the stability of TPX2 during mitotic exit. Mol. Cell. Biol. 25, 10516-10527.
81. Stewart, S. and Fang, G. (2005b). Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res. 65, 8730-8735.
82. Strnad, P., Leidel, S., Vinogradova, T., Euteneuer, U., Khodjakov, A. and Gonczy, P. (2007). Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell 13, 203-213.
83. Sullivan, M. and Morgan. D. O. (2007). Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell. Biol. 8, 894-903.
84. Sumara, I., Quadroni, M., Frei, C., Olma, M. H., Sumara, G., Ricci, R. and Peter, M. (2007). A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev. Cell 12, 887-900.
85. Summers, M. K., Pan, B., Mukhyala, K. and Jackson, P. K. (2008). The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC. Mol. Cell 31, 544-556.
86. Tardat, M., Brustel, J., Kirsh, O., Lefevbre, C., Callanan, M., Sardet, C. and Julien, E. (2010). The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 12, 1086-1093.
87. Tedesco, D., Zhang, J., Trinh, L., Lalehzadeh, G., Meisner, R., Yamaguchi, K. D., Ruderman, D. L., Dinter, H. and Zajchowski, D. A. (2007). The ubiquitin-conjugating enzyme E2-EPF is overexpressed in primary breast cancer and modulates sensitivity to topoisomerase II inhibition. Neoplasia 9, 601-613.
88. Teichner, A., Eytan, E., Sitry-Shevah, D., Miniowitz-Shemtov, S., Dumin, E., Gromis, J. and Hershko, A. (2011). p31comet promotes disassembly of the mitotic checkpoint complex in an ATP-dependent process. Proc. Natl. Acad. Sci. USA 108, 3187-3192.
89. Thrower, J. S., Hoffman, L., Rechsteiner, M. and Pickart, C. M. (2000). Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94-102.
90. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S. et al. (2009). Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 11, 123-132.
91. Tokunaga, F., Nakagawa, T., Nakahara, M., Saeki, Y., Taniguchi, M., Sakata, S., Tanaka, K., Nakano, H. and Iwai, K. (2011). SHARPIN is a component of the NFkB activating linear ubiquitin chain assembly complex. Nature 471, 633-636.
92. van Ree, J. H., Jeganathan, K. B., Malureanu, L. and van Deursen, J. M. (2010). Overexpression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J. Cell Biol. 188, 83-100.
93. Wagner, K. W., Sapinoso, L. M., El-Rifai, W., Frierson, H. F., Butz, N., Mestan, J., Hofmann, F., Deveraux, Q. L. and Hampton, G. M. (2004). Overexpression, genomic amplification and therapeutic potential of inhibiting the UbcH10 ubiquitin conjugase in human carcinomas of diverse anatomic origin. Oncogene 23, 6621-6629.
94. Wei, W., Ayad, N. G., Wan, Y., Zhang, G. J., Kirschner, M. W. and Kaelin, W. G., Jr (2004). Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphasepromoting complex. Nature 428, 194-198.
95. Wertz, I. E., Kusam, S., Lam, C., Okamoto, T., Sandoval, W., Anderson, D. J., Helgason, E., Ernst, J. A., Eby, M., Liu, J. et al. (2011). Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471, 110-114.
96. Whitfield, M. L., Sherlock, G., Saldanha, A. J., Murray, J. I., Ball, C. A., Alexander, K. E., Matese, J. C., Perou, C. M., Hurt, M. M., Brown, P. O. et al. (2002). Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 13, 1977-2000.
97. Wickliffe, K. E., Lorenz, S., Wemmer, D. E., Kuriyan, J. and Rape, M. (2011). The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit e2. Cell 144, 769-781.
98. Williamson, A., Wickliffe, K. E., Mellone, B. G., Song, L., Karpen, G. H. and Rape, M. (2009). Identification of a physiological E2 module for the human anaphasepromoting complex. Proc. Natl. Acad. Sci. USA 106, 18213-18218
99. Williamson, A., Banerjee, S., Zhu, X., Philipp, I., Iavarone, A. T. and Rape, M. (2011). Regulation of ubiquitin chain initiation to control the timing of substrate degradation. Mol. Cell 42, 744-757.
100. Wu, T., Merbl, Y., Huo, Y., Gallop, J. L., Tzur, A. and Kirschner, M. W. (2010). UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 107, 1355-1360.
101. Wu, W. K., Cho, C. H., Lee, C. W., Wu, K., Fan, D., Yu, J. and Sung, J. J. (2010). Proteasome inhibition: a new therapeutic strategy to cancer treatment. Cancer Lett. 293, 15-22.
102. Xia, G., Luo, X., Habu, T., Rizo, J., Matsumoto, T. and Yu, H. (2004). Conformationspecific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J. 23, 3133-3143.
103. Xu, P., Duong, D. M., Seyfried, N. T., Cheng, D., Xie, Y., Robert, J., Rush, J., Hochstrasser, M., Finley, D. and Peng, J. (2009). Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137, 133-145.
104. Ye, Y. and Rape, M. (2009). Building ubiquitin chains: E2 enzymes at work. Nat. Rev Mol. Cell. Biol. 10, 755-764.
105. Young, L. M. and Pagano, M. (2010). Cdc25 phosphatases: differential regulation by ubiquitin-mediated proteolysis. Cell Cycle 9, 4613-4614.
106. Zeng, X., Sigoillot, F., Gaur, S., Choi, S., Pfaff, K. L., Oh, D. C., Hathaway, N., Dimova, N., Cuny, G. D. and King, R. W. (2010). Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 18, 382-395.
107. Zhang, Y., van Deursen, J. and Galardy, P. J. (2011). Overexpression of Ubiquitin Specific Protease 44 (USP44) induces chromosomal instability and is frequently observed in human T-cell leukemia. PLoS ONE 6, e23389.
108. Zhong, W., Feng, H., Santiago, F. E. and Kipreos, E. T. (2003). CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 423, 885-889.
109. Ziv, I., Matiuhin, Y., Kirkpatrick, D. S., Erpapazoglou, Z., Leon, S., Pantazopoulou, M., Kim, W., Gygi, S. P., Haguenauer-Tsapis, R., Reis, N. et al. (2011). A perturbed ubiquitin landscape distinguishes between ubiquitin in trafficking and in proteolysis. Mol. Cell. Proteomics 10, M111 009753.