SCF-mediated Cdh1 degradation defines a negative feedback system that coordinates cell-cycle progression

Cell Reports

Volumn 4, Issue 4, 2013, Pages 803-816

  Fukushima, Hidefumi ^a   Ogura, Kohei ^a   Wan, Lixin ^a   Lu, Ying ^a   Li, Victor ^a   Gao, Daming ^a   Liu, Pengda ^a   Lau, Alan W ^a   Wu, Tao ^a   Kirschner, Marc W ^a   Inuzuka, Hiroyuki ^a   Wei, Wenyi ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN A; POLO LIKE KINASE 1; UBIQUITIN PROTEIN LIGASE; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; NEGATIVE FEEDBACK; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; UBIQUITINATION;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CDH1 PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN A; FEEDBACK, PHYSIOLOGICAL; HEK293 CELLS; HELA CELLS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITINATION; XENOPUS;

EID: 84883287460     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.031     Document Type: Article

References (52)

1. Bashir T., Dorrello N.V., Amador V., Guardavaccaro D., Pagano M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 2004, 428:190-193.
2. Benmaamar R., Pagano M. Involvement of the SCF complex in the control of Cdh1 degradation in S-phase. Cell Cycle 2005, 4:1230-1232.
3. Boehm J.S., Hession M.T., Bulmer S.E., Hahn W.C. Transformation of human and murine fibroblasts without viral oncoproteins. Mol. Cell. Biol. 2005, 25:6464-6474.
4. Brooks C.L., Gu W. p53 regulation by ubiquitin. FEBS Lett. 2011, 585:2803-2809.
5. Cardozo T., Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 2004, 5:739-751.
6. Conradie R., Bruggeman F.J., Ciliberto A., Csikász-Nagy A., Novák B., Westerhoff H.V., Snoep J.L. Restriction point control of the mammalian cell cycle via the cyclin E/Cdk2:p27 complex. FEBS J. 2010, 277:357-367.
7. Dephoure N., Zhou C., Villén J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., Gygi S.P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 2008, 105:10762-10767.
8. Elia A.E., Cantley L.C., Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 2003, 299:1228-1231.
9. Elia A.E., Rellos P., Haire L.F., Chao J.W., Ivins F.J., Hoepker K., Mohammad D., Cantley L.C., Smerdon S.J., Yaffe M.B. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 2003, 115:83-95.
10. Fasano C.A., Dimos J.T., Ivanova N.B., Lowry N., Lemischka I.R., Temple S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 2007, 1:87-99.
11. Fuchs S.Y., Spiegelman V.S., Kumar K.G. The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 2004, 23:2028-2036.
12. Gao D., Inuzuka H., Korenjak M., Tseng A., Wu T., Wan L., Kirschner M., Dyson N., Wei W. Cdh1 regulates cell cycle through modulating the claspin/Chk1 and the Rb/E2F1 pathways. Mol. Biol. Cell 2009, 20:3305-3316.
13. Gao D., Inuzuka H., Tseng A., Chin R.Y., Toker A., Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat. Cell Biol. 2009, 11:397-408.
14. Gao D., Wan L., Inuzuka H., Berg A.H., Tseng A., Zhai B., Shaik S., Bennett E., Tron A.E., Gasser J.A., et al. Rictor forms a complex with Cullin-1 to promote SGK1 ubiquitination and destruction. Mol. Cell 2010, 39:797-808.
15. Gao D., Inuzuka H., Tan M.K., Fukushima H., Locasale J.W., Liu P., Wan L., Zhai B., Chin Y.R., Shaik S., et al. mTOR drives its own activation via SCF(βTrCP)-dependent degradation of the mTOR inhibitor DEPTOR. Mol. Cell 2011, 44:290-303.
16. Harper J.W., Burton J.L., Solomon M.J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 2002, 16:2179-2206.
17. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
18. Hsu J.Y., Reimann J.D., Sørensen C.S., Lukas J., Jackson P.K. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1). Nat. Cell Biol. 2002, 4:358-366.
19. Inuzuka H., Tseng A., Gao D., Zhai B., Zhang Q., Shaik S., Wan L., Ang X.L., Mock C., Yin H., et al. Phosphorylation by casein kinase I promotes the turnover of the Mdm2 oncoprotein via the SCF(beta-TRCP) ubiquitin ligase. Cancer Cell 2010, 18:147-159.
20. Janzen V., Forkert R., Fleming H.E., Saito Y., Waring M.T., Dombkowski D.M., Cheng T., DePinho R.A., Sharpless N.E., Scadden D.T. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
21. Jin J., Shirogane T., Xu L., Nalepa G., Qin J., Elledge S.J., Harper J.W. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 2003, 17:3062-3074.
22. Keck J.M., Summers M.K., Tedesco D., Ekholm-Reed S., Chuang L.C., Jackson P.K., Reed S.I. Cyclin E overexpression impairs progression through mitosis by inhibiting APC(Cdh1). J.Cell Biol. 2007, 178:371-385.
23. Kroll K.L., Salic A.N., Evans L.M., Kirschner M.W. Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 1998, 125:3247-3258.
24. Lassot I., Ségéral E., Berlioz-Torrent C., Durand H., Groussin L., Hai T., Benarous R., Margottin-Goguet F. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase. Mol. Cell. Biol. 2001, 21:2192-2202.
25. Lau A.W., Inuzuka H., Fukushima H., Wan L., Liu P., Gao D., Sun Y., Wei W. Regulation of APC(Cdh1) E3 ligase activity by the Fbw7/cyclin E signaling axis contributes to the tumor suppressor function of Fbw7. Cell Res. 2013, 23:947-961.
26. Listovsky T., Oren Y.S., Yudkovsky Y., Mahbubani H.M., Weiss A.M., Lebendiker M., Brandeis M. Mammalian Cdh1/Fzr mediates its own degradation. EMBO J. 2004, 23:1619-1626.
27. Liu W., Li W., Fujita T., Yang Q., Wan Y. Proteolysis of CDH1 enhances susceptibility to UV radiation-induced apoptosis. Carcinogenesis 2008, 29:263-272.
28. Lu Y., Cross F.R. Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator. Cell 2010, 141:268-279.
29. Lu Z., Hunter T. Ubiquitylation and proteasomal degradation of the p21(Cip1), p27(Kip1) and p57(Kip2) CDK inhibitors. Cell Cycle 2010, 9:2342-2352.
30. Lukas C., Sørensen C.S., Kramer E., Santoni-Rugiu E., Lindeneg C., Peters J.M., Bartek J., Lukas J. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 1999, 401:815-818.
31. Miller J.J., Summers M.K., Hansen D.V., Nachury M.V., Lehman N.L., Loktev A., Jackson P.K. Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev. 2006, 20:2410-2420.
32. Nakajima H., Toyoshima-Morimoto F., Taniguchi E., Nishida E. Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J.Biol. Chem. 2003, 278:25277-25280.
33. Nakayama K.I., Nakayama K. Regulation of the cell cycle by SCF-type ubiquitin ligases. Semin. Cell Dev. Biol. 2005, 16:323-333.
34. Nakayama K.I., Hatakeyama S., Nakayama K. Regulation of the cell cycle at the G1-S transition by proteolysis of cyclin E and p27Kip1. Biochem. Biophys. Res. Commun. 2001, 282:853-860.
35. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin): a Systematical and Chronological Survey of the Development from Fertilized Egg Till the End of Metamorphosis 1967, North Holland, Amsterdam.
36. Oshimori N., Ohsugi M., Yamamoto T. The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat. Cell Biol. 2006, 8:1095-1101.
37. Peng H.B. Xenopus laevis: Practical uses in cell and molecular biology. Solutions and protocols. Methods Cell Biol. 1991, 36:657-662.
38. Peters J.M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 2002, 9:931-943.
39. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
40. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
41. Robbins J.A., Cross F.R. Requirements and reasons for effective inhibition of the anaphase promoting complex activator CDH1. Mol. Biol. Cell 2010, 21:914-925.
42. Seo E., Kim H., Kim R., Yun S., Kim M., Han J.K., Costantini F., Jho E.H. Multiple isoforms of beta-TrCP display differential activities in the regulation of Wnt signaling. Cell. Signal. 2009, 21:43-51.
43. Sharma S.V., Settleman J. Oncogene addiction: setting the stage for molecularly targeted cancer therapy. Genes Dev. 2007, 21:3214-3231.
44. Sørensen C.S., Lukas C., Kramer E.R., Peters J.M., Bartek J., Lukas J. Nonperiodic activity of the human anaphase-promoting complex-Cdh1 ubiquitin ligase results in continuous DNA synthesis uncoupled from mitosis. Mol. Cell. Biol. 2000, 20:7613-7623.
45. Sørensen C.S., Lukas C., Kramer E.R., Peters J.M., Bartek J., Lukas J. A conserved cyclin-binding domain determines functional interplay between anaphase-promoting complex-Cdh1 and cyclin A-Cdk2 during cell cycle progression. Mol. Cell. Biol. 2001, 21:3692-3703.
46. Spiegelman V.S., Stavropoulos P., Latres E., Pagano M., Ronai Z., Slaga T.J., Fuchs S.Y. Induction of beta-transducin repeat-containing protein by JNK signaling and its role in the activation of NF-kappaB. J.Biol. Chem. 2001, 276:27152-27158.
47. Spiegelman V.S., Tang W., Katoh M., Slaga T.J., Fuchs S.Y. Inhibition of HOS expression and activities by Wnt pathway. Oncogene 2002, 21:856-860.
48. Steegmaier M., Hoffmann M., Baum A., Lénárt P., Petronczki M., Krssák M., Gürtler U., Garin-Chesa P., Lieb S., Quant J., et al. BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth invivo. Curr. Biol. 2007, 17:316-322.
49. Wan L., Zou W., Gao D., Inuzuka H., Fukushima H., Berg A.H., Drapp R., Shaik S., Hu D., Lester C., et al. Cdh1 regulates osteoblast functionthrough an APC/C-independent modulation of Smurf1. Mol. Cell 2011, 44:721-733.
50. Wang B., Li Y. Evidence for the direct involvement of betaTrCP in Gli3 protein processing. Proc. Natl. Acad. Sci. USA 2006, 103:33-38.
51. Wäsch R., Cross F.R. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 2002, 418:556-562.
52. Wei W., Ayad N.G., Wan Y., Zhang G.J., Kirschner M.W., Kaelin W.G. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 2004, 428:194-198.