CRL1-FBXO11 promotes Cdt2 ubiquitylation and degradation and regulates Pr-Set7/Set8-mediated cellular migration

Molecular Cell

Volumn 49, Issue 6, 2013, Pages 1147-1158

  Abbas, Tarek ^a   Mueller, Adam C ^a   Shibata, Etsuko ^a   Keaton, Mignon ^a,c   Rossi, Mario ^b   Dutta, Anindya ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c METABOLON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDC 10 DEPENDENT TRANSCRIPT 2 PROTEIN; CRL 1 FBXO 11 PROTEIN; P21 ACTIVATED KINASE; PROTEIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CELL MIGRATION; DEGRADATION; DOWN REGULATION; EPITHELIUM CELL; GENE CONTROL; GENOMIC INSTABILITY; PROTEIN DEGRADATION; UBIQUITINATION;

AMINO ACID SEQUENCE; CELL LINE; CELL MOVEMENT; CONSERVED SEQUENCE; CULLIN PROTEINS; CYCLOHEXIMIDE; F-BOX PROTEINS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; LEUPEPTINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN BINDING; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTEOLYSIS; RNA, SMALL INTERFERING; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84875806981     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.02.003     Document Type: Article

References (42)

1. Abbas T., Dutta A. CRL4Cdt2: master coordinator of cell cycle progression and genome stability. Cell Cycle 2011, 10:241-249.
2. Abbas T., Sivaprasad U., Terai K., Amador V., Pagano M., Dutta A. PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev. 2008, 22:2496-2506.
3. Abbas T., Shibata E., Park J., Jha S., Karnani N., Dutta A. CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 2010, 40:9-21.
4. Angers S., Thorpe C.J., Biechele T.L., Goldenberg S.J., Zheng N., MacCoss M.J., Moon R.T. The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nat. Cell Biol. 2006, 8:348-357.
5. Baraniskin A., Birkenkamp-Demtroder K., Maghnouj A., Zöllner H., Munding J., Klein-Scory S., Reinacher-Schick A., Schwarte-Waldhoff I., Schmiegel W., Hahn S.A. MiR-30a-5p suppresses tumor growth in colon carcinoma by targeting DTL. Carcinogenesis 2012, 33:732-739.
6. 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., Zou L. CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 2010, 40:22-33.
7. Chen X., Zhang Y., Douglas L., Zhou P. UV-damaged DNA-binding proteins are targets of CUL-4A-mediated ubiquitination and degradation. J. Biol. Chem. 2001, 276:48175-48182.
8. Deshaies R.J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 1999, 15:435-467.
9. Duan S., Cermak L., Pagan J.K., Rossi M., Martinengo C., di Celle P.F., Chapuy B., Shipp M., Chiarle R., Pagano M. FBXO11 targets BCL6 for degradation and is inactivated in diffuse large B-cell lymphomas. Nature 2012, 481:90-93.
10. Hardisty-Hughes R.E., Tateossian H., Morse S.A., Romero M.R., Middleton A., Tymowska-Lalanne Z., Hunter A.J., Cheeseman M., Brown S.D. A mutation in the F-box gene, Fbxo11, causes otitis media in the Jeff mouse. Hum. Mol. Genet. 2006, 15:3273-3279.
11. He Y.J., McCall C.M., Hu J., Zeng Y., Xiong Y. DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 2006, 20:2949-2954.
12. Higa L.A., Banks D., Wu M., Kobayashi R., Sun H., Zhang H. L2DTL/CDT2 interacts with the CUL4/DDB1 complex and PCNA and regulates CDT1 proteolysis in response to DNA damage. Cell Cycle 2006, 5:1675-1680.
13. Higa L.A., Wu M., Ye T., Kobayashi R., Sun H., Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 2006, 8:1277-1283.
14. Jackson S., Xiong Y. CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci. 2009, 34:562-570.
15. Jin J., Arias E.E., Chen J., Harper J.W., Walter J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 2006, 23:709-721.
16. Jørgensen S., Eskildsen M., Fugger K., Hansen L., Larsen M.S., Kousholt A.N., Syljuåsen R.G., Trelle M.B., Jensen O.N., Helin K., Sørensen C.S. SET8 is degraded via PCNA-coupled CRL4(CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 2011, 192:43-54.
17. Kim Y., Starostina N.G., Kipreos E.T. The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev. 2008, 22:2507-2519.
18. Kopanja D., Roy N., Stoyanova T., Hess R.A., Bagchi S., Raychaudhuri P. Cul4A is essential for spermatogenesis and male fertility. Dev. Biol. 2011, 352:278-287.
19. Li J., Ng E.K., Ng Y.P., Wong C.Y., Yu J., Jin H., Cheng V.Y., Go M.Y., Cheung P.K., Ebert M.P., et al. Identification of retinoic acid-regulated nuclear matrix-associated protein as a novel regulator of gastric cancer. Br. J. Cancer 2009, 101:691-698.
20. Lin J.J., Milhollen M.A., Smith P.G., Narayanan U., Dutta A. NEDD8-targeting drug MLN4924 elicits DNA rereplication by stabilizing Cdt1 in S phase, triggering checkpoint activation, apoptosis, and senescence in cancer cells. Cancer Res. 2010, 70:10310-10320.
21. Lipkowitz S., Weissman A.M. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat. Rev. Cancer 2011, 11:629-643.
22. Liu L., Yin Y., Li Y., Prevedel L., Lacy E.H., Ma L., Zhou P. Essential role of the CUL4B ubiquitin ligase in extra-embryonic tissue development during mouse embryogenesis. Cell Res. 2012, 22:1258-1269.
23. Mackintosh C., Ordóñez J.L., García-Domínguez D.J., Sevillano V., Llombart-Bosch A., Szuhai K., Scotlandi K., Alberghini M., Sciot R., Sinnaeve F., et al. 1q gain and CDT2 overexpression underlie an aggressive and highly proliferative form of Ewing sarcoma. Oncogene 2012, 31:1287-1298.
24. Moustakas A., Heldin C.H. Induction of epithelial-mesenchymal transition by transforming growth factor β. Semin. Cancer Biol. 2012, 22:446-454.
25. Nag A., Bondar T., Shiv S., Raychaudhuri P. The xeroderma pigmentosum group E gene product DDB2 is a specific target of cullin 4A in mammalian cells. Mol. Cell. Biol. 2001, 21:6738-6747.
26. Nishitani H., Sugimoto N., Roukos V., Nakanishi Y., Saijo M., Obuse C., Tsurimoto T., Nakayama K.I., Nakayama K., Fujita M., et al. Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 2006, 25:1126-1136.
27. Nishitani H., Shiomi Y., Iida H., Michishita M., Takami T., Tsurimoto T. CDK inhibitor p21 is degraded by a proliferating cell nuclear antigen-coupled Cul4-DDB1Cdt2 pathway during S phase and after UV irradiation. J. Biol. Chem. 2008, 283:29045-29052.
28. Oda H., Hübner M.R., Beck D.B., Vermeulen M., Hurwitz J., Spector D.L., Reinberg D. Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 2010, 40:364-376.
29. Pan Z.Q., Kentsis A., Dias D.C., Yamoah K., Wu K. Nedd8 on cullin: building an expressway to protein destruction. Oncogene 2004, 23:1985-1997.
30. Pan H.W., Chou H.Y., Liu S.H., Peng S.Y., Liu C.L., Hsu H.C. Role of L2DTL, cell cycle-regulated nuclear and centrosome protein, in aggressive hepatocellular carcinoma. Cell Cycle 2006, 5:2676-2687.
31. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
32. Podust V.N., Brownell J.E., Gladysheva T.B., Luo R.S., Wang C., Coggins M.B., Pierce J.W., Lightcap E.S., Chau V. A Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kip1 by ubiquitination. Proc. Natl. Acad. Sci. USA 2000, 97:4579-4584.
33. Read M.A., Brownell J.E., Gladysheva T.B., Hottelet M., Parent L.A., Coggins M.B., Pierce J.W., Podust V.N., Luo R.S., Chau V., Palombella V.J. Nedd8 modification of cul-1 activates SCF(beta(TrCP))-dependent ubiquitination of IkappaBalpha. Mol. Cell. Biol. 2000, 20:2326-2333.
34. Sansam C.L., Shepard J.L., Lai K., Ianari A., Danielian P.S., Amsterdam A., Hopkins N., Lees J.A. DTL/CDT2 is essential for both CDT1 regulation and the early G2/M checkpoint. Genes Dev. 2006, 20:3117-3129.
35. Senga T., Sivaprasad U., Zhu W., Park J.H., Arias E.E., Walter J.C., Dutta A. PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem. 2006, 281:6246-6252.
36. 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. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 2009, 458:732-736.
37. Tardat M., Brustel J., Kirsh O., Lefevbre C., Callanan M., Sardet C., Julien E. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 2010, 12:1086-1093.
38. Tasaki T., Mulder L.C., Iwamatsu A., Lee M.J., Davydov I.V., Varshavsky A., Muesing M., Kwon Y.T. A family of mammalian E3 ubiquitin ligases that contain the UBR box motif and recognize N-degrons. Mol. Cell. Biol. 2005, 25:7120-7136.
39. Tateossian H., Hardisty-Hughes R.E., Morse S., Romero M.R., Hilton H., Dean C., Brown S.D. Regulation of TGF-beta signalling by Fbxo11, the gene mutated in the Jeff otitis media mouse mutant. Pathogenetics 2009, 2:5. 10.1186/1755-8417-2-5.
40. Ueki T., Nishidate T., Park J.H., Lin M.L., Shimo A., Hirata K., Nakamura Y., Katagiri T. Involvement of elevated expression of multiple cell-cycle regulator, DTL/RAMP (denticleless/RA-regulated nuclear matrix associated protein), in the growth of breast cancer cells. Oncogene 2008, 27:5672-5683.
41. Wu S., Wang W., Kong X., Congdon L.M., Yokomori K., Kirschner M.W., Rice J.C. Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 2010, 24:2531-2542.
42. Yang F., Sun L., Li Q., Han X., Lei L., Zhang H., Shang Y. SET8 promotes epithelial-mesenchymal transition and confers TWIST dual transcriptional activities. EMBO J. 2012, 31:110-123.