Ubiquitylation of RAG-2 by Skp2-SCF links destruction of the V(D)J recombinase to the cell cycle

Molecular Cell

Volumn 18, Issue 6, 2005, Pages 699-709

  Jiang, Hao ^a   Chang, Fu Chung ^a   Ross, Ashley E ^a   Lee, Jihyun ^a   Nakayama, Keiichi ^b   Nakayama, Keiko ^b   Desiderio, Stephen ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR; PROTEASOME; RAG2 PROTEIN; RECOMBINASE; S PHASE KINASE ASSOCIATED PROTEIN 2; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL LYSATE; DNA CLEAVAGE; DNA RECOMBINATION; DNA REPAIR; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; UBIQUITINATION;

CELL CYCLE; DNA-BINDING PROTEINS; G1 PHASE; HELA CELLS; HUMANS; NUCLEAR PROTEINS; RECOMBINATION, GENETIC; S PHASE; S-PHASE KINASE-ASSOCIATED PROTEINS; UBIQUITIN; VDJ RECOMBINASES;

EID: 20444403003     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.05.011     Document Type: Article

References (39)

1. Cdh1 ubiquitin ligase Nature 428 2004 190 193
2. S. Bhattacharya, J. Garriga, J. Calbo, T. Yong, D.S. Haines, and X. Grana SKP2 associates with p130 and accelerates p130 ubiquitylation and degradation in human cells Oncogene 22 2003 2443 2451
3. G. Bornstein, J. Bloom, D. Sitry-Shevah, K. Nakayama, M. Pagano, and A. Hershko Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase J. Biol. Chem. 278 2003 25752 25757
4. A.C. Carrano, E. Eytan, A. Hershko, and M. Pagano SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27 Nat. Cell Biol. 1 1999 193 199
5. S. Desiderio, W.C. Lin, and Z. Li The cell cycle and V(D)J recombination Curr. Top. Microbiol. Immunol. 217 1996 45 59
6. M.J. Difilippantonio, J. Zhu, H.T. Chen, E. Meffre, M.C. Nussenzweig, E.E. Max, T. Ried, and A. Nussenzweig DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation Nature 404 2000 510 514
7. R. Fotedar, P. Fitzgerald, T. Rousselle, D. Cannella, M. Doree, H. Messier, and A. Fotedar p21 contains independent binding sites for cyclin and cdk2: both sites are required to inhibit cdk2 kinase activity Oncogene 12 1996 2155 2164
8. S.D. Fugmann, A.I. Lee, P.E. Shockett, I.J. Villey, and D.G. Schatz The RAG proteins and V(D)J recombination: complexes, ends, and transposition Annu. Rev. Immunol. 18 2000 495 527
9. T. Fukushima, M. Takata, C. Morrison, R. Araki, A. Fujimori, M. Abe, K. Tatsumi, M. Jasin, P.K. Dhar, and E. Sonoda Genetic analysis of the DNA-dependent protein kinase reveals an inhibitory role of Ku in late S-G2 phase DNA double-strand break repair J. Biol. Chem. 276 2001 44413 44418
10. D. Ganoth, G. Bornstein, T.K. Ko, B. Larsen, M. Tyers, M. Pagano, and A. Hershko The cell cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27 Nat. Cell Biol. 3 2001 321 324
11. Y. Gao, D.O. Ferguson, W. Xie, J.P. Manis, J. Sekiguchi, K.M. Frank, J. Chaudhuri, J. Horner, R.A. DePinho, and F.W. Alt Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development Nature 404 2000 897 900
12. M. Gellert V(D)J recombination: RAG proteins, repair factors, and regulation Annu. Rev. Biochem. 71 2002 101 132
13. A. Hershko, and A. Ciechanover The ubiquitin system Annu. Rev. Biochem. 67 1998 425 479
14. H. Jiang, A.E. Ross, and S. Desiderio Cell cycle-dependent accumulation in vivo of transposition-competent complexes between recombination signal ends and full-length RAG proteins J. Biol. Chem. 279 2004 8478 8486
15. S.Y. Kim, A. Herbst, K.A. Tworkowski, S.E. Salghetti, and W.P. Tansey Skp2 regulates Myc protein stability and activity Mol. Cell 11 2003 1177 1188
16. J. Lee, and S. Desiderio Cyclin A/CDK2 regulates V(D)J recombination by coordinating RAG-2 accumulation and DNA repair Immunity 11 1999 771 781
17. X. Li, Q. Zhao, R. Liao, P. Sun, and X. Wu The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation J. Biol. Chem. 278 2003 30854 30858
18. Z. Li, D.I. Dordai, J. Lee, and S. Desiderio A conserved degradation signal regulates RAG-2 accumulation during cell division and links V(D)J recombination to the cell cycle Immunity 5 1996 575 589
19. M.R. Lieber, Y. Ma, U. Pannicke, and K. Schwarz Mechanism and regulation of human non-homologous DNA end-joining Nat. Rev. Mol. Cell Biol. 4 2003 712 720
20. W.C. Lin, and S. Desiderio Regulation of V(D)J recombination activator protein RAG-2 by phosphorylation Science 260 1993 953 959
21. W.C. Lin, and S. Desiderio Cell cycle regulation of V(D)J recombination-activating protein RAG-2 Proc. Natl. Acad. Sci. USA 91 1994 2733 2737
22. J. Lisztwan, A. Marti, H. Sutterluty, M. Gstaiger, C. Wirbelauer, and W. Krek Association of human CUL-1 and ubiquitin-conjugating enzyme CDC34 with the F-box protein p45(SKP2): evidence for evolutionary conservation in the subunit composition of the CDC34-SCF pathway EMBO J. 17 1998 368 383
23. R.S. Maser, K.J. Monsen, B.E. Nelms, and J.H. Petrini hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks Mol. Cell. Biol. 17 1997 6087 6096
24. R. Mizuta, M. Mizuta, S. Araki, and D. Kitamura RAG2 is down-regulated by cytoplasmic sequestration and ubiquitin-dependent degradation J. Biol. Chem. 277 2002 41423 41427
25. K. Nakayama, H. Nagahama, Y.A. Minamishima, M. Matsumoto, I. Nakamichi, K. Kitagawa, M. Shirane, R. Tsunematsu, T. Tsukiyama, and N. Ishida Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication EMBO J. 19 2000 2069 2081
26. H. Nguyen, D.M. Gitig, and A. Koff Cell-free degradation of p27(kip1), a G1 cyclin-dependent kinase inhibitor, is dependent on CDK2 activity and the proteasome Mol. Cell. Biol. 19 1999 1190 1201
27. C.M. Pickart Mechanisms underlying ubiquitination Annu. Rev. Biochem. 70 2001 503 533
28. M. Schlissel, A. Constantinescu, T. Morrow, M. Baxter, and A. Peng Double-strand signal sequence breaks in V(D)J recombination are blunt, 5′-phosphorylated, RAG-dependent, and cell cycle regulated Genes Dev. 7 1993 2520 2532
29. C. Spruck, H. Strohmaier, M. Watson, A.P. Smith, A. Ryan, T.W. Krek, and S.I. Reed A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1 Mol. Cell 7 2001 639 650
30. H. Sutterluty, E. Chatelain, A. Marti, C. Wirbelauer, M. Senften, U. Muller, and W. Krek p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells Nat. Cell Biol. 1 1999 207 214
31. M. Takata, M.S. Sasaki, E. Sonoda, C. Morrison, M. Hashimoto, H. Utsumi, Y. Yamaguchi-Iwai, A. Shinohara, and S. Takeda Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells EMBO J. 17 1998 5497 5508
32. D. Tedesco, J. Lukas, and S.I. Reed The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF(Skp2) Genes Dev. 16 2002 2946 2957
33. M. Treier, L.M. Staszewski, and D. Bohmann Ubiquitin-dependent c-Jun degradation in vivo is mediated by the δ domain Cell 78 1994 787 798
34. L.M. Tsvetkov, K.H. Yeh, S.J. Lee, H. Sun, and H. Zhang p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27 Curr. Biol. 9 1999 661 664
35. N. von der Lehr, S. Johansson, S. Wu, F. Bahram, A. Castell, C. Cetinkaya, P. Hydbring, I. Weidung, K. Nakayama, and K.I. Nakayama The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription Mol. Cell 11 2003 1189 1200
36. W. Wang, D. Ungermannova, J. Jin, J.W. Harper, and X. Liu Negative regulation of SCF(Skp2) ubiquitin ligase by TGF-beta signaling Oncogene 23 2003 1064 1075
37. W. Wei, N.G. Ayad, Y. Wan, G.-J. Zhang, M.W. Kirschner, and W.G. Kaelin Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex Nature 428 2004 194 198
38. H. Zhang, R. Kobayaashi, K. Galaktionov, and D. Beach p19Skp1 and p45Skp2 are essential elements of the cyclin A-CDK2 S phase kinase Cell 82 1995 915 925
39. C. Zhu, K.D. Mills, D.O. Ferguson, C. Lee, J. Manis, J. Fleming, Y. Gao, C.C. Morton, and F.W. Alt Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations Cell 109 2002 811 821