Specific small molecule inhibitors of skp2-mediated p27 degradation

Chemistry and Biology

Volumn 19, Issue 12, 2012, Pages 1515-1524

  Wu, Lily ^a   Grigoryan, Arsen V ^a   Li, Yunfeng ^b   Hao, Bing ^b   Pagano, Michele ^a,c   Cardozo, Timothy J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN 2; S PHASE KINASE ASSOCIATED PROTEIN 2 INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL TYPE; CRYSTAL STRUCTURE; IMMUNOPRECIPITATION; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS; CDC2-CDC28 KINASES; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P27; HUMANS; MODELS, MOLECULAR; NEOPLASMS; PROTEIN BINDING; S-PHASE KINASE-ASSOCIATED PROTEINS; SMALL MOLECULE LIBRARIES; UBIQUITINATION;

ANIMALIA;

EID: 84871569969     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.09.015     Document Type: Article

References (62)

1. R. Abagyan, and M. Totrov Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins J. Mol. Biol. 235 1994 983 1002
2. R. Abagyan, and M. Totrov High-throughput docking for lead generation Curr. Opin. Chem. Biol. 5 2001 375 382
3. R. Abagyan, M. Totrov, and D. Kuznetsov ICM - A new method for protein modeling and design: Applications to docking and structure prediction from the distorted native conformation J. Comput. Chem. 15 1994 488 506
4. M. Aghajan, N. Jonai, K. Flick, F. Fu, M. Luo, X. Cai, I. Ouni, N. Pierce, X. Tang, and B. Lomenick Chemical genetics screen for enhancers of rapamycin identifies a specific inhibitor of an SCF family E3 ubiquitin ligase Nat. Biotechnol. 28 2010 738 742
5. J. An, M. Totrov, and R. Abagyan Comprehensive identification of "druggable" protein ligand binding sites Genome Inform. 15 2004 31 41
6. A.A. Argyriou, G. Iconomou, and H.P. Kalofonos Bortezomib-induced peripheral neuropathy in multiple myeloma: a comprehensive review of the literature Blood 112 2008 1593 1599
7. J. Bloom, and M. Pagano Deregulated degradation of the cdk inhibitor p27 and malignant transformation Semin. Cancer Biol. 13 2003 41 47
8. 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
9. P.F. Bross, R. Kane, A.T. Farrell, S. Abraham, K. Benson, M.E. Brower, S. Bradley, J.V. Gobburu, A. Goheer, and S.L. Lee Approval summary for bortezomib for injection in the treatment of multiple myeloma Clin. Cancer Res. 10 2004 3954 3964
10. X. Cao, L. Xue, L. Han, L. Ma, T. Chen, and T. Tong WW domain-containing E3 ubiquitin protein ligase 1 (WWP1) delays cellular senescence by promoting p27(Kip1) degradation in human diploid fibroblasts J. Biol. Chem. 286 2011 33447 33456
11. T. Cardozo, and M. Pagano The SCF ubiquitin ligase: insights into a molecular machine Nat. Rev. Mol. Cell Biol. 5 2004 739 751
12. T. Cardozo, and R. Abagyan Druggability of SCF ubiquitin ligase-protein interfaces Methods Enzymol. 399 2005 634 653
13. T. Cardozo, and M. Pagano Wrenches in the works: drug discovery targeting the SCF ubiquitin ligase and APC/C complexes BMC Biochem. 8 Suppl. 1 2007 S9
14. 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
15. D.F. Ceccarelli, X. Tang, B. Pelletier, S. Orlicky, W. Xie, V. Plantevin, D. Neculai, Y.C. Chou, A. Ogunjimi, and A. Al-Hakim An allosteric inhibitor of the human Cdc34 ubiquitin-conjugating enzyme Cell 145 2011 1075 1087
16. A.V. Cheltsov, M. Aoyagi, A. Aleshin, E.C. Yu, T. Gilliland, D. Zhai, A.A. Bobkov, J.C. Reed, R.C. Liddington, and R. Abagyan Vaccinia virus virulence factor N1L is a novel promising target for antiviral therapeutic intervention J. Med. Chem. 53 2010 3899 3906
17. Q. Chen, W. Xie, D.J. Kuhn, P.M. Voorhees, A. Lopez-Girona, D. Mendy, L.G. Corral, V.P. Krenitsky, W. Xu, and L. Moutouh-de Parseval Targeting the p27 E3 ligase SCF(Skp2) results in p27- and Skp2-mediated cell-cycle arrest and activation of autophagy Blood 111 2008 4690 4699
18. I.M. Chu, L. Hengst, and J.M. Slingerland The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy Nat. Rev. Cancer 8 2008 253 267
19. A. Ciechanover Proteolysis: from the lysosome to ubiquitin and the proteasome Nat. Rev. Mol. Cell Biol. 6 2005 79 87
20. N.V. Dorrello, A. Peschiaroli, D. Guardavaccaro, N.H. Colburn, N.E. Sherman, and M. Pagano S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth Science 314 2006 467 471
21. V.A. Florenes, G.M. Maelandsmo, R.S. Kerbel, J.M. Slingerland, J.M. Nesland, and R. Holm Protein expression of the cell-cycle inhibitor p27Kip1 in malignant melanoma: inverse correlation with disease-free survival Am. J. Pathol. 153 1998 305 312
22. D. Frescas, and M. Pagano Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer Nat. Rev. Cancer 8 2008 438 449
23. 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
24. B. Hao, N. Zheng, B.A. Schulman, G. Wu, J.J. Miller, M. Pagano, and N.P. Pavletich Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase Mol. Cell 20 2005 9 19
25. D.D. Hershko Oncogenic properties and prognostic implications of the ubiquitin ligase Skp2 in cancer Cancer 112 2008 1415 1424
26. T. Kamura, T. Hara, S. Kotoshiba, M. Yada, N. Ishida, H. Imaki, S. Hatakeyama, K. Nakayama, and K.I. Nakayama Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation Proc. Natl. Acad. Sci. USA 100 2003 10231 10236
27. T. Kamura, T. Hara, M. Matsumoto, N. Ishida, F. Okumura, S. Hatakeyama, M. Yoshida, K. Nakayama, and K.I. Nakayama Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27(Kip1) at G1 phase Nat. Cell Biol. 6 2004 1229 1235
28. R.C. Kane, R. Dagher, A. Farrell, C.W. Ko, R. Sridhara, R. Justice, and R. Pazdur Bortezomib for the treatment of mantle cell lymphoma Clin. Cancer Res. 13 2007 5291 5294
29. Y. Katagiri, Y. Hozumi, and S. Kondo Knockdown of Skp2 by siRNA inhibits melanoma cell growth in vitro and in vivo J. Dermatol. Sci. 42 2006 215 224
30. Q. Li, M. Murphy, J. Ross, C. Sheehan, and J.A. Carlson Skp2 and p27kip1 expression in melanocytic nevi and melanoma: an inverse relationship J. Cutan. Pathol. 31 2004 633 642
31. H.K. Lin, Z. Chen, G. Wang, C. Nardella, S.W. Lee, C.H. Chan, W.L. Yang, J. Wang, A. Egia, and K.I. Nakayama Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence Nature 464 2010 374 379
32. C.A. Lipinski, F. Lombardo, B.W. Dominy, and P.J. Feeney Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Deliv. Rev. 46 2001 3 26
33. L. Lu, H. Schulz, and D.A. Wolf The F-box protein SKP2 mediates androgen control of p27 stability in LNCaP human prostate cancer cells BMC Cell Biol. 3 2002 22
34. L. Meijer, A. Borgne, O. Mulner, J.P. Chong, J.J. Blow, N. Inagaki, M. Inagaki, J.G. Delcros, and J.P. Moulinoux Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5 Eur. J. Biochem. 243 1997 527 536
35. M. Millard, D. Pathania, F. Grande, S. Xu, and N. Neamati Small-molecule inhibitors of p53-MDM2 interaction: the 2006-2010 update Curr. Pharm. Des. 17 2011 536 559
36. A. Montagnoli, F. Fiore, E. Eytan, A.C. Carrano, G.F. Draetta, A. Hershko, and M. Pagano Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation Genes Dev. 13 1999 1181 1189
37. K.I. Nakayama, and K. Nakayama Ubiquitin ligases: cell-cycle control and cancer Nat. Rev. Cancer 6 2006 369 381
38. K. Nakayama, H. Nagahama, Y.A. Minamishima, S. Miyake, N. Ishida, S. Hatakeyama, M. Kitagawa, S. Iemura, T. Natsume, and K.I. Nakayama Skp2-mediated degradation of p27 regulates progression into mitosis Dev. Cell 6 2004 661 672
39. I. Nickeleit, S. Zender, F. Sasse, R. Geffers, G. Brandes, I. Sörensen, H. Steinmetz, S. Kubicka, T. Carlomagno, and D. Menche Argyrin a reveals a critical role for the tumor suppressor protein p27(kip1) in mediating antitumor activities in response to proteasome inhibition Cancer Cell 14 2008 23 35
40. Y.M. Ning, K. He, R. Dagher, R. Sridhara, A.T. Farrell, R. Justice, and R. Pazdur Liposomal doxorubicin in combination with bortezomib for relapsed or refractory multiple myeloma Oncology (Williston Park) 21 2007 1503 1508 discussion 1511, 1513, 1516 passim
41. S. Orlicky, X. Tang, V. Neduva, N. Elowe, E.D. Brown, F. Sicheri, and M. Tyers An allosteric inhibitor of substrate recognition by the SCF(Cdc4) ubiquitin ligase Nat. Biotechnol. 28 2010 733 737
42. R.Z. Orlowski, and D.J. Kuhn Proteasome inhibitors in cancer therapy: lessons from the first decade Clin. Cancer Res. 14 2008 1649 1657
43. M. Pagano Control of DNA synthesis and mitosis by the Skp2-p27-Cdk1/2 axis Mol. Cell 14 2004 414 416
44. M.D. Petroski, and R.J. Deshaies Function and regulation of cullin-RING ubiquitin ligases Nat. Rev. Mol. Cell Biol. 6 2005 9 20
45. E. Rico-Bautista, C.C. Yang, L. Lu, G.P. Roth, and D.A. Wolf Chemical genetics approach to restoring p27Kip1 reveals novel compounds with antiproliferative activity in prostate cancer cells BMC Biol. 8 2010 153
46. T. Shibahara, T. Onishi, O.E. Franco, K. Arima, and Y. Sugimura Down-regulation of Skp2 is correlated with p27-associated cell cycle arrest induced by phenylacetate in human prostate cancer cells Anticancer Res. 25 3B 2005 1881 1888
47. D. Sitry, M.A. Seeliger, T.K. Ko, D. Ganoth, S.E. Breward, L.S. Itzhaki, M. Pagano, and A. Hershko Three different binding sites of Cks1 are required for p27-ubiquitin ligation J. Biol. Chem. 277 2002 42233 42240
48. D. Skowyra, K.L. Craig, M. Tyers, S.J. Elledge, and J.W. Harper F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex Cell 91 1997 209 219
49. T.A. Soucy, P.G. Smith, M.A. Milhollen, A.J. Berger, J.M. Gavin, S. Adhikari, J.E. Brownell, K.E. Burke, D.P. Cardin, and S. Critchley An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer Nature 458 2009 732 736
50. H. Sumimoto, K. Hirata, S. Yamagata, H. Miyoshi, M. Miyagishi, K. Taira, and Y. Kawakami Effective inhibition of cell growth and invasion of melanoma by combined suppression of BRAF (V599E) and Skp2 with lentiviral RNAi Int. J. Cancer 118 2006 472 476
51. L. Sun, L. Cai, Y. Yu, Q. Meng, X. Cheng, Y. Zhao, G. Sui, and F. Zhang Knockdown of S-phase kinase-associated protein-2 expression in MCF-7 inhibits cell growth and enhances the cytotoxic effects of epirubicin Acta Biochim. Biophys. Sin. (Shanghai) 39 2007 999 1007
52. Y. Sun E3 ubiquitin ligases as cancer targets and biomarkers Neoplasia 8 2006 645 654
53. 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
54. D. Ungermannova, Y. Gao, and X. Liu Ubiquitination of p27Kip1 requires physical interaction with cyclin E and probable phosphate recognition by SKP2 J. Biol. Chem. 280 2005 30301 30309
55. L.T. Vassilev, B.T. Vu, B. Graves, D. Carvajal, F. Podlaski, Z. Filipovic, N. Kong, U. Kammlott, C. Lukacs, and C. Klein In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 2004 844 848
56. H. Wang, J. Blais, D. Ron, and T. Cardozo Structural determinants of PERK inhibitor potency and selectivity Chem. Biol. Drug Des. 76 2010 480 495
57. W. Wang, D. Ungermannova, L. Chen, and X. Liu A negatively charged amino acid in Skp2 is required for Skp2-Cks1 interaction and ubiquitination of p27Kip1 J. Biol. Chem. 278 2003 32390 32396
58. W. Wang, D. Ungermannova, L. Chen, and X. Liu Molecular and biochemical characterization of the Skp2-Cks1 binding interface J. Biol. Chem. 279 2004 51362 51369
59. Z. Wang, M. Cuddy, T. Samuel, K. Welsh, A. Schimmer, F. Hanaii, R. Houghten, C. Pinilla, and J.C. Reed Cellular, biochemical, and genetic analysis of mechanism of small molecule IAP inhibitors J. Biol. Chem. 279 2004 48168 48176
60. C. Woenckhaus, S. Maile, S. Uffmann, M. Bansemir, T. Dittberner, M. Poetsch, and J. Giebel Expression of Skp2 and p27KIP1 in naevi and malignant melanoma of the skin and its relation to clinical outcome Histol. Histopathol. 20 2005 501 508
61. J.J. Wright Combination therapy of bortezomib with novel targeted agents: an emerging treatment strategy Clin. Cancer Res. 16 2010 4094 4104
62. Z.K. Yu, J.L. Gervais, and H. Zhang Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins Proc. Natl. Acad. Sci. USA 95 1998 11324 11329