High-throughput screening alphascreen assay for identification of small-molecule inhibitors of ubiquitin E3 ligase SCFSkp2-Cks1

Journal of Biomolecular Screening

Volumn 18, Issue 8, 2013, Pages 910-920

  Ungermannova, Dana ^a   Lee, Junglim ^a   Zhang, Gan ^a   Dallmann, H Garry ^a   McHenry, Charles S ^a   Liu, Xuedong ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Cks1; E3 ligase; inhibitor; p27kip1; proteolysis; Skp2; ubiquitin

Indexed keywords

ADAPTOR PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN 2; UBIQUITIN PROTEIN LIGASE E3;

ALPHASCREEN ASSAY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CANCER PROGNOSIS; CELL PROLIFERATION; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HIGH THROUGHPUT SCREENING; IC 50; IN VITRO STUDY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SCREENING; STRUCTURE ACTIVITY RELATION; TUMOR CELL; UBIQUITINATION;

CKS1; E3 LIGASE; INHIBITOR; P27KIP1; PROTEOLYSIS; SKP2; UBIQUITIN;

BENZOATES; CDC2-CDC28 KINASES; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DRUG SCREENING ASSAYS, ANTITUMOR; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; HYDROQUINONES; NEOPLASMS; PARA-AMINOBENZOATES; PROTEIN BINDING; S-PHASE KINASE-ASSOCIATED PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84882353683     PISSN: 10870571     EISSN: 1552454X     Source Type: Journal    
DOI: 10.1177/1087057113485789     Document Type: Article

References (28)

1. Sherr C. J., Roberts J. M.. CDK Inhibitors: Positive and Negative Regulators of G1-phase Progression. Genes Dev. 1999 ; 13: 1501-1512
2. Nakayama K. I., Nakayama K.. Ubiquitin Ligases: Cell-Cycle Control and Cancer. Nat. Rev. Cancer. 2006 ; 6: 369-381
3. Jin J., Cardozo T., Lovering R. C., Elledge S. J., Pagano M., Harper J. W.. Systematic Analysis and Nomenclature of Mammalian F-box Proteins. Genes Dev. 2004 ; 18: 2573-2580
4. Ganoth D., Bornstein G., Ko T. K., Larsen B., Tyers M., Pagano M., Hershko A.. The Cell-Cycle Regulatory Protein Cks1 Is Required for SCF(Skp2)-Mediated Ubiquitination of p27. Nat. Cell Biol. 2001 ; 3: 321-324
5. Spruck C., Strohmaier H., Watson M., Smith A. P., Ryan A., Krek T. W., Reed S. I.. A CDK-Independent Function of Mammalian Cks1: Targeting of SCF(Skp2) to the CDK Inhibitor p27Kip1. Mol. Cell. 2001 ; 7: 639-650
6. Sitry D., Seeliger M. A., Ko T. K., Ganoth D., Breward S. E., Itzhaki L. S., Pagano M., Hershko A.. Three Different Binding Sites of Cks1 Are Required for p27-Ubiquitin Ligation. J. Biol. Chem. 2002 ; 277: 42233-42240
7. Wang W., Ungermannova D., Chen L., Liu X.. Molecular and Biochemical Characterization of the Skp2-Cks1 Binding Interface. J. Biol. Chem. 2004 ; 279: 51362-51369
8. Montagnoli A., Fiore F., Eytan E., Carrano A. C., Draetta G. F., Hershko A., Pagano M.. Ubiquitination of p27 Is Regulated by Cdk-Dependent Phosphorylation and Trimeric Complex Formation. Genes Dev. 1999 ; 13: 1181-1189
9. Ungermannova D., Gao Y., Liu X.. Ubiquitination of p27Kip1 Requires Physical Interaction with Cyclin E and Probable Phosphate Recognition by SKP2. J. Biol. Chem. 2005 ; 280: 30301-30309
10. Hao B., Zheng N., Schulman B. A., Wu G., Miller J. J., Pagano M., Pavletich N. P.. Structural Basis of the Cks1-Dependent Recognition of p27(Kip1) by the SCF(Skp2) Ubiquitin Ligase. Mol. Cell. 2005 ; 20: 9-19
11. Chu I. M., Hengst L., Slingerland J. M.. The Cdk Inhibitor p27 in Human Cancer: Prognostic Potential and Relevance to Anticancer Therapy. Nat. Rev. Cancer. 2008 ; 8: 253-267
12. Pagano M., Benmaamar R.. When Protein Destruction Runs Amok, Malignancy Is on the Loose. Cancer Cell. 2003 ; 4: 251-256
13. Hiramatsu Y., Kitagawa K., Suzuki T., Uchida C., Hattori T., Kikuchi H., Oda T., Hatakeyama S., Nakayama K. I., Yamamoto T., et al. Degradation of Tob1 Mediated by SCFSkp2-Dependent Ubiquitination. Cancer Res. 2006 ; 66: 8477-8483
14. Slingerland J., Pagano M.. Regulation of the Cdk Inhibitor p27 and Its Deregulation in Cancer. J. Cell. Physiol. 2000 ; 183: 10-17
15. Craig C., Wersto R., Kim M., Ohri E., Li Z., Katayose D., Lee S. J., Trepel J., Cowan K., Seth P.. A Recombinant Adenovirus Expressing p27Kip1 Induces Cell Cycle Arrest and Loss of Cyclin-Cdk Activity in Human Breast Cancer Cells. Oncogene. 1997 ; 14: 2283-2289
16. Chen J., Willingham T., Shuford M., Nisen P. D.. Tumor Suppression and Inhibition of Aneuploid Cell Accumulation in Human Brain Tumor Cells by Ectopic Overexpression of the Cyclin-Dependent Kinase Inhibitor p27KIP1. J. Clin. Invest. 1996 ; 97: 1983-1988
17. Wang W., Ungermannova D., Chen L., Liu X.. A Negatively Charged Amino Acid in Skp2 Is Required for Skp2-Cks1 Interaction and Ubiquitination of p27Kip1. J. Biol. Chem. 2003 ; 278: 32390-32396
18. Ullman E. F., Kirakossian H., Singh S., Wu Z. P., Irvin B. R., Pease J., Switchenko A C., Irvine J. D., Dafforn A., Skold C. N., et al. Luminescent Oxygen Channeling Immunoassay: Measurement of Particle Binding Kinetics by Chemiluminescence. Proc. Natl. Acad. Sci. U. S. A. 1994 ; 91: 5426-5430
19. Ullman E. F., Kirakossian H., Switchenko A. C., Ishkanian J., Ericson M., Wartchow C. A., Pirio M., Pease J., Irvin B. R., Singh S., et al. Luminescent Oxygen Channeling Assay (LOCI): Sensitive, Broadly Applicable Homogeneous Immunoassay Method. Clin. Chem. 1996 ; 42: 1518-1526
20. Zheng N., Schulman B. A., Song L., Miller J. J., Jeffrey P. D., Wang P., Chu C., Koepp D. M., Elledge S. J., Pagano M., et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF Ubiquitin Ligase Complex. Nature. 2002 ; 416: 703-709
21. Xu K., Belunis C., Chu W., Weber D., Podlaski F, Huang K. S., Reed S. I., Vassilev L. T.. Protein-Protein Interactions Involved in the Recognition of p27 by E3 Ubiquitin Ligase. Biochem. J. 2003 ; 371: 957-964
22. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H. R., Zhang Y., Wrana J. L.. Regulation of the Polarity Protein Par6 by TGFbeta Receptors Controls Epithelial Cell Plasticity. Science. 2005 ; 307: 1603-1609
23. Kaur G., Narayanan V. L., Risbood P. A., Hollingshead M. G., Stinson S. F., Varma R. K., Sausville E. A.. Synthesis, Structure-Activity Relationship, and p210(bcr-abl) Protein Tyrosine Kinase Activity of Novel AG 957 Analogs. Bioorg. Med. Chem. 2005 ; 13: 1749-1761
24. McGovern S. L., Caselli E., Grigorieff N., Shoichet B. K.. A Common Mechanism Underlying Promiscuous Inhibitors from Virtual and High-Throughput Screening. J. Med. Chem. 2002 ; 45: 1712-1722
25. Feng B. Y., Shelat A., Doman T. N., Guy R. K., Shoichet B. K.. High-Throughput Assays for Promiscuous Inhibitors. Nat. Chem. Biol. 2005 ; 1: 146-148
26. Baell J. B., Holloway G. A.. New Substructure Filters for Removal of Pan Assay Interference Compounds (PAINS) from Screening Libraries and for Their Exclusion in Bioassays. J. Med. Chem. 2010 ; 53: 2719-2740
27. Huang K. S., Vassilev L. T.. High-Throughput Screening for Inhibitors of the Cks1-Skp2 Interaction. Methods Enzymol. 2005 ; 399: 717-728
28. Ungermannova D., Parker S. J., Nasveschuk C. G., Chapnick D. A., Phillips A. J., Kuchta R. D., Liu X.. Identification and Mechanistic Studies of a Novel Ubiquitin E1 Inhibitor. J. Biomol. Screen. 2012 ; 17: 421-434