A Selective, Cell-Permeable Nonphosphorylated Bicyclic Peptidyl Inhibitor against Peptidyl-Prolyl Isomerase Pin1

Journal of Medicinal Chemistry

Volumn 58, Issue 15, 2015, Pages 6306-6312

  Jiang, Bisheng ^a   Pei, Dehua ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; MALTOSE BINDING PROTEIN; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN INHIBITOR; BICYCLO COMPOUND; ENZYME INHIBITOR; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYST; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DESIGN; DRUG EFFECT; DRUG POTENCY; DRUG SCREENING; DRUG SYNTHESIS; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; MAMMAL CELL; METABOLIC STABILITY; PEPTIDE LIBRARY; PROTEIN HYDROLYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ANALYSIS; ANTAGONISTS AND INHIBITORS; HELA CELL LINE; PHOSPHORYLATION;

BICYCLO COMPOUNDS; CELL MEMBRANE PERMEABILITY; ENZYME INHIBITORS; HELA CELLS; HUMANS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION;

EID: 84939188830     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/acs.jmedchem.5b00411     Document Type: Article

References (39)

1. Yaffe, M. B.; Schutkowski, M.; Shen, M. H.; Zhou, X. Z.; Stukenberg, P. T.; Rahfeld, J. U.; Xu, J.; Kuang, J.; Kirschner, M. W.; Fischer, G.; Cantley, L. C.; Lu, K. P. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism Science 1997, 278, 1957-1960 10.1126/science.278.5345.1957
2. Schutkowski, M.; Bernhardt, A.; Zhou, X. Z.; Shen, M.; Reimer, U.; Rahfeld, J. U.; Lu, K. P.; Fischer, G. Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition Biochemistry 1998, 37, 5566-5575 10.1021/bi973060z
3. Fischer, G.; Aumuller, T. Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes Rev. Physiol. Biochem. Pharmacol. 2004, 148, 105-150 10.1007/s10254-003-0011-3
4. Lu, P. J.; Zhou, X. Z.; Shen, M. H.; Lu, K. P. Function of WW domains as phosphoserine- or phosphothreonine-binding modules Science 1999, 283, 1325-1328 10.1126/science.283.5406.1325
5. Verdecia, M.; Bowman, M.; Lu, K. P.; Hunter, T.; Noel, J. P. Structural basis for phosphoserine-proline recognition by group IV WW domains Nat. Struct. Biol. 2000, 7, 639-643 10.1038/77929
6. Lu, K. P.; Zhou, X. Z. The prolyl isomerase Pin1: a pivotal new twist in phosphorylation signaling and disease Nat. Rev. Mol. Cell Biol. 2007, 8, 904-916 10.1038/nrm2261
7. Liou, Y. C.; Ryo, A.; Huang, H. K.; Lu, P. J.; Bronson, R.; Fujimori, F.; Uchida, T.; Hunter, T.; Lu, K. P. Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 1335-1340 10.1073/pnas.032404099
8. Yu, Q.; Geng, Y.; Sicinski, P. Specific protection against breast cancers by cyclin D1 ablation Nature 2001, 411, 1017-1021 10.1038/35082500
9. Yeh, E. S.; Lew, B. O.; Means, A. R. The loss of Pin1 deregulates cyclin E and sensitizes mouse embryo fibroblasts to genomic instability J. Biol. Chem. 2006, 281, 241-251 10.1074/jbc.M505770200
10. Wulf, G. M.; Ryo, A.; Wulf, G. G.; Lee, S. W.; Niu, T. H.; Petkova, V.; Lu, K. P. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1 EMBO J. 2001, 20, 3459-3472 10.1093/emboj/20.13.3459
11. Monje, P.; Hernandez-Losa, J.; Lyons, R. J.; Castellone, M. D.; Gutkind, J. S. Regulation of the transcriptional activity of c-Fos by ERK: a novel role for the prolyl isomerase Pin1 J. Biol. Chem. 2005, 280, 35081-35084 10.1074/jbc.C500353200
12. Ryo, A.; Suizu, F.; Yoshida, Y.; Perrem, K.; Liou, Y. C.; Wulf, G.; Rottapel, R.; Yamaoka, S.; Lu, K. P. Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitinmediated proteolysis of p65/RelA Mol. Cell 2003, 12, 1413-1426 10.1016/S1097-2765(03)00490-8
13. Crenshaw, D. G.; Yang, J.; Means, A. R.; Kornbluth, S. The mitotic peptidyl-prolyl isomerase, Pin1, interacts with Cdc25 and Plx1 EMBO J. 1998, 17, 1315-1327 10.1093/emboj/17.5.1315
14. Stukenberg, P. T.; Kirschner, M. W. Pin1 acts catalytically to promote a conformational change in Cdc25 Mol. Cell 2001, 7, 1071-1083 10.1016/S1097-2765(01)00245-3
15. Okamoto, K.; Sagata, N. Mechanism for inactivation of the mitotic inhibitory kinase Wee1 at M phase Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 3753-3758 10.1073/pnas.0607357104
16. Ryo, A.; Nakamura, N.; Wulf, G.; Liou, Y. C.; Lu, K. P. Pin1 regulates turnover and subcellular localization of β-catenin by inhibiting its interaction with APC Nat. Cell Biol. 2001, 3, 793-801 10.1038/ncb0901-793
17. Ryo, A.; Uemura, H.; Ishiguro, H.; Saitoh, T.; Yamaguchi, A.; Perrem, K.; Kubota, Y.; Lu, K. P.; Aoki, I. Stable suppression of tumorigenicity by Pin1-targeted RNA interference in prostate cancer Clin. Cancer Res. 2005, 11, 7523-7531 10.1158/1078-0432.CCR-05-0457
18. Lu, K. P.; Hanes, S. D.; Hunter, T. A human peptidyl-prolyl isomerase essential for regulation of mitosis Nature 1996, 380, 544-547 10.1038/380544a0
19. Winkler, K. E.; Swenson, K. I.; Kornbluth, S.; Means, A. R. Requirement of the prolyl isomerase Pin1 for the replication checkpoint Science 2000, 287, 1644-1647 10.1126/science.287.5458.1644
20. Driver, J. A.; Lu, K. P. Pin1: a new genetic link between Alzheimer's disease, cancer and aging Curr. Aging Sci. 2010, 3, 158-165 10.2174/1874609811003030158
21. Hennig, L.; Christner, C.; Kipping, M.; Schelbert, B.; Rucknagel, K. P.; Grabley, S.; Kullertz, G.; Fischer, G. Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone Biochemistry 1998, 37, 5953-5960 10.1021/bi973162p
22. Uchida, T.; Takamiya, M.; Takahashi, M.; Miyashita, H.; Ikeda, H.; Terada, T.; Matsuo, Y.; Shirouzu, M.; Yokoyama, S.; Fujimori, F.; Hunter, T. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation Chem. Biol. 2003, 10, 15-24 10.1016/S1074-5521(02)00310-1
23. Tatara, Y.; Lin, Y.-C.; Bamba, Y.; Mori, T.; Uchida, T. Dipentamethylene thiuram monosulfide is a novel inhibitor of Pin1 Biochem. Biophys. Res. Commun. 2009, 384, 394-398 10.1016/j.bbrc.2009.04.144
24. Mori, T.; Hidaka, M.; Lin, Y. C.; Yoshizawa, I.; Okabe, T.; Egashira, S.; Kojima, H.; Nagano, T.; Koketsu, M.; Takamiya, M.; Uchida, T. A high-throughput screen for inhibitors of the prolyl isomerase, Pin1, identifies a seaweed polyphenol that reduces adipose cell differentiation Biochem. Biophys. Res. Commun. 2011, 406, 439-447 10.1016/j.bbrc.2011.02.066
25. Moore, J.; Potter, A. Pin1 inhibitors: pitfalls, progress and cellular pharmacology Bioorg. Med. Chem. Lett. 2013, 23, 4283-4291 10.1016/j.bmcl.2013.05.088
26. Bayer, E.; Thutewohl, M.; Christner, C.; Tradler, T.; Osterkamp, F.; Waldmann, H.; Bayer, P. Identification of hPin1 inhibitors that induce apoptosis in a mammalian Ras transformed cell line Chem. Commun. 2005, 516-518 10.1039/b414037k
27. Wildemann, D.; Erdmann, F.; Alvarez, B. H.; Stoller, G.; Zhou, X. Z.; Fanghanel, J.; Schutkowski, M.; Lu, K. P.; Fischer, G. Nanomolar inhibitors of the peptidyl prolyl cis/trans isomerase Pin1 from combinatorial peptide libraries J. Med. Chem. 2006, 49, 2147-2150 10.1021/jm060036n
28. Guo, C.; Hou, X.; Dong, L.; Marakovits, J.; Greasley, S.; Dagostino, E.; Ferre, R.; Johnson, M. C.; Humphries, P. S.; Li, H.; Paderes, G. D.; Piraino, J.; Kraynov, E.; Murray, B. W. Structure-based design of novel human Pin1 inhibitors (III): optimizing affinity beyond the phosphate recognition pocket Bioorg. Med. Chem. Lett. 2014, 24, 4187-4191 10.1016/j.bmcl.2014.07.044
29. Duncan, K. E.; Dempsey, B. R.; Killip, L. E.; Adams, J.; Bailey, M. L.; Lajoie, G. A.; Litchfield, D. W.; Brandl, C. J.; Shaw, G. S.; Shilton, B. H. Discovery and characterization of a nonphosphorylated cyclic peptide inhibitor of the peptidylprolyl isomerase, Pin1 J. Med. Chem. 2011, 54, 3854-3865 10.1021/jm200156c
30. Xu, G. G.; Slebodnick, C.; Etzkorn, F. A. Cyclohexyl ketone inhibitors of Pin1 dock in a trans-diaxial cyclohexane conformation PLoS One 2012, 7, e44226 10.1371/journal.pone.0044226
31. Liu, T.; Liu, Y.; Kao, H.; Pei, D. Membrane permeable cyclic peptidyl inhibitors against human peptidyl-prolyl isomerase pin1 J. Med. Chem. 2010, 53, 2494-2501 10.1021/jm901778v
32. Lian, W.; Jiang, B.; Qian, Z.; Pei, D. Cell-permeable bicyclic peptide inhibitors against intracellular proteins J. Am. Chem. Soc. 2014, 136, 9830-9833 10.1021/ja503710n
33. Lian, W. L.; Upadhyaya, P.; Rhodes, C.; Liu, Y.; Pei, D. Screening bicyclic peptide libraries for protein-protein interaction inhibitors: discovery of a rumor necrosis factor-α antagonist J. Am. Chem. Soc. 2013, 135, 11990-11995 10.1021/ja405106u
34. Shen, M.; Stukenberg, P. T.; Kirschner, M. W.; Lu, K. P. The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins Genes Dev. 1998, 12, 706-720 10.1101/gad.12.5.706
35. Joo, S. H.; Xiao, Q.; Ling, Y.; Gopishetty, B.; Pei, D. High-throughput sequence determination of cyclic peptide library members by partial Edman degradation/mass spectrometry J. Am. Chem. Soc. 2006, 128, 13000-13009 10.1021/ja063722k
36. Kofron, J. L.; Kuzmic, P.; Kishore, V.; Colonbonilla, E.; Rich, D. H. Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay Biochemistry 1991, 30, 6127-6134 10.1021/bi00239a007
37. Hansen, M. B.; Nielsen, S. E.; Berg, K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill J. Immunol. Methods 1989, 119, 203-210 10.1016/0022-1759(89)90397-9
38. Reineke, E. L.; Lam, M.; Liu, O.; Liu, Y.; Stanya, K. J.; Chang, K. S.; Means, A. R.; Kao, H. Y. Degradation of the tumor suppressor PML by Pin1 contributes to the cancer phenotype of breast cancer MDA-MB-231 cells Mol. Cell. Biol. 2008, 28, 997-1006 10.1128/MCB.01848-07
39. Reineke, E. L.; Lam, M.; Liu, O.; Liu, Y.; Stanya, K. J.; Chang, K. S.; Means, A. R.; Kao, H. Y. Degradation of the tumor suppressor PML by Pin1 contributes to the cancer phenotype of breast cancer MDA-MB-231 cells Mol. Cell. Biol. 2008, 28, 997-1006 10.1128/MCB.01848-07