Structural basis for high-affinity peptide inhibition of human Pin1

ACS Chemical Biology

Volumn 2, Issue 5, 2007, Pages 320-328

  Zhang, Yan ^a   Daum, Sebastian ^b   Wildermann, Dirk ^b   Zhou, Xiao Zhen ^c   Verdecia, Mark A ^a   Bowman, Marianne E ^a   Lücke, Christian ^b   Hunter, Tony ^d   Lu, Kun Ping ^c   Fischer, Gunter ^b   Noel, Joseph P ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE DERIVATIVE; PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE PIN1; PEPTIDYLPROLYL ISOMERASE PIN1 INHIBITOR; POLYKETIDE; PROTEIN INHIBITOR; RAPAMYCIN; TACROLIMUS; UNCLASSIFIED DRUG; ENZYME INHIBITOR; LIGAND; NIMA INTERACTING PEPTIDYLPROLYL ISOMERASE; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; OLIGOPEPTIDE; PEPTIDE LIBRARY;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG STRUCTURE; DRUG SYNTHESIS; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ENZYME SPECIFICITY; HUMAN; ISOMERISM; STRUCTURE ACTIVITY RELATION; SYNTHESIS;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENZYME INHIBITORS; HUMANS; ISOMERISM; LIGANDS; MODELS, MOLECULAR; OLIGOPEPTIDES; PEPTIDE LIBRARY; PEPTIDYLPROLYL ISOMERASE; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 34347384233     PISSN: 15548929     EISSN: None     Source Type: Journal    
DOI: 10.1021/cb7000044     Document Type: Article

References (55)

1. Schmid, F. X. (1995) Protein folding. Prolyl isomerases join the fold, Curr. Biol. 5, 993-994.
2. Edlich, F., and Fischer, G. (2006) Pharmacological targeting of catalyzed protein folding: the example of peptide bond cis/trans isomerases, Handb. Exp. Pharmacol. 172, 359-404.
3. Lu, K. P., Suizu, F., Zhou, X. Z., Finn, G., Lam, P., and Wulf, G. (2006) Targeting carcinogenesis: a role for the prolyl isomerase Pin1? Mol. Carcinog. 45, 397-402.
4. Etzkorn, F. A. (2006) Pint flips Alzheimer's switch, ACS Chem. Biol. 1, 214-216.
5. Handschumacher, R. E., Harding, M. W., Rice, J., Drugge, R. J., and Speicher, D. W. (1984) Cyclophilin: a specific cytosolic binding protein for cyclosporin A, Science 226, 544-547.
6. Harding, M. W., Galat, A., Uehling, D. E., and Schreiber, S. L. (1989) A receptor for the immunosuppressant FK506 is a cis-trans peptidylprolyl isomerase, Nature 341, 758-760.
7. Rahfeld, J. U., Schierhorn, A., Mann, K., and Fischer, G. (1994) A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli, FEBS Lett. 343, 65-69.
8. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F. X. (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins, Nature 337, 476-478.
9. Takahashi, N., Hayano, T., and Suzuki, M. (1989) Peptidyl-prolyl cistrans isomerase is the cyclosporin A-binding protein cyclophilin, Nature 337, 473-475.
10. Siekierka, J. J., Hung, S. H., Poe, M., Lin, C. S., and Sigal, N. H. (1989) A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin, Nature 341, 755-757.
11. Lu, K. P., Hanes, S. D., and Hunter, T. (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis, Nature 380, 544-547.
12. Ranganathan, R., Lu, K. P., Hunter, T., and Noel, J. P. (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent, Cell 89, 875-886.
13. Lu, K. P., Liou, Y. C., and Zhou, X. Z. (2002) Pinning down proline-directed phosphorylation signaling, Trends Cell Biol. 12, 164-172.
14. Wulf, G., Finn, G., Suizu, F., and Lu, K. P. (2005) Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat. Cell Biol. 7, 435-441.
15. Liou, Y. C., Ryo, A., Huang, H. K., Lu, P. J., Bronson, R., Fujimori, F., Uchida, T., Hunter, T., and Lu, K. P. (2002) Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes, Proc. Natl. Acad. Sci. U.S.A. 99, 1335-1340.
16. Wulf, G. M., Ryo, A., Wulf, G. G., Lee, S. W., Niu, T., Petkova, V., and Lu, K. P. (2001) Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1, EMBO J. 20, 3459-3472.
17. Dominguez-Sola, D., and Dalla-Favera, R. (2004) PINning down the c-Myc oncoprotein, Nat. Cell Biol. 6, 288-289.
18. Ryo, A., Nakamura, M., Wulf, G., Liou, Y. C., and Lu, K. P. (2001) Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC, Nat. Cell Biol. 3, 793-801.
19. Zheng, H., You, H., Zhou, X. Z., Murray, S. A., Uchida, T., Wulf, G., Gu, L., Tang, X., Lu, K. P., and Xiao, Z. X. (2002) The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response, Nature 419, 849-853.
20. Zacchi, P., Gostissa, M., Uchida, T., Salvagno, C., Avolio, F., Volinia, S., Ronai, Z., Blandino, G., Schneider, C., and Del Sal, G. (2002) The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults, Nature 419, 853-857.
21. Lu, P. J., Zhou, X. Z., Shen, M., and Lu, K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules, Science 283, 1325-1328.
22. Verdecia, M. A., Bowman, M. E., Lu, K. P., Hunter, T., and Noel, J. P. (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains, Nat. Struct. Biol. 7, 639-643.
23. Yaffe, M. B., Schutkowski, M., Shen, M., Zhou, X. Z., Stukenberg, P. T., Rahfeld, J. U., Xu, J., Kuang, J., Kirschner, M. W., Fischer, G., Cantley, L. C., and Lu, K. P. (1997) Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism, Science 278, 1957-1960.
24. Zhou, X. Z., Kops, O., Werner, A., Lu, P. J., Shen, M., Stoller, G., Kullertz, G., Stark, M., Fischer, G., and Lu, K. P. (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins, Mol. Cell 6, 873-883.
25. Stukenberg, P. T., and Kirschner, M. W. (2001) Pin1 acts catalytically to promote a conformational change in Cdc25, Mol. Cell 7, 1071-1083.
26. Sears, R. C. (2004) The life cycle of c-myc: from synthesis to degradation, Cell Cycle 3, 1333-1137.
27. Bao, L., Kimzey, A., Sauter, G., Sowadski, J. M., Lu, K. P., and Wang, D. G. (2004) Prevalent overexpression of prolyl isomerase Pin1 in human cancers, Am. J. Pathol. 164, 1727-1737.
28. Kim, C. J., Cho, Y. G., Park, Y. G., Nam, S. W., Kim, S. Y., Lee, S. H., Yoo, N. J., Lee, J. Y., and Park, W. S. (2005) Pin1 overexpression in colorectal cancer and its correlation with aberrant beta-catenin expression, World J. Gastroenterol. 11, 5006-5009.
29. Ayala, G., Wang, D., Wulf, G., Frolov, A., Li, R., Sowadski, J., Wheeler, T. M., Lu, K. P., and Bao, L. (2003) The prolyl isomerase Pin1 is a novel prognostic marker in human prostate cancer, Cancer Res. 63, 6244-6251.
30. Nakashima, M., Meirmanov, S., Naruke, Y., Kondo, H., Saenko, V., Rogounovitch, T., Shimizu-Yoshida, Y., Takamura, N., Namba, H., Ito, M., Abrosimov, A., Lushnikov, E., Roumiantsev, P., Tsyb, A., Yamashita, S., and Sekine, I. (2004) Cyclin D1 overexpression in thyroid tumours from a radio-contaminated area and its correlation with Pin1 and aberrant beta-catenin expression, J. Pathol. 202, 446-455.
31. Rippmann, J. F., Hobbie, S., Daiber, C., Guilliard, B., Bauer, M., Birk, J., Nar, H., Garin-Chesa, P., Rettig, W. J., and Schnapp, A. (2000) Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis, Cell Growth Differ. 11, 409-416.
32. Ryo, A., Uemura, H., Ishiguro, H., Saitoh, T., Yamaguchi, A., Perrem, K., Kubota, Y., Lu, K. P., and Aoki, I. (2005) Stable suppression of tumorigenicity by Pin1-targeted RNA interference in prostate cancer, Clin. Cancer Res. 11, 7523-7531.
33. Wulf, G., Garg, P., Liou, Y. C., Iglehart, D., and Lu, K. P. (2004) Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis, EMBO J. 23, 3397-3407.
34. Suizu, F., Ryo, A., Wulf, G., Lim, J., and Lu, K. P. (2006) Pin1 regulates centrosome duplication, and its overexpression induces centrosome amplification, chromosome instability, and oncogenesis, Mol. Cell Biol. 26, 1463-1479.
35. Wildemann, D., Erdmann, F., Alvarez, B. H., Stoller, G., Zhou, X. Z., Fanghanel, J., Schutkowski, M., Lu, K. P., and Fischer, C. (2006) Nanomolar inhibitors of the peptidyl prolyl cis/trans inomerase Pin1 from combinatorial peptide libraries, J. Med. Chem. 49, 2147-2150.
36. Schiene, C., Reimer, U., Schutkowski, M., and Fischer, G. (1998) Mapping the stereospecificity of peptidyl prolyl cis/trans isomerases, FEBS Lett. 432, 202-206.
37. Zhang, Y., Fussel, S., Reimer, U., Schutkowski, M., and Fischer, G. (2002) Substrate-based design of reversible Pin1 inhibitors, Biochemistry 41, 11868-11877.
38. Andrews, D. M., Kitchin, J., and Seale, P. W. (1991) Solid-phase synthesis of a range of O-phosphorylated peptides by pont-assembly phosphitylation and oxidation, Int. J. Pept. Protein Res. 38, 469-475.
39. Perich, J. W., and Reynolds, E. C. (1991) Fmoc/solid-phase synthesis of Tyr(P)-containing peptides through t-butyl phosphate protection, Int. J. Pept. Protein Res. 37, 572-575.
40. Perich, J. W., Ruzzene, M., Pinna, L. A., and Reynolds, E. C. (1994) Efficient Fmoc/solid-phase peptide synthesis of O-phosphotyrosyl-containing peptides and their use as phosphatase substrates, Int. J. Pept. Protein Res. 43, 39-46.
41. Orford, K., Crockett, C., Jensen, J. P., Weissman, A. M., and Byers, S. W. (1997) Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin, J. Biol. Chem. 272, 24735-24738.
42. Janowski, B., Wollner, S., Schutkowski, M., and Fischer, G. (1997) A protease-free assay for peptidyl prolyl cis/trans inomerasen using standard peptide substrates, Anal Biochem 252, 299-307.
43. Kofron, J. L., Kuzmic, P., Kishore, V., Colon-Bonilla, E., and Rich, D. H. (1991) Determination of kinetic constants for peptidyl prolyl cistrans isomerases by an improved spectrophotometric assay, Biochemistry 30, 6127-6134.
44. Carcia-Echeverria, C., Kofron, J. L., Kuzmic, P., and Rich, D. H. (1993) A continuous spectrophotometric direct assay for peptidyl prolyl cis-trans isomerases, Biochem. Biophys. Res. Commun. 191, 70-75.
45. Otwinowski, Z., and Minor, W. (1997) HKL: processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
46. Navaza, J. (1994) AMoRe: an automated package for molecular replacement, Acta Crystallogr. A50, 157-163.
47. CCP4 (1994) Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D50, 760-763.
48. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, C. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D 54, 905-921.
49. Brunger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures, Nature 355, 472-475.
50. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement, Acta Crystallogr. D57, 122-133.
51. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
52. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
53. DeLano, W. L. (2002) DeLano Scientific, San Canon, CA, USA.
54. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
55. Baine, P. (1986) Comparison of rate constants determined by two-dimensional NMR spectroscopy with rate constants determined by other NMR techniques, Magn. Reson. Chem. 24, 304-307.