Peptidyl-prolyl isomerase Pin1 controls down-regulation of conventional protein kinase C isozymes

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 13262-13278

  Abrahamsen, Hilde ^a,b   O'Neill, Audrey K ^a   Kannan, Natarajan ^a,c   Kruse, Nicole ^a   Taylor, Susan S ^a   Jennings, Patricia A ^a   Newton, Alexandra C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF OSLO   (Norway)

^c University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOWN-REGULATION; HYDROPHOBIC MOTIFS; ISOMERASES; PEPTIDE BONDS; PEPTIDYL-PROLYL ISOMERASE; PHORBOL ESTERS; PHOSPHORYLATION SITES; PHYSIOLOGICAL AGONISTS; PROTEIN KINASE C;

ESTERS; HYDROPHOBICITY; PHOSPHORYLATION;

ISOENZYMES;

ISOENZYME; PEPTIDYLPROLYL ISOMERASE PIN1; PHORBOL ESTER; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA;

ANIMAL CELL; ARTICLE; BIOCATALYSIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; HYDROPHOBICITY; ISOMERIZATION; MOLECULAR DOCKING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; BOMBESIN; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; FIBROBLASTS; HELA CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; ISOENZYMES; MICE; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; NEUROTRANSMITTER AGENTS; PEPTIDYLPROLYL ISOMERASE; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-DELTA; PROTEIN-SERINE-THREONINE KINASES; RATS; SUBSTRATE SPECIFICITY; UBIQUITINATION;

EID: 84859765114     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349753     Document Type: Article

References (66)

1. 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 (Pubitemid 40637396)
2. Lu, K. P., Hanes, S. D., and Hunter, T. (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380, 544-547 (Pubitemid 26111332)
3. 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 (Pubitemid 28013239)
4. Lu, K. P. (2004) Pinning down cell signaling, cancer and Alzheimer's disease. Trends Biochem. Sci. 29, 200-209
5. Liou, Y. C., Sun, A., Ryo, A., Zhou, X. Z., Yu, Z. X., Huang, H. K., Uchida, T., Bronson, R., Bing, G., Li, X., Hunter, T., and Lu, K. P. (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424, 556-561 (Pubitemid 36975777)
6. 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 (Pubitemid 32634353)
7. Ryo, A., Nakamura, M., Wulf, G., Liou, Y. C., and Lu, K. P. (2001) Pin1 regulates turnover and subcellular localization of β-catenin by inhibiting its interaction with APC. Nat. Cell Biol. 3, 793-801 (Pubitemid 32842684)
8. 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 (Pubitemid 37255170)
9. 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 (Pubitemid 38529775)
10. Yeh, E. S., and Means, A. R. (2007) PIN1, the cell cycle and cancer. Nat. Rev. Cancer 7, 381-388 (Pubitemid 46652482)
11. Chen, D., Purohit, A., Halilovic, E., Doxsey, S. J., and Newton, A. C. (2004) Centrosomal anchoring of protein kinase C βII by pericentrin controls microtubule organization, spindle function, and cytokinesis. J. Biol. Chem. 279, 4829-4839 (Pubitemid 38199078)
12. Levin, D. E., Fields, F. O., Kunisawa, R., Bishop, J. M., and Thorner, J. (1990) A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62, 213-224
13. Yang, C., and Kazanietz, M. G. (2003) Divergence and complexities in DAGsignaling: looking beyond PKC. Trends Pharmacol. Sci. 24, 602-608 (Pubitemid 37357145)
14. Sedwick, C. E., and Altman, A. (2004) Perspectives on PKCθ in T cell activation. Mol. Immunol. 41, 675-686
15. Newton, A. C. (2003) Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem. J. 370, 361-371
16. Newton, A. C. (2010) Protein kinase C: poised to signal. Am. J. Physiol. Endocrinol. Metab. 298, E395-E402
17. Dutil, E. M., Toker, A., and Newton, A. C. (1998) Regulation of conventional protein kinase C isozymes by phosphoinositide-dependent kinase 1 (PDK-1). Curr. Biol. 8, 1366-1375 (Pubitemid 29020145)
18. Le Good, J. A., Ziegler, W. H., Parekh, D. B., Alessi, D. R., Cohen, P., and Parker, P. J. (1998) Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281, 2042-2045 (Pubitemid 28475494)
19. Sonnenburg, E. D., Gao, T., and Newton, A. C. (2001) The phosphoinositide- dependent kinase, PDK-1, phosphorylates conventional protein kinase C isozymes by a mechanism that is independent of phosphoinositide 3-kinase. J. Biol. Chem. 276, 45289-45297
20. Dutil, E. M., and Newton, A. C. (2000) Dual role of pseudosubstrate in the coordinated regulation of protein kinase C by phosphorylation and diacylglycerol. J. Biol. Chem. 275, 10697-10701 (Pubitemid 30202138)
21. Gao, T., Toker, A., and Newton, A. C. (2001) The carboxyl terminus of protein kinase C provides a switch to regulate its interaction with the phosphoinositide-dependent kinase, PDK-1. J. Biol. Chem. 276, 19588-19596
22. Chou, M. M., Hou, W., Johnson, J., Graham, L. K., Lee, M. H., Chen, C. S., Newton, A. C., Schaffhausen, B. S., and Toker, A. (1998) Regulation of protein kinase Cζ by PI 3-kinase and PDK-1. Curr. Biol. 8, 1069-1077 (Pubitemid 28451031)
23. Facchinetti, V., Ouyang, W., Wei, H., Soto, N., Lazorchak, A., Gould, C., Lowry, C., Newton, A. C., Mao, Y., Miao, R. Q., Sessa, W. C., Qin, J., Zhang, P., Su, B., and Jacinto, E. (2008) The mammalian target of rapamycin complex 2 controls folding and stability of Akt and protein kinase C. EMBO J. 27, 1932-1943
24. Ikenoue, T., Inoki, K., Yang, Q., Zhou, X., and Guan, K. L. (2008) Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling. EMBO J. 27, 1919-1931
25. Oh, W. J., Wu, C. C., Kim, S. J., Facchinetti, V., Julien, L. A., Finlan, M., Roux, P. P., Su, B., and Jacinto, E. (2010) mTORC2 can associate with ribosomes to promote cotranslational phosphorylation and stability of nascent Akt polypeptide. EMBO J. 29, 3939-3951
26. Behn-Krappa, A., and Newton, A. C. (1999) The hydrophobic phosphorylation motif of conventional protein kinase C is regulated by autophosphorylation. Curr. Biol. 9, 728-737 (Pubitemid 29350851)
27. Edwards, A. S., Faux, M. C., Scott, J. D., and Newton, A. C. (1999) Carboxyl- terminal phosphorylation regulates the function and subcellular localization of protein kinase C βII. J. Biol. Chem. 274, 6461-6468 (Pubitemid 29111061)
28. Bornancin, F., and Parker, P. J. (1996) Phosphorylation of threonine 638 critically controls the dephosphorylation and inactivation of protein kinase Cα. Curr. Biol. 6, 1114-1123 (Pubitemid 26368745)
29. Goode, N. T., Hajibagheri, M. A., and Parker, P. J. (1995) Protein kinase C (PKC)-induced PKC down-regulation. Association with up-regulation of vesicle traffic. J. Biol. Chem. 270, 2669-2673
30. Lee, H. W., Smith, L., Pettit, G. R., and Bingham Smith, J. (1996) Dephosphorylation of activated protein kinase C contributes to downregulation by bryostatin. Am. J. Physiol. Cell Physiol. 271, C304-C311 (Pubitemid 26298805)
31. Lee, H. W., Smith, L., Pettit, G. R., and Smith, J. B. (1997) Bryostatin 1 and phorbol ester down-modulate protein kinase C-α and -ε via the ubiquitin/proteasome pathway in human fibroblasts. Mol. Pharmacol. 51, 439-447 (Pubitemid 27118480)
32. Lu, Z., Liu, D., Hornia, A., Devonish, W., Pagano, M., and Foster, D. A. (1998) Activation of protein kinase C triggers its ubiquitination and degradation. Mol. Cell Biol. 18, 839-845 (Pubitemid 28063417)
33. Jaken, S., Tashjian, A. H., Jr., and Blumberg, P. M. (1981) Characterization of phorbol ester receptors and their down-modulation in GH4C1 rat pituitary cells. Cancer Res. 41, 2175-2181 (Pubitemid 11111412)
34. Dutil, E. M., Keranen, L. M., DePaoli-Roach, A. A., and Newton, A. C. (1994) In vivo regulation of protein kinase C by trans-phosphorylation followed by autophosphorylation. J. Biol. Chem. 269, 29359-29362 (Pubitemid 24365074)
35. Warfel, N. A., and Newton, A. C. (2012) Pleckstrin homology domain leucine-rich repeat protein phosphatase (PHLPP): a new player in cell signaling. J. Biol. Chem. 287, 3610-3616
36. Gao, T., Brognard, J., and Newton, A. C. (2008) The phosphatase PHLPP controls the cellular levels of protein kinase C. J. Biol. Chem. 283, 6300-6311
37. Keranen, L. M., Dutil, E. M., and Newton, A. C. (1995) Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr. Biol. 5, 1394-1403 (Pubitemid 3008935)
38. Hansra, G., Bornancin, F., Whelan, R., Hemmings, B. A., and Parker, P. J. (1996) 12-O-Tetradecanoylphorbol-13-acetate-induced dephosphorylation of protein kinase Cα correlates with the presence of a membrane-associated protein phosphatase 2A heterotrimer. J. Biol. Chem. 271, 32785-32788
39. Hansra, G., Garcia-Paramio, P., Prevostel, C., Whelan, R. D., Bornancin, F., and Parker, P. J. (1999) Multisite dephosphorylation and desensitization of conventional protein kinase C isotypes. Biochem. J. 342, 337-344 (Pubitemid 29425355)
40. Leontieva, O. V., and Black, J. D. (2004) Identification of two distinct pathways of protein kinase Cα down-regulation in intestinal epithelial cells. J. Biol. Chem. 279, 5788-5801 (Pubitemid 38220610)
41. Gao, T., and Newton, A. C. (2002) The turn motif is a phosphorylation switch that regulates the binding of Hsp70 to protein kinase C. J. Biol. Chem. 277, 31585-31592 (Pubitemid 34968961)
42. Gao, T., and Newton, A. C. (2006) Invariant Leu preceding turn motif phosphorylation site controls the interaction of protein kinase C with Hsp70. J. Biol. Chem. 281, 32461-32468 (Pubitemid 46036801)
43. Edwards, A. S., and Newton, A. C. (1997) Phosphorylation at conserved carboxyl-terminal hydrophobic motif regulates the catalytic and regulatory domains of protein kinase C. J. Biol. Chem. 272, 18382-18390 (Pubitemid 27306431)
44. Cenni, V., Dppler, H., Sonnenburg, E. D., Maraldi, N., Newton, A. C., and Toker, A. (2002) Regulation of novel protein kinase Cε by phosphorylation. Biochem. J. 363, 537-545 (Pubitemid 34526374)
45. Kramer, A., and Schneider-Mergener, J. (1998) Synthesis and screening of peptide libraries on continuous cellulose membrane supports. Methods Mol. Biol. 87, 25-39
46. Amarzguioui, M., and Prydz, H. (2004) An algorithm for selection of functional siRNA sequences. Biochem. Biophys. Res. Commun. 316, 1050-1058 (Pubitemid 38369059)
47. 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 (Pubitemid 27513514)
48. Schiene-Fischer, C., Habazettl, J., Schmid, F. X., and Fischer, G. (2002) The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase. Nat. Struct. Biol. 9, 419-424 (Pubitemid 34568785)
49. 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 (Pubitemid 34136494)
50. Uchida, T., Takamiya, M., Takahashi, M., Miyashita, H., Ikeda, H., Terada, T., Matsuo, Y., Shirouzu, M., Yokoyama, S., Fujimori, F., and Hunter, T. (2003) Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol. 10, 15-24 (Pubitemid 36154470)
51. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
52. Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K., and Varshavsky, A. (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243, 1576-1583 (Pubitemid 19090506)
53. Pickart, C. M., and Fushman, D. (2004) Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610-616 (Pubitemid 39535722)
54. 1 and is essential for its activation. J. Biol. Chem. 269, 19578-19584
55. Lu, K. P., Liou, Y. C., and Zhou, X. Z. (2002) Pinning down proline-directed phosphorylation signaling. Trends Cell Biol. 12, 164-172 (Pubitemid 34442238)
56. Grodsky, N., Li, Y., Bouzida, D., Love, R., Jensen, J., Nodes, B., Nonomiya, J., and Grant, S. (2006) Structure of the catalytic domain of human protein kinase C βII complexed with a bisindolylmaleimide inhibitor. Biochemistry 45, 13970-13981 (Pubitemid 44846186)
57. Hauge, C., Antal, T. L., Hirschberg, D., Doehn, U., Thorup, K., Idrissova, L., Hansen, K., Jensen, O. N., Jørgensen, T. J., Biondi, R. M., and Frödin, M. (2007) Mechanism for activation of the growth factor-activated AGC kinases by turn motif phosphorylation. EMBO J. 26, 2251-2261 (Pubitemid 46685864)
58. Szallasi, Z., Smith, C. B., and Blumberg, P. M. (1994) Dissociation of phorbol esters leads to immediate redistribution to the cytosol of protein kinases Cα and Cδ in mouse keratinocytes. J. Biol. Chem. 269, 27159-27162 (Pubitemid 24346526)
59. Yeh, E., Cunningham, M., Arnold, H., Chasse, D., Monteith, T., Ivaldi, G., Hahn, W. C., Stukenberg, P. T., Shenolikar, S., Uchida, T., Counter, C. M., Nevins, J. R., Means, A. R., and Sears, R. (2004) A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat. Cell Biol. 6, 308-318 (Pubitemid 38584820)
60. Ryo, A., Suizu, F., Yoshida, Y., Perrem, K., Liou, Y. C., Wulf, G., Rottapel, R., Yamaoka, S., and Lu, K. P. (2003) Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12, 1413-1426 (Pubitemid 38037011)
61. Mantovani, F., Piazza, S., Gostissa, M., Strano, S., Zacchi, P., Mantovani, R., Blandino, G., and Del Sal, G. (2004) Pin1 links the activities of c-Abl and p300 in regulating p73 function. Mol. Cell 14, 625-636 (Pubitemid 38739084)
62. 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 (Pubitemid 35238572)
63. 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 (Pubitemid 35238573)
64. Pinton, P., Rimessi, A., Marchi, S., Orsini, F., Migliaccio, E., Giorgio, M., Contursi, C., Minucci, S., Mantovani, F., Wieckowski, M. R., Del Sal, G., Pelicci, P. G., and Rizzuto, R. (2007) Protein kinase Cβ and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 315, 659-663 (Pubitemid 46214712)
65. Shen, Z. J., Esnault, S., Rosenthal, L. A., Szakaly, R. J., Sorkness, R. L., Westmark, P. R., Sandor, M., and Malter, J. S. (2008) Pin1 regulates TGF-β1 production by activated human and murine eosinophils and contributes to allergic lung fibrosis. J. Clin. Investig. 118, 479-490 (Pubitemid 351206539)
66. Lahn, M., Kohler, G., Sundell, K., Su, C., Li, S., Paterson, B. M., and Bumol, T. F. (2004) Protein kinase Cα expression in breast and ovarian cancer. Oncology 67, 1-10 (Pubitemid 39370344)