Molecular mechanisms of the phospho-dependent prolyl cis/trans isomerase Pin1

FEBS Journal

Volumn 274, Issue 20, 2007, Pages 5211-5222

  Lippens, G ^a   Landrieu, I ^a   Smet, C ^b  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b CNRS   (France)

Author keywords

Cell cycle; CKS subunit; Dynamics; Enzyme; Interaction module; Phosphorylation; Pin1; Prolyl cis trans isomerase; Protein degradation; Protein structure

Indexed keywords

PEPTIDYLPROLYL ISOMERASE PIN1; POLYPEPTIDE; PROLINE; SERINE; THREONINE;

BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL CYCLE PROGRESSION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; SHORT SURVEY;

HUMANS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION;

EID: 34848907217     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06057.x     Document Type: Short Survey

References (91)

1. Lang K, Schmid FX Fischer G (1987) Catalysis of protein folding by prolyl isomerase. Nature 329, 268 270.
2. Fischer G, Tradler T Zarnt T (1998) The mode of action of peptidyl prolyl cis/trans isomerases in vivo: binding vs. catalysis. FEBS Lett 426, 17 20.
3. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117 121.
4. Sokolskaja E Luban J (2006) Cyclophilin, TRIM5, and innate immunity to HIV-1. Curr Opin Microbiol 9, 404 408.
5. Bosco DA, Eisenmesser EZ, Pochapsky S, Sundquist WI Kern D (2002) Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc Natl Acad Sci USA 99, 5247 5252.
6. Brazin KN, Mallis RJ, Fulton DB Andreotti AH (2002) Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc Natl Acad Sci USA 99, 1899 1904.
7. Sarkar P, Reichman C, Saleh T, Birge RB Kalodimos CG (2007) Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol Cell 25, 413 426.
8. Dolinski K, Muir S, Cardenas M Heitman J (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94, 13093 13098.
9. Hanes SD, Shank PR Bostian KA (1989) Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae. Yeast 5, 55 72.
10. Lu KP, Hanes SD Hunter T (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380, 544 547.
11. Lu KP (2000) Phosphorylation-dependent prolyl isomerization: a novel cell cycle regulatory mechanism. Prog Cell Cycle Res 4, 83 96.
12. Joseph JD, Yeh ES, Swenson KI, Means AR Winkler. (2003) The peptidyl-prolyl isomerase Pin1. Prog Cell Cycle Res 5, 477 487.
13. Landrieu I, Smet C, Wieruszeski JM, Sambo AV, Wintjens R, Buee L Lippens G (2006) Exploring the molecular function of PIN1 by nuclear magnetic resonance. Curr Protein Pept Sci 7, 179 194.
14. Wulf G, Finn G, Suizu F Lu KP (2005) Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat Cell Biol 7, 435 441.
15. Wulf G, Ryo A, Liou YC Lu KP (2003) The prolyl isomerase Pin1 in breast development and cancer. Breast Cancer Res 5, 76 82.
16. Lu KP (2004) Pinning down cell signaling, cancer and Alzheimer's disease. Trends Biochem Sci 29, 200 209.
17. Butterfield DA, Abdul HM, Opii W, Newman SF, Joshi G, Ansari MA Sultana R (2006) Pin1 in Alzheimer's disease. J Neurochem 98, 1697 1706.
18. Ranganathan R, Lu KP, Hunter T Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89, 875 886.
19. Verdecia MA, Bowman ME, Lu KP, Hunter T Noel JP (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 7, 639 643.
20. Jacobs DM, Saxena K, Vogtherr M, Bernado P, Pons M Fiebig KM (2003) Peptide binding induces large scale changes in inter-domain mobility in human Pin1. J Biol Chem 278, 26174 26182.
21. Bayer E, Goettsch S, Mueller JW, Griewel B, Guiberman E, Mayr LM Bayer P (2003) Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. J Biol Chem 278, 26183 26193.
22. Landrieu I, Wieruszeski JM, Wintjens R, Inze D Lippens G (2002) Solution structure of the single-domain prolyl cis/trans isomerase PIN1At from Arabidopsis thaliana. J Mol Biol 320, 321 332.
23. Li Z, Li H, Devasahayam G, Gemmill T, Chaturvedi V, Hanes SD Van Roey P (2003) Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. J Biol Chem 278, 26183 26193.
24. Namanja AT, Peng T, Zintsmaster JS, Elson AC, Shakour MG Peng JW (2007) Substrate recognition reduces side-chain flexibility for conserved hydrophobic residues in human Pin1. Structure 15, 313 327.
25. Labeikovsky W, Eisenmesser EZ, Bosco DA Kern D (2007) Structure and dynamics of Pin1 during catalysis by NMR. J Mol Biol 367, 1370 1381.
26. Behrsin CD, Bailey ML, Bateman KS, Hamilton KS, Wahl LM, Brandl CJ, Shilton BH Litchfield DW (2007) Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution. J Mol Biol 365, 1143 1162.
27. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J Hanes SD (2000) The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19, 3727 3738.
28. Zhang Y, Daum S, Wildemann D, Zhou XZ, Verdecia MA, Bowman ME, Lücke C, Hunter T, Lu KP, Fischer G et al. (2007) Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. ACS Chem Biol 2, 320 328.
29. Wintjens R, Wieruszeski JM, Drobecq H, Rousselot-Pailley P, Buee L, Lippens G Landrieu I (2001) 1H NMR study on the binding of Pin1 Trp-Trp domain with phosphothreonine peptides. J Biol Chem 276, 25150 25156.
30. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li SH, Li X et al. (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440, 528 534.
31. Ramelot TA Nicholson LK (2001) Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J Mol Biol 307, 871 884.
32. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G et al. (1997) Sequence specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278, 1957 1960.
33. Yeh ES, Lew BO Means AR (2006) The loss of PIN1 deregulates cyclin E and sensitizes mouse embryo fibroblasts to genomic instability. J Biol Chem 281, 241 251.
34. Orlicky S, Tang X, Willems A, Tyers M Sicheri F (2003) Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112, 243 256.
35. van Drogen F, Sangfelt O, Malyukova A, Matskova L, Yeh E, Means AR Reed SI (2006) Ubiquitylation of cyclin E requires the sequential function of SCF complexes containing distinct hCdc4 isoforms. Mol Cell 23, 37 48.
36. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, Mendenhall MD, Sicheri F, Pawson T Tyers M (2001) Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414, 514 521.
37. Smet C, Wieruszeski JM, Buee L, Landrieu I Lippens G (2005) Regulation of Pin1 peptidyl-prolyl cis/trans isomerase activity by its WW binding module on a multi-phosphorylated peptide of Tau protein. FEBS Lett 579, 4159 4164.
38. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41, 6573 6582.
39. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32, 1037 1049.
40. Lu PJ, Wulf G, Zhou XZ, Davies P Lu KP (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399, 784 788.
41. Daly NL, Hoffmann R, Otvos L Jr. Craik DJ (2000) Role of phosphorylation in the conformation of tau peptides implicated in Alzheimer's disease. Biochemistry 39, 9039 9046.
42. Lippens G, Sillen A, Smet C, Wieruszeski JM, Leroy A, Buee L Landrieu I (2006) Studying the natively unfolded neuronal Tau protein by solution NMR spectroscopy. Protein Pept Lett 13, 235 246.
43. Stukenberg PT Kirschner MW (2001) Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 7, 1071 1083.
44. Bielska AA Zondlo NJ (2006) Hyperphosphorylation of tau induces local polyproline II helix. Biochemistry 45, 5527 5537.
45. Davis FM, Tsao TY, Fowler SK Rao PN (1983) Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 80, 2926 2930.
46. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, Kullertz G, Stark M, Fischer G Lu KP (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 6, 873 883.
47. Brown NR, Noble ME, Endicott JA Johnson LN (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1, 438 443.
48. Kofron JL, Kuzmic P, Kishore V, Colon-Bonuilla E Rich D (1991) Determination of kinetic constants for petidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry 30, 6127 6134.
49. Landrieu I, Lacosse L, Leroy A, Wieruszeski JM, Trivelli X, Sillen A, Sibille N, Schwalbe H, Saxena K, Langer T et al. (2006) NMR analysis of a Tau phosphorylation pattern. J Am Chem Soc 128, 3575 3583.
50. Patra D, Wang SX, Kumagai A Dunphy WG (1999) The xenopus Suc1/Cks protein promotes the phosphorylation of G(2)/M regulators. J Biol Chem 274, 36839 36842.
51. Arvai AS, Bourne Y, Hickey MJ Tainer JA (1995) Crystal structure of the human cell cycle protein CksHs1: single domain fold with similarity to kinase N-lobe domain. J Mol Biol 249, 835 842.
52. Bourne Y, Arvai AS, Bernstein SL, Watson MH, Reed SI, Endicott JE, Noble ME, Johnson LN Tainer JA (1995) Crystal structure of the cell cycle-regulatory protein suc1 reveals a beta-hinge conformational switch. Proc Natl Acad Sci USA 92, 10232 10236.
53. Bourne Y, Watson MH, Hickey MJ, Holmes W, Rocque W, Reed SI Tainer JA (1996) Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell 84, 863 874.
54. Suc1 and the WW domain of Pin1 bind to the same phospho-threonine/proline epitope. J Biol Chem 276, 1434 1438.
55. Spruck C, Strohmaier H, Watson M, Smith AP, Ryan A, Krek TW Reed SI (2001) A CDK-independent function of mammalian Cks1: targeting of SCFSkp2 to the CDK inhibitor p27Kip1. Mol Cell 7, 639 650.
56. Ganoth D, Bornstein G, Ko TK, Larsen B, Tyers M, Pagano M Hershko A (2001) The cell-cycle regulatory protein Cks1 is required for SCF (Skp2)-mediated ubiquitinylation of p27. Nat Cell Biol 3, 321 324.
57. Hao B, Zheng N, Schulman BA, Wu G, Miller JJ, Pagano M Pavletich NP (2005) Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase. Mol Cell 20, 9 19.
58. Sudakin V, Shteinberg M, Ganoth D, Hershko J Hershko A (1997) Binding of activated cyclosome to p13(suc1). Use for affinity purification. J Biol Chem 272, 18051 18059.
59. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Petkova V Lu KP (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.
60. Bernis C, Vigneron S, Burgess A, Labbe JC, Fesquet D, Castro A Lorca T (2007) Pin1 stabilizes Emi1 during G2 phase by preventing its association with SCF(βTrcp). EMBO Rep 8, 91 98.
61. Hsu T, McRackan D, Vincent TS Gert de Couet H (2001) Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis. Nat Cell Biol 3, 538 543.
62. Shimura H, Schwartz D, Gygi SP Kosik KS (2004) CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 279, 4869 4876.
63. Murata S, Minami Y, Chiba T Tanaka K (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2, 1133 1138.
64. Seet BT, Dikic I, Zhou MM Pawson T (2006) Reading protein modifications with interaction domains. Nat Rev Mol Cell Biol 7, 473 483.
65. Hani J, Schelbert B, Bernhardt A, Domdey H, Fischer G, Wiebauer K Rahfeld JU (1999) Mutations in a peptidylprolyl-cis/trans-isomerase gene lead to a defect in 3′-end formation of a pre-mRNA in Saccharomyces cerevisiae. J Biol Chem 274, 108 116.
66. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J Hanes SD (2000) The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19, 3727 3738.
67. Morris DP, Phatnani HP Greenleaf AL (1999) Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA-3′-end formation. J Biol Chem 274, 31583 31587.
68. Albert A, Lavoie S Vincent M (1999) A hyperphosphorylated form of RNA polymerase II is the major interphase antigen of the phosphoprotein antibody MPM-2 and interacts with the peptidyl-prolyl isomerase Pin1. J Cell Sci 112, 2493 2500.
69. Myers JK, Morris DP, Greenleaf AL Oas TG (2001) Phosphorylation of RNA polymerase II CTD fragments results in tight binding to the WW domain from the yeast prolyl isomerase Ess1. Biochemistry 40, 8479 8486.
70. Kops O, Zhou XZ Lu KP (2002) Pin1 modulates the dephosphorylation of the RNA polymerase II C-terminal domain by yeast Fcp1. Febs Lett 513, 305 311.
71. Xu YX, Hirose Y, Zhou XZ, Lu KP Manley JL (2003) Pin1 modulates the structure and function of human RNA polymerase II. Genes Dev 17, 2765 2776.
72. Palancade B, Marshall NF, Tremeau-Bravard A, Bensaude O, Dahmus ME Dubois MF (2004) Dephosphorylation of RNA polymerase II by CTD-phosphatase FCP1 is inhibited by phospho-CTD associating proteins. J Mol Biol 335, 415 424.
73. Gemmill TR, Wu X Hanes SD (2005) Vanishingly low levels of Ess1 prolyl-isomerase activity are sufficient for growth in Saccharomyces cerevisiae. J Biol Chem 280, 15510 15517.
74. Wu X, Chang A, Sudol M Hanes SD (2001) Genetic interactions between the ESS1 prolyl-isomerase and the RSP5 ubiquitin ligase reveal opposing effects on RNA polymerase II function. Curr Genet 40, 234 242.
75. Fujimori F, Gunji W, Kikuchi J, Mogi T, Ohashi Y, Makino T, Oyama A, Okuhara K, Uchida T Murakami Y (2001) Crosstalk of prolyl isomerases, Pin1/Ess1, and cyclophilin A. Biochem Biophys Res Commun 289, 181 190.
76. Arevalo-Rodriguez M, Cardenas ME, Wu X, Hanes SD Heitman J (2000) Cyclophilin A and Ess1 interact with and regulate silencing by the Sin3-Rpd3 histone deacetylase. EMBO J 19, 3739 3749.
77. Fanghanel J, Akiyama H, Uchida C Uchida T (2006) Comparative analysis of enzyme activities and mRNA levels of peptidyl prolyl cis/trans isomerases in various organs of wild type and Pin1-/- mice. FEBS Lett 580, 3237 3245.
78. Saitoh T, Tun-Kyi A, Ryo A, Yamamoto M, Finn G, Fujita T, Akira S, Yamamoto N, Lu KP Yamaoka S (2006) Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat Immunol 7, 598 605.
79. Mamane Y, Sharma S, Petropoulos L, Lin R Hiscott J (2000) Posttranslational regulation of IRF-4 activity by the immunophilin FKBP52. Immunity 12, 129 140.
80. Shen ZJ, Esnault S Malter JS (2005) The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat Immunol 6, 1280 1287.
81. Esnault S, Braun RK, Shen ZJ, Xiang Z, Heninger E, Love RB, Sandor M Malter JS (2007) Pin1 modulates the type 1 immune response. PLoS ONE 2, e226 doi:.
82. Lu PJ, Zhou XZ, Liou YC, Noel JP Lu KP (2001) Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J Biol Chem 277, 2381 2384.
83. Eckerdt F, Yuan J, Saxena K, Martin B, Kappel S, Lindenau C, Kramer A, Naumann S, Daum S, Fischer G et al. (2005) Polo-like kinase 1-mediated phosphorylation stabilizes Pin1 by inhibiting its ubiquitination in human cells. J Biol Chem 280, 36575 36583.
84. Smet C, Sambo AV, Wieruszeski JM, Leroy A, Landrieu I, Buee L Lippens G (2004) The peptidyl prolyl cis/trans-isomerase Pin1 recognizes the phospho-Thr212-Pro213 site on Tau. Biochemistry 43, 2032 2040.
85. Yeh ES Means AR (2007) PIN1, the cell cycle and cancer. Nat Rev Cancer 7, 381 388.
86. Bao L, Kimzey A, Sauter G, Sowadski JM, Lu KP Wang DG (2004) Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am J Pathol 164, 1727 1737.
87. Zheng H, You H, Zhou XZ, Murray SA, Uchida T, Wulf G, Gu L, Tang X, Lu KP Xiao ZX (2002) The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response. Nature 419, 849 853.
88. Zacchi P, Gostissa M, Uchida T, Salvagno C, Avolio F, Volinia S, Ronai Z, Blandino G, Schneider C Del Sal G (2002) The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 419, 853 857.
89. Yeh E, Cunningham M, Arnold H, Chasse D, Monteith T, Ivaldi G, Hahn WC, Stukenberg PT, Shenolikar S, Uchida T et al. (2004) A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 6, 308 318.
90. Toledo F Wahl GM (2006) Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 6, 909 923.
91. Ross CA Poirier MA (2005) What is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol 6, 891 898.