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Science 12 December 1997:
Vol. 278. no. 5345, pp. 1957 - 1960
DOI: 10.1126/science.278.5345.1957
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Reports

Sequence-Specific and Phosphorylation-Dependent Proline Isomerization: A Potential Mitotic Regulatory Mechanism

Michael B. Yaffe, * Mike Schutkowski, * Minhui Shen, * Xiao Zhen Zhou, P. Todd Stukenberg, Jens-Ulrich Rahfeld, Jian Xu, Jian Kuang, Marc W. Kirschner, Gunter Fischer, Lewis C. Cantley, Kun Ping Lu dagger

Pin1 is an essential and conserved mitotic peptidyl-prolyl isomerase (PPIase) that is distinct from members of two other families of conventional PPIases, cyclophilins and FKBPs (FK-506 binding proteins). In response to their phosphorylation during mitosis, Pin1 binds and regulates members of a highly conserved set of proteins that overlaps with antigens recognized by the mitosis-specific monoclonal antibody MPM-2. Pin1 is here shown to be a phosphorylation-dependent PPIase that specifically recognizes the phosphoserine-proline or phosphothreonine-proline bonds present in mitotic phosphoproteins. Both Pin1 and MPM-2 selected similar phosphorylated serine-proline-containing peptides, providing the basis for the specific interaction between Pin1 and MPM-2 antigens. Pin1 preferentially isomerized proline residues preceded by phosphorylated serine or threonine with up to 1300-fold selectivity compared with unphosphorylated peptides. Pin1 may thus regulate mitotic progression by catalyzing sequence-specific and phosphorylation-dependent proline isomerization.

M. B. Yaffe, Division of Signal Transduction, Department of Medicine and Department of Surgery, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA.
M. Schutkowski, J.-U. Rahfeld, G. Fischer, Max-Planck Research Unit on Enzymology of Protein Folding, Kurth-Mothes Strasse 3, 06120 Halle, Germany.
M. Shen and X. Z. Zhou, Cancer Biology Program, Division of Hematology and Oncology, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA.
P. T. Stukenberg and M. W. Kirschner, Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.
J. Xu, Division of Signal Transduction, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA.
J. Kuang, Department of Clinical Investigation, University of Texas M.D. Anderson Cancer Center, Houston, TX 77030, USA.
L. C. Cantley, Division of Signal Transduction, Department of Medicine, Beth Israel Deaconess Medical Center, and Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.
K. P. Lu, Cancer Biology Program, Division of Hematology/Oncology, Department of Medicine, Beth Israel Deaconess Medical Center, and Division on Aging, Harvard Medical School, 330 Brookline Avenue, HIM 1047, Boston, MA 02215, USA.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: klu{at}bidmc.harvard.edu

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Phospho-Carboxyl-Terminal Domain Binding and the Role of a Prolyl Isomerase in Pre-mRNA 3'-End Formation.
D. P. Morris, H. P. Phatnani, and A. L. Greenleaf (1999)
J. Biol. Chem. 274, 31583-31587
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Function of WW Domains as Phosphoserine- or Phosphothreonine-Binding Modules.
P. Lu, X. Z. Zhou, M. Shen, and K. P. Lu (1999)
Science 283, 1325-1328
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Characterization of Raf-1 Activation in Mitosis.
A. D. Laird, D. K. Morrison, and D. Shalloway (1999)
J. Biol. Chem. 274, 4430-4439
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Transcription Factor Phosphorylation by pp90rsk2. IDENTIFICATION OF Fos KINASE AND NGFI-B KINASE I AS pp90rsk2.
K. D. Swanson, L. K. Taylor, L. Haung, A. L. Burlingame, and G. E. Landreth (1999)
J. Biol. Chem. 274, 3385-3395
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Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF auto-amplification.
A Karaiskou, C Jessus, T Brassac, and R Ozon (1999)
J. Cell Sci. 112, 3747-3756
   Abstract »    PDF »
The C-terminal domain of the Cdc2 inhibitory kinase Myt1 interacts with Cdc2 complexes and is required for inhibition of G(2)/M progression.
N. Wells, N Watanabe, T Tokusumi, W Jiang, M. Verdecia, and T Hunter (1999)
J. Cell Sci. 112, 3361-3371
   Abstract »    PDF »
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.
A Albert, S Lavoie, and M Vincent (1999)
J. Cell Sci. 112, 2493-2500
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The Assembly of Progesterone Receptor-hsp90 Complexes Using Purified Proteins.
H. Kosano, B. Stensgard, M. C. Charlesworth, N. McMahon, and D. Toft (1998)
J. Biol. Chem. 273, 32973-32979
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Ssp1, a Site-specific Parvulin Homolog from Neurospora crassa Active in Protein Folding.
O. Kops, C. Eckerskorn, S. Hottenrott, G. Fischer, H. Mi, and M. Tropschug (1998)
J. Biol. Chem. 273, 31971-31976
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The Cyclophilin-like Domain Mediates the Association of Ran-Binding Protein 2 with Subunits of the 19 S Regulatory Complex of the Proteasome.
P. A. Ferreira, C. Yunfei, D. Schick, and R. Roepman (1998)
J. Biol. Chem. 273, 24676-24682
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Antibody catalysis of peptidyl-prolyl cis-trans isomerization in the folding of RNase T1.
L. Ma, L. C. Hsieh-Wilson, and P. G. Schultz (1998)
PNAS 95, 7251-7256
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Phosphorylation Sites in the Autoinhibitory Domain Participate in p70s6k Activation Loop Phosphorylation.
P. B. Dennis, N. Pullen, R. B. Pearson, S. C. Kozma, and G. Thomas (1998)
J. Biol. Chem. 273, 14845-14852
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The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins.
M. Shen, P. T. Stukenberg, M. W. Kirschner, and K. P. Lu (1998)
Genes & Dev. 12, 706-720
   Abstract »    Full Text »
Signaling Through Scaffold, Anchoring, and Adaptor Proteins.
T. Pawson and J. D. Scott (1997)
Science 278, 2075-2080
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Comparison of Folding Rates of Homologous Prokaryotic and Eukaryotic Proteins.
M. Widmann and P. Christen (2000)
J. Biol. Chem. 275, 18619-18622
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Critical Role of WW Domain Phosphorylation in Regulating Phosphoserine Binding Activity and Pin1 Function.
P.-J. Lu, X. Z. Zhou, Y.-C. Liou, J. P. Noel, and K. P. Lu (2002)
J. Biol. Chem. 277, 2381-2384
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Peptide and Protein Library Screening Defines Optimal Substrate Motifs for AKT/PKB.
T. Obata, M. B. Yaffe, G. G. Leparc, E. T. Piro, H. Maegawa, A. Kashiwagi, R. Kikkawa, and L. C. Cantley (2000)
J. Biol. Chem. 275, 36108-36115
   Abstract »    Full Text »    PDF »
p13SUC1 and the WW Domain of PIN1 Bind to the Same Phosphothreonine-Proline Epitope.
I. Landrieu, B. Odaert, J.-M. Wieruszeski, H. Drobecq, P. Rousselot-Pailley, D. Inze, and G. Lippens (2001)
J. Biol. Chem. 276, 1434-1438
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Functional Replacement of the Essential ESS1 in Yeast by the Plant Parvulin DlPar13.
M. Metzner, G. Stoller, K. P. Rucknagel, K. P. Lu, G. Fischer, M. Luckner, and G. Kullertz (2001)
J. Biol. Chem. 276, 13524-13529
   Abstract »    Full Text »    PDF »
Functional Conservation of Phosphorylation-specific Prolyl Isomerases in Plants.
J.-L. Yao, O. Kops, P.-J. Lu, and K. P. Lu (2001)
J. Biol. Chem. 276, 13517-13523
   Abstract »    Full Text »    PDF »


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