The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins

Genes and Development

Volumn 12, Issue 5, 1998, Pages 706-720

  Shen, Minhui ^a   Stukenberg, P Todd ^a   Kirschner, Marc W ^a   Lu, Kun Ping ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cdc2; Cell cycle control; Mitosis; Peptidyl prolyl isomerase; Phosphoproteins; Pin1

Indexed keywords

ISOMERASE;

ARTICLE; CELL CYCLE; ENZYME BINDING; ENZYME SPECIFICITY; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; XENOPUS;

EID: 0032031634     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.5.706     Document Type: Article

References (60)

1. Bailly, E., M. McCaffrey, N. Touchot, A. Zahraoui, B. Goud, and M. Bornens. 1991. Phosphorylation of two small GTP-binding proteins of the Rab family by p34cdc2. Nature 350: 715-718.
2. Blangy, A., H.A. Lane, P. d'Herin, M. Harper, M. Kress, and E.A. Nigg. 1995. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83: 1159-1169.
3. Booher, R.N., P.S. Holman, and A. Fattaey. 1997. Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol Chem. 272: 22300-22306.
4. Coleman, T.R. and W.G. Dunphy. 1994. Cdc2 regulatory factors. Curr. Opin. Cell Biol. 6: 877-882.
5. Coleman, T.R., Z. Tang, and W.G. Dunphy. 1993. Negative regulation of the weel protein kinase by direct action of the nim1/cdr1 mitotic inducer. Cell 72: 919-929.
6. Davis, F.M., T.Y. Tsao, S.K. Fowler, and P.N. Rao. 1983. Monclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. 80: 2926-2930.
7. Davis, F.M., D.A. Wright, J.E. Penkala, and P.N. Rao. 1989. Mitosis-specific monoclonal antibodies block cleavage in amphibian embryos. Cell Struct. Funct. 14: 271-217.
8. Fischer, G. 1994. Peptidyl-prolyl cis/trans isomerases. Angew. Chem. Intl. Ed. Engl. 33: 1415-1436.
9. Golsteyn, R.M., K.E. Mundt, A.M. Fry, and E.A. Nigg. 1995. Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J. Cell Biol 129: 1617-1628.
10. Hamanaka, R., M.R. Smith, P.M. O'Connor, S. Maloid, K. Mihalic, J.L. Spivak, D.L. Longo, and D.K. Ferris. 1995. Polo-like kinase is a cell cycle-regulated kinase activated during mitosis. J. Biol. Chem. 270: 21086-21091.
11. Hanes, S.D., P.R. Shank, and K.A. Bostian. 1989. Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae. Yeast 5: 55-72.
12. Heald, R. and F. McKeon. 1990. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61: 579-589.
13. Hecht, R.M., M. Berg-Zabelshansky, P.N. Rao, and F.M. Davis. 1987. Conditional absence of mitosis-specific antigens in a temperature-sensitive embryonic-arrest mutant of Caenorhabditis elegans. J. Cell Sci. 87: 305-314.
14. Heintz, N., H.L. Sive, and R.G. Roeder. 1983. Regulation of human histone gene expression: Kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol. Cell. Biol. 3: 539-550.
15. Hirano, T. and T.J. Mitchison. 1991. Cell cycle control of higher-order chromatin assembly around naked DNA in vitro. J. Cell Biol. 115: 1479-1489.
16. Izumi, T. and J.L. Mailer. 1993. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol. Biol. Cell. 4: 1337-1350.
17. Izumi, T., D.H. Walker, and J.L. Maller. 1992. Periodic changes in phosphorylation of the Xenopus cdc25 phosphatase regulate its activity. Mol. Biol. Cell. 3: 927-939.
18. Johnson, R.T. and P.N. Rao. 1970. Mammalian cell fusion: Induction of premature chromosome condensation in interphase nuclei. Nature 226: 717-722.
19. Keryer, G., F.M. Davis, P.N. Rao, and J. Beisson. 1987. Protein phosphorylation and dynamics of cytoskeletal structures associated with basal bodies in Paramecium. Cell Motil Cytoskeleton 8: 44-54.
20. King, R.W., P.K. Jackson, and M.W. Kirschner. 1994. Mitosis in transition. Cell 79: 563-571.
21. King, R.W., J.M. Peters, S. Tugendreich, M. Rolfe, P. Hieter, and M.W. Kirschner. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81: 279-288.
22. Krek, W. and E.A. Nigg. 1991. Mutations of p34cdc2 kinase activation in vertebrates. EMBO J. 10: 3331-3341.
23. Kuang, J. and C.L. Ashorn. 1993. At least two kinases phosphorylate the MPM-2 epitope during Xenopus oocyte maturation. J. Cell Biol 123: 859-868.
24. Kuang, J., J.Y. Zhao, D.A. Wright, G.F. Saunders, and P.N. Rao. 1989. Mitosis specific monoclonal antibody MPM-2 inhibits Xenopus oocyte maturation and depletes maturation promoting activity. Proc. Natl. Acad. Sci. 86: 4982-4986.
25. Kuang, J., C.L. Ashorn, M. Gonzalez-Kuyvenhoven, and J.E. Penkala. 1994. cdc25 is one of the MPM-2 antigens involved in the activation of maturation-promoting factor. Mol Biol. Cell. 5: 135-145.
26. Kumagai, A. and W.G. Dunphy. 1996. Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science 273: 1377-1380.
27. Lee, T.H., C. Turck, and M.W. Kirschner. 1994. Inhibition of cde2 activation by INH/PP2A. Mol Biol. Cell. 5: 323-338.
28. Lu, K.P. and T. Hunter. 1995. Evidence for a NIMA-like mitotic pathway in vertebrate cells. Cell 81: 413-424.
29. Lu, K.P., S.A. Osmani, and A.R. Means. 1993. Properties and regulation of the cell cycle-specific NIMA protein kinase of Aspergillus nidulans. J. Biol. Chem. 268: 8769-8776.
30. Lu, K.P., S.D. Hanes, and T. Hunter. 1996. A human peptidylprolyl isomerase essential for regulation of mitosis. Nature 380: 544-547.
31. Maleszka, R., S.D. Hanes, R.L. Hackett, C.H. de Couet, and G.L. Miklos. 1996. The Drosophila melanogaster dodo (dod) gene, conserved in humans, is functionally interchangeable with the ESS1 cell division gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 93: 447-451.
32. Matsumoto-Taniura, N., F. Pirollet, R. Monroe, L. Gerace, and J.M. Westendorf. 1996. Identification of novel M phase phosphoproteins by expression cloning. Mol Biol. Cell. 7: 1455-1469.
33. Mueller, P.R., T.R. Coleman, A. Kumagai, and W.G. Dunphy. 1995. Myt1: A membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270: 86-90.
34. Murray, A. W. 1991. Cell cycle extracts. Methods Cell. Biol. 36: 581-605.
35. Muslin, A.J., J.W. Tanner, P.M. Allen, and A.S. Shaw. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84: 889-897.
36. Nigg, E.A. 1995. Cyclin-dependent protein kinases: Key regulators of the eukaryote cell cycle. BioEssays 17: 471-480.
37. Nurse, P. 1994. Ordering S phase and M phase. Cell 79: 547-550.
38. Ogg, S., B. Gabrielli, and H. Piwnica-Worms. 1994. Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. J. Biol. Chem. 269: 30461-30469.
39. Pawson, T. 1995. Protein modules and signalling networks. Nature 373: 573-580.
40. Pines, J. and T. Hunter. 1991. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115: 1-17.
41. Poon, R.Y., H. Toyoshima, and T. Hunter. 1995. Redistribution of the CDK inhibitor p27 between different cyclin.CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet irradiation. Mol. Biol. Cell. 6: 1197-1213.
42. Ranganathan, R., K.P. Lu, T. Hunter, and J.P. Noel. 1997. Structural and functional analysis of the mitotic peptidyl-prolyl isomerase Pin1 suggests that substrate recognition is phosphorylation dependent. Cell 89: 875-886.
43. Renzi, L., M.S. Gersch, M.S. Campbell, L. Wu, S.A. Osmani, and G.J. Gorbsky. 1997. MPM-2 antibody-reactive phosphorylations can be created in detergent-extracted cells by kinetochore-bound and soluble kinases. J. Cell. Sci. 110: 2013-2025.
44. Reynisdottir, I. and J. Massague. 1997. The subcellular locations of p15(Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2. Genes & Dev. 11: 492-503.
45. Russell, P. and P. Nurse. 1986. cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45: 145-153.
46. Schmid, F.X. 1995. Prolyl isomerases join the fold. Curr. Biol. 5: 993-994.
47. Schreiber, S.L. 1991. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science 251: 283-287.
48. Solomon, M.J., M. Glotzer, T.H. Lee, M. Philippe, and M.W. Kirschner. 1990. Cyclin activation of p34cdc2. Cell 63: 1013-1024.
49. Strausfeld, U., A. Fernandez, J.P. Capony, F. Girard, N. Lautredou, J. Derancourt, J.C. Labbe, and N.J. Lamb. 1994. Activation of p34cdc2 protein kinase by microinjection of human cdc25C into mammalian cells. Requirement for prior phosphorylation of cdc25C by p34cdc2 on sites phosphorylated at mitosis. J. Biol. Chem. 269: 5989-6000.
50. Stukenberg, P.T., K.D. Lustig, T.J. McGarry, R.W. King, J. Kuang, and M.W. Kirschner. 1997. Systematic identification of mitotic phosphoproteins. Curr. Biol. 7: 338-348.
51. Taagepera, S., P.N. Rao, F.H. Drake, and G.J. Gorbsky. 1993. DNA topoisomerase II alpha is the major chromosome protein recognized by the mitotic phosphoprotein antibody MPM-2. Proc. Natl. Acad. Sci. 90: 8407-8411.
52. Taagepera, S., P. Dent, J.H. Her, T.W. Sturgill, and G.J. Gorbsky. 1994. The MPM-2 antibody inhibits mitogen-activated protein kinase activity by binding to an epitope containing phosphothreonine-183. Mol. Biol. Cell. 5: 1243-1251.
53. Vandre, D.D., F.M. Davis, P.N. Rao, and G.G. Borisy. 1984. Phosphoproteins are components of mitotic microtubule organizing centers. Proc. Natl. Acad. Sci. 81: 4439-4443.
54. Vandre, D.D., F.M. Davis, P.N. Rao, and G.G. Borisy. 1986. Distribution of cytoskeletal proteins sharing a conserved phosphorylated epitope. Eur. J. Cell. Biol. 41: 72-81.
55. Vandre, D.D., V.E. Centonze, J. Peloquin, R.M. Tombes, and G.G. Borisy. 1991. Proteins of the mammalian mitotic spindle: phosphorylation/dephosphorylation of MAP-4 during mitosis. J. Cell Sci. 98: 577-588.
56. Westendorf, J.M., P.N. Rao, and L. Gerace. 1994. Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. 91: 714-718.
57. Wordeman, L., F.M. Davis, P.N. Rao, and W.Z. Cande. 1989. Distribution of phosphorylated spindle-associated proteins in the diatom Stephanopyxis turris. Cell. Motil. Cytoskeleton 12: 33-41.
58. Yaffe, M.B., M. Schutkowski, M. Shen, X.Z. Zhou, P.T. Stukenberg, J. Rahfeld, J. Xu, J. Kuang, M.W. Kirschner, G. Fischer, L.C. Cantley, and K.P. Lu. 1997. Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism. Science 278:1957-1960.
59. Ye, X.S., G. Xu, R.T. Pu, R.R. Fincher, S.L. McGuire, A.H. Osmani, and S.A. Osmani. 1995. The NIMA protein kinase is hyperphosphorylated and activated downstream of p34cdc2/ cyclin B: coordination of two mitosis promoting kinases EMBO J. 14: 986-994.
60. Yu, H., J.M. Peters, R.W. King, A. Page, P. Hieter, and M.W. Kirschner. 1988, Identification of a cullin homology regtion in a subunit of the anaphase-promoting complex. Science (in press).