Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer's disease

BioEssays

Volumn 25, Issue 2, 2003, Pages 174-181

  Lu, Kun Ping ^a,c   Liou, Yih Cherng ^a   Vincent, Inez ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; ISOMERASE; PEPTIDYLPROLYL ISOMERASE PIN1; PROLINE; SERINE PROTEINASE; THREONINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CARCINOGENESIS; CELL CYCLE; CHEMICAL BOND; CONFORMATIONAL TRANSITION; DISEASE COURSE; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; ISOMERISM; MITOSIS; NERVE CELL; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ALZHEIMER DISEASE; HUMANS; ISOMERISM; MITOSIS; MODELS, NEUROLOGICAL; NEURONS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION; PROLINE;

EID: 0037322816     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.10223     Document Type: Article

References (85)

1. Selkoe DJ. The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol 1998;8:447-453.
2. Spillantini MG, Goedert M. Tau protein pathology in neurodegenerative diseases. Trends Neurosci 1998;21:428-433.
3. Lee VM. Tauists and beta-aptists united-well almost! Science 2001;293:1446-1447.
4. Lee VM, Balin BJ, Otvos L Jr, Trojanowski JQ. A68: a major subunit of paired helical filaments and derivatized forms of normal Tau. Science 1991;251:675-678.
5. Goedert M, Spillantini MG, Cairns NJ, Crowther RA. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 1992;8:159-168.
6. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Watanabe A, Titani K, Ihara Y. Hyperphosphorylation of tau in PHF. Neurobiol Aging 1995;16:365-371.
7. Hanger DP, Betts JC, Loviny TL, Blackstock WP, Anderton BH. New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry J Neurochem 1998;71:2465-2476.
8. Vincent I, Rosado M, Davies P. Mitotic mechanisms in Alzheimer's disease? J Cell Biol 1996;132:413-425.
9. Vincent I, Zheng JH, Dickson DW, Kress Y, Davies P. Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol Aging 1998;19:287-296.
10. Husseman JW, Nochlin D, Vincent I. Mitotic activation: a convergent mechanism for a cohort of neurodegenerative diseases. Neurobiol Aging 2000;21:815-828.
11. Nagy Z, Esiri MM, Smith AD. The cell division cycle and the pathophysiology of Alzheimer's disease. Neuroscience 1998;87:731-739.
12. Raina AK, Monteiro MJ, McShea A, Smith MA. The role of cell cycle-mediated events in Alzheimer's disease. Int J Exp Pathol 1999;80:71-76.
13. Vincent I. Cycling to the finish. Neurobiol Aging 2000;21:757-760.
14. Yang Y, Geldmacher DS, Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 2001;21:2661-2668.
15. Lu KP, Hanes SD, Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996;380:544-547.
16. Yaffe MB, et al. Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism. Science 1997;278:1957-1960.
17. Shen M, Stukenberg PT, Kirschner MW, Lu KP. The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev 1998;12:706-720.
18. Lu PJ, Zhou XZ, Shen M, Lu KP. A function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 1999;283:1325-1328.
19. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 1999;399:784-788.
20. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, Küllertz G, Stark M, Fischer G, Lu KP. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 2000;6:873-883.
21. Lu KP, Liou YC, Zhou XZ. Pinning down the proline-directed phosphorylation signaling. Trends Cell Biol 2002;12:164-172.
22. Morgan DO. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 1997;13:261-291.
23. Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2001;2:21-32.
24. Davis FM, Tsao TY, Fowler SK, Rao PN. Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 1983;80:2926-2930.
25. Matsumoto-Taniura N, Pirollet NF, Monroe R, Gerace L, Westendorf JM. Identification of novel M phase phosphoproteins by expression cloning. Mol Biol Cell 1996;7:1455-1469.
26. Stukenberg PT, Lustig KD, McGarry TJ, King RW, Kuang J, Kirschner MW. Systematic identification of mitotic phosphoproteins. Curr Biol 1997;7:338-348.
27. Izumi T, Maller JL. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol Blot Cell 1993;4:1337-1350.
28. Lee TH, Solomon MJ, Mumby MC, Kirschner MW. INH, a negative regulator of MPF, is a form of protein phosphatase 2A. Cell 1991;64:415-423.
29. Che S, Wu W, Nelman-Gonzalez M, Stukenberg T, Clark R, Kuang J. A phosphatase activity in Xenopus oocyte extracts preferentially dephosphorylates the MPM-2 epitope. FEBS Lett 1998;424:225-233.
30. Hunter T. Prolyl isomerase and nuclear function. Cell 1998;92:141-143.
31. Zhou XZ, Lu PJ, Wulf G, Lu KP. Phosphorylation-dependent prolyl isomerization: A novel signaling regulatory mechanism. Cell Mol Life Sci 1999;56:788-806.
32. Schutkowski M, Bernhardt A, Zhou XZ, Shen M, Reimer U, Rahfeld JU, Lu KP, Fischer G. Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition. Biochemistry 1998;37:5566-5575.
33. Daly NL, Hoffmann R, Otvos L Jr, Craik DJ. Role of phosphorylation in the conformation of tau peptides implicated in Alzheimer's disease. Biochemistry 2000;39:9039-9046.
34. Ranganathan R, Lu KP, Hunter T, Noel JP. Structural and functional analysis of the mitotic peptidyl-prolyl isomerase Pin1 suggests that substrate recognition is phosphorylation dependent. Cell 1997;89:875-886.
35. Winkler KE, Swenson KI, Kornbluth S, Means AR. Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 2000;287:1644-1647.
36. Rippmann JF, Hobbie S, Daiber C, Guilliard B, Bauer M, Birk J, Nar H, Garin-Chesa P, Rettig WJ, Schnapp A. Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis [In Process Citation]. Cell Growth Differ 2000;11:409-416.
37. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J, Hanes SD. The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. Embo J 2000;19:3727-3738.
38. Liou YC, Ryo R, Huang HK, Lu PJ, Bronson R, Fujimori F, Uchida U, Hunter T, Lu KP. Loss of Pin1 function in the mouse resembles the cyclin D1-null phenotypes. Proc Natl Acad Sci USA 2002;99:1335-1340.
39. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Lu KP. Pin1 is overexpressed in breast cancer and potentiates the transcriptional activity of phosphorylated c-Jun towards the cyclin D1 gene. EMBO J 2001;20:3459-3472.
40. Ryo A, Nakamura N, Wulf G, Liou YC, Lu KP. Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nature Cell Biol 2001;3:793-801.
41. Ryo A, Liou YC, Wulf G, Nakamura N, Lee SW, Lu KP. Pin1 is an E2F target gene essential for the Neu/Ras-induced transformation of mammary epithelial cells. Mol Cell Biol 2002;22:5281-5295.
42. Maleszka R, Hanes SD, Hackett RL, de CH, Miklos GL. 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 USA 1996;93:447-451.
43. Fujimori F, Takahashi K, Uchida C, Uchida T. Mice lacking Pin1 develop normally, but are defective in entering cell cycle from G(0) arrest. Biochem Biophys Res Commun 1999;265:658-663.
44. Yao JL, Kops O, Lu PJ, Lu KP. Functional conservation of phosphorylation-specific prolyl isomerases in plants. J Biol Chem 2001;276:13517-13523.
45. Weiwad M, Kullertz G, Schutkowski M, Fischer G. Evidence that the substrate backbone conformation is critical to phosphorylation by p42 MAP kinase. FEBS Lett 2000;478:39-42.
46. Brown NR, Noble ME, Endicott JA, Johnson LN. The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1999;1:438-443.
47. Stukenberg PT, Kirschner MW. Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 2001;7:1071-1083.
48. Deshaies RJ, Ferrell JE Jr. Multisite phosphorylation and the countdown to S phase. Cell 2001;107:819-822.
49. Greenberg SG, Davies P, Schein JD, Binder LI. Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 1992;267:564-569.
50. Preuss U, Doring F, Illenberger S, Mandelkow EM. Cell cycle-dependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol Biol Cell 1995;6:1397-1410.
51. Illenberger S, Zheng-Fischhofer Q, Preuss U, Stamer K, Baumann K, Trinczek B, Biernat J, Godemann R, Mandelkow EM, Mandelkow E. The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol Biol Cell 1998;9:1495-1512.
52. Preuss U, Mandelkow EM. Mitotic phosphorylation of tau protein in neuronal cell lines resembles phosphorylation in Alzheimer's disease. Eur J Cell Biol 1998;76:176-184.
53. Dranovsky A, Vincent I, Gregori L, Schwarzman A, Colflesh D, Enghild J, Strittmatter W, Davies P, Goldgaber D. Cdc2 phosphorylation of nucleolin demarcates mitotic stages and Alzheimer's disease pathology. Neurobiol Aging 2001;22:517-528.
54. Kondratick CM, Vandre DD. Alzheimer's disease neurofibrillary tangles contain mitosis-specific phosphoepitopes. J Neurochem 1996;67:2405-2416.
55. Suzuki T, Oishi M, Marshak DR, Czernik AJ, Nairn AC, Greengard P. Cell cycle-dependent regulation of the phosphorylation and metabolism of the Alzheimer amyloid precursor protein. Embo J 1994;13:1114-1122.
56. King KL, Cidlowski JA. Cell cycle and apoptosis: common pathways to life and death. J Cell Biochem 1995;58:175-180.
57. Park DS, Farinelli SE, Greene LA. Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J Biol Chem 1996;271:8161-8169.
58. Smale G, Nichols NR, Brady DR, Finch CE, Horton WE Jr. Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 1995;133:225-230.
59. Li WP, Chan WY, Lai HW, Yew DT. Terminal dUTP nick end labeling (TUNEL) positive cells in the different regions of the brain in normal aging and Alzheimer patients. J Mol Neurosci 1997;8:75-82.
60. Ding XL, Husseman J, Tomashevski A, Nochlin D, Jin LW, Vincent I. The cell cycle Cdc25A tyrosine phosphatase is activated in degenerating postmitotic neurons in Alzheimer's disease. Am J Pathol 2000;157:1983-1990.
61. Vincent I, Bu B, Tomashevski A, Husseman J, Nochlin D, Jin L-W. Constitutive Cdc25B activity in adult brain neurons with M phase-type alterations in Alzheimer neurodegeneration. Neuroscience 2001;105:639-650.
62. Tomashevski A, Husseman J, Jin L-W, Nochlin D, Vincent I. Constitutive Wee1 activity in adult brain neurons with M phase-type alterations in Alzheimer neurodegeneration. J Alz Dis 2001;3:195-207.
63. Vincent I, Jicha G, Rosado M, Dickson DW. Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 1997;17:3588-3598.
64. Nagy Z, Esiri MM, Cato AM, Smith AD. Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol 1997;94:6-15.
65. Busser J, Geldmacher DS, Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 1998;18:2801-2807.
66. Zhu X, Rottkamp CA, Raina AK, Brewer GJ, Ghanbari HA, Boux H, Smith MA. Neuronal CDK7 in hippocampus is related to aging and alzheimer disease. Neurobiol Aging 2000;21:807-813.
67. Konishi Y, Lehtinen M, Donovan N, Bonni A. Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol Cell 2002;9:1005-1016.
68. Dhavan R, Tsai LH. A decade of CDK5. Nat Rev Mol Cell Biol 2001;2:749-759.
69. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999;402:615-622.
70. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000;405:360-364.
71. Takashima A, Murayama M, Yasutake K, Takahashi H, Yokoyama M, Ishiguro K. Involvement of cyclin dependent kinase5 activator p25 on tau phosphorylation in mouse brain. Neurosci Lett 2001;306:37-40.
72. Yoo BC, Lubec G. p25 protein in neurodegeneration. Nature 2001;411:763-764.
73. Ahlijanian MK, et al. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA 2000;97:2910-2915.
74. Bian F, Nath R, Sobocinski G, Booher RN, Lipinski WJ, Callahan MJ, Pack A, Wang KK, Walker LC. Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J Comp Neurol 2002;446:257-266.
75. Alvarez A, Munoz JP, Maccioni RB. A Cdk5-p35 stable complex is involved in the beta-amyloid-induced deregulation of Cdk5 activity in hippocampal neurons. Exp Cell Res 2001;264:266-274.
76. Sontag E, Nunbhakdi-Craig V, Lee G, Bloom GS, Mumby MC. Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 1996;17:1201-1207.
77. Kops O, Zhou XZ, Lu KP. Pin1 enhances the dephosphorylation of the C-terminal domain of the RNA polymerase II by Fcp1. FEBS Lett 2002;513:305-311.
78. Lu PJ, Zhou XZ, Liou YC, Noel JP, Lu KP. Critical role of WW domain phosphorylation in regulating its phosphoserine-binding activity and the Pin1 function. J Biol Chem 2002;277:2381-2384.
79. Takashima A, et al. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci USA 1998;95:9637-9641.
80. Wang X, Luebbe P, Gruenstein E, Zemlan F. Apolipoprotein E (ApoE) peptide regulates tau phosphorylation via two different signaling pathways. J Neurosci Res 1998;51:658-665.
81. Takashima A, Honda T, Yasutake K, Michel G, Murayama O, Murayama M, Ishiguro K, Yamaguchi H. Activation of tau protein kinase I/glycogen synthase kinase-3beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci Res 1998;31:317-323.
82. Gong CX, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K. Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain. J Neurochem 1995;65:732-738.
83. Alonso A, Zaidi T, Novak M, Grundke-Iqbal I, Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA 2001;98:6923-6928.
84. Wang JZ, Gong CX, Zaidi T, Grundke-Iqbal I, Iqbal K. Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and-2B. J Biol Chem 1995;270:4854-4860.
85. Gordon-Krajcer W, Yang L, Ksiezak-Reding H. Conformation of paired helical filaments blocks dephosphorylation of epitopes shared with fetal tau except Ser199/202 and Ser202/Thr205. Brain Res 2000;856:163-175.