Role of cdk5 in the pathogenesis of Alzheimer's disease

NeuroSignals

Volumn 12, Issue 4-5, 2003, Pages 209-214

  Lau, Lit Fui ^a   Ahlijanian, Michael K ^a  

^a PFIZER INC   (United States)

Author keywords

Alzheimer's disease; Amyloid peptide; Amyloid precursor protein; Calpain; cdk5; Neurofibrillary tangles; p25; Paired helical filament; Phosphorylation; Tau

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CYCLIN DEPENDENT KINASE 5; PRESENILIN 1; PROLINE; PROTEIN SERINE KINASE; TAU PROTEIN; THREONINE PROTEINASE;

ALZHEIMER DISEASE; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; PATHOGENESIS; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; REVIEW; SENILE PLAQUE;

ALZHEIMER DISEASE; ANIMALS; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; DISEASE MODELS, ANIMAL; HUMANS; NEUROFIBRILLARY TANGLES; SENILE PLAQUES; TAU PROTEINS;

EID: 0348010574     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000074622     Document Type: Review

References (74)

1. Hardy J, Selkoe DJ: Medicine - The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 2002;297:353-356.
2. Götz J, Chen F, van Dorpe J, Nitsch RM: Formation of neurofibrillary tangles in P301L tau transgenic mice induced by A242 fibrils. Science 2001;293:1491-1495.
3. Lewis J, Dickson DW, Lin W-L, et al.: Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001;293:1487-1491.
4. Braak H, Braak E: Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 1995;16:271-278; discussion pp 8-84.
5. Alonso AdC, 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.
6. Lau LF, Schachter JB, Seymour PA, Sanner MA: Tau protein phosphorylation as a therapeutic target in Alzheimer's disease. Curr Top Med Chem 2002;2:395-415.
7. Lew J, Huang Q-Q, Qi Z, et al.: A brain-specific activator of cyclin-dependent kinase 5. Nature 1994;371:423-426.
8. Tsai L-H, Deialle I, Caviness VS Jr, Chae T, Harlow E: p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 1994;371:419-423.
9. Humbert S, Dhavan R, Tsai L-H: p39 activates cdk5 in neurons and is associated with the actin cycoskeleton. J Cell Sci 2000;113:975-983.
10. Tang D, Yeung J, Lee KY, et al.: An isoform of the neuronal cyclin-dependent kinase 5 (cdk5) activator. J Biol Chem 1995;270:26897-26903.
11. Brown NR, Noble MEM, Endicott JA, et al.: The crystal structure of cyclin A. Structure 1995;3:1235-1247.
12. Chou K-C, Watenpaugh KD, Heinrikson RL: A model of the complex between cyclin-dependent kinase 5 and the activation domain of neuronal cdk5 activator. Biochem Biophys Res Commun 1999;259:420-428.
13. Zheng M, Leung CL, Liem RKH: Region specific coexpression of cyclin-dependent kinase 5 (cdk5) and its activators P35 and P39, in the developing and adult nervous system. J Neurobiol 1998;35:141-159.
14. Ino H, Ishizuka T, Chiba T, Tatibana M: Expression of cdk5 (PSSALRE kinase), a neural and cdc2-related protein kinase, in the mature and developing mouse central and peripheral nervous systems. Brain Res 1994;661:196-206.
15. Tsai L-H, Takahashi T, Caviness VS, Harlow E: Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 1993;119:1029-1040.
16. Dhavan R, Tsai L-H: A decade of cdk5. Nature Rev Mol Cell Biol 2001;2:749-759.
17. Smith DS, Tsai L-H: Cdk5 behind the wheel: A role in trafficking and transport? Trends Cell Biol 2002;12:28-36.
18. Smith DS, Greer PL, Tsai L-H: Cdk5 on the brain. Cell Growth Differ 2001;12:277-283.
19. Anderton BH, Betts J, Blackstock WP, et al.: Sites of phosphorylation in tau and factors affecting their regulation. Biochem Soc Symp 2001;67:73-80.
20. Hanger DP, Betts JC, Loviny TLF, Blackstock WP, Anderton BH: New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nano electrospray mass spectrometry. J Neurochem 1998;71:2465-2476.
21. Lund ET, McKenna R, Evans DB, Sharma SK, Mathews WR: Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry. J Neurochem 2001;76:1221-1232.
22. Liu F, Iqbal K, Grundke-Iqbal I, Gong CX: Involvement of aberrant glycosylation in phosphorylation of tau by cdk5 and GSK-3 beta. FEBS Lett 2002;530:209-214.
23. Baumann K, Mandelkow EM, Biernat J, Piwnica-Worms H, Mandelkow E: Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett 1993;336:417-424.
24. Paudel HK, Lew J, Ali Z, Wang JH: Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J Biol Chem 1993;268:23512-23518.
25. Arioka M, Tsukamoto M, Ishiguro K, et al.: Tau protein kinase II is involved in the regulation of the normal phosphorylation state of tau protein. J Neurochem 1993;60:461-468.
26. Sengupta A, Wu Q, Grundke-Iqbal I, Iqbal K, Singh TJ: Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5. Mol Cell Biol 1997;167:99-105.
27. Patrick GN, Zukerberg L, Mikolic M, de la Monte S, Dikkes P, Tsai L-H: Conversion of p35 to p25 deregulates cdk5 activity and promotes neurodegeneration. Nature 1999;402:615-622.
28. Michel G, Mercken M, Murayama M, et al.: Characterization of tau phosphorylation in glycogen synthase kinase-3beta and cyclin dependent kinase-5 activator (p23) transfected cells. Biochim Biophys Acta 1998;1380:177-182.
29. Bu BT, Li J, Davies P, Vincent I: Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J Neurosci 2002;22:6515-6525.
30. Nguyen MD, Lariviere RC, Julien J-P: Deregulation of cdk5 in a mouse model of ALS: Toxicity alleviated by perikaryal neurofilament inclusions. Neuron 2001;30:135-147.
31. Ahlijanian MK, Barrezueta NX, Williams RD, 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.
32. Bian F, Nath R, Sobocinski G, et al.: Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J Comp Neurology 2002;446:257-266.
33. Noble W, Olm V, Takata K, et al.: Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 2003;38:555-565.
34. Keck S, Nitsch R, Grune T, Ullrich O: Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 2003;85:115-122.
35. Keller JN, Hanni KB, Markesbery WR: Impaired proteasome function in Alzheimer's disease. J Neurochem 2000;75:436-439.
36. Boutillier AL, Kienlen-Campard P, Loeffler JP: Depolarization regulates cyclin D1 degradation and neuronal apoptosis: A hypothesis about the role of the ubiquitin/proteasome signalling pathway. Eur J Neurosci 1999;11:441-448.
37. Qiu JH, Asai A, Chi S, Saito N, Hamada H, Kirino T: Proteasome inhibitors induce cytochrome c-caspase-3-like protease-mediated apoptosis in cultured cortical neurons. J Neurosci 2000;20:259-265.
38. Sengupta A, Kabat J, Novak M, Wu Q, Grundke-Iqbal I, Iqbal K: Phosphorylation of tau at both Thr 231 and Ser 262 is required for maximal inhibition of its binding to microtubules. Arch Biochem Biophys 1998;357:299-309.
39. Evans DB, Rank KB, Bhattacharya K, Thomsen DR, Gurney ME, Sharma SK: Tau phosphorylation at serine 396 and serine 404 by human recombinant tau protein kinase II inhibits tau's ability to promote microtubule assembly. J Biol Chem 2000;275:24977-24983.
40. Li GB, Faibushevich A, Turunen BJ, et al.: Stabilization of the cyclin-dependent kinase 5 activator, p35, by paclitaxel decreases beta-amyloid toxicity in cortical neurons. J Neurochem 2003;84:347-362.
41. Town T, Zolton J, Shaffner R, et al.: p35/Cdk5 pathway mediates soluble amyloid-beta peptide-induced tau phosphorylation in vitro. J Neurosci Res 2002;69:362-372.
42. Alvarez A, Toro R, Caceres A, Maccioni RB: Inhibition of tau phosphorylating protein kinase cdk5 prevents A-amyloid-induced neuronal death. FEBS Lett 1999;459:421-426.
43. Lee M, Kwon YT, Li M, Peng J, Friedlander RM, Tsai L-H: Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000;405:360-364.
44. Wei W, Wang X, Kusiak JW: Signaling events in amyloid beta-peptide-induced neuronal death and insulin-like growth factor I protection. J Biol Chem 2002;277:17649-17656.
45. Michaelis ML, Ranciat N, Chen Y, et al.: Protection against beta-amyloid toxicity in primary neurons by paclitaxel (Taxol). J Neurochem 1998;70:1623-1627.
46. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A: Tau is essential to beta-amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 2002;99:6364-6369.
47. Bancher C, Brunner C, Lassmann H, et al.: Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles and neuropil threads. Brain Res 1989;477:90-99.
48. Augustinack JC, Sanders JL, Tsai LH, Hyman BT: Colocalization and fluorescence resonance energy transfer between cdk5 and AT8 suggests a close association in pre-neurofibrillary tangles and neurofibrillary tangles. J Neuropathol Exp Neurol 2002;61:557-564.
49. Takahashi M, Iseki E, Kosaka K: Cdk5 and munc-18/p67 co-localization in early stage neurofibrillary tangles-bearing neurons in Alzheimer type dementia brains. J Neurol Sci 2000;172:63-69.
50. Pei JJ, Grundke-Iqbal I, Iqbal K, Bogdanovic N, Winblad B, Cowburn RF: Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration. Brain Res 1998;797:267-277.
51. Lee KY, Clark AW, Rosales JL, Chapman K, Fung T, Johnston RN: Elevated neuronal Cdc2-like kinase activity in the Alzheimer disease brain. Neurosci Res 1999;34:21-29.
52. Kusakawa G, Saito T, Ohuki R, Ishiguro K, Kishimoto T, Hisanaga S: Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 2000;275:17166-17172.
53. Nath R, Davis M, Probert AW, et al.: Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem Biophys Res Commun 2000;274:16-21.
54. Patzke H, Tsai L-H: Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. J Biol Chem 2002;277:8054-8060.
55. Tseng HC, Zhou Y, Shen Y, Tsai LH: A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett 2002;523:58-62.
56. Grynspan F, Griffin WR, Cataldo A, Katayama S, Nixon RA: Active site directed antibodies identify calpain II as an early appearing and pervasive component of neurofibrillary pathology in Alzheimer's disease. Brain Res 1997;763:145-158.
57. Hashiguchi M, Saito T, Hisanaga S, Hashiguchi T: Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser(202)/Thr(205) of human tau. J Biol Chem 2002;277:44525-44530.
58. Patrick GN, Zhou PB, Kwon YT, Howley PM, Tsai LH: P35, the neuronal-specific activator of cyclin-dependent kinase 5 (cdk5) is degraded by the ubiquitin-proteasome pathway. J Biol Chem 1998;273:24057-24064.
59. Van den Haute C, Spittaels K, Van Dorpe J, et al.: Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol Dis 2001;8:32-44.
60. Patzke H, Maddineni U, Ayala R, et al: Partial rescue of the p35-/- brain phenotype by low expression of a neuronal-specific enolase p25 transgene. J Neurosci 2003;23:2769-2778.
61. Saito K, Elce JS, Hamos JE, Nixon RA: Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: A potential molecular basis for neuronal degeneration. Proc Natl Acad Sci USA 1993;90:2628-2632.
62. Taniguchi S, Fujita Y, Hayashi S, et al.: Calpain-mediated degradation of p35 to p25 in postmortem human and rat brains. FEBS Lett 2001;489:46-50.
63. Mattson MP, Chan SL: Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium 2003;34:385-397.
64. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K: Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 1985;82:4245-4249.
65. Gibson GE: Interactions of oxidative stress with cellular calcium dynamics and glucose metabolism in Alzheimer's disease. Free Radic Biol Med 2002;32:1061-1070.
66. Takashima A, Murayama M, Yasutake K, Takahashi H, Yokoyama M, Ishiguro K: Involvement of cyclin dependent kinase 5 activator p25 on tau phosphorylation in mouse brain. Neurosci Lett 2001;306:37-40.
67. Tandon A, Yu H, Wang L, et al.: Brain levels of CDK5 activator p25 are not increased in Alzheimer's or other neurodegenerative diseases with neurofibrillary tangles. J Neurochem 2003;86:572-581.
68. Yoo BC, Lubec G: p25 protein in neurodegeneration. Nature 2001;411:763-764; discussion, pp 4-5.
69. Liu F, Su Y, Li BL, et al.: Regulation of amyloid precursor protein (APP) phosphorylation and processing by p35.Cdk5 and p25/Cdk5. FEBS Lett 2003;547:193-196.
70. Iijima K-I, Ando K, Takeda S, et al.: Neuron-specific phosphorylation of Alzheimer's s-amyloid precursor protein by cyclin-dependent kinase 5. J Neurochem 2000;75:1085-1091.
71. Ramelot TA, Nicholson LK: Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J Mol Biol 2001;307:871-884.
72. Ando K, Iijima K, Elliott JI, Kirino Y, Suzuki T: Phosphorylation- dependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of beta-amyloid. J Biol Chem 2001;276:40353-40361.
73. Wolfe MS, Xia WM, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ: Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 1999;398:513-517.
74. Lau KF, Howlett DR, Kesavapany S, et al.: Cyclin-dependent kinase-5/p35 phosphorylates Presenilin 1 to regulate carboxy-terminal fragment stability. Mol Cell Neurosci 2002;20:13-20.