Cyclin-dependent kinase-5 in neurodegeneration

Journal of Neurochemistry

Volumn 88, Issue 6, 2004, Pages 1313-1326

  Shelton, Shirley B ^a   Johnson, Gail V W ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b Department of Psychiatry   (United States)

Author keywords

Apoptosis; CDK5; Neurodegeneration; p25; p35; Protein phosphorylation

Indexed keywords

CYCLIN DEPENDENT KINASE 5;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CELL SURVIVAL; DEGENERATIVE DISEASE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

EID: 1642269125     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2003.02328.x     Document Type: Review

References (169)

1. Agarwal-Mawal A. and Paudel H. K. (2001) Neuronal Cdc2-like protein kinase (Cdk5/p25) is associated with protein phosphatase 1 and phosphorylates inhibitor-2. J. Biol. Chem. 276, 23712-23718.
2. Ahlijanian M. K., Barrezueta N. X., Williams R. D. et al. (2000) Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc. Natl Acad. Sci. USA 97, 2910-2915.
3. Alvarez A., Toro R., Caceres A. and Maccioni R. B. (1999) Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett. 459, 421-426.
4. Alvarez G., Munoz-Montano J. R., Satrustegui J., Avila J., Bogonez E. and Diaz-Nido J. (2002) Regulation of tau phosphorylation and protection against beta-amyloid-induced neurodegeneration by lithium. Possible implications for Alzheimer's disease. Bipolar Disord. 4, 153-165.
5. Andersson M., Hilbertson A. and Cenci M. A. (1999) Striatal fosB expression is causally linked with 1-DOPA-induced abnormal involuntary movements and the associated upregulation of striatal prodynorphin mRNA in a rat model of Parkinson's disease. Neurobiol. Dis. 6, 461-474.
6. Andorfer C., Kress Y., Espinoza M., De Silva R., Tucker K. L., Barde Y. A., Duff K. and Davies P. (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem. 86, 582-590.
7. Angelo M., Plattner F., Irvine E. E. and Giese K. P. (2003) Improved reversal learning and altered fear conditioning in transgenic mice with regionally restricted p25 expression. Eur. J. Neurosci. 18, 423-431.
8. Augustinack J. C., Sanders J. L., Tsai L. H. and Hyman B. T. (2002) 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. 61, 557-564.
9. Bajaj N. P., Al-Sarraj S. T., Anderson V., Kibble M., Leigh N. and Miller C. C. (1998) Cyclin-dependent kinase-5 is associated with lipofuscin in motor neurones in amyotrophic lateral sclerosis. Neurosci. Lett. 245, 45-48.
10. Barrow C. J. and Zagorski M. G. (1991) Solution structures of beta peptide and its constituent fragments: relation to amyloid deposition. Science 253, 179-182.
11. Bian F., Nath R., Sobocinski G., Booher R. N., Lipinski W. J., Callahan M. J., Pack A., Wang K. K. and Walker L. C. (2002) Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J. Comp. Neurol. 446, 257-266.
12. Bibb J. A., Snyder G. L., Nishi A. et al. (1999) Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 402, 669-671.
13. Bibb J. A., Chen J., Taylor J. R. et al. (2001a) Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380.
14. Bibb J. A., Nishi A., O'Callaghan J. P. et al. (2001b) Phosphorylation of protein phosphatase inhibitor-1 by Cdk5. J. Biol. Chem. 276, 14490-14497.
15. Borghi R., Giliberto L., Assini A., Delacourte A., Perry G., Smith M. A., Strocchi P., Zaccheo D. and Tabaton M. (2002) Increase of cdk5 is related to neurofibrillary pathology in progressive supranuclear palsy. Neurology 58, 589-592.
16. Braak H. and Braak E. (1997) Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol. Aging 18, S85-S88.
17. Brion J. P. and Couck A. M. (1995) Cortical and brainstem-type Lewy bodies are immunoreactive for the cyclin-dependent kinase 5. Am. J. Pathol. 147, 1465-1476.
18. Bu B., Li J., Davies P. and Vincent I. (2002) Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J. Neurosci. 22, 6515-6525.
19. Chae T., Kwon Y. T., Bronson R., Dikkes P., Li E. and Tsai L. H. (1997) Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42.
20. Chen J., Zhang Y., Kelz M. B., Steffen C., Ang E. S., Zeng L. and Nestler E. J. (2000) Induction of cyclin-dependent kinase 5 in the hippocampus by chronic electroconvulsive seizures: role of [Delta]FosB. J. Neurosci. 20, 8965-8971.
21. Cheng K., Li Z., Fu W. Y., Wang J. H., Fu A. K. and Ip N. Y. (2002) Pctairel interacts with p35 and is a novel substrate for Cdk5/p35. J. Biol. Chem. 277, 31988-31993.
22. Citron M., Westaway D., Xia W. et al. (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat. Med. 3, 67-72.
23. Cyr M., Beaulieu J. M., Laakso A., Somikova T. D., Yao W. D., Bohn L. M., Gainetdinov R. R. and Caron M. G. (2003) Sustained elevation of extracellular dopamine causes motor dysfunction and selective degeneration of striatal GABAergic neurons. Proc. Natl Acad. Sci. USA 100, 11035-11040.
24. Davis P. K., Dudek S. M. and Johnson G. V. (1997) Select alterations in protein kinases and phosphatases during apoptosis of differentiated PC12 cells. J. Neurochem. 68, 2338-2347.
25. De Strooper B. (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38, 9-12.
26. Fahn S. (2003) Description of Parkinson's disease as a clinical syndrome. Ann. NY Acad. Sci. 991, 1-14.
27. Ferreira A., Lu Q., Orecchio L. and Kosik K. S. (1997) Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar A beta. Mol. Cell. Neurosci. 9, 220-234.
28. Fischer A., Sananbenesi F., Schrick C., Spiess J. and Radulovic J. (2002) Cyclin-dependent kinase 5 is required for associative learning. J. Neurosci. 22, 3700-3707.
29. Fischer A., Sananbenesi F., Schrick C., Spiess J. and Radulovic J. (2003) Regulation of contextual fear conditioning by baseline and inducible septo-hippocampal cyclin-dependent kinase 5. Neuropharmacology 44, 1089-1099.
30. Fletcher A. I., Shuang R., Giovannucci D. R., Zhang L., Bittner M. A. and Stuenkel E. L. (1999) Regulation of exocytosis by cyclin-dependent kinase 5 via phosphorylation of Munc18. J. Biol. Chem. 274, 4027-4035.
31. Floyd S. R., Porro E. B., Slepnev V. I., Ochoa G. C., Tsai L. H. and De Camilli P. (2001) Amphiphysin 1 binds the cyclin-dependent kinase (cdk) 5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 276, 8104-8110.
32. Fu A. K., Fu W. Y., Cheung J., Tsim K. W., Ip F. C., Wang J. H. and lp N. Y. (2001) Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction. Nat. Neurosci. 4, 374-381.
33. Fu W. Y., Fu A. K., Lok K. C., Ip F. C. and Ip N. Y. (2002) Induction of Cdk5 activity in rat skeletal muscle after nerve injury. Neuroreport 13, 243-247.
34. Gong C. X., Grundke-Iqbal I., Damuni Z. and Iqbal K. (1994) Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease. FEBS Lett. 341, 94-98.
35. Gong X., Tang X., Wiedmann M., Wang X., Peng J., Zheng D., Blair L. A., Marshall J. and Mao Z. (2003) Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38, 33-46.
36. Green S. L., Vulliet P. R., Pinter M. J. and Cork L. C. (1998) Alterations in cyclin-dependent protein kinase 5 (CDK5) protein levels, activity and immunocytochemistry in canine motor neuron disease. J. Neuropathol. Exp. Neurol. 57, 1070-1077.
37. Gupta A., Tsai L. H. and Wynshaw-Boris A. (2002) Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3, 342-355.
38. Gupta A., Sanada K., Miyamoto D. T., Rovelstad S., Nadarajah B., Pearlman A. L., Brunstrom J. and Tsai L. H. (2003) Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci. 6, 1284-1291.
39. Hallows J. L., Chen K., DePinho R. A. and Vincent I. (2003) Decreased cyclin-dependent kinase 5 (cdk5) activity is accompanied by redistribution of cdk5 and cytoskeletal proteins and increased cytoskeletal protein phosphorylation in p35 null mice. J. Neurosci. 23, 10633-10644.
40. Hamdane M., Sambo A. V., Delobel P., Begard S., Violleau A., Delacourte A., Bertrand P., Benavides J. and Buee L. (2003) Mitotic-like Tau phosphorylation by p25/Cdk5 kinase corhplex. J. Biol. Chem. 278, 34026-34034.
41. Hashiguchi M., Saito T., Hisanaga S. and Hashiguchi T. (2002) Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human tau. J. Biol. Chem. 277, 44525-44530.
42. Hellmich M. R., Pant H. C., Wada E. and Battey J. F. (1992) Neuronal cdc2-like kinase: a cdc2-related protein kinase with predominantly neuronal expression. Proc. Natl Acad. Sci. USA 89, 10867-10871.
43. Honjyo Y., Kawamoto Y., Nakamura S., Nakano S. and Akiguchi I. (2001) P39 immunoreactivity in glial cytoplasmic inclusions in brains with multiple system atrophy. Acta Neuropathol. (Berlin) 101, 190-194.
44. Honma N., Asada A., Takeshita S. et al. (2003) Apoptosis-associated tyrosine kinase is a Cdk5 activator p35 binding protein. Biochem. Biophys. Res. Commun. 310, 398-404.
45. Hoshi M., Sato M., Matsumoto S., Noguchi A., Yasutake K., Yoshida N. and Sato K. (2003) Spherical aggregates of beta-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3beta. Proc. Natl Acad. Sci. USA 100, 6370-6375.
46. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F. and Cole G. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
47. Huang D., Patrick G., Moffat J., Tsai L. H. and Andrews B. (1999) Mammalian Cdk5 is a functional homologue of the budding yeast Pho85 cyclin-dependent protein kinase. Proc. Natl Acad. Sci. USA 96, 14445-14450.
48. Huang K. X. and Paudel H. K. (2000) Ser67-phosphorylated inhibitor 1 is a potent protein phosphatase I inhibitor. Proc. Natl Acad. Sci. USA 97, 5824-5829.
49. Huang Q. Q., Lee K. Y. and Wang J. H. (1996) A novel yeast protein showing specific association with the cyclin-dependent kinase 5. FEBS Lett. 378, 48-50.
50. Humbert S., Dhavan R. and Tsai L. (2000) p39 activates cdk5 in neurons, and is associated with the actin cytoskeleton. J. Cell Sci. 113, 975-983.
51. Iijima K., Ando K., Takeda S., Satoh Y., Seki T., Itohara S., Greengard P., Kirino Y., Naim A. C. and Suzuki T. (2000) Neuron-specific phosphorylation of Alzheimer's beta-amyloid precursor protein by cyclin-dependent kinase 5. J. Neurochem. 75, 1085-1091.
52. Ishiguro K., Takamatsu M., Tomizawa K., Omori A., Takahashi M., Arioka M., Uchida T. and Imahori K. (1992) Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J. Biol. Chem. 267, 10897-10901.
53. Jeffrey P. D., Russo A. A., Polyak K., Gibbs E., Hurwitz J., Massague J. and Pavletich N. P. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376, 313-320.
54. Jeong Y. G., Rosales J. L., Marzban H., Sillitoe R. V., Park D. G., Hawkes R. and Lee K. Y. (2003) The cyclin-dependent kinase 5 activator, p39, is expressed in stripes in the mouse cerebellum. Neuroscience 118, 323-334.
55. Johnson G. V. and Bailey C. D. (2002) Tau, where are we now? J. Alzheimers Dis. 4, 375-398.
56. Johnson G. V. W. and Hartigan J. A. (1999) Tau protein in normal and Alzheimer's disease brain: an update. Alzheimers Dis. Rev. 3, 125-141.
57. Julien J. P. (1999) Neurofilament functions in health and disease. Curr. Opin. Neurobiol. 9, 554-560.
58. Julien J. P. (2001) Amyotrophic lateral sclerosis: unfolding the toxicity of the misfolded. Cell 104, 581-591.
59. Kato G. and Maeda S. (1999) Neuron-specific Cdk5 kinase is responsible for mitosis-independent phosphorylation of c-Src at Ser75 in human Y79 retinoblastoma cells. J. Biochem. (Tokyo) 126, 957-961.
60. Kerokoski P., Suuronen T., Salminen A., Soininen H. and Pirttila T. (2001) The levels of cdk5 and p35 proteins and tau phosphorylation are reduced during neuronal apoptosis. Biochem. Biophys. Res. Commun. 280, 998-1002.
61. Kerokoski P., Suuronen T., Salminen A., Soininen H. and Pirttila T. (2002a) Influence of phosphorylation of p35, an activator of cyclin-dependent kinase 5 (cdk5), on the proteolysis of p35. Brain Res. Mol. Brain Res. 106, 50-56.
62. Kerokoski P., Suuronen T., Salminen A., Soininen H. and Pirttila T. (2002b) Cleavage of the cyclin-dependent kinase 5 activator p35 to p25 does not induce tau hyperphosphorylation. Biochem. Biophys. Res. Commun. 298, 693-698.
63. Kesavapany S., Lau K. F., McLoughlin D. M., Brownlees J., Ackerley S., Leigh P. N., Shaw C. E. and Miller C. C. (2001) p35/cdk5 binds and phosphorylates beta-catenin and regulates beta-catenin/presenilin-1 interaction. Eur J. Neurosci. 13, 241-247.
64. Kesavapany S., Lau K. F., Ackerley S., Banner S. J., Shemilt S. J., Cooper J. D., Leigh P. N., Shaw C. E., McLoughlin D. M. and Miller C. C. (2003) Identification of a novel, membrane-associated neuronal kinase, cyclin-dependent kinase 5/p35-regulated kinase. J. Neurosci. 23, 4975-4983.
65. Keshvara L., Magdaleno S., Benhayon D. and Curran T. (2002) Cyclin-dependent kinase 5 phosphorylates disabled I independently of Reelin signaling. J. Neurosci. 22, 4869-4877.
66. Kirschenbaum F., Hsu S. C., Cordell B. and McCarthy J. V. (2001) Substitution of a glycogen synthase kinase-3beta phosphorylation site in presenilin 1 separates presenilin function from beta-catenin signaling. J. Biol. Chem. 276, 7366-7375.
67. Kobayashi S., Ishiguro K., Omori A., Takamatsu M., Arioka M., Imahori K. and Uchida T. (1993) A cdc2-related kinase PSSALRE/cdk5 is homologous with the 30 kDa subunit of tau protein kinase II, a proline-directed protein kinase associated with microtubule. FEBS Lett. 335, 171-175.
68. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T. and Hisanaga S. (2000) Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275, 17166-17172.
69. Kwon Y. T., Tsai L. H. and Crandall J. E. (1999) Callosal axon guidance defects in p35 (-/-) mice. J. Comp. Neurol. 415, 218-229.
70. Kwon Y. T., Gupta A., Zhou Y., Nikolic M. and Tsai L. H. (2000) Regulation of N-cadherin-mediated adhesion by the p35-Cdk5 kinase. Curr. Biol. 10, 363-372.
71. Lau K. F., Howlett D. R., Kesavapany S., Standen C. L., Dingwall C., McLoughlin D. M. and Miller C. C. (2002a) Cyclin-dependent kinase-5/p35 phosphorylates Presenilin 1 to regulate carboxy-terminal fragment stability. Mol. Cell. Neurosci. 20, 13-20.
72. Lau L. F., Seymour P. A., Sanner M. A. and Schachter J. B. (2002b) Cdk5 as a drug target for the treatment of Alzheimer's disease. J. Mol. Neurosci. 19, 267-273.
73. Le Roch K., Sestier C., Dorin D., Waters N., Kappes B., Chakrabarti D., Meijer L. and Doerig C. (2000) Activation of a Plasmodium falciparum cdc2-related kinase by heterologous p25 and cyclin H. Functional characterization of a P. falciparum cyclin homologue. J. Biol. Chem. 275, 8952-8958.
74. Lee K. Y., Helbing C. C., Choi K. S., Johnston R. N. and Wang J. H. (1997) Neuronal Cdc2-like kinase (Nclk) binds and phosphorylates the retinoblastoma protein. J. Biol. Chem. 272, 5622-5626.
75. Lee M. S., Kwon Y. T., Li M., Peng J., Friedlander R. M. and Tsai L. H. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364.
76. Lew J., Winkfein R. J., Paudel H. K. and Wang J. H. (1992a) Brain proline-directed protein kinase is a neurofilament kinase which displays high sequence homology to p34cdc2. J. Biol. Chem. 267, 25922-25926.
77. Lew J., Beaudette K., Litwin C. M. and Wang J. H. (1992b) Purification and characterization of a novel proline-directed protein kinase from bovine brain. J. Biol. Chem. 267, 13383-13390.
78. Lew J., Huang Q. Q., Qi Z., Winkfein R. J., Aebersold R., Hunt T. and Wang J. H. (1994) A brain-specific activator of cyclin-dependent kinase 5. Nature 371, 423-426.
79. Li B. S., Sun M. K., Zhang L., Takahashi S., Ma W., Vinade L., Kulkarni A. B., Brady R. O. and Pant H. C. (2001) Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc. Natl Acad. Sci. USA 98, 12742-12747.
80. Li B. S., Zhang L., Takahashi S., Ma W., Jaffe H., Kulkarni A. B. and Pant H. C. (2002) Cyclin-dependent kinase 5 prevents neuronal apoptosis by negative regulation of c-Jun N-terminal kinase 3. EMBO J. 21, 324-333.
81. Li B. S., Ma W., Jaffe H., Zheng Y., Takahashi S., Zhang L., Kulkarni A. B. and Pant H. C. (2003) Cdk5 is involved in neuregulin-dependent activation of PI-3 kinase and Akt activity mediating neuronal survival. J. Biol. Chem.
82. Litersky J. M. and Johnson G. V. (1992) Phosphorylation by cAMP-dependent protein kinase inhibits the degradation of tau by calpain. J. Biol. Chem. 267, 1563-1568.
83. Liu D. X. and Greene L. A. (2001) Neuronal apoptosis at the GI/S cell cycle checkpoint. Cell Tissue Res. 305, 217-228.
84. Liu F., Ma X. H., Ule J., Bibb J. A., Nishi A., DeMaggio A. J., Yan Z., Nairn A. C. and Greengard P. (2001) Regulation of cyclin-dependent kinase 5 and casein kinase 1 by metabotropic glutamate receptors. Proc. Natl Acad. Sci. USA 98, 11062-11068.
85. Liu F., Iqbal K., Grundke-Iqbal I. and Gong C. X. (2002a) Involvement of aberrant glycosylation in phosphorylation of tau by cdk5 and GSK-3beta. FEBS Lett. 530, 209-214.
86. Liu F., Virshup D. M., Nairn A. C. and Greengard P. (2002b) Mechanism of regulation of casein kinase I activity by group I metabotropic glutamate receptors. J. Biol. Chem. 277, 45393-45399.
87. Liu F., Su Y., Li B., Zhou Y., Ryder J., Gonzalez-DeWhitt P., May P. C. and Ni B. (2003) Regulation of amyloid precursor protein (APP) phosphorylation and processing by p35/Cdk5 and p25/Cdk5. FEBS Lett. 547, 193-196.
88. Lund E. T., McKenna R., Evans D. B., Sharma S. K. and Mathews W. R. (2001) Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry. J. Neurochem. 76, 1221-1232.
89. Ma E. and Haddad G. (1999) A Drosophila CDK5alpha-like molecule and its possible role in response to O(2) deprivation. Biochem. Biophys. Res. Commun. 261, 459-463.
90. Martin C. P., Vazquez J., Avila J. and Moreno F. J. (2002) P24, a glycogen synthase kinase 3 (GSK 3) inhibitor. Biochim. Biophys. Acta 1586, 113-122.
91. Matsubara M., Kusubata M., Ishiguro K., Uchida T., Titani K. and Taniguchi H. (1996) Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem. 271, 21108-21113.
92. Matsuura I., Bondarenko V. A., Maeda T., Kachi S., Yamazaki M., Usukura J., Hayashi F. and Yamazaki A. (2000) Phosphorylation by cyclin-dependent protein kinase 5 of the regulatory subunit of retinal cGMP phosphodiesterase. I. Identification of the kinase and its role in the turnoff of phosphodiesterase in vitro. J. Biol. Chem. 275, 32950-32957.
93. Meikrantz W. and Schlegel R. (1996) Suppression of apoptosis by dominant negative mutants of cyclin-dependent protein kinases. J. Biol. Chem. 271, 10205-10209.
94. Meyerson M., Enders G. H., Wu C. L., Su L. K., Gorka C., Nelson C., Harlow E. and Tsai L. H. (1992) A family of human cdc2-related protein kinases. EMBO J. 11, 2909-2917.
95. Michaelis M. L. (2003) Drugs targeting Alzheimer's disease: some things old and some things new. J. Pharmacol. Exp. Ther. 304, 897-904.
96. Morrison R. S., Kinoshita Y., Johnson M. D., Guo W. and Garden G. A. (2003) p-53-Dependent cell death signaling in neurons. Neurochem. Res. 28, 15-27.
97. Muravenko O. V., Gizatullin R. Z., Protopopov A. I., Kashuba V. I., Zabarovsky E. R. and Zelenin A. V. (2000) Assignment of CDK5R2 coding for the cyclin-dependent kinase 5, regulatory subunit 2 (NCK5AI protein) to human chromosome band 2q35 by fluorescent in situ hybridization. Cytogenet. Cell Genet. 89, 160-161.
98. Nakamura S., Kawamoto Y., Nakano S., Ikemoto A., Akiguchi I. and Kimura J. (1997) Cyclin-dependent kinase 5 in Lewy body-like inclusions in anterior horn cells of a patient with sporadic amyotrophic lateral sclerosis. Neurology 48, 267-270.
99. Nakamura S., Kawamoto Y., Nakano S., Akiguchi I. and Kimura J. (1998) Cyclin-dependent kinase 5 and mitogen-activated protein kinase in glial cytoplasmic inclusions in multiple system atrophy. J. Neuropathol. Exp. Neurol. 57, 690-698.
100. Nakano S., Akiguchi I., Nakamura S., Satoi H., Kawashima S. and Kimura J. (1999) Aberrant expression of cyclin-dependent kinase 5 in inclusion body myositis. Neurology 53, 1671-1676.
101. Namgung U., Choi B., Lee J., Jun S. and Kim K. T. (2002) Activation of cyclin-dependent kinase 5 (Cdk5) is involved in axonal regeneration. Program no. 535.12, in 2002 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, D.C.
102. Nath R., Davis M., Probert A. W., Kupina N. C., Ren X., Schielke G. P. and Wang K. K. (2000) Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem. Biophys. Res. Commun. 274, 16-21.
103. Neystat M., Rzhetskaya M., Oo T. F., Kholodilov N., Yarygina O., Wilson A., El-Khodor B. F. and Burke R. E. (2001) Expression of cyclin-dependent kinase 5 and its activator p35 in models of induced apoptotic death in neurons of the substantia nigra in vivo. J. Neurochem. 77, 1611-1625.
104. Nguyen M. D., Lariviere R. C. and Julien J. P. (2001) Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron 30, 135-147.
105. Nguyen K. C., Rosales J. L., Barboza M. and Lee K. Y. (2002a) Controversies over p25 in Alzheimer's disease. J. Alzheimers Dis. 4, 123-126.
106. Nguyen M. D., Mushynski W. E. and Julien J. P. (2002b) Cycling at the interface between neurodevelopment and neurodegeneration. Cell Death Differ 9, 1294-1306.
107. Nguyen M. D., Boudreau M., Kriz J., Couillard-Despres S., Kaplan D. R. and Julien J. P. (2003) Cell cycle regulators in the neuronal death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase 1. J. Neurosci. 23, 2131-2140.
108. Niethammer M., Smith D. S., Ayala R., Peng J., Ko J., Lee M. S., Morabito M. and Tsai L. H. (2000) NUDEL is a novel Cdk5 substrate that associates with LIS I and cytoplasmic dynein. Neuron 28, 697-711.
109. Nikolic M., Dudek H., Kwon Y. T., Ramos Y. F. and Tsai L. H. (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10, 816-825.
110. Nikolic M., Chou M. M., Lu W., Mayer B. J. and Tsai L. H. (1998) The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pakl activity. Nature 395, 194-198.
111. Nilden F., Backstrom A. and Bark C. (1998) Molecular cloning and characterisation of a mouse gene encoding an isoform of the neuronal cyclin-dependent kinase 5 (CDK5) activator. Biochim. Biophys. Acta 1398, 371-376.
112. Nishizawa M., Kanaya Y. and Toh E. A. (1999) Mouse cyclin-dependent kinase (Cdk) 5 is a functional homologue of a yeast Cdk, pho85 kinase. J. Biol. Chem. 274, 33859-33862.
113. Noble W., Olm V., Takata K. et al. (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38, 555-565.
114. Nunan J. and Small D. H. (2002) Proteolytic processing of the amyloid-beta protein precursor of Alzheimer's disease. Essays Biochem. 38, 37-49.
115. Ohshima T., Ward J. M., Huh C. G., Longenecker G., Veeranna Pant H. C., Brady R. O., Martin L. J. and Kulkarni A. B. (1996) Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl Acad. Sci. USA 93, 11173-11178.
116. Otth C., Concha I. I., Arendt T., Stieler J., Schliebs R., Gonzalez-Billault C. and Maccioni R. B. (2002) AbetaPP induces cdk5-dependent tau hyperphosphorylation in transgenic mice Tg2576. J. Alzheimers Dis. 4, 417-430.
117. Paglini G., Peris L., Diez-Guerra J., Quiroga S. and Caceres A. (2001) The Cdk5-p35 kinase associates with the Golgi apparatus and regulates membrane traffic. EMBO Rep. 2, 1139-1144.
118. Patrick G. N., Zhou P., Kwon Y. T., Howley P. M. and Tsai L. H. (1998) p35, The neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J. Biol. Chem. 273, 24057-24064.
119. Patrick G. N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P. and Tsai L. H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622.
120. Patzke H. and Tsai L. H. (2002) Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. J. Biol. Chem. 277, 8054-8060.
121. Patzke H., Maddineni U., Ayala R., Morabito M., Volker J., Dikkes P., Ahlijanian M. K. and Tsai L. H. (2003) Partial rescue of the p35-/-brain phenotype by low expression of a neuronal-specific enolase p25 transgene. J. Neurosci. 23, 2769-2778.
122. Paudel H. K., Lew J., Ali Z. and Wang J. H. (1993) 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. 268, 23512-23518.
123. Picconi B., Centonze D., Hakansson K., Bemardi G., Greengard P., Fisone G., Cenci M. A. and Calabresi P. (2003) Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat. Neurosci. 6, 501-506.
124. Pigino G., Paglini G., Ulloa L., Avila J. and Caceres A. (1997) Analysis of the expression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J. Cell Sci. 110, 257-270.
125. Rajgopal Y. and Vemuri M. C. (2001) Ethanol induced changes in cyclin-dependent kinase-5 activity and its activators, P35, P67 (Munc-18) in rat brain. Neurosci. Lett. 308, 173-176.
126. Rashid T., Banerjee M. and Nikolic M. (2001) Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. J. Biol. Chem. 276, 49043-49052.
127. Rosales J. L., Lee B. C., Modarressi M., Sarker K., Lee K. Y., Jeong Y. G. and Oko R. (2004) Outer dense fibers serve as functional target for Cdk5/p35 in the developing sperm tail. J. Biol. Chem. 279, 1224-1232.
128. Rosen D. R., Siddique T., Patterson D. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62.
129. Sahlgren C. M., Mikhailov A., Vaittinen S., Pallari H. M., Kalimo H., Pant H. C. and Eriksson J. E. (2003) Cdk5 regulates the organization of nestin and its association with p35. Mol. Cell Biol. 23, 5090-5106.
130. Saito K., Elce J. S., Hamos J. E. and Nixon R. A. (1993) 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 90, 2628-2632.
131. Saito T., Onuki R., Fujita Y., Kusakawa G., Ishiguro K., Bibb J. A., Kishimoto T. and Hisanaga S. (2003) Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation. J. Neurosci. 23, 1189-1197.
132. Sasaki Y., Cheng C., Uchida Y. et al. (2002) Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35, 907-920.
133. Sastry P. S. and Rao K. S. (2000) Apoptosis and the nervous system. J. Neurochem. 74, 1-20.
134. Sharma P., Veeranna Sharma M., Amin N. D., Sihag R. K., Grant P., Ahn N., Kulkarni A. B. and Pant H. C. (2002a) Phosphorylation of MEK1 by cdk5/p35 down-regulates the mitogen-activated protein kinase pathway. J. Biol. Chem. 277, 528-534.
135. Sharma S. K., Brock D. A., Ammann R. R., DeShazo T., Khosla M., Gomer R. H. and Weeks G. (2002b) The cdk5 homologue, crp, regulates endocytosis and secretion in Dictyostelium and is necessary for optimum growth and differentiation. Dev. Biol. 247, 1-10.
136. Shetty K. T., Kaech S., Link W. T., Jaffe H., Flores C. M., Wray S., Pant H. C. and Beushausen S. (1995) Molecular characterization of a neuronal-specific protein that stimulates the activity of Cdk5. J. Neurochem. 64, 1988-1995.
137. Sisodiya S. M., Thom M., Lin W. R., Bajaj N. P., Cross J. H. and Harding B. N. (2002) Abnormal expression of cdk5 in focal cortical dysplasia in humans. Neurosci. Lett. 328, 217-220.
138. Smith P. D., Crocker S. J., Jackson-Lewis V., Callaghan S. M., Slack R. S., Lee R., Hayley S., Przedborski S., Anisman H. and Park D. S. (2002) Inhibition of cyclin-dependent kinase 5 (cdk5) prevents dopamine neuron degeneration and locomotor deficits in an MPTP mouse model of Parkinson's disease. Program no. 487.7, in 2002 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, D.C.
139. Spittaels K., Van den Haute C., Van Dorpe J. et al. (2000) Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem. 275, 41340-41349.
140. Strocchi P., Pession A. and Dozza B. (2003) Up-regulation of cDK5/p35 by oxidative stress in human neuroblastoma IMR-32 cells. J. Cell Biochem. 88, 758-765.
141. Takahashi K., Hamada N. and Yamamoto D. (2002) Ras target protein canoe is a substrate for Cdc2 and Cdk5 kinases. Arch. Insect Biochem. Physiol. 49, 102-107.
142. Takahashi S., Saito T., Hisanaga S. I., Pant H. C. and Kulkarni A. B. (2003) Tau phosphorylation by cyclin-dependent kinase5/p39 during brain development reduces its affinity for microtubules. J. Biol. Chem. 278, 10506-10515.
143. Takashima A., Murayama M., Yasutake K., Takahashi H., Yokoyama M. and Ishiguro K. (2001) Involvement of cyclin dependent kinase5 activator p25 on tau phosphorylation in mouse brain. Neurosci. Lett. 306, 37-40.
144. Tan T. C., Valova V. A., Malladi C. S. et al. (2003) Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 5, 701-710.
145. Tandon A., Yu H., Wang L. et al. (2003) Brain levels of CDK5 activator p25 are not increased in Alzheimer's or other neurodegenerative diseases with neurofibrillary tangles. J. Neurochem. 86, 572-581.
146. Tang D., Yeung J., Lee K. Y., Matsushita M., Matsui H., Tomizawa K., Hatase O. and Wang J. H. (1995) An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. J. Biol. Chem. 270, 26897-26903.
147. Tarricone C., Dhavan R., Peng J., Areces L. B., Tsai L. H. and Musacchio A. (2001) Structure and regulation of the CDK5-p25 (nck5a) complex. Mol. Cell 8, 657-669.
148. Tekumalla P. K., Calon F., Rahman Z., Birdi S., Rajput A. H., Horny-kiewicz O., Di Paolo T., Bedard P. J. and Nestler E. J. (2001) Elevated levels of DeltaFosB and RGS9 in striatum in Parkinson's disease. Biol. Psychiat. 50, 813-816.
149. Tomizawa K., Ohta J., Matsushita M., Moriwaki A., Li S. T., Takei K. and Matsui H. (2002) Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 22, 2590-2597.
150. Tsai L. H. (2003) The role of cyclin-dependent kinase 5 in brain development and degeneration. Cell. Mol. Biol. Lett. 8, 546-547.
151. Tsai L. H., Takahashi T., Caviness V. S. Jr and Harlow E. (1993) Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119, 1029-1040.
152. Tsai L. H., Delalle I., Caviness V. S. Jr, Chae T. and Harlow E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423.
153. Tseng H. C., Zhou Y., Shen Y. and Tsai L. H. (2002) A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett. 523, 58-62.
154. Uchida T., Ishiguro, K., Ohnuma J., Takamatsu M., Yonekura S. and Imahori K. (1994) Precursor of cdk5 activator, the 23 kDa subunit of tau protein kinase II: its sequence and developmental change in brain. FEBS Lett. 355, 35-40.
155. Van den Haute C., Spittaels K., Van Dorpe J., Lasrado R., Vandezande K., Laenen I., Geerts H. and Van Leuven F. (2001) Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol. Dis. 8, 32-44.
156. Vartiainen N., Keksa-Goldsteine V., Goldsteins G. and Koistinaho J. (2002) Aspirin provides cyclin-dependent kinase 5-dependent protection against subsequent hypoxia/reoxygenation damage in culture. J. Neurochem. 82, 329-335.
157. Walling A. D. (1999) Amyotrophic lateral sclerosis: Lou Gehrig's disease. Am. Fam. Physician 59, 1489-1496.
158. Wang J., Liu S., Fu Y., Wang J. H. and Lu Y. (2003) Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat. Neurosci.
159. Weishaupt J. H., Kussmaul L., Grotsch P., Heckel A., Rohde G., Romig H., Bahr M. and Gillardon F. (2003) Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction. Mol. Cell. Neurosci. 24, 489-502.
160. Wong P. C., Pardo C. A., Borchelt D. R., Lee M. K., Copeland N. G., Jenkins N. A., Sisodia S. S., Cleveland D. W. and Price D. L. (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14, 1105-1116.
161. Xie Z., Sanada K., Samuels B. A., Shih H. and Tsai L. H. (2003) Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114, 469-482.
162. Xiong W., Pestell R. and Rosner M. R. (1997) Role of cyclins in neuronal differentiation of immortalized hippocampal cells. Mol. Cell Biol. 17, 6585-6597.
163. Xiong Y., Zhang H. and Beach D. (1992) D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71, 505-514.
164. Yang H. S. and Hinds P. W. (2003) Increased ezrin expression and activation by CDK5 coincident with acquisition of the senescent phenotype. Mol. Cell 11, 1163-1176.
165. Yoo B. C. and Lubec G. (2001) p25 protein in neurodegeneration. Nature 411, 763-765.
166. Zhang J. and Johnson G. V. (2000) Tau protein is hyperphosphorylated in a site-specific manner in apoptotic neuronal PC12 cells. J. Neurochem. 75, 2346-2357.
167. Zhang J., Krishnamurthy P. K. and Johnson G. V. (2002a) Cdk5 phosphorylates p53 and regulates its activity. J. Neurochem. 81, 307-313.
168. Zhang Y., McLaughlin R., Goodyer C. and LeBlanc A. (2002b) Selective cytotoxicity of intracellular amyloid beta peptide 1-42 through p53 and Bax in cultured primary human neurons. J. Cell Biol. 156, 519-529.
169. Zukerberg L. R., Patrick G. N., Nikolic M., Humbert S., Wu C. L., Lanier L. M., Gertler F. B., Vidal M., Van Etten R. A. and Tsai L. H. (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite out-growth. Neuron 26, 633-646.