Cdk5, a therapeutic target for Alzheimer's disease?

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1697, Issue 1-2, 2004, Pages 137-142

  Tsai, Li Huei ^a   Lee, Ming Sum ^a   Cruz, Jonathan ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

amyloid; AD; Alzheimer's disease; Amyloid precursor protein; APP; Calpain; Cdk; Cdk5; Cyclin dependent kinase; GDNF; Glia derived neurotrophic factor; Glycosylphosphatidylinositol; GPI; Neurofibrillary tangle; Neurotoxicity; NMDA; p25

Indexed keywords

AMYLOID BETA PROTEIN; CALPAIN; CYCLIN DEPENDENT KINASE 5; DOPAMINE; PROTEIN P25; PROTEIN P35; TAU PROTEIN;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; BRAIN; BRAIN FUNCTION; BRAIN NERVE CELL; CONFERENCE PAPER; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; LEARNING; MEMORY; NERVE FIBER; NEUROFILAMENT; NEUROTOXICITY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TARGETING; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; ENZYME INHIBITORS; HUMANS; NERVE TISSUE PROTEINS;

EID: 1542328910     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2003.11.019     Document Type: Conference Paper

References (70)

1. Dhavan R., Tsai L.H. A decade of CDK5. Nat. Rev., Mol. Cell Biol. 2:2001;749-759.
2. Chae T., Kwon Y.T., Bronson R., Dikkes P., Li E., Tsai L.H. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron. 18:1997;29-42.
3. Ko J., Humbert S., Bronson R.T., Takahashi S., Kulkarni A.B., Li E., Tsai L.H. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 21:2001;6758-6771.
4. Ohshima T., Ward J.M., Huh C.G., Longenecker G., Veeranna, Pant H.C., Brady R.O., Martin L.J., Kulkarni A.B. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. U. S. A. 93:1996;11173-11178.
5. Dhavan R., Greer P.L., Morabito M.A., Orlando L.R., Tsai L.H. The cyclin-dependent kinase 5 activators p35 and p39 interact with the alpha-subunit of Ca2+/calmodulin-dependent protein kinase II and alpha-actinin-1 in a calcium-dependent manner. J. Neurosci. 22:2002;7879-7891.
6. Fischer A., Sananbenesi F., Schrick C., Spiess J., Radulovic J. Cyclin-dependent kinase 5 is required for associative learning. J. Neurosci. 22:2002;3700-3707.
7. Li B.S., Sun M.K., Zhang L., Takahashi S., Ma W., Vinade L., Kulkarni A.B., Brady R.O., Pant H.C. Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc. Natl. Acad. Sci. U. S. A. 98:2001;12742-12747.
8. Tan T.C., Valova V.A., Malladi C.S., Graham M.E., Berven L.A., Jupp O.J., Hansra G., McClure S.J., Sarcevic B., Boadle R.A., Larsen M.R., Cousin M.A., Robinson P.J. Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 5:2003;701-710.
9. Tomizawa K., Ohta J., Matsushita M., Moriwaki A., Li S.T., Takei K., Matsui H. Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 22:2002;2590-2597.
10. Bibb J.A., Snyder G.L., Nishi A., Yan Z., Meijer L., Fienberg A.A., Tsai L.H., Kwon Y.T., Girault J.A., Czernik A.J., Huganir R.L., Hemmings H.C. Jr., Nairn A.C., Greengard P. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature. 402:1999;669-671.
11. Bibb J.A., Chen J., Taylor J.R., Svenningsson P., Nishi A., Snyder G.L., Yan Z., Sagawa Z.K., Ouimet C.C., Nairn A.C., Nestler E.J., Greengard P. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature. 410:2001;376-380.
12. Chen J., Zhang Y., Kelz M.B., Steffen C., Ang E.S., Zeng L., Nestler E.J. Induction of cyclin-dependent kinase 5 in the hippocampus by chronic electroconvulsive seizures: role of [Delta]FosB. J. Neurosci. 20:2000;8965-8971.
13. Tang D., Chun A.C., Zhang M., Wang J.H. Cyclin-dependent kinase 5 (Cdk5) activation domain of neuronal Cdk5 activator. Evidence of the existence of cyclin fold in neuronal Cdk5a activator. J. Biol. Chem. 272:1997;12318-12327.
14. Brown N.R., Noble M.E., Endicott J.A., Garman E.F., Wakatsuki S., Mitchell E., Rasmussen B., Hunt T., Johnson L.N. The crystal structure of cyclin A. Structure. 3:1995;1235-1247.
15. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature. 402:1999;615-622.
16. Patrick G.N., Zhou P., Kwon Y.T., Howley P.M., Tsai L.H. p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteosome pathway. J. Biol. Chem. 273:1998;24057-24064.
17. Tarricone C., Dhavan R., Peng J., Areces L.B., Tsai L.H., Musacchio A. Structure and regulation of the CDK5-p25(nck5a) complex. Mol. Cell. 8:2001;657-669.
18. Humbert S., Dhavan R., Tsai L. p39 activates cdk5 in neurons, and is associated with the actin cytoskeleton. J. Cell Sci. 113:2000;975-983.
19. Cooper J.A., Howell B.W. Lipoprotein receptors: signaling functions in the brain? Cell. 97:1999;671-674.
20. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24:2001;1005-1039.
21. Herz J. The LDL receptor gene family: (un)expected signal transducers in the brain. Neuron. 29:2001;571-581.
22. Keshvara L., Magdaleno S., Benhayon D., Curran T. Cyclin-dependent kinase 5 phosphorylates disabled 1 independently of Reelin signaling. J. Neurosci. 22:2002;4869-4877.
23. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature. 364:1993;717-721.
24. Niethammer M., Smith D.S., Ayala R., Peng J., Ko J., Lee M.S., Morabito M., Tsai L.H. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron. 28:2000;697-711.
25. Sasaki S., Shionoya A., Ishida M., Gambello M.J., Yingling J., Wynshaw-Boris A., Hirotsune S. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron. 28:2000;681-696.
26. Toyo-oka K., Shionoya A., Gambello M.J., Cardoso C., Leventer R., Ward H.L., Ayala R., Tsai L.H., Dobyns W., Ledbetter D., Hirotsune S., Wynshaw-Boris A. 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat. Genet. 34:2003;274-285.
27. Connell-Crowley L., Le Gall M., Vo D.J., Giniger E. The cyclin-dependent kinase Cdk5 controls multiple aspects of axon patterning in vivo. Curr. Biol. 10:2000;599-602.
28. Nikolic M., Dudek H., Kwon Y.T., Ramos Y.F., Tsai L.H. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10:1996;816-825.
29. Pigino G., Paglini G., Ulloa L., Avila J., Caceres A. Analysis of the expression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J. Cell Sci. 110(Pt 2):1997;257-270.
30. Ledda F., Paratcha G., Ibanez C.F. Target-derived GFRalpha1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5. Neuron. 36:2002;387-401.
31. Sasaki Y., Cheng C., Uchida Y., Nakajima O., Ohshima T., Yagi T., Taniguchi M., Nakayama T., Kishida R., Kudo Y., Ohno S., Nakamura F., Goshima Y. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron. 35:2002;907-920.
32. Fletcher A.I., Shuang R., Giovannucci D.R., Zhang L., Bittner M.A., Stuenkel E.L. Regulation of exocytosis by cyclin-dependent kinase 5 via phosphorylation of Munc18. J. Biol. Chem. 274:1999;4027-4035.
33. Floyd S.R., Porro E.B., Slepnev V.I., Ochoa G.C., Tsai L.H., De Camilli P. Amphiphysin 1 binds the cyclin-dependent kinase (cdk) 5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 276:2001;8104-8110.
34. Matsubara M., Kusubata M., Ishiguro K., Uchida T., Titani K., Taniguchi H. Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem. 271:1996;21108-21113.
35. Shuang R., Zhang L., Fletcher A., Groblewski G.E., Pevsner J., Stuenkel E.L. Regulation of Munc-18/syntaxin 1A interaction by cyclin-dependent kinase 5 in nerve endings. J. Biol. Chem. 273:1998;4957-4966.
36. Greengard P., Allen P.B., Nairn A.C. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron. 23:1999;435-447.
37. Lee M.S., Kwon Y.T., Li M., Peng J., Friedlander R.M., Tsai L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature. 405:2000;360-364.
38. Nath R., Davis M., Probert A.W., Kupina N.C., Ren X., Schielke G.P., Wang K.K. Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem. Biophys. Res. Commun. 274:2000;16-21.
39. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275:2000;17166-17172.
40. Kerokoski P., Suuronen T., Salminen A., Soininen H., Pirttila T. Influence of phosphorylation of p35, an activator of cyclin-dependent kinase 5 (cdk5), on the proteolysis of p35. Brain Res. Mol. Brain Res. 106:2002;50.
41. Saito T., Onuki R., Fujita Y., Kusakawa G., Ishiguro K., Bibb J.A., Kishimoto T., Hisanaga S. Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation. J. Neurosci. 23:2003;1189-1197.
42. Tseng H.C., Zhou Y., Shen Y., Tsai L.H. A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett. 523:2002;58-62.
43. Bu B., Li J., Davies P., Vincent I. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J. Neurosci. 22:2002;6515-6525.
44. Nguyen M.D., Lariviere R.C., Julien J.P. Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron. 30:2001;135-147.
45. Otth C., Concha I.I., Arendt T., Stieler J., Schliebs R., Gonzalez-Billault C., Maccioni R.B. AbetaPP induces cdk5-dependent tau hyperphosphorylation in transgenic mice Tg2576. J. Alzheimer's Dis. 4:2002;417-430.
46. Town T., Zolton J., Shaffner R., Schnell B., Crescentini R., Wu Y., Zeng J., DelleDonne A., Obregon D., Tan J., Mullan M. p35/Cdk5 pathway mediates soluble amyloid-beta peptide-induced tau phosphorylation in vitro. J. Neurosci. Res. 69:2002;362-372.
47. Alvarez A., Toro R., Caceres A., Maccioni R.B. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett. 459:1999;421-426.
48. Imahori K., Uchida T. Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. (Tokyo). 121:1997;179-188.
49. Sobue K., Agarwal-Mawal A., Li W., Sun W., Miura Y., Paudel H.K. Interaction of neuronal Cdc2-like protein kinase with microtubule-associated protein tau. J. Biol. Chem. 275:2000;16673-16680.
50. Baumann K., Mandelkow E.M., Biernat J., Piwnica-Worms H., Mandelkow E. Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 336:1993;417-424.
51. Flaherty D.B., Soria J.P., Tomasiewicz H.G., Wood J.G. Phosphorylation of human tau protein by microtubule-associated kinases: GSK3beta and cdk5 are key participants. J. Neurosci. Res. 62:2000;463-472.
52. Ishiguro K., Sato K., Takamatsu M., Park J., Uchida T., Imahori K. Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites. Neurosci. Lett. 202:1995;81-84.
53. Lund E.T., McKenna R., Evans D.B., Sharma S.K., Mathews W.R. Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry. J. Neurochem. 76:2001;1221-1232.
54. Liu W.K., Williams R.T., Hall F.L., Dickson D.W., Yen S.H. Detection of a Cdc2-related kinase associated with Alzheimer paired helical filaments. Am. J. Pathol. 146:1995;228-238.
55. Yamaguchi H., Ishiguro K., Uchida T., Takashima A., Lemere C.A., Imahori K. Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol. (Berl.). 92:1996;232-241.
56. Augustinack J.C., Sanders J.L., Tsai L.H., Hyman B.T. 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. 61:2002;557-564.
57. Pei J.J., Grundke-Iqbal I., Iqbal K., Bogdanovic N., Winblad B., Cowburn R.F. Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration. Brain Res. 797:1998;267-277.
58. Ahlijanian M.K., Barrezueta N.X., Williams R.D., Jakowski A., Kowsz K.P., McCarthy S., Coskran T., Carlo A., Seymour P.A., Burkhardt J.E., Nelson R.B., McNeish J.D. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc. Natl. Acad. Sci. U. S. A. 97:2000;2910-2915.
59. Bian F., Nath R., Sobocinski G., Booher R.N., Lipinski W.J., Callahan M.J., Pack A., Wang K.K., Walker L.C. Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J. Comp. Neurol. 446:2002;257-266.
60. Van den Haute C., Spittaels K., Van Dorpe J., Lasrado R., Vandezande K., Laenen I., Geerts H., Van Leuven F. Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol. Dis. 8:2001;32-44.
61. Noble W., Olm V., Takata K., Casey E., Mary O., Meyerson J., Gaynor K., LaFrancois J., Wang L., Kondo T., Davies P., Burns M., Veeranna, Nixon R., Dickson D., Matsuoka Y., Ahlijanian M., Lau L.F., Duff K. Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron. 38:2003;555-565.
62. Cruz J.C., Tseng H.C., Goldman J.A., Shih H., Tsai L.H. Aberrant cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron. 40:2003;471-483.
63. Hashiguchi M., Saito T., Hisanaga S., Hashiguchi T. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human tau. J. Biol. Chem. 277:2002;44525-44530.
64. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature. 399:1999;A23-A31.
65. Iijima K., Ando K., Takeda S., Satoh Y., Seki T., Itohara S., Greengard P., Kirino Y., Nairn A.C., Suzuki T. Neuron-specific phosphorylation of Alzheimer's beta-amyloid precursor protein by cyclin-dependent kinase 5. J. Neurochem. 75:2000;1085-1091.
66. Aplin A.E., Gibb G.M., Jacobsen J.S., Gallo J.M., Anderton B.H. In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3beta. J. Neurochem. 67:1996;699-707.
67. Standen C.L., Brownlees J., Grierson A.J., Kesavapany S., Lau K.F., McLoughlin D.M., Miller C.C. Phosphorylation of thr(668) in the cytoplasmic domain of the Alzheimer's disease amyloid precursor protein by stress-activated protein kinase 1b (Jun N-terminal kinase-3). J. Neurochem. 76:2001;316-320.
68. Suzuki T., Oishi M., Marshak D.R., Czernik A.J., Nairn A.C., Greengard P. Cell cycle-dependent regulation of the phosphorylation and metabolism of the Alzheimer amyloid precursor protein. EMBO J. 13:1994;1114-1122.
69. Ando K., Iijima K.I., Elliott J.I., 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. 276:2001;40353-40361.
70. Lee M.S., Kao S.C., Lemere C.A., Tseng H.C., Zhou Y., Neve R., Ahlijanian M.K., Tsai L.H. APP processing is regulated by cytoplasmic phosphorylation. J. Cell Biol. 163:2003;83-95.