Brain levels of CDK5 activator p25 are not increased in Alzheimer's or other neurodegenerative diseases with neurofibrillary tangles

Journal of Neurochemistry

Volumn 86, Issue 3, 2003, Pages 572-581

  Tandon, Anurag ^a,c   Yu, Haung ^c   Wang, Linda ^c   Rogaeva, Ekaterina ^a,c   Sato, Christine ^c   Chishti, M Azhar ^c   Kawarai, Toshitaka ^c   Hasegawa, Hiroshi ^c   Chen, Fusheng ^c   Davies, Peter ^d   Fraser, Paul E ^a,c   Westaway, David ^b,c   St George Hyslop, Peter H ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

amyloid; Neurofibrillary tangles; Tau

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN PROTEIN; CALPAIN; CYCLIN DEPENDENT KINASE 5; ENZYME ACTIVATOR; PROTEIN P25; PROTEIN P35; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICOBASAL DEGENERATION; DEGENERATIVE DISEASE; DOWN SYNDROME; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMAN; HUMAN TISSUE; MALE; NEUROFIBRILLARY TANGLE; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; BRAIN; BRAIN CHEMISTRY; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NEUROFIBRILLARY TANGLES;

EID: 0041803010     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01865.x     Document Type: Article

References (48)

1. 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. and McNeish J. D. (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.
2. Alvarez A., Munoz J. P. and Maccioni R. B. (2001) A Cdk5-p35 stable complex is involved in the beta-amyloid-induced deregulation of Cdk5 activity in hippocampal neurons. Exp. Cell Res. 264, 266-274.
3. 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.
4. 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, Näirn A. C. and Greengard P. (1999) Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 402, 669-671.
5. 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. and Greengard P. (2001a) Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380.
6. Bibb J. A., Nishi A., O'Callaghan J. P., Ule J., Lan M., Snyder G. L., Horiuchi A., Saito T., Hisanaga S., Czernik A. J., Nairn A. C. and Greengard P. (2001b) Phosphorylation of protein phosphatase inhibitor-1 by Cdk5. J. Biol. Chem. 276, 14490-14497.
7. 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.
8. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A. and Hof P. R. (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Brain Res. Rev. 33, 95-130.
9. 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.
10. Chishti M. A., Yang D. S., Janus C., Phinney A. L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P. E., Carlson G. A., St George-Hyslop P. H. and Westaway D. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 276, 21562-21570.
11. Delalle I., Bhide P. G., Caviness V. S. Jr and Tsai L. H. (1997) Temporal and spatial patterns of expression of p35, a regulatory subunit of cyclin-dependent kinase 5, in the nervous system of the mouse. J. Neurocytol. 26, 283-296.
12. Drewes G., Trinczek B., Illenberger S., Biemat J., Schmitt-Ulms G., Meyer H. E., Mandelkow E. M. and Mandelkow E. (1995) Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates taumicrotubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J. Biol. Chem. 270, 7679-7688.
13. Flaherty D. B., Soria J. P., Tomasiewicz H. G. and Wood J. G. (2000) Phosphorylation of human tau protein by microtubule-associated kinases: GSK3beta and cdk5 are key participants. J. Neurosci. Res. 62, 463-472.
14. Greenberg S. G. and Davies P. (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl Acad. Sci. USA 87, 5827-5831.
15. 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.
16. Honjyo Y., Kawamoto Y., Nakamura S., Nakano S. and Akiguchi I. (1999) Immunohistochemical localization of CDK5 activator p39 in the rat brain. Neuroreport 10, 3375-3379.
17. Huang D. Y., Goedert M., Jakes R., Weisgraber K. H., Garner C. C., Saunders A. M., Pericak-Vance M. A., Schmechel D. E., Roses A. D. and Strittmatter W. J. (1994) Isoform-specific interactions of apolipoprotein E with the microtubule-associated protein MAP2c: implications for Alzheimer's disease. Neurosci. Lett. 182, 55-58.
18. Huang D. Y., Weisgraber K. H., Goedert M., Saunders A. M., Roses A. D. and Strittmatter W. J. (1995) ApoE3 binding to tau tandem repeat I is abolished by tau serine262 phosphorylation. Neurosci. Lett. 192, 209-212.
19. Ishiguro K., Shiratsuchi A., Sato S., Omori A., Arioka M., Kobayashi S., Uchida T. and Imahori K. (1993) Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett. 325, 167-172.
20. Janus C., Pearson J., McLaurin J., Mathews P. M., Jiang Y., Schmidt S. D., Chishti M. A., Horne P., Heslin D., French J., Mount H. T., Nixon R. A., Mercken M., Bergeron C., Fraser P. E., St George-Hyslop P. H. and Westaway D. (2000) A beta-peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408, 979-982.
21. Kerokoski P., Suuronen T., Salminen A., Soininen H. and Pirttila T. (2002) Cleavage of the cyclin-dependent kinase 5 activator p35 to p25 does not induce tau hyperphosphorylation. Biochem. Biophys. Res. Commun 298, 693-698.
22. 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.
23. 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.
24. 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.
25. 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.
26. Li G., Faibushevich A., Turunen B. J., Yoon S. O., Georg G., Michaelis M. L. and Dobrowsky R. T. (2003) Stabilization of the cyclin-dependent kinase 5 activator, p35, by paclitaxel decreases beta-amyloid toxicity in cortical neurons. J. Neurochem. 84, 347-362.
27. Lu Q. and Wood J. G. (1993) Functional studies of Alzheimer's disease tau protein. J. Neurosci. 13, 508-515.
28. Lue L. F., Kuo Y. M., Roher A. E., Brachova L., Shen Y., Sue L., Beach T., Kurth J. H., Rydel R. E. and Rogers J. (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol 155, 853-862.
29. McLean C. A., Chemy R. A., Fraser F. W., Fuller S. J., Smith M. J., Beyreuther K., Bush A. I. and Masters C. L. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866.
30. Nguyen K. C., Rosales J. L., Barboza M. and Lee K. Y. (2002) Controversies over p25 in Alzheimer's disease. J. Alzheimer's Dis. 4, 123-126.
31. 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.
32. Ohshima T., Ogawa M., Veeranna Hirasawa M., Longenecker G., Ishiguro K., Pant H. C., Brady R. O., Kulkarni A. B. and Mikoshiba K. (2001) Synergistic contributions of cyclin-dependant kinase 5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc. Natl Acad. Sci. USA 98, 2764-2769.
33. 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.
34. Patrick G. N., Zukerberg L., de la Nikolic M. M. S., Dikkes P. and Tsai L. H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622.
35. Patrick G. N., Zukerberg L., de la Nikolic M. M. S., Dikkes P. and Tsai L. H. (2001) p25 protein in neurodegeneration: Reply. Nature 411, 764-765.
36. 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.
37. Saunders A. M., Strittmatter W. J., Schmechel D., St George-Hyslop P. H., Pericak-Vance M. A., Joo S. H., Rosi B. L., Gusella J. F., Crapper-MacLachlan D. R. and Alberts M. J. (1993) Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43, 1467-1472.
38. Strittmatter W. J., Saunders A. M., Goedert M., Weisgraber K. H., Dong L. M., Jakes R., Huang D. Y., Pericak-Vance M., Schmechel D. and Roses A. D. (1994) Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease. Proc. Natl Acad. Sci. USA 91, 11183-11186.
39. 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.
40. Tanaka T., Veeranna Ohshima T., Rajan P., Amin N. D., Cho A., Sreenath T., Pant H. C., Brady R. O. and Kulkami A. B. (2001) Neuronal cyclin-dependent kinase 5 activity is critical for survival. J. Neurosci. 21, 550-558.
41. 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.
42. Taniguchi S., Fujita Y., Hayashi S., Kakita A., Takahashi H., Murayama S., Saido T. C., Hisanaga S., Iwatsubo T. and Hasegawa M. (2001) Calpain-mediated degradation of p35 to p25 in postmortem human and rat brains. FEBS Lett. 489, 46-50.
43. 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.
44. 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.
45. 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.
46. Veeranna Shetty K. T., Takahashi M., Grant P. and Pant H. C. (2000) Cdk5 and MAPK are associated with complexes of cytoskeletal proteins in rat brain. Brain Res. Mol. Brain Res. 76, 229-236.
47. Wang J., Dickson D. W., Trojanowski J. Q. and Lee V. M. (1999) The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp. Neurol. 158, 328-337.
48. Yoo B. C. and Lubec G. (2001) p25 protein in neurodegeneration. Nature 411, 763-764.