Stabilization of the cyclin-dependent kinase 5 activator, p35, by paclitaxel decreases β-amyloid toxicity in cortical neurons

Journal of Neurochemistry

Volumn 84, Issue 2, 2003, Pages 347-362

  Li, Guibin ^a   Faibushevich, Alexander ^a   Turunen, Brandon J ^a   Yoon, Sung Ok ^b   Georg, Gunda ^a   Michaelis, Mary L ^a   Dobrowsky, Rick T ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Amyloid ; Calpain; Cyclin dependent kinase 5; Microtubules; Paclitaxel; Tau

Indexed keywords

AMYLOID BETA PROTEIN; CALPAIN; CYCLIN DEPENDENT KINASE 5; PACLITAXEL; PROTEIN P35; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CELL; CELL DEATH; CHROMOSOME 17; COMPLEX FORMATION; ENZYME ACTIVATION; GENE MUTATION; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NONHUMAN; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AMYLOID BETA-PROTEIN; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BLOOD-BRAIN BARRIER; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; ENZYME ACTIVATION; MACROMOLECULAR SUBSTANCES; MICE; MICE, TRANSGENIC; MICROTUBULES; NERVE TISSUE PROTEINS; NEURONS; PACLITAXEL; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; TAU PROTEINS;

ANIMALIA;

EID: 0037269505     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01526.x     Document Type: Article

References (61)

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., 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.
3. 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.
4. Amato S. F., Swart J. M., Berg M., Wanebo H. J., Mehta S. R. and Chiles T. C. (1998) Transient stimulation of the c-Jun - NH2-terminal kinase/activator protein 1 pathway and inhibition of extracellular signal-regulated kinase are early effects in paclitaxel-mediated apoptosis in human B lymphoblasts. Cancer Res. 58, 241-247.
5. van Asperen J., van Tellingen O., Sparreboom A., Schinkel A. H., Borst P., Nooijen W. J. and Beijnen J. H. (1997) Enhanced oral bio-availability of paclitaxel in mice treated with the P-glycoprotein blocker SDZ PSC 833. Br. J. Cancer 76, 1181-1183.
6. Billingsley M. L. and Kincaid R. L. (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem. J. 323, 577-591.
7. Blagosklonny M. V. and Fojo T. (1999) Molecular effects of paclitaxel: myths and reality (a critical review). Int. J. Cancer 83, 151-156.
8. Blagosklonny M. V., Schulte T., Nguyen P., Trepel J. and Neckers L. M. (1996) Taxol-induced apoptosis and phosphorylation of Bcl-2 protein involves c-Raf-1 and represents a novel c-Raf-1 signal transduction pathway. Cancer Res. 56, 1851-1854.
9. Blagosklonny M. V., Giannakakou P., el Deiry W. S., Kingston D. G., Higgs P. I., Neckers L. and Fojo T. (1997) Raf-1/bcl-2 phosphorylation: a step from microtubule damage to cell death. Cancer Res. 57, 130-135.
10. Brouty-Boye D., Kolonias D., Wu C. J., Savaraj N. and Lampidis T. J. (1995) Relationship of multidrug resistance to rhodamine-123 selectivity between carcinoma and normal epithelial cells: taxol and vinblastine modulate drug efflux. Cancer Res. 55, 1633-1638.
11. Busciglio J., Lorenzo A., Yeh J. and Yanker B. A. (1995) β-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14, 879-888.
12. Cavaletti G., Cavalletti E., Oggioni N., Sottani C., Minoia C., D'Incalci M., Zucchetti M., Marmiroli P. and Tredici G. (2000) Distribution of paclitaxel within the nervous system of the rat after repeated intravenous administration. Neurotoxicology 21, 389-393.
13. Dhavan R., Tsai L. H. and Tsai L. H. (2001) A decade of cdk5. Nat. Rev. Mol. Cell Biol. 2, 749-759.
14. Ding A. H., Porteu F., Sanchez E. and Nathan C. F. (1990) Shared actions of endotoxin and taxol on TNF receptors and release. Science 248, 370-372.
15. Evans D. B., Rank K. B., Bhattacharya K., Thomsen D. R., Gurney M. E. and Sharma S. K. (2000) 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. 275, 24977-24983.
16. Figueroa-Masot X. A., Hetman M., Higgins M. J., Kokot N. and Xia Z. (2001) Taxol induces apoptosis in cortical neurons by a mechanism independent of Bcl-2 phosphorylation. J. Neurosci. 21, 4657-4667.
17. Goedert M. (1997) The neurofibrillary pathology of Alzheimer's disease. Neuroscientist 3, 131-141.
18. Goedert M., Crowther R. A. and Spillantini M. G. (1998) Tau mutations cause frontotemporal dementias. Neuron 21, 955-958.
19. He T. C., Zhou S., da Costa L. T., Yu J., Kinzler K. W. and Vogelstein B. (1998) A simplified system for generating recombinant adenoviruses. Proc. Natl Acad. Sci. USA 95, 2509-2514.
20. Heimans J. J., Vermorken J. B., Wolbers J. G., Eeltink C. M., Meijer O. W., Taphoom M. J. and Beijnen J. H. (1994) Paclitaxel (taxol) concentrations in brain tumor tissue. Ann. Oncol. 5, 951-953.
21. Huang Y. and Wang K. K. (2001) The calpain family and human disease. Trends Mol. Med. 7, 355-362.
22. Ino H., Ishizuka T., Chiba T. and Tatibana M. (1994) Expression of CDK5 (PSSALRE kinase), a neural cdc2-related protein kinase, in the mature and developing mouse central and peripheral nervous systems. Brain Res. 661, 196-206.
23. Jordan M. A., Toso R. J., Thrower D. and Wilson L. (1993) Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. USA 90, 9552-9556.
24. 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.
25. Lee V. M., Daughenbaugh R. and Trojanowski J. Q. (1994) Microtubule stabilizing drugs for the treatment of Alzheimer's disease. Neurobiol. Aging 15, S87-S89.
26. Lee V. M., Goedert M. and Trojanowski J. Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159.
27. Lee K. Y., Clark A. W., Rosales J. L., Chapman K., Fung T. and Johnston R. N. (1999) Elevated neuronal Cdc2-like kinase activity in the Alzheimer disease brain. Neurosci. Res. 34, 21-29.
28. 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.
29. Liu Y., Ali S. M., Boge T. C., Georg G. I., Victory S., Zygmunt J., Marquez R. T. and Himes R. H. (2002) A systematic SAR study of C10 modified paclitaxel analogues using a combinatorial approach. Comb. Chem. High Throughput Screen 5, 39-48.
30. Maccioni R. B., Otth C., Concha I. I. and Munoz J. P. (2001) The protein kinase Cdk5. Structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. Eur. J. Biochem. 268, 1518-1527.
31. Manthey C. L., Qureshi N., Stutz P. L. and Vogel S. N. (1993) Lipopolysaccharide antagonists block taxol-induced signaling in murine macrophages. J. Exp. Med. 178, 695-702.
32. 2+ exchanger in neuronal and non-neuronal cells. Brain Res. 661, 104-116.
33. Michaelis M. L., Ranciat N., Chen T., Bechtel M. R. R., Hepperle M., Liu Y. and Georg G. (1998) Protection against β-amyloid toxicity in primary neurons by paclitaxel (taxol). J. Neurochem. 70, 1623-1627.
34. Michaelis M. L., Chen Y., Hill S., Reiff E., Georg G., Kice A. and Audus K. (2002) Amyloid peptide toxicity and microtubule-stabilizing drugs. J. Mol. Neurosci. 19, 101-105.
35. Nakagawa T. and Yuan J. (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150, 887-894.
36. 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.
37. 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.
38. 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 LIS1 and cytoplasmic dynein. Neuron 28, 697-711.
39. Nikolic M. and Tsai L. H. (2000) Activity and regulation of p35/Cdk5 kinase complex. Meth Enzymol. 325, 200-213.
40. 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.
41. Patrick G. N., Zukerberg L., de Nikolic M., La M. S., Dikkes P. and Tsai L. H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622.
42. Patrick G. N., Zukerberg L., de Nikolic M., La M. S., Dikkes P. and Tsai L. H. (2001) reply: p25 protein in neurodegeneration. Nature 411, 764-765.
43. Patzke H. and Tsai L. H. (2002a) Calpain-mediated cleavage of the cyclin-dependent kinase 5 activator p39 to p29. J. Biol. Chem. 277, 8054-8060.
44. Patzke H. and Tsai L. H. (2002b) Cdk5 sinks into ALS. Trends Neurosci. 25, 8-10.
45. Rapoport M., Dawson H. N., Lester I. B., Vitek M. P. and Ferreira A. (2002) Tau is essential to β-amyloid-induced neurotoxicity. Proc. Natl Acad. Sci. USA 99, 6364-6369.
46. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T. D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D. and Younkin S. (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat. Med. 2, 864-870.
47. Selkoe D. J. (2001a) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766.
48. Selkoe D. J. (2001b) Clearing the brain's amyloid cobwebs. Neuron 32, 177-180.
49. Siman R., Flood D. G., Thinakaran G. and Neumar R. W. (2001) Endoplasmic reticulum stress-induced cysteine protease activation in cortical neurons: effect of an Alzheimer's disease-linked presenilin-1 knock-in mutation. J. Biol. Chem. 276, 44736-44743.
50. Sobue K., Agarwal-Mawal A., Li W., Sun W., Miura Y. and Paudel H. K. (2000) Interaction of neuronal Cdc2-like protein kinase with microtubule-associated protein tau. J. Biol. Chem. 275, 16673-16680.
51. Spillantini M. G., Murrell J. R., Goedert M., Farlow M. R., Klug A. and Ghetti B. (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl Acad. Sci. USA 95, 7737-7741.
52. 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.
53. Teraski T. and Tsuji A. (1995) Controlling transport and metabolism, in Peptide Based Drug Design (Taylor M. D. and Amidon G. L., eds), pp. 297-316. Amer. Chem. Soc., Washington, DC.
54. Thiel V. E. and Audus K. L. (2001) Nitric oxide and blood-brain barrier integrity. Antioxid. Redox Signal. 3, 273-278.
55. 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.
56. Wang K. K. (2000) Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 20-26.
57. Wang T. H., Wang H. S., Ichijo H., Giannakakou P., Foster J. S., Fojo T. and Wimalasena J. (1998) Microtubule-interfering agents activate c-Jun N-terminal kinase/stress-activated protein kinase through both Ras and apoptosis signal-regulating kinase pathways. J. Biol. Chem. 273, 4928-4936.
58. Xie H. and Johnson G. V. (1997) Ceramide selectively decreases tau levels in differentiated PC 12 cells through modulation of calpain I. J. Neurochem. 69, 1020-1030.
59. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T. and Tohyama M. (2001) Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 276, 13935-13940.
60. Yoo B. C. and Lubec G. (2001) p25 protein in neurodegeneration. Nature 411, 763-764.
61. 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 outgrowth. Neuron 26, 633-646.