Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction

Molecular and Cellular Neuroscience

Volumn 24, Issue 2, 2003, Pages 489-502

  Weishaupt, Jochen H ^a   Kussmaul, Lothar ^b   Grötsch, Philipp ^a   Heckel, Armin ^b   Rohde, G ^a   Romig, H ^b   Bähr, Mathias ^a   Gillardon, Frank ^b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; INDOLINONE A; INDOLINONE B; INDOLINONE C; INDOLINONE D; PROTEIN P25; PROTEIN P35; STAUROSPORINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL CYCLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG ACTIVITY; DRUG EFFECT; DRUG SCREENING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; MALE; MITOSIS; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PREVENTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; REGULATORY MECHANISM;

EID: 0142250831     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-7431(03)00221-5     Document Type: Article

References (47)

1. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death a succession of necrosis or apoptosis depending on mitochondrial function . Neuron. 15:1995;961-973.
2. Bamberger A.M., Jenatschke S., Erdmann I., Schulte H.M. Progestin-dependent stimulation of the human leukemia inhibitory factor promoter in SKUT-1B uterine tumor cells. J. Reprod. Immunol. 33:1997;189-201.
3. Barres B.A., Silverstein B.E., Corey D.P., Chun L.L. Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron. 1:1988;791-803.
4. 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.
5. Copani A., Condorelli F., Caruso A., Vancheri C., Sala A., Giuffrida Stella A.M., Canonico P.L., Nicoletti F., Sortino M.A. Mitotic signaling by beta-amyloid causes neuronal death. FASEB J. 13:1999;2225-2234.
6. Courtney M.J., Coffey E.T. The mechanism of Ara-C-induced apoptosis of differentiating cerebellar granule neurons. Eur. J. Neurosci. 11:1999;1073-1084.
7. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:2000;95-105.
8. Evans D.B., Rank K.B., Sharma S.K. A scintillation proximity assay for studying inhibitors of human tau protein kinase II/cdk5 using a 96-well format. J. Biochem. Biophys. Methods. 50:2002;151-161.
9. 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.
10. Freeman R.S., Estus S., Johnson E.M. Jr. Analysis of cell cycle-related gene expression in postmitotic neurons selective induction of cyclin D1 during programmed cell death . Neuron. 12:1994;343-355.
11. Gong X., Tang X., Wiedmann M., Wang X., Peng J., Zheng D., Blair L.A., Marshall J., Mao Z. CDK5-mediated inhibition of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron. 38:2003;33-46.
12. Heintz N. Cell death and the cell cycle a relationship between transformation and neurodegeneration? Trends Biochem. Sci. 18:1993;157-159.
13. Hirooka K., Tomizawa K., Matsui H., Tokuda M., Itano T., Hasegawa E., Wang J.H., Hatase O. Developmental alteration of the expression and kinase activity of cyclin-dependent kinase 5 (Cdk5)/p35nck5a in the rat retina. J. Neurochem. 67:1996;2478-2483.
14. Kermer P., Klöcker N., Bähr M. Neuronal death after brain injury models, mechanisms, and therapeutic strategies in vivo . Cell Tissue Res. 298:1999;383-395.
15. Kermer P., Klöcker N., Weishaupt J.H., Bähr M. Transection of the optic nerve in rats Studying neuronal death and survival in vivo . Brain Res. Brain Res. Protocis. 7:2001;255-260.
16. Klöcker N., Cellerino A., Bähr M. Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells in vivo. J. Neurosci. 18:1998;1038-1046.
17. Konishi Y., Lehtinen M., Donovan N., Bonni A. Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol. Cell. 9:2002;1005-1016.
18. Leclerc S., Garnier M., Hoessel R., Marko D., Bibb J.A., Snyder G.L., Greengard P., Biernat J., Wu Y.Z., Mandelkow E.M., Eisenbrand G., Meijer L. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease a property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276:2001;251-260.
19. 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.
20. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science. 298:2002;1912-1934.
21. Meyerson M., Enders G.H., Wu C.L., Su L.K., Gorka C., Nelson C., Harlow E., Tsai L.H. A family of human cdc2-related protein kinases. EMBO J. 11:1992;2909-2917.
22. Muller H.W., Beckh S., Seifert W. Neurotrophic factor for central neurons. Proc. Natl. Acad. Sci. USA. 81:1984;1248-1252.
23. Nakamura S., Kawamoto Y., Nakano S., Ikemoto A., Akiguchi I., Kimura J. Cyclin-dependent kinase 5 in Lewy body-like inclusions in anterior horn cells of a patient with sporadic amyotrophic lateral sclerosis. Neurology. 48:1997;267-270.
24. 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.
25. Nicotera P., Leist M., Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol. Lett. 103:1998;139-142.
26. Nikolic M., Chou M.M., Lu W., Mayer B.J., Tsai L.H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature. 395:1998;194-198.
27. 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.
28. O'Hare M., Wang F., Park D.S. Cyclin-dependent kinases as potential targets to improve stroke outcome. Pharmacol. Ther. 93:2002;135-143.
29. Osuga H., Osuga S., Wang F., Fetni R., Hogan M.J., Slack R.S., Hakim A.M., Ikeda J.E., Park D.S. Cyclin-dependent kinases as a therapeutic target for stroke. Proc. Natl. Acad. Sci. USA. 97:2000;10254-10259.
30. Padmanabhan J., Park D.S., Greene L.A., Shelanski M.L. Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J. Neurosci. 19:1999;8747-8756.
31. Paglini G., Pigino G., Kunda P., Morfini G., Maccioni R., Quiroga S., Ferreira A., Caceres A. Evidence for the participation of the neuron-specific CDK5 activator p35 during laminin-enhanced axonal growth. J. Neurosci. 18:1998;9858-9869.
32. Park D.S., Farinelli S.E., Greene L.A. Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J. Biol. Chem. 271:1996;8161-8169.
33. Park D.S., Levine B., Ferrari G., Greene L.A. Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J. Neurosci. 17:1997;8975-8983.
34. Park D.S., Morris E.J., Greene L.A., Geller H.M. G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J. Neurosci. 17:1997;1256-1270.
35. Park D.S., Morris E.J., Stefanis L., Troy C.M., Shelanski M.L., Geller H.M., Greene L.A. Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation, and oxidative stress. J. Neurosci. 18:1998;830-840.
36. 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.
37. Raha S., Myint A.T., Johnstone L., Robinson B.H. Control of oxygen free radical formation from mitochondrial complex I roles for protein kinase A and pyruvate dehydrogenase kinase . Free Radical Biol. Med. 32:2002;421-430.
38. Reed J.C. Mechanisms of apoptosis. Am. J. Pathol. 157:2000;1415-1430.
39. Rubin L.L., Gatchalian C.L., Rimon G., Brooks S.F. The molecular mechanisms of neuronal apoptosis. Curr. Opin. Neurobiol. 4:1994;696-702.
40. Sims N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J. Neurochem. 55:1990;698-707.
41. Tang D., Yeung J., Lee K.Y., Matsushita M., Matsui H., Tomizawa K., Hatase O., Wang J.H. An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. J. Biol. Chem. 270:1995;26897-26903.
42. Tsai L.H., Takahashi T., Caviness V.S. Jr., Harlow E. Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development. 119:1993;1029-1040.
43. van den Heuvel S., Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science. 262:1993;2050-2054.
44. 2/M phase arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis. J. Biol. Chem.
45. Walker D. Small-molecule inhibitors of cyclin-dependent kinases molecular tools and potential therapeutics . Curr. Top. Microbiol. Immunol. 227:1998;149-162.
46. Wüllner U., Seyfried J., Groscurth P., Beinroth S., Winter S., Gleichmann M., Heneka M., Loschmann P., Schulz J.B., Weller M., Klockgether T. Glutathione depletion and neuronal cell death the role of reactive oxygen intermediates and mitochondrial function . Brain Res. 826:1999;53-62.
47. 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., Tsai L.H. Cables links Cdk5 and c-Abl and facilitate Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron. 26:2000;633-646.