Inhibition of multiple pathways accounts for the antiapoptotic effects of flavopiridol on potassium withdrawal-induced apoptosis in neurons

Journal of Molecular Neuroscience

Volumn 26, Issue 1, 2005, Pages 71-84

  Verdaguer, Ester ^a   Jordà, Elvira G ^a   Alvira, Daniel ^a   Jiménez, Andrés ^a   Canudas, Anna Maria ^a   Folch, Jaume ^b   Rimbau, Victor ^a   Pallàs, Mercè ^a   Camins, Antoni ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b FACULTAT DE MEDICINA I CIÈNCIES DE LA SALUT   (Spain)

Author keywords

Apoptosis; CDK; Cell cycle; Flavopiridol; GSK 3 ; MEF2

Indexed keywords

CYCLIN DEPENDENT KINASE 5; FLAVOPIRIDOL; GLYCOGEN SYNTHASE KINASE 3BETA; POTASSIUM; PROTEIN P25;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; NERVE CELL; NEUROPROTECTION; NONHUMAN; RAT;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL CYCLE; CEREBELLUM; CYCLIN-DEPENDENT KINASES; FLAVONOIDS; FLOW CYTOMETRY; MODELS, NEUROLOGICAL; NEURONS; PIPERIDINES; POTASSIUM; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 22344449621     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1385/JMN:26:03:71     Document Type: Article

References (75)

1. Alavez S., Pedroza D., and Morán J. (2003) Mechanisms of cell death by deprivation of depolarizing conditions during cerebellar granule neuron maturation. Neurochem. Int. 43, 581-590.
2. Allsopp T. E., McLuckie J., Kerr L. E., Macleod M., Sharkey J., and Kelly J. S. (2000) Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis. Cell Death Differ. 7, 984-993.
3. Alvarez A., Toro R., Cáceres A., and Maccioni R. B. (1999). Inhibition of tau phosphorylating protein kinase CDK5 prevents β-amyloid-induced neuronal death. FEBS Lett. 459, 421-426.
4. Armstrong R.C., Aja T. J., Hoang K. D., Gaur S., Bai X., Alnemri E. S., et al. (1997) Activation of the CD3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J. Neurosci. 17, 553-562.
5. Atabay C., Cagnoli C. M., Kharlamov E., Ikonomovic M. D., and Manev H. (1996) Removal of serum from primary cultures of cerebellar granule neurons induces oxidative stress and DNA fragmentation: protection with antioxidants and glutamate receptor antagonists. J. Neurosci. Res. 43, 465-475.
6. Beserli C. G. and Johnson M. J. (2003) JNK-independent activation of c-Jun during neuronal apoptosis induced by multiple DNA-damaging agents. J. Biol. Chem. 278, 22357-22366.
7. Boutillier A. L., Kienlen-Campard P., and Loeffler J. P. (1999) Depolarization regulates cyclin D1 degradation and neuronal apoptosis: a hypothesis about the role of the ubiquitin/proteasome signalling pathway. Eur. J. Neurosci. 11, 441-448.
8. Boutillier A. L., Trinh E., and Loeffler J. P. (2000) Caspase-dependent cleavage of the retinoblastoma protein is an early step in neuronal apoptosis. Oncogene 19, 2171-2178.
9. Contestabile A. (2002) Cerebellar granule cells as a model to study mechanisms of neuronal apoptosis or survival in vivo and in vitro. Cerebellum 1, 41-55.
10. Copani A., Condorelli F., Caruso A., Vancheri C., Sala, A., Giuffrida Stella A. M., et al. (1999) Mitotic signalling by (-amyloid causes neuronal death. FASEB J. 13, 225-234.
11. Cross D. A., Culbert A. A., Chalmers K. A., Facci L., Skaper S. D., and Reith A. D. (2001) Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurons from death. J. Neurochem. 77, 94-102.
12. D'Mello S. R., Kuan C. Y., Flavell R. A., and Rakic P. (2000) Caspase-3 is required for apoptosis-associated DNA fragmentation but not for cell death in neurons deprived of potassium. J. Neurosci. Res. 59, 24-31.
13. Dodel R. C., Du Y., Bales, K. R., Ling Z., Carvey P. M., and Paul S. M. (1999) Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death. Mol. Brain Res. 64, 141-148.
14. Facci L., Stevens D. A., and Skaper S. D. (2003) Glycogen synthase kinase-3 inhibitors protect central neurons against excitotoxicity. Neuroreport 14, 1467-1470.
15. Gerhardt E., Kügler S., Leist M., Beier C., Berliocchi L., Volbracht C., et al. (2001) Cascade of caspase activation in potassium-deprived cerebellar granule neurons: targets for treatment with peptide and protein inhibitors of apoptosis. Mol. Cell. Neurosci. 17, 717-731.
16. Giardina S. F. and Beart P. M. (2002) Kainate receptor-mediated apoptosis in primary cultures of cerebellar granule cells is attenuated by mitogen-activated protein and cyclin-dependent kinase inhibitors. Br. J. Pharmacol. 135, 1733-1745.
17. Ginham R., Harrison D. C., Facci L., Skaper S., and Philpott K. L. (2001) Upregulation of death pathway molecules in rat cerebellar granule neurons undergoing apoptosis. Neurosci. Lett. 302, 113-116.
18. Gong X., Tang X., Wiedmann M., Wang X., Peng J., Zheng D., et al. (2003) Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38, 33-46.
19. Greene L. A., Biswas S. C., and Liu D. X. (2004) Cell cycle molecules and vertebrate neuron death: E2F at the hub. Cell Death Differ. 11, 49-60.
20. Hetman M., Cavanaugh J. E., Kimelman D., and Xia Z. (2000) Role of glycogen synthase kinase-3(in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20, 2567-2574.
21. Hongisto V., Smeds N., Brecht S., Herdegen T., Courtney M. J., and Coffey E. T. (2003) Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol. Cell. Biol. 23, 6027-6036.
22. Kinloch R. A., Treherne J. M., Furness L. M., and Hajimohamadreza I. (1999) The pharmacology of apoptosis. Trends Pharmacol. Sci. 20, 35-42.
23. Knockaert M., Greengard P., and Meijer L. (2002) Pharmacological inhibitors of cyclin-dependent kinases. Trends Pharmacol. Sci. 23, 417-425.
24. Klein J. A. and Ackerman S. L. (2003) Oxidative stress, cell cycle and neurodegeneration. J. Clin. Invest. 111, 785-793.
25. Konishi Y., Lehtinen M., Donovan N., and Bonni A. (2002) Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol. Cell 9, 1005-1016.
26. Kusukawa G. I., Saito T., Onuki R., Ishiguro K., Kishimoto T., and Hisinaga, S. I. (2000) Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator top 25. J. Biol. Chem. 275, 17166-17172.
27. Leclerc S., Garnier M., Hoessel R., Marko D., Bibb J. A., Snyder G. L., et al. (2001) 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, 251-260.
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. Lim A. C. B. and Qi R. Z. (2003) Cyclin-dependent kinases in neuronal development and degeneration. J. Alzheimer Dis. 5, 329-335.
30. Liu T., Perry G., Chan H. W., Verdile G., Martins R. N., Smith M. A., and Atwood C. S. (2004) Amyloid-β-induced toxicity of primary neurons is dependent upon differentiation-associated increases in tau and cyclin-dependent kinase 5 expression. J. Neurochem. 88, 554-563.
31. Lukovic D., Komoriya A., Packard B. Z., and Ucker D. S. (2003) Caspase activity is not sufficient to execute cell death. Exp. Cell Res. 289, 384-395.
32. Mao Z., Bonni A., Xia F., Nadal-Vicens M., and Greenberg M. E. (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286, 785-790.
33. Marks N., Berg M. J., Guidotti A., and Saito M. (1998) Activation of caspase-3 and apoptosis in cerebellar granule cells. J. Neurosci. 52, 334-341.
34. McShea A., Wahl A. F., and Smith M. A. (1999) Re-entry into the cell cycle: a mechanism for neurodegeneration in Alzheimer disease. Med. Hypotheses 52, 525-527.
35. Monaco E. A. and Vallano M. L. (2003) Cyclin-dependent kinase inhibitor: cancer killers to neuronal guardians. Curr. Med. Chem. 10, 367-379.
36. Nagy Z., Esiri M. M., and Smith A. D. (1997) Expression of cell division markers in the hippocampus in Alzheimer's disease and other neurodegenerative conditions. Acta Neuropathol. 93, 294-300.
37. Nahle Z., Polakoff J., Davuluri R. V., McCurrach M. E., Jacobson M. D., Narita M., et al. (2002) Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell. Biol. 4, 859-864.
38. Nath R., Mcginnis K., Dutta S., Shivers B., and Wang K. K. W. (2001) Inhibition of p38 kinase mimics survival signal-linked protection againts apoptosis in rat cerebellar granule neurons. Cell. Mol. Biol. Lett. 6, 173-184.
39. Nath R., Raser K. J., Stafford D., Hajimohammadreza I., Posner A., Allen H., et al. (1996) Nonerythroid α-spectrin breakdown by calpain and interleukin 1β-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem. J. 319, 683-690.
40. Neville M., Berg M. J., Guidotti A., and Saito M. (1998) Activation of caspase-3 and apoptosis in cerebellar granule cells. J. Neurosci. Res. 52, 334-341.
41. Nguyen M. D., Boudreau M., Kriz J., Couillard-Després 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 I. J. Neurosci. 23, 2131-2140.
42. Nguyen M. D., Mushynski W. E., and Julien J. P. (2002) Cycling at the interface between neurodevelopment and neurodegeneration. Cell Death Differ. 9, 1294-1306.
43. O'Hare M., Hou S. T., Morris E. J., Cregan S. P., Xu Q., Slack R. S., and Park D. S. (2000) Induction and modulation of cerebellar granule neuron death by E2F-1. J. Biol. Chem. 275, 25358-25364.
44. O'Hare M., Wang F., and Park D. S. (2002) Cyclin-dependent kinases as potential targets to improve stroke outcome. Pharmacol. Ther. 93, 135-143.
45. Otth C., Mendoza-Naranjo A., Mujica A., Zambrano A., Concha I. I., and Maccioni R. B. (2003) Modulation of the JNK and p38 pathways by CDK5 protein kinase in a transgenic mouse model of Alzheimer's disease. Neuroreport 14, 2403-2409.
46. Padmanabhan J., Park D. S., Greene L. A., and Shelansky M. L. (1999) Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J. Neurosci. 19, 8747-8756.
47. Park D. S., Levine B., Ferrari, G., and Greene L. A. (1997) Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J. Neurosci. 17, 8975-8973.
48. Park D. S., Obeidat A., Giovanni A., Greene L. A. (2000) Cell cycle regulators in neuronal cell death evoked by excitotoxic stress: implications for neurodegeneration and its treatment. Neurobiol. Aging 21, 771-781.
49. 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.
50. Phiel C. J., Wilson C. A., Lee V. M., and Klein P. S. (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439.
51. Raina A. K., Hochman A., Zhu X., Rottkamp C. A., Nunomura A., Siedlak S. L., et al. (2001) Abortive apoptosis in Alzheimer's disease. Acta Neuropathol. 101, 305-310.
52. Raina A. K., Monteiro M. J., Mcshea A., and Smith M. A. (1999) The role of cell cycle-mediated events in Alzheimer's. Int. J. Exp. Pathol. 80, 71-76.
53. Ranganathan S. and Bowser R. (2003) Alterations in G1 to S phase cell-cycle regulators during amytrophic lateral sclerosis. Am. J. Pathol. 162, 823-835.
54. Ranganathan S., Scudire S., and Bowser R. (2001) Hyperphosphorylation of the retinoblastoma gene product and altered subcellular distribution of E2F-1 during Alzheimer's disease and amyotrophic lateral sclerosis. J. Alzheimer Dis. 3, 377-385.
55. Robertson J. D. and Orrenius S. (2002) Role of mitochondria in toxic cell death. Toxicology 181-182, 491-496.
56. Sausville E. A. (2002) Complexities in the development of cyclin-dependent kinase inhibitor drugs. Trends Mol. Med. 8, S32-S37.
57. Schang L. M. (2002) Cyclin-dependent kinases as cellular targets for antiviral drugs. J. Antimicrob. Chemother. 50, 779-792.
58. Smith D. S. and Tsai L. H. (2002) Cdk5 behind the wheel: a role in trafficking and transport? Trends Cell Biol. 12, 28-36.
59. Smith D. S., Greer P. L., and Tsai L. H. (2001) Cdk5 on the brain. Cell Growth Differ. 12, 277-283.
60. Smith P. D., Crocker S. J., Lewis V. J., Jordan-Sciutto K. L., Hayley S., Mount M. P., et al. (2003) Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 100, 13650-13655.
61. Stefanis L., Park D. S., Friedman W. J., and Greene L. A. (1999) Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J. Neurosci. 19, 6235-6247.
62. Tanabe H., Eguchi Y., Shimizu S., Martinou J. C., and Tsujimoto Y. (1998) Death-signalling cascade in mouse cerebellar granule neurons. Eur. J. Neurosci. 10, 1403-1411.
63. Taylor J., Gatchalin C. L., Keen G., and Rubin L. L. (1997) Apoptosis in cerebellar granule neurons: Involvement of interleukin-1β converting enzyme-like proteases. J. Neurochem. 68, 1598-1605.
64. Verdaguer E., Jord E. G., Canudas A. M., Jiménez A., Pubill D., Escubedo E., Camarasa J., Pallas M., Camins A. (2004a) Antiapoptotic effects of roscovitine in cerebellar granule cells deprived of serum and potassium: a cell cycle-related mechanism. Neurochem. Int. 44, 251-261.
65. Verdaguer E., Jiménez A., Canudas A. M., Jorda E. G., Sureda F. X., Pallas M., Camins A. (2004b). Inhibition of cell cycle pathway by flavopiridol promotes survival of cerebellar granule cells after an excitotoxic treatment. J. Pharmacol. Exp. Ther. 308, 609-616.
66. Verdaguer E., Garcia-Jorda E., Canudas A. M., Dominguez E., Jiménez A., Pubill D., et al. (2002) Kainic acid-induced apoptosis in cerebellar granule neurons: an attempt at cell cycle re-entry. Neuroreport 18(4), 413-416.
67. Volbracht C., Leist M., Kolb S. A., and Nicotera P. (2001) Apoptosis in caspase-inhibited neurons. Mol. Med. 7, 36-48.
68. Watson A., Eilers A., Lallemand D., Kyriakis J., Rubin L. L., and Ham J. (1998) Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons. J. Neurosci. 18, 751-762.
69. Weishaupt J. H., Neusch C., and Bähr M. (2003) Cyclin-dependent kinase 5 and neuronal cell death. Cell Tissue Res. 312, 1-8.
70. Yang Y., Geldmacher D. S., and Herrup K. (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J. Neurosci. 21, 2661-2668.
71. Yang Y., Mufson E. J., and Herrup K. (2003) Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23, 2557-2563.
72. Zamzami N. and Kroemer G. (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2, 267-271.
73. Zhai S., Senderowicz A. M., Sausville E. A., and Figg W. D. (2002) Flavopiridol, a novel cyclin-dependent kinase inhibitor, in clinical development. Ann. Pharmacother. 36, 905-911.
74. Zheng Y. L., Li B. S., Amin N. D., Albers W., and Pant H. C. (2002) Apeptide derived from cyclin-dependent kinase activator (p35) specifically inhibits Cdk5 activity and phosphorylation of tau protein in transfected cells. Eur. J. Biochem. 269, 4427-4434.
75. Zhu X., Raina A. K., Boux H., Simmons Z. L., Takeda A., and Smith M. A. (2000) Activation of oncogenic pathways in degenerating neurons in Alzheimer disease. Int. J. Dev. Neurosci. 18, 433-437.