GSK3β inhibition is involved in the neuroprotective effects of cyclin-dependent kinase inhibitors in neurons

Pharmacological Research

Volumn 65, Issue 1, 2012, Pages 66-73

  De La Torre, Aurelio Vazquez ^a   Junyent, Felix ^a,b   Folch, Jaume ^b   Pelegrí, Carme ^a   Vilaplana, Jordi ^a   Auladell, Carme ^a   Beas Zarate, Carlos ^c   Pallàs, Mercè ^a   Verdaguer, Ester ^a   Camins, Antoni ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c UNIVERSITY OF GUADALAJARA   (Mexico)

Author keywords

Apoptosis; Cerebellar granular cells; Flavopiridol; GSK3 ; Roscovitine

Indexed keywords

2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; BRAIN PROTEIN; FLAVOPIRIDOL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; PROTEIN GSK3BETA; PROTEIN KINASE B; ROSCOVITINE; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOASSAY; CELL ACTIVATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; GRANULE CELL; MEDIATOR RELEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CEREBELLUM; CYCLIN-DEPENDENT KINASES; CYTOPROTECTION; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVONOIDS; GLYCOGEN SYNTHASE KINASE 3; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PIPERIDINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-JUN; PURINES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84855983255     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2011.08.006     Document Type: Article

References (53)

1. L.M. Wang, and D.M. Ren Flavopiridol, the first cyclin-dependent kinase inhibitor: recent advances in combination chemotherapy Mini Rev Med Chem 10 2010 1058 1070
2. F. Rizzolio, T. Tuccinardi, I. Caligiuri, C. Lucchetti, and A. Giordano CDK inhibitors: from the bench to clinical trials Curr Drug Targets 11 2010 279 290
3. J. Wosierska-Gdek, and M. Maurer Promotion of apoptosis in cancer cells by selective purine-derived pharmacological CDK inhibitors: one outcome, many mechanisms Curr Pharm Des 17 2011 256 271
4. J. Wojciechowski, M. Horky, M. Gueorguieva, and J. Wesierska-Gadek Rapid onset of nucleolar disintegration preceding cell cycle arrest in roscovitine-induced apoptosis of human MCF-7 breast cancer cells Int J Cancer 106 2003 486 495 (Pubitemid 36969788)
5. J. Wsierska-Gdek, A. Borza, O. Komina, and M. Maurer Impact of roscovitine, a selective CDK inhibitor, on cancer cells: bi-functionality increases its therapeutic potential Acta Biochim Pol 56 3 2009 495 501
6. E. Verdaguer, E.G. Jordá, A.M. Canudas, A. Jiménez, D. Pubill, E. Escubedo, J. Camarasa, M. Pallàs, and A. Camins Antiapoptotic effects of roscovitine in cerebellar granule cells deprived of serum and potassium: a cell cycle-related mechanism Neurochem Int 44 2004 251 261 (Pubitemid 37340135)
7. A. Giovanni, F. Wirtz-Brugger, E. Keramaris, R. Slack, and D.S. Park Involvement of cell cycle elements, cyclin-dependent kinases, pRb, and E2F x DP, in B-amyloid-induced neuronal death J Biol Chem 274 1999 19011 19016
8. J. Padmanabhan, D.S. Park, L.A. Greene, and Shelanski ML Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis J Neurosci 19 1999 8747 8756 (Pubitemid 30226696)
9. M. Mirjany, L. Ho, and G.M. Pasinetti Role of cyclooxygenase-2 in neuronal cell cycle activity and glutamate-mediated excitotoxicity J Pharmacol Exp Ther 301 2002 494 500 (Pubitemid 34429959)
10. E. Verdaguer, A. Jiménez, A.M. Canudas, E.G. Jordà, F.X. Sureda, M. Pallàs, and A. Camins Inhibition of cell cycle pathway by flavopiridol promotes survival of cerebellar granule cells after an excitotoxic treatment J Pharmacol Exp Ther 308 2004 609 616 (Pubitemid 38134223)
11. Z. Zhang, X. Cao, N. Xiong, H. Wang, J. Huang, S. Sun, and Z. Liang and DNA polymerase-beta is required for 1-methyl-4-phenylpyridinium-induced apoptotic death in neurons Apoptosis 15 2010 105 115
12. G.D. Hilton, B.A. Stoica, K.R. Byrnes, and A.I. Faden Roscovitine reduces neuronal loss, glial activation, and neurologic deficits after brain trauma J Cereb Blood Flow Metab 28 2008 1845 1859
13. F. Wang, D. Corbett, H. Osuga, S. Osuga, J.E. Ikeda, R.S. Slack, M.J. Hogan, A.M. Hakim, and D.S. Park Inhibition of cyclin-dependent kinases improves CA1 neuronal survival and behavioral performance after global ischemia in the rat J Cereb Blood Flow Metab 22 2002 171 182 (Pubitemid 34135648)
14. R.A. Smith, T. Walker, X. Xie, and S.T. Hou Involvement of the transcription factor E2F1/Rb in kainic acid-induced death of murine cerebellar granule cells Brain Res Mol Brain Res 116 2003 70 79 (Pubitemid 36993698)
15. S. Leclerc, M. Garnier, R. Hoessel, D. Marko, J.A. Bibb, G.L. Snyder, P. Greengard, J. Biernat, Y.Z. Wu, E.M. Mandelkow, G. Eisenbrand, and L.J. Meijer Indirubins inhibit glycogen synthase kinase-3β and CDK5/P25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease: a property common to most cyclin-dependent kinase inhibitors? Biol Chem 276 2001 251 260 (Pubitemid 32050314)
16. G.O. Iyirhiaro, T.B. Brust, J. Rashidian, Z. Galehdar, A. Osman, M. Phillips, R.S. Slack, B.A. Macvicar, and D.S. Park Delayed combinatorial treatment with flavopiridol and minocycline provides longer term protection for neuronal soma but not dendrites following global ischemia J Neurochem 105 2008 703 713 (Pubitemid 351562716)
17. A. Camins, E. Verdaguer, J. Folch, A.M. Canudas, and M. Pallàs The role of CDK5/P25 formation/inhibition in neurodegeneration Drug News Perspect 19 2006 453 460 (Pubitemid 46050819)
18. S.H. Kim, and T.A. Ryan CDK5 serves as a major control point in neurotransmitter release Neuron 67 2010 797 809
19. B. Menn, S. Bach, T.L. Blevins, M. Campbell, L. Meijer, and S. Timsit Delayed treatment with systemic (S)-roscovitine provides neuroprotection and inhibits in vivo CDK5 activity increase in animal stroke models PLoS One 5 2010 e12117
20. J. Rashidian, M.W. Rousseaux, K. Venderova, D. Qu, S.M. Callaghan, M. Phillips, R.J. Bland, M.J. During, Z. Mao, R.S. Slack, and D.S. Park Essential role of cytoplasmic cdk5 and Prx2 in multiple ischemic injury models, in vivo J Neurosci 29 2009 12497 12505
21. M. Hamdane, A. Bretteville, A.V. Sambo, K. Schindowski, S. Bégard, A. Delacourte, P. Bertrand, and L. Buée p25/Cdk5-mediated retinoblastoma phosphorylation is an early event in neuronal cell death J Cell Sci 118 2005 1291 1298 (Pubitemid 40528698)
22. B. Tian, Q. Yang, and Z. Mao Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death Nat Cell Biol 11 2009 211 218
23. K. Chergui, P. Svenningsson, and P. Greengard Cyclin-dependent kinase 5 regulates dopaminergic and glutamatergic transmission in the striatum Proc Natl Acad Sci USA 101 2004 2191 2196 (Pubitemid 38229037)
24. K. Tomizawa, J. Ohta, M. Matsushita, A. Moriwaki, S.T. Li, K. Takei, and H. Matsui Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity J Neurosci 22 2002 2590 2597 (Pubitemid 37465808)
25. B.S. Li, M.K. Sun, L. Zhang, S. Takahashi, W. Ma, L. Vinade, A.B. Kulkarni, R.O. Brady, and H.C. Pant Regulation of NMDA receptors by cyclin-dependent kinase-5 Proc Natl Acad Sci USA 98 2001 12742 12747 (Pubitemid 33020016)
26. Z. Buraei, G. Schofield, and K.S. Elmslie Roscovitine differentially affects CaV2 and Kv channels by binding to the open state Neuropharmacology 52 2007 883 894 (Pubitemid 46237642)
27. Z. Yan, P. Chi, J.A. Bibb, T.A. Ryan, and P. Greengard Roscovitine: a novel regulator of P/Q-type calcium channels and transmitter release in central neurons J Physiol 540 2002 761 770 (Pubitemid 35190150)
28. A. Ivanov, R. Tyzio, Y. Zilberter, and Y. Ben-Ari (R)-roscovitine, a cyclin-dependent kinase inhibitor, enhances tonic GABA inhibition in rat hippocampus Neuroscience 156 2008 277 288
29. J. Bain, L. Plater, M. Elliott, N. Shpiro, C.J. Hastie, H. McLauchlan, I. Klevernic, J.S. Arthur, D.R. Alessi, and P. Cohen The selectivity of protein kinase inhibitors: a further update Biochem J 408 2007 297 315
30. A.V. De la Torre, F. Junyent, J. Folch, C. Pelegrí, J. Vilaplana, C. Auladell, C. Beas-Zarate, M. Pallàs, A. Camins, and E. Verdaguer Study of the pathways involved in apoptosis induced by PI3K inhibition in cerebellar granule neurons Neurochem Int 59 2011 159 167
31. D.A. Cross, A.A. Culbert, K.A. Chalmers, L. Facci, S.D. Skaper, and A.D. Reith Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death J Neurochem 77 2001 94 102 (Pubitemid 32245083)
32. T.M. Miller, M.G. Tansey, E.M. Johnson Jr., and D.J. Creedon Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization- and insulin-like growth factor I-mediated survival of cerebellar granule cells J Biol Chem 272 1997 9847 9853 (Pubitemid 27171651)
33. P.C. Chin, N. Majdzadeh, and S.R. D'Mello Inhibition of GSK3beta is a common event in neuroprotection by different survival factors Brain Res Mol Brain Res 137 2005 193 201 (Pubitemid 40798902)
34. L. Facci, D.A. Stevens, and S.D. Skaper Glycogen synthase kinase-3 inhibitors protect central neurons against excitotoxicity Neuroreport 14 2003 1467 1470 (Pubitemid 37083129)
35. M. Medina, and J. Avila Glycogen synthase kinase-3 (GSK-3) inhibitors for the treatment of Alzheimer's disease Curr Pharm Des 16 2010 2790 2798
36. J. Avila, F. Wandosell, and F. Hernández Role of glycogen synthase kinase-3 in Alzheimer's disease pathogenesis and glycogen synthase kinase-3 inhibitors Expert Rev Neurother 10 2010 703 710
37. D. Krämer, and L. Minichiello Cell culture of primary cerebellar granule cells Methods Mol Biol 633 2010 233 239
38. L.E. Rameh, C. Chen, and L.C. Cantley Phosphatidylinositol (3,4,5) P3 interacts with SH2 Domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins Cell 83 1995 821 830
39. K. Shimoke, S. Yamagishi, M. Yamada, T. Ikeuchi, and H. Hatanaka Inhibition of phosphatidylinositol 3-kinase activity elevates c-Jun N-terminal kinase activity in apoptosis of cultured cerebellar granule neurons Brain Res Dev Brain Res 112 1999 245 253 (Pubitemid 29083269)
40. M. Tajes, M. Yeste-Velasco, X. Zhu, S.P. Chou, M.A. Smith, M. Pallàs, A. Camins, and G. Casadesús Activation of Akt by lithium: pro-survival pathways in aging Mech Ageing Dev 130 2009 253 261
41. H. Eldar-Finkelman, A. Licht-Murava, S. Pietrokovski, and M. Eisenstein Substrate competitive GSK-3 inhibitors - strategy and implications Biochim Biophys Acta 1804 2010 598 603
42. J.A. Quiroz, R. Machado-Vieira, C.A. Zarate Jr., and H.K. Manji Novel insights into lithium's mechanism of action: neurotrophic and neuroprotective effects Neuropsychobiology 62 2010 50 60
43. J.P. Lopes, C.R. Oliveira, and P. Agostinho Cdk5 acts as a mediator of neuronal cell cycle re-entry triggered by amyloid-beta and prion peptides Cell Cycle 8 2009 97 104
44. K. Ago, Y. Saegusa, J. Nishimura, Y. Dewa, S. Kemmochi, M. Kawai, T. Harada, K. Mitsumori, and M. Shibutani Involvement of glycogen synthase kinase-3beta signaling and aberrant nucleocytoplasmic localization of retinoblastoma protein in tumor promotion in a rat two-stage thyroid carcinogenesis model Exp Toxicol Pathol 62 2010 269 280
45. P.D. Smith, S.J. Crocker, V. Jackson-Lewis, K.L. Jordan-Sciutto, S. Hayley, M.P. Mount, M.J. O'Hare, S. Callaghan, R.S. Slack, S. Przedborski, H. Anisman, and D.S. Park Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease Proc Natl Acad Sci USA 100 2003 13650 13655 (Pubitemid 37444794)
46. D. Alvira, M. Tajes, E. Verdaguer, S.G. de Arriba, C. Allgaier, C. Matute, R. Trullas, A. Jiménez, M. Pallàs, and A. Camins Inhibition of cyclin-dependent kinases is neuroprotective in 1-methyl-4-phenylpyridinium-induced apoptosis in neurons Neuroscience 146 2007 350 365 (Pubitemid 46654625)
47. E. Verdaguer, A. Susana Gde, A. Clemens, M. Pallàs, and A. Camins Implication of the transcription factor E2F-1 in the modulation of neuronal apoptosis Biomed Pharmacother 61 2007 390 399 (Pubitemid 47239339)
48. C.G. Besirli, and E.M. Johnson Jr. JNK-independent activation of c-Jun during neuronal apoptosis induced by multiple DNA-damaging agents J Biol Chem 278 2003 22357 22366 (Pubitemid 36830285)
49. M.H. Ghahremani, E. Keramaris, T. Shree, Z. Xia, R.J. Davis, R. Flavell, R.S. Slack, and D.S. Park Interaction of the c-Jun/JNK pathway and cyclin-dependent kinases in death of embryonic cortical neurons evoked by DNA damage J Biol Chem 277 2002 35586 35596
50. V. Hongisto, N. Smeds, S. Brecht, T. Herdegen, M.J. Courtney, and E.T. Coffey Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3 Mol Cell Biol 23 2003 6027 6036 (Pubitemid 37013083)
51. J.M. Beaulieu, R.R. Gainetdinov, and M.G. Caron Akt/GSK3 signaling in the action of psychotropic drugs Annu Rev Pharmacol Toxicol 49 2009 327 347
52. X. Li, W. Zhu, M.S. Roh, A.B. Friedman, K. Rosborough, and R.S. Jope In vivo regulation of glycogen synthase kinase-3beta (GSK3beta) by serotonergic activity in mouse brain Neuropsychopharmacology 29 2004 1426 1431 (Pubitemid 38982234)
53. I. Cernak, B. Stoica, K.R. Byrnes, S. Di Giovanni, and A.I. Faden Role of the cell cycle in the pathobiology of central nervous system trauma Cell Cycle 4 2005 1286 1293 (Pubitemid 41365402)