Study of the pathways involved in apoptosis induced by PI3K inhibition in cerebellar granule neurons

Neurochemistry International

Volumn 59, Issue 2, 2011, Pages 159-167

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

^a Nucli Universitari de Pedralbes   (Spain)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d UNIVERSITY OF GUADALAJARA   (Mexico)

Author keywords

BrdU; Caspase 6; CDK5 p25; Cell cycle; LY294002

Indexed keywords

2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; BETA ACTIN; BETA CATENIN; CALPAIN; CASPASE; CASPASE 3; CASPASE 6; CASPASE 9; CYCLIN D; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 5; CYCLIN E; FODRIN; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; PROTEIN KINASE B;

ANIMAL CELL; APOPTOSIS; ARTICLE; CEREBELLAR GRANULE NEURON; CONTROLLED STUDY; DNA FRAGMENTATION; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; MOUSE; NERVE CELL; NONHUMAN; POTASSIUM DEFICIENCY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CEREBELLUM; CYTOPLASMIC GRANULES; FLOW CYTOMETRY; MICE; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79960373301     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.03.027     Document Type: Article

References (55)

1. T.E. Allsopp, J. McLuckie, L.E. Kerr, M. Macleod, J. Sharkey, and J.S. Kelly Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis Cell Death Differ. 7 2000 984 993
2. S. Bauer, and P.H. Patterson The cell cycle-apoptosis connection revisited in the adult brain J. Cell Biol. 171 2005 641 650 (Pubitemid 41668723)
3. D.J. Bonda, H.P. Lee, W. Kudo, X. Zhu, M.A. Smith, and H.G. Lee Pathological implications of cell cycle re-entry in Alzheimer disease Expert Rev. Mol. Med. 12 2010 e19
4. C.A. Bondy, and C.M. Cheng Signaling by insulin-like growth factor 1 in brain Eur. J. Pharmacol. 490 2004 25 31 (Pubitemid 38482159)
5. T. Borsello, and G. Forloni JNK signalling: a possible target to prevent neurodegeneration Curr. Pharm. Des. 13 2007 1875 1886 (Pubitemid 47010160)
6. S.R. Bruckner, S.P. Tammariello, C.Y. Kuan, R.A. Flavell, P. Rakic, and S. Estus JNK3 contributes to c-Jun activation and apoptosis but not oxidative stress in nerve growth factor-deprived sympathetic neurons J. Neurochem. 78 2001 298 303 (Pubitemid 32664411)
7. A. Camins, E. Verdaguer, J. Folch, A.M. Canudas, and M. Palls The role of CDK5/P25 formation/inhibition in neurodegeneration Drug News Perspect. 19 2006 453 460 (Pubitemid 46050819)
8. A. Camins, N. Crespo-Biel, F. Junyent, E. Verdaguer, A.M. Canudas, and M. Palls Calpains as a target for therapy of neurodegenerative diseases: putative role of lithium Curr. Drug Metab. 10 2009 433 447
9. A. Camins, F.X. Sureda, F. Junyent, E. Verdaguer, J. Folch, C. Beas-Zarate, and M. Pallas An overview of investigational antiapoptotic drugs with potential application for the treatment of neurodegenerative disorders Expert Opin. Invest. Drugs. 19 2010 587 604
10. L. Cao, D.X. Cao, X.W. Su, L.J. Chen, A.L. Liu, W.J. Jian, Y.P. Wu, P.X. Qiu, and G.M. Yan Activation of PI3-K/Akt pathway for thermal preconditioning to protect cultured cerebellar granule neurons against low potassium-induced apoptosis Acta Pharmacol. Sin. 28 2007 173 179 (Pubitemid 46155533)
11. S.R. Datta, A. Brunet, and M.E. Greenberg Cellular survival: a play in three Akts Genes Dev. 13 1999 2905 2927
12. L. Galluzzi, K. Blomgren, and G. Kroemer Mitochondrial membrane permeabilization in neuronal injury Nat. Rev. Neurosci. 10 2009 481 494
13. L. Galluzzi, E. Morselli, O. Kepp, and G. Kroemer Targeting post-mitochondrial effectors of apoptosis for neuroprotection Biochim. Biophys. Acta 1787 2009 402 413
14. C. Harris, A.C. Maroney, and E.M. Johnson Jr Identification of JNK-dependent and-independent components of cerebellar granule neuron apoptosis J. Neurochem. 83 2002 992 1001 (Pubitemid 35316050)
15. T. Hisatomi, T. Ishibashi, J.W. Miller, and G. Kroemer Pharmacological inhibition of mitochondrial membrane permeabilization for europrotection Exp. Neurol. 218 2009 347 352
16. 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)
17. J.P. Hughes, D.R. Ward, L. Facci, J.C. Richardson, and S.D. Skaper Apoptosis-associated tyrosine kinase and neuronal cell death Neurochem. Res. 35 2010 588 597
18. T. Ikeuchi, K. Shimoke, T. Kubo, M. Yamada, and H. Hatanaka Apoptosis-inducing and-preventing signal transduction pathways in cultured cerebellar granule neurons Hum. Cell 11 1998 125 140
19. B. Ikiz, and S. Przedborski A sequel to the tale of p25/Cdk5 in neurodegeneration Neuron 60 5 2008 731 732
20. N. Jin, A.D. Kovács, Z. Sui, S. Dewhurst, and S.B. Maggirwar Opposite effects of lithium and valproic acid on trophic factor deprivation-induced glycogen synthase kinase-3 activation, c-Jun expression and neuronal cell death Neuropharmacology 48 2005 576 583 (Pubitemid 40332415)
21. D. Kim, C.L. Frank, M.M. Dobbin, R.K. Tsunemoto, W. Tu, P.L. Peng, J.S. Guan, B.H. Lee, L.Y. Moy, P. Giusti, N. Broodie, R. Mazitschek, I. Delalle, S.J. Haggarty, R.L. Neve, Y. Lu, and L.H. Tsai Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity Neuron 60 2008 803 817
22. I.I. Kruman, R.P. Wersto, F. Cardozo-Pelaez, L. Smilenov, S.L. Chan, F.J. Chrest, R. Emokpae Jr.; M. Gorospe, and M.P. Mattson Cell cycle activation linked to neuronal cell death initiated by DNA damage Neuron 41 2004 549 561 (Pubitemid 38253067)
23. A.C. LeBlanc The role of apoptotic pathways in Alzheimer's disease neurodegeneration and cell death Curr. Alzheimer Res. 2 2005 389 402
24. X. Liu, C.N. Kim, J. Pohl, and X. Wang Purification and characterization of an interleukin-1b-converting enzyme family protease that activates cysteine protease P32 (CPP32) J. Biol. Chem. 271 1996 13371 13376 (Pubitemid 26185376)
25. 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
26. S. Majd, A. Zarifkar, K. Rastegar, and M.A. Takhshid Different fibrillar Abeta 1-42 concentrations induce adult hippocampal neurons to reenter various phases of the cell cycle Brain Res. 1218 2008 224 229
27. C.T. Mendes, F.B. Mury, E. de Sá Moreira, F.L. Alberto, O.V. Forlenza, E. Dias-Neto, and W.F. Gattaz Lithium reduces Gsk3b mRNA levels: implications for Alzheimer Disease Eur. Arch. Psychiatry Clin. Neurosci. 259 2009 16 22
28. 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)
29. S. Miyamoto, A.N. Murphy, and J.H. Brown Akt mediated mitochondrial protection in the heart: metabolic and survival pathways to the rescue J. Bioenerg. Biomembr. 41 2009 169 180
30. + Eur. J. Biochem. 266 1999 886 891 (Pubitemid 30010106)
31. R.L. Neve, and D.L. McPhie The cell cycle as a therapeutic target for Alzheimer's disease Pharmacol. Ther. 111 2006 99 113 (Pubitemid 43786202)
32. W.T. O'Brien, and P.S. Klein Validating GSK3 as an in vivo target of lithium action Biochem. Soc. Trans. 37 2009 1133 1138
33. K. Orth, K. O'Rourke, G.S. Salvesen, and V.M. Dixit Molecular ordering of apoptotic mammalian CED-3/ICE-like proteases J. Biol. Chem. 271 1996 20977 20980 (Pubitemid 26292938)
34. G. Perry, A. Nunomura, and M.A. Smith A suicide note from Alzheimer disease neurons? Nat. Med. 4 1998 897 898 (Pubitemid 28364026)
35. G. Raivich C-Jun expression, activation and function in neural cell death, inflammation and repair J. Neurochem. 107 2008 898 906
36. E.M. Ribe, E. Serrano-Saiz, N. Akpan, and C.M. Troy Mechanisms of neuronal death in disease: defining the models and the players Biochem. J. 415 2008 165 182
37. S. Samantaray, S.K. Ray, and N.L. Banik Calpain as a potential therapeutic target in Parkinson's disease CNS Neurol. Disord.: Drug Targets 7 2008 305 312
38. 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 Dev. Brain Res. 112 1998 245 253
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. S. Subramaniam, J. Strelau, and K. Unsicker Growth differentiation factor-15 prevents low potassium-induced cell death of cerebellar granule neurons by differential regulation of Akt and ERK pathways J. Biol. Chem. 278 2003 8904 8912 (Pubitemid 36800366)
41. F.X. Sureda, F. Junyent, E. Verdaguer, C. Auladell, C. Pelegri, J. Vilaplana, J. Folch, A.M. Canudas, C.B. Zarate, M. Palls, and A. Camins Antiapoptotic drugs: a therapeutic strategy for the prevention of neurodegenerative diseases Curr. Pharm. Des. 17 2011 230 245
42. M. Tajes, M. Yeste-Velasco, X. Zhu, S.P. Chou, M.A. Smith, M. Palls, A. Camins, and G. Casadesús Activation of Akt by lithium: pro-survival pathways in aging Mech. Ageing Dev. 130 2009 253 261
43. A. Thakur, S.L. Siedlak, S.L. James, D.J. Bonda, A. Rao, K.M. Webber, A. Camins, M. Palls, G. Casadesus, H.G. Lee, R. Bowser, A.K. Raina, G. Perry, M.A. Smith, and X. Zhu Retinoblastoma protein phosphorylation at multiple sites is associated with neurofibrillary pathology in Alzheimer disease Int. J. Clin. Exp. Pathol. 1 2008 134 146
44. 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
45. K.M. Vasudevan, and L.A. Garraway AKT signaling in physiology and disease Curr. Top. Microbiol. Immunol. 347 2010 105 133
46. E. Verdaguer, E.G. Jord, D. Alvira, A. Jiménez, A.M. Canudas, J. Folch, V. Rimbau, M. Palls, and A. Camins Inhibition of multiple pathways accounts for the antiapoptotic effects of flavopiridol on potassium withdrawal-induced apoptosis in neurons J. Mol. Neurosci. 26 2005 71 84 (Pubitemid 41003428)
47. P.S. Vosler, C.S. Brennan, and J. Chen Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration Mol. Neurobiol. 38 2008 78 100
48. A. Watson, A. Eilers, D. Lallemand, J. Kyriakis, L. Rubin Lee, and J. Ham Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons J. Neurosci. 18 1998 751 762 (Pubitemid 28041911)
49. M. Yeste-Velasco, J. Folch, R. Trulls, M.A. Abad, M. Enguita, M. Palls, and A. Camins Glycogen synthase kinase-3 is involved in the regulation of the cell cycle in cerebellar granule cells Neuropharmacology 53 2007 295 307 (Pubitemid 47187455)
50. M. Yeste-Velasco, J. Folch, A. Jiménez, V. Rimbau, M. Palls, and A. Camins GSK-3 beta inhibition and prevention of mitochondrial apoptosis inducing factor release are not involved in the antioxidant properties of SB-415286 Eur. J. Pharmacol. 588 2008 239 243
51. M. Yeste-Velasco, J. Folch, G. Casadesús, M.A. Smith, M. Palls, and A. Camins Neuroprotection by c-Jun NH2-terminal kinase inhibitor SP600125 against potassium deprivation-induced apoptosis involves the Akt pathway and inhibition of cell cycle reentry Neuroscience 159 2009 1135 1147
52. M. Yeste-Velasco, J. Folch, M. Palls, and A. Camins The p38(MAPK) signaling pathway regulates neuronal apoptosis through the phosphorylation of the retinoblastoma protein Neurochem. Int. 54 2009 99 105
53. Z. Zhang, T. Wang, X. Cao, S. Sun, and L. Wang 6-OHDA induces cycle reentry and apoptosis of PC12 cells through activation of ERK1/2 signaling pathway J. Huazhong Univ. Sci. Technolo. Med. Sci. 29 2009 97 100
54. Z. Zhang, X. Cao, N. Xiong, H. Wang, J. Huang, S. Sun, Z. Liang, and T. Wang DNA polymerase-beta is required for 1-methyl-4-phenylpyridinium-induced apoptotic death in neurons Apoptosis 15 2010 105 115
55. X. Zhu, A.K. Raina, and M.A. Smith Cell cycle events in neurons. Proliferation or death? Am. J. Pathol. 155 1999 327 329 (Pubitemid 29370381)