Reactive oxygen species participate in the p38-mediated apoptosis induced by potassium deprivation and staurosporine in cerebellar granule neurons

International Journal of Biochemistry and Cell Biology

Volumn 43, Issue 9, 2011, Pages 1373-1382

  Ramiro Cortés, Yazmín ^a   Guemez Gamboa, Alicia ^a   Morán, Julio ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Antioxidants; Apoptosis; Caspase; NADPH oxidase; p38; Reactive oxygen species; Staurosporine

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STAUROSPORINE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; MOUSE; NONHUMAN; PARTICIPANT OBSERVATION; POTASSIUM DEFICIENCY; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 2; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CASPASES; CEREBELLUM; ENZYME ACTIVATION; ENZYME ASSAYS; IMIDAZOLES; KAEMPFEROLS; NADPH OXIDASE; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POTASSIUM; PYRIDINES; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; STAUROSPORINE;

EID: 79960918410     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2011.06.001     Document Type: Article

References (47)

1. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol Rev 87 2007 245 313 (Pubitemid 46209993)
2. A. Caballero-Benitez, and J. Moran Caspase activation pathways induced by staurosporine and low potassium: role of caspase-2 J Neurosci Res 71 2003 383 396 (Pubitemid 36159497)
3. J. Cao, M.M. Semenova, V.T. Solovyan, J. Han, E.T. Coffey, and M.J. Courtney Distinct requirements for p38alpha and c-Jun N-terminal kinase stress-activated protein kinases in different forms of apoptotic neuronal death J Biol Chem 279 2004 35903 35913 (Pubitemid 39100597)
4. L. Chen, L. Liu, J. Yin, Y. Luo, and S. Huang Hydrogen peroxide-induced neuronal apoptosis is associated with inhibition of protein phosphatase 2A and 5, leading to activation of MAPK pathway Int J Biochem Cell Biol 41 2009 1284 1295
5. A. Coyoy, A. Valencia, A. Guemez-Gamboa, and J. Moran Role of NADPH oxidase in the apoptotic death of cultured cerebellar granule neurons Free Radic Biol Med 45 2008 1056 1064
6. I. D'Alimonte, P. Ballerini, E. Nargi, S. Buccella, P. Giuliani, and P. Di Iorio Staurosporine-induced apoptosis in astrocytes is prevented by A1 adenosine receptor activation Neurosci Lett 418 2007 66 71 (Pubitemid 46602691)
7. S.R. D'Mello, C. Galli, T. Ciotti, and P. Calissano Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP Proc Natl Acad Sci USA 90 1993 10989 10993 (Pubitemid 23354354)
8. P.M. Dang, A. Stensballe, T. Boussetta, H. Raad, C. Dewas, and Y. Kroviarski A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites J Clin Invest 116 2006 2033 2043 (Pubitemid 44033327)
9. S.P. Davies, H. Reddy, M. Caivano, and P. Cohen Specificity and mechanism of action of some commonly used protein kinase inhibitors Biochem J 351 2000 95 105
10. J. el Benna, L.P. Faust, and B.M. Babior The phosphorylation of the respiratory burst oxidase component p47phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases J Biol Chem 269 1994 23431 23436
11. P. Ferri, T. Cecchini, S. Ciaroni, P. Ambrogini, R. Cuppini, and S. Santi Vitamin E affects cell death in adult rat dentate gyrus J Neurocytol 32 2003 1155 1164 (Pubitemid 39004724)
12. J.C. Fitzgerald, C. Ufer, L.A. De Girolamo, H. Kuhn, and E.E. Billett Monoamine oxidase-A modulates apoptotic cell death induced by staurosporine in human neuroblastoma cells J Neurochem 103 2007 2189 2199 (Pubitemid 350173561)
13. V. Gallo, A. Kingsbury, R. Balazs, and O.S. Jorgensen The role of depolarization in the survival and differentiation of cerebellar granule cells in culture J Neurosci 7 1987 2203 2213 (Pubitemid 17114929)
14. B. Ge, H. Gram, F. Di Padova, B. Huang, L. New, and R.J. Ulevitch MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation of p38alpha Science 295 2002 1291 1294 (Pubitemid 34157620)
15. K. Godl, J. Wissing, A. Kurtenbach, P. Habenberger, S. Blencke, and H. Gutbrod An efficient proteomics method to identify the cellular targets of protein kinase inhibitors Proc Natl Acad Sci USA 100 2003 15434 15439 (Pubitemid 38021007)
16. M. Gomez-Lazaro, M.F. Galindo, R.M. Melero-Fernandez de Mera, F.J. Fernandez-Gomez, C.G. Concannon, and M.F. Segura Reactive oxygen species and p38 mitogen-activated protein kinase activate Bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate Mol Pharmacol 71 2007 736 743 (Pubitemid 46294084)
17. Y. Gotoh, and J.A. Cooper Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction J Biol Chem 273 1998 17477 17482 (Pubitemid 28355079)
18. L.J. Greenlund, T.L. Deckwerth, and E.M. Johnson Jr. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death Neuron 14 1995 303 315
19. A. Guemez-Gamboa, and J. Moran NOX2 mediates apoptotic death induced by staurosporine but not by potassium deprivation in cerebellar granule neurons J Neurosci Res 87 2009 2531 2540
20. J. Harada, and M. Sugimoto An inhibitor of p38 and JNK MAP kinases prevents activation of caspase and apoptosis of cultured cerebellar granule neurons Jpn J Pharmacol 79 1999 369 378 (Pubitemid 29168148)
21. J.T. Hong, J.H. Yen, L. Wang, Y.H. Lo, Z.T. Chen, and M.J. Wu Regulation of heme oxygenase-1 expression and MAPK pathways in response to kaempferol and rhamnocitrin in PC12 cells Toxicol Appl Pharmacol 237 2009 59 68
22. F.J. Martin-Romero, E. Garcia-Martin, and C. Gutierrez-Merino Inhibition of oxidative stress produced by plasma membrane NADH oxidase delays low-potassium-induced apoptosis of cerebellar granule cells J Neurochem 82 2002 705 715 (Pubitemid 34831508)
23. J. Moran, and A.J. Patel Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during development Brain Res Dev Brain Res 46 1989 97 105 (Pubitemid 19061067)
24. J. Moran, T. Itoh, U.R. Reddy, M. Chen, E.S. Alnemri, and D. Pleasure Caspase-3 expression by cerebellar granule neurons is regulated by calcium and cyclic AMP J Neurochem 73 1999 568 577 (Pubitemid 29339829)
25. S. Morton, R.J. Davis, and P. Cohen Signalling pathways involved in multisite phosphorylation of the transcription factor ATF-2 FEBS Lett 572 2004 177 183 (Pubitemid 39092532)
26. R. Nath, K. McGinnis, S. Dutta, B. Shivers, and K.K. Wang Inhibition of p38 kinase mimics survival signal-linked protection against apoptosis in rat cerebellar granule neurons Cell Mol Biol Lett 6 2001 173 184 (Pubitemid 32588277)
27. K. Ono, and J. Han The p38 signal transduction pathway: activation and function Cell Signal 12 2000 1 13 (Pubitemid 30017963)
28. A. Porras, S. Zuluaga, E. Black, A. Valladares, A.M. Alvarez, and C. Ambrosino P38 alpha mitogen-activated protein kinase sensitizes cells to apoptosis induced by different stimuli Mol Biol Cell 15 2004 922 933 (Pubitemid 38146504)
29. I. Qadri, M. Iwahashi, J.M. Capasso, M.W. Hopken, S. Flores, and J. Schaack Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1 Biochem J 378 2004 919 928 (Pubitemid 38406869)
30. M. Raman, W. Chen, and M.H. Cobb Differential regulation and properties of MAPKs Oncogene 26 2007 3100 3112 (Pubitemid 46763006)
31. M. Raman, S. Earnest, K. Zhang, Y. Zhao, and M.H. Cobb TAO kinases mediate activation of p38 in response to DNA damage EMBO J 26 2007 2005 2014 (Pubitemid 46625802)
32. Y. Ramiro-Cortes, and J. Moran Role of oxidative stress and JNK pathway in apoptotic death induced by potassium deprivation and staurosporine in cerebellar granule neurons Neurochem Int 55 2009 581 592
33. H. Sakurai, H. Miyoshi, J. Mizukami, and T. Sugita Phosphorylation- dependent activation of TAK1 mitogen-activated protein kinase kinase kinase by TAB1 FEBS Lett 474 2000 141 145 (Pubitemid 30330823)
34. J.M. Salvador, P.R. Mittelstadt, T. Guszczynski, T.D. Copeland, H. Yamaguchi, and E. Appella Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases Nat Immunol 6 2005 390 395 (Pubitemid 41716779)
35. A.K. Samhan-Arias, F.J. Martin-Romero, and C. Gutierrez-Merino Kaempferol blocks oxidative stress in cerebellar granule cells and reveals a key role for reactive oxygen species production at the plasma membrane in the commitment to apoptosis Free Radic Biol Med 37 2004 48 61 (Pubitemid 38746650)
36. J.B. Schulz, M. Weller, and T. Klockgether Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species J Neurosci 16 1996 4696 4706 (Pubitemid 26251065)
37. K. Takeda, and H. Ichijo Neuronal p38 MAPK signalling: an emerging regulator of cell fate and function in the nervous system Genes Cells 7 2002 1099 1111 (Pubitemid 35264519)
38. S.P. Tammariello, M.T. Quinn, and S. Estus NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons J Neurosci 20 2000 RC53
39. N.A. Thornberry, T.A. Rano, E.P. Peterson, D.M. Rasper, T. Timkey, and M. Garcia-Calvo A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis J Biol Chem 272 1997 17907 17911 (Pubitemid 27306365)
40. K. Tobiume, A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, and K. Takeda ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis EMBO Rep 2 2001 222 228 (Pubitemid 32273301)
41. A. Valencia, and J. Moran Role of oxidative stress in the apoptotic cell death of cultured cerebellar granule neurons J Neurosci Res 64 2001 284 297 (Pubitemid 32385697)
42. W.F. Waas, H.H. Lo, and K.N. Dalby The kinetic mechanism of the dual phosphorylation of the ATF2 transcription factor by p38 mitogen-activated protein (MAP) kinase alpha. Implications for signal/response profiles of MAP kinase pathways J Biol Chem 276 2001 5676 5684
43. 2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3 J Neurosci Res 72 2003 508 519 (Pubitemid 36523425)
44. S. Yamagishi, M. Yamada, Y. Ishikawa, T. Matsumoto, T. Ikeuchi, and H. Hatanaka p38 mitogen-activated protein kinase regulates low potassium-induced c-Jun phosphorylation and apoptosis in cultured cerebellar granule neurons J Biol Chem 276 2001 5129 5133
45. T. Zarubin, and J. Han Activation and signaling of the p38 MAP kinase pathway Cell Res 15 2005 11 18 (Pubitemid 41653958)
46. M. Zhou, R. Dominguez, and M. Baudry Superoxide dismutase/catalase mimetics but not MAP kinase inhibitors are neuroprotective against oxygen/glucose deprivation-induced neuronal death in hippocampus J Neurochem 103 2007 2212 2223 (Pubitemid 350173556)
47. S. Zhuang, J.T. Demirs, and I.E. Kochevar p38 mitogen-activated protein kinase mediates bid cleavage, mitochondrial dysfunction, and caspase-3 activation during apoptosis induced by singlet oxygen but not by hydrogen peroxide J Biol Chem 275 2000 25939 25948