Calcineurin and Erk1/2-signaling pathways are involved in the antiapoptotic effect of cyclosporin A on astrocytes exposed to simulated ischemia in vitro

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 374, Issue 2, 2006, Pages 127-139

  Gabryel, Bozena ^a   Pudelko, Anna ^a   Adamczyk, Jakub ^b   Fischer, Ireneusz ^a   Malecki, Andrzej ^a  

^a UNIVERSITY OF SILESIA   (Poland)

^b MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

Akt; Apoptosis; Astrocytes; Calcineurin; Cyclosporin A; Erk1 2; Ischemia

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CALCINEURIN; CASPASE 3; CYCLOSPORIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL XL; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ASTROCYTE; CELL PROTECTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IN VITRO STUDY; ISCHEMIA; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANDROSTADIENES; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ASTROCYTES; BCL-X PROTEIN; BLOTTING, WESTERN; CALCINEURIN; CASPASE 3; CELL HYPOXIA; CYCLOSPORINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVONOIDS; IMMUNOBLOTTING; IMMUNOSUPPRESSIVE AGENTS; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

EID: 33750455119     PISSN: 00281298     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00210-006-0106-x     Document Type: Article

References (60)

1. Arnette D, Gibson TB, Lawrence MC, January B, Khoo S, McGlynn K, Vanderbilt CA, Cobb MH (2003) Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic beta cells. J Biol Chem 278:32517-32525
2. Asai A, Qiu J, Narita Y, Chi S, Saito N, Shinoura N, Hamada H, Kuchino Y, Kirino T (1999) High level calcineurin activity predisposes neuronal cells to apoptosis. J Biol Chem 274:34450-34458
3. Aschner M (1998) Astrocytic functions and physiological reactions to injury: the potential to induce and/or exacerbate neuronal dysfunction - a forum position paper. Neurotoxicology 19:7-18
4. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and-independent mechanisms. Science 286:1358-1362
5. Bradford MM (1976) A rapid and sensitive method for the quantification of 'microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248-251
6. Burgering BM, Coffer PJ (1995) Protein kinase B (c-Akt) in phosphatidilinositol-3-OH kinase signal. Nature 376:599-602
7. Butcher SP, Henshall DC, Teramura Y, Iwasaki K, Sharkey J (1997) Neuroprotective actions of FK506 in experimental stroke: in vivo evidence against an antiexcitotoxic mechanism. J Neurosci 17:6939-6946
8. Chinopoulos C, Starkov AA, Fiskum G (2003) Cyclosporin A-insensitive permeability transition in brain mitochondria: inhibition by 2-aminoethoxydiphenyl borate. J Biol Chem 278:27382-27889
9. Ciechomska I, Pyrzynska B, Kazmierczak P, Kaminska B (2003) Inhibition of Akt kinase signaling and activation of Forkhead are indispensable for upregulation of FasL expression in apoptosis of glioma cells. Oncogene 23:7617-7627
10. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241
11. Dignam JD, Lebovitz RM, Roeder RG (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11:1474-1489
12. Domanska-Janik K, Buzanska L, Dluzniewska J, Kozlowska H, Sarnowska A, Zablocka B (2004) Neuroprotection by cyclosporin A following transient brain ischemia correlates with the inhibition of the early efflux of cytochrome C to cytoplasm. Brain Res Mol Brain Res 121:50-59
13. Drake M, Friberg H, Boris-Moller F, Sakata K, Wieloch T (1996) The immunosuppressant FK506 ameliorates ischaemic damage in the rat brain. Acta Physiol Scand 158:155-159
14. Dramsi S, Scheid MP, Maiti A, Hojabrpour P, Chen X, Schubert K, Goodlett DR, Aebersold R, Duronio V (2002) Identification of a novel phosphorylation site, Ser-170, as a regulator of bad proapoptotic activity. J Biol Chem 277:6399-6405
15. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR (1995) Synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 92:7686-7689
16. El Bekay R, Alvarez M, Monteseirin J, Alba G, Chacon P, Vega A, Martin-Nieto J, Jimenez J, Pintado E, Bedoya FJ, Sobrino F (2003) Oxidative stress is a critical mediator of the angiotensin II signal in human neutrophils: involvement of mitogen-activated protein kinase, calcineurin, and the transcription factor NF-kappaB. Blood 102:662-671
17. Franke TF, Kaplan DR, Cantley LC (1997) PI3K: downstream AKTion blocks apoptosis. Cell 88:435-437
18. Fruman DA, Klee CB, Bierer BE, Burakoff SJ (1992) Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc Natl Acad Sci USA 89:3686-3690
19. Fujita Y, Izawa Y, Ali N, Kanematsu Y, Tsuchiya K, Hamano S, Tamaki T, Yoshizumi M (2006) Pramipexole protects against H2O2-induced PC12 cell death. Naunyn-Schmiedebergs Arch Pharmacol 372:257-266
20. Gabryel B, Adamczyk J, Huzarska M, Pudełko A, Trzeciak HI (2002) Aniracetam attenuates apoptosis of astrocytes subjected to simulated ischemia in vitro. Neurotoxicology 23:385-395
21. Gabryel B, Toborek T, Malecki A (2005) Immunophilin ligands attenuate damage in rat astrocyte cultures simultaneously depleted of glutathione and exposed to simulated ischemia in vitro. Comparison with N-acetylcysteine. Neurotoxicology 26:373-384
22. Gabryel B, Malecki A (2006) Ebselen attenuates oxidative stress in ischemic astrocytes depleted of glutathione. Comparison with glutathione precursors. Pharmacol Rep 58:381-392
23. 2 is involved in the antiapoptotic effect of FK506 and cyclosporin A on astrocytes exposed to simulated ischemia in vitro. J Pharm Sci (in press)
24. Garcia-Cozar FJ, Okamura H, Aramburu JF, Shaw KTY, Pelletier R, Showalter R, Villafranca E, Rao A (1998) Two-side interaction of nuclear factor of activated T cells with activated calcineurin. J Biol Chem 273:23877-23883
25. Harada H, Becknell B, Wilm M, Mann M, Huang LJ, Taylor SS, Scott JD, Korsmeyer SJ (1999) Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell 3:413-422
26. Hertz L, Juurlink BHJ, Szuchet S (1985) Cell cultures. In: Lajtha A (ed) Handbook of neurochemistry. Plenum, New York, pp 603-661
27. Heusch WL, Maneckjee R (1998) Signaling pathways involved in nicotine regulation of apoptosis of human lung cancer cells. Carcinogenesis 19:551-556
28. Ikeda Y, Miura T, Sakamoto J, Miki T, Tanno M, Kobayashi H, Ohori K, Takahashi A, Shimamoto K (2006) Activation of ERK and suppression of calcineurin are interacting mechanisms of cardioprotection afforded by delta-opioid receptor activation. Basic Res Cardiol
29. Jiang Z, Zuang Y, Chen X, Lam PY, Yang H, Xu Q, Yu ACH (2002) Activation of Erk1/2 and Akt in astrocytes under ischemia. Biochem Biophys Res Commun 294:726-733
30. Kawano T, Fukunaga K, Takeuchi Y, Morioka M, Yano S, Hamada J, Ushio Y, Miyamoto E (2001) Neuroprotective effect of sodium orthovanadate on delayed neuronal death after transient forebrain ischemia in gerbil hippocampus. J Cereb Blood Flow Metab 21:1268-1280
31. Klee CB, Ren H, Wang X (1998) Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273:13367-13370
32. Kristian T, Gertsch J, Bates TE, Siesjo BK (2000) Characteristics of the calcium-triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone O. J Neurochem 74:1999-2009
33. Lee JI, Ganster RW, Geller DA, Burckart GJ, Thomson AW, Lu L (1999) Cyclosporine A inhibits the expression of co-stimulatory molecules on in vitro-generated dendritic cells: association with reduced nuclear translocation of nuclear factor kappa B. Transplantation 68:1255-1263
34. Matsuda T, Takuma K, Asano S, Kishida K, Mori K, Maeda S, Baba A (1998) Protection by calcineurin inhibitors against reperfusion injury of cultured rat astrocytes. J Neurochem 70:2004-2011
35. Mattson MP, Goodman Y, Luo H, Fu W, Furukawa K (1997) Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res 49:681-697
36. Miyata K, Omori N, Uchino H, Yamaguchi T, Isshiki A, Shibasaki F (2001) Involvement of the brain-derived neurotrophic factor/ TrkB pathway in neuroprotective effect of cyclosporin A in forebrain ischemia. Neuroscience 105:571-578
37. Murozono M, Matsumoto S, Matsumoto E, Isshiki A, Watanabe Y (2004) Neuroprotective and neurotoxic effects of cyclosporine A on transient focal ischemia in mdr1a knockout mice. Eur J Pharmacol 498:115-118
38. Pende M, Fischer TL, Simpson PB, Russell JT, Blenis J, Gallo V (1997) Neurotransmitter-and growth factor induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ribosomal S6 kinase pathway. J Neurosci 15:1291-1301
39. Phillis JW, Diaz FG, O'Regan MH, Pilitsis JG (2002) Effects of immunosuppressants, calcineurin inhibition, and blockade of endoplasmic reticulum calcium channels on free fatty acid efflux from the ischemic/reperfused rat cerebral cortex. Brain Res 957:12-24
40. Pyrzynska B, Lis A, Mosieniak G, Kaminska B (2001) Cyclosporin A-sensitive signaling pathway involving calcineurin regulates survival of reactive astrocytes. Neurochem Int 38:409-415
41. Reichert SA, Kim-Han JS, Dugan LL (2001) The mitochondrial permeability transition pore and nitric oxide synthase mediate early mitochondrial depolarization in astrocytes during oxygenglucose deprivation. J Neurosci 21:6608-6616
42. Reyman KG, Schmidt W, Striggow F, Reiser G (2000) Immunophilins in the CNS-potential targets for neuroprotective processes in the brain after cerebral ischemia. Restor Neurol Neurosci 16:33
43. Scheid MP, Schubert KM, Duronio V (1999) Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase. J Biol Chem 274:31108-31113
44. 2+-activated cell death in mammalian cells. J Cell Biol 131:735-743
45. Simmons ML, Murphy S (1992) Induction of nitric oxide synthase in glial cells. J Neurochem 59:897-905
46. Sinigaglia-Coimbra R, Cavalheiro EA, Coimbra C (2002) Protective effect of systemic treatment with cyclosporine A after global ischemia in rats. J Neurol Sci 203:273-276
47. Sweat JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10
48. Takuma K, Baba A, Matsuda T (2004) Astrocyte apoptosis: implications for neuroprotection. Prog Neurobiol 72:111-127
49. Thanos D, Maniatis T (1985) NF-κB, a lesson in family values. Cell 80:529-532
50. Uchino H, Elmer E, Uchino K, Lindvall O, Siesjö BK (1995) Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischemia in the rat. Acta Physiol Scand 155:469-471
51. Uchino H, Minamikawa-Tachino R, Kristian T, Perkins G, Narazaki M, Siesjo BK, Shibasaki F (2002) Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochondrial permeability transition. Neurobiol Dis 10: 219-233
52. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F, McKeon F, Bobo T, Franke TF, Reed JC (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284:339-343
53. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180
54. Wiessner C, Neumann-Haefelin T, Vogel P, Back T, Hossmann KA (1995) Transient forebrain ischemia induces an immediate-early gene encoding the mitogen-activated protein kinase phosphatase 3CH134 in the adult rat brain. Neuroscience 64:959-966
55. Yamaguchi T, Miyata K, Shibasaki F, Isshiki A, Uchino H (2006) Effect of cyclosporin a on immediate early gene in rat global ischemia and its neuroprotection. J Pharmacol Sci 100:73-81
56. Yoshimoto T, Uchino H, He QP, Li PA, Siesjo BK (2001) Cyclosporin A, but not FK506, prevents the downregulation of phosphorylated Akt after transient focal ischemia in the rat. Brain Res 899:148-158
57. Yung HW, Tolkovsky AM (2003) Erasure of kinase phosphorylation in astrocytes during oxygen-glucose deprivation is controlled by ATP levels and activation of phosphatases. J Neurochem 86:1281-1288
58. Yujiri T, Sather S, Fanger GR, Johnson GL (1998) Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption. Science 282:1911-1914
59. Zawadzka M, Kaminska B (2003) Immunosuppressant FK506 affects multiple signaling pathways and modulates gene expression in astrocytes. Mol Cell Neurosci 22:202-209
60. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87:619-628