Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus

Journal of Neuroscience

Volumn 20, Issue 12, 2000, Pages 4506-4514

  Sugino, Toshiyuki ^a   Nozaki, Kazuhiko ^a   Takagi, Yasushi ^a   Hattori, Itaro ^a   Hashimoto, Nobuo ^a   Moriguchi, Tetsuo ^a   Nishida, Eisuke ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

c Jun N terminal kinase (JNK); Delayed neuronal death (DND); Extracellular signal regulated kinase (ERK); Gerbil; Hippocampus; Mitogen activated protein kinase (MAPK); p38 mitogen activated protein kinase (p38); Transient global ischemia

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; GERBIL; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0034659866     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-12-04506.2000     Document Type: Article

References (57)

1. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, Shiojima I, Hiroi Y, Yazaki Y (1997) Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 100:1813-1821.
2. Alessandrini A, Namura S, Moskowitz MA, Bonventre JV (1999) MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci USA 96:12866-12869.
3. Antonawich FJ, Krajewski S, Reed JC, Davis JN (1998) Bcl-xl Bax interaction after transient global ischemia. J Cereb Blood Flow Metab 18:882-886.
4. Assefa Z, Vantieghem A, Declercq W, Vandenabeele P, Vandenheede JR, Merlevede W, de Witte P, Agostinis P (1999) The activation of c-Jun N-terminal kinase and p38 mitogen-activated protein kinase signaling pathways protects HeLa cells from apoptosis following photodynamic therapy with hypcricin. J Biol Chem 274:8788-8796.
5. Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct signaling pathways. Science 260:181-186.
6. Boulton TG, Nyc SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD (1991) ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663-675.
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Cano E, Mahadcvan LC (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20:117-122.
9. Cobb MH, Goldsmith EJ (1995) How MAP kinases are regulated. J Biol Chem 270:14843-14846.
10. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364:229-233.
11. Davis RJ (1999) Signal transduction by the c-Jun N-terminal kinase. Biochem Soc Symp 64:1-12.
12. Ferrer I, Ballabriga J, Pozas E (1997) Transient forebrain ischemia in the adult gerbil is associated with a complex c-Jun response. NeuroReport 8:2483-2487.
13. Fiore RS, Murphy TH, Sanghera JS, Pelech SL, Barahan JM (1993) Activation of mitogen-activated protein kinase by glutamate receptor stimulation in rat primary cortical cultures. J Neurochem 61:1626-1633.
14. Flood DG, Finn JP, Walton KM, Dionne CA, Contreras PC, Miller MS, Bhat RV (1998) Immunolocalization of the mitogen-activated protein kinases p42MAPK and JNK1, and their regulatory kinases MEK1 and MEK4, in adult rat central nervous system. J Comp Neurol 398:373-392.
15. Fukuda M, Gotoh Y, Tachihana T, Dell K, Hattori S. Yoneda Y, Nishida E (1995) Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 11:239-244.
16. Giasson BI, Bruening W, Durham HD, Murshynski WE (1999) Activation of stress-activated kinases correlates with neurite outgrowth induced by protease inhibition in PC12 cells. J Neurochem 72:1081-1087.
17. Ginsberg MD, Prado R, Dietrich WD, Busto R, Watson BD (1987) Hyperglycemia reduces the extent of cerebral infarction in rats. Stroke 18:570-574.
18. Gonzalez-Zulueta M, Feldman AB, Klesse LJ, Kalb RG, Dillman JF, Parada LF, Dawson TM, Dawson VL (2000) Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 97:436-441.
19. Herdegen T, Claret F-X, Kallunki T, Martin-Villalba A, Winter C, Hunter T, Karin M (1998) Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J Neurosci 18:5124-5135.
20. Himi T, Ishizaki Y, Murota S (1998) A caspase inhibitor blocks ischaemia-induced delayed neuronal death in the gerbil. Eur J Neurosci 10:777-781.
21. Hu BR, Wieloch T (1994) Tyrosine phosphorylation and activation of mitogen-activated protein kinase in the rat brain following transient cerebral ischemia. J Neurochem 62:1357-1367.
22. Huang S, Jiang Y, Li Z, Nishida E, Mathias P, Lin S, Ulevitch RJ, Nemerow GR, Han J (1997) Apoptosis signaling pathway in T cells is composed of ICE/Ced-3 family proteases and MAP kinase kinase 6b. Immunity 6:739-749.
23. Kawasaki H, Morooka T, Shimohama S, Kimura J, Hirano T, Gotoh Y, Nishida E (1997) Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J Biol Chem 272:18518-18521.
24. Kindy MS (1993) Inhibition of tyrosine phosphorylation prevents delayed neuronal death following cerebral ischemia. J Cereb Blood Flow Metab 13:372-377.
25. Kirino T (1982) Delayed neuronal death on the gerbil hippocampus following ischemia. Brain Res 239:57-69.
26. Kummer JL, Rao PK, Heidenreich KA (1997) Apoptosis induced by withdrawal of trophic factors is mediated by p38 mitogen-activated protein kinase. J Biol Chem 272:20490-20494.
27. Kurino M, Fukunaga K, Ushio Y, Miyamoto E (1995) Activation of mitogen-activated kinase in cultured rat hippocampal neurons by stimulation of glutamate receptors. J Neurochem 65:1282-1289.
28. Kyriakis JM, Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18:567-577.
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Larsen JK, Yamboliev IA, Weber LA, Gerthoffer WT (1997) Phosphorylation of the 27 kDa heat shock protein via p38 MAP kinase and MAPKAP kinase in smooth muscle. Am J Physiol 273:L930-L940.
31. Leary JJ, Brigati DJ, Ward DC (1983) Rapid and sensitive colorimetric method for visualizing biotin-labeled DNA probes hybridized to DNA or RNA immobilized on nitrocellulose: bio-blots. Proc Natl Acad Sci USA 80:4045-4049.
32. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Heys JR, Landvatter SW, Strickler JE, McLaughlin MM, Siemens IR, Fisher SM, Livi GP, White JR, Adams JL, Young PR (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739-746.
33. Maroney AC, Glicksman MA, Basma AN, Walton KM, Ernest Jr K, Murphy CA, Bartlett BA, Finn JP, Angeles T, Matsuda Y, Neff NT, Dionne CA (1998) Motoneuron apoptosis is blocked by CEP-1347 (KT 7515), a novel inhibitor of the JNK signaling pathway. J Neurosci 18:104-111.
34. Mitani A, Namba S, Ikemune K, Yanase H, Arai T, Kataoka K (1998) Postischemic enhancement of N-methyl-D aspartic acid (NMDA) and non-NMDA receptor-mediated responses in hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 18:1088-1098.
35. Mizukami Y, Yoshioka K, Morimoto S, Yoshida K (1997) A novel mechanism of JNK1 activation. J Biol Chem 272:16657-16662.
36. Morooka T, Nishida E (1998) Requiremen: of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J Biol Chem 273:24285-24288.
37. Nagarkatti DS, Sha'afi RI (1998) Role of p38 MAP kinase in myocardial stress. J Mol Cell Cardiol 30:1651-1664.
38. Nishida E, Gotoh Y (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem Sci 18:128-131.
39. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y (1995) Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001-1011.
40. Ozawa H, Shioda S, Dohi K, Matsumoto H, Mizushima H, Zhou CJ, Funahashi H, Nakai Y, Nakajo S, Matsumoto K (1999) Delayed neuronal cell death in the rat hippocampus is mediated by the mitogen-activated protein kinase signal transduction pathway. Neurosci Lett 262:57-60.
41. Pang L, Sawada T, Decker SJ, Saltiel AR (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem 270:13585-13588.
42. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498.
43. Robinson MJ, Cobb MH (1997) Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9:180-186.
44. Robinson MJ, Stippec SA, Goldsmith E, White M, Cobb MH (1998) A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr Biol 8:1141-1150.
45. Rosen LB, Ginty DD, Weber MJ, Greenberg ME (1994) Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12:1207-1221.
46. Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9:726-735.
47. Sgambato V, Pages C, Rogard M, Besson MJ, Caboche J (1998) Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J Neurosci 18:8814-8825.
48. Thiessen DD, Goar S (1970) Stereotaxic atlas of the hypothalamus of the mongolian gerbil. J Comp Neurol 140:123-128.
49. Tokime T, Nozaki K, Kikuchi H (1996) Neuroprotective effect of FK506, an immunosuppressant, on transient global ischemia in gerbil. Neurosci Lett 206:81-84.
50. Toyoshima F, Moriguchi T, Nishida E (1997) Fas induces cytoplasmic apoptotic responses and activation of the MKK7-JNK/SAPK and MKK6-p38 pathways independent of CPP32-like proteases. J Cell Biol 139:1005-1015.
51. Walton KM, DiRocco R, Bartlett BA, Koury E, Marcy VR, Jarvis B, Schaefer EM, Bhat RV (1998) Activation of p38MAPK in microglia after ischemia. J Neurochem 70:1764-1767.
52. Waters SB, Holt KH, Ross SE, Syu LJ, Guan KL, Saltiel AR, Koretzky GA, Pessin JE (1995) Desensitization of Ras activation by a feedback disassociation of the SOS-Grb2 complex. J Biol Chem 270:20883-20886.
53. Weinbrenner C, Liu G-S, Cohen MV, Downey JM (1997) Phosphorylation of tyrosine 182 of p38 mitogen-activated protein kinase correlates with the protection of preconditioning in the rabbit heart. J Mol Cell Cardiol 29:2383-2391.
54. Whitmarsh AJ, Yang S-H, Su MS-S, Sharrocks AD, Davis RJ (1997) Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol Cell Biol 17:2360-2371.
55. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
56. Yang DD, Kuan CY, Whitmarsh AJ, Rincon M, Zheng TS, Davis RJ, Rakic P, Flavell RA (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389:865-867.
57. Yin T, Sandhu G, Wolfgang CD, Burrier A, Webb RL, Rigcl DF, Hai T, Whelan J (1997) Tissue-specific pattern of stress kinase activation in ischemic/reperfused heart and kidney. J Biol Chem 272:19943-19950.