Ischemia leads to apoptosis - and necrosis-like neuron death in the ischemic rat hippocampus

Brain Pathology

Volumn 14, Issue 4, 2004, Pages 415-424

  Müller, Georg Johannes ^a   Stadelmann, Christine ^b   Bastholm, Lone ^a   Elling, Folmer ^a   Lassmann, Hans ^c   Johansen, Flemming Fryd ^a,d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d NONE   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; SERUM ALBUMIN; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL DEGENERATION; CELL STRUCTURE; CHROMATIN CONDENSATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVATION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; NONHUMAN; NUCLEOLUS; PROTEIN EXPRESSION; RAT; UPREGULATION;

EID: 8744291025     PISSN: 10156305     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2004.tb00085.x     Document Type: Article

References (60)

1. Behrens A, Sibilia M, Wagner EF (1999) Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 21: 326-329
2. Bering R, Diemer NH, Draguhn A, Johansen FF (1995) Co-localization of somatostatin mRNA and parvalbumin in dorsal rat hippocampus after cerebral ischemia. Hippocampus 5: 341-348
3. Biggiogera M, Bottone MG, Pellicciari C (1997) Nuclear ribonucleoprotein-containing structures undergo severe rearrangement during spontaneous thymocyte apoptosis. A morphological study by electron microscopy. Histochem Cell Biol 107: 331-336
4. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9: 1180-1186
5. Cao G, Luo Y, Nagayama T, Pei W, Stetler RA, Graham SH, Chen J (2002) Cloning and characterization of rat caspase-9: implications for a role in mediating caspase-3 activation and hippocampal cell death after transient cerebral ischemia. J Cereb Blood Flow Metab 22: 534-546
6. Carboni S, Hiver A, Szyndralewiez C, Gaillard P, Gotteland JP, Vitte PA (2004) AS601245 (1,3-benzothiazol-2-yl (2-[[2-(3-pyridinyl) ethyl] amino]-4 pyrimidinyl) acetonitrile): a c-Jun NH2-terminal protein kinase inhibitor with neuroprotective properties. J Pharmacol Exp Ther 310: 25-32
7. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, Simon RP (1998). Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18: 4914-4928
8. Colbourne F, Sutherland GR, Auer RN (1999) Electron microscopic evidence aganist apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 19: 4200-4210
9. Columbaro M, Gobbi P, Renò F, Luchetti F, Santi S, Valmori A, Falcieri E (1999) A multiple technical approach to the study of apoptotic cell micronuclei. Scanning 8: 541-548
10. Desphande JK, Bergstedt K, Lindén T, Kalimo H, Wieloch T (1992) Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence aganinst programmed cell death. Exp Brain Res 88: 91-105
11. Endres M, Namura S, Shimizu-Sasamata M, Waeber C, Zhang L, Gómez-Isla T, Hyman BT, Moskowitz MA (1998) Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J Cereb Blood Flow Metab 18: 238-247
12. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM Jr (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127: 1717-1727
13. Evert BO, Wullner U, Klockgether T (2000) Cell death in polyglutamine diseases. Cell Tissue Res 301: 189-204
14. Ferrer I, Pozas E, Marti M, Blanco R, Planas AM (1997) Methyl-azoxymethanol acetate-induced apoptosis in the external granule layer of the developing cerebellum of the rat is associated with strong c-Jun expression and formation of high molecular weight c-Jun complexes. J Neuropathol Exp Neurol 56: 1-9
15. Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, Elling F, Leist M, Jäättelä M (2001) Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 153: 999-1010
16. Garrah JM, Bisby MA, Rossiter JP (1998) Immunolabelling of the cytoplasm and processes of apoptotic facial motorneurons following axotomy in the neonatal rat. Acta Neuropathol 95: 223-228
17. Gillardon F, Kiprianova I, Sandkühler J, Hossmann K-A, Spranger M (1999) Inhibition of caspases prevents cell death of hippocampal CA1 neurons, but not impairment of hippocampal long-term potentiation following global ischemia. Neuroscience 93: 1219-1222
18. Gillardon F, Böttiger B, Schmitz B, Zimmermann M, Hossmann KA (1997) Activation of CPP-32 protease in hippocampal neurons following ischemia and epilepsy. Mol Brain Res 50: 16-22
19. Gillardon F, Spranger M, Tiesler C, Hossmann KA (1999). Expression of cell death-associated phospho-c-Jun and p53-activated gene 608 in hippocampal CA1 neurons following global ischemia. Mol Brain Res 73: 138-143.
20. Gold R, Schmid M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV, Lassmann H (1994) Differentiation between cellular apoptosis and necrosis by combined use of in situ tailing and nick translation techniques. Lab Invest 71: 219-225
21. Gorman AM, Ceccatelli S, Orrenius S (2000) Role of mitochondria in neuronal apoptosis. Dev Neurosci 22: 348-358
22. Ham J, Eilers A, Whitfield J, Neame SJ, Shah B (2000) c-Jun and the transcriptional control of neuronal apoptosis. Biochem Pharmacol 60, 1015-1021
23. Han BH, Xu D, Choi J, Han Y, Xanthoudakis S, Roy S, Tam J, Vaillancourt J, Colucci J, Siman R, Giroux A, Robertson GS, Zamboni R, Nicholson DW, Holtzman DM (2002) Selective, reversible caspase-3 inhibitor is neuroprotective and reveals distinct pathways of cell death after neonatal hypoxic-ischemic brain injury. J Biol Chem 277: 30128-30136
24. 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
25. Horky M, Wurzer G, Kotala V, Anton M, Vojtesek B, Vacha J, Wesierska-Gadek J (2001) Segregation of nucleolar components coincides with caspase-3 activation in cisplatin-treated HeLa cells. J Cell Sci 114: 663-670
26. Horn M, Schlote W (1992) Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol 85: 79-87
27. Ito U, Spat M, Walker JT Jr, Klatzo I (1975) Experimental cerebral ischemia in Mongolian gerbils: I. Light microscopic observations. Acta Neuropathol 32: 209-233
28. Jäättelä M, Tschopp J (2003) Caspase-independent cell death in T lymphocytes. Nat Immunol 4: 416-423
29. Johansen FF (1993) Interneurons in rat hippocampus after cerebral ischemia. Morphometric, functional, and therapeutic investigations. Acta Neurol Scand Suppl 150: 1-32
30. Kallunki T, Su B, Tsigelny I, Sluss HK, Derijard B, Moore G, Davis R, Karin M (1994) JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev 8: 2996-3007
31. Keane RW, Srinivasan A, Foster LM, Testa MP, Ord R, Nonner D, Wang HG, Reed JC, Bredesen DE, Kayalar C (1997) Activation of CPP32 during apoptosis of neurons and astrocytes. J Neurosci Res 48: 168-180
32. Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257
33. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239: 57-69
34. Kirino T, Sano K (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol 62: 201-208
35. Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong C, Bao J, Banasiak KJ, Haddad GG, Flavell RA, Davis RJ, Rakic P (2003) A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci U S A 100: 15184-15189
36. Leist M, Jäättelä M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2: 589-598
37. Li H, Colbourne F, Sun P, Zhao Z, Buchan AM, ladecola C (2000) Caspase inhibitors reduce neuronal injury after focal but not global ischemia in rats. Stroke 31: 176-182
38. Lindner LE (1993) Improvements in the silver-staining technique for nucleolar organizer regions (AgNOR). J Histochem Cytochem 41: 439-445
39. Lockshin RA, Zakeri Z (2001) Programmed cell death and apoptosis: origins of the theory. Nat Rev Mol Cell Biol 2: 545-550
40. Martelli AM, Robuffo I, Bortul R, Ochs RL, Luchetti F, Cocco L, Zweyer M, Bareggi R, Falcieri E (2000) Behavior of nucleolar proteins during the course of apoptosis in camptothecin-treated HL60 cells. J Cell Biochem 78: 264-277
41. Mathiasen IS, Jäättelä M (2002) Triggering caspase-independent cell death to combat cancer. Trends Mol Med 8: 212-220
42. Matsuoka Y, Okazaki M, Zhao H, Asai S, Ishikawa K, Kitamura Y (1999) Phosphorylation of c-Jun and its localization with heme oxygenase-1 and cyclooxygenase-2 in CA1 pyramidal neurons after transient forebrain ischemia. J Cereb Blood Flow Metab 19: 1247-1255
43. Minden A, Lin A, Smeal T, Derijard B, Cobb M, Davis R, Karin M. (1994) c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol Cell Biol 14: 6683-6688
44. Ni B, Wu X, Su Y, Stephenson D, Smalstig EB, Clemens J, Paul SM (1998) Transient global forebrain ischemia induces a prolonged expression of the caspase-3 mRNA in rat hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 18: 248-256
45. 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
46. Petito CK, Feldmann E, Pulsinelli WA, Plum F (1987) Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37: 1281-1286
47. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11: 491-499
48. Rami A, Agarwal R, Botez G, Winckler J (2000) mu-Calpain activation, DNA fragmentation, and synergistic effects of caspase and calpain inhibitors in protecting hippocampal neurons from ischemic damage. Brain Res 866: 299-312
49. Schotte P, Declercq W, Van Huffel S, Vandenabeele P, Beyaert R (1999) Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett 442: 117-121
50. Smith M-L, Bendek G, Dahlgren N, Rosen I, Wieloch T, Siesjö BK (1984) Models for studying long-term recovery following forebrain ischemia in the rat. A 2-vessel occlusion model. Acta Neurol Scand 69: 385-401
51. Srinivasan A, Roth KA, Sayers RO, Shindler KS, Wong AM, Fritz LC, Tomaselli K (1998) In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ 5: 1004-1016
52. Stadelmann C, Mews I, Srinivasan A, Deckwerth TL, Lassmann H, Brück W (2001) Expression of cell death-associated proteins in neuronal apoptosis associated with pontosubicular neuron necrosis. Brain Pathol 11: 273-281
53. Stadelmann C, Brück W, Bancher C, Jellinger K, Lassmann H (1998) Alzheimer disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis. J Neuropathol Exp Neurol 5: 456-464
54. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Brück W, Jellinger K, Lassmann H (1999) Activation of caspase-3 in single neurons and authophagic granules of granulovacuoler degeneration in Alzheimer's disease. Am J Pathol 155: 1459-1466
55. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, De Vos K, Totty N, Sterling A, Fiers W, Vandenabeele P, Grooten J (1998) Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett 438: 150-158
56. Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68: 251-306
57. Yamashima T (2000) Implications of cysteine proteases calpain, cathepsin and scaspse in ischemic neuronal death of primates. Progress Neurobiol 62: 273-295
58. Yuan J, Yankner BY (2000) Apoptosis in the nervous system. Nature 407: 802-809
59. Zeng Y-S, Xu Z-C (2000) Co-ecistence of necrosis and apoptosis in rat hippocampus following transient forebrain ischemia. Neurosci Res 37: 113-125
60. Zhan R-Z, Wu C, Fujihara H, Taga K, Qi S, Naito M, Shimoji K (2001) Both caspase dependent and caspase-independent pathways may be involved in hippocampal CA1 neuronal death because of loss of cytochrome c from mitochondria in a rat forebrain ischemia model. J Cereb Blood Flow Metabol 21: 529-540