Caspase-mediated death of newly formed neurons in the adult rat dentate gyrus following status epilepticus

European Journal of Neuroscience

Volumn 16, Issue 8, 2002, Pages 1463-1471

  Ekdahl, Christine T ^a   Mohapel, Paul ^a   Weber, Ekkehard ^b   Bahr, Ben ^c   Blomgren, Klas ^d,e   Lindvall, Olle ^a  

^a LUND UNIVERSITY   (Sweden)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

Author keywords

Apoptosis; Epilepsy; Neurogenesis; PARP; Proliferation

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; BROXURIDINE; CALPAIN; CASPASE; CASPASE INHIBITOR; CATHEPSIN; CATHEPSIN B; CYSTEINE PROTEINASE; MARKER; NEURON SPECIFIC NUCLEAR PROTEIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL DEGENERATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

EID: 0036428732     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02202.x     Document Type: Article

References (61)

1. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nature Med., 8, 963-970.
2. Arvidsson, A., Kokaia, Z. & Lindvall, O. (2001) N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur. J. Neurosci., 14, 10-18.
3. Au-Yeung, K.K., Zhu, D.Y.O., K. & Siow, Y.L. (2001) Inhibition of stress-activated protein kinase in the ischemic/reperfused heart: Role of magnesium tanshinoate B in preventing apoptosis. Biochem. Pharmacol., 62, 483-493.
4. Bahr, B.A., Bendiske, J., Brown, Q.B., Munirathinam, S., Caba, E., Rudin, M., Urwyler, S., Sauter, A. & Rogers, G. (2002) Survival signaling and selective neuroprotection through glutamatergic transmission. Exp. Neurol., 174, 37-47.
5. Bahr, B.A., Tiriveedhi, S., Park, G.Y. & Lynch, G. (1995) Induction of calpain-mediated spectrin fragments by pathogenic treatments in long-term hippocampal slices. J. Pharmacol. Exp. Ther., 273, 902-908.
6. Becker, A.J., Gillardon, F., Blumcke, I., Langendorfer, D., Beck, H. & Wiestler, O.D. (1999) Differential regulation of apoptosis-related genes in resistant and vulnerable subfields of the rat epileptic hippocampus. Brain Res. Mol. Brain Res., 67, 172-176.
7. Bednarski, E., Vanderklish, P., Gall, C., Saido, T.C., Bahr, B.A. & Lynch, G. (1995) Translational suppression of calpain I reduces NMDA-induced spectrin proteolysis and pathophysiology in cultured hippocampal slices. Brain Res., 694, 147-157.
8. Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M. & Lindvall, O. (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. USA, 94, 10432- 10437.
9. Bi, X., Chang, V., Siman, R., Tocco, G. & Baudry, M. (1996) Regional distribution and time-course of calpain activation following kainate-induced seizure activity in adult rat brain. Brain Res., 726, 98-108.
10. Blomgren, K., Zhu, C., Wang, X., Karlsson, J.O., Leverin, A.L., Bahr, B.A., Mallard, C. & Hagberg, H. (2001) Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia- ischemia: A mechanism of 'pathological apoptosis'? J. Biol. Chem., 276, 10191-10198.
11. Buki, A., Okonkwo, D.O., Wang, K.K. & Povlishock, J.T. (2000) Cytochrome c release and caspase activation in traumatic axonal injury. J. Neurosci., 20, 2825-2834.
12. Cameron, H.A. & McKay, R.D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol., 435, 406-417.
13. Cameron, H.A., Woolley, C.S., McEwen, B.S. & Gould, E. (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience, 56, 337-344.
14. Chan, S.L. & Mattson, M.P. (1999) Caspase and calpain substrates: Roles in synaptic plasticity and cell death. J. Neurosci. Res., 58, 167-190.
15. Cheng, A., Chan, S.L., Milhavet, O., Wang, S. & Mattson, M.P. (2001) p38 MAP Kinase mediates nitric oxide-induced apoptosis of neural progenitor cells. J. Biol. Chem., 276, 43320-43327.
16. Chua, B.T., Guo, K. & Li, P. (2000) Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. J. Biol. Chem., 275, 5131-5135.
17. Coggeshall, R.E. & Lekan, H.A. (1996) Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J. Comp. Neurol., 364, 6-15. [Erratum appears in J. Comp. Neurol., 369, 162].
18. Cohen, G.M. (1997) Caspases: The executioners of apoptosis. Biochem. J., 326, 1-16.
19. Covolan, L., Ribeiro, L.T., Longo, B.M. & Mello, L.E. (2000a) Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus. Hippocampus, 10, 169- 180.
20. Covolan, L., Smith, R.L. & Mello, L.E.A.M. (2000b) Ultrastructural identification of dentate granule cell death from pilocarpine-induced seizures. Epilepsy Res., 41, 9-21.
21. D'Sa-Eipper, C. & Roth, K.A. (2000) Caspase regulation of neuronal progenitor cell apoptosis. Dev. Neurosci., 22, 116-124.
22. Dolbeare, F. (1995) Bromodeoxyuridine: A diagnostic tool in biology and medicine, Part I: Historical perspectives, histochemical methods and cell kinetics. Histochem. J., 27, 339-369.
23. Duman, R.S., Malberg, J. & Nakagawa, S. (2001) Regulation of adult neurogenesis by psychotropic drugs and stress. J. Pharmacol. Exp. Ther., 299, 401-407.
24. Ekdahl, C.T., Mohapel, P., ElmÈr, E. & Lindvall, O. (2001) Caspase inhibitors increase short-term survival of progenitor cell progeny in the adult rat dentate gyrus following status epilepticus. Eur. J. Neurosci., 14, 937-945.
25. Erhardt, J.A., Ohlstein, E.H., Toomey, J.R., Gabriel, M.A., Willette, R.N., Yue, T.L., Barone, F.C. & Parsons, A.A. (2001) Activation of caspase-3/caspase-3-like activity in rat cardiomyocytes by an RGD peptide, but not the GPIIb/IIIa antagonist lotrafiban. Thromb. Res., 103, 143-148.
26. Faherty, C.J., Xanthoudakis, S. & Smeyne, R.J. (1999) Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res. Mol. Brain Res., 70, 159-163.
27. Fiebiger, E., Meraner, P., Weber, E., Fang, I.F., Stingl, G., Ploegh, H. & Maurer, D. (2001) Cytokines regulate proteolysis in major histocompatibility complex class II-dependent antigen presentation by dendritic cells. J. Exp. Med., 193, 881-892.
28. Foghsgaard, L., Wissing, D., Mauch, D., Lademann, U., Bastholm, L., Boes, M., Elling, F., Leist, M. & Jaattela, 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.
29. Gage, F.H., Kempermann, G., Palmer, T.D., Peterson, D.A. & Ray, J. (1998) Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol., 36, 249-266.
30. Gao, G. & Dou, Q.P. (2000) N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J. Cell. Biochem., 80, 53-72.
31. Gillardon, F., Bottiger, B., Schmitz, B., Zimmermann, M. & Hossmann, K.A. (1997) Activation of CPP-32 protease in hippocampal neurons following ischemia and epilepsy. Brain Res. Mol. Brain Res., 50, 16-22.
32. Gray, J., Haran, M.M., Schneider, K., Vesce, S., Ray, A.M., Owen, D., White, I.R., Cutler, P. & Davis, J.B. (2001) Evidence that inhibition of cathepsin-B contributes to the neuroprotective properties of caspase inhibitor Ac-YVAD-cmk. J. Biol. Chem., 26, 26.
33. Gray, W.P. & Sundstrom, L.E. (1998) Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res., 790, 52-59.
34. Han, H., Wang, H., Long, H., Nattel, S. & Wang, Z. (2001) Oxidative preconditioning and apoptosis in L-cells. Roles of protein kinase B and mitogen-activated protein kinases. J. Biol. Chem., 276, 26357-26364.
35. Henshall, D.C., Chen, J. & Simon, R.P. (2000) Involvement of caspase-3-like protease in the mechanism of cell death following focally evoked limbic seizures. J. Neurochem., 74, 1215-1223.
36. Herceg, Z. & Wang, Z.Q. (2001) Functions of poly (ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res., 477, 97-110.
37. Hetman, M., Filipkowski, R.K., Domagala, W. & Kaczmarek, L. (1995) Elevated cathepsin D expression in kainate-evoked rat brain neurodegeneration. Exp. Neurol., 136, 53-63.
38. Ishisaka, R., Utsumi, T., Yabuki, M., Kanno, T., Furuno, T., Inoue, M. & Utsumi, K. (1998) Activation of caspase-3-like protease by digitonin-treated lysosomes. FEBS Lett., 435, 233-236.
39. Johnson, D.E. (2000) Noncaspase proteases in apoptosis. Leukemia, 14, 1695-1703.
40. Kidd, V.J., Lahti, J.M. & Teitz, T. (2000) Proteolytic regulation of apoptosis. Semin. Cell Dev. Biol., 11, 191-201.
41. Kirschke, H., Clausen, T., Gohring, B., Gunther, D., Heucke, E., Laube, F., Lowe, E., Neef, H., Papesch, H., Peinze, S., Plehn, G., Rebmann, U., Rinne, A., Rudrich, R. & Weber, E. (1997) Concentrations of lysosomal cysteine proteases are decreased in renal cell carcinoma compared with normal kidney. J. Cancer Res. Clin. Oncol., 123, 402-406.
42. Kondratyev, A. & Gale, K. (2000) Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res. Mol. Brain Res., 75, 216-224.
43. Liu, J., Solway, K., Messing, R.O. & Sharp, F.R. (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci., 18, 7768-7778.
44. Lothman, E.W., Bertram, E.H., Bekenstein, J.W. & Perlin, J.B. (1989) Self-sustaining limbic status epilepticus induced by 'continuous' hippocampal stimulation: Electrographic and behavioral characteristics. Epilepsy Res., 3, 107-119.
45. McGinnis, K.M., Gnegy, M.E., Park, Y.H., Mukerjee, N. & Wang, K.K. (1999) Procaspase-3 and poly (ADP) ribose polymerase (PARP) are calpain substrates. Biochem. Biophys. Res. Commun., 263, 94-99.
46. Nakagawa, E., Aimi, Y., Yasuhara, O., Tooyama, I., Shimada, M., McGeer, P.L. & Kimura, H. (2000) Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia, 41, 10-18.
47. Nakagawa, T. & Yuan, J. (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol., 150, 887-894.
48. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. & Lowenstein, D.H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci., 17, 3727-3738.
49. Paxinos, G. & Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates. Academic Press, Inc., San Diego.
50. Racine, R.J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32, 281-294.
51. Scharff, C. (2000) Chasing fate and function of new neurons in adult brains. Curr. Opin. Neurobiol., 10, 774-783.
52. Sloviter, R.S., Dean, E., Sollas, A.L. & Goodman, J.H. (1996) Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J. Comp. Neurol., 366, 516-533.
53. Soldani, C., Bottone, M.G., Pellicciari, C. & Scovassi, A.I. (2001) Two-color fluorescence detection of poly (ADP-ribose) polymerase-1 (PARP-1) cleavage and DNA strand breaks in etoposide-induced apoptotic cells. Eur. J. Histochem., 45, 389-392.
54. Stoka, V., Turk, B., Schendel, S.L., Kim, T.H., Cirman, T., Snipas, S.J., Ellerby, L.M., Bredesen, D., Freeze, H., Abrahamson, M., Bromme, D., Krajewski, S., Reed, J.C., Yin, X.M., Turk, V. & Salvesen, G.S. (2001) Lysosomal protease pathways to apoptosis. Cleavage of bid, not procaspases, is the most likely route. J. Biol. Chem., 276, 3149-3157.
55. Tominaga, K., Nakanishi, H., Yasuda, Y. & Yamamoto, K. (1998) Excitotoxin-induced neuronal death is associated with response of a unique intracellular aspartic proteinase, cathepsin. Eur. J. Neurochem., 71, 2574-2584.
56. 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.
57. Wang, K.K. (2000) Calpain and caspase: Can you tell the difference? Trends Neurosci., 23, 20-26.
58. Wang, K.K., Posmantur, R., Nadimpalli, R., Nath, R., Mohan, P., Nixon, R.A., Talanian, R.V., Keegan, M., Herzog, L. & Allen, H. (1998) Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch. Biochem. Biophys., 356, 187-196.
59. Wolf, B.B., Goldstein, J.C., Stennicke, H.R., Beere, H., Amarante-Mendes, G.P., Salvesen, G.S. & Green, D.R. (1999) Calpain functions in a caspase-independent manner to promote apoptosis- like events during platelet activation. Blood, 94, 1683-1692.
60. Yamashima, T. (2000) Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol., 62, 273-295.
61. Yan, X.X., Najbauer, J., Woo, C.C., Dashtipour, K., Ribak, C.E. & Leon, M. (2001) Expression of active caspase-3 in mitotic and postmitotic cells of the rat forebrain. J. Comp. Neurol., 433, 4-22.