Differential insult-dependent recruitment of the intrinsic mitochondrial pathway during neuronal programmed cell death

Cellular and Molecular Life Sciences

Volumn 66, Issue 1, 2009, Pages 156-172

  Diwakarla, S ^a   Nagley, P ^b   Hughes, M L R ^b,c   Chen, B ^a   Beart, P M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

AIF; Bax; Cell death; Cytochrome c; Excitotoxicity; Mitochondrial membrane potential; Neurons; Proteases

Indexed keywords

APOPTOSIS INDUCING FACTOR; CALCIUM; CALPAIN; CASPASE; CASPASE 3; CYTOCHROME C; DIMETHADIONE; MEMBRANE PROTEIN; PROTEINASE; SERINE PROTEINASE OMI;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CALCIUM CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITOTOXICITY; GRANULE CELL; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PROTEIN LOCALIZATION;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; CALCIUM; CALPAIN; CASPASE 3; CELLS, CULTURED; ENZYME ACTIVATION; HYDROGEN PEROXIDE; KAINIC ACID; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; STAUROSPORINE;

EID: 58149505960     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8490-7     Document Type: Article

References (54)

1. Tatton, W. G. and Olanow, C. W. (1999) Apoptosis in neurodegenerative diseases: the role of mitochondria. Biochim. Biophys. Acta. 1410, 195-213.
2. Beal, M. F. (2005) Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 58, 495-505.
3. Green, D. and Kroemer, G. (1998) The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 8, 267-271.
4. Lim, M. L., Mercer, L. D., Nagley, P. and Beart, P. M. (2007) Rotenone and MPP+ preferentially redistribute apoptosis-inducing factor in apoptotic dopamine neurons. Neuroreport. 18, 307-312.
5. Polster, B. M. and Fiskum, G. (2004) Mitochondrial mechanisms of neural cell apoptosis. J. Neurochem. 90, 1281-1289.
6. Kroemer, G., Galluzzi, L. and Brenner, C. (2007) Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163.
7. Lim, M. L., Lum, M. G., Hansen, T. M., Roucou, X. and Nagley, P. (2002) On the release of cytochrome c from mitochondria during cell death signaling. J. Biomed. Sci. 9, 488-506.
8. Ankarcrona, M., Dypbukt, J. M., Bonfoco, E., Zhivotovsky, B., Orrenius, S., Lipton, S. A. and Nicotera, P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15, 961-973.
9. Luetjens, C. M., Bui, N. T., Sengpiel, B., Munstermann, G., Poppe, M., Krohn, A. J., Bauerbach, E., Krieglstein, J. and Prehn, J. H. (2000) Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 20, 5715-5723.
10. Smith, D. J., Ng, H., Kluck, R. M. and Nagley, P. (2008) The mitochondrial gateway to cell death. IUBMB Life. 60, 383-389.
11. Hardwick, J. M. and Polster, B. M. (2002) Bax, along with lipid conspirators, allows cytochrome c to escape mitochondria. Mol. Cell. 10, 963-965.
12. Gill, M. B. and Perez-Polo, J. R. (2008) Hypoxia ischemia-mediated cell death in neonatal rat brain. Neurochem. Res.
13. Zhang, Z., Yang, X., Zhang, S., Ma, X. and Kong, J. (2007) BNIP3 upregulation and EndoG translocation in delayed neuronal death in stroke and in hypoxia. Stroke. 38, 1606-1613.
14. Cande, C., Vahsen, N., Garrido, C. and Kroemer, G. (2004) Apoptosis-inducing factor (AIF): caspase-independent after all. Cell Death Differ. 11, 591-595.
15. Blomgren, K., Leist, M. and Groc, L. (2007) Pathological apoptosis in the developing brain. Apoptosis. 12, 993-1010.
16. Orrenius, S., Zhivotovsky, B. and Nicotera, P. (2003) Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4, 552-565.
17. Polster, B. M., Basanez, G., Etxebarria, A., Hardwick, J. M. and Nicholls, D. G. (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem. 280, 6447-6454.
18. Yu, S. W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M. and Dawson, V. L. (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 297, 259-263.
19. Yu, S. W., Wang, H., Dawson, T. M. and Dawson, V. L. (2003) Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol. Dis. 14, 303-317.
20. Degterev, A. and Yuan, J. (2008) Expansion and evolution of cell death programmes. Nat. Rev. Mol. Cell Biol. 9, 378-390.
21. Clarke, P. G. (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl). 181, 195-213.
22. Giardina, S. F., Cheung, N. S., Reid, M. T. and Beart, P. M. (1998) Kainate-induced apoptosis in cultured murine cerebellar granule cells elevates expression of the cell cycle gene cyclin D1. J. Neurochem. 71, 1325-1328.
23. D'Mello, S. R., Galli, C., Ciotti, T. and Calissano, P. (1993) 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, 10989-10993.
24. Beart, P. M., Lim, M. L., Chen, B., Diwakarla, S., Mercer, L. D., Cheung, N. S. and Nagley, P. (2007) Hierarchical recruitment by AMPA but not staurosporine of pro-apoptotic mitochondrial signaling in cultured cortical neurons: evidence for caspase-dependent/ independent cross-talk. J. Neurochem. 103, 2408-2427.
25. Lim, M. L., Chen, B., Beart, P. M. and Nagley, P. (2006) Relative timing of redistribution of cytochrome c and Smac/ DIABLO from mitochondria during apoptosis assessed by double immunocytochemistry on mammalian cells. Exp. Cell Res. 312, 1174-1184.
26. Cheung, N. S., Pascoe, C. J., Giardina, S. F., John, C. A. and Beart, P. M. (1998) Micromolar L-glutamate induces extensive apoptosis in an apoptotic-necrotic continuum of insult-dependent, excitotoxic injury in cultured cortical neurones. Neuropharmacology. 37, 1419-1429.
27. Rego, A. C., Ward, M. W. and Nicholls, D. G. (2001) Mitochondria control ampa/kainate receptor-induced cytoplasmic calcium deregulation in rat cerebellar granule cells. J. Neurosci. 21, 1893-1901.
28. Giardina, S. F. and Beart, P. M. (2001) Excitotoxic profiles of novel, low-affinity kainate receptor agonists in primary cultures of murine cerebellar granule cells. Neuropharmacology. 41, 421-432.
29. Assefa, Z., Bultynck, G., Szlufcik, K., Nadif Kasri, N., Vermassen, E., Goris, J., Missiaen, L., Callewaert, G., Parys, J. B. and De Smedt, H. (2004) Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J. Biol. Chem. 279, 43227-43236.
30. Wu, H. Y., Tomizawa, K., Oda, Y., Wei, F. Y., Lu, Y. F., Matsushita, M., Li, S. T., Moriwaki, A. and Matsui, H. (2004) Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J. Biol. Chem. 279, 4929-4940.
31. Nath, R., Raser, K. J., Stafford, D., Hajimohammadreza, I., Posner, A., Allen, H., Talanian, R. V., Yuen, P., Gilbertsen, R. B. and Wang, K. K. (1996) Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem. J. 319 (Pt 3), 683-690.
32. Atlante, A., Calissano, P., Bobba, A., Giannattasio, S., Marra, E. and Passarella, S. (2001) Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett. 497, 1-5.
33. Arnoult, D., Parone, P., Martinou, J. C., Antonsson, B., Estaquier, J. and Ameisen, J. C. (2002) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J. Cell Biol. 159, 923-929.
34. Du, C., Fang, M., Li, Y., Li, L. and Wang, X. (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102, 33-42.
35. Verhagen, A. M., Ekert, P. G., Pakusch, M., Silke, J., Connolly, L. M., Reid, G. E., Moritz, R. L., Simpson, R. J. and Vaux, D. L. (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102, 43-53.
36. Cadet, J. L., Jayanthi, S. and Deng, X. (2003) Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. Faseb J. 17, 1775-1788.
37. Volbracht, C., Chua, B. T., Ng, C. P., Bahr, B. A., Hong, W. and Li, P. (2005) The critical role of calpain versus caspase activation in excitotoxic injury induced by nitric oxide. J. Neurochem. 93, 1280-1292.
38. Daugas, E., Susin, S. A., Zamzami, N., Ferri, K. F., Irinopoulou, T., Larochette, N., Prevost, M. C., Leber, B., Andrews, D., Penninger, J. and Kroemer, G. (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. Faseb J. 14, 729-739.
39. Wang, H., Yu, S. W., Koh, D. W., Lew, J., Coombs, C., Bowers, W., Federoff, H. J., Poirier, G. G., Dawson, T. M. and Dawson, V. L. (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J. Neurosci. 24, 10963-10973.
40. Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M. and Kroemer, G. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397, 441-446.
41. Yuan, J., Lipinski, M. and Degterev, A. (2003) Diversity in the mechanisms of neuronal cell death. Neuron. 40, 401-413.
42. Leist, M. and Jaattela, M. (2001) Triggering of apoptosis by cathepsins. Cell Death Differ. 8, 324-326.
43. Deshmukh, M., Kuida, K. and Johnson, E. M., Jr. (2000) Caspase inhibition extends the commitment to neuronal death beyond cytochrome c release to the point of mitochondrial depolarization. J. Cell Biol. 150, 131-143.
44. Zhou, L. L., Zhou, L. Y., Luo, K. Q. and Chang, D. C. (2005) Smac/DIABLO and cytochrome c are released from mitochondria through a similar mechanism during UV-induced apoptosis. Apoptosis. 10, 289-299.
45. Miller, T. M., Moulder, K. L., Knudson, C. M., Creedon, D. J., Deshmukh, M., Korsmeyer, S. J. and Johnson, E. M., Jr. (1997) Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139, 205-217.
46. Cheung, E. C., Melanson-Drapeau, L., Cregan, S. P., Vanderluit, J. L., Ferguson, K. L., McIntosh, W. C., Park, D. S., Bennett, S. A. and Slack, R. S. (2005) Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J. Neurosci. 25, 1324-1334.
47. Brustovetsky, N., Dubinsky, J. M., Antonsson, B. and Jemmerson, R. (2003) Two pathways for tBID-induced cytochrome c release from rat brain mitochondria: BAK- versus BAX-dependence. J. Neurochem. 84, 196-207.
48. Budd, S. L. and Nicholls, D. G. (1996) Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67, 2282-2291.
49. Goll, D. E., Thompson, V. F., Li, H., Wei, W. and Cong, J. (2003) The calpain system. Physiol. Rev. 83, 731-801.
50. Takano, J., Tomioka, M., Tsubuki, S., Higuchi, M., Iwata, N., Itohara, S., Maki, M. and Saido, T. C. (2005) Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J. Biol. Chem. 280, 16175-16184.
51. Du, Y., Bales, K. R., Dodel, R. C., Hamilton-Byrd, E., Horn, J. W., Czilli, D. L., Simmons, L. K., Ni, B. and Paul, S. M. (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc. Natl. Acad. Sci. USA. 94, 11657-11662.
52. Bizat, N., Hermel, J. M., Humbert, S., Jacquard, C., Creminon, C., Escartin, C., Saudou, F., Krajewski, S., Hantraye, P. and Brouillet, E. (2003) In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3. J. Biol. Chem. 278, 43245-43253.
53. Cheung, N. S., Peng, Z. F., Chen, M. J., Moore, P. K. and Whiteman, M. (2007) Hydrogen sulfide induced neuronal death occurs via glutamate receptor and is associated with calpain activation and lysosomal rupture in mouse primary cortical neurons. Neuropharmacology. 53, 505-514.
54. Susin, S. A., Daugas, E., Ravagnan, L., Samejima, K., Zamzami, N., Loeffler, M., Costantini, P., Ferri, K. F., Irinopoulou, T., Prevost, M. C., Brothers, G., Mak, T. W., Penninger, J., Earnshaw, W. C. and Kroemer, G. (2000) Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192, 571-580.