Mechanisms of Caspase-Independent Neuronal Death: Energy Depletion and Free Radical Generation

Journal of Neuroscience

Volumn 23, Issue 35, 2003, Pages 11015-11025

  Lang Rollin, Isabelle C J ^a   Rideout, Hardy J ^a   Noticewala, Manish ^a   Stefanis, Leonidas ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

AIF; ATP; Autophagy; Caspase inhibition; Cytochrome c; Mitochondria; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; BENZYLOXYCARBONYLASPARTYL FLUOROMETHYL KETONE; CAMPTOTHECIN; CASPASE; CYTOCHROME C; DNA TOPOISOMERASE INHIBITOR; FREE RADICAL; GLUCOSE; KETONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; TEMPOL; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN CELL; CELL ENERGY; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NERVE CELL CULTURE; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TARGETING; RAT;

EID: 0348010284     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-35-11015.2003     Document Type: Article

References (62)

1. Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC (2002) Mitochondrial release of apoptosis-inducing factor occurs down-stream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923-929.
2. Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ (2003) Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 22:4385-4399.
3. Bonini MG, Mason RP, Augusto O (2002) The mechanism by which 4-hydroxy-2, 2, 6, 6-tetramethylpiperidene-1-oxyl (tempol) diverts peroxynitrite decomposition from nitrating to nitrosating species. Chem Res Toxicol 15:506-511.
4. Bossy-Wetzel E, Newmeyer DD, Green DR (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17:37-49.
5. Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85:7972-7976.
6. Cai J, Jones DP (1998) Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401-11404.
7. 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.
8. Chang LK, Johnson Jr EM (2002) Cyclosporin A inhibits caspase-independent death of NGF-deprived sympathetic neurons: a potential role for mitochondrial permeability transition. J Cell Biol 157:771-778.
9. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195-213.
10. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, Yu SW, Dawson TM, Dawson VL, Park DS, Kroemer G, Slack RS (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 158:507-517.
11. Cutillas B, Espejo M, Gil J, Ferrer I, Ambrosio S (1999) Caspase inhibition protects nigral neurons against 6-OHDA-induced retrograde degeneration. NeuroReport 10:2605-2608.
12. Cuzzocrea S, McDonald MC, Mazzon E, Siriwardena D, Costantino G, Fulia F, Cucinotta G, Gitto E, Cordaro S, Barberi I, De Sarro A, Caputi AP, Thiemermann C (2000) Effects of tempol, a membrane-permeable radical scavenger in a gerbil model of brain injury. Brain Res 875:96-106.
13. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N, Prevost MC, Leber B, Andrews D, Penninger J, Kroemer G (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 14:729-739.
14. Dussmann H, Rehm M, Kogel D, Prehn JH (2003) Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J Cell Sci 116:525-536.
15. Dyckens J (1997) Mitochondrial free radical production and oxidative pathophysiology: implication for neurodegenerative disease. In: Mitochondria and free radicals in neurodegenerative diseases (Beal MF, Howell N, Bodis-Wollner I, eds), pp 29-55. New York: Wiley-Liss.
16. Elmore SP, Qian T, Grissom SF, Lemasters JJ (2001) The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15:2286-2287.
17. Fleury C, Mignotte B, Vayssiere JL (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131-141.
18. Friedman WJ, Ibanez CF, Hallbook F, Persson H, Cain LD, Dreyfus CF, Black IB (1993) Differential actions of neurotrophins in the locus coeruleus and basal forebrain. Exp Neurol 119:72-78.
19. Green D, Kroemer G (1998) The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol 8:267-271.
20. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309-1312.
21. Hsu LJ, Sagara Y, Arroyo A, Rockenstein E, Sisk A, Mallory M, Wong J, Takenouchi T, Hashimoto M, Masliah E (2000) alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am J Pathol 157:401-410.
22. Keramaris E, Stefanis L, MacLaurin J, Harada N, Takaku K, Ishikawa T, Taketo MM, Robertson GS, Nicholson DW, Slack RS, Park DS (2000) Involvement of caspase 3 in apoptotic death of cortical neurons evoked by DNA damage. Mol Cell Neurosci 15:368-379.
23. Khaspekov L, Friberg H, Halestrap A, Viktorov I, Wieloch T (1999) Cyclosporin A and its nonimmunosuppressive analogue N-Me-Val-4-cyclosporin A mitigate glucose/oxygen deprivation-induced damage to rat cultured hippocampal neurons. Eur J Neurosci 11:3194-3198.
24. Knoblach SM, Nikolaeva M, Huang X, Fan L, Krajewski S, Reed JC, Faden AI (2002) Multiple caspases are activated after traumatic brain injury: evidence for involvement in functional outcome. J Neurotrauma 19:1155-1170.
25. Krohn AJ, Preis E, Prehn JH (1998) Staurosporine-induced apoptosis of cultured rat hippocampal neurons involves caspase-1-like proteases as upstream initiators and increased production of superoxide as a main downstream effector. J Neurosci 18:8186-8197.
26. Larsen KE, Sulzer D (2002) Autophagy in neurons: a review. Histol Histopathol 17:897-908.
27. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, Crowe RA, Cascio WE, Bradham CA, Brenner DA, Herman B (1998) The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta 1366:177-196.
28. Li M, Ona VO, Chen M, Kaul M, Tenneti L, Zhang X, Stieg PE, Lipton SA, Friedlander RM (2000) Functional role and therapeutic implications of neuronal caspase-1 and -3 in a mouse model of traumatic spinal cord injury. Neuroscience 99:333-342.
29. Metivier D, Dallaporta B, Zamzami N, Larochette N, Susin SA, Marzo I, Kroemer G (1998) Cytofluorometric detection of mitochondrial alterations in early CD95/Fas/APO-1-triggered apoptosis of Jurkat T lymphoma cells. Comparison of seven mitochondrion-specific fluorochromes. Immunol Lett 61:157-163.
30. Mootha VK, Wei MC, Buttle KF, Scorrano L, Panoutsakopoulou V, Mannella CA, Korsmeyer SJ (2001) A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J 20:661-671.
31. Morris EJ, Geller HM (1996) Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity. J Cell Biol 134:757-770.
32. Morris EJ, Keramaris E, Rideout HJ, Slack RS, Dyson NJ, Stefanis L, Park DS (2001) Cyclin-dependent kinases and P53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J Neurosci 21:5017-5026.
33. Mortimore GE, Poso AR (1986) The lysosomal pathway of intracellular proteolysis in liver: regulation by amino acids. Adv Enzyme Regul 25:257-276.
34. Pampfer S, Cordi S, Vanderheyden I, Van Der Smissen P, Courtoy PJ, Van Cauwenberge A, Alexandre H, Donnay I, De Hertogh R (2001) Expression and role of Bcl-2 in rat blastocysts exposed to high D-glucose. Diabetes 50:143-149.
35. Park DS, Morris EJ, Padmanabhan J, Shelanski ML, Geller HM, Greene LA (1998) Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents. J Cell Biol 143:457-467.
36. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P (2000) Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275:992-998.
37. Radi R, Cassina A, Hodara R, Quijano C, Castro L (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33:1451-1464.
38. Ricci JE, Gottlieb RA, Green DR (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160:65-75.
39. Rideout HJ, Stefanis L (2001) Caspase inhibition: a potential therapeutic strategy in neurological diseases. Histol Histopathol 16:895-908.
40. Rideout HJ, Stefanis L (2002) Proteasomal inhibition-induced inclusion formation and death in cortical neurons require transcription and ubiquitination. Mol Cell Neurosci 21:223-238.
41. Rideout HJ, Zang E, Yeasmin M, Gordon R, Jabado O, Park DS, Stefanis L (2001) Inhibitors of trypsin-like serine proteases prevent DNA damage-induced neuronal death by acting upstream of the mitochondrial checkpoint and of p53 induction. Neuroscience 107:339-352.
42. Rukenstein A, Rydel RE, Greene LA (1991) Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms. J Neurosci 11:2552-2563.
43. Saeki K, Yuo A, Okuma E, Yazaki Y, Susin SA, Kroemer G, Takaku F (2000) Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ 7:1263-1269.
44. Sakuma H, Yamamoto M, Okumura M, Kojima T, Maruyama T, Yasuda (2002) High glucose inhibits apoptosis in human coronary artery smooth muscle cells by increasing bcl-xL and bfl-1/A1. Am J Physiol Cell Physiol 283:C422-C428.
45. Schaffer SW, Croft CB, Solodushko V (2000) Cardioprotective effect of chronic hyperglycemia: effect on hypoxia-induced apoptosis and necrosis. Am J Physiol Heart Circ Physiol 278:H1948-H1954.
46. Schulz JB, Weller M, Moskowitz MA (1999) Caspases as treatment targets in stroke and neurodegenerative diseases. Ann Neurol 45:421-429.
47. Seglen PO, Gordon PB (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 79:1889-1892.
48. Selznick LA, Zheng TS, Flavell RA, Rakic P, Roth KA (2000) Amyloid beta-induced neuronal death is bax-dependent but caspase-independent. J Neuropathol Exp Neurol 59:271-279.
49. Stefanis L, Troy CM, Qi H, Greene LA (1997) Inhibitors of trypsin-like serine proteases inhibit processing of the caspase Nedd-2 and protect PC12 cells and sympathetic neurons from death evoked by withdrawal of trophic support. J Neurochem 69:1425-1437.
50. Stefanis L, Park DS, Friedman WJ, Greene LA (1999) Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J Neurosci 19:6235-6247.
51. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA (2001) Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci 21:9549-9560.
52. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
53. Tennyson VM, Gershon MD, Sherman DL, Behringer RR, Raz R, Crotty DA, Wolgemuth DJ (1993) Structural abnormalities associated with congenital megacolon in transgenic mice that overexpress the Hoxa-4 gene. Dev Dyn 98:128-153.
54. Thiemermann C, McDonald MC, Cuzzocrea S (2001) The stable nitroxide, Tempol, attenuates the effects of peroxynitrite and oxygen-derived free radicals. Crit Care Med 29:223-224.
55. Troy CM, Rabacchi SA, Hohl JB, Angelastro JM, Greene LA, Shelanski ML (2001) Death in the balance: alternative participation of the caspase-2 and -9 pathways in neuronal death induced by nerve growth factor deprivation. J Neurosci 21:5007-5016.
56. van Deurs B, Holm PK, Sandvig K (1996) Inhibition of the vacuolar H(+)-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur J Cell Biol 69:343-350.
57. Wang X, Yang C, Chai J, Shi Y, Xue D (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298:1587-1592.
58. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS (1998) Bax involvement in p53-mediated neuronal cell death. J Neurosci 18:1363-1373.
59. Xue L, Fletcher GC, Tolkovsky AM (1999) Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 14:180-198.
60. Xue L, Fletcher GC, Tolkovsky AM (2001) Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr Biol 11:361-365.
61. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23:33-42.
62. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367-377.