Apoptosis inducing factor mediates caspase-independent 1-methyl-4- phenylpyridinium toxicity in dopaminergic cells

Journal of Neurochemistry

Volumn 94, Issue 6, 2005, Pages 1685-1695

  Chu, Charleen T ^a,c   Zhu, Jian Hui ^a   Cao, Guodong ^a   Signore, Armando ^a   Wang, Suping ^a   Chen, Jun ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Dopaminergic cells; Mitochondria; Neuronal cell death; Parkinson's disease; Primary midbrain neurons; RNA interference

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; APOPTOSIS INDUCING FACTOR; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE; CASPASE 9; CASPASE INHIBITOR; MITOCHONDRIAL PROTEIN; NEUROTOXIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL NUCLEUS; CONTROLLED STUDY; DEGENERATIVE DISEASE; DNA STRAND BREAKAGE; DNA VECTOR; DOPAMINERGIC NERVE CELL; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; MESENCEPHALON; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE;

1-METHYL-4-PHENYLPYRIDINIUM; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASES; CELL LINE; DNA FRAGMENTATION; DOPAMINE; DOWN-REGULATION; FLAVOPROTEINS; MEMBRANE PROTEINS; MESENCEPHALON; MICE; MPTP POISONING; NERVE DEGENERATION; NEURONS; PROTEIN TRANSPORT; RNA INTERFERENCE;

PARKINSONIA; RODENTIA;

EID: 24944576007     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03329.x     Document Type: Article

References (46)

1. Betarbet R., Sherer T. B., Di Monte D. A. and Greenamyre J. T. (2002) Mechanistic approaches to Parkinson's disease pathogenesis. Brain Pathol. 12, 499-510.
2. Bidere N., Lorenzo H. K., Carmona S., Laforge M., Harper F., Dumont C. and Senik A. (2003) Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J. Biol. Chem. 278, 31 401-31 411.
3. Bilsland J., Roy S., Xanthoudakis S., Nicholson D. W., Han Y., Grimm E., Hefti F. and Harper S. J. (2002) Caspase inhibitors attenuate 1-methyl-4-phenylpyridinium toxicity in primary cultures of mesencephalic dopaminergic neurons. J. Neurosci. 22, 2637-2649.
4. Byrd J. C. and Alho H. (1987) Differentiation of PC12 pheochromocytoma cells by sodium butyrate. Brain Res. 428, 151-155.
5. Callio J., Oury T. D. and Chu C. T. (2005) Manganese superoxide dismutase protects against 6-hydroxydopamine injury in mouse brains. J. Biol. Chem. 280, 18 536-18 542.
6. Cao G., Clark R. S., Pei W., Yin W., Zhang F., Sun F. Y., Graham S. H. and Chen J. (2003) Translocation of apoptosis-inducing factor in vulnerable neurons after transient cerebral ischemia and in neuronal cultures after oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 23, 1137-1150.
7. Cao G., Xiao M., Sun F. Y., Xiao X., Pei W., Li J., Graham S. H., Simon R. P., and Chen J. (2004) Cloning of a novel Apaf-1-interacting protein: a potent suppressor of apoptosis and ischemic neuronal cell death. J Neurosci. 24, 6189-6201.
8. Chen J., Jing K., Chen M., Pei W., Kawaguchi K., Greenberg D. A., Simon R. P. (1997) Early detection of DNA strand breaks in the brain after transient focal ischemia: implication for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem. 69, 232-245.
9. Choi H. K., Won L. A., Kontur P. J., Hammond D. N., Fox A. P., Wainer B. H., Hoffmann P. C. and Heller A. (1991) Immortalization of embryonic mesencephalic dopaminergic neurons by somatic cell fusion. Brain Res. 552, 67-76.
10. Choi W. S., Yoon S. Y., Oh T. H., Choi E. J., O'Malley K. L. and Oh Y. J. (1999) Two distinct mechanisms are involved in 6-hydroxydopamine- and MPP+- induced dopaminergic neuronal cell death: role of caspases, ROS, and JNK. J. Neurosci. Res. 57, 86-94.
11. Chu C. T., Levinthal D. J., Kulich S. M., Chalovich E. M. and DeFranco D. B. (2004) Oxidative neuronal injury. The dark side of ERK1/2. Eur. J. Biochem. 271, 2060-2066.
12. Cregan S. P., Fortin A., MacLaurin J. G. et al. (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J. Cell Biol. 158, 507-517.
13. Dauer W. and Przedborski S. (2003) Parkinson's disease: mechanisms and models. Neuron 39, 889-909.
14. Daugas E., Susin S. A., Zamzami N. et al. (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14, 729-739.
15. Dawson T. M. and Dawson V. L. (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822.
16. Dodel R. C., Du Y., Bales K. R., Ling Z. D., Carvey P. M. and Paul S. M. (1998) Peptide inhibitors of caspase-3-like proteases attenuate 1-methyl-4-phenylpyridinum-induced toxicity of cultured fetal rat mesencephalic dopamine neurons. Neuroscience 86, 701-707.
17. Eberhardt O. and Schulz J. B. (2003) Apoptotic mechanisms and antiapoptotic therapy in the MPTP model of Parkinson's disease. Toxicol. Lett. 139, 135-151.
18. Eberhardt O., Coelln R. V., Kugler S. et al. (2000) Protection by synergistic effects of adenovirus-mediated X-chromosome-linked inhibitor of apoptosis and glial cell line-derived neurotrophic factor gene transfer in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neurosci. 20, 9126-9134.
19. Eguchi Y., Shimizu S. and Tsujimoto Y. (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57, 1835-1840.
20. Florez-McClure M. L., Linseman D. A., Chu C. T., Barker P. A., Bouchard R. J., Le S. S., Laessig T. A. and Heidenreich K. A. (2004) The p75 neurotrophin receptor can induce autophagy and death of cerebellar Purkinje neurons. J. Neurosci. 24, 4498-4509.
21. Gomez-Santos C., Ferrer I., Santidrian A. F., Barrachina M., Gil J. and Ambrosio S. (2003) Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells. J. Neurosci. Res. 73, 341-350.
22. Han B. S., Hong H. S., Choi W. S., Markelonis G. J., Oh T. H. and Oh Y. J. (2003) Caspase-dependent and -independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment. J. Neurosci. 23, 5069-5078.
23. Hartmann A., Troadec J. D., Hunot S., Kikly K., Faucheux B. A., Mouatt-Prigent A., Ruberg M., Agid Y. and Hirsch E. C. (2001) Caspase-8 is an effector in apoptotic death of dopaminergic neurons in Parkinson's disease, but pathway inhibition results in neuronal necrosis. J. Neurosci. 21, 2247-2255.
24. Holtz W. A. and O'Malley K. L. (2003) Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J. Biol. Chem. 278, 19 367-19 377.
25. Horbinski C. and Chu C. T. (2005) Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic. Biol. Med. 38, 2-11.
26. Joza N., Susin S. A., Daugas E. et al. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410, 549-554.
27. Kaul S., Kanthasamy A., Kitazawa M., Anantharam V. and Kanthasamy A. G. (2003) Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur. J. Neurosci. 18, 1387-1401.
28. Lotharius J., Dugan L. L. and O'Malley K. L. (1999) Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J. Neurosci. 19, 1284-1293.
29. McCullough K. D., Martindale J. L., Klotz L. O., Aw T. Y. and Holbrook N. J. (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21, 1249-1259.
30. Mochizuki H., Nakamura N., Nishi K. and Mizuno Y. (1994) Apoptosis is induced by 1-methyl-4-phenylpyridinium ion (MPP+) in ventral mesencephalic-striatal co-culture in rat. Neurosci. Lett. 170, 191-194.
31. Nicotera P., Leist M., Fava E., Berliocchi L. and Volbracht C. (2000) Energy requirement for caspase activation and neuronal cell death. Brain Pathol. 10, 276-282.
32. Offen D., Beart P. M., Cheung N. S., Pascoe C. J., Hochman A., Gorodin S., Melamed E., Bernard R. and Bernard O. (1998) Transgenic mice expressing human Bcl-2 in their neurons are resistant to 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity. Proc. Natl Acad. Sci. USA 95, 5789-5794.
33. Potts P. R., Singh S., Knezek M., Thompson C. B. and Deshmukh M. (2003) Critical function of endogenous XIAP in regulating caspase activation during sympathetic neuronal apoptosis. J. Cell Biol. 163, 789-799.
34. Ryu E. J., Harding H. P., Angelastro J. M., Vitolo O. V., Ron D. and Greene L. A. (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22, 10690-10698.
35. Susin S. A., Lorenzo H. K., Zamzami N. et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
36. Tatton N. A. and Kish S. J. (1997) In situ detection of apoptotic nuclei in the substantia nigra compacta of 1-methyl-4-phenyl-1,2,3,6-tetra- hydropyridine-treated mice using terminal deoxynucleotidyl transferase labelling and acridine orange staining. Neuroscience 77, 1037-1048.
37. Tolkovsky A. M., Xue L., Fletcher G. C. and Borutaite V. (2002) Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease? Biochimie 84, 233-240.
38. Turmel H., Hartmann A., Parain K., Douhou A., Srinivasan A., Agid Y. and Hirsch E. C. (2001) Caspase-3 activation in 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP)-treated mice. Mov. Disord. 16, 185-189.
39. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberalere G., Offen D., Korsmeyer S. J. and Przedborski S. (2001) Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. Proc. Natl Acad. Sci. USA 98, 2837-2842.
40. 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, 10 963-10 973.
41. Yang L., Matthews R. T., Schulz J. B., Klockgether T., Liao A. W., Martinou J. C., Penney J. B. Jr, Hyman B. T. and Beal M. F. (1998) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyride neurotoxiciry is attenuated in mice overexpressing Bcl-2. J. Neurosci. 18, 8145-8152.
42. Yang L., Sugama S., Mischak R. P., Kiaei M., Bizat N., Brouillet E., Joh T. H. and Beal M. F. (2004) A novel systemically active caspase inhibitor attenuates the toxicities of MPTP, malonate, and 3NP in vivo. Neurobiol Dis 17, 250-259.
43. 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.
44. Zaidi A. U., McDonough J. S., Klocke B. J., Latham C. B., Korsmeyer S. J., Flavell R. A., Schmidt R. E. and Roth K. A. (2001) Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J. Neuropathol. Exp. Neurol. 60, 937-945.
45. Zhang X., Chen J., Du Graham S. H. L., Kochanek P. M., Draviam R., Guo F., Nathaniel P. D., Szabo C., Watkins S. C. and Clark R. S. (2002) Intranuclear localization of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. J. Neurochem. 82, 181-191.
46. Zhu J.-H., Guo F., Shelbume J., Watkins S. and Chu C. T. (2003) Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases. Brain Pathol. 13, 473-481.