Rotenone-induced caspase 9/3-independent and -dependent cell death in undifferentiated and differentiated human neural stem cells

Journal of Neurochemistry

Volumn 92, Issue 3, 2005, Pages 462-476

  Li, Jiang ^a   Spletter, Maria L ^a   Johnson, Delinda A ^a   Wright, Lynda S ^b   Svendsen, Clive N ^b   Johnson, Jeffrey A ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; ATP; Camptothecin; Caspase 3; Human neural stem cell; Rotenone

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAMPTOTHECIN; CASPASE 3; CASPASE 9; CYTOCHROME C; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; REACTIVE OXYGEN METABOLITE; ROTENONE;

APOPTOSIS; ARTICLE; CELL DEATH; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NICK END LABELING; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; CAMPTOTHECIN; CASPASE 3; CASPASE 9; CASPASES; CELL DEATH; CELL DIFFERENTIATION; CELLS, CULTURED; DNA FRAGMENTATION; DNA TOPOISOMERASES, TYPE I; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; IN SITU NICK-END LABELING; MODELS, BIOLOGICAL; NEURONS; REACTIVE OXYGEN SPECIES; ROTENONE; STEM CELLS; UNCOUPLING AGENTS;

EID: 13244277666     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02872.x     Document Type: Article

References (59)

1. Acehan D., Jiang X., Morgan D. G., Heuser J. E., Wang X. and Akey C. W. (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell 9, 423-432.
2. Ahmadi F. A., Linseman D. A., Grammatopoulos T. N., Jones S. M., Bouchard R. J., Freed C. R., Heidenreich K. A. and Zawada W. M. (2003) The pesticide rotenone induces caspase-3-mediated apoptosis in ventral mesencephalic dopaminergic neurons. J. Neurochem. 87, 914-921.
3. Barrientos A. and Moraes C. T. (1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 274, 16 188-16 197.
4. Caldwell M. A., He X., Wilkie N., Pollack S., Marshall G., Wafford K. A. and Svendsen C. N. (2001) Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 19, 475-479.
5. Carpenter M. K., Cui X., Hu Z. Y., Jackson J., Sherman S., Seiger A. and Wahlberg L. U. (1999) In vitro expansion of a multipotent population of human neural progenitor cells. Exp. Neurol. 158, 265-278.
6. Cedrola S., Guzzi G., Ferrari D., Gritti A., Vescovi A. L., Pendergrass J. C. and La Porta C. A. (2003) Inorganic mercury changes the fate of murine CNS stem cells. FASEB J. 17, 869-871.
7. Chalmers-Redman R. M., Priestley T., Kemp J. A. and Fine A. (1997) In vitro propagation and inducible differentiation of multipotential progenitor cells from human fetal brain. Neurosdence 76, 1121-1128.
8. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X. and Fontaine E. (2001) Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J. Biol. Chem. 276, 41 394-41 398.
9. Chen Q., Chai Y. C., Mazumder S., Jiang C., Macklis R. M., Chisolm G. M. and Almasan A. (2003) The late increase in intracellular free radical oxygen species during apoptosis is associated with cytochrome c release, caspase activation, and mitochondrial dysfunction. Cell Death Differ. 10, 323-334.
10. Dawson T. M. and Dawson V. L. (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822.
11. Eckert A., Keil U., Marques C. A., Bonert A., Frey C., Schussel K. and Muller W. E. (2003) Mitochondrial dysfunction, apoptotic cell death, and Alzheimer's disease. Biochem. Pharmacol. 66, 1627-1634.
12. Eguchi Y., Shimizu S. and Tsujimoto Y. (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57, 1835-1840.
13. Fields R. D. and Stevens-Graham B. (2002) New insights into neuron-glia communication. Science 298, 556-562.
14. Gao H. M., Liu B. and Hong J. S. (2003) Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 23, 6181-6187.
15. Higuchi M., Honda T., Proske R. J. and Yeh E. T. (1998) Regulation of reactive oxygen species-induced apoptosis and necrosis by caspase 3-like proteases. Oncogene 17, 2753-2760.
16. Hoglinger G. U., Carrard G., Michel P. P., Medja F., Lombes A., Ruberg M., Friguet B. and Hirsch E. C. (2003) Dysfunction of mitochondrial complex I and the proteasome: interactions between two biochemical deficits in a cellular model of Parkinson's disease. J. Neurochem. 86, 1297-1307.
17. Isenberg J. S. and Klaunig J. E. (2000) Role of the mitochondrial membrane permeability transition (MPT) in rotenone-induced apoptosis in liver cells. Toxicol. Sci. 53, 340-351.
18. Jakel R. J., Schneider B. L. and Svendsen C. N. (2004) Using human neural stem cells to model neurological disease. Nat. Rev. Genet. 5, 136-144.
19. 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.
20. Kerr J. F., Wyllie A. H. and Currie A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
21. 2+ and neurodegenerative disease. Eur. J. Pharmacol. 447, 177-188.
22. Kroemer G., Dallaporta B. and Resche-Rigon M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60, 619-642.
23. Kuida K., Haydar T. F., Kuan C. Y., Gu Y., Taya C., Karasuyama H., Su M. S., Rakic P. and Flavell R. A. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325-337.
24. Kuwana T. and Newmeyer D. D. (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 15, 691-699.
25. Lang-Rollin I. C., Rideout H. J., Noticewala M. and Stefanis L. (2003) Mechanisms of caspase-independent neuronal death: energy depletion and free radical generation. J. Neurosci. 23, 11 015-11 025.
26. Lapointe N., St-Hilaire M., Martinoli M. G., Blanchet J., Gould P., Rouillard C. and Cicchetti F. (2004) Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J. 18, 717-719.
27. Leist M., Single B., Castoldi A. F., Kuhnle S. and Nicotera P. (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185, 1481-1486.
28. Lesauskaite V., Epistolato M. C., Ivanoviene L. and Tanganelli P. (2004) Apoptosis of cardiomyocytes in explanted and transplanted hearts. Comparison of results from in situ TUNEL, ISEL, and ISOL reactions. Am. J. Clin. Pathol. 121, 108-116.
29. Li J., Lee J. M. and Johnson J. A. (2002) Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells. J. Biol Chem. 277, 388-394.
30. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J. A. and Robinson J. P. (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278, 8516-8525.
31. Liu X., Kim C. N., Yang J., Jemmerson R. and Wang X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147-157.
32. Morris E. J. and Geller H. M. (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.
33. Nair V. D., Yuen T., Olanow C. W. and Sealfon S. C. (2004) Early single cell bifurcation of pro-and anti-apoptotic states during oxidative stress. J. Biol. Chem. 279, 27 494-27 501.
34. Newhouse K., Hsuan S. L., Chang S. H., Cai B., Wang Y. and Xia Z. (2004) Rotenone-induced apoptosis is mediated by p38 and JNK MAP kinases in human dopaminergic SH-SY5Y cells. Toxicol. Sci. 79, 137-146.
35. Pompeiano M., Blaschke A. J., Flavell R. A., Srinivasan A. and Chun J. (2000) Decreased apoptosis in proliferative and postmitotic regions of the caspase 3-deficient embryonic central nervous system. J. Comp. Neurol. 423, 1-12.
36. Pulkkanen K. J., Laukkanen M. O., Naarala J. and Yla-Herttuala S. (2000) False-positive apoptosis signal in mouse kidney and liver detected with TUNEL assay. Apoptosis 5, 329-333.
37. Ray D. E. (1991) Pesticides derived from plants and other organisms, in Handbook of Pesticide Toxicology (Hayes W. J. Jr and Laws E. R. Jr, eds). pp. 2-3. Academic Press, New York.
38. Ribas J. and Boix J. (2004) Cell differentiation, caspase inhibition, and macromolecular synthesis blockage, but not BCL-2 or BCL-XL proteins, protect SH-SY5Y cells from apoptosis triggered by two CDK inhibitory drugs. Exp. Cell Res. 295, 9-24.
39. Rolo A. P., Palmeira C. M., Holy J. M. and Wallace K. B. (2004) Role of mitochondrial dysfunction in combined bile acid-induced cytotoxicity: the switch between apoptosis and necrosis. Toxicol. Sci. 79, 196-204.
40. Roy M. and Sapolsky R. (1999) Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? Trends Neurosci. 22, 419-422.
41. Sherer T. B., Betarbet R., Stout A. K., Lund S., Baptista M., Panov A. V., Cookson M. R. and Greenamyre J. T. (2002) An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J. Neurosci. 22, 7006-7015.
42. Sherer T. B., Betarbet R., Testa C. M., Seo B. B., Richardson J. R., Kim J. H., Miller G. W., Yagi T., Matsuno-Yagi A. and Greenamyre J. T. (2003) Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23, 10 756-10 764.
43. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H. and Tsujimoto Y. (1996) Retardation of chemical hypoxia-induced necrotic cell death by Bcl-2 and ICE inhibitors: possible involvement of common mediators in apoptotic and necrotic signal transductions. Oncogene 12, 2045-2050.
44. Sloviter R. S. (2002) Apoptosis: a guide for the perplexed. Trends Pharmacol. Sci. 23, 19-24.
45. Stefanelli C., Bonavita R, Stanic I. et al. (1997) ATP depletion inhibits glucocorticoid-induced thymocyte apoptosis. Biochem. J. 322, 909-917.
46. Stefanis L., Park D. S., Friedman W. J. and Greene L. A. (1999) Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J. Neurosci. 19, 6235-6247.
47. Stevens B., Porta S., Haak L. L., Gallo V. and Fields R. D. (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36, 855-868.
48. Susin S. A., Zamzami N., Castedo M., Daugas E., Wang H. G., Geley S., Fassy F., Reed J. C. and Kroemer G. (1997) The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 186, 25-37.
49. Susin S. A., Lorenzo H. K., Zamzami N. et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
50. Torres-Roca J. F., Tung J. W., Greenwald D. R., Brown J. M., Herzenberg L. A. and Katsikis P. D. (2000) An early oxygen-dependent step is required for dexamethasone-induced apoptosis of immature mouse thymocytes. J. Immunol 165, 4822-4830.
51. Ulukan H. and Swaan P. W. (2002) Camptothecins: a review of their chemotherapeutic potential. Drugs 62, 2039-2057.
52. Valencia A. and Moran J. (2004) Reactive oxygen species induce different cell death mechanisms in cultured neurons. Free Radic. Biol. Med., 36, 1112-1125.
53. Vrablic A. S., Albright C. D., Craciunescu C. N., Salganik R. I. and Zeisel S. H. (2001) Altered mitochondrial function and overgeneration of reactive oxygen species precede the induction of apoptosis by 1-O-octadecyl-2-methyl-rac-glycero-3-phosphocholine in p53-defective hepatocytes. FASEB J. 15, 1739-1744.
54. 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.
55. Wang X., Qin Z. H., Leng Y., Wang Y., Jin X., Chase T. N. and Bennett M. C. (2002) Prostaglandin A1 inhibits rotenone-induced apoptosis in SH-SY5Y cells. J. Neurochem. 83, 1094-1102.
56. Woo M. H., Losasso C., Guo H., Pattarello L., Benedetti P. and Bjornsti M. A. (2003) Locking the DNA topoisomerase I protein clamp inhibits DNA rotation and induces cell lethality. Proc. Natl Acad. Sci. USA 100, 13 767-13 772.
57. Wright L. S., Li J., Caldwell M. A., Wallace K., Johnson J. A. and Svendsen C. N. (2003) Gene expression in human neural stem cells: effects of leukemia inhibitory factor. J. Neurochem. 86, 179-195.
58. +-ATPase to hypertrophy and its marker genes in cardiac myocytes. J. Biol. Chem. 274, 19 323-19 328.
59. Zhang C., Gong Y., Ma H., An C., Chen D. and Chen Z. L. (2001) Reactive oxygen species involved in trichosanthin-induced apoptosis of human choriocarcinoma cells. Biochem. J. 355, 653-661.