Uncoupling of ATP-depletion and cell death in human dopaminergic neurons

NeuroToxicology

Volumn 33, Issue 4, 2012, Pages 769-779

  Pöltl, Dominik ^a   Schildknecht, Stefan ^a   Karreman, Christiaan ^a   Leist, Marcel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Caspases; Dopamine; LUHMES; MPP+; Oxidative stress; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; ADENOSINE TRIPHOSPHATE; ASCORBIC ACID; CASPASE; CASPASE INHIBITOR; CEP 1347; DEFEROXAMINE; DICHLORODIHYDROFLUORESCEIN DIACETATE; DOPAMINE; LACTATE DEHYDROGENASE; Q VD OPH; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RESAZURIN; UNCLASSIFIED DRUG; ZVAD OME FMK;

ARTICLE; CELL ASSAY; CELL ENERGY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY TEST; DOPAMINE METABOLISM; DOPAMINERGIC NERVE CELL; DRUG EFFICACY; DRUG MECHANISM; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME RELEASE; FEMALE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MITOCHONDRIAL RESPIRATION; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PRIORITY JOURNAL; WESTERN BLOTTING;

1-METHYL-4-PHENYLPYRIDINIUM; ADENOSINE TRIPHOSPHATE; ANTIOXIDANTS; APOPTOSIS; CASPASE INHIBITORS; CASPASES; CELLS, CULTURED; CYTOPROTECTION; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; ENZYME ACTIVATION; GENES, REPORTER; HUMANS; IRON CHELATING AGENTS; MITOCHONDRIA; OXIDATIVE STRESS; PROTEIN KINASE INHIBITORS; TIME FACTORS; TRANSFECTION; UNCOUPLING AGENTS;

EID: 84864510172     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.12.007     Document Type: Article

References (58)

1. Asaithambi A., Kanthasamy A., Saminathan H., Anantharam V., Kanthasamy A.G. Protein kinase D1 (PKD1) activation mediates a compensatory protective response during early stages of oxidative stress-induced neuronal degeneration. Mol Neurodegener 2011, 6:43.
2. Barber-Singh J., Seo B.B., Matsuno-Yagi A., Yagi T. Protective role of rAAV-NDI1, serotype 5, in an acute MPTP mouse Parkinson's model. Parkinsons Dis 2010, 2011:438370.
3. Behrouz B., Drolet R.E., Sayed Z.A., Lookingland K.J., Goudreau J.L. Unique responses to mitochondrial complex I inhibition in tuberoinfundibular dopamine neurons may impart resistance to toxic insult. Neuroscience 2007, 147:592-598.
4. Berliocchi L., Fava E., Leist M., Horvat V., Dinsdale D., Read D., et al. Botulinum neurotoxin C initiates two different programs for neurite degeneration and neuronal apoptosis. J Cell Biol 2005, 168:607-618.
5. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 2000, 3:1301-1306.
6. Bezard E., Przedborski S. A tale on animal models of Parkinson's disease. Mov Disord 2011, 26:993-1002.
7. Blomgren K., Leist M., Groc L. Pathological apoptosis in the developing brain. Apoptosis 2007, 12:993-1010.
8. Boll J.B., Geist M.A., Kaminski Schierle G.S., Petersen K., Leist M., Vaudano E. Improvement of embryonic dopaminergic neurone survival in culture and after grafting into the striatum of hemiparkinsonian rats by CEP-1347. J Neurochem 2004, 88:698-707.
9. + model of Parkinson's disease for high-throughput drug screenings. Neurodegener Dis 2004, 1:175-183.
10. Cassidy-Stone A., Chipuk J.E., Ingerman E., Song C., Yoo C., Kuwana T., et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 2008, 14:193-204.
11. Chan P., DeLanney L.E., Irwin I., Langston J.W., Di Monte D. Rapid ATP loss caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mouse brain. J Neurochem 1991, 57:348-351.
12. +, or paraquat. Proc Natl Acad Sci U S A 2008, 105:15136-15141.
13. Chung C.Y., Seo H., Sonntag K.C., Brooks A., Lin L., Isacson O. Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Hum Mol Genet 2005, 14:1709-1725.
14. Cui M., Tang X., Christian W.V., Yoon Y., Tieu K. Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J Biol Chem 2010, 285:11740-11752.
15. Dagda R.K., Cherra S.J., Kulich S.M., Tandon A., Park D., Chu C.T. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 2009, 284:13843-13855.
16. Di Monte D.A. The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins. Lancet Neurol 2003, 2:531-538.
17. DiMauro S., Schon E.A. Mitochondrial disorders in the nervous system. Annu Rev Neurosci 2008, 31:91-123.
18. Falsig J., Latta M., Leist M. Defined inflammatory states in astrocyte cultures: correlation with susceptibility towards CD95-driven apoptosis. J Neurochem 2004, 88:181-193.
19. Foghsgaard L., Wissing D., Mauch D., Lademann U., Bastholm L., Boes M., et al. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 2001, 153:999-1010.
20. Galluzzi L., Aaronson S.A., Abrams J., Alnemri E.S., Andrews D.W., Baehrecke E.H., et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 2009, 16:1093-1107.
21. Greenamyre J.T., Sherer T.B., Betarbet R., Panov A.V. Complex I. Parkinson's disease. IUBMB Life 2001, 52:135-141.
22. Hansson O., Castilho R.F., Kaminski Schierle G.S., Karlsson J., Nicotera P., Leist M., et al. Additive effects of caspase inhibitor and lazaroid on the survival of transplanted rat and human embryonic dopamine neurons. Exp Neurol 2000, 164:102-111.
23. Hirt U.A., Leist M. Rapid, noninflammatory and PS-dependent phagocytic clearance of necrotic cells. Cell Death Differ 2003, 10:1156-1164.
24. Huber H.J., Duessmann H., Wenus J., Kilbride S.M., Prehn J.H. Mathematical modelling of the mitochondrial apoptosis pathway. Biochim Biophys Acta 2011, 1813:608-615.
25. + toxicity: role of BDNF gene expression. Brain Res Mol Brain Res 1996, 41:14-26.
26. + in the nigrostriatal and mesolimbic dopaminergic pathways. Neurosci Lett 1995, 196:93-96.
27. Iadecola C., Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat Neurosci 2011, 14:1363-1368.
28. Kaneko M., Saito Y., Saito H., Matsumoto T., Matsuda Y., Vaught J.L., et al. Neurotrophic 3,9-bis[(alkylthio)methyl]-and-bis(alkoxymethyl)-K-252a derivatives. J Med Chem 1997, 40:1863-1869.
29. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983, 219:979-980.
30. Latta M., Künstle G., Leist M., Wendel A. Metabolic depletion of ATP by fructose inversely controls CD95- and tumor necrosis factor receptor 1-mediated hepatic apoptosis. J Exp Med 2000, 191:1975-1985.
31. Leander Johansen J., Dago L., Tornoe J., Rosenblad C., Kusk P. A new versatile and compact lentiviral vector. Mol Biotechnol 2005, 29:47-56.
32. Leist M., Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001, 2:589-598.
33. Leist M., Single B., Castoldi A.F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997, 185:1481-1486.
34. Leist M., Single B., Naumann H., Fava E., Simon B., Kuhnle S., et al. Nitric oxide inhibits execution of apoptosis at two distinct ATP-dependent steps upstream and downstream of mitochondrial cytochrome c release. Biochem Biophys Res Commun 1999, 258:215-221.
35. Leist M., Volbracht C., Fava E., Nicotera P. 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis. Mol Pharmacol 1998, 54:789-801.
36. Lotharius J., Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci 2002, 3:932-942.
37. Lotharius J., Falsig J., van Beek J., Payne S., Dringen R., Brundin P., et al. Progressive degeneration of human mesencephalic neuron-derived cells triggered by dopamine-dependent oxidative stress is dependent on the mixed-lineage kinase pathway. J Neurosci 2005, 25:6329-6342.
38. Lotharius J., O'Malley K.L. The parkinsonism-inducing drug 1-methyl-4-phenylpyridinium triggers intracellular dopamine oxidation. A novel mechanism of toxicity. J Biol Chem 2000, 275:38581-38588.
39. Lutz A.K., Exner N., Fett M.E., Schlehe J.S., Kloos K., Lammermann K., et al. Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem 2009, 284:22938-22951.
40. Müller G.J., Geist M.A., Veng L.M., Willesen M.G., Johansen F.F., Leist M., et al. A role for mixed lineage kinases in granule cell apoptosis induced by cytoskeletal disruption. J Neurochem 2006, 96:1242-1252.
41. Nicotra A., Parvez S. Apoptotic molecules and MPTP-induced cell death. Neurotoxicol Teratol 2002, 24:599-605.
42. Orrenius S., Nicotera P., Zhivotovsky B. Cell death mechanisms and their implications in toxicology. Toxicol Sci 2011, 119:3-19.
43. Richardson J.R., Caudle W.M., Guillot T.S., Watson J.L., Nakamaru-Ogiso E., Seo B.B., et al. Obligatory role for complex I inhibition in the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Toxicol Sci 2007, 95:196-204.
44. Schapira A.H. Complex I: inhibitors, inhibition and neurodegeneration. Exp Neurol 2010, 224:331-335.
45. Schapira A.H., Mann V.M., Cooper J.M., Krige D., Jenner P.J., Marsden C.D. Mitochondrial function in Parkinson's disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann Neurol 1992, 32(Suppl.):S116-S124.
46. Schildknecht S., Pape R., Müller N., Robotta M., Marquardt A., Bürkle A., et al. Neuroprotection by minocycline caused by direct and specific scavenging of peroxynitrite. J Biol Chem 2011, 286:4991-5002.
47. Schildknecht S., Pöltl D., Nagel D.M., Matt F., Scholz D., Lotharius J., et al. Requirement of a dopaminergic neuronal phenotype for toxicity of low concentrations of 1-methyl-4-phenylpyridinium to human cells. Toxicol Appl Pharmacol 2009, 241:23-35.
48. Scholz D., Pöltl D., Genewsky A., Weng M., Waldmann T., Schildknecht S., et al. Rapid, complete and large-scale generation of post-mitotic neurons from the human LUHMES cell line. J Neurochem 2011, 119:957-971.
49. Schon E.A., Przedborski S. Mitochondria: the next (neurode)generation. Neuron 2011, 70:1033-1053.
50. Schotte P., Declercq W., Van Huffel S., Vandenabeele P., Beyaert R. Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett 1999, 442:117-121.
51. She H., Yang Q., Shepherd K., Smith Y., Miller G., Testa C., et al. Direct regulation of complex I by mitochondrial MEF2D is disrupted in a mouse model of Parkinson disease and in human patients. J Clin Invest 2011, 121:930-940.
52. Stephans S.E., Miller G.W., Levey A.I., Greenamyre J.T. Acute mitochondrial and chronic toxicological effects of 1-methyl-4-phenylpyridinium in human neuroblastoma cells. Neurotoxicology 2002, 23:569-580.
53. Sundstrom E., Samuelsson E.B. Comparison of key steps in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity in rodents. Pharmacol Toxicol 1997, 81:226-231.
54. Tymianski M. Emerging mechanisms of disrupted cellular signaling in brain ischemia. Nat Neurosci 2011, 14:1369-1373.
55. Volbracht C., Leist M., Kolb S.A., Nicotera P. Apoptosis in caspase-inhibited neurons. Mol Med 2001, 7:36-48.
56. Volbracht C., Leist M., Nicotera P. ATP controls neuronal apoptosis triggered by microtubule breakdown or potassium deprivation. Mol Med 1999, 5:477-489.
57. von Bohlen und Halbach O. Modeling neurodegenerative diseases in vivo review. Neurodegener Dis 2005, 2:313-320.
58. Zhou C., Huang Y., Przedborski S. Oxidative stress in Parkinson's disease: a mechanism of pathogenic and therapeutic significance. Ann N Y Acad Sci 2008, 1147:93-104.