Interaction of mitochondrial respiratory inhibitors and excitotoxins potentiates cell death in hippocampal slice cultures

Journal of Neuroscience Research

Volumn 86, Issue 15, 2008, Pages 3306-3313

  Schuh, Rosemary A ^a,b   Matthews, Christopher C ^a,b   Fishman, Paul S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Mitochondria; Neurodegenerative disease; Oxidative stress

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; MONOCLONAL ANTIBODY; N METHYL DEXTRO ASPARTIC ACID; PESTICIDE; PROPIDIUM IODIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; TETRYLAMMONIUM CHLORIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN SLICE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME INHIBITION; IMMUNOHISTOCHEMISTRY; MITOCHONDRIAL RESPIRATION; NERVE CELL; NEUROTOXICITY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; TISSUE CULTURE;

ANIMALS; CELL DEATH; CELL RESPIRATION; DRUG INTERACTIONS; EXCITATORY AMINO ACID AGONISTS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MITOCHONDRIA; N-METHYLASPARTATE; NEURONS; NEUROTOXINS; ORGAN CULTURE TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; ROTENONE; TETRAETHYLAMMONIUM; UNCOUPLING AGENTS;

EID: 57049162931     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21772     Document Type: Article

References (39)

1. 2 elevation, not ATP depletion. J Neurosci 25:10029-10040.
2. Beal MF. 1998. Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366:211-223.
3. Bernardi P, Petronilli V, Di Lisa F, Forte M. 2001. A mitochondrial perspective on cell death. Trends Biochem Sci 26:112-117.
4. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3:1301-1306.
5. Bonde C, Noraberg J, Noer H, Zimmer J. 2005. Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation in hippocampal slice cultures. Neuroscience 136:779-794.
6. Budd SL, Nicholls DG. 1996. Mitochondria, calcium regulation and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 67:2282-2291.
7. Castilho RF, Ward MW, Nicholls DG. 1999. Oxidative stress, mitochondrial function and acute glutamate excitotoxicity in cultured cerebellar granule neurons. J Neurochem 72:1394-1401.
8. Corrigan FM, Wienburg CL, Shore RF, Daniel SE, Mann D. 2000. Organochlorine insecticides in substantia nigra in Parkinson's disease. J Toxicol Environ Health A59:229-234.
9. Dauer W, Przedborski S. 2003. Parkinson's disease: mechanisms and models. Neuron 39:889-909.
10. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW. 1995. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15:6377-6388.
11. Fleming L, Mann JB, Bean J, Briggle T, Sanchez-Ramos JR 1994. Parkinson's disease and brain levels of organochlorine pesticides. Ann Neurol 36:100-103.
12. 2+ entry during NMDA receptor activation. FASEB J 20:E245-E259.
13. Kaal EC, Vlug AS, Versleijen WJ, Kuilman M, Joosten EA, Bär PR. 2000. Chronic mitochondrial inhibition induces selective motorneuron death in vitro: a new model for amyotrophic lateral sclerosis. J Neurochem 74:158-1165.
14. Keeney PM, Capaldi RA, Bennett JP. 2006. Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J Neurosci 26:5256-5264.
15. Khodorov B, Pinelis V, Vergun O, Storozhevykh T, Vinskaya N. 1996. Mitochondrial deenergization underlies neuronal calcium overload following a prolonged glutamate challenge. FEBS Lett 397:230-234.
16. Kress GJ, Reynolds IJ. 2005. Dopaminergic neurotoxins require excitotoxic stimulation in organotypic cultures. Neurobiol Dis 20:639-645.
17. Kristensen BW, Noraberg J, Zimmer J. 2001. Comparison of excitotoxic pro.les of ATPA. AMPA, KA and NMDA in organotypic slice cultures. Brain Res 917:21-44.
18. Kristián T, Weatherby TM, Bates TE, Fiskum G. 2002. Heterogeneity of the calcium-induced permeability transition in isolated non-synaptic brain mitochondria. J Neurochem 83:1297-1308.
19. LeCouteur DG, McLean AJ, Taylor MC, Woodham BL, Board PG. 1999. Pesticides and Parkinson's disease. Biomed Pharmacother 53:122-130.
20. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA, Robinson JP. 2003. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 278:8516-8525.
21. Matthews CC, Zielke HR, Parks DA, Fishman PS. 2003. Glutamate-pyruvate transaminase protects against glutamate toxicity in hippocampal slices. Brain Res 978:59-64.
22. Nicholls DG. 2004. Mitochondrial dysfunction and glutamate excitoxicity studied in primary neuronal cultures. Curr Mol Med 4:149-177.
23. Niknahad H, O'Brien PJ. 1996. Antidotal effect of dihydroxyacetone against cyanide toxicity in vivo. Toxicol Appl Pharmacol 138:186-191.
24. Panov A, Dikalov S, Shalbuyeva N, Taylor G, Sherer T, Greenamyre JT. 2005. Rotenone model of Parkinson's disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J Biol Chem 280:42026-42035.
25. Priyadarshi A, Khuder SA, Schaub EA, Priyadarshi SS. 2001. Environmental risk factors and Parkinson's disease: a metaanlaysis. Environ Res 86:122-127.
26. Reynolds I, Hastings TG. 1995. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15:3318-3327.
27. Rothstein JD. 1995. Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin Neurosci 3:348-359.
28. Sattler R, Rothstein JD. 2006. Regulation and dysregulation of glutamate transporters. Hdbk Exp Pharmacol 175:277-303.
29. Schindler AF, Olson EC, Spitzer NC, Montal M. 1996. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
30. Starkov AA, Chinopoulos C, Fiskum G. 2004. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36:257-264.
31. Swerdlow RH, Parks JK, Miller SW, Tuttle JB, Trimmer PA, Sheehan JP, Bennett JP, Davis RE, Parker WD. 1996. Origin and functional consequences of the complex I defect in Parkinson's disease. Ann Neurol 40:663-671.
32. Thomas B, Beal MF. 2007. Parkinson's disease. Hum Mol Genet 16:R183-R194.
33. Thompson SM, Fortunato C, McKinney RA, Müller M, Gähwiler BH. 1996. Mechanisms underlying the neuropathological consequences of epileptic activity in the rat hippocampus in vitro. J Comp Neurol 372:515-528.
34. Van Westerlaak MG, Joosten EA, Gribnau AA, Cools AR, Bar PR. 2001. Chronic mitochondrial inhibition induces glutamate-mediated corticomotoneuron death in an organotypic culture model. Exp Neurol 167:393-400.
35. Vornov JJ, Tasker RC, Park J. 1995. Neurotoxicity of acute glutamate transport blockade depends on coactivation of both NMDA and AMPA/kainate receptors in organotypic hippocampal cultures. Exp Neurol 133:7-17.
36. Vornov JJ, Park J, Thomas AG. 1998. Regional vulnerability to endogenous oxidative stress in organotypic hippocampal cultures. Exp Neurol 149:109-122.
37. Wu Y, Johnson SW. 2007. Rotenone potentiates NMDA currents in substantia nigra dopamine neurons. Neurosci Lett 421:96-100.
38. Xu G, Perez-Pinzon MA, Sick TJ. 2003. Mitochondrial complex I inhibition produces selective damage to hippocampal sub.eld CA1 in organotypic slice cultures. Neurotox Res 5:529-538.
39. Yadava N, Nicholls DG. 2007. Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone. J Neurosci 27:7310-7317.