Intrinsic bioenergetic properties and stress sensitivity of dopaminergic synaptosomes

Journal of Neuroscience

Volumn 31, Issue 12, 2011, Pages 4524-4534

  Choi, Sung W ^a   Gerencser, Akos A ^a   Lee, Donna W ^a   Rajagopalan, Subramanian ^a   Nicholls, David G ^a   Andersen, Julie K ^a   Brand, Martin D ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE TRANSPORTER; 4-(4-DIETHYLAMINOSTYRYL)-N-METHYLPYRIDINIUM; CALCIUM; DOPAMINE; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; PYRIDINIUM DERIVATIVE;

AGE; ANIMAL CELL; ARTICLE; BIOENERGY; BRAIN CORTEX; BRAIN SYNAPTOSOME; CELL RESPIRATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; TISSUE SPECIFICITY; AGING; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENERGY METABOLISM; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; KINETICS; MEMBRANE POTENTIAL; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHYSIOLOGY; SYNAPTOSOME;

AGING; ANIMALS; CALCIUM; CORPUS STRIATUM; DOPAMINE; ENERGY METABOLISM; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; INDICATORS AND REAGENTS; KINETICS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PYRIDINIUM COMPOUNDS; SYNAPTOSOMES;

EID: 79953005999     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5817-10.2011     Document Type: Article

References (52)

1. Andersen PH (1989) The dopamine inhibitor GBR 12909: selectivity and molecular mechanism of action. Eur J Pharmacol 166:493-504.
2. Antier D, Carswell HV, Brosnan MJ, Hamilton CA, Macrae IM, Groves S, Jardine E, Reid JL, Dominiczak AE (2004) Increased levels of superoxide in brains from old female rats. Free Radic Res 38:177-183. (Pubitemid 38181174)
3. Arluison M, Dietl M, Thibault J (1984) Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: a topographical study. Brain Res Bull 13:269-285. (Pubitemid 14004854)
4. Bertoni-Freddari C, Fattoretti P, Pieroni M, Meier-Ruge W, Ulrich J (1992) Enlargement of synaptic size as a compensative reaction in aging and dementia. Pathol Res Pract 188:612-615.
5. Bertoni-Freddari C, Fattoretti P, Casoli T, Spagna C, Meier-Ruge W, Ulrich J (1993) Morphological plasticity of synaptic mitochondria during aging. Brain Res 628:193-200. (Pubitemid 23331609)
6. Bertoni-Freddari C, Fattoretti P, Paoloni R, Caselli U, Galeazzi L, Meier-Ruge W (1996) Synaptic structural dynamics and aging. Gerontology 42:170-180. (Pubitemid 26183967)
7. Bertoni-Freddari C, Mocchegiani E, Malavolta M, Casoli T, Di Stefano G, Fattoretti P (2006) Synaptic and mitochondrial physiopathologic changes in the aging nervous system and the role of zinc ion homeostasis. Mech Ageing Dev 127:590-596.
8. 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.
9. Bisaglia M, Soriano ME, Arduini I, Mammi S, Bubacco L (2010) Molecular characterization of dopamine-derived quinones reactivity toward NADH and glutathione: implications for mitochondrial dysfunction in Parkinson disease. Biochim Biophys Acta 1802:699-706.
10. Bowling AC, Mutisya EM, Walker LC, Price DL, Cork LC, Beal MF (1993) Age-dependent impairment of mitochondrial function in primate brain. J Neurochem 60:1964-1967. (Pubitemid 23127610)
11. Brenner-Lavie H, Klein E, Zuk R, Gazawi H, Ljubuncic P, Ben-Shachar D (2008) Dopamine modulates mitochondrial function in viable SH-SY5Y cells possibly via its interaction with complex I: relevance to dopamine pathology in schizophrenia. Biochim Biophys Acta 1777:173-185. (Pubitemid 351162862)
12. Brenner-Lavie H, Klein E, Ben-Shachar D (2009) Mitochondrial complex I as a novel target for intraneuronal DA: modulation of respiration in intact cells. Biochem Pharmacol 78:85-95.
13. Calabresi P, Centonze D, Bernardi G (2000) Cellular factors controlling neuronal vulnerability in the brain: a lesson from the striatum. Neurology 55:1249-1255.
14. Cantuti-Castelvetri I, Shukitt-Hale B, Joseph JA (2003) Dopamine neurotoxicity: age-dependent behavioral and histological effects. Neurobiol Aging 24:697-706. (Pubitemid 37288868)
15. Chinta SJ, Kumar MJ, Hsu M, Rajagopalan S, Kaur D, Rane A, Nicholls DG, Choi J, Andersen JK (2007) Inducible alterations of glutathione levels in adult dopaminergic midbrain neurons result in nigrostriatal degeneration. J Neurosci 27:13997-14006. (Pubitemid 351377875)
16. Choi SW, Gerencser AA, Nicholls DG (2009) Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J Neurochem 109:1179-1191.
17. Davey GP, Canevari L, Clark JB (1997) Threshold effects in synaptosomal and nonsynaptic mitochondria from hippocampal CA1 and paramedian neocortex brain regions. J Neurochem 69:2564-2570. (Pubitemid 27495444)
18. Davey GP, Peuchen S, Clark JB (1998) Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J Biol Chem 273:12753-12757. (Pubitemid 28246828)
19. Dawson TM, Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302:819-822. (Pubitemid 37339614)
20. Dunkley PR, Jarvie PE, Robinson PJ (2008) A rapid Percoll gradient procedure for preparation of synaptosomes. Nat Protoc 3:1718-1728.
21. Evans MS, Collings MA, Brewer GJ (1998) Electrophysiology of embryonic, adult and aged rat hippocampal neurons in serum-free culture. J Neurosci Methods 79:37-46. (Pubitemid 28248239)
22. Ferrándiz ML, Martínez M, De Juan E, Díez A, Bustos G, Miquel J (1994) Impairment of mitochondrial oxidative phosphorylation in the brain of aged mice. Brain Res 644:335-338. (Pubitemid 24127992)
23. Freund TF, Powell JF, Smith AD (1984) Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13:1189-1215. (Pubitemid 15198966)
24. 2+ concentration. Cell Calcium 30:311-321.
25. Gerencser AA, Nicholls DG (2008) Measurement of instantaneous velocity vectors of organelle transport: mitochondrial transport and bioenergetics in hippocampal neurons. Biophys J 95:3079-3099.
26. Gerencser AA, Doczi J, Töröcsik B, Bossy-Wetzel E, Adam-Vizi V (2008) Mitochondrial swelling measurement in situ by optimized spatial filtering: astrocyte-neuron differences. Biophys J 95:2583-2598.
27. Gerencser AA, Neilson A, Choi SW, Edman U, Yadava N, Oh RJ, Ferrick DA, Nicholls DG, Brand MD (2009) Quantitative microplate-based respirometry with correction for oxygen diffusion. Anal Chem 81:6868-6878.
28. 1 ATP synthase during aging. Possible involvement of oxygen free radicals. Ann N Y Acad Sci 786:62-71.
29. Hersch SM, Yi H, Heilman CJ, Edwards RH, Levey AI (1997) Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J Comp Neurol 388:211-227. (Pubitemid 27471497)
30. Joyce OJ, Farmer MK, Tipton KF, Porter RK (2003) Oxidative phosphorylation by in situ synaptosomal mitochondria from whole brain of young and old rats. J Neurochem 86:1032-1041. (Pubitemid 36992217)
31. 2 production and bioenergetics in rat brain synaptosomes. Biochim Biophys Acta 1777:783-788.
32. Kumar MJ, Nicholls DG, Andersen JK (2003) Oxidative alpha-ketoglutarate dehydrogenase inhibition via subtle elevations in monoamine oxidase B levels results in loss of spare respiratory capacity: implications for Parkinson's disease. J Biol Chem 278:46432-46439. (Pubitemid 37452214)
33. Liang CL, Wang TT, Luby-Phelps K, German DC (2007) Mitochondria mass is low in mouse substantia nigra dopamine neurons: implications for Parkinson's disease. Exp Neurol 203:370-380. (Pubitemid 46149588)
34. Mason JN, Farmer H, Tomlinson ID, Schwartz JW, Savchenko V, DeFelice LJ, Rosenthal SJ, Blakely RD (2005) Novel fluorescence-based approaches for the study of biogenic amine transporter localization, activity, and regulation. J Neurosci Methods 143:3-25. (Pubitemid 40348785)
35. 2+ receptors in single nerve terminals. J Biol Chem 277:47796-47803.
36. Miyazaki I, Asanuma M (2008) Dopaminergic neuron-specific oxidative stress caused by dopamine itself. Acta Med Okayama 62:141-150.
37. Mizuno Y, Ohta S, Tanaka M, Takamiya S, Suzuki K, Sato T, Oya H, Ozawa T, Kagawa Y (1989) Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem Biophys Res Commun 163:1450-1455. (Pubitemid 19244751)
38. Nicholls DG (2004) Mitochondrial membrane potential and aging. Aging Cell 3:35-40.
39. Nicholls DG (2006) Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J Biol Chem 281:14864-14874.
40. 3 receptor-induced increases in calcium levels in individual brain nerve terminals. J Neurochem 67:581-592.
41. Nirenberg MJ, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM (1996) The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J Neurosci 16:436-447. (Pubitemid 26028804)
42. Parihar MS, Brewer GJ (2007) Simultaneous age-related depolarization of mitochondrial membrane potential and increased mitochondrial reactive oxygen species production correlate with age-related glutamate excitotoxicity in rat hippocampal neurons. J Neurosci Res 85:1018-1032. (Pubitemid 46580343)
43. Peters A, Sethares C, Luebke JI (2008) Synapses are lost during aging in the primate prefrontal cortex. Neuroscience 152:970-981.
44. Rabinovic AD, Lewis DA, Hastings TG (2000) Role of oxidative changes in the degeneration of dopamine terminals after injection of neurotoxic levels of dopamine. Neuroscience 101:67-76.
45. Richardson JR, Caudle WM, Guillot TS, Watson JL, Nakamaru-Ogiso E, Seo BB, Sherer TB, Greenamyre JT, Yagi T, Matsuno-Yagi A, Miller GW (2007) Obligatory role for complex I inhibition in the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Toxicol Sci 95:196-204.
46. Schapira AH, Cooper JM, Dexter D, Jenner P, Clark JB, Marsden CD (1989) Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1:1269. (Pubitemid 19140359)
47. Scheff SW, DeKosky ST, Price DA (1990) Quantitative assessment of cortical synaptic density in Alzheimer's disease. Neurobiol Aging 11:29-37. (Pubitemid 20097857)
48. Shoffner JM, Watts RL, Juncos JL, Torroni A, Wallace DC (1991) Mitochondrial oxidative phosphorylation defects in Parkinson's disease. Ann Neurol 30:332-339.
49. Solmi R, Pallotti F, Rugolo M, Genova ML, Estornell E, Ghetti P, Pugnaloni A, Biagini G, Rizzoli C, Lenaz G (1994) Lack of major mitochondrial bioenergetic changes in cultured skin fibroblasts from aged individuals. Biochem Mol Biol Int 33:477-484. (Pubitemid 24212057)
50. Torres GE, Gainetdinov RR, Caron MG (2003) Plasma membrane monoamine transporters: structure, regulation and function. Nat Rev Neurosci 4:13-25. (Pubitemid 37271085)
51. Williams SM, Goldman-Rakic PS (1993) Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cereb Cortex 3:199-222. (Pubitemid 23184929)
52. 2+ channels. J Neurochem 55:303-310.