Calcium entry and α-synuclein inclusions elevate dendritic mitochondrial oxidant stress in dopaminergic neurons

Journal of Neuroscience

Volumn 33, Issue 24, 2013, Pages 10154-10164

  Dryanovski, Dilyan I ^a   Guzman, Jaime N ^a   Xie, Zhong ^a   Galteri, Daniel J ^a   Volpicelli Daley, Laura A ^c   Lee, Virginia M Y ^c   Miller, Richard J ^a   Schumacker, Paul T ^b   James Surmeier, D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM CHANNEL L TYPE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM CONDUCTANCE; CALCIUM TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; DOPAMINERGIC NERVE CELL; EPIFLUORESCENCE MICROSCOPY; LASER MICROSCOPY; MOUSE; NEWBORN; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATIC CELL; SUBSTANTIA NIGRA PARS COMPACTA;

ACETYLCYSTEINE; ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITES; DOPAMINERGIC NEURONS; FREE RADICAL SCAVENGERS; GREEN FLUORESCENT PROTEINS; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; NG-NITROARGININE METHYL ESTER; OXIDATION-REDUCTION; OXIDATIVE STRESS; PATCH-CLAMP TECHNIQUES; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; STATISTICS, NONPARAMETRIC; TERT-BUTYLHYDROPEROXIDE; TYROSINE 3-MONOOXYGENASE;

EID: 84878892468     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5311-12.2013     Document Type: Article

References (39)

1. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313. CrossRef Medline
2. Bolam JP, Pissadaki EK (2012) Living on the edge with too many mouths to feed: why dopamine neurons die. Mov Disord 27:1478-1483. CrossRef Medline
3. Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 318:121-134. CrossRef Medline
4. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, Edling Y, Chan PH, Swanson RA (2009) NADPHoxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 12:857-863. CrossRef Medline
5. Cardozo DL (1993) Midbrain dopaminergic neurons from postnatal rat in long-term primary culture. Neuroscience 56:409-421. CrossRef Medline
6. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, Surmeier DJ (2007) 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447:1081-1086. CrossRef Medline
7. Choi DH, Cristóvão AC, Guhathakurta S, Lee J, Joh TH, Beal MF, KimYS (2012) NADPH oxidase 1-mediated oxidative stress leads to dopamine neuron death in Parkinson's disease. Antioxid Redox Signal 16:1033-1045. CrossRef Medline
8. Chu Y, Kordower JH (2007) Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: Is this the target for Parkinson's disease? Neurobiol Dis 25:134-149. CrossRef Medline
9. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, Spencer B, Masliah E, Lee SJ (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci U S A 106:13010-13015. CrossRef Medline
10. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, Iwatsubo T (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4:160-164. CrossRef Medline
11. Ghafourifar P, Cadenas E (2005) Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26:190-195. CrossRef Medline
12. Gohil VM, Sheth SA, Nilsson R, Wojtovich AP, Lee JH, Perocchi F, Chen W, Clish CB, Ayata C, Brookes PS, Mootha VK (2010) Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat Biotechnol 28:249-255. CrossRef Medline
13. Guo JL, Lee VM (2013) Neurofibrillary tangle-like tau pathology induced by synthetic tau fibrils in primary neurons over-expressing mutant tau. FEBS Lett 587:717-723. CrossRef Medline
14. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011-11019. CrossRef Medline
15. Guzman JN, Sánchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, Surmeier DJ (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468:696-700. CrossRef Medline
16. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279:13044-13053. CrossRef Medline
17. Hornykiewicz O (1966) Dopamine (3-hydroxytyramine) and brain function. Pharmacol Rev 18:925-964.Medline
18. Ivannikov MV, Sugimori M, Llinás RR (2010) Calcium clearance and its energy requirements in cerebellar neurons. Cell Calcium 47:507-513. CrossRef Medline
19. Khaliq ZM, Bean BP (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltagedependent sodium conductances. J Neurosci 30:7401-7413. CrossRef Medline
20. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM (2009) Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci U S A 106:20051-20056. CrossRef Medline
21. Marks JD, Boriboun C, Wang J (2005) Mitochondrial nitric oxide mediates decreased vulnerability of hippocampal neurons from immature animals to NMDA. J Neurosci 25:6561-6575. CrossRef Medline
22. Martin LJ, Pan Y, Price AC, Sterling W, Copeland NG, Jenkins NA, Price DL, Lee MK (2006) Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J Neurosci 26:41-50. CrossRef Medline
23. Masuko S, Nakajima S, Nakajima Y (1992) Dissociated high-purity dopaminergic neuron cultures from the substantia nigra and the ventral tegmental area of the postnatal rat. Neuroscience 49:347-364. CrossRef Medline
24. Mercuri NB, Bonci A, Calabresi P, Stratta F, Stefani A, Bernardi G (1994) Effects of dihydropyridine calcium antagonists on rat midbrain dopaminergic neurones. Br J Pharmacol 113:831-838. CrossRef Medline
25. Moore DJ, West AB, Dawson VL, Dawson TM (2005) Molecular pathophysiology of Parkinson's disease. Annu Rev Neurosci 28:57-87. CrossRef Medline
26. Nedergaard S, Flatman JA, Engberg I (1993) Nifedipine- and omegaconotoxin- sensitive Ca2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol 466:727-747.Medline
27. Neuhoff H, Neu A, Liss B, Roeper J (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22:1290-1302.Medline
28. Perrone-Capano C, Di Porzio U (2000) Genetic and epigenetic control of midbrain dopaminergic neuron development. Int J Dev Biol 44:679-687.Medline
29. Rayport S, Sulzer D, Shi WX, Sawasdikosol S, Monaco J, Batson D, Rajendran G (1992) Identified postnatal mesolimbic dopamine neurons in culture: morphology and electrophysiology. J Neurosci 12:4264-4280.Medline
30. Riederer P, Wuketich S (1976) Time course of nigrostriatal degeneration in parkinson's disease. A detailed study of influential factors in human brain amine analysis. J Neural Transm 38:277-301. CrossRef Medline
31. Rodríguez-Enríquez S, Juárez O, Rodríguez-Zavala JS, Moreno-Sánchez R (2001) Multisite control of the Crabtree effect in ascites hepatoma cells. Eur J Biochem 268:2512-2519. CrossRef Medline
32. Schapira AH (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol 7:97-109. CrossRef Medline
33. Schiavone S, Jaquet V, Sorce S, Dubois-Dauphin M, Hultqvist M, Bäckdahl Colaianna M, Cuomo V, Trabace L, Krause KH (2012) NADPH oxidase elevations in pyramidal neurons drive psychosocial stress-induced neuropathology. Transl Psychiatry 2:e111. CrossRef Medline
34. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388:839-840. CrossRef Medline
35. Sulzer D (2007) Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci 30:244-250. CrossRef Medline
36. Surmeier DJ, Guzman JN, Sánchez-Padilla J, Schumacker PT (2011) The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson's disease. Neuroscience 198:221-231. CrossRef Medline
37. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A, Meaney DF, Trojanowski JQ, Lee VM (2011) Exogenous alphasynuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72:57-71. CrossRef Medline
38. Wilson CJ, Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83:3084-3100.Medline
39. Wu JW, Herman M, Liu L, Simoes S, Acker CM, Figueroa H, Steinberg JI, Margittai M, Kayed R, Zurzolo C, Di Paolo G, Duff KE (2013) Small misfolded Tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J Biol Chem 288:1856-1870. CrossRef Medline