Single-cell redox imaging demonstrates a distinctive response of dopaminergic neurons to oxidative insults

Antioxidants and Redox Signaling

Volumn 15, Issue 4, 2011, Pages 855-871

  Horowitz, Maxx P ^a,b,c   Milanese, Chiara ^c,d,e   Di Maio, Roberto ^c,d,e   Hu, Xiaoping ^c,d   Montero, Laura M ^c,d   Sanders, Laurie H ^c,d   Tapias, Victor ^c,d   Sepe, Sara ^f   Van Cappellen, Wiggert A ^g   Burton, Edward A ^b,c,d,h   Greenamyre, John Timothy ^b,c,d   Mastroberardino, Pier G ^c,d,g  

^a Medical Scientist Training Program   (United States)

^b Center for Neuroscience   (United States)

^c Department of Neurology ^*  (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e Fondazione RiMED   (Italy)

^f ROMA TRE UNIVERSITY   (Italy)

^g ERASMUS MEDICAL CENTER   (Netherlands)

^h VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; PROTEIN THIOL; ROTENONE; SUPEROXIDE; THIOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN NERVE CELL; CELLULAR STRESS RESPONSE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; HUMAN; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; LARVA; MAMMAL; MESENCEPHALON; MOLECULAR IMAGING; NERVE CELL CULTURE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SINGLE CELL REDOX IMAGING; SUBSTANTIA NIGRA PARS COMPACTA; VALIDATION STUDY; ZEBRA FISH;

ANIMALS; ASTROCYTES; BRAIN MAPPING; CELLS, CULTURED; DOPAMINE; IMMUNOHISTOCHEMISTRY; NEURONS; OXIDATION-REDUCTION; PARKINSON DISEASE; RATS; REACTIVE OXYGEN SPECIES; SINGLE-CELL ANALYSIS; SUBSTANTIA NIGRA; ZEBRAFISH;

DANIO RERIO; MAMMALIA;

EID: 79954631595     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2010.3629     Document Type: Article

References (64)

1. Adimora NJ, Jones DP, and Kemp ML. A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses. Antioxid Redox Signal 13: 731-743, 2010.
2. Alam M and Schmidt WJ. Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats. Behav Brain Res 136: 317-324, 2002. (Pubitemid 35246417)
3. Anantharam V, Lehrmann E, Kanthasamy A, Yang Y, Banerjee P, Becker KG, Freed WJ, and Kanthasamy AG. Microarray analysis of oxidative stress regulated genes in mesencephalic dopaminergic neuronal cells: relevance to oxidative damage in Parkinson's disease. Neurochem Int 50: 834-847, 2007. (Pubitemid 46722646)
4. Antunes F and Cadenas E. Estimation of H2O2 gradients across biomembranes. FEBS Lett 475: 121-126, 2000. (Pubitemid 30365063)
5. Avshalumov MV, Chen BT, Koó s T, Tepper JM, and Rice ME. Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive potassium channels. J Neurosci 25: 4222-4231, 2005. (Pubitemid 40628766)
6. Bai Q and Burton EA. Cis-acting elements responsible for dopaminergic neuron-specific expression of zebrafish slc6a3 (dopamine transporter) in vivo are located remote from the transcriptional start site. Neuroscience 164: 1138-1151, 2009.
7. Bai Q, Garver JA, Hukriede NA, and Burton EA. Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Res 35: 6501-6516, 2007. (Pubitemid 350111618)
8. Bean BP. The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465, 2007. (Pubitemid 46789230)
9. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, and Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3: 1301-1306, 2000.
10. Björklund A and Dunnett SB. Dopamine neuron systems in the brain: an update. Trends Neurosci 30: 194-202, 2007. (Pubitemid 46654237)
11. Bodhinathan K, Kumar A, and Foster TC. Intracellular redox state alters NMDA receptor response during aging through Ca2 +/calmodulin-dependent protein kinase II. J Neurosci 30: 1914-1924, 2010.
12. Bonci A, Grillner P, Mercuri NB, and Bernardi G. L-Type calcium channels mediate a slow excitatory synaptic transmission in rat midbrain dopaminergic neurons. J Neurosci 18: 6693-703, 1998. (Pubitemid 28388001)
13. Cai S-Q and Sesti F. Oxidation of a potassium channel causes progressive sensory function loss during aging. Nat Neurosci 12: 611-617, 2009.
14. Chan CS, Gertler TS, and Surmeier DJ. A molecular basis for the increased vulnerability of substantia nigra dopamine neurons in aging and Parkinson's disease. Mov Disord 25 Suppl 1: S63-S70, 2010.
15. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, and Surmeier DJ. "Rejuvenation" protects neurons in mouse models of Parkinson's disease. Nature 447: 1081-1086, 2007. (Pubitemid 47014425)
16. Coetzee WA, Nakamura TY, and Faivre JF. Effects of thiolmodifying agents on KATP channels in guinea pig ventricular cells. Am J Physiol 269: H1625-H1633, 1995. (Pubitemid 3005966)
17. Cross JV and Templeton DJ. Regulation of signal transduction through protein cysteine oxidation. Antioxid Redox Signal 8: 1819-1827, 2006. (Pubitemid 44726354)
18. Dawson TM, Mandir AS, and Lee MK. Animal models of PD: pieces of the same puzzle? Neuron 35: 219-222, 2002. (Pubitemid 34876725)
19. Fearnley JM and Lees AJ. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114 (Pt 5): 2283-2301, 1991.
20. Filomeni G and Ciriolo MR. Redox control of apoptosis: an update. Antioxid Redox Signal 8: 2187-2192, 2006. (Pubitemid 46489643)
21. Finkel T. Ageing: a toast to long life. Nature 425: 132-133, 2003.
22. Franco R and Cidlowski JA. SLCO/OATP-like transport of glutathione in FasL-induced apoptosis: glutathione efflux is coupled to an organic anion exchange and is necessary for the progression of the execution phase of apoptosis. J Biol Chem 281: 29542-29557, 2006. (Pubitemid 44536962)
23. Frank LE, Caldera-Siu AD, and Pothos EN. Primary dissociated midbrain dopamine cell cultures from rodent neonates. J Vis Exp (21): pii: 820, 2008.
24. Gamper N, Zaika O, Li Y, Martin P, Hernandez CC, Perez MR, Wang AYC, Jaffe DB, and Shapiro MS. Oxidative modification of M-type K( + ) channels as a mechanism of cytoprotective neuronal silencing. EMBO J 25: 4996-5004, 2006. (Pubitemid 44607043)
25. Grasbon-Frodl EM, Andersson A, and Brundin P. Lazaroid treatment prevents death of cultured rat embryonic mesencephalic neurons following glutathione depletion. J Neurochem 67: 1653-1660, 1996. (Pubitemid 26314223)
26. Gutscher M, Pauleau A-L, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, and Dick TP. Real-time imaging of the intracellular glutathione redox potential. Nat Methods 5: 553-559, 2008. (Pubitemid 351761764)
27. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, and Surmeier DJ. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468: 696-700, 2010.
28. Halliwell B. The antioxidant paradox. Lancet 355: 1179-1180, 2000. (Pubitemid 30172947)
29. Halliwell B and Gutteridge J. Free Radicals in Biology and Medicine. NewYork: OxfordUniversity Press, Inc., 2007, p. 704.
30. Hirsch E, Graybiel AM, and Agid YA. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334: 345-348, 1988.
31. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, and Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197, 2001. (Pubitemid 32118373)
32. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 53 Suppl 3: S26-S36; discussion S36-S38, 2003.
33. Jenner P and Olanow CW. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 47: S161-S170, 1996. (Pubitemid 26422582)
34. Johnson-Cadwell LI, Jekabsons MB, Wang A, Polster BM, and Nicholls DG. "Mild Uncoupling" does not decrease mitochondrial superoxide levels in cultured cerebellar granule neurons but decreases spare respiratory capacity and increases toxicity to glutamate and oxidative stress. J Neurochem 101: 1619-1631, 2007. (Pubitemid 46848858)
35. Kemp M, Go Y-M, and Jones DP. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 44: 921-937, 2008.
36. Kirlin WG, Cai J, Thompson SA, Diaz D, Kavanagh TJ, and Jones DP. Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic Biol Med 27: 1208-1218, 1999. (Pubitemid 30001481)
37. Langston JW, Ballard P, Tetrud JW, and Irwin I. Chronic Parkinsonism in humans due to a product of meperidineanalog synthesis. Science 219: 979-980, 1983. (Pubitemid 13189531)
38. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, and Jakob U. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci USA 105: 8197-8202, 2008. (Pubitemid 351904734)
39. Leichert LI and Jakob U. Protein thiol modifications visualized in vivo. PLoS Biol 2: e333, 2004.
40. Lin E, Cavanaugh JE, Leak RK, Perez RG, and Zigmond MJ. Rapid activation of ERK by 6-hydroxydopamine promotes survival of dopaminergic cells. J Neurosci Res 86: 108-117, 2008.
41. Lin T-K, Hughes G, Muratovska A, Blaikie FH, Brookes PS, Darley-Usmar V, Smith RAJ, and Murphy MP. Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach. J Biol Chem 277: 17048-17056, 2002. (Pubitemid 34967734)
42. Liss B, Bruns R, and Roeper J. Alternative sulfonylurea receptor expression defines metabolic sensitivity of K-ATP channels in dopaminergic midbrain neurons. EMBO J 18: 833-846, 1999. (Pubitemid 29082263)
43. Liss B, Haeckel O, Wildmann J, Miki T, Seino S, and Roeper J. K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons. Nat Neurosci 8: 1742-1751, 2005. (Pubitemid 41683203)
44. Liss B and Roeper J. Individual dopamine midbrain neurons: functional diversity and flexibility in health and disease. Brain Res Rev 58: 314-321, 2008.
45. Mastroberardino PG, Hoffman EK, Horowitz MP, Betarbet R, Taylor G, Cheng D, Na HM, Gutekunst C-A, Gearing M, Trojanowski JQ, Anderson M, Chu CT, Peng J, and Greenamyre JT. A novel transferrin/TfR2-mediated mitochondrial iron transport system is disrupted in Parkinson's disease. Neurobiol Dis 34: 417-431, 2009.
46. Mastroberardino PG, Orr AL, Hu X, Na HM, and Greenamyre JT. A FRET-based method to study protein thiol oxidation in histological preparations. Free Radic Biol Med 45: 971-981, 2008.
47. McCormack AL, Thiruchelvam M, Manning-Bog AB, Thiffault C, Langston JW, Cory-Slechta DA, and Di Monte DA. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol Dis 10: 119-127, 2002. (Pubitemid 34775465)
48. McCubrey JA, Lahair MM, and Franklin RA. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8: 1775-1789, 2006. (Pubitemid 44726351)
49. Meyer AJ and Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 13: 621-650, 2010.
50. Nagorni M and Hell SW. 4Pi-confocal microscopy provides three-dimensional images of the microtubule network with 100-to 150-nm resolution. J Struct Biol 123: 236-247, 1998. (Pubitemid 29048648)
51. Nakamura K, Wright DA, Wiatr T, Kowlessur D, Milstien S, Lei XG, and Kang UJ. Preferential resistance of dopaminergic neurons to the toxicity of glutathione depletion is independent of cellular glutathione peroxidase and is mediated by tetrahydrobiopterin. J Neurochem 74: 2305-2314, 2000. (Pubitemid 30314205)
52. Nedergaard S, Flatman JA, and Engberg I. Nifedipine-and omega-conotoxin-sensitive Ca2 + conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol (Lond) 466: 727-747, 1993. (Pubitemid 23225251)
53. Panov A, Dikalov S, Shalbuyeva N, Taylor G, Sherer T, and Greenamyre JT. Rotenone model of Parkinson disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J Biol Chem 280: 42026-42035, 2005. (Pubitemid 43023171)
54. Pignatelli A, Kobayashi K, Okano H, and Belluzzi O. Functional properties of dopaminergic neurones in the mouse olfactory bulb. J Physiol (Lond) 564: 501-514, 2005. (Pubitemid 40585049)
55. Puopolo M, Raviola E, and Bean BP. Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. J Neurosci 27: 645-656, 2007. (Pubitemid 46143768)
56. Rayport S, Sulzer D, Shi WX, Sawasdikosol S, Monaco J, Batson D, and Rajendran G. Identified postnatal mesolimbic dopamine neurons in culture: morphology and electrophysiology. J Neurosci 12: 4264-4280, 1992.
57. Requejo R, Hurd TR, Costa NJ, and Murphy MP. Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J 277: 1465-1480, 2010.
58. Rinne JO. Nigral degeneration in Parkinson's disease. Mov Disord 8 Suppl 1: S31-S5, 1993.
59. Schafer FQ and Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001. (Pubitemid 32463931)
60. Sherer TB, Betarbet R, Stout AK, Lund S, Baptista M, Panov AV, Cookson MR, and Greenamyre JT. An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J Neurosci 22: 7006-7015, 2002. (Pubitemid 35379158)
61. Toffa S, Kunikowska GM, Zeng BY, Jenner P, and Marsden CD. Glutathione depletion in rat brain does not cause nigrostriatal pathway degeneration. JNeural Transm104: 67-75, 1997. (Pubitemid 27073230)
62. Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549-561, 2008.
63. Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322-328, 1999. (Pubitemid 29395424)
64. Zhu J-H, Kulich SM, Oury TD, and Chu CT. Cytoplasmic aggregates of phosphorylated extracellular signal-regulated protein kinases in Lewy body diseases. Am J Pathol 161: 2087-2098, 2002. (Pubitemid 35434855)