A Single Dopamine Pathway Underlies Progressive Locomotor Deficits in a Drosophila Model of Parkinson Disease

Cell Reports

Volumn 5, Issue 4, 2013, Pages 952-960

  Riemensperger, Thomas ^a,b   Issa, Abdul Raouf ^a   Pech, Ulrike ^b   Coulom, Hélène ^a   Nguyễn, Mỹ Vân ^a   Cassar, Marlène ^a   Jacquet, Mélanie ^a   Fiala, André ^b   Birman, Serge ^a  

^a CNRS   (France)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CLIMBING; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DROSOPHILA; FEMALE; HEMISPHERE; INNERVATION; KENYON CELL; MOTOR DYSFUNCTION; MUSHROOM BODY; NERVE CELL; NERVE FUNCTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STARTLE REFLEX;

BASIDIOMYCOTA;

ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; LOCOMOTION; MUSHROOM BODIES; OXIDATIVE STRESS; PARKINSON DISEASE; SIGNAL TRANSDUCTION; STARTLE REACTION; TRPC CATION CHANNELS;

EID: 84888436644     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.10.032     Document Type: Article

References (59)

1. Aso Y., Siwanowicz I., Bräcker L., Ito K., Kitamoto T., Tanimoto H. Specific dopaminergic neurons for the formation of labile aversive memory. Curr. Biol. 2010, 20:1445-1451.
2. Auluck P.K., Chan H.Y.E., Trojanowski J.Q., Lee V.M.Y., Bonini N.M. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 2002, 295:865-868.
3. Auluck P.K., Meulener M.C., Bonini N.M. Mechanisms of Suppression of {alpha}-Synuclein Neurotoxicity by Geldanamycin in Drosophila. J.Biol. Chem. 2005, 280:2873-2878.
4. Barone M.C., Sykiotis G.P., Bohmann D. Genetic activation of Nrf2 signaling is sufficient to ameliorate neurodegenerative phenotypes in a Drosophila model of Parkinson's disease. Dis. Model. Mech. 2011, 4:701-707.
5. Beninger R.J. The role of dopamine in locomotor activity and learning. Brain Res. 1983, 287:173-196.
6. Bushey D., Cirelli C. From genetics to structure to function: exploring sleep in Drosophila. Int. Rev. Neurobiol. 2011, 99:213-244.
7. Butler E.K., Voigt A., Lutz A.K., Toegel J.P., Gerhardt E., Karsten P., Falkenburger B., Reinartz A., Winklhofer K.F., Schulz J.B. The mitochondrial chaperone protein TRAP1 mitigates α-Synuclein toxicity. PLoS Genet. 2012, 8:e1002488.
8. Chaudhuri A., Bowling K., Funderburk C., Lawal H., Inamdar A., Wang Z., O'Donnell J.M. Interaction of genetic and environmental factors ina Drosophila parkinsonism model. J.Neurosci. 2007, 27:2457-2467.
9. Claridge-Chang A., Roorda R.D., Vrontou E., Sjulson L., Li H., Hirsh J., Miesenböck G. Writing memories with light-addressable reinforcement circuitry. Cell 2009, 139:405-415.
10. Cooper A.A., Gitler A.D., Cashikar A., Haynes C.M., Hill K.J., Bhullar B., Liu K., Xu K., Strathearn K.E., Liu F., et al. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006, 313:324-328.
11. Corti O., Lesage S., Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 2011, 91:1161-1218.
12. Coulom H., Birman S. Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J.Neurosci. 2004, 24:10993-10998.
13. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39:889-909.
14. Davis R.L. Traces of Drosophila memory. Neuron 2011, 70:8-19.
15. Devine M.J., Gwinn K., Singleton A., Hardy J. Parkinson's disease and α-synuclein expression. Mov. Disord. 2011, 26:2160-2168.
16. Dunnett S.B., Bentivoglio M., Bjorklund A., Hökfelt T. Dopamine, Volume 21 (Handbook of Chemical Neuroanatomy) 2005, Elsevier Science.
17. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
18. Feinberg E.H., Vanhoven M.K., Bendesky A., Wang G., Fetter R.D., Shen K., Bargmann C.I. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57:353-363.
19. Fiala A. Olfaction and olfactory learning in Drosophila: recent progress. Curr. Opin. Neurobiol. 2007, 17:720-726.
20. Forno L.S. Neuropathology of Parkinson's disease. J.Neuropathol. Exp. Neurol. 1996, 55:259-272.
21. Friggi-Grelin F., Coulom H., Meller M., Gomez D., Hirsh J., Birman S. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J.Neurobiol. 2003, 54:618-627.
22. Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 1996, 379:606-612.
23. Gordon M.D., Scott K. Motor control in a Drosophila taste circuit. Neuron 2009, 61:373-384.
24. Hamada F.N., Rosenzweig M., Kang K., Pulver S.R., Ghezzi A., Jegla T.J., Garrity P.A. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008, 454:217-220.
25. Heisenberg M. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 2003, 4:266-275.
26. Helfrich-Förster C., Wulf J., de Belle J.S. Mushroom body influence on locomotor activity and circadian rhythms in Drosophila melanogaster. J.Neurogenet. 2002, 16:73-109.
27. Hosamani R., Ramesh S.R., Muralidhara Attenuation of rotenone-induced mitochondrial oxidative damage and neurotoxicty in Drosophila melanogaster supplemented with creatine. Neurochem. Res. 2010, 35:1402-1412.
28. Howse P.E. Brain structure and behavior in insects. Annu. Rev. Entomol. 1975, 20:359-379.
29. Islam R., Yang L., Sah M., Kannan K., Anamani D., Vijayan C., Kwok J., Cantino M.E., Beal M.F., Fridell Y.-W.C. A neuroprotective role of the human uncoupling protein 2 (hUCP2) in a Drosophila Parkinson's disease model. Neurobiol. Dis. 2012, 46:137-146.
30. Kahsai L., Zars T. Learning and memory in Drosophila: behavior, genetics, and neural systems. Int. Rev. Neurobiol. 2011, 99:139-167.
31. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J.Neurobiol. 2001, 47:81-92.
32. Krashes M.J., Keene A.C., Leung B., Armstrong J.D., Waddell S. Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 2007, 53:103-115.
33. Lawal H.O., Chang H.-Y., Terrell A.N., Brooks E.S., Pulido D., Simon A.F., Krantz D.E. The Drosophila vesicular monoamine transporter reduces pesticide-induced loss of dopaminergic neurons. Neurobiol. Dis. 2010, 40:102-112.
34. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
35. Li H., Chaney S., Roberts I.J., Forte M., Hirsh J. Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr. Biol. 2000, 10:211-214.
36. Lim Y., Kehm V.M., Lee E.B., Soper J.H., Li C., Trojanowski J.Q., Lee V.M.-Y. α-Syn suppression reverses synaptic and memory defects in a mouse model of dementia with Lewy bodies. J.Neurosci. 2011, 31:10076-10087.
37. Liu G., Seiler H., Wen A., Zars T., Ito K., Wolf R., Heisenberg M., Liu L. Distinct memory traces for two visual features in the Drosophila brain. Nature 2006, 439:551-556.
38. Liu C., Plaçais P.-Y., Yamagata N., Pfeiffer B.D., Aso Y., Friedrich A.B., Siwanowicz I., Rubin G.M., Preat T., Tanimoto H. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 2012, 488:512-516.
39. Lundblad M., Decressac M., Mattsson B., Björklund A. Impaired neurotransmission caused by overexpression of α-synuclein in nigral dopamine neurons. Proc. Natl. Acad. Sci. USA 2012, 109:3213-3219.
40. Mao Z., Davis R.L. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 2009, 3:5.
41. Martin J.R., Ernst R., Heisenberg M. Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn. Mem. 1998, 5:179-191.
42. Nässel D.R., Elekes K. Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res. 1992, 267:147-167.
43. Pech U., Pooryasin A., Birman S., Fiala A. Localization of the contacts between Kenyon cells and aminergic neurons in the Drosophila melanogaster brain using splitGFP reconstitution. J.Comp. Neurol. 2013, 521:3992-4026.
44. Pech U., Dipt S., Barth J., Singh P., Jauch M., Thum A.S., Fiala A., Riemensperger T. Mushroom body miscellanea: transgenic Drosophila strains expressing anatomical and physiological sensor proteins in Kenyon cells. Front Neural Circuits 2013, 7:147.
45. Polymeropoulos M.H. Genetics of Parkinson's disease. Ann. N Y Acad. Sci. 2000, 920:28-32.
46. Riemensperger T., Völler T., Stock P., Buchner E., Fiala A. Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 2005, 15:1953-1960.
47. Riemensperger T., Isabel G., Coulom H., Neuser K., Seugnet L., Kume K., Iché-Torres M., Cassar M., Strauss R., Preat T., et al. Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proc. Natl. Acad. Sci. USA 2011, 108:834-839.
48. Rival T., Soustelle L., Strambi C., Besson M.-T., Iché M., Birman S. Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr. Biol. 2004, 14:599-605.
49. Ruta V., Datta S.R., Vasconcelos M.L., Freeland J., Looger L.L., Axel R. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 2010, 468:686-690.
50. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
51. Scott D.A., Tabarean I., Tang Y., Cartier A., Masliah E., Roy S. A pathologic cascade leading to synaptic dysfunction in alpha-synuclein-induced neurodegeneration. J.Neurosci. 2010, 30:8083-8095.
52. Serway C.N., Kaufman R.R., Strauss R., de Belle J.S. Mushroombodies enhance initial motor activity in Drosophila. J.Neurogenet. 2009, 23:173-184.
53. Shulman J.M., De Jager P.L., Feany M.B. Parkinson's disease: genetics and pathogenesis. Annu. Rev. Pathol. 2011, 6:193-222.
54. Tanaka N.K., Tanimoto H., Ito K. Neuronal assemblies of the Drosophila mushroom body. J.Comp. Neurol. 2008, 508:711-755.
55. Trinh K., Moore K., Wes P.D., Muchowski P.J., Dey J., Andrews L., Pallanck L.J. Induction of the phase II detoxification pathway suppresses neuron loss in Drosophila models of Parkinson's disease. J.Neurosci. 2008, 28:465-472.
56. Waddell S. Reinforcement signalling in Drosophila; dopamine does it all after all. Curr. Opin. Neurobiol. 2013, 23:324-329.
57. Yellman C., Tao H., He B., Hirsh J. Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila. Proc. Natl. Acad. Sci. USA 1997, 94:4131-4136.
58. Zars T., Fischer M., Schulz R., Heisenberg M. Localization of a short-term memory in Drosophila. Science 2000, 288:672-675.
59. Zhou Q.Y., Palmiter R.D. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 1995, 83:1197-1209.