Loss of vesicular dopamine release precedes tauopathy in degenerative dopaminergic neurons in a Drosophila model expressing human tau

Acta Neuropathologica

Volumn 125, Issue 5, 2013, Pages 711-725

  Wu, Ting Han ^a   Lu, Yu Ning ^a   Chuang, Chia Lung ^a   Wu, Chia Lin ^b   Chiang, Ann Shyn ^a   Krantz, David E ^c   Chang, Hui Yun ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dopamine; MAPT; Neuron degeneration; Parkinson's disease; Tau; Tauopathy

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALKALINE PHOSPHATASE; CASPASE 3; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3BETA; TAU PROTEIN; VESICULAR MONOAMINE TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; FRUIT FLY MODEL; GENE OVEREXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MOLECULAR CLONING; MOLECULAR PATHOLOGY; MOLECULAR WEIGHT; MOTOR DYSFUNCTION; NERVE CELL; NERVE CELL DEGENERATION; NERVE ENDING; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SEROTONINERGIC NERVE CELL; SYNAPSE VESICLE; TAUOPATHY; WESTERN BLOTTING; AGE; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; DROSOPHILA; METABOLISM; MOTOR ACTIVITY; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; DROSOPHILA; HUMANS; MOTOR ACTIVITY; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; TAU PROTEINS; TAUOPATHIES; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84886684036     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1105-x     Document Type: Article

References (60)

1. Aso Y, Herb A, Ogueta M, Siwanowicz I, Templier T, Friedrich AB, Ito K, Scholz H, Tanimoto H (2012) Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet 8:e1002768
2. Benzer S (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Nat Acad Sci USA 58:1112- 1119
3. Berg I, Nilsson KP, Thor S, Hammarstrom P (2010) Efficient imaging of amyloid deposits in Drosophila models of human amyloidoses. Nat Protoc 5:935-944
4. Berry JA, Cervantes-Sandoval I, Nicholas EP, Davis RL (2012) Dopamine is required for learning and forgetting in Drosophila. Neuron 74:530-542
5. Binder LI, Guillozet-Bongaarts AL, Garcia-Sierra F, Berry RW (2005) Tau, tangles, and Alzheimer's disease. Biochim Biophys Acta 1739:216-223
6. Bonini NM, Fortini ME (2003) Human neurodegenerative disease modeling using Drosophila. Annu Rev Neurosci 26:627-656
7. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, Gohl D, Sillies M, Certel S, Waddell S (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433-437
8. Chang HY, Grygoruk A, Brooks ES, Ackerson LC, Maidment NT, Bainton RL, Krantz DE (2006) Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine. Mol Psychiatr 11:99-113
9. Chang HY, Ready DF (2000) Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 290:1978-1980
10. Chang YC, Hung WT, Chang YC, Chang HC, Wu CL, Chiang AS, Jackson GR, Sang TK (2011) Pathogenic VCP/TER94 alleles are dominant actives and contribute to neurodegeneration by altering cellular ATP level in a Drosophila IBMPFD model. PLoS Genet 7:e1001288
11. Conway KA, Rochet JC, Bieganski RM, Lansbury PT Jr (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294:1346-1349
12. Crowther RA (1991) Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc Nat Acad Sci USA 88:2288-2292
13. Dawson TM, Ko HS, Dawson VL (2010) Genetic animal models of Parkinson's disease. Neuron 66:646-661
14. de Calignon A, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT (2012) Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73:685-697
15. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086-1089
16. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, Beecham GW, Wang L, Zuchner S, Konidari I, Wang G, Singer C, Nahab F, Scott B, Stajich JM, Pericak-Vance M, Haines J, Vance JM, Martin E (2010) Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 74:97-109
17. Farrer M, Skipper L, Berg M, Bisceglio G, Hanson M, Hardy J, Adam A, Gwinn-Hardy K, Aasly J (2002) The tau H1 haplotype is associated with Parkinson's disease in the Norwegian population. Neurosci Lett 322:83-86
18. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612
19. Guillot TS, Miller GW (2009) Protective actions of the vesicular monoamine transporter 2 (VMAT2) in monoaminergic neurons. Mol Neurobiol 39:149-170
20. Hoglinger GU, Melhem NM, Dickson DW, Sleiman PM, Wang LS, Klei L, Rademakers R, de Silva R, Litvan I, Riley DE, van Swieten JC, Wszolek ZK, Uitti RJ, Vandrovcova J, Hurtig HI, Gross RG, Maetzler W, Goldwurm S, Tolosa E, Borroni B, Pastor P, Cantwell LB, Han MR, Dillman A, van der Brug MP, Gibbs JR, Cookson MR, Hernandez DG, Singleton AB, Farrer MJ, Yu CE, Golbe LI, Revesz T, Hardy J, Lees AJ, Devlin B, Hakonarson H, Muller U, Schellenberg GD (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet 43:699-705
21. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinicopathological study of 100 cases. J Neurol Neurosurg Psychiat 55:181-184
22. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 50-splicesite mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705
23. Jackson GR, Wiedau-Pazos M, Sang TK, Wagle N, Brown CA, Massachi S, Geschwind DH (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34:509-519
24. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD (2003) Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Nat Acad Sci USA 100:9980-9985
25. Kwok JB, Teber ET, Loy C, Hallupp M, Nicholson G, Mellick GD, Buchanan DD, Silburn PA, Schofield PR (2004) Tau haplotypes regulate transcription and are associated with Parkinson's disease. Ann Neurol 55:329-334
26. Lawal HO, Chang HY, Terrell AN, Brooks ES, Pulido D, Simon AF, Krantz DE (2010) The Drosophila vesicular monoamine transporter reduces pesticide-induced loss of dopaminergic neurons. Neurobiol Dis 40:102-112
27. Lee T, Luo L (2001) Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci 24:251-254
28. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159
29. Liu Y, Edwards RH (1997) The role of vesicular transport proteins in synaptic transmission and neural degeneration. Annu Rev Neurosci 20:125-156
30. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E (2003) Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging 24:1079-1085
31. Mao Z, Davis RL (2009) Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circ 3:5
32. Maraganore DM, de Andrade M, Lesnick TG, Strain KJ, Farrer MJ, Rocca WA, Pant PV, Frazer KA, Cox DR, Ballinger DG (2005) High-resolution whole-genome association study of Parkinson disease. Am J Hum Genet 77:685-693
33. Mershin A, Pavlopoulos E, Fitch O, Braden BC, Nanopoulos DV, Skoulakis EM (2004) Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn Mem 11:277-287
34. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195
35. Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, Schmitz Y, Krantz DE, Kobayashi K, Edwards RH, Sulzer D (2009) Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 62:218-229
36. Myers AJ, Pittman AM, Zhao AS, Rohrer K, Kaleem M, Marlowe L, Lees A, Leung D, McKeith IG, Perry RH, Morris CM, Trojanowski JQ, Clark C, Karlawish J, Arnold S, Forman MS, Van Deerlin V, de Silva R, Hardy J (2007) The MAPT H1c risk haplotype is associated with increased expression of tau and especially of 4 repeat containing transcripts. Neurobiol Dis 25:561-570
37. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, Nicoll RA, Edwards RH (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65:66-79
38. Pankratz N, Wilk JB, Latourelle JC, DeStefano AL, Halter C, Pugh EW, Doheny KF, Gusella JF, Nichols WC, Foroud T, Myers RH (2009) Genomewide association study for susceptibility genes contributing to familial Parkinson disease. Hum Genet 124:593-605
39. Qin H, Cressy M, Li W, Coravos JS, Izzi SA, Dubnau J (2012) Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr Biol 22:608-614
40. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A (2005) In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25:4766-4778
41. Riemensperger T, Isabel G, Coulom H, Neuser K, Seugnet L, Kume K, Iche-Torres M, Cassar M, Strauss R, Preat T, Hirsh J, Birman S (2011) Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proc Nat Acad Sci USA 108:834-839
42. Riemensperger T, Voller T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15:1953-1960
43. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerriere A, Vital A, Dumanchin C, Feuillette S, Brice A, Vercelletto M, Dubas F, Frebourg T, Campion D (2006) APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38:24-26
44. Sang TK, Chang HY, Lawless GM, Ratnaparkhi A, Mee L, Ackerson LC, Maidment NT, Krantz DE, Jackson GR (2007) A Drosophila model of mutant human parkin-induced toxicity demonstrates selective loss of dopaminergic neurons and dependence on cellular dopamine. J Neurosci 27:981-992
45. Shulman JM, De Jager PL, Feany MB (2011) Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol 6:193-222
46. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, Lichtner P, Scholz SW, Hernandez DG, Kruger R, Federoff M, Klein C, Goate A, Perlmutter J, Bonin M, Nalls MA, Illig T, Gieger C, Houlden H, Steffens M, Okun MS, Racette BA, Cookson MR, Foote KD, Fernandez HH, Schreiber S, Arepalli S, Zonozi R, Gwinn K, van der Brug M, Lopez G, Chanock SJ, Schatzkin A, Park Y, Hollenbeck A, Gao J, Huang X, Wood NW, Lorenz D, Deuschl G, Chen H, Riess O, Hardy JA, Singleton AB, Gasser T (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41:1308-1312
47. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302:841
48. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388:839-840
49. Steinhilb ML, Dias-Santagata D, Fulga TA, Felch DL, Feany MB (2007) Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol Biol Cell 18:5060-5068
50. Steinhilb ML, Dias-Santagata D, Mulkearns EE, Shulman JM, Biernat J, Mandelkow EM, Feany MB (2007) S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila. J Neurosci Res 85:1271-1278
51. Talmat-Amar Y, Arribat Y, Redt-Clouet C, Feuillette S, Bouge AL, Lecourtois M, Parmentier ML (2011) Important neuronal toxicity of microtubule-bound Tau in vivo in Drosophila. Hum Mol Genet 20:3738-3745
52. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A Sens Neural Behav Physiol 157:263-277
53. Varkey J, Chen P, Jemmerson R, Abrams JM (1999) Altered cytochrome c display precedes apoptotic cell death in Drosophila. J Cell Biol 144:701-710
54. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282
55. Williams-Gray CH, Evans JR, Goris A, Foltynie T, Ban M, Robbins TW, Brayne C, Kolachana BS, Weinberger DR, Sawcer SJ, Barker RA (2009) The distinct cognitive syndromes of Parkinson's disease: 5 year follow-up of the Campaign cohort. Brain 132:2958-2969
56. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293: 711-714
57. Wray S, Lewis PA (2010) A tangled web - tau and sporadic Parkinson's disease. Front Psychiat 1:150
58. Xu J, Kao SY, Lee FJ, Song W, Jin LW, Yankner BA (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med 8:600-606
59. Zabetian CP, Hutter CM, Factor SA, Nutt JG, Higgins DS, Griffith A, Roberts JW, Leis BC, Kay DM, Yearout D, Montimurro JS, Edwards KL, Samii A, Payami H (2007) Association analysis of MAPT H1 haplotype and subhaplotypes in Parkinson's disease. Ann Neurol 62:137-144
60. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, Stoessl AJ, Pfeiffer RF, Patenge N, Carbajal IC, Vieregge P, Asmus F, Muller-Myhsok B, Dickson DW, Meitinger T, Strom TM, Wszolek ZK, Gasser T (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44:601-607