Human disease models in drosophila melanogaster and the role of the fly in therapeutic drug discovery

Pharmacological Reviews

Volumn 63, Issue 2, 2011, Pages 411-436

  Pandey, Udai Bhan ^a   Nichols, Charles D ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 HYDROXY 2 DIPROPYLAMINOTETRALIN; ALPHA SYNUCLEIN; AMPHETAMINE; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; APOMORPHINE; ATYPICAL ANTIPSYCHOTIC AGENT; CARBAMAZEPINE; DOPAMINE RECEPTOR STIMULATING AGENT; ETHOSUXIMIDE; FRAGILE X MENTAL RETARDATION PROTEIN; GABAPENTIN; GAMMA SECRETASE INHIBITOR; GLUTAMINE; LAMOTRIGINE; PHENCYCLIDINE; PHENYTOIN; POTASSIUM BROMIDE; PRESENILIN; PRESENILIN INHIBITOR; PROTEIN INHIBITOR; PSYCHOTROPIC AGENT; RAS PROTEIN; SEROTONIN UPTAKE INHIBITOR; SHAKER POTASSIUM CHANNEL; UBIQUITIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID; VIGABATRIN;

ALZHEIMER DISEASE; ANTICONVULSANT ACTIVITY; ANTICONVULSANT THERAPY; ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; CARDIOVASCULAR DISEASE; CENTRAL NERVOUS SYSTEM DISEASE; COGNITION; COGNITIVE DEFECT; DEPRESSION; DIABETES MELLITUS; DISEASE MODEL; DROSOPHILA MELANOGASTER; DRUG ABSORPTION; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG EFFICACY; DRUG ELIMINATION; DRUG SCREENING; EMBRYO DEVELOPMENT; EPILEPSY; FLOW CYTOMETRY; FLY; FRAGILE X SYNDROME; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HIGH THROUGHPUT SCREENING; HUMAN; HUNTINGTON CHOREA; INFECTION; INFLAMMATORY DISEASE; KENNEDY DISEASE; LIFE CYCLE; LOSS OF FUNCTION MUTATION; MOLECULAR BIOLOGY; MOLECULAR GENETICS; MOOD DISORDER; NEOPLASM; NERVE DEGENERATION; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; ORGANOGENESIS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PSYCHOSIS; SCHIZOPHRENIA; SEIZURE; SIGNAL TRANSDUCTION; SLEEP; SLEEP DISORDER; STEADY STATE; TRIPLET REPEAT EXPANSION DISEASE; ZEBRA FISH;

ANIMALS; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DRUG DELIVERY SYSTEMS; DRUG DESIGN; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; SPECIES SPECIFICITY;

EID: 79955749505     PISSN: 00316997     EISSN: 15210081     Source Type: Journal    
DOI: 10.1124/pr.110.003293     Document Type: Article

References (277)

1. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
2. Akasaka T and Ocorr K (2009) Drug discovery through functional screening in the Drosophila heart. Methods Mol Biol 577:235-249.
3. Alayari NN, Vogler G, Taghli-Lamallem O, Ocorr K, Bodmer R and Cammarato A (2009) Fluorescent labeling of Drosophila heart structures. J Vis Exp doi:10.3791/1423.
4. Alekseyenko OV, Lee C, and Kravitz EA (2010) Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS ONE 5:e10806.
5. Andretic R, Kim YC, Jones FS, Han KA, and Greenspan RJ (2008) Drosophila D1 dopamine receptor mediates caffeine-induced arousal. Proc Natl Acad Sci USA 105:20392-20397.
6. Anichtchik O, Diekmann H, Fleming A, Roach A, Goldsmith P, and Rubinsztein DC (2008) Loss of PINK1 function affects development and results in neurodegeneration in zebrafish. J Neurosci 28:8199-8207.
7. Apostol BL, Kazantsev A, Raffioni S, Illes K, Pallos J, Bodai L, Slepko N, Bear JE, Gertler FB, Hersch S, et al. (2003) A cell-based assay for aggregation inhibitors as therapeutics of polyglutamine-repeat disease and validation in Drosophila. Proc Natl Acad Sci USA 100:5950-5955.
8. Arias AM (2008) Drosophila melanogaster and the development of biology in the 20th century. Methods Mol Biol 420:1-25.
9. Aritakula A and Ramasamy A (2008) Drosophila-based in vivo assay for the validation of inhibitors of the epidermal growth factor receptor/Ras pathway. J Biosci 33:731-742.
10. Auluck PK and Bonini NM (2002) Pharmacological prevention of Parkinson disease in Drosophila. Nat Med 8:1185-1186.
11. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, and Bonini NM (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865-868.
12. Avanesian A, Khodayari B, Felgner JS, and Jafari M (2010) Lamotrigine extends lifespan but compromises health span in Drosophila melanogaster. Biogerontology 11:45-52.
13. Bainton RJ, Tsai LT, Singh CM, Moore MS, Neckameyer WS, and Heberlein U (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10:187-194.
14. Baker KD and Thummel CS (2007) Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab 6:257-266.
15. Bandmann O and Burton EA (2010) Genetic zebrafish models of neurodegenerative diseases. Neurobiol Dis 40:58-65.
16. Batlevi Y, Martin DN, Pandey UB, Simon CR, Powers CM, Taylor JP, and Baehrecke EH (2010) Dynein light chain 1 is required for autophagy, protein clearance, and cell death in Drosophila. Proc Natl Acad Sci USA 107:742-747.
17. Bellen HJ, Tong C, and Tsuda H (2010) 100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future. Nat Rev Neurosci 11:514-522.
18. Benzer S (1971) From the gene to behavior. JAMA 218:1015-1022.
19. Bina S, Wright VM, Fisher KH, Milo M, and Zeidler MP (2010) Transcriptional targets of Drosophila JAK/STAT pathway signalling as effectors of haematopoietic tumour formation. EMBO Rep 11:201-207.
20. Blard O, Feuillette S, Bou J, Chaumette B, Frébourg T, Campion D, and Lecourtois M (2007) Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum Mol Genet 16:555-566.
21. Bonifati V, Rizzu P, Squitieri F, Krieger E, Vanacore N, van Swieten JC, Brice A, van Duijn CM, Oostra B, Meco G, et al. (2003) DJ-1(PARK7), a novel gene for autosomal recessive, early onset parkinsonism. Neurol Sci 24:159-160.
22. Bradu A, Ma L, Bloor JW, and Podoleanu A (2009) Dual optical coherence tomography/fluorescence microscopy for monitoring of Drosophila melanogaster larval heart. J Biophotonics 2:380-388.
23. Brand AH and Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
24. Branson K, Robie AA, Bender J, Perona P, and Dickinson MH (2009) Highthroughput ethomics in large groups of Drosophila. Nat Methods 6:451-457.
25. Braun T and Woollard A (2009) RUNX factors in development: lessons from invertebrate model systems. Blood Cells Mol Dis 43:43-48.
26. Brignull HR, Moore FE, Tang SJ, and Morimoto RI (2006) Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. J Neurosci 26:7597-7606.
27. Bryantsev AL and Cripps RM (2009) Cardiac gene regulatory networks in Drosophila. Biochim Biophys Acta 1789:343-353.
28. Cagan RL and Ready DF (1989) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346-362.
29. Cao P, Yuan Y, Pehek EA, Moise AR, Huang Y, Palczewski K, and Feng Z (2010) Alpha-synuclein disrupted dopamine homeostasis leads to dopaminergic neuron degeneration in Caenorhabditis elegans. PLoS One 5:e9312.
30. C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012-2018.
31. Cha GH, Kim S, Park J, Lee E, Kim M, Lee SB, Kim JM, Chung J, and Cho KS (2005) Parkin negatively regulates JNK pathway in the dopaminergic neurons of Drosophila. Proc Natl Acad Sci USA 102:10345-10350.
32. Chang S, Bray SM, Li Z, Zarnescu DC, He C, Jin P, and Warren ST (2008) Identification of small molecules rescuing fragile X syndrome phenotypes in Drosophila. Nat Chem Biol 4:256-263.
33. Chee FC, Mudher A, Cuttle MF, Newman TA, MacKay D, Lovestone S, and Shepherd D (2005) Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Neurobiol Dis 20:918-928.
34. Chen X, Li Y, Huang J, Cao D, Yang G, Liu W, Lu H, and Guo A (2007) Study of tauopathies by comparing Drosophila and human tau in Drosophila. Cell Tissue Res 329:169-178.
35. Chen YC, Cheng CH, Chen GD, Hung CC, Yang CH, Hwang SP, Kawakami K, Wu BK, and Huang CJ (2009) Recapitulation of zebrafish sncga expression pattern and labeling the habenular complex in transgenic zebrafish using green fluorescent protein reporter gene. Dev Dyn 238:746-754.
36. Choma MA, Izatt SD, Wessells RJ, Bodmer R, and Izatt JA (2006) Images in cardiovascular medicine: in vivo imaging of the adult Drosophila melanogaster heart with real-time optical coherence tomography. Circulation 114:e35-e36.
37. Choi CH, McBride SM, Schoenfeld BP, Liebelt DA, Ferreiro D, Ferrick NJ, Hinchey P, Kollaros M, Rudominer RL, Terlizzi AM, et al. (2010) Age-dependent cognitive impairment in a Drosophila fragile X model and its pharmacological rescue. Biogerontology 11:347-362.
38. Christofori G and Semb H (1999) The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci 24:73-76.
39. Chung BY, Kilman VL, Keath JR, Pitman JL, and Allada R (2009) The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 19:386-390.
40. Cirelli C (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci 10:549-560.
41. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, and Tononi G (2005) Reduced sleep in Drosophila Shaker mutants. Nature 434:1087-1092.
42. Cooper AS, Rymond KE, Ward MA, Bocook EL, and Cooper RL (2009) Monitoring heart function in larval Drosophila melanogaster for physiological studies. J Vis Exp doi: 10.3791/1596.
43. Coulom H and Birman S (2004) Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J Neurosci 24:10993-10998.
44. Crowther DC, Kinghorn KJ, Miranda E, Page R, Curry JA, Duthie FA, Gubb DC, and Lomas DA (2005) Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer's disease. Neuroscience 132:123-135.
45. Dankert H, Wang L, Hoopfer ED, Anderson DJ, and Perona P (2009) Automated monitoring and analysis of social behavior in Drosophila. Nat Methods 6:297-303.
46. Dasari S and Cooper RL (2006) Direct influence of serotonin on the larval heart of Drosophila melanogaster. J Comp Physiol B 176:349-357.
47. Dasari S, Viele K, Turner AC, and Cooper RL (2007) Influence of PCPA and MDMA (ecstasy) on physiology, development and behavior in Drosophila melanogaster. Eur J Neurosci 26:424-438.
48. Davis RL (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 28:275-302.
49. Desai UA, Pallos J, Ma AA, Stockwell BR, Thompson LM, Marsh JL, and Diamond MI (2006) Biologically active molecules that reduce polyglutamine aggregation and toxicity. Hum Mol Genet 15:2114-2124.
50. DiAngelo JR and Birnbaum MJ (2009) Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol Cell Biol 29:6341-6352.
51. Dierick HA and Greenspan RJ (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39:678-682.
52. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156.
53. Dockendorff TC, Su HS, McBride SM, Yang Z, Choi CH, Siwicki KK, Sehgal A, and Jongens TA (2002) Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34:973-984.
54. Drake J, Link CD, and Butterfield DA (2003) Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid beta-peptide (1-42) in a transgenic Caenorhabditis elegans model. Neurobiol Aging 24:415-520.
55. Draper I, Kurshan PT, McBride E, Jackson FR, and Kopin AS (2007) Locomotor activity is regulated by D2-like receptors in Drosophila: an anatomic and functional analysis. Dev Neurobiol 67:378-393.
56. Dzitoyeva S, Dimitrijevic N, and Manev H (2003) Gamma-aminobutyric acid B receptor 1 mediates behavior-impairing actions of alcohol in Drosophila: adult RNA interference and pharmacological evidence. Proc Natl Acad Sci USA 100: 5485-5490.
57. Evans PD and Maqueira B (2005) Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5:111-118.
58. Faber PW, Alter JR, MacDonald ME, and Hart AC (1999) Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc Natl Acad Sci USA 96:179-184.
59. Fay DS, Fluet A, Johnson CJ, and Link CD (1998) In vivo aggregation of betaamyloid peptide variants. J Neurochem 71:1616-1625.
60. Feany MB and Bender WW (2000) A Drosophila model of Parkinson's disease. Nature 404:394-398.
61. Ferrandon D, Imler JL, Hetru C, and Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862-874.
62. Feuillette S, Miguel L, Frébourg T, Campion D, and Lecourtois M (2010) Drosophila models of human tauopathies indicate that Tau protein toxicity in vivo is mediated by soluble cytosolic phosphorylated forms of the protein. J Neurochem 113:895-903.
63. Finelli A, Kelkar A, Song HJ, Yang H, and Konsolaki M (2004) A model for studying Alzheimer's Abeta42-induced toxicity in Drosophila melanogaster. Mol Cell Neurosci 26:365-375.
64. Flinn L, Mortiboys H, Volkmann K, Köster RW, Ingham PW, and Bandmann O (2009) Complex I deficiency and dopaminergic neuronal cell loss in parkindeficient zebrafish (Danio rerio). Brain 132:1613-1623.
65. Foltenyi K, Andretic R, Newport JW, and Greenspan RJ (2007) Neurohormonal and neuromodulatory control of sleep in Drosophila. Cold Spring Harb Symp Quant Biol 72:565-571.
66. Franceschini N and Kirschfeld K (1971) Pseudopupil phenomena in the compound eye of drosophila. Kybernetik 9:159-182.
67. Furukubo-Tokunaga K (2009) Modeling schizophrenia in flies. Prog Brain Res 179: 107-115.
68. Ganetzky B and Wu CF (1982) Indirect suppression involving behavioral mutants with altered nerve excitability in Drosophila melanogaster. Genetics 100:597-614.
69. Geyer MA (2008) Developing translational animal models for symptoms of schizophrenia or bipolar mania. Neurotox Res 14:71-78.
70. Giasson BI and Lee VM (2003) Are ubiquitination pathways central to Parkinson's disease? Cell 114:1-8.
71. Goldenberg MM (2010) Overview of drugs used for epilepsy and seizures: etiology, diagnosis, and treatment. P T 35:392-415.
72. Gordon P, Hingula L, Krasny ML, Swienckowski JL, Pokrywka NJ, and Raley-Susman KM (2008) The invertebrate microtubule-associated protein PTL-1 functions in mechanosensation and development in Caenorhabditis elegans. Dev Genes Evol 218:541-551.
73. Gosai SJ, Kwak JH, Luke CJ, Long OS, King DE, Kovatch KJ, Johnston PA, Shun TY, Lazo JS, Perlmutter DH, et al. (2010) Automated high-content live animal drug screening using C. elegans expressing the aggregation prone serpin 1-antitrypsin Z. PLoS One 5:e15460.
74. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, and Pallanck LJ (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci USA 100:4078-4083.
75. Greenspan RJ (2008) The origins of behavioral genetics. Curr Biol 18:R192-R198.
76. Grosjean Y, Grillet M, Augustin H, Ferveur JF, and Featherstone DE (2008) A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nat Neurosci 11:54-61.
77. Gu H and O'Dowd DK (2006) Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J Neurosci 26:265-272.
78. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, Gordesky-Gold B, Sintasath L, Bonini NM, and Goldstein LS (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40:25-40.
79. Hamamichi S, Rivas RN, Knight AL, Cao S, Caldwell KA, and Caldwell GA (2008) Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model. Proc Natl Acad Sci USA 105:728-733.
80. Hamasaka Y, Rieger D, Parmentier ML, Grau Y, Helfrich-Förster C, and Nässel DR (2007) Glutamate and its metabotropic receptor in Drosophila clock neuron circuits. J Comp Neurol 505:32-45.
81. Hamasaka Y, Wegener C, and Nässel DR (2005) GABA modulates Drosophila circadian clock neurons via GABAB receptors and decreases in calcium. J Neurobiol 65:225-240.
82. Harrington AJ, Hamamichi S, Caldwell GA, and Caldwell KA (2010) C. elegans as a model organism to investigate molecular pathways involved with Parkinson's disease. Dev Dyn 239:1282-1295.
83. Haselton AT and Fridell YW (2010) Adult Drosophila melanogaster as a model for the study of glucose homeostasis. Aging 2:523-526.
84. Hassan WM, Merin DA, Fonte V, and Link CD (2009) AIP-1 ameliorates betaamyloid peptide toxicity in a Caenorhabditis elegans Alzheimer's disease model. Hum Mol Genet 18:2739-2747.
85. Hattori N and Mizuno Y (2004) Pathogenetic mechanisms of parkin in Parkinson's disease. Lancet 364:722-724.
86. Haywood AF and Staveley BE (2004) Parkin counteracts symptoms in a Drosophila model of Parkinson's disease. BMC Neurosci 5:14.
87. Heiser V, Engemann S, Bröcker W, Dunkel I, Boeddrich A, Waelter S, Nordhoff E, Lurz R, Schugardt N, Rautenberg S, et al. (2002) Identification of benzothiazoles as potential polyglutamine aggregation inhibitors of Huntington's disease by using an automated filter retardation assay. Proc Natl Acad Sci USA 99:16400-16406.
88. Hendricks JC, Kirk D, Panckeri K, Miller MS, and Pack AI (2003) Modafinil maintains waking in the fruit fly drosophila melanogaster. Sleep 26:139-146.
89. Henshall TL, Tucker B, Lumsden AL, Nornes S, Lardelli MT, and Richards RI (2009) Selective neuronal requirement for huntingtin in the developing zebrafish. Hum Mol Genet 18:4830-4842.
90. Hetru C and Hoffmann JA (2009) NF-kappaB in the immune response of Drosophila. Cold Spring Harb Perspect Biol 1:a000232.
91. Hirsh J, Riemensperger T, Coulom H, Iché M, Coupar J, and Birman S (2010) Roles of dopamine in circadian rhythmicity and extreme light sensitivity of circadian entrainment. Curr Biol 20:209-214.
92. Hirota T, Lee JW, Lewis WG, Zhang EE, Breton G, Liu X, Garcia M, Peters EC, Etchegaray JP, Traver D, et al. (2010) High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIα as a clock regulatory kinase. PLoS Biol 8:e1000559.
93. Hockly E, Tse J, Barker AL, Moolman DL, Beunard JL, Revington AP, Holt K, Sunshine S, Moffitt H, Sathasivam K, et al. (2006) Evaluation of the benzothiazole aggregation inhibitors riluzole and PGL-135 as therapeutics for Huntington's disease. Neurobiol Dis 21:228-236.
94. Hornsten A, Lieberthal J, Fadia S, Malins R, Ha L, Xu X, Daigle I, Markowitz M, O'Connor G, Plasterk R, et al. (2007) APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proc Natl Acad Sci USA 104:1971-1976.
95. Horowitz A and Simons M (2008) Branching morphogenesis. Circ Res 103:784-795.
96. Humbert PO, Grzeschik NA, Brumby AM, Galea R, Elsum I, and Richardson HE (2008) Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27:6888-6907.
97. Ibáñez P, Bonnet AM, Débarges B, Lohmann E, Tison F, Pollak P, Agid Y, Dürr A, and Brice A (2004) Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 364:1169-1171.
98. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, and Benzer S (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci USA 104:8253-8256.
99. Jackson GR, Wiedau-Pazos M, Sang TK, Wagle N, Brown CA, Massachi S, and Geschwind DH (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34: 509-519.
100. Januschke J and Gonzalez C (2008) Drosophila asymmetric division, polarity and cancer. Oncogene 27:6994-7002.
101. Jiang H, Jiang Q, and Feng J (2004) Parkin increases dopamine uptake by enhancing the cell surface expression of dopamine transporter. J Biol Chem 279:54380-54386.
102. Jin P, Duan R, Qurashi A, Qin Y, Tian D, Rosser TC, Liu H, Feng Y, and Warren ST (2007) Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome. Neuron 55:556-564.
103. Johnson O, Becnel J, and Nichols CD (2008) Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158:1292-1300.
104. Johnson O, Becnel J, and Nichols CD (2009) Serotonin 5-HT1A-like, 5-HT2, and 5-HT7 receptors modulate learning and memory in drosophila. 50th Annual Drosophila Research Conference; 4-8 Mar 2009; Chicago IL. Abstract 599B. The Genetics Society of America, Bethesda, MD.
105. Joshi P, Liang JO, DiMonte K, Sullivan J, and Pimplikar SW (2009) Amyloid precursor protein is required for convergent-extension movements during Zebrafish development. Dev Biol 335:1-11.
106. Kaplan DD, Zimmermann G, Suyama K, Meyer T, and Scott MP (2008) A nucleostemin family GTPase, NS3, acts in serotonergic neurons to regulate insulin signaling and control body size. Genes Dev 22:1877-1893.
107. Karpinar DP, Balija MB, Kügler S, Opazo F, Rezaei-Ghaleh N, Wender N, Kim HY, Taschenberger G, Falkenburger BH, Heise H, et al. (2009) Pre-fibrillar alphasynuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models. EMBO J 28:3256-3268.
108. Kauppila S, Maaty WS, Chen P, Tomar RS, Eby MT, Chapo J, Chew S, Rathore N, Zachariah S, Sinha SK, et al. (2003) Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 22:4860-4867.
109. Kim IM, Wolf MJ, and Rockman HA (2010) Gene deletion screen for cardiomyopathy in adult Drosophila identifies a new notch ligand. Circ Res 106:1233-1243.
110. Kim SK and Rulifson EJ (2004) Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:316-320.
111. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, and Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392:605-608.
112. Koh K, Evans JM, Hendricks JC, and Sehgal A (2006) A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci USA 103:13843-13847.
113. Koh K, Joiner WJ, Wu MN, Yue Z, Smith CJ, and Sehgal A (2008) Identification of SLEEPLESS, a sleep promoting factor. Science 321:372-376.
114. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, and Schellenberg GD (2003) Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci USA 100:9980-9985.
115. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, and Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416-427.
116. Krogsgaard-Larsen P, Frølund B, and Frydenvang K (2000) GABA uptake inhibitors. Design, molecular pharmacology and therapeutic aspects. Curr Pharm Des 6:1193-1209.
117. Krüger R, Kuhn W, Müller T, Woitalla D, Graeber M, Kösel S, Przuntek H, Epplen JT, 1998 Ala30Pro mutation in the gene encoding alphasynuclein in Parkinson's disease. Nat Genet 18:106-108.
118. Kuebler D and Tanouye MA (2000) Modifications of seizure susceptibility in Drosophila. J Neurophysiol 83:998-1009.
119. Kuklinski NJ, Berglund EC, and Ewing AG (2010) Micellar capillary electrophoresis-electrochemical detection of neurochemicals from Drosophila. J Sep Sci 33: 388-393.
120. Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1-28.
121. Kuwahara T, Koyama A, Gengyo-Ando K, Masuda M, Kowa H, Tsunoda M, Mitani S, and Iwatsubo T (2006) Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans. J Biol Chem 281:334-340.
122. Kuwahara T, Koyama A, Koyama S, Yoshina S, Ren CH, Kato T, Mitani S, and Iwatsubo T (2008) A systematic RNAi screen reveals involvement of endocytic pathway in neuronal dysfunction in alpha-synuclein transgenic C. elegans. Hum Mol Genet 17:2997-3009.
123. La Spada AR and Taylor JP (2010) Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat Rev Genet 11:247-258.
124. La Spada AR and Taylor JP (2003) Polyglutamines placed into context. Neuron 38:681-684.
125. Lacomblez L, Bensimon G, Leigh PN, Guillet P, and Meininger V (1996) Doseranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet 347:1425-1431.
126. Lakso M, Vartiainen S, Moilanen AM, Sirviö J, Thomas JH, Nass R, Blakely RD, and Wong G (2003) Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J Neurochem 86:165-172.
127. Langheinrich U (2003) Zebrafish: a new model on the pharmaceutical catwalk. Bioessays 25:904-912.
128. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC, Han KA, Wolf FW, Perona P, and Anderson DJ (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522-536.
129. Lee J and Wu CF (2002) Electroconvulsive seizure behavior in Drosophila: analysis of the physiological repertoire underlying a stereotyped action pattern in bangsensitive mutants. J Neurosci 22:11065-11079.
130. Lesage S, Dürr A, Tazir M, Lohmann E, Leutenegger AL, Janin S, Pollak P, Brice A, and French Parkinson's Disease Genetics Study Group (2006) LRRK2 G2019S as a cause of Parkinson's disease in North African Arabs. N Engl J Med 354:422-423.
131. Link CD (1995) Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc Natl Acad Sci USA 92:9368-9372.
132. Link CD, Johnson CJ, Fonte V, Paupard M, Hall DH, Styren S, Mathis CA, and Klunk WE (2001) Visualization of fibrillar amyloid deposits in living, transgenic Caenorhabditis elegans animals using the sensitive amyloid dye, X-34. Neurobiol Aging 22:217-226.
133. Liu L, Johnson WA, and Welsh MJ (2003) Drosophila DEG/ENaC pickpocket genes are expressed in the tracheal system, where they may be involved in liquid clearance. Proc Natl Acad Sci USA 100:2128-2133.
134. Liu X, Krause WC, and Davis RL (2007) GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 56:1090-1102.
135. Lloyd TE and Taylor JP (2010) Flightless flies: Drosophila models of neuromuscular disease. Ann NY Acad Sci 1184:e1-e20.
136. Luheshi LM, Tartaglia GG, Brorsson AC, Pawar AP, Watson IE, Chiti F, Vendruscolo M, Lomas DA, Dobson CM, and Crowther DC (2007) Systematic in vivo analysis of the intrinsic determinants of amyloid beta pathogenicity. PLoS Biol 5:e290.
137. Lumsden AL, Henshall TL, Dayan S, Lardelli MT, and Richards RI (2007) Huntingtin-deficient zebrafish exhibit defects in iron utilization and development. Hum Mol Genet 16:1905-1920.
138. Luo L, Tully T, and White K (1992) Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9:595-605.
139. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, et al. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87:493-506.
140. Margulies C, Tully T, and Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15:R700-R713.
141. Marvanova M and Nichols CD (2007) Identification of neuroprotective compounds of caenorhabditis elegans dopaminergic neurons against 6-OHDA. J Mol Neurosci 31:127-137.
142. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, and Bainton RJ (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29:3538-3550.
143. McClung C and Hirsh J (1998) Stereotypic behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Curr Biol 8:109-112.
144. McGuire SE, Roman G, and Davis RL (2004) Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet 20:384-391.
145. Meeker ND and Trede NS (2008) Immunology and zebrafish: spawning new models of human disease. Dev Comp Immunol 32:745-757.
146. Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO, and Sherman MY (2002) Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157:997-1004.
147. Micchelli CA and Perrimon N (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475-479.
148. Micchelli CA, Esler WP, Kimberly WT, Jack C, Berezovska O, Kornilova A, Hyman BT, Perrimon N, and Wolfe MS (2003) Gamma-secretase/presenilin inhibitors for Alzheimer's disease phenocopy Notch mutations in Drosophila. FASEB J 17:79-81.
149. Miyasaka T, Ding Z, Gengyo-Ando K, Oue M, Yamaguchi H, Mitani S, and Ihara Y (2005) Progressive neurodegeneration in C. elegans model of tauopathy. Neurobiol Dis 20:372-383.
150. Moffatt MF, Kabesch M, Liang L, Dixon AL, Strachan D, Heath S, Depner M, von Berg A, Bufe A, Rietschel E, et al. (2007) Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448:470-473.
151. Molina GA, Watkins SC, and Tsang M (2007) Generation of FGF reporter transgenic zebrafish and their utility in chemical screens. BMC Dev Biol 7:62.
152. Montell C (2005) The TRP superfamily of cation channels. Sci STKE (272):re3.
153. Moore DJ, Zhang L, Troncoso J, Lee MK, Hattori N, Mizuno Y, Dawson TM, and Dawson VL (2005) Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum Mol Genet 14:71-84.
154. Moore MS, DeZazzo J, Luk AY, Tully T, Singh CM, and Heberlein U (1998) Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93:997-1007.
155. Morales J, Hiesinger PR, Schroeder AJ, Kume K, Verstreken P, Jackson FR, Nelson DL, and Hassan BA (2002) Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34:961-972.
156. Mudher A, Shepherd D, Newman TA, Mildren P, Jukes JP, Squire A, Mears A, Drummond JA, Berg S, MacKay D, et al. (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol Psychiatry 9:522-530.
157. Nagaraj R and Banerjee U (2004) The little R cell that could. Int J Dev Biol 48:755-760.
158. Nasonkin I, Alikasifoglu A, Ambrose C, Cahill P, Cheng M, Sarniak A, Egan M, and Thomas PM (1999) A novel sulfonylurea receptor family member expressed in the embryonic Drosophila dorsal vessel and tracheal system. J Biol Chem 274:29420-29425.
159. Nass R, Hahn MK, Jessen T, McDonald PW, Carvelli L, and Blakely RD (2005) A genetic screen in Caenorhabditis elegans for dopamine neuron insensitivity to 6-hydroxydopamine identifies dopamine transporter mutants impacting transporter biosynthesis and trafficking. J Neurochem 94:774-785.
160. Nass R, Hall DH, Miller DM 3rd, and Blakely RD (2002) Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci USA 99:3264-3269.
161. Nässel DR and Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42-104.
162. Neckameyer WS, Coleman CM, Eadie S, and Goodwin SF (2007) Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster. Genes Brain Behav 6:756-769.
163. Neckameyer WS (2010) A trophic role for serotonin in the development of a simple feeding circuit. Dev Neurosci 32:217-237.
164. Nedelsky NB, Pennuto M, Smith RB, Palazzolo I, Moore J, Nie Z, Neale G, and Taylor JP (2010) Native functions of the androgen receptor are essential to pathogenesis in a Drosophila model of spinobulbar muscular atrophy. Neuron 67:936-952.
165. Neely GG, Kuba K, Cammarato A, Isobe K, Amann S, Zhang L, Murata M, Elmén L, Gupta V, Arora S, et al. (2010) A global in vivo Drosophila RNAi screen identifies NOT3 as a conserved regulator of heart function. Cell 141:142-153.
166. Nestler EJ and Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161-1169.
167. Newman M, Verdile G, Martins RN, and Lardelli M (2011) Zebrafish as a tool in Alzheimer's disease research. Biochim Biophys Acta 1812:346-352.
168. Nichols CD (2006) Drosophila melanogaster neurobiology, neuropharmacology, and how the fly can inform central nervous system drug discovery. Pharmacol Ther 112:677-700.
169. Nichols CD (2007) 5-HT2 receptors in Drosophila are expressed in the brain and modulate aspects of circadian behaviors. Dev Neurobiol 67:752-763.
170. Nichols CD and Sanders-Bush E (2002) A single dose of lysergic acid diethylamide influences gene expression patterns within the mammalian brain. Neuropsychopharmacology 26:634-642.
171. Nichols CD, Ronesi J, Pratt W, and Sanders-Bush E (2002) Hallucinogens and Drosophila: linking serotonin receptor activation to behavior. Neuroscience 115: 979-984.
172. Nishimura I, Yang Y, and Lu B (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116:671-682.
173. Nornes S, Groth C, Camp E, Ey P, and Lardelli M (2003) Developmental control of Presenilin1 expression, endoproteolysis, and interaction in zebrafish embryos. Exp Cell Res 289:124-132.
174. Null B, Liu CW, Hedehus M, Conolly S, and Davis RW (2008) High-resolution, in vivo magnetic resonance imaging of Drosophila at 18.8 Tesla. PLoS ONE 3:e2817.
175. Ocorr K, Akasaka T, and Bodmer R (2007a) Age-related cardiac disease model of Drosophila. Mech Ageing Dev 128:112-116.
176. Ocorr K, Perrin L, Lim HY, Qian L, Wu X, and Bodmer R (2007b) Genetic control of heart function and aging in Drosophila. Trends Cardiovasc Med 17:177-182.
177. Ocorr KA, Crawley T, Gibson G, and Bodmer R (2007c) Genetic variation for cardiac dysfunction in Drosophila. PLoS ONE 2:e601.
178. Olivier JP, Raabe T, Henkemeyer M, Dickson B, Mbamalu G, Margolis B, Schlessinger J, Hafen E, and Pawson T (1993) A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73:179-191.
179. Pagliarini RA and Xu T (2003) A genetic screen in Drosophila for metastatic behavior. Science 302:1227-1231.
180. Paisán-Ruíz C, Jain S, Evans EW, Gilks WP, Simón J, van der Brug M, López de Munain A, Aparicio S, Gil AM, Khan N, et al. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44:595-600.
181. Pandey UB, Batlevi Y, Baehrecke EH, and Taylor JP (2007a) HDAC6 at the intersection of autophagy, the ubiquitin-proteasome system and neurodegeneration. Autophagy 3:643-645.
182. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, et al. (2007b) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859-863.
183. Paquet D, Bhat R, Sydow A, Mandelkow EM, Berg S, Hellberg S, Fälting J, Distel M, Köster RW, Schmid B, et al. (2009) A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest 119:1382-1395.
184. Parker JA, Arango M, Abderrahmane S, Lambert E, Tourette C, Catoire H, and Néri C (2005) Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat Genet 37:349-350.
185. Parker JA, Connolly JB, Wellington C, Hayden M, Dausset J, and Neri C (2001) Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proc Natl Acad Sci USA 98:13318-13323.
186. Pavlidis P and Tanouye MA (1995) Seizures and failures in the giant fiber pathway of Drosophila bang-sensitive paralytic mutants. J Neurosci 15:5810-5819.
187. Pereira PS, Teixeira A, Pinho S, Ferreira P, Fernandes J, Oliveira C, Seruca R, Suriano G, and Casares F (2006) E-cadherin missense mutations, associated with hereditary diffuse gastric cancer (HDGC) syndrome, display distinct invasive behaviors and genetic interactions with the Wnt and Notch pathways in Drosophila epithelia. Hum Mol Genet 15:1704-1712.
188. Pesah Y, Burgess H, Middlebrooks B, Ronningen K, Prosser J, Tirunagaru V, Zysk J, and Mardon G (2005) Whole-mount analysis reveals normal numbers of dopaminergic neurons following misexpression of alpha-Synuclein in Drosophila. Genesis 41:154-159.
189. Pesah Y, Pham T, Burgess H, Middlebrooks B, Verstreken P, Zhou Y, Harding M, Bellen H, and Mardon G (2004) Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress. Development 131:2183-2194.
190. Peterson RT, Link BA, Dowling JE, and Schreiber SL (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci USA 97:12965-12969.
191. Pollitt SK, Pallos J, Shao J, Desai UA, Ma AA, Thompson LM, Marsh JL, and Diamond MI (2003) A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor. Neuron 40:685-694.
192. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, et al. (1997) Mutation in the β-synuclein gene identified in families with Parkinson's disease. Science 276:2045-2047.
193. Pulak R (2006) Techniques for analysis, sorting, and dispensing of C. elegans on the COPAS flow-sorting system. Methods Mol Biol 351:275-286.
194. Quinn WG, Harris WA, and Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 71:708-712.
195. Ragland M, Hutter C, Zabetian C, and Edwards K (2009) Association between the ubiquitin carboxyl-terminal esterase L1 gene (UCHL1) S18Y variant and Parkinson's Disease: a HuGE review and meta-analysis. Am J Epidemiol 170:1344-1357.
196. Rand MD (2010) Drosophotoxicology: the growing potential for Drosophila in neurotoxicology. Neurotoxicol Teratol 32:74-83.
197. Rand MD, Kearney AL, Dao J, and Clason T (2010) Permeabilization of Drosophila embryos for introduction of small molecules. Insect Biochem Mol Biol 40:792-804.
198. Ready DF, Hanson TE, and Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217-240.
199. Reim I and Frasch M (2010) Genetic and genomic dissection of cardiogenesis in the Drosophila model. Pediatr Cardiol 31:325-334.
200. Reiter LT, Potocki L, Chien S, Gribskov M, and Bier E (2001) E A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11:1114-1125.
201. Reith ME, Zhen J, and Chen N (2006) The importance of company: Naα and Cl influence substrate interaction with SLC6 transporters and other proteins. Handb Exp Pharmacol 175:75-93.
202. Ren Y, Zhao J, and Feng J (2003) J Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation. J Neurosci 23:3316-3324.
203. Reynolds ER, Stauffer EA, Feeney L, Rojahn E, Jacobs B, and McKeever C (2003) Treatment with the antiepileptic drugs phenytoin and gabapentin ameliorates seizure and paralysis of Drosophila bang-sensitive mutants. J Neurobiol 58:503-513.
204. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S, Haggarty SJ, Kokel D, Rubin LL, Peterson RT, et al. (2010) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327:348-351.
205. Rikke BA, Murakami S, and Johnson TE (2000) Paralogy and orthology of tyrosine kinases that can extend the life span of Caenorhabditis elegans. Mol Biol Evol 17:671-683.
206. Roeder T, Isermann K, and Kabesch M (2009) Drosophila in asthma research. Am J Respir Crit Care Med 179:979-983.
207. Roman G, Endo K, Zong L, and Davis RL (2001) P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci USA 98:12602-12607.
208. Romero E, Cha GH, Verstreken P, Ly CV, Hughes RE, Bellen HJ, and Botas J (2008) Suppression of neurodegeneration and increased neurotransmission caused by expanded full-length huntingtin accumulating in the cytoplasm. Neuron 57:27-40.
209. Rothenfluh A and Heberlein U (2002) Drugs, flies, and videotape: the effects of ethanol and cocaine on Drosophila locomotion. Curr Opin Neurobiol 12:639-645.
210. Ruaud AF and Thummel CS (2008) Serotonin and insulin signaling team up to control growth in Drosophila. Genes Dev 22:1851-1855.
211. Rubin GM and Lewis EB (2000) A brief history of Drosophila's contributions to genome research. Science 287:2216-2218.
212. Rulifson EJ, Kim SK, and Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118-1120.
213. Sang TK, Chang HY, Lawless GM, Ratnaparkhi A, Mee L, Ackerson LC, Maidment NT, Krantz DE, and 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.
214. Satta R, Dimitrijevic N, and Manev H (2003) Drosophila metabolize 1,4-butanediol into gamma-hydroxybutyric acid in vivo. Eur J Pharmacol 473:149-152.
215. Sawamura N, Ando T, Maruyama Y, Fujimuro M, Mochizuki H, Honjo K, Shimoda M, Toda H, Sawamura-Yamamoto T, Makuch LA, et al. (2008) Nuclear DISC1 regulates CRE-mediated gene transcription and sleep homeostasis in the fruit fly. Mol Psychiatry 13:1138-1148.
216. Schwarz TL, Tempel BL, Papazian DM, Jan YN, and Jan LY (1988) Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature 331:137-142.
217. Scott R, Bourtchuladze R, Gossweiler S, Dubnau J, and Tully T (2002) CREB and the discovery of cognitive enhancers. J Mol Neurosci 19:171-177.
218. Seidner GA, Ye Y, Faraday MM, Alvord WG, and Fortini ME (2006) Modeling clinically heterogeneous presenilin mutations with transgenic Drosophila. Curr Biol 16:1026-1033.
219. Selby L, Zhang C, and Sun QQ. (2007) Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci Lett 412:227-232.
220. Settivari R, Levora J, and Nass R (2009) The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in Caenorhabditis elegans models of manganism and parkinson disease. J Biol Chem 284:35758-35768.
221. Shaw PJ, Cirelli C, Greenspan RJ, and Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834-1837.
222. Shiga Y and Tanaka-Matakatsu M (1996) A nuclear GFP/β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev Growth Differ 38:99-106.
223. Simon MA, Bowtell DD, Dodson GS, Laverty TR, and Rubin GM (1991) Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701-716.
224. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, et al. (2003) β-Synuclein locus triplication causes Parkinson's disease. Science 302:841.
225. Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, Rottinghaus GE, and Zars T (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105:5579-5584.
226. Sekine T, Yamaguchi T, Hamano K, Siomi H, Saez L, Ishida N, and Shimoda M (2008) Circadian phenotypes of Drosophila fragile x mutants in alternative genetic backgrounds. Zoolog Sci 25:561-571.
227. Smith WW, Pei Z, Jiang H, Dawson VL, Dawson TM, and Ross CA (2006) Kinase activity of mutant LRRK2 mediates neuronal toxicity. Nat Neurosci 9:1231-1233.
228. Sofola OA, Jin P, Qin Y, Duan R, Liu H, de Haro M, Nelson DL, and Botas J (2007) RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 55:565-571.
229. Sofola O, Sundram V, Ng F, Kleyner Y, Morales J, Botas J, Jackson FR, and Nelson DL (2008) The Drosophila FMRP and LARK RNA-binding proteins function together to regulate eye development and circadian behavior. J Neurosci 28:10200-10205.
230. Song J and Tanouye MA (2006) Seizure suppression by shakB2, a gap junction mutation in Drosophila. J Neurophysiol 95:627-635.
231. Sonnhammer EL and Durbin R (1997) Analysis of protein domain families in Caenorhabditis elegans. Genomics 46:200-216.
232. Springer W, Hoppe T, Schmidt E, and Baumeister R (2005) A Caenorhabditis elegans Parkin mutant with altered solubility couples alpha-synuclein aggregation to proteotoxic stress. Hum Mol Genet 14:3407-3423.
233. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL, Kazantsev A, Schmidt E, Zhu YZ, Greenwald M, et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743.
234. Stilwell GE, Saraswati S, Littleton JT, and Chouinard SW (2006) Development of a Drosophila seizure model for in vivo high-throughput drug screening. Eur J Neurosci 24:2211-2222.
235. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, and Klämbt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587-597.
236. Struhl G and Greenwald I (1999) Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398:522-525.
237. Sullivan E, Tucker EM, and Dale IL (1999) Measurement of [Ca2α] using the Fluorometric Imaging Plate Reader (FLIPR). Methods Mol Biol 114:125-133.
238. Sun Z and Gitler AD (2008) Discovery and characterization of three novel synuclein genes in zebrafish. Dev Dyn 237:2490-2495.
239. Takeyama K, Ito S, Yamamoto A, Tanimoto H, Furutani T, Kanuka H, Miura M, Tabata T, and Kato S (2002) Androgen-dependent neurodegeneration by polyglutamine-expanded human androgen receptor in Drosophila. Neuron 35:855-864.
240. Tan JS, Lin F, and Tanouye MA (2004) Potassium bromide, an anticonvulsant, is effective at alleviating seizures in the Drosophila bang-sensitive mutant bang senseless. Brain Res 1020:45-52.
241. Tan EK and Schapira AH (2008) Uniting Chinese across Asia: the LRRK2 Gly2385Arg risk variant. Eur J Neurol 15:203-204.
242. Taylor JP, Hardy J, and Fischbeck KH (2002) Toxic proteins in neurodegenerative disease. Science 296:1991-1995.
243. Teschendorf D and Link CD (2009) What have worm models told us about the mechanisms of neuronal dysfunction in human neurodegenerative diseases? Mol Neurodegener 4:38.
244. Torres G and Horowitz JM (1998) Activating properties of cocaine and cocaethylene in a behavioral preparation of Drosophila melanogaster. Synapse 29:148-161.
245. Tsang M (2010) Zebrafish: A tool for chemical screens. Birth Defects Res C Embryo Today 90:185-192.
246. Tucker B, Richards RI, and Lardelli M (2006) Contribution of mGluR and Fmr1 functional pathways to neurite morphogenesis, craniofacial development and fragile X syndrome. Hum Mol Genet 15:3446-3458.
247. Tully T and Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263-277.
248. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304:1158-1160.
249. van Ham TJ, Thijssen KL, Breitling R, Hofstra RM, Plasterk RH, and Nollen EA (2008) C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. PLoS Genet (3):e1000027.
250. Van Tijn P, Paridaen JT, Van Rooijen C, and Zivkovic D (2009) Zebrafish models for familial Alzheimer's disease. 6th European Zebrafish Genetics and Development Meeting; 15-19 July 2009; Rome Italy. Abstract 293. Adria Congrex srl and Meetitaly, Rimini, Italy.
251. Van't Padje S, Chaudhry B, Severijnen LA, van der Linde HC, Mientjes EJ, Oostra BA, and Willemsen R (2009) Reduction in fragile X related 1 protein causes cardiomyopathy and muscular dystrophy in zebrafish. J Exp Biol 212:2564-2570.
252. Ved R, Saha S, Westlund B, Perier C, Burnam L, Sluder A, Hoener M, Rodrigues CM, Alfonso A, Steer C, et al. (2005) Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J Biol Chem 280:42655-42668.
253. Vidal M and Cagan RL (2006) Drosophila models for cancer research. Curr Opin Genet Dev 16:10-16.
254. Vogler G and Ocorr K (2009) Visualizing the beating heart in Drosophila. J Vis Exp doi: 10.3791/1425.
255. Waddell S (2010) Dopamine reveals neural circuit mechanisms of fly memory. Trends in neurosciences 33:457-464.
256. Wagner C, Isermann K, Fehrenbach H, and Roeder T (2008) Molecular architecture of the fruit fly's airway epithelial immune system. BMC Genomics 9:446.
257. Wan L, Dockendorff TC, Jongens TA, and Dreyfuss G (2000) Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein. Mol Cell Biol 20:8536-8547.
258. Wang S, Tulina N, Carlin DL, and Rulifson EJ (2007) The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proc Natl Acad Sci USA 104:19873-19878.
259. West AB, Moore DJ, Biskup S, Bugayenko A, Smith WW, Ross CA, Dawson VL, and Dawson TM (2005) Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc Natl Acad Sci USA 102:16842-16847.
260. West AB, Moore DJ, Choi C, Andrabi SA, Li X, Dikeman D, Biskup S, Zhang Z, Lim KL, Dawson VL, et al. (2007) Parkinson's disease-associated mutations in LRRK2 link enhanced GTP-binding and kinase activities to neuronal toxicity. Hum. Mol. Genet 16:223-232.
261. Whitten J (1957) The post-embryonic development of the tracheal system in Drosophila melanogaster. Q J Microsc Sci 98:123-150.
262. Williams DW, Tyrer M, and Shepherd D (2000) Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J Comp Neurol 428:630-640.
263. Wittenburg N, Eimer S, Lakowski B, Röhrig S, Rudolph C, and Baumeister R (2009) Presenilin is required for proper morphology and function of neurons in C. elegans. Nature 406:306-309.
264. Woods IG, Kelly PD, Chu F, Ngo-Hazelett P, Yan YL, Huang H, Postlethwait JH, and Talbot WS (2000) A comparative map of the zebrafish genome. Genome Res 10:1903-1914.
265. Wolf FW and Heberlein U (2003) In vertebrate models of drug abuse. J Neurobiol 54:161-178.
266. Wolf MJ and Rockman HA (2008) Drosophila melanogaster as a model system for genetics of postnatal cardiac function. Drug discovery today Disease models 5:117-123.
267. Wu CL, Xia S, Fu TF, Wang H, Chen YH, Leong D, Chiang AS, and Tully T (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10:1578-1586.
268. Wu L and Silverman N (2007) Fighting infection fly-style. Fly (Austin) 1:106-109.
269. Wu M and Sato TN (2008) On the mechanics of cardiac function of Drosophila embryo. PLoS ONE 3:e4045.
270. Wu M, Pastor-Pareja JC, and Xu T (2010) Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 463:545-548.
271. Wu Y, Wu Z, Butko P, Christen Y, Lambert MP, Klein WL, Link CD, and Luo Y (2006) Amyloid-beta-induced pathological behaviors are suppressed by Ginkgo biloba extract EGb 761 and ginkgolides in transgenic Caenorhabditis elegans. J Neurosci 26:13102-13113.
272. Xi Y, Ryan J, Noble S, Yu M, Yilbas AE, and Ekker M (2010) Impaired dopaminergic neuron development and locomotor function in zebrafish with loss of pink1 function. Eur J Neurosci 31:623-633.
273. Ye Y, Lukinova N, and Fortini ME (1999) Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 398:525-529.
274. Yuan Q, Lin F, Zheng X, and Sehgal A (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115-127.
275. Zhang X, Smith DL, Meriin AB, Engemann S, Russel DE, Roark M, Washington SL, Maxwell MM, Marsh JL, Thompson LM, et al. (2005) A potent small molecule inhibits polyglutamine aggregation in Huntington's disease neurons and suppresses neurodegeneration in vivo. Proc Natl Acad Sci USA 102:892-897.
276. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, and Broadie K (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107:591-603.
277. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, et al. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44: 601-607.