Drosophila as a screening tool to study human neurodegenerative diseases

Journal of Neurochemistry

Volumn 127, Issue 4, 2013, Pages 453-460

  Lenz, Sarah ^a   Karsten, Peter ^a   Schulz, Jörg B ^a,b   Voigt, Aaron ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b JARA Translational Brain Medicine   (Germany)

Author keywords

Alzheimer's disease; Drosophila melanogaster; gene regulation; mutagenesis; neurodegenerative diseases; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; CELL PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HELICASE; PARKIN; PINK1 PROTEIN; POLYGLUTAMINE; PROTEINASE ACTIVATED RECEPTOR 1; SHORT HAIRPIN RNA; TAU PROTEIN; TRANSCRIPTION FACTOR GAL4; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; DISEASE MODEL; DNA MODIFICATION; DROSOPHILA; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INSERTION; GENE INTERACTION; GENE MAPPING; GENE SILENCING; GENETIC MODEL; GENETIC PARAMETERS; GENETIC RECOMBINATION; GENETIC SCREENING; GENOME; HIGH THROUGHPUT SEQUENCING; LOSS OF FUNCTION MUTATION; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE GENETICS; REVIEW; RNA INTERFERENCE; ROUGH EYE PHENOTYPE;

ALZHEIMER'S DISEASE; DROSOPHILA MELANOGASTER; GENE REGULATION; MUTAGENESIS; NEURODEGENERATIVE DISEASES; PARKINSON'S DISEASE;

ANIMALS; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; HUMANS; NEURODEGENERATIVE DISEASES; PHOTORECEPTOR CELLS, INVERTEBRATE;

ANIMALIA; DROSOPHILA MELANOGASTER; MUS;

EID: 84887065883     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12446     Document Type: Review

References (66)

1. Adams M. D., Celniker S. E., Holt R. A., et al,. (2000) The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
2. Akimoto A., Wada H., and, Hayashi S., (2005) Enhancer trapping with a red fluorescent protein reporter in Drosophila. Dev. Dyn. 233, 993-997.
3. Ambegaokar S. S., and, Jackson G. R., (2011) Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation. Hum. Mol. Genet. 20, 4947-4977.
4. Bartolome C., Maside X., and, Charlesworth B., (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol. Biol. Evol. 19, 926-937.
5. Bellen H. J., Levis R. W., Liao G., et al,. (2004) The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761-781.
6. Bellen H. J., Levis R. W., He Y., et al,. (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188, 731-743.
7. Berger J., Suzuki T., Senti K. A., Stubbs J., Schaffner G., and, Dickson B. J., (2001) Genetic mapping with SNP markers in Drosophila. Nat. Genet. 29, 475-481.
8. Bier E., (2005) Drosophila, the golden bug, emerges as a tool for human genetics. Nat. Rev. Genet. 6, 9-23.
9. Bier E., Vaessin H., Shepherd S., et al,. (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3, 1273-1287.
10. Bilen J., and, Bonini N. M., (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet. 3, 1950-1964.
11. Blard O., Feuillette S., Bou J., Chaumette B., Frebourg T., Campion D., and, Lecourtois M., (2007) Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum. Mol. Genet. 16, 555-566.
12. Blumenstiel J. P., Noll A. C., Griffiths J. A., Perera A. G., Walton K. N., Gilliland W. D., Hawley R. S., and, Staehling-Hampton K., (2009) Identification of EMS-induced mutations in Drosophila melanogaster by whole-genome sequencing. Genetics 182, 25-32.
13. Brand A. H., and, Perrimon N., (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
14. Butler E. K., Voigt A., Lutz A. K., et al,. (2012) The mitochondrial chaperone protein TRAP1 mitigates alpha-Synuclein toxicity. PLoS Genet. 8, e1002488.
15. Cao W., Song H. J., Gangi T., Kelkar A., Antani I., Garza D., and, Konsolaki M., (2008) Identification of novel genes that modify phenotypes induced by Alzheimer's beta-amyloid overexpression in Drosophila. Genetics 178, 1457-1471.
16. Chang H. C., Dimlich D. N., Yokokura T., et al,. (2008) Modeling spinal muscular atrophy in Drosophila. PLoS ONE 3, e3209.
17. Chatterjee S., Sang T. K., Lawless G. M., and, Jackson G. R., (2009) Dissociation of tau toxicity and phosphorylation: role of GSK-3beta, MARK and Cdk5 in a Drosophila model. Hum. Mol. Genet. 18, 164-177.
18. Choi C. M., Vilain S., Langen M., Van Kelst S., De Geest N., Yan J., Verstreken P., and, Hassan B. A., (2009) Conditional mutagenesis in Drosophila. Science 324, 54.
19. Clark I. E., Dodson M. W., Jiang C., Cao J. H., Huh J. R., Seol J. H., Yoo S. J., Hay B. A., and, Guo M., (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441, 1162-1166.
20. Cooley L., Kelley R., and, Spradling A., (1988) Insertional mutagenesis of the Drosophila genome with single P elements. Science 239, 1121-1128.
21. Costa A. C., Loh S. H., and, Martins L. M., (2013) Drosophila Trap1 protects against mitochondrial dysfunction in a PINK1/parkin model of Parkinson's disease. Cell Death Dis. 4, e467.
22. Dietzl G., Chen D., Schnorrer F., et al,. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
23. Doumanis J., Wada K., Kino Y., Moore A. W., and, Nukina N., (2009) RNAi screening in Drosophila cells identifies new modifiers of mutant huntingtin aggregation. PLoS ONE 4, e7275.
24. Esposito G., Vos M., Vilain S., Swerts J., De Sousa Valadas J., Van Meensel S., Schaap O., and, Verstreken P., (2013) Aconitase causes iron toxicity in Drosophila pink1 mutants. PLoS Genet. 9, e1003478.
25. Fernandes C., and, Rao Y., (2011) Genome-wide screen for modifiers of Parkinson's disease genes in Drosophila. Mol. Brain 4, 17.
26. Fernandez-Funez P., Nino-Rosales M. L., de Gouyon B., et al,. (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408, 101-106.
27. Greene J. C., Whitworth A. J., Andrews L. A., Parker T. J., and, Pallanck L. J., (2005) Genetic and genomic studies of Drosophila parkin mutants implicate oxidative stress and innate immune responses in pathogenesis. Hum. Mol. Genet. 14, 799-811.
28. Greenspan R. J., (2004) Fly Pushing-The Theory and Practice of Drosophila Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
29. Higashiyama H., Hirose F., Yamaguchi M., Inoue Y. H., Fujikake N., Matsukage A., and, Kakizuka A., (2002) Identification of ter94, Drosophila VCP, as a modulator of polyglutamine-induced neurodegeneration. Cell Death Differ. 9, 264-273.
30. Hoehne M., de Couet H. G., Stuermer C. A., and, Fischbach K. F., (2005) Loss- and gain-of-function analysis of the lipid raft proteins Reggie/Flotillin in Drosophila: they are posttranslationally regulated, and misexpression interferes with wing and eye development. Mol. Cell. Neurosci. 30, 326-338.
31. Hummel T., and, Klambt C., (2008) P-element mutagenesis. Methods Mol. Biol. 420, 97-117.
32. Ito K., Sass H., Urban J., Hofbauer A., and, Schneuwly S., (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res. 290, 1-10.
33. Jackson G. R., Wiedau-Pazos M., Sang T. K., Wagle N., Brown C. A., Massachi S., and, Geschwind D. H., (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34, 509-519.
34. Kao C. F., and, Lee T., (2013) Reverse genetics by loss-of-function mosaic analysis in Drosophila. Cold Spring Harb. Protoc. doi: 10.1101/pdb.prot071670.
35. Kazemi-Esfarjani P., and, Benzer S., (2000) Genetic suppression of polyglutamine toxicity in Drosophila. Science 287, 1837-1840.
36. Kennerdell J. R., and, Carthew R. W., (2000) Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 18, 896-898.
37. Kim H., Kim K., Kim J., Kim S. H., and, Yim J., (2012) Mutagenesis by imprecise excision of the piggyBac transposon in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 417, 335-339.
38. Kumar J. P., (2012) Building an ommatidium one cell at a time. Dev. Dyn. 241, 136-149.
39. Latouche M., Lasbleiz C., Martin E., et al,. (2007) A conditional pan-neuronal Drosophila model of spinocerebellar ataxia 7 with a reversible adult phenotype suitable for identifying modifier genes. J. Neurosci. 27, 2483-2492.
40. Lawal H. O., Terrell A., Lam H. A., et al,. (2012) Drosophila modifier screens to identify novel neuropsychiatric drugs including aminergic agents for the possible treatment of Parkinson's disease and depression. Mol Psychiatry. doi: 10.1038/mp.2012.170.
41. Lessing D., and, Bonini N. M., (2008) Polyglutamine genes interact to modulate the severity and progression of neurodegeneration in Drosophila. PLoS Biol. 6, e29.
42. Li L. B., Yu Z., Teng X., and, Bonini N. M., (2008) RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature 453, 1107-1111.
43. Llamusi B., Bargiela A., Fernandez-Costa J. M., Garcia-Lopez A., Klima R., Feiguin F., and, Artero R., (2013) Muscleblind, BSF and TBPH are mislocalized in the muscle sarcomere of a Drosophila myotonic dystrophy model. Dis. Model Mech. 6, 184-196.
44. Metaxakis A., Oehler S., Klinakis A., and, Savakis C., (2005) Minos as a genetic and genomic tool in Drosophila melanogaster. Genetics, 171, 571-581.
45. 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.
46. Nusslein-Volhard C., and, Wieschaus E., (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
47. O'Kane C. J., and, Gehring W. J., (1987) Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl Acad. Sci. USA 84, 9123-9127.
48. Osterwalder T., Yoon K. S., White B. H., and, Keshishian H., (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl Acad. Sci. USA 98, 12596-12601.
49. Park J., Lee S. B., Lee S., et al,. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161.
50. Park J., Al-Ramahi I., Tan Q., et al,. (2013) RAS-MAPK-MSK1 pathway modulates ataxin 1 protein levels and toxicity in SCA1. Nature 498, 325-331.
51. Peter A., Schottler P., Werner M., et al,. (2002) Mapping and identification of essential gene functions on the X chromosome of Drosophila. EMBO Rep. 3, 34-38.
52. Rao D. D., Vorhies J. S., Senzer N., and, Nemunaitis J., (2009) siRNA vs. shRNA: similarities and differences. Adv. Drug Deliv. Rev. 61, 746-759.
53. Rong Y. S., Titen S. W., Xie H. B., et al,. (2002) Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 16, 1568-1581.
54. Rubin G. M., Yandell M. D., Wortman J. R., et al,. (2000) Comparative genomics of the eukaryotes. Science 287, 2204-2215.
55. Ryder E., and, Russell S., (2003) Transposable elements as tools for genomics and genetics in Drosophila. Brief. Funct. Genomic Proteomic 2, 57-71.
56. Shulman J. M., and, Feany M. B., (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165, 1233-1242.
57. Shulman J. M., Shulman L. M., Weiner W. J., and, Feany M. B., (2003) From fruit fly to bedside: translating lessons from Drosophila models of neurodegenerative disease. Curr. Opin. Neurol. 16, 443-449.
58. Spradling A. C., Stern D. M., Kiss I., Roote J., Laverty T., and, Rubin G. M., (1995) Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl Acad. Sci. USA 92, 10824-10830.
59. St Johnston D., (2002) The art and design of genetic screens: Drosophila melanogaster. Nat. Rev. Genet. 3, 176-188.
60. Tan L., Schedl P., Song H. J., Garza D., and, Konsolaki M., (2008) The Toll->NFkappaB signaling pathway mediates the neuropathological effects of the human Alzheimer's Abeta42 polypeptide in Drosophila. PLoS ONE 3, e3966.
61. Thibault S. T., Singer M. A., Miyazaki W. Y., et al,. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287.
62. Venken K. J., and, Bellen H. J., (2012) Genome-wide manipulations of Drosophila melanogaster with transposons, Flp recombinase, and PhiC31 integrase. Methods Mol. Biol. 859, 203-228.
63. Voßfeldt H., Butzlaff M., Prüßing K., et al,. (2012) Large-scale screen for modifiers of ataxin-3-derived polyglutamine-induced toxicity in Drosophila. PLoS ONE 7, e47452.
64. Yang Y., Gehrke S., Haque M. E., et al,. (2005) Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl Acad. Sci. USA 102, 13670-13675.
65. Zhang S., Binari R., Zhou R., and, Perrimon N., (2010) A genomewide RNA interference screen for modifiers of aggregates formation by mutant Huntingtin in Drosophila. Genetics 184, 1165-1179.
66. Zhang L., Karsten P., Hamm S., et al,. (2013) TRAP1 rescues PINK1 loss-of-function phenotypes. Hum Mol Genet 22, 2829-2841.