Drosophila models of tauopathies: What have we learned?

International Journal of Alzheimer's Disease

Volumn , Issue , 2012, Pages

  Gistelinck, Marc ^a,b,c   Lambert, Jean Charles ^c   Callaerts, Patrick ^a,b   Dermaut, Bart ^c   Dourlen, Pierre ^c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALPAIN; DNA; FILAMIN; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM ION; PROTEINASE ACTIVATED RECEPTOR 1; TARGET OF RAPAMYCIN KINASE; TAU PROTEIN; TRANSGELIN; WNT PROTEIN;

ACTIN FILAMENT; BRAIN DEGENERATION; DISEASE MODEL; DNA REPAIR; DROSOPHILA; GENETIC SCREENING; LARVA; LEARNING; LETHALITY; LIFESPAN; MEMORY; MICROTUBULE; MUSHROOM BODY; NERVE FIBER TRANSPORT; NEUROMUSCULAR SYNAPSE; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVIEW; TAUOPATHY;

EID: 84863652660     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.1155/2012/970980     Document Type: Review

References (78)

1. Bellen H. J., Tong C., Tsuda H., 100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future Nature Reviews Neuroscience 2010 11 7 514 522
2. Lessing D., Bonini N. M., Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants Nature Reviews Genetics 2009 10 6 359 370
3. Bier E., Drosophila, the golden bug, emerges as a tool for human genetics Nature Reviews Genetics 2005 6 1 9 23 (Pubitemid 39657894)
4. Bilen J., Bonini N. M., Drosophila as a model for human neurodegenerative disease Annual Review of Genetics 2005 39 153 171 (Pubitemid 43011111)
5. Feany M. B., Bender W. W., A Drosophila model of Parkinson's disease Nature 2000 404 6776 394 398 (Pubitemid 30164341)
6. Wittmann C. W., Wszolek M. F., Shulman J. M., Salvaterra P. M., Lewis J., Hutton M., Feany M. B., Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles Science 2001 293 5530 711 714 (Pubitemid 32728676)
7. Jackson G. R., Wiedau-Pazos M., Sang T. K., Wagle N., Brown C. A., Massachi S., Geschwind D. H., Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila Neuron 2002 34 4 509 519 (Pubitemid 34628749)
8. Li Y., Ray P., Rao E. J., Shi C., Guo W., Chen X., Woodruff E. A., Fushimi K., Wu J. Y., A Drosophila model for TDP-43 proteinopathy Proceedings of the National Academy of Sciences of the United States of America 2010 107 7 3169 3174
9. Dermaut B., Kumar-Singh S., Rademakers R., Theuns J., Cruts M., van Broeckhoven C., Tau is central in the genetic Alzheimer-frontotemporal dementia spectrum Trends in Genetics 2005 21 12 664 672 (Pubitemid 41608689)
10. Adams M. D., Sekelsky J. J., From sequence to phenotype: reverse genetics in Drosophila melanogaster Nature Reviews Genetics 2002 3 3 189 198 (Pubitemid 34506587)
11. Brand A. H., Perrimon N., Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 1993 118 2 401 415 (Pubitemid 23214028)
12. McGuire S. E., Le P. T., Osborn A. J., Matsumoto K., Davis R. L., Spatiotemporal rescue of memory dysfunction in Drosophila Science 2003 302 5651 1765 1768 (Pubitemid 37505740)
13. Osterwalder T., Yoon K. S., White B. H., Keshishian H., A conditional tissue-specific transgene expression system using inducible GAL4 Proceedings of the National Academy of Sciences of the United States of America 2001 98 22 12596 12601 (Pubitemid 33019991)
14. Burcin M. M., Schiedner G., Kochanek S., Tsai S. Y., O'Malley B. W., Adenovirus-mediated regulable target gene expression in vivo Proceedings of the National Academy of Sciences of the United States of America 1999 96 2 355 360 (Pubitemid 29061212)
15. Bellen H. J., Levis R. W., He Y., Carlson J. W., Evans-Holm M., Bae E., Kim J., Metaxakis A., Savakis C., Schulze K. L., Hoskins R. A., Spradling A. C., The Drosophila gene disruption project: progress using transposons with distinctive site specificities Genetics 2011 188 3 731 743
16. Golic K. G., Lindquist S., The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome Cell 1989 59 3 499 509 (Pubitemid 19284463)
17. St Johnston D., The art and design of genetic screens: Drosophila melanogaster Nature Reviews Genetics 2002 3 3 176 188 (Pubitemid 34506586)
18. Ito K., Sass H., Urban J., Hofbauer A., Schneuwly S., GALA4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system Cell and Tissue Research 1997 290 1 1 10 (Pubitemid 27460119)
19. Murray M. J., Merritt D. J., Brand A. H., Whitington P. M., In vivo dynamics of axon pathfinding in the Drosophilia CNS: a time-lapse study of an identified motorneuron Journal of Neurobiology 1998 37 4 607 621 (Pubitemid 28549221)
20. Callahan C. A., Thomas J. B., Tau- -galactosidase, an axon-targeted fusion protein Proceedings of the National Academy of Sciences of the United States of America 1994 91 13 5972 5976
21. Williams D. W., Tyrer M., Shepherd D., Tau and tau reporters disrupt central projections of sensory neurons in Drosophila The Journal of Comparative Neurology 2000 428 4 630 640
22. Karsten S. L., Sang T. K., Gehman L., Chatterjee S., Liu J., Lawless G. M., Sengupta S., Berry R., Pomakian J., Oh H. S., Schulz C., Hui K. S., Wiedau-Pazos M., Vinters H. V., Binder L., Geschwind D. H., Jackson G. R., A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration Neuron 2006 51 5 549 560 (Pubitemid 44314079)
23. Chatterjee S., Sang T. K., Lawless G. M., Jackson G. R., Dissociation of tau toxicity and phosphorylation: role of GSK-3, MARK and Cdk5 in a Drosophila model Human Molecular Genetics 2009 18 1 164 177
24. Kosmidis S., Grammenoudi S., Papanikolopoulou K., Skoulakis E. M. C., Differential effects of tau on the integrity and function of neurons essential for learning in Drosophila Journal of Neuroscience 2010 30 2 464 477
25. Nishimura I., Yang Y., Lu B., PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila Cell 2004 116 5 671 682 (Pubitemid 38326726)
26. Steinhilb M. L., Dias-Santagata D., Fulga T. A., Felch D. L., Feany M. B., Tau phosphorylation sites work in concert to promote neurotoxicity in vivo Molecular Biology of the Cell 2007 18 12 5060 5068 (Pubitemid 350246705)
27. Steinhilb M. L., Dias-Santagata D., Mulkearns E. E., Shulman J. M., Biernat J., Mandelkow E. M., Feany M. B., S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila Journal of Neuroscience Research 2007 85 6 1271 1278 (Pubitemid 46724370)
28. Iijima-Ando K., Zhao L., Gatt A., Shenton C., Iijima K., A DNA damage-activated checkpoint kinase phosphorylates tau and enhances tau-induced neurodegeneration Human Molecular Genetics 2010 19 10 1930 1938
29. Khurana V., Lu Y., Steinhilb M. L., Oldham S., Shulman J. M., Feany M. B., TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model Current Biology 2006 16 3 230 241 (Pubitemid 43190222)
30. Reinecke J. B., DeVos S. L., McGrath J. P., Implicating calpain in tau-mediated toxicity in vivo PLoS ONE 2011 6 8
31. Khurana V., Elson-Schwab I., Fulga T. A., Sharp K. A., Loewen C. A., Mulkearns E., Tyynel J., Scherzer C. R., Feany M. B., Lysosomal dysfunction promotes cleavage and neurotoxicity of tau in vivo PLoS Genetics 2010 6 7
32. Mershin A., Pavlopoulos E., Fitch O., Braden B. C., Nanopoulos D. V., Skoulakis E. M. C., Learning and memory deficits upon tau accumulation in Drosophila mushroom body neurons Learning and Memory 2004 11 3 277 287 (Pubitemid 38697893)
33. Doerflinger H., Benton R., Shulman J. M., st Johnston D., The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium Development 2003 130 17 3965 3975 (Pubitemid 37063416)
34. Feuillette S., Miguel L., Frébourg T., Campion D., Lecourtois M., Drosophila models of human tauopathies indicate that tau protein toxicity in vivo is mediated by soluble cytosolic phosphorylated forms of the protein Journal of Neurochemistry 2010 113 4 895 903
35. Micklem D. R., Dasgupta R., Elliott H., Gergely F., Davidson C., Brand A., Gonzlez-Reyes A., Johnston D. S., The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila Current Biology 1997 7 7 468 478 (Pubitemid 27308970)
36. Heidary G., Fortini M. E., Identification and characterization of the Drosophila tau homolog Mechanisms of Development 2001 108 1-2 171 178 (Pubitemid 32923065)
37. Tian A. G., Deng W. M., Par-1 and tau regulate the anterior-posterior gradient of microtubules in Drosophila oocytes Developmental Biology 2009 327 2 458 464
38. Da Cruz A. B., Schwrzel M., Schulze S., Niyyati M., Heisenberg M., Kretzschmar D., Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila Molecular Biology of the Cell 2005 16 5 2433 2442 (Pubitemid 40632224)
39. Chen X., Li Y., Huang J., Cao D., Yang G., Liu W., Lu H., Guo A., Study of tauopathies by comparing Drosophila and human tau in Drosophila Cell and Tissue Research 2007 329 1 169 178 (Pubitemid 46686106)
40. Ubhi K. K., Shaibah H., Newman T. A., Shepherd D., Mudher A., A comparison of the neuronal dysfunction caused by Drosophila tau and human tau in a Drosophila model of tauopathies Invertebrate Neuroscience 2007 7 3 165 171 (Pubitemid 47339788)
41. Shulman J. M., Feany M. B., Genetic modifiers of tauopathy in Drosophila Genetics 2003 165 3 1233 1242 (Pubitemid 38020245)
42. Ambegaokar S. S., Jackson G. R., Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation Human Molecular Genetics 2011 20 4947 4977
43. Blard O., Feuillette S., Bou J., Chaumette B., Frébourg T., Campion D., Lecourtois M., Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila Human Molecular Genetics 2007 16 5 555 566 (Pubitemid 46522618)
44. Pichaud F., Desplan C., A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia Development 2001 128 6 815 826 (Pubitemid 32288193)
45. Gambis A., Dourlen P., Steller H., Mollereau B., Two-color in vivo imaging of photoreceptor apoptosis and development in Drosophila Developmental Biology 2011 351 1 128 134
46. Dermaut B., Norga K. K., Kania A., Verstreken P., Pan H., Zhou Y., Callaerts P., Bellen H. J., Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer Journal of Cell Biology 2005 170 1 127 139 (Pubitemid 40994102)
47. Yeh P. A., Chien J. Y., Chou C. C., Huang Y. F., Tang C. Y., Wang H. Y., Su M. T., Drosophila notal bristle as a novel assessment tool for pathogenic study of tau toxicity and screening of therapeutic compounds Biochemical and Biophysical Research Communications 2010 391 1 510 516
48. Folwell J., Cowan C. M., Ubhi K. K., Shiabh H., Newman T. A., Shepherd D., Mudher A., A exacerbates the neuronal dysfunction caused by human tau expression in a Drosophila model of Alzheimer's disease Experimental Neurology 2010 223 2 401 409
49. Talmat-Amar Y., Arribat Y., Redt-Clouet C., Important neuronal toxicity of microtubule-bound tau in vivo in Drosophila Human Molecular Genetics 2011 20 3738 3745
50. Colodner K. J., Feany M. B., Glial fibrillary tangles and JAK/STAT-mediated glial and neuronal cell death in a Drosophila model of glial tauopathy Journal of Neuroscience 2010 30 48 16102 16113
51. Torroja L., Chu H., Kotovsky I., White K., Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport Current Biology 1999 9 9 489 492 (Pubitemid 29228622)
52. Falzone T. L., Gunawardena S., McCleary D., Reis G. F., Goldstein L. S., Kinesin-1 transport reductions enhance human tau hyperphosphorylation, aggregation and neurodegeneration in animal models of tauopathies Human Molecular Genetics 2010 19 22 4399 4408
53. Ali Y. O., Ruan K., Zhai R. G., NMNAT suppresses tau-induced neurodegeneration by promoting clearance of hyperphosphorylated tau oligomers in a Drosophila model of tauopathy Human Molecular Genetics 2012 21 2 237 250
54. Dias-Santagata D., Fulga T. A., Duttaroy A., Feany M. B., Oxidative stress mediates tau-induced neurodegeneration in Drosophila Journal of Clinical Investigation 2007 117 1 236 245 (Pubitemid 46055207)
55. Mudher A., Shepherd D., Newman T. A., Mildren P., Jukes J. P., Squire A., Mears A., Berg S., MacKay D., Asuni A. A., Bhat R., Lovestone S., GSK-3 inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila Molecular Psychiatry 2004 9 5 522 530 (Pubitemid 38903508)
56. Gindhart J. G. Jr., Desai C. J., Beushausen S., Zinn K., Goldstein L. S. B., Kinesin light chains are essential for axonal transport in Drosophila Journal of Cell Biology 1998 141 2 443 454 (Pubitemid 28237092)
57. Martin M. A., Iyadurai S. J., Gassman A., Gindhart J. G. Jr., Hays T. S., Saxton W. M., Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport Molecular Biology of the Cell 1999 10 11 3717 3728 (Pubitemid 29534021)
58. Luan H., Lemon W. C., Peabody N. C., Pohl J. B., Zelensky P. K., Wang D., Nitabach M. N., Holmes T. C., White B. H., Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila Journal of Neuroscience 2006 26 2 573 584 (Pubitemid 43237123)
59. Peabody N. C., Diao F., Luan H., Wang H., Dewey E. M., Honegger H. W., White B. H., Bursicon functions within the Drosophila CNS to modulate wing expansion behavior, hormone secretion, and cell death Journal of Neuroscience 2008 28 53 14379 14391
60. Loveall B. J., Deitcher D. L., The essential role of bursicon during Drosophila development BMC Developmental Biology 2010 10, article 92
61. Roman G., Davis R. L., Molecular biology and anatomy of Drosophila olfactory associative learning BioEssays 2001 23 7 571 581 (Pubitemid 32665011)
62. Ambegaokar S. S., Jackson G. R., Interaction between eye pigment genes and tau-induced neurodegeneration in Drosophila melanogaster Genetics 2010 186 1 435 442
63. Cowan C. M., Bossing T., Page A., Shepherd D., Mudher A., Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo Acta Neuropathologica 2010 120 5 593 604
64. Cowan C. M., Shepherd D., Mudher A., Insights from Drosophila models of Alzheimer's disease Biochemical Society Transactions 2010 38 4 988 992
65. Feuillette S., Deramecourt V., Laquerriere A., Duyckaerts C., Delisle M. B., Maurage C. A., Blum D., Buée L., Frébourg T., Campion D., Lecourtois M., Filamin-A and Myosin VI colocalize with fibrillary tau protein in Alzheimer's disease and FTDP-17 brains Brain Research 2010 1345 182 189
66. Fulga T. A., Elson-Schwab I., Khurana V., Steinhilb M. L., Spires T. L., Hyman B. T., Feany M. B., Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo Nature Cell Biology 2007 9 2 139 148 (Pubitemid 46420856)
67. Chee F. C., Mudher A., Cuttle M. F., Newman T. A., MacKay D., Lovestone S., Shepherd D., Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions Neurobiology of Disease 2005 20 3 918 928 (Pubitemid 41619367)
68. Feuillette S., Blard O., Lecourtois M., Frébourg T., Campion D., Dumanchin C., Tau is not normally degraded by the proteasome Journal of Neuroscience Research 2005 80 3 400 405 (Pubitemid 40780828)
69. Loewen C. A., Feany M. B., The unfolded protein response protects from tau neurotoxicity in vivo PLoS ONE 2010 5 9
70. Mendes C. S., Levet C., Chatelain G., Dourlen P., Fouillet A., Dichtel-Danjoy M. L., Gambis A., Ryoo H. D., Steller H., Mollereau B., ER stress protects from retinal degeneration EMBO Journal 2009 28 9 1296 1307
71. Sengupta S., Horowitz P. M., Karsten S. L., Jackson G. R., Geschwind D. H., Fu Y., Berry R. W., Binder L. I., Degradation of tau protein by puromycin-sensitive aminopeptidase in vitro Biochemistry 2006 45 50 15111 15119 (Pubitemid 44937024)
72. Chow K. M., Guan H., Hersh L. B., Aminopeptidases do not directly degrade tau protein Molecular Neurodegeneration 2010 5 1, article 48
73. Menzies F. M., Hourez R., Imarisio S., Raspe M., Sadiq O., Chandraratna D., O'Kane C., Rock K. L., Reits E., Goldberg A. L., Rubinsztein D. C., Puromycin-sensitive aminopeptidase protects against aggregation-prone proteins via autophagy Human Molecular Genetics 2010 19 23 4573 4586
74. Iijima K., Gatt A., Iijima-Ando K., Tau Ser262 phosphorylation is critical for A 42-induced tau toxicity in a transgenic Drosophila model of Alzheimer's disease. Human Molecular Genetics 2010 19 15 2947 2957
75. Grammenoudi S., Kosmidis S., Skoulakis E. M. C., Cell type-specific processing of human tau proteins in Drosophila FEBS Letters 2006 580 19 4602 4606 (Pubitemid 44189378)
76. Papanikolopoulou K., Kosmidis S., Grammenoudi S., Skoulakis E. M. C., Phosphorylation differentiates tau-dependent neuronal toxicity and dysfunction Biochemical Society Transactions 2010 38 4 981 987
77. Papanikolopoulou K., Skoulakis E. M. C., The power and richness of modelling tauopathies in Drosophila Molecular Neurobiology 2011 44 1 122 133
78. Shulman J. M., Chipendo P., Chibnik L. B., Aubin C., Tran D., Keenan B. T., Kramer P. L., Schneider J. A., Bennett D. A., Feany M. B., De Jager P. L., Functional screening of Alzheimer pathology genome-wide association signals in Drosophila American Journal of Human Genetics 2011 88 2 232 238