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International Journal of Alzheimer’s Disease
Volume 2012 (2012), Article ID 970980, 14 pages
Drosophila Models of Tauopathies: What Have We Learned?
1Laboratory of Behavioral and Developmental Genetics, Center for Human Genetics, University of Leuven, 3000 Leuven, Belgium
2VIB Center for the Biology of Disease, 3000 Leuven, Belgium
3INSERM U744, Institut Pasteur de Lille, Université Lille Nord de France, 1 Rue du Professeur Calmette, 59019 Lille Cedex, France
Received 21 February 2012; Accepted 8 April 2012
Academic Editor: David Blum
Copyright © 2012 Marc Gistelinck et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- H. J. Bellen, C. Tong, and H. Tsuda, “100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future,” Nature Reviews Neuroscience, vol. 11, no. 7, pp. 514–522, 2010.
- D. Lessing and N. M. Bonini, “Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants,” Nature Reviews Genetics, vol. 10, no. 6, pp. 359–370, 2009.
- E. Bier, “Drosophila, the golden bug, emerges as a tool for human genetics,” Nature Reviews Genetics, vol. 6, no. 1, pp. 9–23, 2005.
- J. Bilen and N. M. Bonini, “Drosophila as a model for human neurodegenerative disease,” Annual Review of Genetics, vol. 39, pp. 153–171, 2005.
- M. B. Feany and W. W. Bender, “A Drosophila model of Parkinson's disease,” Nature, vol. 404, no. 6776, pp. 394–398, 2000.
- C. W. Wittmann, M. F. Wszolek, J. M. Shulman et al., “Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles,” Science, vol. 293, no. 5530, pp. 711–714, 2001.
- G. R. Jackson, M. Wiedau-Pazos, T. K. Sang et al., “Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila,” Neuron, vol. 34, no. 4, pp. 509–519, 2002.
- Y. Li, P. Ray, E. J. Rao et al., “A Drosophila model for TDP-43 proteinopathy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 7, pp. 3169–3174, 2010.
- B. Dermaut, S. Kumar-Singh, R. Rademakers, J. Theuns, M. Cruts, and C. van Broeckhoven, “Tau is central in the genetic Alzheimer-frontotemporal dementia spectrum,” Trends in Genetics, vol. 21, no. 12, pp. 664–672, 2005.
- M. D. Adams and J. J. Sekelsky, “From sequence to phenotype: reverse genetics in Drosophila melanogaster,” Nature Reviews Genetics, vol. 3, no. 3, pp. 189–198, 2002.
- A. H. Brand and N. Perrimon, “Targeted gene expression as a means of altering cell fates and generating dominant phenotypes,” Development, vol. 118, no. 2, pp. 401–415, 1993.
- S. E. McGuire, P. T. Le, A. J. Osborn, K. Matsumoto, and R. L. Davis, “Spatiotemporal rescue of memory dysfunction in Drosophila,” Science, vol. 302, no. 5651, pp. 1765–1768, 2003.
- T. Osterwalder, K. S. Yoon, B. H. White, and H. Keshishian, “A conditional tissue-specific transgene expression system using inducible GAL4,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 22, pp. 12596–12601, 2001.
- M. M. Burcin, G. Schiedner, S. Kochanek, S. Y. Tsai, and B. W. O'Malley, “Adenovirus-mediated regulable target gene expression in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 2, pp. 355–360, 1999.
- H. J. Bellen, R. W. Levis, Y. He et al., “The Drosophila gene disruption project: progress using transposons with distinctive site specificities,” Genetics, vol. 188, no. 3, pp. 731–743, 2011.
- K. G. Golic and S. Lindquist, “The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome,” Cell, vol. 59, no. 3, pp. 499–509, 1989.
- D. St Johnston, “The art and design of genetic screens: Drosophila melanogaster,” Nature Reviews Genetics, vol. 3, no. 3, pp. 176–188, 2002.
- K. Ito, H. Sass, J. Urban, A. Hofbauer, and S. Schneuwly, “GALA4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system,” Cell and Tissue Research, vol. 290, no. 1, pp. 1–10, 1997.
- M. J. Murray, D. J. Merritt, A. H. Brand, and P. M. Whitington, “In vivo dynamics of axon pathfinding in the Drosophilia CNS: a time-lapse study of an identified motorneuron,” Journal of Neurobiology, vol. 37, no. 4, pp. 607–621, 1998.
- C. A. Callahan and J. B. Thomas, “Tau-β-galactosidase, an axon-targeted fusion protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 13, pp. 5972–5976, 1994.
- D. W. Williams, M. Tyrer, and D. Shepherd, “Tau and tau reporters disrupt central projections of sensory neurons in Drosophila,” The Journal of Comparative Neurology, vol. 428, no. 4, pp. 630–640, 2000.
- S. L. Karsten, T. K. Sang, L. Gehman et al., “A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration,” Neuron, vol. 51, no. 5, pp. 549–560, 2006.
- S. Chatterjee, T. K. Sang, G. M. Lawless, and G. R. Jackson, “Dissociation of tau toxicity and phosphorylation: role of GSK-3β, MARK and Cdk5 in a Drosophila model,” Human Molecular Genetics, vol. 18, no. 1, pp. 164–177, 2009.
- S. Kosmidis, S. Grammenoudi, K. Papanikolopoulou, and E. M. C. Skoulakis, “Differential effects of tau on the integrity and function of neurons essential for learning in Drosophila,” Journal of Neuroscience, vol. 30, no. 2, pp. 464–477, 2010.
- I. Nishimura, Y. Yang, and B. Lu, “PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila,” Cell, vol. 116, no. 5, pp. 671–682, 2004.
- M. L. Steinhilb, D. Dias-Santagata, T. A. Fulga, D. L. Felch, and M. B. Feany, “Tau phosphorylation sites work in concert to promote neurotoxicity in vivo,” Molecular Biology of the Cell, vol. 18, no. 12, pp. 5060–5068, 2007.
- M. L. Steinhilb, D. Dias-Santagata, E. E. Mulkearns et al., “S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila,” Journal of Neuroscience Research, vol. 85, no. 6, pp. 1271–1278, 2007.
- K. Iijima-Ando, L. Zhao, A. Gatt, C. Shenton, and K. Iijima, “A DNA damage-activated checkpoint kinase phosphorylates tau and enhances tau-induced neurodegeneration,” Human Molecular Genetics, vol. 19, no. 10, pp. 1930–1938, 2010.
- V. Khurana, Y. Lu, M. L. Steinhilb, S. Oldham, J. M. Shulman, and M. B. Feany, “TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model,” Current Biology, vol. 16, no. 3, pp. 230–241, 2006.
- J. B. Reinecke, S. L. DeVos, J. P. McGrath, et al., “Implicating calpain in tau-mediated toxicity in vivo,” PLoS ONE, vol. 6, no. 8, Article ID e23865, 2011.
- V. Khurana, I. Elson-Schwab, T. A. Fulga et al., “Lysosomal dysfunction promotes cleavage and neurotoxicity of tau in vivo,” PLoS Genetics, vol. 6, no. 7, Article ID e1001026, 2010.
- A. Mershin, E. Pavlopoulos, O. Fitch, B. C. Braden, D. V. Nanopoulos, and E. M. C. Skoulakis, “Learning and memory deficits upon tau accumulation in Drosophila mushroom body neurons,” Learning and Memory, vol. 11, no. 3, pp. 277–287, 2004.
- H. Doerflinger, R. Benton, J. M. Shulman, and D. st Johnston, “The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium,” Development, vol. 130, no. 17, pp. 3965–3975, 2003.
- S. Feuillette, L. Miguel, T. Frébourg, D. Campion, and M. Lecourtois, “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, vol. 113, no. 4, pp. 895–903, 2010.
- D. R. Micklem, R. Dasgupta, H. Elliott et al., “The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila,” Current Biology, vol. 7, no. 7, pp. 468–478, 1997.
- G. Heidary and M. E. Fortini, “Identification and characterization of the Drosophila tau homolog,” Mechanisms of Development, vol. 108, no. 1-2, pp. 171–178, 2001.
- A. G. Tian and W. M. Deng, “Par-1 and tau regulate the anterior-posterior gradient of microtubules in Drosophila oocytes,” Developmental Biology, vol. 327, no. 2, pp. 458–464, 2009.
- A. B. Da Cruz, M. Schwärzel, S. Schulze, M. Niyyati, M. Heisenberg, and D. Kretzschmar, “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, vol. 16, no. 5, pp. 2433–2442, 2005.
- X. Chen, Y. Li, J. Huang et al., “Study of tauopathies by comparing Drosophila and human tau in Drosophila,” Cell and Tissue Research, vol. 329, no. 1, pp. 169–178, 2007.
- K. K. Ubhi, H. Shaibah, T. A. Newman, D. Shepherd, and A. Mudher, “A comparison of the neuronal dysfunction caused by Drosophila tau and human tau in a Drosophila model of tauopathies,” Invertebrate Neuroscience, vol. 7, no. 3, pp. 165–171, 2007.
- J. M. Shulman and M. B. Feany, “Genetic modifiers of tauopathy in Drosophila,” Genetics, vol. 165, no. 3, pp. 1233–1242, 2003.
- S. S. Ambegaokar and G. R. Jackson, “Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation,” Human Molecular Genetics, vol. 20, pp. 4947–4977, 2011.
- O. Blard, S. Feuillette, J. Bou et al., “Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila,” Human Molecular Genetics, vol. 16, no. 5, pp. 555–566, 2007.
- F. Pichaud and C. Desplan, “A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia,” Development, vol. 128, no. 6, pp. 815–826, 2001.
- A. Gambis, P. Dourlen, H. Steller, and B. Mollereau, “Two-color in vivo imaging of photoreceptor apoptosis and development in Drosophila,” Developmental Biology, vol. 351, no. 1, pp. 128–134, 2011.
- B. Dermaut, K. K. Norga, A. Kania et al., “Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer,” Journal of Cell Biology, vol. 170, no. 1, pp. 127–139, 2005.
- P. A. Yeh, J. Y. Chien, C. C. Chou et al., “Drosophila notal bristle as a novel assessment tool for pathogenic study of tau toxicity and screening of therapeutic compounds,” Biochemical and Biophysical Research Communications, vol. 391, no. 1, pp. 510–516, 2010.
- J. Folwell, C. M. Cowan, K. K. Ubhi et al., “Aβ exacerbates the neuronal dysfunction caused by human tau expression in a Drosophila model of Alzheimer's disease,” Experimental Neurology, vol. 223, no. 2, pp. 401–409, 2010.
- Y. Talmat-Amar, Y. Arribat, C. Redt-Clouet, et al., “Important neuronal toxicity of microtubule-bound tau in vivo in Drosophila,” Human Molecular Genetics, vol. 20, pp. 3738–3745, 2011.
- K. J. Colodner and M. B. Feany, “Glial fibrillary tangles and JAK/STAT-mediated glial and neuronal cell death in a Drosophila model of glial tauopathy,” Journal of Neuroscience, vol. 30, no. 48, pp. 16102–16113, 2010.
- L. Torroja, H. Chu, I. Kotovsky, and K. White, “Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport,” Current Biology, vol. 9, no. 9, pp. 489–492, 1999.
- T. L. Falzone, S. Gunawardena, D. McCleary, G. F. Reis, and L. S. Goldstein, “Kinesin-1 transport reductions enhance human tau hyperphosphorylation, aggregation and neurodegeneration in animal models of tauopathies,” Human Molecular Genetics, vol. 19, no. 22, pp. 4399–4408, 2010.
- Y. O. Ali, K. Ruan, and R. G. Zhai, “NMNAT suppresses tau-induced neurodegeneration by promoting clearance of hyperphosphorylated tau oligomers in a Drosophila model of tauopathy,” Human Molecular Genetics, vol. 21, no. 2, pp. 237–250, 2012.
- D. Dias-Santagata, T. A. Fulga, A. Duttaroy, and M. B. Feany, “Oxidative stress mediates tau-induced neurodegeneration in Drosophila,” Journal of Clinical Investigation, vol. 117, no. 1, pp. 236–245, 2007.
- A. Mudher, D. Shepherd, T. A. Newman et al., “GSK-3β inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila,” Molecular Psychiatry, vol. 9, no. 5, pp. 522–530, 2004.
- J. G. Gindhart Jr., C. J. Desai, S. Beushausen, K. Zinn, and L. S. B. Goldstein, “Kinesin light chains are essential for axonal transport in Drosophila,” Journal of Cell Biology, vol. 141, no. 2, pp. 443–454, 1998.
- M. A. Martin, S. J. Iyadurai, A. Gassman, J. G. Gindhart Jr., T. S. Hays, and W. M. Saxton, “Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport,” Molecular Biology of the Cell, vol. 10, no. 11, pp. 3717–3728, 1999.
- H. Luan, W. C. Lemon, N. C. Peabody et al., “Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila,” Journal of Neuroscience, vol. 26, no. 2, pp. 573–584, 2006.
- N. C. Peabody, F. Diao, H. Luan et al., “Bursicon functions within the Drosophila CNS to modulate wing expansion behavior, hormone secretion, and cell death,” Journal of Neuroscience, vol. 28, no. 53, pp. 14379–14391, 2008.
- B. J. Loveall and D. L. Deitcher, “The essential role of bursicon during Drosophila development,” BMC Developmental Biology, vol. 10, article 92, 2010.
- G. Roman and R. L. Davis, “Molecular biology and anatomy of Drosophila olfactory associative learning,” BioEssays, vol. 23, no. 7, pp. 571–581, 2001.
- S. S. Ambegaokar and G. R. Jackson, “Interaction between eye pigment genes and tau-induced neurodegeneration in Drosophila melanogaster,” Genetics, vol. 186, no. 1, pp. 435–442, 2010.
- C. M. Cowan, T. Bossing, A. Page, D. Shepherd, and A. Mudher, “Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo,” Acta Neuropathologica, vol. 120, no. 5, pp. 593–604, 2010.
- C. M. Cowan, D. Shepherd, and A. Mudher, “Insights from Drosophila models of Alzheimer's disease,” Biochemical Society Transactions, vol. 38, no. 4, pp. 988–992, 2010.
- S. Feuillette, V. Deramecourt, A. Laquerriere et al., “Filamin-A and Myosin VI colocalize with fibrillary tau protein in Alzheimer's disease and FTDP-17 brains,” Brain Research, vol. 1345, pp. 182–189, 2010.
- T. A. Fulga, I. Elson-Schwab, V. Khurana et al., “Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo,” Nature Cell Biology, vol. 9, no. 2, pp. 139–148, 2007.
- F. C. Chee, A. Mudher, M. F. Cuttle et al., “Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions,” Neurobiology of Disease, vol. 20, no. 3, pp. 918–928, 2005.
- S. Feuillette, O. Blard, M. Lecourtois, T. Frébourg, D. Campion, and C. Dumanchin, “Tau is not normally degraded by the proteasome,” Journal of Neuroscience Research, vol. 80, no. 3, pp. 400–405, 2005.
- C. A. Loewen and M. B. Feany, “The unfolded protein response protects from tau neurotoxicity in vivo,” PLoS ONE, vol. 5, no. 9, Article ID e13084, 2010.
- C. S. Mendes, C. Levet, G. Chatelain et al., “ER stress protects from retinal degeneration,” EMBO Journal, vol. 28, no. 9, pp. 1296–1307, 2009.
- S. Sengupta, P. M. Horowitz, S. L. Karsten et al., “Degradation of tau protein by puromycin-sensitive aminopeptidase in vitro,” Biochemistry, vol. 45, no. 50, pp. 15111–15119, 2006.
- K. M. Chow, H. Guan, and L. B. Hersh, “Aminopeptidases do not directly degrade tau protein,” Molecular Neurodegeneration, vol. 5, no. 1, article 48, 2010.
- F. M. Menzies, R. Hourez, S. Imarisio et al., “Puromycin-sensitive aminopeptidase protects against aggregation-prone proteins via autophagy,” Human Molecular Genetics, vol. 19, no. 23, pp. 4573–4586, 2010.
- K. Iijima, A. Gatt, and K. Iijima-Ando, “Tau Ser262 phosphorylation is critical for Aβ42-induced tau toxicity in a transgenic Drosophila model of Alzheimer's disease.,” Human Molecular Genetics, vol. 19, no. 15, pp. 2947–2957, 2010.
- S. Grammenoudi, S. Kosmidis, and E. M. C. Skoulakis, “Cell type-specific processing of human tau proteins in Drosophila,” FEBS Letters, vol. 580, no. 19, pp. 4602–4606, 2006.
- K. Papanikolopoulou, S. Kosmidis, S. Grammenoudi, and E. M. C. Skoulakis, “Phosphorylation differentiates tau-dependent neuronal toxicity and dysfunction,” Biochemical Society Transactions, vol. 38, no. 4, pp. 981–987, 2010.
- K. Papanikolopoulou and E. M. C. Skoulakis, “The power and richness of modelling tauopathies in Drosophila,” Molecular Neurobiology, vol. 44, no. 1, pp. 122–133, 2011.
- J. M. Shulman, P. Chipendo, L. B. Chibnik et al., “Functional screening of Alzheimer pathology genome-wide association signals in Drosophila,” American Journal of Human Genetics, vol. 88, no. 2, pp. 232–238, 2011.