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REVIEW

Drosophila as a model to study the role of glia in neurodegeneration

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Pages 69-79 | Received 25 May 2015, Accepted 23 Jul 2015, Published online: 24 Aug 2015

References

  • Aigouy, B., Lepelletier, L., & Giangrande, A. (2008). Glial chain migration requires pioneer cells. J Neurosci, 28, 11635–11641.
  • Altenhein, B. (2015). Glial cell progenitors in the Drosophila embryo. Glia, 63, 1291–1302.
  • Augustin, H., Grosjean, Y., Chen, K., Sheng, Q., & Featherstone, D. E. (2007). Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci, 27, 111–123.
  • Benzer, S. (1967). Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci U S A, 58, 1112–1119.
  • Benzer, S. (1971). From the gene to behavior. JAMA, 218, 1015–1022.
  • Bergmann, A., Tugentman, M., Shilo, B. Z., & Steller, H. (2002). Regulation of cell number by MAPK-dependent control of apoptosis: a mechanism for trophic survival signaling. Dev Cell, 2, 159–170.
  • Besson, M. T., Dupont, P., Fridell, Y. W., & Lievens, J. C. (2010). Increased energy metabolism rescues glia-induced pathology in a Drosophila model of Huntington's disease. Hum Mol Genet, 19, 3372–3382.
  • Block, M. L., Zecca, L., & Hong, J. S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci, 8, 57–69.
  • Boillee, S., Vande Velde, C., & Cleveland, D. W. (2006). ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron, 52, 39–59.
  • Bolkan, B. J., & Kretzschmar, D. (2014). Loss of Tau results in defects in photoreceptor development and progressive neuronal degeneration in Drosophila. Dev Neurobiol, 74, 1210–1225.
  • Bolkan, B. J., Triphan, T., & Kretzschmar, D. (2012). beta-secretase cleavage of the fly amyloid precursor protein is required for glial survival. J Neurosci, 32, 16181–16192.
  • Booth, G. E., Kinrade, E. F., & Hidalgo, A. (2000). Glia maintain follower neuron survival during Drosophila CNS development. Development, 127, 237–244.
  • Borycz, J., Borycz, J. A., Edwards, T. N., Boulianne, G. L., & Meinertzhagen, I. A. (2012). The metabolism of histamine in the Drosophila optic lobe involves an ommatidial pathway: beta-alanine recycles through the retina. J Exp Biol, 215, 1399–1411.
  • Borycz, J., Borycz, J. A., Loubani, M., & Meinertzhagen, I. A. (2002). tan and ebony genes regulate a novel pathway for transmitter metabolism at fly photoreceptor terminals. J Neurosci, 22, 10549–10557.
  • Brand, A. H., & Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401–415.
  • Bruijn, L. I., Becher, M. W., Lee, M. K., Anderson, K. L., Jenkins, N. A., Copeland, N. G., et al. (1997). ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron, 18, 327–338.
  • Buchanan, R. L., & Benzer, S. (1993). Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron, 10, 839–850.
  • Campbell, G., Goring, H., Lin, T., Spana, E., Andersson, S., Doe, C. Q., & Tomlinson, A. (1994). RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development, 120, 2957–2966.
  • Casci, I., & Pandey, U. B. (2015). A fruitful endeavor: modeling ALS in the fruit fly. Brain Res, 1607, 47–74.
  • Chaturvedi, R., Reddig, K., & Li, H. S. (2014). Long-distance mechanism of neurotransmitter recycling mediated by glial network facilitates visual function in Drosophila. Proc Natl Acad Sci U S A, 111, 2812–2817.
  • Chen, Y., Yang, M., Deng, J., Chen, X., Ye, Y., Zhu, L., et al. (2011). Expression of human FUS protein in Drosophila leads to progressive neurodegeneration. Protein Cell, 2, 477–486.
  • Chotard, C., & Salecker, I. (2007). Glial cell development and function in the Drosophila visual system. Neuron Glia Biol, 3, 17–25.
  • Colodner, K. J., & Feany, M. B. (2010). Glial fibrillary tangles and JAK/STAT-mediated glial and neuronal cell death in a Drosophila model of glial tauopathy. J Neurosci, 30, 16102–16113.
  • Comas, D., Petit, F., & Preat, T. (2004). Drosophila long-term memory formation involves regulation of cathepsin activity. Nature, 430, 460–463.
  • Conforti, L., Gilley, J., & Coleman, M. P. (2014). Wallerian degeneration: an emerging axon death pathway linking injury and disease. Nat Rev Neurosci, 15, 394–409.
  • Cowan, C. M., Sealey, M. A., Quraishe, S., Targett, M. T., Marcellus, K., Allan, D., & Mudher, A. (2011). Modelling tauopathies in Drosophila: insights from the fruit fly. Int J Alzheimers Dis, 2011, 598157.
  • Daigle, J. G., Lanson, N. A., Jr., Smith, R. B., Casci, I., Maltare, A., Monaghan, J., et al. (2013). RNA-binding ability of FUS regulates neurodegeneration, cytoplasmic mislocalization and incorporation into stress granules associated with FUS carrying ALS-linked mutations. Hum Mol Genet, 22, 1193–1205.
  • Diaper, D. C., Adachi, Y., Lazarou, L., Greenstein, M., Simoes, F. A., Di Domenico, A., et al. (2013). Drosophila TDP-43 dysfunction in glia and muscle cells cause cytological and behavioural phenotypes that characterize ALS and FTLD. Hum Mol Genet, 22, 3883–3893.
  • Dias-Santagata, D., Fulga, T. A., Duttaroy, A., & Feany, M. B. (2007). Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J Clin Invest, 117, 236–245.
  • Dotti, M. T., Buccoliero, R., Lee, A., Gorospe, J. R., Flint, D., Galluzzi, P., et al. (2009). An infantile case of Alexander disease unusual for its MRI features and a GFAP allele carrying both the p.Arg79His mutation and the p.Glu223Gln coding variant. J Neurol, 256, 679–682.
  • Edwards, T. N., & Meinertzhagen, I. A. (2010). The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol, 90, 471–497.
  • Enomoto, H. (2005). Regulation of neural development by glial cell line-derived neurotrophic factor family ligands. Anat Sci Int, 80, 42–52.
  • Estes, P. S., Daniel, S. G., McCallum, A. P., Boehringer, A. V., Sukhina, A. S., Zwick, R. A., & Zarnescu, D. C. (2013). Motor neurons and glia exhibit specific individualized responses to TDP-43 expression in a Drosophila model of amyotrophic lateral sclerosis. Dis Model Mech, 6, 721–733.
  • Evans, J. R., & Barker, R. A. (2008). Neurotrophic factors as a therapeutic target for Parkinson's disease. Expert Opin Ther Targets, 12, 437–447.
  • Faber, P. W., Alter, J. R., MacDonald, M. E., & Hart, A. C. (1999). Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc Natl Acad Sci U S A, 96, 179–184.
  • Fang, Y., Soares, L., Teng, X., Geary, M., & Bonini, N. M. (2012). A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr Biol, 22, 590–595.
  • Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell, 87, 651–660.
  • Freeman, M. R., & Doherty, J. (2006). Glial cell biology in Drosophila and vertebrates. Trends Neurosci, 29, 82–90.
  • Fuentes-Medel, Y., Logan, M. A., Ashley, J., Ataman, B., Budnik, V., & Freeman, M. R. (2009). Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol, 7, e1000184.
  • Gistelinck, M., Lambert, J. C., Callaerts, P., Dermaut, B., & Dourlen, P. (2012). Drosophila models of tauopathies: what have we learned? Int J Alzheimers Dis, 2012, 970980.
  • Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., et al. (1994). Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264, 1772–1775.
  • Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., Travers, A. A., & Technau, G. M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development, 121, 317–332.
  • Hartenstein, V. (2011). Morphological diversity and development of glia in Drosophila. Glia, 59, 1237–1252.
  • Hegde, V. R., Vogel, R., & Feany, M. B. (2014). Glia are critical for the neuropathology of complex I deficiency in Drosophila. Hum Mol Genet, 23, 4686–4692.
  • Hidalgo, A., Kato, K., Sutcliffe, B., McIlroy, G., Bishop, S., & Alahmed, S. (2011). Trophic neuron-glia interactions and cell number adjustments in the fruit fly. Glia, 59, 1296–1303.
  • Hidalgo, A., Kinrade, E. F., & Georgiou, M. (2001). The Drosophila neuregulin vein maintains glial survival during axon guidance in the CNS. Dev Cell, 1, 679–690.
  • Hirth, F. (2010). Drosophila melanogaster in the study of human neurodegeneration. CNS Neurol Disord Drug Targets, 9, 504–523.
  • Hoopfer, E. D., McLaughlin, T., Watts, R. J., Schuldiner, O., O’Leary, D. D., & Luo, L. (2006). Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron, 50, 883–895.
  • Hopkins, P. C. (2013). Neurodegeneration in a Drosophila model for the function of TMCC2, an amyloid protein precursor-interacting and apolipoprotein E-binding protein. PLoS One, 8, e55810.
  • Hopkins, P. C., Sainz-Fuertes, R., & Lovestone, S. (2011). The impact of a novel apolipoprotein E and amyloid-beta protein precursor-interacting protein on the production of amyloid-beta. J Alzheimers Dis, 26, 239–253.
  • Hotta, Y., & Benzer, S. (1970). Genetic dissection of the Drosophila nervous system by means of mosaics. Proc Natl Acad Sci U S A, 67, 1156–1163.
  • Hotta, Y., & Benzer, S. (1972). Mapping of behaviour in Drosophila mosaics. Nature, 240, 527–535.
  • Huang, Z., Zang, K., & Reichardt, L. F. (2005). The origin recognition core complex regulates dendrite and spine development in postmitotic neurons. J Cell Biol, 170, 527–535.
  • Islam, R., Kumimoto, E. L., Bao, H., & Zhang, B. (2012). ALS-linked SOD1 in glial cells enhances ss-N-Methylamino L-Alanine (BMAA)-induced toxicity in Drosophila. F1000Res, 1, 47.
  • Jackson, F. R., & Haydon, P. G. (2008). Glial cell regulation of neurotransmission and behavior in Drosophila. Neuron Glia Biol, 4, 11–17.
  • Jackson, G. R., Wiedau-Pazos, M., Sang, T. K., Wagle, N., Brown, C. A., Massachi, S., & Geschwind, D. H. (2002). Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron, 34, 509–519.
  • Joardar, A., Menzl, J., Podolsky, T. C., Manzo, E., Estes, P. S., Ashford, S., & Zarnescu, D. C. (2015). PPAR gamma activation is neuroprotective in a Drosophila model of ALS based on TDP-43. Hum Mol Genet, 24, 1741–1754.
  • Jones, B. W. (2001). Glial cell development in the Drosophila embryo. Bioessays, 23, 877–887.
  • Kato, K., Awasaki, T., & Ito, K. (2009). Neuronal programmed cell death induces glial cell division in the adult Drosophila brain. Development, 136, 51–59.
  • Kato, K., Forero, M. G., Fenton, J. C., & Hidalgo, A. (2011). The glial regenerative response to central nervous system injury is enabled by pros-notch and pros-NFkappaB feedback. PLoS Biol, 9, e1001133.
  • Keller, L. C., Cheng, L., Locke, C. J., Muller, M., Fetter, R. D., & Davis, G. W. (2011). Glial-derived prodegenerative signaling in the Drosophila neuromuscular system. Neuron, 72, 760–775.
  • Kerschensteiner, M., & Hohlfeld, R. (2003). Neurotrophic factors protect myelin from attack. Int MS J, 10, 2–4.
  • Kim J. Y., Jang W., Lee H. W., Park E., & Kim C. (2012). Neurodegeneration of Drosophila drop-dead mutants is associated with hypoxia in the brain. Genes Brain Behav, 11, 177–184.
  • Konopka, R. J., & Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A, 68, 2112–2116.
  • Kretzschmar, D. (2009). Swiss cheese et allii, some of the first neurodegenerative mutants isolated in Drosophila. J Neurogenet, 23, 34–41.
  • Kretzschmar, D., Hasan, G., Sharma, S., Heisenberg, M., & Benzer, S. (1997). The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J Neurosci, 17, 7425–7432.
  • Kretzschmar, D., Tschape, J., Bettencourt Da Cruz, A., Asan, E., Poeck, B., Strauss, R., & Pflugfelder, G. O. (2005). Glial and neuronal expression of polyglutamine proteins induce behavioral changes and aggregate formation in Drosophila. Glia, 49, 59–72.
  • Lalancette-Hebert, M., Gowing, G., Simard, A., Weng, Y. C., & Kriz, J. (2007). Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci, 27, 2596–2605.
  • Learte, A. R., Forero, M. G., & Hidalgo, A. (2008). Gliatrophic and gliatropic roles of PVF/PVR signaling during axon guidance. Glia, 56, 164–176.
  • Lee, Y. M., & Sun, Y. H. (2015). Maintenance of Glia in the Optic Lamina Is Mediated by EGFR Signaling by Photoreceptors in Adult Drosophila. PLoS Genet, 11, e1005187.
  • Lehmann, F. O., & Cierotzki, V. (2010). Locomotor performance in the Drosophila brain mutant drop-dead. Comp Biochem Physiol A Mol Integr Physiol, 156, 337–343.
  • Lessing, D., & Bonini, N. M. (2009). Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants. Nat Rev Genet, 10, 359–370.
  • Lievens, J. C., Iche, M., Laval, M., Faivre-Sarrailh, C., & Birman, S. (2008). AKT-sensitive or insensitive pathways of toxicity in glial cells and neurons in Drosophila models of Huntington's disease. Hum Mol Genet, 17, 882–894.
  • Lievens, J. C., Rival, T., Iche, M., Chneiweiss, H., & Birman, S. (2005). Expanded polyglutamine peptides disrupt EGF receptor signaling and glutamate transporter expression in Drosophila. Hum Mol Genet, 14, 713–724.
  • Lin, D. M., & Goodman, C. S. (1994). Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron, 13, 507–523.
  • Lindholm, P., & Saarma, M. (2010). Novel CDNF/MANF family of neurotrophic factors. Dev Neurobiol, 70, 360–371.
  • Liu, L., Zhang, K., Sandoval, H., Yamamoto, S., Jaiswal, M., Sanz, E., et al. (2015). Glial lipid droplets and ROS induced by mitochondrial defects promote neurodegeneration. Cell, 160, 177–190.
  • Logan, M. A., Hackett, R., Doherty, J., Sheehan, A., Speese, S. D., & Freeman, M. R. (2012). Negative regulation of glial engulfment activity by Draper terminates glial responses to axon injury. Nat Neurosci, 15, 722–730.
  • Lu, B., & Vogel, H. (2009). Drosophila models of neurodegenerative diseases. Annu Rev Pathol, 4, 315–342.
  • MacDonald, J. M., Beach, M. G., Porpiglia, E., Sheehan, A. E., Watts, R. J., & Freeman, M. R. (2006). The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron, 50, 869–881.
  • Mallik, M., & Lakhotia, S. C. (2010). Modifiers and mechanisms of multi-system polyglutamine neurodegenerative disorders: lessons from fly models. J Genet, 89, 497–526.
  • Marin-Teva, J. L., Cuadros, M. A., Calvente, R., Almendros, A., & Navascues, J. (1999). Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development. J Comp Neurol, 412, 255–275.
  • Matsuno, M., Horiuchi, J., Yuasa, Y., Ofusa, K., Miyashita, T., Masuda, T., & Saitoe, M. (2015). Long-term memory formation in Drosophila requires training-dependent glial transcription. J Neurosci, 35, 5557–5565.
  • McIlroy, G., Foldi, I., Aurikko, J., Wentzell, J. S., Lim, M. A., Fenton, J. C., et al. (2013). Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nat Neurosci, 16, 1248–1256.
  • Meyerowitz, E. M., & Kankel, D. R. (1978). A genetic analysis of visual system development in Drosophilia melanogaster. Dev Biol, 62, 112–142.
  • Miller, D., Hannon, C., & Ganetzky, B. (2012). A mutation in Drosophila Aldolase causes temperature-sensitive paralysis, shortened lifespan, and neurodegeneration. J Neurogenet, 26, 317–327.
  • Min, K. T., & Benzer, S. (1997). Spongecake and eggroll: two hereditary diseases in Drosophila resemble patterns of human brain degeneration. Curr Biol, 7, 885–888.
  • Min, K. T., & Benzer, S. (1999). Preventing neurodegeneration in the Drosophila mutant bubblegum. Science, 284, 1985–1988.
  • Muhlig-Versen, M., da Cruz, A. B., Tschape, J. A., Moser, M., Buttner, R., Athenstaedt, K., et al. (2005). Loss of Swiss cheese/neuropathy target esterase activity causes disruption of phosphatidylcholine homeostasis and neuronal and glial death in adult Drosophila. J Neurosci, 25, 2865–2873.
  • Napoletano, F., Occhi, S., Calamita, P., Volpi, V., Blanc, E., Charroux, B., et al. (2011). Polyglutamine Atrophin provokes neurodegeneration in Drosophila by repressing fat. EMBO J, 30, 945–958.
  • Navarro, J. A., Ohmann, E., Sanchez, D., Botella, J. A., Liebisch, G., Molto, M. D., et al. (2010). Altered lipid metabolism in a Drosophila model of Friedreich's ataxia. Hum Mol Genet, 19, 2828–2840.
  • Neukomm, L. J., Burdett, T. C., Gonzalez, M. A., Zuchner, S., & Freeman, M. R. (2014). Rapid in vivo forward genetic approach for identifying axon death genes in Drosophila. Proc Natl Acad Sci U S A, 111, 9965–9970.
  • Neumann, H., Kotter, M. R., & Franklin, R. J. (2009). Debris clearance by microglia: an essential link between degeneration and regeneration. Brain, 132, 288–295.
  • Niki, E. (2009). Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med, 47, 469–484.
  • Nisoli, I., Chauvin, J. P., Napoletano, F., Calamita, P., Zanin, V., Fanto, M., & Charroux, B. (2010). Neurodegeneration by polyglutamine Atrophin is not rescued by induction of autophagy. Cell Death Differ, 17, 1577–1587.
  • Oberheim, N. A., Wang, X., Goldman, S., & Nedergaard, M. (2006). Astrocytic complexity distinguishes the human brain. Trends Neurosci, 29, 547–553.
  • Ohayon, D., Pattyn, A., Venteo, S., Valmier, J., Carroll, P., & Garces, A. (2009). Zfh1 promotes survival of a peripheral glia subtype by antagonizing a Jun N-terminal kinase-dependent apoptotic pathway. EMBO J, 28, 3228–3243.
  • Osterloh, J. M., Yang, J., Rooney, T. M., Fox, A. N., Adalbert, R., Powell, E. H., et al. (2012). dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science, 337, 481–484.
  • Palgi, M., Lindstrom, R., Peranen, J., Piepponen, T. P., Saarma, M., & Heino, T. I. (2009). Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons. Proc Natl Acad Sci U S A, 106, 2429–2434.
  • Pantazis, A., Segaran, A., Liu, C. H., Nikolaev, A., Rister, J., Thum, A. S., et al. (2008). Distinct roles for two histamine receptors (hclA and hclB) at the Drosophila photoreceptor synapse. J Neurosci, 28, 7250–7259.
  • Park, S. H., Lee, S., Hong, Y. K., Hwang, S., Lee, J. H., Bang, S. M., et al. (2013). Suppressive effects of SuHeXiang Wan on amyloid-beta42-induced extracellular signal-regulated kinase hyperactivation and glial cell proliferation in a transgenic Drosophila model of Alzheimer's disease. Biol Pharm Bull, 36, 390–398.
  • Parnaik, R., Raff, M. C., & Scholes, J. (2000). Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr Biol, 10, 857–860.
  • Pearce, M. M., Spartz, E. J., Hong, W., Luo, L., & Kopito, R. R. (2015). Prion-like transmission of neuronal huntingtin aggregates to phagocytic glia in the Drosophila brain. Nat Commun, 6, 6768.
  • Petersen, A. J., Katzenberger, R. J., & Wassarman, D. A. (2013). The innate immune response transcription factor relish is necessary for neurodegeneration in a Drosophila model of ataxia-telangiectasia. Genetics, 194, 133–142.
  • Petersen, A. J., Rimkus, S. A., & Wassarman, D. A. (2012). ATM kinase inhibition in glial cells activates the innate immune response and causes neurodegeneration in Drosophila. Proc Natl Acad Sci U S A, 109, E656–664.
  • Phillips, S. E., Woodruff, E. A., 3rd, Liang, P., Patten, M., & Broadie, K. (2008). Neuronal loss of Drosophila NPC1a causes cholesterol aggregation and age-progressive neurodegeneration. J Neurosci, 28, 6569–6582.
  • Rahman, M., Ham, H., Liu, X., Sugiura, Y., Orth, K., & Kramer, H. (2012). Visual neurotransmission in Drosophila requires expression of Fic in glial capitate projections. Nat Neurosci, 15, 871–875.
  • Reed, T. T. (2011). Lipid peroxidation and neurodegenerative disease. Free Radic Biol Med, 51, 1302–1319.
  • Rival, T., Soustelle, L., Strambi, C., Besson, M. T., Iche, M., & Birman, S. (2004). Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol, 14, 599–605.
  • Rogina, B., Benzer, S., & Helfand, S. L. (1997). Drosophila drop-dead mutations accelerate the time course of age-related markers. Proc Natl Acad Sci U S A, 94, 6303–6306.
  • Romero-Calderon, R., Uhlenbrock, G., Borycz, J., Simon, A. F., Grygoruk, A., Yee, S. K., et al. (2008). A glial variant of the vesicular monoamine transporter is required to store histamine in the Drosophila visual system. PLoS Genet, 4, e1000245.
  • Ross, C. A. (2002). Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron, 35, 819–822.
  • Sansone, C. L., & Blumenthal, E. M. (2013). Neurodegeneration in drop-dead mutant Drosophila melanogaster is associated with the respiratory system but not with Hypoxia. PLoS One, 8, e68032.
  • Sanchez, D., Lopez-Arias, B., Torroja, L., Canal, I., Wang, X., Bastiani, M. J., & Ganfornina, M. D. (2006). Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr Biol, 16, 680–686.
  • Sasayama, H., Shimamura, M., Tokuda, T., Azuma, Y., Yoshida, T., Mizuno, T., et al. (2012). Knockdown of the Drosophila fused in sarcoma (FUS) homologue causes deficient locomotive behavior and shortening of motoneuron terminal branches. PLoS One, 7, e39483.
  • Savill, J., Dransfield, I., Gregory, C., & Haslett, C. (2002). A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol, 2, 965–975.
  • Sepp, K. J., Schulte, J., & Auld, V. J. (2001). Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol, 238, 47–63.
  • Sofroniew, M. V. (2009). Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci, 32, 638–647.
  • Stratoulias, V., & Heino, T. I. (2015). MANF silencing, immunity induction or autophagy trigger an unusual cell type in metamorphosing Drosophila brain. Cell Mol Life Sci, 72, 1989–2004.
  • Sun, M., & Chen, L. (2015). Studying tauopathies in Drosophila: A fruitful model. Exp Neurol,
  • Sutcliffe, B., Forero, M. G., Zhu, B., Robinson, I. M., & Hidalgo, A. (2013). Neuron-type specific functions of DNT1, DNT2 and Spz at the Drosophila neuromuscular junction. PLoS One, 8, e75902.
  • Tamura, T., Sone, M., Yamashita, M., Wanker, E. E., & Okazawa, H. (2009). Glial cell lineage expression of mutant ataxin-1 and huntingtin induces developmental and late-onset neuronal pathologies in Drosophila models. PLoS One, 4, e4262.
  • Tasdemir-Yilmaz, O. E., & Freeman, M. R. (2014). Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev, 28, 20–33.
  • Technau, G. M., Berger, C., & Urbach, R. (2006). Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev Dyn, 235, 861–869.
  • Venkatachalam, K., Long, A. A., Elsaesser, R., Nikolaeva, D., Broadie, K., & Montell, C. (2008). Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell, 135, 838–851.
  • Wagner, B., Natarajan, A., Grunaug, S., Kroismayr, R., Wagner, E. F., & Sibilia, M. (2006). Neuronal survival depends on EGFR signaling in cortical but not midbrain astrocytes. EMBO J, 25, 752–762.
  • Wang, J. W., Brent, J. R., Tomlinson, A., Shneider, N. A., & McCabe, B. D. (2011a). The ALS-associated proteins FUS and TDP-43 function together to affect Drosophila locomotion and life span. J Clin Invest, 121, 4118–4126.
  • Wang, L., Colodner, K. J., & Feany, M. B. (2011b). Protein misfolding and oxidative stress promote glial-mediated neurodegeneration in an Alexander disease model. J Neurosci, 31, 2868–2877.
  • Warrick, J. M., Paulson, H. L., Gray-Board, G. L., Bui, Q. T., Fischbeck, K. H., Pittman, R. N., & Bonini, N. M. (1998). Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell, 93, 939–949.
  • Watson, M. R., Lagow, R. D., Xu, K., Zhang, B., & Bonini, N. M. (2008). A drosophila model for amyotrophic lateral sclerosis reveals motor neuron damage by human SOD1. J Biol Chem, 283, 24972–24981.
  • Wittmann, C. W., Wszolek, M. F., Shulman, J. M., Salvaterra, P. M., Lewis, J., Hutton, M., & Feany, M. B. (2001). Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science, 293, 711–714.
  • Wong, P. C., Pardo, C. A., Borchelt, D. R., Lee, M. K., Copeland, N. G., Jenkins, N. A., et al. (1995). An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron, 14, 1105–1116.
  • Xiong, W. C., & Montell, C. (1995). Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron, 14, 581–590.
  • Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A., & Montell, C. (1994). repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev, 8, 981–994.
  • Xu, T., & Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development, 117, 1223–1237.
  • Yamazaki, D., Horiuchi, J., Ueno, K., Ueno, T., Saeki, S., Matsuno, M., et al. (2014). Glial dysfunction causes age-related memory impairment in Drosophila. Neuron, 84, 753–763.
  • Yuasa, Y., Okabe, M., Yoshikawa, S., Tabuchi, K., Xiong, W. C., Hiromi, Y., & Okano, H. (2003). Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS and BTB transcription factors. Development, 130, 2419–2428.
  • Zhou, Z., Hartwieg, E., & Horvitz, H. R. (2001). CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell, 104, 43–56.
  • Zhu, B., Pennack, J. A., McQuilton, P., Forero, M. G., Mizuguchi, K., Sutcliffe, B., et al. (2008). Drosophila neurotrophins reveal a common mechanism for nervous system formation. PLoS Biol, 6, e284.
  • Ziegenfuss, J. S., Biswas, R., Avery, M. A., Hong, K., Sheehan, A. E., Yeung, Y. G., et al. (2008). Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature, 453, 935–939.

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