Skip to main content
SpringerLink
Log in

Unraveling Alzheimer’s Disease Using Drosophila

  • Chapter
  • First Online:
Insights into Human Neurodegeneration: Lessons Learnt from Drosophila

Abstract

Alzheimer’s disease (AD) is a debilitating neurodegenerative disorder that predominantly affects people aged over 65 years. AD is marked by cognitive deficits and memory problems that worsen with age and ultimately results in death. Pathology of AD includes aggregation of the amyloid beta peptide into extracellular plaques and the presence of hyperphosphorylated tau in intracellular neurofibrillary tangles. Given that many factors are involved in the disease along with the ability to study individual aspects of disease pathology under controlled conditions, several genetically tractable animal models have been developed. Despite years of research, treatments remain limited and many therapies that yield promising data in animal models fail to translate it in humans. Here, we discuss the use of a highly versatile Drosophila melanogaster (aka fruit fly) model to study AD. The genetic machinery is conserved from fly to humans. The Drosophila eye has proved to be a genetically tractable model to study neurodegenerative disorders and for genetic and chemical screens. We highlight the utility of modeling AD by expressing human Aβ42 in the developing Drosophila retina. This system has been used recently to uncover new factors involved in the pathological activation of cell death pathways in AD. We discuss these findings and their role in the search for new disease treatments.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abramov, A. Y., Canevari, L., & Duchen, M. R. (2004). Calcium signals induced by amyloid beta peptide and their consequences in neurons and astrocytes in culture. Biochimica et Biophysica Acta, 1742, 81–87.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, A. G., Marfil, V., & Li, C. (2014). Use of Caenorhabditis elegans as a model to study Alzheimer’s disease and other neurodegenerative diseases. Frontiers in Genetics, 5, 279.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alzheimer’s Association. (2018). 2018 Alzheimer’s disease facts and figures. Alzheimers Dement, 14, 367–429.

    Article  Google Scholar 

  • Arnés, M., Casas-Tintó, S., Malmendal, A., & Ferrús, A. (2017). Amyloid β42 peptide is toxic to non-neural cells in Drosophila yielding a characteristic metabolite profile and the effect can be suppressed by PI3K. Biology Open, 6, 1664–1671.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bagyinszky, E., Youn, Y. C., An, S. S., & Kim, S. (2014). The genetics of Alzheimer’s disease. Clinical Interventions in Aging, 9, 535–551.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bassett, A. R., Tibbit, C., Ponting, C. P., & Liu, J. L. (2013). Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Reports, 4, 220–228.

    Google Scholar 

  • Belfiori-Carrasco, L. F., Marcora, M. S., Bocai, N. I., Ceriani, M. F., Morelli, L., & Castaño, E. M. (2017). A novel genetic screen identifies modifiers of age-dependent amyloid β toxicity in the. Frontiers in Aging Neuroscience, 9, 61.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellen, H. J., Tong, C., & Tsuda, H. (2010). 100 years of Drosophila research and its impact on vertebrate neuroscience: A history lesson for the future. Nature Reviews. Neuroscience, 11, 514–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bier, E. (2005). Drosophila, the golden bug, emerges as a tool for human genetics. Nature Reviews Genetics, 6, 9–23.

    Article  CAS  PubMed  Google Scholar 

  • Bolkan, B. J., & Kretzschmar, D. (2014). Loss of Tau results in defects in photoreceptor development and progressive neuronal degeneration in Drosophila. Developmental Neurobiology, 74, 1210–1225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonini, N. M., & Fortini, M. E. (2003). Human neurodegenerative disease modeling using Drosophila. Annual Review of Neuroscience, 26, 627–656.

    Article  CAS  PubMed  Google Scholar 

  • Brand, A. H., & Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401–415.

    CAS  PubMed  Google Scholar 

  • Cao, W., Song, H. J., Gangi, T., Kelkar, A., Antani, I., Garza, D., & Konsolaki, M. (2008). Identification of novel genes that modify phenotypes induced by Alzheimer’s beta-amyloid overexpression in Drosophila. Genetics, 178, 1457–1471.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carmine-Simmen, K., Proctor, T., Tschäpe, J., Poeck, B., Triphan, T., Strauss, R., & Kretzschmar, D. (2009). Neurotoxic effects induced by the Drosophila amyloid-beta peptide suggest a conserved toxic function. Neurobiology of Disease, 33, 274–281.

    Article  CAS  PubMed  Google Scholar 

  • Casas-Tinto, S., Zhang, Y., Sanchez-Garcia, J., Gomez-Velazquez, M., Rincon-Limas, D. E., & Fernandez-Funez, P. (2011). The ER stress factor XBP1s prevents amyloid-beta neurotoxicity. Human Molecular Genetics, 20, 2144–2160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceravolo, R., Borghetti, D., Kiferle, L., Tognoni, G., Giorgetti, A., Neglia, D., Sassi, N., Frosini, D., Rossi, C., Petrozzi, L., et al. (2008). CSF phosporylated TAU protein levels correlate with cerebral glucose metabolism assessed with PET in Alzheimer’s disease. Brain Research Bulletin, 76, 80–84.

    Article  CAS  PubMed  Google Scholar 

  • Chang, H. Y., Sang, T. K., & Chiang, A. S. (2018). Untangling the Tauopathy for Alzheimer’s disease and parkinsonism. Journal of Biomedical Science, 25, 54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chatterjee, S., Sang, T. K., Lawless, G. M., & Jackson, G. R. (2009). Dissociation of tau toxicity and phosphorylation: Role of GSK-3beta, MARK and Cdk5 in a Drosophila model. Human Molecular Genetics, 18(1), 164–177.

    Article  CAS  PubMed  Google Scholar 

  • Chishti, M. A., Yang, D. S., Janus, C., Phinney, A. L., Horne, P., Pearson, J., Strome, R., Zuker, N., Loukides, J., French, J., Turner, S., Lozza, G., Grilli, M., Kunicki, S., Morissette, C., Paquette, J., Gervais, F., Bergeron, C., Fraser, P. E., Carlson, G. A., George-Hyslop, P. S., & Westaway, D. (2001). Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. The Journal of Biological Chemistry, 276(24), 21562–21570.

    Article  CAS  PubMed  Google Scholar 

  • Cline, E. N., Bicca, M. A., Viola, K. L., & Klein, W. L. (2018). The amyloid-β oligomer hypothesis: Beginning of the third decade. Journal of Alzheimer’s Disease, 64, S567–S610.

    Google Scholar 

  • Cohen, S. M. (1993). Imaginal disc development. In M. Bate & A. M. Arias (Eds.), The development of Drosophila melanogaster (pp. 747–841). New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Cohen, R. M., Rezai-Zadeh, K., Weitz, T. M., Rentsendorj, A., Gate, D., Spivak, I., Bholat, Y., Vasilevko, V., Glabe, C. G., Breunig, J. J., Rakic, P., Davtyan, H., Agadjanyan, M. G., Kepe, V., Barrio, J. R., Bannykh, S., Szekely, C. A., Pechnick, R. N., & Town, T. (2013). A transgenic Alzheimer rat with plaques, tau pathology, behavioral impairment, oligomeric aβ, and frank neuronal loss. The Journal of Neuroscience, 33(15), 6245–6256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colligris, P., Perez de Lara, M. J., Colligris, B., & Pintor, J. (2018). Ocular manifestations of Alzheimer’s and other neurodegenerative diseases: The prospect of the eye as a tool for the early diagnosis of Alzheimer’s disease. Journal of Ophthalmology, 2018, 8538573.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Connolly, J. B., Roberts, I. J., Armstrong, J. D., Kaiser, K., Forte, M., Tully, T., & O’Kane, C. J. (1996). Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science, 274, 2104–2107.

    Google Scholar 

  • Crowther, D. C., Kinghorn, K. J., Miranda, E., Page, R., Curry, J. A., Duthie, F. A., Gubb, D. C., & Lomas, D. A. (2005). Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer’s disease. Neuroscience, 132, 123–135.

    Article  CAS  PubMed  Google Scholar 

  • Cutler, T., Sarkar, A., Moran, M., Steffensmeier, A., Puli, O. R., Mancini, G., Tare, M., Gogia, N., & Singh, A. (2015). Drosophila eye model to study neuroprotective role of CREB binding protein (CBP) in Alzheimer’s disease. PLoS One, 10, e0137691.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doody, R. S., Aisen, P. S., & Iwatsubo, T. (2013). Semagacestat for treatment of Alzheimer’s disease. The New England Journal of Medicine, 369, 1661.

    Article  CAS  PubMed  Google Scholar 

  • Echeverria, V., Ducatenzeiler, A., Alhonen, L., Janne, J., Grant, S. M., Wandosell, F., Muro, A., Baralle, F., Li, H., Duff, K., Szyf, M., & Cuello, A. C. (2004). Rat transgenic models with a phenotype of intracellular Abeta accumulation in hippocampus and cortex. Journal of Alzheimer’s Disease, 6(3), 209–219.

    Google Scholar 

  • Fernandez-Funez, P., Sanchez-Garcia, J., & Rincon-Limas, D. E. (2013). Unraveling the basis of neurodegeneration using the Drosophila eye. In Molecular genetics of axial patterning, growth and disease in the Drosophila eye. New York: Springer.

    Google Scholar 

  • Fernandez-Funez, P., Sanchez-Garcia, J., de Mena, L., Zhang, Y., Levites, Y., Khare, S., Golde, T. E., & Rincon-Limas, D. E. (2016). Holdase activity of secreted Hsp70 masks amyloid-β42 neurotoxicity in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 113, E5212–E5221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finelli, A., Kelkar, A., Song, H. J., Yang, H., & Konsolaki, M. (2004). A model for studying Alzheimer’s Abeta42-induced toxicity in Drosophila melanogaster. Molecular and Cellular Neurosciences, 26, 365–375.

    Article  CAS  PubMed  Google Scholar 

  • Fossgreen, A., Brückner, B., Czech, C., Masters, C. L., Beyreuther, K., & Paro, R. (1998). Transgenic Drosophila expressing human amyloid precursor protein show gamma-secretase activity and a blistered-wing phenotype. Proceedings of the National Academy of Sciences of the United States of America, 95, 13703–13708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulga, T. A., Elson-Schwab, I., Khurana, V., Steinhilb, M. L., Spires, T. L., Hyman, B. T., & Feany, M. B. (2007). Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nature Cell Biology, 9, 139–148.

    Article  CAS  PubMed  Google Scholar 

  • Gandy, S., Simon, A. J., Steele, J. W., Lublin, A. L., Lah, J. J., Walker, L. C., Levey, A. I., Krafft, G. A., Levy, E., Checler, F., et al. (2010). Days to criterion as an indicator of toxicity associated with human Alzheimer amyloid-beta oligomers. Annals of Neurology, 68, 220–230.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gladstone, M., & Su, T. T. (2011). Chemical genetics and drug screening in Drosophila cancer models. Journal of Genetics and Genomics, 38, 497–504.

    Article  CAS  PubMed  Google Scholar 

  • Glenner, G. G., & Wong, C. W. (1984). Alzheimer’s disease and Down’s syndrome: Sharing of a unique cerebrovascular amyloid fibril protein. Biochemical and Biophysical Research Communications, 122, 1131–1135.

    Article  CAS  PubMed  Google Scholar 

  • Gold, M. (2017). Phase II clinical trials of anti-amyloid β antibodies: When is enough, enough? Alzheimers Dement (NY), 3, 402–409.

    Google Scholar 

  • Goldman, D. P., Fillit, H., & Neumann, P. (2018). Accelerating Alzheimer’s disease drug innovations from the research pipeline to patients. Alzheimers Dement, 14, 833–836.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gratuze, M., Cisbani, G., Cicchetti, F., & Planel, E. (2016). Is Huntington’s disease a tauopathy? Brain, 139, 1014–1025.

    Article  PubMed  Google Scholar 

  • Greeve, I., Kretzschmar, D., Tschäpe, J. A., Beyn, A., Brellinger, C., Schweizer, M., Nitsch, R. M., & Reifegerste, R. (2004). Age-dependent neurodegeneration and Alzheimer-amyloid plaque formation in transgenic Drosophila. The Journal of Neuroscience, 24, 3899–3906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., & Binder, L. I. (1986). Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proceedings of the National Academy of Sciences of the United States of America, 83, 4913–4917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen, D. V., Hanson, J. E., & Sheng, M. (2018). Microglia in Alzheimer’s disease. The Journal of Cell Biology, 217, 459–472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardy, J., & Selkoe, D. J. (2002). The amyloid hypothesis of Alzheimer’s disease: Progress and problems on the road to therapeutics. Science, 297, 353–356.

    Article  CAS  PubMed  Google Scholar 

  • Hartley, S. L., Handen, B. L., Devenny, D., Mihaila, I., Hardison, R., Lao, P. J., Klunk, W. E., Bulova, P., Johnson, S. C., & Christian, B. T. (2017). Cognitive decline and brain amyloid-β accumulation across 3 years in adults with Down syndrome. Neurobiology of Aging, 58, 68–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hazelett, D. J., Bourouis, M., Walldorf, U., & Treisman, J. E. (1998). Decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development, 125(18), 3741–3751.

    CAS  PubMed  Google Scholar 

  • He, Y., & Jasper, H. (2014). Studying aging in Drosophila. Methods, 68, 129–133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert, L. E., Weuve, J., Scherr, P. A., & Evans, D. A. (2013). Alzheimer disease in the United States (2010–2050) estimated using the 2010 census. Neurology, 80, 1778–1783.

    Article  PubMed  PubMed Central  Google Scholar 

  • Held, L. I. J. (2002). The eye disc. In L. I. Held (Ed.), Imaginal disc (pp. 197–236). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Hornsten, A., Lieberthal, J., Fadia, S., Malins, R., Ha, L., Xu, X., Daigle, I., Markowitz, M., O’Connor, G., Plasterk, R., & Li, C. (2007). APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proceedings of the National Academy of Sciences of the United States of America, 104(6), 1971–1976.

    Google Scholar 

  • Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., & Cole, G. (1996). Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science, 274(5284), 99–102.

    Article  CAS  PubMed  Google Scholar 

  • Iijima, K., Liu, H. P., Chiang, A. S., Hearn, S. A., Konsolaki, M., & Zhong, Y. (2004). Dissecting the pathological effects of human Abeta40 and Abeta42 in Drosophila: A potential model for Alzheimer’s disease. Proceedings of the National Academy of Sciences of the United States of America, 101, 6623–6628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iijima-Ando, K., & Iijima, K. (2010). Transgenic Drosophila models of Alzheimer’s disease and tauopathies. Brain Structure & Function, 214, 245–262.

    Article  CAS  Google Scholar 

  • Iliadi, K. G., Knight, D., & Boulianne, G. L. (2012). Healthy aging – Insights from Drosophila. Frontiers in Physiology, 3, 106.

    Article  PubMed  PubMed Central  Google Scholar 

  • Isik, A. T. (2010). Late onset Alzheimer’s disease in older people. Clinical Interventions in Aging, 5, 307–311.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jäättelä, M., Wissing, D., Kokholm, K., Kallunki, T., & Egeblad, M. (1998). Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. The EMBO Journal, 17, 6124–6134.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jack, C. R., Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Haeberlein, S. B., Holtzman, D. M., Jagust, W., Jessen, F., Karlawish, J., et al. (2018). NIA-AA Research Framework: Toward a biological definition of Alzheimer’s disease. Alzheimers Dement, 14, 535–562.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jankowsky, J. L., & Zheng, H. (2017). Practical considerations for choosing a mouse model of Alzheimer’s disease. Molecular Neurodegeneration, 12, 89.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jankowsky, J. L., Fadale, D. J., Anderson, J., Xu, G. M., Gonzales, V., Jenkins, N. A., Copeland, N. G., Lee, M. K., Younkin, L. H., Wagner, S. L., Younkin, S. G., & Borchelt, D. R. (2004). Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: Evidence for augmentation of a 42-specific gamma secretase. Human Molecular Genetics, 13(2), 159–170.

    Article  CAS  PubMed  Google Scholar 

  • Jeon, Y., Lee, S., Shin, M., Lee, J. H., Suh, Y. S., Hwang, S., Yun, H. S., & Cho, K. S. (2017). Phenotypic differences between Drosophila Alzheimer’s disease models expressing human Aβ42 in the developing eye and brain. Animal Cells and Systems (Seoul), 21, 160–168.

    Article  CAS  Google Scholar 

  • Joshi, P., Liang, J. O., DiMonte, K., Sullivan, J., & Pimplikar, S. W. (2009). Amyloid precursor protein is required for convergent-extension movements during zebrafish development. Developmental Biology, 335(1), 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Karin, M., Liu, Z., & Zandi, E. (1997). AP-1 function and regulation. Current Opinion in Cell Biology, 9, 240–246.

    Article  CAS  PubMed  Google Scholar 

  • Khurana, V., Lu, Y., Steinhilb, M. L., Oldham, S., Shulman, J. M., & Feany, M. B. (2006). TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Current Biology, 16(3), 230–241.

    Article  CAS  PubMed  Google Scholar 

  • King, A. (2018). The search for better animal models of Alzheimer’s disease. Nature, 559, S13–S15.

    Article  CAS  PubMed  Google Scholar 

  • Klunk, W. E., Engler, H., Nordberg, A., Bacskai, B. J., Wang, Y., Price, J. C., Bergström, M., Hyman, B. T., Långström, B., & Mathis, C. A. (2003). Imaging the pathology of Alzheimer’s disease: Amyloid-imaging with positron emission tomography. Neuroimaging Clinics of North America, 13(781–789), ix.

    Google Scholar 

  • Kosik, K. S., Joachim, C. L., & Selkoe, D. J. (1986). Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proceedings of the National Academy of Sciences of the United States of America, 83, 4044–4048.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruppa, A. J., Ott, S., Chandraratna, D. S., Irving, J. A., Page, R. M., Speretta, E., Seto, T., Camargo, L. M., Marciniak, S. J., Lomas, D. A., et al. (2013). Suppression of Aβ toxicity by puromycin-sensitive aminopeptidase is independent of its proteolytic activity. Biochimica et Biophysica Acta, 1832, 2115–2126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, J. P. (2011). My what big eyes you have: How the Drosophila retina grows. Developmental Neurobiology, 71, 1133–1152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutoku, Y., Ohsawa, Y., Kuwano, R., Ikeuchi, T., Inoue, H., Ataka, S., Shimada, H., Mori, H., & Sunada, Y. (2015). A second pedigree with amyloid-less familial Alzheimer’s disease harboring an identical mutation in the amyloid precursor protein gene (E693delta). Internal Medicine, 54, 205–208.

    Article  PubMed  Google Scholar 

  • Lee, V. M., Balin, B. J., Otvos, L., & Trojanowski, J. Q. (1991). A68: A major subunit of paired helical filaments and derivatized forms of normal Tau. Science, 251, 675–678.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S., Bang, S. M., Hong, Y. K., Lee, J. H., Jeong, H., Park, S. H., Liu, Q. F., Lee, I. S., & Cho, K. S. (2016). The calcineurin inhibitor Sarah (Nebula) exacerbates Aβ42 phenotypes in a Drosophila model of Alzheimer’s disease. Disease Models & Mechanisms, 9, 295–306.

    Article  CAS  Google Scholar 

  • Lenz, S., Karsten, P., Schulz, J. B., & Voigt, A. (2013). Drosophila as a screening tool to study human neurodegenerative diseases. Journal of Neurochemistry, 127, 453–460.

    Article  CAS  PubMed  Google Scholar 

  • Levitan, D., Doyle, T. G., Brousseau, D., Lee, M. K., Thinakaran, G., Slunt, H. H., Sisodia, S. S., & Greenwald, I. (1996). Assessment of normal and mutant human presenilin function in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 93(25), 14940–14944.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, D. M., & Goodman, C. S. (1994). Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron, 13, 507–523.

    Article  CAS  PubMed  Google Scholar 

  • Link, C. D. (1995). Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 92(20), 9368–9372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, H., Han, M., Li, Q., Zhang, X., Wang, W. A., & Huang, F. D. (2015a). Automated rapid iterative negative geotaxis assay and its use in a genetic screen for modifiers of Aβ(42)-induced locomotor decline in Drosophila. Neuroscience Bulletin, 31, 541–549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Q. F., Lee, J. H., Kim, Y. M., Lee, S., Hong, Y. K., Hwang, S., Oh, Y., Lee, K., Yun, H. S., Lee, I. S., et al. (2015b). In vivo screening of traditional medicinal plants for neuroprotective activity against Aβ42 cytotoxicity by using Drosophila models of Alzheimer’s disease. Biological & Pharmaceutical Bulletin, 38, 1891–1901.

    Article  CAS  Google Scholar 

  • Lleó, A., Blesa, R., Queralt, R., Ezquerra, M., Molinuevo, J. L., Peña-Casanova, J., Rojo, A., & Oliva, R. (2002). Frequency of mutations in the presenilin and amyloid precursor protein genes in early-onset Alzheimer disease in Spain. Archives of Neurology, 59, 1759–1763.

    Article  PubMed  Google Scholar 

  • Loy, C. T., Schofield, P. R., Turner, A. M., & Kwok, J. B. (2014). Genetics of dementia. Lancet, 383, 828–840.

    Article  CAS  PubMed  Google Scholar 

  • Luna, S., Cameron, D. J., & Ethell, D. W. (2013). Amyloid-β and APP deficiencies cause severe cerebrovascular defects: Important work for an old villain. PLoS One, 8(9), e75052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, L., Tully, T., & White, K. (1992). Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron, 9, 595–605.

    Article  CAS  PubMed  Google Scholar 

  • Marder, K. (2010). Tarenflurbil in patients with mild Alzheimer’s disease. Current Neurology and Neuroscience Reports, 10, 336–337.

    Article  PubMed  Google Scholar 

  • Martin-Blanco, E., Gampel, A., Ring, J., Virdee, K., Kirov, N., Tolkovsky, A. M., & Martinez-Arias, A. (1998). Puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes & Development, 12, 557–570.

    Article  CAS  Google Scholar 

  • Martin-Peña, A., Rincon-Limas, D. E., & Fernandez-Funez, P. (2017). Anti-Aβ single-chain variable fragment antibodies restore memory acquisition in a Drosophila model of Alzheimer’s disease. Scientific Reports, 7, 11268.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martín-Peña, A., Rincón-Limas, D. E., & Fernandez-Fúnez, P. (2018). Engineered Hsp70 chaperones prevent Aβ42-induced memory impairments in a Drosophila model of Alzheimer’s disease. Scientific Reports, 8, 9915.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masters, C. L., Simms, G., Weinman, N. A., Multhaup, G., McDonald, B. L., & Beyreuther, K. (1985). Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proceedings of the National Academy of Sciences of the United States of America, 82, 4245–4249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthews, K. A., Xu, W., Gaglioti, A. H., Holt, J. B., Croft, J. B., Mack, D., & McGuire, L. C. (2018). Racial and ethnic estimates of Alzheimer’s disease and related dementias in the United States (2015–2060) in adults aged ≥65 years. Alzheimers Dement, 15(1), 17–24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mattsson, N., Zetterberg, H., Hansson, O., Andreasen, N., Parnetti, L., Jonsson, M., Herukka, S. K., van der Flier, W. M., Blankenstein, M. A., Ewers, M., et al. (2009). CSF biomarkers and incipient Alzheimer disease in patients with mild cognitive impairment. JAMA, 302, 385–393.

    Article  CAS  PubMed  Google Scholar 

  • McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K., & Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science, 302, 1765–1768.

    Article  CAS  PubMed  Google Scholar 

  • McGuire, S. E., Mao, Z., & Davis, R. L. (2004). Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Science’s STKE, 2004, pl6.

    PubMed  Google Scholar 

  • McGurk, L., Berson, A., & Bonini, N. M. (2015). Drosophila as an in vivo model for human neurodegenerative disease. Genetics, 201, 377–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology, 34, 939–944.

    Article  CAS  PubMed  Google Scholar 

  • McKoy, A. F., Chen, J., Schupbach, T., & Hecht, M. H. (2012). A novel inhibitor of amyloid β (Aβ) peptide aggregation: From high throughput screening to efficacy in an animal model of Alzheimer disease. The Journal of Biological Chemistry, 287, 38992–39000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mershin, A., Pavlopoulos, E., Fitch, O., Braden, B. C., Nanopoulos, D. V., & Skoulakis, E. M. (2004). Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learning & Memory, 11, 277–287.

    Article  Google Scholar 

  • Migheli, A., Butler, M., Brown, K., & Shelanski, M. L. (1988). Light and electron microscope localization of the microtubule-associated tau protein in rat brain. The Journal of Neuroscience, 8, 1846–1851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirzabekov, T., Lin, M. C., Yuan, W. L., Marshall, P. J., Carman, M., Tomaselli, K., Lieberburg, I., & Kagan, B. L. (1994). Channel formation in planar lipid bilayers by a neurotoxic fragment of the beta-amyloid peptide. Biochemical and Biophysical Research Communications, 202, 1142–1148.

    Article  CAS  PubMed  Google Scholar 

  • Moore, B. D., Martin, J., de Mena, L., Sanchez, J., Cruz, P. E., Ceballos-Diaz, C., Ladd, T. B., Ran, Y., Levites, Y., Kukar, T. L., et al. (2018). Short Aβ peptides attenuate Aβ42 toxicity in vivo. The Journal of Experimental Medicine, 215, 283–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran, M. T., Tare, M., Kango-Singh, M., & Singh, A. (2013). Homeotic gene teashirt (tsh) has a neuroprotective function in amyloid-beta 42 mediated neurodegeneration. PLoS One, 8, e80829.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moses, K., & Rubin, G. M. (1991). Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes & Development, 5, 583–593.

    Article  CAS  Google Scholar 

  • Mosser, D. D., Caron, A. W., Bourget, L., Denis-Larose, C., & Massie, B. (1997). Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Molecular and Cellular Biology, 17, 5317–5327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller, R., Heinrich, M., Heck, S., Blohm, D., & Richter-Landsberg, C. (1997). Expression of microtubule-associated proteins MAP 2 and tau in cultured rat brain oligodendrocytes. Cell and Tissue Research, 288, 239–249.

    Article  PubMed  Google Scholar 

  • Newman, M., Ebrahimie, E., & Lardelli, M. (2014). Using the zebrafish model for Alzheimer’s disease research. Frontiers in Genetics, 5, 189.

    PubMed  PubMed Central  Google Scholar 

  • Nornes, S., Groth, C., Camp, E., Ey, P., & Lardelli, M. (2003). Developmental control of Presenilin1 expression, endoproteolysis, and interaction in zebrafish embryos. Exp Cell Res, 289(1), 124–132.

    Article  CAS  PubMed  Google Scholar 

  • Nornes, S., Newman, M., Verdile, G., Wells, S., Stoick-Cooper, C. L., Tucker, B., Frederich-Sleptsova, I., Martins, R., & Lardelli, M. (2008). Interference with splicing of Presenilin transcripts has potent dominant negative effects on Presenilin activity. Human Molecular Genetics, 17(3), 402–412.

    Article  CAS  PubMed  Google Scholar 

  • Oddo, S., Caccamo, A., Shepherd, J. D., Murphy, M. P., Golde, T. E., Kayed, R., Metherate, R., Mattson, M. P., Akbari, Y., & LaFerla, F. M. (2003). Triple-transgenic model of Alzheimer’s disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction. Neuron, 39(3), 409–421.

    Google Scholar 

  • O’Keefe, L., & Denton, D. (2018). Using Drosophila models of amyloid toxicity to study autophagy in the pathogenesis of Alzheimer’s disease. BioMed Research International, 2018, 5195416.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ortman, J. M., Velkoff, V. A., & Hogan, H. (2014). An aging nation: The older population in the United States. In Current population reports. Washington, DC: U.S. Census Bureau.

    Google Scholar 

  • Pandey, U. B., & Nichols, C. D. (2011). Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacological Reviews, 63, 411–436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papasozomenos, S. C., & Binder, L. I. (1987). Phosphorylation determines two distinct species of Tau in the central nervous system. Cell Motility and the Cytoskeleton, 8, 210–226.

    Article  CAS  PubMed  Google Scholar 

  • Pham, H. M., Xu, A., Schriner, S. E., Sevrioukov, E. A., & Jafari, M. (2018). Cinnamaldehyde improves lifespan and healthspan in Drosophila melanogaster models for Alzheimer’s disease. BioMed Research International, 2018, 3570830.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Phelan, P., Nakagawa, M., Wilkin, M. B., Moffat, K. G., O’Kane, C. J., Davies, J. A., & Bacon, J. P. (1996). Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. The Journal of Neuroscience, 16(3), 1101–1113.

    Google Scholar 

  • Ray, A., Speese, S. D., & Logan, M. A. (2017). Glial Draper rescues AB toxicity in a Drosophila model of Alzheimer’s disease. The Journal of Neuroscience, 37, 11881–11893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ready, D. F., Hanson, T. E., & Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Developmental Biology, 53, 217–240.

    Article  CAS  PubMed  Google Scholar 

  • Reiter, L. T., Potocki, L., Chien, S., Gribskov, M., & Bier, E. (2001). A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Research, 11, 1114–1125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, E. R. (2018). Shortened lifespan and other age-related defects in bang sensitive mutants of Drosophila melanogaster. G3: Genes, Genomes, Genetics, 8(12), 3953–3960.

    CAS  Google Scholar 

  • Rival, T., Page, R. M., Chandraratna, D. S., Sendall, T. J., Ryder, E., Liu, B., Lewis, H., Rosahl, T., Hider, R., Camargo, L. M., et al. (2009). Fenton chemistry and oxidative stress mediate the toxicity of the beta-amyloid peptide in a Drosophila model of Alzheimer’s disease. The European Journal of Neuroscience, 29, 1335–1347.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rooke, J., Pan, D., Xu, T., & Rubin, G. M. (1996). KUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis. Science, 273, 1227–1231.

    Article  CAS  PubMed  Google Scholar 

  • Sarkar, A., Irwin, M., Singh, A., & Riccetti, M. (2016). Alzheimer’s disease: The silver tsunami of the 21st century. Neural Regeneration Research, 11, 693–697.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarkar, A., Gogia, N., Glenn, N., Singh, A., Jones, G., Powers, N., Srivastava, A., & Kango-Singh, M. (2018). A soy protein Lunasin can ameliorate amyloid-beta 42 mediated neurodegeneration in Drosophila eye. Scientific Reports, 8, 13545.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Selkoe, D. J., & Hardy, J. (2016). The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Molecular Medicine, 8, 595–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sepp, K. J., Schulte, J., & Auld, V. J. (2001). Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental Biology, 238(1), 47–63.

    Article  CAS  PubMed  Google Scholar 

  • Sevigny, J., Chiao, P., Bussière, T., Weinreb, P. H., Williams, L., Maier, M., Dunstan, R., Salloway, S., Chen, T., Ling, Y., et al. (2016). The antibody aducanumab reduces Aβ plaques in Alzheimer’s disease. Nature, 537, 50–56.

    Article  CAS  PubMed  Google Scholar 

  • Shirwany, N. A., Payette, D., Xie, J., & Guo, Q. (2007). The amyloid beta ion channel hypothesis of Alzheimer’s disease. Neuropsychiatric Disease and Treatment, 3, 597–612.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, A., & Irvine, K. D. (2012). Drosophila as a model for understanding development and disease. Developmental Dynamics, 241, 1–2.

    Article  PubMed  Google Scholar 

  • Singh, A., Lim, J., & Choi, K.-W. (2005). Dorso-ventral boundary is required for organizing growth and planar polarity in the Drosophila eye. In M. Mlodzik (Ed.), Planar cell polarization during development: Advances in developmental biology and biochemistry (pp. 59–91). San Diego: Elsevier Science & Technology Books.

    Chapter  Google Scholar 

  • Singh, A., Tare, M., Puli, O. R., & Kango-Singh, M. (2012). A glimpse into dorso-ventral patterning of the Drosophila eye. Developmental Dynamics, 241, 69–84.

    Article  PubMed  Google Scholar 

  • Singh, S. K., Gaur, R., Kumar, A., Fatima, R., Mishra, L., & Srikrishna, S. (2014). The flavonoid derivative 2-(4′ Benzyloxyphenyl)-3-hydroxy-chromen-4-one protects against Aβ42-induced neurodegeneration in transgenic Drosophila: Insights from in silico and in vivo studies. Neurotoxicity Research, 26, 331–350.

    Article  CAS  PubMed  Google Scholar 

  • Steffensmeier, A. M., Tare, M., Puli, O. R., Modi, R., Nainaparampil, J., Kango-Singh, M., & Singh, A. (2013). Novel neuroprotective function of apical-basal polarity gene crumbs in amyloid beta 42 (aβ42) mediated neurodegeneration. PLoS One, 8, e78717.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Struhl, G., & Greenwald, I. (1999). Presenilin is required for activity and nuclear access of notch in Drosophila. Nature, 398, 522–525.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Y., Yolitz, J., Wang, C., Spangler, E., Zhan, M., & Zou, S. (2013). Aging studies in Drosophila melanogaster. Methods in Molecular Biology, 1048, 77–93.

    Article  CAS  PubMed  Google Scholar 

  • Tan, F. H. P., & Azzam, G. (2017). Drosophila melanogaster: Deciphering Alzheimer’s disease. The Malaysian Journal of Medical Sciences, 24, 6–20.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan, L., Schedl, P., Song, H. J., Garza, D., & 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tare, M., Modi, R. M., Nainaparampil, J. J., Puli, O. R., Bedi, S., Fernandez-Funez, P., Kango-Singh, M., & Singh, A. (2011). Activation of JNK signaling mediates amyloid-ß-dependent cell death. PLoS One, 6, e24361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tare, M., Puli, O. R., & Singh, A. (2013). Molecular genetic mechanisms of axial patterning: Mechanistic insights into generation of axes in the developing eye. In A. Singh & M. Kango-Singh (Eds.), Molecular genetics of axial patterning, growth and disease in the Drosophila eye (pp. 37–75). New York/Heidelberg/Dordrecht/London: Springer.

    Chapter  Google Scholar 

  • Tomiyama, T., Nagata, T., Shimada, H., Teraoka, R., Fukushima, A., Kanemitsu, H., Takuma, H., Kuwano, R., Imagawa, M., Ataka, S., et al. (2008). A new amyloid beta variant favoring oligomerization in Alzheimer’s-type dementia. Annals of Neurology, 63, 377–387.

    Article  CAS  PubMed  Google Scholar 

  • Torroja, L., Chu, H., Kotovsky, I., & White, K. (1999). Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Current Biology, 9, 489–492.

    Article  CAS  PubMed  Google Scholar 

  • Treusch, S., Hamamichi, S., Goodman, J. L., Matlack, K. E., Chung, C. Y., Baru, V., Shulman, J. M., Parrado, A., Bevis, B. J., Valastyan, J. S., Han, H., Lindhagen-Persson, M., Reiman, E. M., Evans, D. A., Bennett, D. A., Olofsson, A., DeJager, P. L., Tanzi, R. E., Caldwell, K. A., Caldwell, G. A., & Lindquist, S. (2011). Functional links between Aβ toxicity, endocytic trafficking, and Alzheimer’s disease risk factors in yeast. Science, 334(6060), 1241–1245.

    Google Scholar 

  • Villain, N., Chételat, G., Grassiot, B., Bourgeat, P., Jones, G., Ellis, K. A., Ames, D., Martins, R. N., Eustache, F., Salvado, O., et al. (2012). Regional dynamics of amyloid-β deposition in healthy elderly, mild cognitive impairment and Alzheimer’s disease: A voxelwise PiB-PET longitudinal study. Brain, 135, 2126–2139.

    Article  PubMed  Google Scholar 

  • Wang, L., Chiang, H. C., Wu, W., Liang, B., Xie, Z., Yao, X., Ma, W., Du, S., & Zhong, Y. (2012). Epidermal growth factor receptor is a preferred target for treating amyloid-β-induced memory loss. Proceedings of the National Academy of Sciences of the United States of America, 109, 16743–16748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Kim, J. R., Lee, S. B., Kim, Y. J., Jung, M. Y., Kwon, H. W., & Ahn, Y. J. (2014). Effects of curcuminoids identified in rhizomes of Curcuma longa on BACE-1 inhibitory and behavioral activity and lifespan of Alzheimer’s disease Drosophila models. BMC Complementary and Alternative Medicine, 14, 88.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wasco, W., Bupp, K., Magendantz, M., Gusella, J. F., Tanzi, R. E., & Solomon, F. (1992). Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid beta protein precursor. Proceedings of the National Academy of Sciences of the United States of America, 89, 10758–10762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, D. W., Tyrer, M., & Shepherd, D. (2000). Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. The Journal of Comparative Neurology, 428, 630–640.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wood, J. G., Mirra, S. S., Pollock, N. J., & Binder, L. I. (1986). Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau). Proceedings of the National Academy of Sciences of the United States of America, 83, 4040–4043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, L., Rosa-Neto, P., Hsiung, G. Y., Sadovnick, A. D., Masellis, M., Black, S. E., Jia, J., & Gauthier, S. (2012). Early-onset familial Alzheimer’s disease (EOFAD). The Canadian Journal of Neurological Sciences, 39, 436–445.

    Article  PubMed  Google Scholar 

  • Yagi, Y., Tomita, S., Nakamura, M., & Suzuki, T. (2000). Overexpression of human amyloid precursor protein in Drosophila. Molecular Cell Biology Research Communications, 4, 43–49.

    Article  CAS  PubMed  Google Scholar 

  • Ye, Y., & Fortini, M. E. (1999). Apoptotic activities of wild-type and Alzheimer’s disease-related mutant presenilins in Drosophila melanogaster. The Journal of Cell Biology, 146, 1351–1364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye, Y., Lukinova, N., & Fortini, M. E. (1999). Neurogenic phenotypes and altered notch processing in Drosophila Presenilin mutants. Nature, 398, 525–529.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Schuellein Chair Endowment Fund to Amit Singh supports Catherine Yeates. Amit Singh is supported by the National Institute of General Medical Sciences (NIGMS) – 1 R15 GM124654-01, Schuellein Chair Endowment Fund, STEM Catalyst Grant, and start-up support from the University of Dayton. Madhuri Kango-Singh is supported by start-up research funds from the University of Dayton, and a subaward from NIH grant R01CA183991 (PI Nakano).

Conflict of Interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biology, University of Dayton, Dayton, OH, USA

    Catherine J. Yeates, Ankita Sarkar, Madhuri Kango-Singh & Amit Singh

  2. Premedical Program, University of Dayton, Dayton, OH, USA

    Madhuri Kango-Singh & Amit Singh

  3. Center for Tissue Regeneration and Engineering at Dayton (TREND), University of Dayton, Dayton, OH, USA

    Madhuri Kango-Singh & Amit Singh

  4. The Integrative Science and Engineering Center, University of Dayton, Dayton, OH, USA

    Madhuri Kango-Singh & Amit Singh

  5. Center for Genomic Advocacy (TCGA), Indiana State University, Terre Haute, IN, USA

    Amit Singh

Authors
  1. Catherine J. Yeates
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ankita Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Madhuri Kango-Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amit Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amit Singh .

Editor information

Editors and Affiliations

  1. Department of Molecular and Human Genetics, Banaras Hindu University, Varanasi, Uttar Pradesh, India

    Mousumi Mutsuddi

  2. Department of Molecular and Human Genetics, Banaras Hindu University, Varanasi, Uttar Pradesh, India

    Ashim Mukherjee

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yeates, C.J., Sarkar, A., Kango-Singh, M., Singh, A. (2019). Unraveling Alzheimer’s Disease Using Drosophila. In: Mutsuddi, M., Mukherjee, A. (eds) Insights into Human Neurodegeneration: Lessons Learnt from Drosophila. Springer, Singapore. https://doi.org/10.1007/978-981-13-2218-1_9

Download citation

Publish with us

Policies and ethics

Search

Navigation