Interactions between amyloid precursor protein-like (APPL) and MAGUK scaffolding proteins contribute to appetitive long-term memory in Drosophila melanogaster

References

• Andlauer, T.F.M., Scholz-Kornehl, S., Tian, R., Kirchner, M., Babikir, H.A., Depner, H., … Sigrist, S.J. (2014). Drep-2 is a novel synaptic protein important for learning and memory. eLife, 3, 1–24. doi:10.7554/eLife.03895
   Web of Science ®Google Scholar
• Ashley, J., Packard, M., Ataman, B., & Budnik, V. (2005). Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/mint. Journal of Neuroscience, 25, 5943–5955. doi:10.1523/JNEUROSCI.1144-05.2005
   PubMed Web of Science ®Google Scholar
• Astorga, C., Jorquera, R.A., Ramírez, M., Kohler, A., López, E., Delgado, R., … Sierralta, J. (2016). Presynaptic DLG regulates synaptic function through the localization of voltage-activated Ca2+ channels. Scientific Reports, 6, 14. doi:10.1038/srep32132
   PubMed Web of Science ®Google Scholar
• Balklava, Z., Niehage, C., Currinn, H., Mellor, L., Guscott, B., Poulin, G., … Wassmer, T. (2015). The amyloid precursor protein controls PIKfyve function. PLoS One, 10, e0130485. doi:10.1371/journal.pone.0130485
   PubMed Web of Science ®Google Scholar
• Baust, T., Czupalla, C., Krause, E., Bourel-Bonnet, L., & Hoflack, B. (2006). Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proceedings of the National Academy of Sciences of the United States of America, 103, 3159–3164. doi:10.1073/pnas.0511062103
   PubMed Web of Science ®Google Scholar
• Beher, D., Hesse, L., Masters, C.L., & Multhaup, G. (1996). Regulation of amyloid protein precursor (APP) binding to collagen and mapping of the binding sites on APP and collagen type I. Journal of Biological Chemistry, 271, 1613–1620. doi:10.1074/jbc.271.3.1613
   PubMed Web of Science ®Google Scholar
• Bourdet, I., Preat, T., & Goguel, V. (2015). The full-length form of the Drosophila amyloid precursor protein is involved in memory formation. Journal of Neuroscience, 35, 1043–1051. doi:10.1523/JNEUROSCI.2093-14.2015
   PubMed Web of Science ®Google Scholar
• Bouzaiane, E., Trannoy, S., Scheunemann, L., Plaçais, P.Y., & Preat, T. (2015). Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. Cell Reports, 11, 1280–1292. doi:10.1016/j.celrep.2015.04.044
   PubMed Web of Science ®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.
   PubMed Web of Science ®Google Scholar
• Butz, S., Okamoto, M., & Sudhof, T.C. (1998). A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell, 94, 773–782. doi:10.1016/S0092-8674(00)81736-5
   PubMed Web of Science ®Google Scholar
• Chen, K., & Featherstone, D.E. (2011). Pre and postsynaptic roles for Drosophila CASK. Molecular and Cellular Neuroscience 48, 171–182. doi:10.1016/j.mcn.2011.07.009
   PubMed Web of Science ®Google Scholar
• Cho, K.O., Hunt, C.A., & Kennedy, M.B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron, 9, 929–942. doi:10.1016/0896-6273(92)90245-9
   PubMed Web of Science ®Google Scholar
• Colomb, J., Kaiser, L., Chabaud, M.A., & Preat, T. (2009). Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Genes, Brain and Behavior, 8, 407–415. doi:10.1111/j.1601-183X.2009.00482.x
   PubMed Web of Science ®Google Scholar
• Conboy, L., Murphy, K.J., & Regan, C.M. (2005). Amyloid precursor protein expression in the rat hippocampal dentate gyrus modulates during memory consolidation. Journal of Neurochemistry, 95, 1677–1688. doi:10.1111/j.1471-4159.2005.03484.x
   PubMed Web of Science ®Google Scholar
• Crittenden, J.R., Skoulakis, E.M.C., Han, K.-A., Kalderon, D., & Davis, R.L. (1998). Tripartite mushroom body architecture revealed by antigenic markers. Learning & Memory, 5, 38–51.
   PubMed Web of Science ®Google Scholar
• Currinn, H., Guscott, B., Balklava, Z., Rothnie, A., & Wassmer, T. (2016). APP controls the formation of PI(3,5)P(2) vesicles through its binding of the PIKfyve complex. Cellular and Molecular Life Sciences, 73, 393–408. doi:10.1007/s00018-015-1993-0
   PubMed Web of Science ®Google Scholar
• Doyle, E., Bruce, M.T., Breen, K.C., Smith, D.C., Anderton, B., & Regan, C.M. (1990). Intraventricular infusions of antibodies to amyloid-β-protein precursor impair the acquisition of a passive avoidance response in the rat. Neuroscience Letters, 115, 97–102. doi:10.1016/0304-3940(90)90524-D
   PubMed Web of Science ®Google Scholar
• Ehrlich, I., & Malinow, R. (2004). Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. Journal of Neuroscience, 24, 916–927. doi:10.1523/JNEUROSCI.4733-03.2004
   PubMed Web of Science ®Google Scholar
• Fulterer, A., Andlauer, T.F.M., Ender, A., Maglione, M., Eyring, K., Woitkuhn, J., Lehmann, M., … Sigrist, S.J. (2018). Active zone scaffold protein ratios tune functional diversity across brain synapses. Cell Reports, 23, 1259–1274. doi:10.1016/j.celrep.2018.03.126
   PubMed Web of Science ®Google Scholar
• Goguel, V., Belair, A.-L., Ayaz, D., Lampin-Saint-Amaux, A., Scaplehorn, N., Hassan, B.A., & Preat, T. (2011). Drosophila amyloid precursor protein-like is required for long-term memory. Journal of Neuroscience, 31, 1032–1037. doi:10.1523/JNEUROSCI.2896-10.2011
   PubMed Web of Science ®Google Scholar
• Gross, G.G., Lone, G.M., Leung, L.K., Hartenstein, V., & Guo, M. (2013). X11/Mint genes control polarized localization of axonal membrane proteins in vivo. Journal of Neuroscience, 33, 8575–8586. doi:10.1523/JNEUROSCI.5749-12.2013
   PubMed Web of Science ®Google Scholar
• Gupta, V.K., Pech, U., Bhukel, A., Fulterer, A., Ender, A., Mauermann, S.F., … Sigrist, S.J. (2016). Spermidine suppresses age-associated memory impairment by preventing adverse increase of presynaptic active zone size and release. PLoS Biology, 14, e1002563. doi:10.1371/journal.pbio.1002563
   PubMed Web of Science ®Google Scholar
• Hata, Y., Butz, S., & Südhof, T.C. (1996). CASK: A novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. Journal of Neuroscience, 16, 2488–2494. doi:10.1523/JNEUROSCI.16-08-02488.1996
   PubMed Web of Science ®Google Scholar
• Haynes, P.R., Christmann, B.L., & Griffith, L.C. (2015). A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster. eLife, 4, e03868. doi:10.7554/eLife.03868
   PubMed Web of Science ®Google Scholar
• Heisenberg, M. (2003). Mushroom body memoir: From maps to models. Nature Reviews Neuroscience, 4, 266–275. doi:10.1038/nrn1074
   PubMed Web of Science ®Google Scholar
• Hodge, J.J.L., Mullasseril, P., & Griffith, L.C. (2006). Activity-dependent gating of CaMKII autonomous activity by Drosophila CASK. Neuron, 51, 327–337. doi:10.1016/j.neuron.2006.06.020
   PubMed Web of Science ®Google Scholar
• Hoe, H.S., Fu, Z., Makarova, A., Lee, J.Y., Lu, C., Feng, L., … Rebeck, G.W. (2009). The effects of amyloid precursor protein on postsynaptic composition and activity. Journal of Biological Chemistry, 284, 8495–8506. doi:10.1074/jbc.M900141200
   PubMed Web of Science ®Google Scholar
• Hubner, N.C., Bird, A.W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., … Mann, M. (2010). Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. Journal of Cell Biology, 189, 739–754. doi:10.1083/jcb.200911091
   PubMed Web of Science ®Google Scholar
• Ito, K., Awano, W., Suzuki, K., Hiromi, Y., & Yamamoto, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development, 124, 761–771.
   PubMed Web of Science ®Google Scholar
• Jenett, A., Rubin, G.M., Ngo, T.-T.B., Shepherd, D., Murphy, C., Dionne, H., … Zugates, C.T. (2012). A GAL4-driver line resource for Drosophila neurobiology. Cell Reports, 2, 991–1001. doi:10.1016/j.celrep.2012.09.011
   PubMed Web of Science ®Google Scholar
• Kim, E., Cho, K.O., Rothschild, A., & Sheng, M. (1996). Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins. Neuron, 17, 103–113. doi:10.1016/S0896-6273(00)80284-6
   PubMed Web of Science ®Google Scholar
• Kim, E., & Sheng, M. (2004). PDZ domain proteins of synapses. Nature Reviews Neuroscience, 5, 771–781. doi:10.1038/nrn1517
   PubMed Web of Science ®Google Scholar
• Kittel, R.J., Wichmann, C., Rasse, T.M., Fouquet, W., Schmidt, M., Schmid, A., … Sigrist, S.J. (2006). Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science, 312, 1051–1054. doi:10.1126/science.1126308
   PubMed Web of Science ®Google Scholar
• Krashes, M.J., Keene, A.C., Leung, B., Armstrong, J.D., & Waddell, S. (2007). Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron, 53, 103–115. doi:10.1016/j.neuron.2006.11.021
   PubMed Web of Science ®Google Scholar
• Krashes, M.J., & Waddell, S. (2008). Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. Journal of Neuroscience, 28, 3103–3113. doi:10.1523/JNEUROSCI.5333-07.2008
   PubMed Web of Science ®Google Scholar
• Lee, P.-T., Lin, H.-W., Chang, Y.-H., Fu, T.-F., Dubnau, J., Hirsh, J., … Chiang, A.-S. (2011). Serotonin-mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 108, 13794–13799. doi:10.1073/pnas.1019483108
   PubMed Web of Science ®Google Scholar
• Leonoudakis, D., Conti, L.R., Radeke, C.M., McGuire, L.M.M., & Vandenberg, C.A. (2004). A Multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels. Journal of Biological Chemistry, 279, 19051–19063. doi:10.1074/jbc.M400284200
   PubMed Web of Science ®Google Scholar
• Lin, E.I., Jeyifous, O., & Green, W.N. (2013). CASK regulates SAP97 conformation and its interactions with AMPA and NMDA receptors. Journal of Neuroscience, 33, 12067–12076. doi:10.1523/JNEUROSCI.0816-13.2013
   PubMed Web of Science ®Google Scholar
• Luo, L.Q., Martin-Morris, L.E., & White, K. (1990). Identification, secretion, and neural expression of APPL, a Drosophila protein similar to human amyloid protein precursor. Journal of Neuroscience, 10, 3849–3861. doi:10.1523/JNEUROSCI.10-12-03849.1990
   PubMed Web of Science ®Google Scholar
• Mackler, J.M., Drummond, J.A., Loewen, C.A., Robinson, I.M., & Reist, N.E. (2002). The C2B Ca2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature, 418, 340–344. doi:10.1038/nature00846
   PubMed Web of Science ®Google Scholar
• Malik, B.R., Gillespie, J.M., & Hodge, J.J.L. (2013). CASK and CaMKII function in the mushroom body α'/β' neurons during Drosophila memory formation. Frontiers in Neural Circuits, 7, 52. doi:10.3389/fncir.2013.00052
   PubMed Web of Science ®Google Scholar
• Marcello, E., Gardoni, F., Mauceri, D., Romorini, S., Jeromin, A., Epis, R., … Di Luca, M. (2007). Synapse-associated protein-97 mediates alpha-secretase ADAM10 trafficking and promotes its activity. Journal of Neuroscience, 27, 1682–1691. doi:10.1523/JNEUROSCI.3439-06.2007
   PubMed Web of Science ®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. doi:10.1126/science.1089035
   PubMed Web of Science ®Google Scholar
• Montagna, E., Dorostkar, M.M., & Herms, J. (2017). The role of APP in structural spine plasticity. Frontiers in Molecular Neuroscience, 10, 1–7. doi:10.3389/fnmol.2017.00136
   PubMed Web of Science ®Google Scholar
• Mucke, L., & Selkoe, D.J. (2012). Neurotoxicity of amyloid β-protein: Synaptic and network dysfunction. Cold Spring Harbor Perspectives in Medicine, 2, a006338. doi:10.1101/cshperspect.a006338
   PubMed Web of Science ®Google Scholar
• Niehage, C., Stange, C., Anitei, M., & Hoflack, B. (2014). Liposome-based assays to study membrane-associated protein networks. Methods in Enzymology, 534, 223–243. doi:10.1016/B978-0-12-397926-1.00013-5
   PubMed Web of Science ®Google Scholar
• Okamoto, M., & Südhof, T.C. (1997). Mints, Munc 18-interacting proteins in synaptic vesicle exocytosis. Journal of Biological Chemistry, 272, 31459–31464. doi:10.1074/jbc.272.50.31459
   PubMed Web of Science ®Google Scholar
• Oliva, C., Escobedo, P., Astorga, C., Molina, C., & Sierralta, J. (2012). Role of the MAGUK protein family in synapse formation and function. Developmental Neurobiology, 72, 57–72. doi:10.1002/dneu.20949
   PubMed Web of Science ®Google Scholar
• Palop, J.J., & Mucke, L. (2010). Amyloid-Β-induced neuronal dysfunction in Alzheimer’s disease: From synapses toward neural networks. Nature Neuroscience, 13, 812–818. doi:10.1038/nn.2583
   PubMed Web of Science ®Google Scholar
• Pocha, S.M., Wassmer, T., Niehage, C., Hoflack, B., & Knust, E. (2011). Retromer controls epithelial cell polarity by trafficking the apical determinant crumbs. Current Biology, 21, 1111–1117. doi:10.1016/j.cub.2011.05.007
   PubMed Web of Science ®Google Scholar
• Poo, M.M., Pignatelli, M., Ryan, T.J., Tonegawa, S., Bonhoeffer, T., Martin, K.C., … Stevens, C. (2016). What is memory? The present state of the engram. BMC Biology, 14, 40. doi:10.1186/s12915-016-0261-6
   PubMed Web of Science ®Google Scholar
• Porter, A.P., White, G.R.M., Mack, N.A., & Malliri, A. (2019). The interaction between CASK and the tumour suppressor Dlg1 regulates mitotic spindle orientation in mammalian epithelia. Journal of Cell Science, 132, jcs230086. doi:10.1242/jcs.230086
   PubMed Web of Science ®Google Scholar
• Preat, T., & Goguel, V. (2016). Role of Drosophila amyloid precursor protein in memory formation. Frontiers in Molecular Neuroscience, 9, 1–7. doi:10.3389/fnmol.2016.00142
   PubMed Web of Science ®Google Scholar
• Rice, H.C., Young-Pearse, T.L., & Selkoe, D.J. (2013). Systematic evaluation of candidate ligands regulating ectodomain shedding of amyloid precursor protein. Biochemistry, 52, 3264–3277. doi:10.1021/bi400165f
   PubMed Web of Science ®Google Scholar
• Rieche, F., Carmine-Simmen, K., Poeck, B., Kretzschmar, D., & Strauss, R. (2018). Drosophila full-length amyloid precursor protein is required for visual working memory and prevents age-related memory impairment. Current Biology, 28, 817–823. doi:10.1016/j.cub.2018.01.077
   PubMed Web of Science ®Google Scholar
• Shariati, S.A.M., & De Strooper, B. (2013). Redundancy and divergence in the amyloid precursor protein family. FEBS Letters, 587, 2036–2045. doi:10.1016/j.febslet.2013.05.026
   PubMed Web of Science ®Google Scholar
• Slomnicki, L.P., & Lesniak, W. (2008). A putative role of the amyloid precursor protein (APP) intracellular domain (AICD) in transcription. Acta Neurobiologiae Experimentalis, 68, 219–228.
   PubMed Web of Science ®Google Scholar
• Soukup, S.F., Pocha, S.M., Yuan, M., & Knust, E. (2013). DLin-7 is required in postsynaptic lamina neurons to prevent light-induced photoreceptor degeneration in Drosophila. Current Biology, 23, 1349–1354. doi:10.1016/j.cub.2013.05.060
   PubMed Web of Science ®Google Scholar
• Styr, B., & Slutsky, I. (2018). Imbalance between firing homeostasis and synaptic plasticity drives early-phase Alzheimer’s disease. Nature Neuroscience, 21, 463–473. doi:10.1038/s41593-018-0080-x
   PubMed Web of Science ®Google Scholar
• Südhof, T.C. (2004). The synaptic vesicle cycle. Annual Review of Neuroscience, 27, 509–547. doi:10.1146/annurev.neuro.26.041002.131412
   PubMed Web of Science ®Google Scholar
• Tejedor, F.J., Bokhari, A., Rogero, O., Gorczyca, M., Zhang, J., Kim, E., … Budnik, V. (1997). Essential role for dlg in synaptic clustering of Shaker K + channels in vivo. Journal of Neuroscience, 17, 152–159. doi:10.1523/JNEUROSCI.17-01-00152.1997
   PubMed Web of Science ®Google Scholar
• Tempel, B.L., Bonini, N., Dawson, D.R., & Quinn, W.G. (1983). Reward learning in normal and mutant Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 80, 1482–1486. doi:10.1073/pnas.80.5.1482
   PubMed Web of Science ®Google Scholar
• Thomas, U., Kobler, O., & Gundelfinger, E.D. (2010). The Drosophila larval neuromuscular junction as a model for scaffold complexes at glutamatergic synapses: Benefits and limitations. Journal of Neurogenetics, 24, 109–119. doi:10.3109/01677063.2010.493589
   PubMed Web of Science ®Google Scholar
• Torroja, L., Luo, L., & White, K. (1996). APPL, the Drosophila member of the APP-family, exhibits differential trafficking and processing in CNS neurons. Journal of Neuroscience, 16, 4638–4650. doi:10.1523/JNEUROSCI.16-15-04638.1996
   PubMed Web of Science ®Google Scholar
• Torroja, L., Packard, M., Gorczyca, M., White, K., & Budnik, V. (1999). The Drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. Journal of Neuroscience, 19, 7793–7803. doi:10.1523/JNEUROSCI.19-18-07793.1999
   PubMed Web of Science ®Google Scholar
• Trannoy, S., Redt-Clouet, C., Dura, J.M., & Preat, T. (2011). Parallel processing of appetitive short- and long-term memories in Drosophila. Current Biology, 21, 1647–1653. doi:10.1016/j.cub.2011.08.032
   PubMed Web of Science ®Google Scholar
• Turrel, O., Goguel, V., & Preat, T. (2017). Drosophila neprilysin 1 rescues memory deficits caused by amyloid-β peptide. Journal of Neuroscience, 37, 10334–10345. doi:10.1523/JNEUROSCI.1634-17.2017
   PubMed Web of Science ®Google Scholar
• Turrel, O., Lampin-Saint-Amaux, A., Preat, T., & Goguel, V. (2016). Drosophila neprilysins are involved in middle-term and long-term memory. Journal of Neuroscience, 36, 9535–9546. doi:10.1523/JNEUROSCI.3730-15.2016
   PubMed Web of Science ®Google Scholar
• Walter, A.M., Böhme, M.A., & Sigrist, S.J. (2018). Vesicle release site organization at synaptic active zones. Neuroscience Research, 127, 3–13. doi:10.1016/j.neures.2017.12.006
   PubMed Web of Science ®Google Scholar
• Wang, Z., Wang, B., Yang, L., Guo, Q., Aithmitti, N., Songyang, Z., & Zheng, H. (2009). Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. Journal of Neuroscience, 29, 10788–10801. doi:10.1523/JNEUROSCI.2132-09.2009
   PubMed Web of Science ®Google Scholar
• Williamson, T.G., Mok, S.S., Henry, A., Cappai, R., Lander, A.D., Nurcombe, V., … Small, D.H. (1996). Secreted glypican binds to the amyloid precursor protein of Alzheimer’s disease (APP) and inhibits APP-induced neurite outgrowth. Journal of Biological Chemistry, 271, 31215–31221. doi:10.1074/jbc.271.49.31215
   PubMed Web of Science ®Google Scholar
• Woods, D.F., & Bryant, P.J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell, 66, 451–464. doi:10.1016/0092-8674(81)90009-X
   PubMed Web of Science ®Google Scholar
• Yang, M.Y., Armstrong, J.D., Vilinsky, I., Strausfeld, N.J., & Kaiser, K. (1995). Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron, 15, 45–54. doi:10.1016/0896-6273(95)90063-2
   PubMed Web of Science ®Google Scholar
• Yang, C.H., Shih, M.F.M., Chang, C.C., Chiang, M.H., Shih, H.W., Tsai, Y.L., Chiang, A.S., … Wu, C.L. (2016). Additive expression of consolidated memory through Drosophila mushroom body subsets. PLoS Genetics, 12, e1006061. doi:10.1371/journal.pgen.1006061
   PubMed Web of Science ®Google Scholar
• Zheng, H., & Koo, E.H. (2011). Biology and pathophysiology of the amyloid precursor protein. Molecular Neurodegeneration, 6, 1–16. doi:10.1186/1750-1326-6-27
   PubMed Web of Science ®Google Scholar