Importin-α2 mediates brain development, learning and memory consolidation in Drosophila

References

• Abramoff, M.D., Magelhaes, P.J., & Ram, S. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.
   Google Scholar
• Ahn, H.J., Hernandez, C.M., Levenson, J.M., Lubin, F.D., Liou, H.C., & Sweatt, J.D. (2008). c-Rel, an NF-kappaB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation. Learning & Memory, 15, 539–549. doi:10.1101/lm.866408
   PubMed Web of Science ®Google Scholar
• Akalal, D.B., Yu, D., & Davis, R.L. (2011). The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants. The Journal of Neuroscience, 31, 5643–5647. doi:10.1523/JNEUROSCI.3190-10.2011
   PubMed Web of Science ®Google Scholar
• Akhtar, A., & Gasser, S.M. (2007). The nuclear envelope and transcriptional control. Nature Reviews Genetics, 8, 507–517. doi:10.1038/nrg2122
   PubMed Web of Science ®Google Scholar
• Alberini, C.M. (2009). Transcription factors in long term memory and synaptic plasticity. Physiological Reviews, 89, 121–145. doi:10.1152/physrev.00017.2008
   PubMed Web of Science ®Google Scholar
• Araya, G.H., Magwire, M.M., Huang, W., Serrano-Negron, Y.L., Mackay, T.F.C., & Anholt, R.R.H. (2015). The genetic basis for variation in olfactory behavior in Drosophila melanogaster. Chemical Senses, 40, 233–243. doi:10.1093/chemse/bjv001
   PubMed Web of Science ®Google Scholar
• Armstrong, J.D., de Belle, J.S., Wang, Z., & Kaiser, K. (1998). Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila . Learning & Memory, 5, 102–114.
   PubMed Web of Science ®Google Scholar
• Asaoka, M., Hanyu-Nakamura, K., Nakamura, A., & Kobayashi, S. (2019). Maternal Nanos inhibits Importin-α2/Pendulin-dependent nuclear import to prevent somatic gene expression in the Drosophila germline. PLOS Genetics, 15, e1008090. doi:10.1371/journal.pgen.1008090
   PubMed Web of Science ®Google Scholar
• Bailey, C.H., & Kandel, E.R. (1994). Structural changes underlying long-term memory storage in Aplysia: A molecular perspective. Sem Neurosci, 6, 35–44. doi:10.1006/smns.1994.1005
   Google Scholar
• Baker, S.E., Lorenzen, J.A., Miller, S.W., Bunch, T.A., Jannuzi, A.L., Ginsberg, M.H., … Brower, D.L. (2002). Genetic interaction between integrins and moleskin, a gene encoding a Drosophila homolog of importin-7. Genetics, 162, 285–296.
   PubMed Web of Science ®Google Scholar
• Behnisch, T., YuanXiang, P., Bethge, P., Parvez, S., Chen, Y., Yu, J., … Kreutz, M.R. (2011). Nuclear translocation of Jacob in hippocampal neurons after stimuli inducing long-term potentiation but not long-term depression. PLoS ONE, 6, e17276. doi:10.1371/journal.pone.0017276
   PubMed Web of Science ®Google Scholar
• Behrens, P., Brinkmann, U., & Wellmann, A. (2003). CSE1L/CAS: Its role in proliferation and apoptosis. Apoptosis, 8, 39–44. doi:10.1023/a:1021644918117
   PubMed Web of Science ®Google Scholar
• Blum, A.L., Li, W., Cressy, M., & Dubnau, J. (2009). Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Current Biology, 19, 1341–1350. doi:10.1016/j.cub.2009.07.016
   PubMed Web of Science ®Google Scholar
• Blumröder, R., Glunz, A., Dunkelberger, B.S., Serway, C.N., Berger, C., Mentzel, B., … Raabe, T. (2016). Mcm3 replicative helicase mutation impairs neuroblast proliferation and memory in Drosophila. Genes, Brain and Behavior, 15, 647–659. doi:10.1111/gbb.12304
   PubMed Web of Science ®Google Scholar
• Boquet, I., Hitier, R., Dumas, M., Chaminade, M., & Préat, T. (2000). Central brain postembryonic development in Drosophila: Implication of genes expressed at the interhemispheric junction. Journal of Neurobiology, 42, 33–48. doi:10.1002/(SICI)1097-4695(200001)42:1<33::AID-NEU4>3.0.CO;2-T
   PubMedGoogle Scholar
• Bosveld, F., Ainslie, A., & Bellaïche, Y. (2017). Sequential activities of Dynein, Mud and Asp in centrosome-spindle coupling maintain centrosome number upon mitosis. Journal of Cell Science, 130, 3557–3567. doi:10.1242/jcs.201350
   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
• Busto, G.U., Cervantes-Sandoval, I., & Davis, R.L. (2010). Olfactory learning in Drosophila. Physiology (Bethesda), 25, 338–346. doi:10.1152/physiol.00026.2010
   PubMed Web of Science ®Google Scholar
• Ch’ng, T.H., DeSalvo, M., Lin, P., Vashisht, A., Wohlschlegel, J.A., & Martin, K.C. (2015). Cell biological mechanisms of activity-dependent synapse to nucleus translocation of CRTC1 in neurons. Frontiers in Molecular Neuroscience, 8, 48.
   PubMed Web of Science ®Google Scholar
• Chen, J.W., Barker, A.R., & Wakefield, J.G. (2015). The Ran pathway in Drosophila melanogaster mitosis. Frontiers in Cell and Developmental Biology, 3, 74. doi:10.3389/fcell.2015.00074
   PubMedGoogle Scholar
• Chen, C.C., Wu, J.K., Lin, H.W., Pai, T.P., Fu, T.F., Wu, C.L., … Chiang, A.S. (2012). Visualizing long-term memory formation in two neurons of the Drosophila brain. Science, 335, 678–685. doi:10.1126/science.1212735
   PubMed Web of Science ®Google Scholar
• Cognigni, P., Felsenberg, J., & Waddell, S. (2018). Do the right thing: Neural network mechanisms of memory formation, expression and update in Drosophila. Current Opinion in Neurobiology, 49, 51–58. doi:10.1016/j.conb.2017.12.002
   PubMed Web of Science ®Google Scholar
• Cox, L.J., Hengst, U., Gurskaya, N.G., Lukyanov, K.A., & Jaffrey, S.R. (2008). Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nature Cell Biology, 10, 149–159. doi:10.1038/ncb1677
   PubMed Web of Science ®Google Scholar
• Crittenden, J.R., Skoulakis, E.M.C., Han, K., 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
• Dasso, M. (2001). Running on Ran: Nuclear transport and the mitotic spindle. Cell, 104, 321–324. doi:10.1016/S0092-8674(01)00218-5
   PubMed Web of Science ®Google Scholar
• de Belle, J.S., & Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science, 263, 692–695. doi:10.1126/science.8303280
   PubMed Web of Science ®Google Scholar
• de Belle, J.S., & Heisenberg, M. (1996). Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: A case study of the mushroom body miniature gene (mbm). Proceedings of the National Academy of Sciences of the United States of America, 93, 9875–9880. doi:10.1073/pnas.93.18.9875
   PubMed Web of Science ®Google Scholar
• de Belle, J.S., & Kanzaki, R. (1999). Protocerebral olfactory processing. In B. S. Hansson (Ed.), Insect Olfaction (pp. 243–281). Stuttgart: Springer Verlag.
   Google Scholar
• Demerec, M. (1950). Biology of Drosophila. New York: John Wiley & Sons.
   Google Scholar
• Dubnau, J., & Chiang, A. S. (2013). Systems memory consolidation in Drosophila. Curr Opin Neurobiol, 23(1), 84–91.
   Google Scholar
• DeZazzo, J., & Tully, T. (1995). Dissection of memory formation: From behavioral pharmacology to molecular genetics. Trends in Neurosciences, 18, 212–218. doi:10.1016/0166-2236(95)93905-D
   PubMed Web of Science ®Google Scholar
• Dias, S.M., Cerione, R.A., & Wilson, K.F. (2010). Unloading RNAs in the cytoplasm: An “importin” task. Nucleus, 1, 139–143. doi:10.4161/nucl.1.2.10919
   PubMed Web of Science ®Google Scholar
• Dunkelberger, B.M. (2008). The effects of mushroom body lobe disruption on learning and memory (Doctoral dissertation). Las Vegas: University of Nevada.
   Google Scholar
• Frank, D.A., & Greenberg, M.E. (1994). CREB: A mediator of long-term memory from mollusks to mammals. Cell, 79, 5–8. doi:10.1016/0092-8674(94)90394-8
   PubMed Web of Science ®Google Scholar
• Gerber, B., Tanimoto, H., & Heisenberg, M. (2004). An engram found? Evaluating the evidence from fruit flies. Current Opinion in Neurobiology, 14, 737–744. doi:10.1016/j.conb.2004.10.014
   PubMed Web of Science ®Google Scholar
• Giarrè, M., Török, I., Schmitt, R., Gorjánácz, M., Kiss, I., & Mechler, B.M. (2002). Patterns of importin-alpha expression during Drosophila spermatogenesis. Journal of Structural Biology, 140, 279–290. doi:10.1016/S1047-8477(02)00543-9
   PubMed Web of Science ®Google Scholar
• Ginsburg, M.L. (2002). Characterization of the pleiotropic effects of the Drosophila gene mushroom body miniature B (Master's thesis). Las Vegas: University of Nevada.
   Google Scholar
• Gorjánácz, M., Ádám, G., Török, I., Mechler, B.M., Szlanka, T., & Kiss, I. (2002). Importin-α2 is critically required for the assembly of ring canals during Drosophila oogenesis. Developmental Biology, 217, 271–282. doi:10.1006/dbio.2002.0827
   Google Scholar
• Gorjánácz, M., Török, I., Pomozi, I., Garab, G., Szlanka, T., Kiss, I., & Mechler, B.M. (2006). Domains of importin-α2 required for ring canal assembly during Drosophila oogenesis. Journal of Structural Biology, 154, 27–41. doi:10.1016/j.jsb.2005.12.007
   PubMed Web of Science ®Google Scholar
• Guven-Ozkan, T., & Davis, R.L. (2014). Functional neuroanatomy of Drosophila olfactory memory formation. Learning & Memory, 21, 519–526. doi:10.1101/lm.034363.114
   PubMed Web of Science ®Google Scholar
• Hanz, S., & Fainzilber, M. (2006). Retrograde signaling in injured nerve – the axon reaction revisited. Journal of Neurochemistry, 99, 13–19. doi:10.1111/j.1471-4159.2006.04089.x
   PubMed Web of Science ®Google Scholar
• Hawk, J.D., & Abel, T. (2011). The role of NR4A transcription factors in memory formation. Brain Research Bulletin, 85, 21–29. doi:10.1016/j.brainresbull.2011.02.001
   PubMed Web of Science ®Google Scholar
• Heisenberg, M. (1980). Mutants of brain structure and function: What is the significance of the mushroom bodies for behavior? In O. Siddiqi, P. Babu, L. M. Hall, & J. C. Hall (Eds.), Development and Neurobiology of Drosophila (pp. 373–390). New York: Plenum.
   Google Scholar
• Heisenberg, M. (1989). Neuronal plasticity and brain function. In H. Rahmann (Ed.), Fundamentals of Memory Formation (pp. 3–45). Stuttgart: Fischer.
   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
• Heisenberg, M., & Böhl, K. (1979). Isolation of anatomical brain mutants of Drosophila by histological means. Zeitschrift für Naturforschung C, 34, 143–147. doi:10.1515/znc-1979-1-228
   Web of Science ®Google Scholar
• Heisenberg, M., Borst, A., Wagner, S., & Byers, D. (1985). Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics, 2, 1–30. doi:10.3109/01677068509100140
   PubMed Web of Science ®Google Scholar
• Heisenberg, M., Heusipp, M., & Wanke, C. (1995). Structural plasticity in the Drosophila brain. The Journal of Neuroscience, 15, 1951–1960. doi:10.1523/JNEUROSCI.15-03-01951.1995
   PubMed Web of Science ®Google Scholar
• Homem, C.C., & Knoblich, J.A. (2012). Drosophila neuroblasts: A model for stem cell biology. Development, 139, 4297–4310. doi:10.1242/dev.080515
   PubMed Web of Science ®Google Scholar
• Hood, J.K., & Silver, P.A. (1998). Cse1p is required for export of Srp1p/importin-alpha from the nucleus in Saccharomyces cerevisiae. Journal of Biological Chemistry, 273, 35142–35146. doi:10.1074/jbc.273.52.35142
   PubMedGoogle Scholar
• Horiuchi, J., Jiang, W., Zhou, H., Wu, P., & Yin, J.C. (2004). Phosphorylation of conserved casein kinase sites regulates cAMP-response element-binding protein DNA binding in Drosophila. Journal of Biological Chemistry, 279, 12117–12125. doi:10.1074/jbc.M212839200
   PubMed Web of Science ®Google Scholar
• Hovhanyan, A., Herter, E.K., Pfannstiel, J., Gallant, P., & Raabe, T. (2014). Drosophila mbm is a nucleolar myc and casein kinase 2 target required for ribosome biogenesis and cell growth of central brain neuroblasts. Molecular and Cellular Biology, 34, 1878–1891. doi:10.1128/MCB.00658-13
   PubMed Web of Science ®Google Scholar
• Hovhanyan, A., & Raabe, T. (2009). Structural brain mutants: Mushroom body defect (mud): A case study. Journal of Neurogenetics, 23, 42–47. doi:10.1080/01677060802471700
   PubMed Web of Science ®Google Scholar
• Isabel, G., Pascual, A., & Préat, T. (2004). Exclusive consolidated memory phases in Drosophila. Science, 304, 1024–1027. doi:10.1126/science.1094932
   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
• Ito, K., & Hotta, Y. (1992). Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Developmental Biology, 149, 134–148. doi:10.1016/0012-1606(92)90270-Q
   PubMed Web of Science ®Google Scholar
• Jacob, P.F., & Waddell, S. (2019). Spaced training forms complementary long-term memories of opposite valence in Drosophila. bioRxiv, 785618. doi:10.1101/785618
   Google Scholar
• Jang, A.R., Moravcevic, K., Saez, L., Young, M.W., & Sehgal, A. (2015). Drosophila TIM binds Importin α1, and acts as an adapter to transport PER to the nucleus. PLOS Genetics, 11, e1004974. doi:10.1371/journal.pgen.1004974
   PubMed Web of Science ®Google Scholar
• Jeffrey, R.A., Ch’ng, T.H., O'Dell, T.J., & Martin, K.C. (2009). Activity-dependent anchoring of importin alpha at the synapse involves regulated binding to the cytoplasmic tail of the NR1-1a subunit of the NMDA receptor. The Journal of Neuroscience, 29, 15613–15620. doi:10.1523/JNEUROSCI.3314-09.2009
   PubMed Web of Science ®Google Scholar
• Jordan, B.A., & Kreutz, M.R. (2009). Nucleocytoplasmic protein shuttling: The direct route in synapse-to-nucleus signaling. Trends in Neurosciences, 32, 392–401. doi:10.1016/j.tins.2009.04.001
   PubMed Web of Science ®Google Scholar
• Kahsai, L., & Zars, T. (2011). Learning and memory in Drosophila: Behavior, genetics, and neural systems. International Review of Neurobiology, 99, 139–167. doi:10.1016/B978-0-12-387003-2.00006-9
   PubMed Web of Science ®Google Scholar
• Kim, I., Kim, D., Han, S.M., Chin, M.U., Nam, H.J., Cho, H.P., … Moon, Y.H. (2000). Truncated form of Importin α 2 identified in breast cancer cell inhibits nuclear import of p53. Journal of Biological Chemistry, 275, 23139–23145. doi:10.1074/jbc.M909256199
   PubMed Web of Science ®Google Scholar
• Kogan, J.H., Frankland, P.W., Blendy, J.A., Coblentz, J., Marowitz, Z., Schütz, G., & Silva, A.J. (1997). Spaced training induces normal long-term memory in CREB mutant mice. Current Biology, 7, 1–11. doi:10.1016/S0960-9822(06)00022-4
   PubMed Web of Science ®Google Scholar
• Korwek, Z., Tudelska, K., Nałęcz-Jawecki, P., Czerkies, M., Prus, W., Markiewicz, J., … Lipniacki, T. (2016). Importins promote high-frequency NF-κB oscillations increasing information channel capacity. Biology Direct, 11, 61. doi:10.1186/s13062-016-0164-z
   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
• Kumar, J.P., Wilkie, G.S., Tekotte, H., Moses, K., & Davis, I. (2001). Perturbing nuclear transport in Drosophila eye imaginal discs causes specific cell adhesion and axon guidance defects. Developmental Biology, 240, 315–325. doi:10.1006/dbio.2001.0468
   PubMed Web of Science ®Google Scholar
• Kurusu, M., Maruyama, Y., Adachi, Y., Okabe, M., Suzuki, E., & Furukubo-Tokunaga, K. (2009). A conserved nuclear receptor, Tailless, is required for efficient proliferation and prolonged maintenance of mushroom body progenitors in the Drosophila brain. Developmental Biology, 326, 224–236. doi:10.1016/j.ydbio.2008.11.013
   PubMed Web of Science ®Google Scholar
• Kutay, U., Bischoff, F.R., Kostka, S., Kraft, R., & Görlich, D. (1997). Export of Importin α from the nucleus is mediated by a specific nuclear transport factor. Cell, 90, 1061–1071. doi:10.1016/S0092-8674(00)80372-4
   PubMed Web of Science ®Google Scholar
• Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–685. doi:10.1038/227680a0
   PubMed Web of Science ®Google Scholar
• Lagasse, F., Moreno, C., Préat, T., & Mery, F. (2012). Functional and evolutionary trade-offs co-occur between two consolidated memory phases in Drosophila melanogaster. Proceedings of the Royal Society - Biological Sciences, 279, 4015–4023. doi:10.1098/rspb.2012.1457
   Google Scholar
• Lai, K.O., Zhao, Y., Ch’ng, T.H., & Martin, K.C. (2008). Importin-mediated retrograde transport of CREB2 from distal processes to the nucleus in neurons. Proceedings of the National Academy of Sciences of the United States of America, 105, 17175–17180. doi:10.1073/pnas.0803906105
   PubMed Web of Science ®Google Scholar
• Lee, Y., Jang, A.R., Francey, L.J., Sehgal, A., & Hogenesch, J.B. (2015). KPNB1 mediates PER/CRY nuclear translocation and circadian clock function. Elife, 4, e08647. doi:10.7554/eLife.08647
   Web of Science ®Google Scholar
• Lee, T., Lee, A., & Luo, L. (1999). Development of the Drosophila mushroom bodies: Sequential generation of three distinct types of neurons from a neuroblast. Development, 126, 4065–4076.
   PubMed Web of Science ®Google Scholar
• Li, Q., Zhang, X., Hu, W., Liang, X., Zhang, F., Wang, L., … Zhong, Y. (2016). Importin-7 mediates memory consolidation through regulation of nuclear translocation of training-activated MAPK in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 113, 3072–3077. doi:10.1073/pnas.1520401113
   PubMed Web of Science ®Google Scholar
• Liu, Z., Steward, R., & Luo, L. (2000). Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nature Cell Biology, 2, 776–783. doi:10.1038/35041011
   PubMed Web of Science ®Google Scholar
• Mason, D.A., Fleming, R.J., & Goldfarb, D.S. (2002). Drosophila melanogaster importin alpha1 and alpha3 can replace importin alpha2 during spermatogenesis but not oogenesis. Genetics, 161, 157–170.
   PubMed Web of Science ®Google Scholar
• McBride, K.M., Banninger, G., McDonald, C., & Reich, N.C. (2002). Regulated nuclear import of the STAT1 transcription factor by direct binding of importin-alpha. Embo J, 21, 1754–1763. doi:10.1093/emboj/21.7.1754
   PubMed Web of Science ®Google Scholar
• McBride, S.M., Choi, C.H., Wang, Y., Liebelt, D., Braunstein, E., Ferreiro, D., … Jongens, T.A. (2005). Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron, 45, 753–764. doi:10.1016/j.neuron.2005.01.038
   PubMed Web of Science ®Google Scholar
• Michel, C.K., Kraft, R., & Restifo, L.L. (2004). Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. The Journal of Neuroscience, 24, 5798–5809. doi:10.1523/JNEUROSCI.1102-04.2004
   PubMed Web of Science ®Google Scholar
• Middeler, G., Zerf, K., Jenovai, S., Thulig, A., Tschödrich-Rotter, M., Kubitscheck, U., & Peters, R. (1997). The tumor suppressor p53 is subject to both nuclear import and export, and both are fast, energy-dependent and lectin-inhibited. Oncogene, 14, 1407–1417. doi:10.1038/sj.onc.1200949
   PubMed Web of Science ®Google Scholar
• Moreau-Fauvarque, C., Taillebourg, E., Boissoneau, E., Mesnard, J., & Dura, J.M. (1998). The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mechanisms of Development, 78, 47–61. doi:10.1016/S0925-4773(98)00147-6
   PubMed Web of Science ®Google Scholar
• Moreau-Fauvarque, C., Taillebourg, E., Préat, T., & Dura, J.-M. (2002). Mutation of linotte causes behavioral defects independently of pigeon in Drosophila. Neuroreport, 13, 2309–2312. doi:10.1097/00001756-200212030-00028
   PubMed Web of Science ®Google Scholar
• Mosca, T.J., & Schwarz, T.L. (2010a). Drosophila Importin-α2 is involved in synapse, axon and muscle development. PLoS ONE, 5, e15223. doi:10.1371/journal.pone.0015223
   PubMed Web of Science ®Google Scholar
• Mosca, T.J., & Schwarz, T.L. (2010b). The nuclear import of Frizzled2-C by Importins-beta11 and alpha2 promotes postsynaptic development. Nature Neuroscience, 13, 935–943. doi:10.1038/nn.2593
   PubMed Web of Science ®Google Scholar
• Oka, M., & Yoneda, Y. (2018). Importin α: Functions as a nuclear transport factor and beyond. Proceedings of the Japan Academy, Series B, Physical and Biological Sciences, 94, 259–274. doi:10.2183/pjab.94.018
   PubMed Web of Science ®Google Scholar
• Pai, T.P., Chen, C.C., Lin, H.H., Chin, A.L., Lai, J.S., Lee, P.T., … Chiang, A.S. (2013). Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. Proceedings of the National Academy of Sciences of the United States of America, 110, 7898–7903. doi:10.1073/pnas.1216336110
   PubMed Web of Science ®Google Scholar
• Pascual, A., & Préat, T. (2001). Localization of long-term memory within the Drosophila mushroom body. Science, 294, 1115–1117. doi:10.1126/science.1064200
   PubMed Web of Science ®Google Scholar
• Pavlopoulos, E., Anezaki, M., & Skoulakis, E.M. (2008). Neuralized is expressed in the alpha/beta lobes of adult Drosophila mushroom bodies and facilitates olfactory long-term memory formation. Proceedings of the National Academy of Sciences of the United States of America, 105, 14674–14679. doi:10.1073/pnas.0801605105
   PubMed Web of Science ®Google Scholar
• Perry, R.B., & Fainzilber, M. (2009). Nuclear transport factors in neuronal function. Seminars in Cell and Developmental Biology, 20, 600–606. doi:10.1016/j.semcdb.2009.04.014
   PubMed Web of Science ®Google Scholar
• Phadnis, N., Hsieh, E., & Malik, H.S. (2012). Birth, death, and replacement of karyopherins in Drosophila. Molecular Biology and Evolution, 29, 1429–1440. doi:10.1093/molbev/msr306
   PubMed Web of Science ®Google Scholar
• Plaçais, P.Y., Trannoy, S., Isabel, G., Aso, Y., Siwanowicz, I., Belliart-Guérin, G., … Préat, T. (2012). Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nature Neuroscience, 15, 592–599. doi:10.1038/nn.3055
   PubMed Web of Science ®Google Scholar
• Presente, A., Boyles, R.S., Serway, C.N., de Belle, J.S., & Andres, A.J. (2004). Notch is required for long-term memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 101, 1764–1768. doi:10.1073/pnas.0308259100
   PubMed Web of Science ®Google Scholar
• Pumroy, R.A., & Cingolani, G. (2015). Diversification of importin-α isoforms in cellular trafficking and disease states. Biochemical Journal, 466, 13–28. doi:10.1042/BJ20141186
   PubMed Web of Science ®Google Scholar
• Qin, H., Cressy, M., Li, W., Coravos, J.S., Izzi, S.A., & Dubnau, J. (2012). Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Current Biology, 22, 608–614. doi:10.1016/j.cub.2012.02.014
   PubMed Web of Science ®Google Scholar
• Renn, S.C., Armstrong, J.D., Yang, M., Wang, Z., An, X., Kaiser, K., & Taghert, P.H. (1999). Genetic analysis of the Drosophila ellipsoid body neuropil: Organization and development of the central complex. Journal of Neurobiology, 41, 189–207. doi:10.1002/(SICI)1097-4695(19991105)41:2<189::AID-NEU3>3.0.CO;2-Q
   PubMedGoogle Scholar
• Reuter, J.E., Nardine, T.M., Penton, A., Billuart, P., Scott, E.K., Usui, T., Uemura, T., & … Uo, L. (2003). A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development, 130, 1203–1213. doi:10.1242/dev.00319
   PubMed Web of Science ®Google Scholar
• Ricker, J.P., & Hirsch, J. (1985). Evolution of an instinct under long-term divergent selection for geotaxis in domesticated populations of Drosophila melanogaster. Journal of Comparative Psychology, 99, 380–390. doi:10.1037//0735-7036.99.4.380
   PubMed Web of Science ®Google Scholar
• Rokia-Mille, B.S., Tinette, S., Engler, G., Arthaud, L., Tares, S., & Robichon, A. (2008). Continued neurogenesis in adult Drosophila as a mechanism for recruiting environmental cue-dependent variants. PLoS ONE, 3, e2395. doi:10.1371/journal.pone.0002395
   PubMed Web of Science ®Google Scholar
• Sachan, N., Mishra, A.K., Mutsuddi, M., & Mukherjee, A. (2013). The Drosophila Importin-α3 is required for nuclear import of notch in vivo and it displays synergistic effects with notch receptor on cell proliferation. PLoS ONE, 8, e68247. doi:10.1371/journal.pone.0068247
   PubMed Web of Science ®Google Scholar
• Séjourné, J., Plaçais, P.Y., Aso, Y., Siwanowicz, I., Trannoy, S., Thoma, V., … Préat, T. (2011). Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nature Neuroscience, 14, 903–910. doi:10.1038/nn.2846
   PubMed Web of Science ®Google Scholar
• Serway, C.N. (2010). Genes involved in mushroom body development and behavior in Drosophila (Doctoral dissertation). Las Vegas: University of Nevada.
   Google Scholar
• Serway, C.N., Kaufman, R.R., Strauss, R., & Steven de Belle, J. (2009). Mushroom bodies enhance initial motor activity in Drosophila. Journal of Neurogenetics, 23, 173–184. doi:10.1080/01677060802572895
   PubMed Web of Science ®Google Scholar
• Siller, H.Q., & Doe, C.Q. (2009). Spindle orientation during asymmetric cell division. Nature Cell Biology, 11, 365–374. doi:10.1038/ncb0409-365
   PubMed Web of Science ®Google Scholar
• Solomon, D.A., Stepto, A., Au, W.H., Adachi, Y., Diaper, D.C., Hall, R., … Hirth, F. (2018). A feedback loop between dipeptide-repeat protein, TDP-43 and karyopherin-α mediates C9orf72-related neurodegeneration. Brain, 141, 2908–2924. doi:10.1093/brain/awy241
   PubMed Web of Science ®Google Scholar
• Sousa-Nunes, R., & Somers, W.G. (2013). Mechanisms of asymmetric progenitor divisions in the Drosophila central nervous system. Advances in Experimental Medicine and Biology, 786, 79–102. doi:10.1007/978-94-007-6621-1
   PubMed Web of Science ®Google Scholar
• Tabone, C.J., & de Belle, J.S. (2011). Second-order conditioning in Drosophila. Learning & Memory, 18, 250–253. doi:10.1101/lm.2035411
   PubMed Web of Science ®Google Scholar
• Takemura, S.Y., Aso, Y., Hige, T., Wong, A., Lu, Z., Xu, C.S., … Scheffer, L.K. (2017). A connectome of a learning and memory center in the adult Drosophila brain. Elife, 6, e26975. doi:10.7554/eLife.26975
   PubMed Web of Science ®Google Scholar
• Thomas, R., Edwards, M., & Marks, R. (1996). Translocation of the retinoblastoma gene product during mitosis. Experimental Cell Research, 223, 227–232. doi:10.1006/excr.1996.0076
   PubMed Web of Science ®Google Scholar
• Thompson, K.R., Otis, K.O., Chen, D.Y., Zhao, Y., O’Dell, T.J., & Martin, K.C. (2004). Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway. Neuron, 44, 997–1009. doi:10.1016/S0896-6273(04)00761-5
   PubMed Web of Science ®Google Scholar
• Thran, J., Poeck, B., & Strauss, R. (2013). Serum response factor-mediated gene regulation in a Drosophila visual working memory. Current Biology, 23, 1756–1763. doi:10.1016/j.cub.2013.07.034
   PubMed Web of Science ®Google Scholar
• Ting, C.Y., Herman, T., Yonekura, S., Gao, S., Wang, J., Serpe, M., … Lee, C.H. (2007). Tiling of r7 axons in the Drosophila visual system is mediated both by transduction of an activin signal to the nucleus and by mutual repulsion. Neuron, 56, 793–806. doi:10.1016/j.neuron.2007.09.033
   PubMed Web of Science ®Google Scholar
• Toma, D.P., White, K.P., Hirsch, J., & Greenspan, R.J. (2002). Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nature Genetics, 31, 349–353. doi:10.1038/ng893
   PubMed Web of Science ®Google Scholar
• Török, I., Strand, D., Schmitt, R., Tick, G., Török, T., Kiss, I., & Mechler, B.M. (1995). The overgrown hematopoietic organs-31 tumor suppressor gene of Drosophila encodes an importin-like protein accumulating in the nucleus at the onset of mitosis. Journal of Cell Biology, 129, 1473–1489. doi:10.1083/jcb.129.6.1473
   PubMed Web of Science ®Google Scholar
• Trannoy, S., Redt-Clouet, C., Dura, J.M., & Préat, 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
• Tully, T., Préat, T., Boynton, S.C., & Del Vecchio, M. (1994). Genetic dissection of consolidated memory in Drosophila. Cell, 79, 35–47. doi:10.1016/0092-8674(94)90398-0
   PubMed Web of Science ®Google Scholar
• Tully, T., & Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. Journal of Comparative Physiology, 157, 263–277. doi:10.1007/BF01350033
   PubMed Web of Science ®Google Scholar
• Vaskova, M., Bentley, A.M., Marshall, S., Reid, P., Thummel, C.S., & Andres, A.J. (2000). Genetic analysis of the Drosophila 63F early puff. Characterization of mutations in E63-1 and maggie, a putative Tom22. Genetics, 156, 229–244.
   PubMed Web of Science ®Google Scholar
• Waeber, G., & Habener, J.F. (1991). Nuclear translocation and DNA recognition signals colocalized within the bZIP domain of cAMP response element binding protein CREB. Molecular Endocrinology, 5, 1431–1438. doi:10.1210/mend-5-10-1431
   PubMedGoogle Scholar
• Wagatsuma, A., Azami, S., Sakura, M., Hatakeyama, D., Aonuma, H., & Ito, E. (2006). De Novo synthesis of CREB in a presynaptic neuron is required for synaptic enhancement involved in memory consolidation. Journal of Neuroscience Research, 84, 954–960. doi:10.1002/jnr.21012
   PubMed Web of Science ®Google Scholar
• Wang, X., Amei, A., de Belle, J.S., & Roberts, S.P. (2018). Environmental effects on Drosophila brain development and learning. The Journal of Experimental Biology, 221, jeb169375. doi:10.1242/jeb.169375
   PubMed Web of Science ®Google Scholar
• Wang, X., Green, D.S., Roberts, S.P., & de Belle, J.S. (2007). Thermal disruption of mushroom body development and odor learning in Drosophila. PLoS ONE, 2, e1125. doi:10.1371/journal.pone.0001125
   PubMed Web of Science ®Google Scholar
• Wang, S., Lu, Y., Yin, M.X., Wang, C., Wu, W., Li, J., … Zhang, L. (2016). Importin α1 mediates Yorkie nuclear import via an N-terminal non-canonical nuclear localization signal. Journal of Biological Chemistry, 291, 7926–7937. doi:10.1074/jbc.M115.700823
   PubMed Web of Science ®Google Scholar
• Wang, H., Shao, N., Ding, Q., Cui, J., Reddy, E., & Rao, V. (1997). BRCA1 proteins are transported to the nucleus in the absence of serum and splice variants BRCA1a, BRCA1b are tyrosine phosphoproteins that associate with E2F, cyclins and cyclin dependent kinases. Oncogene, 15, 143–157. doi:10.1038/sj.onc.1201252
   PubMed Web of Science ®Google Scholar
• Yasuhara, N., Yamagishi, R., Arai, Y., Mehmood, R., Kimoto, C., Fujita, T., Touma, K., Kaneko, A., Kamikawa, Y., Moriyama, T., Yanagida, T., Kaneko, H., & Yoneda, Y. (2013). Importin alpha subtypes determine differential transcription factor localization in embryonic stem cells maintenance. Dev Cell, 26(2), 123-35. doi: 10.1016/j.devcel.2013.06.022.
   Google Scholar
• Yin, J.C., & Tully, T. (1996). CREB and the formation of long-term memory. Current Opinion in Neurobiology, 6, 264–268. doi:10.1016/s0959-4388(96)80082-1
   PubMed Web of Science ®Google Scholar
• Yin, J.C.P., Wallach, J.S., Del Vecchio, M., Wilder, E.L., Zhou, H., Quinn, W.G., & Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell, 79, 49–58. doi:10.1016/0092-8674(94)90399-9
   PubMed Web of Science ®Google Scholar
• Yu, D., Akalal, D.B., & Davis, R.L. (2006). Drosophila α/β mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron, 52, 845–855. doi:10.1016/j.neuron.2006.10.030
   PubMed Web of Science ®Google Scholar
• Yudin, D., Hanz, S., Yoo, S., Iavnilovitch, E., Willis, D., Gradus, T., … Fainzilber, M. (2008). Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron, 59, 241–252. doi:10.1016/j.neuron.2008.05.029
   PubMed Web of Science ®Google Scholar
• Zar, J.H. (2010). Biostatistical Analysis (5th ed.). New York: Pearson.
   Google Scholar
• Zars, T., Fischer, M., Schulz, R., & Heisenberg, M. (2000). Localization of a short-term memory in Drosophila. Science, 288, 672–675. doi:10.1126/science.288.5466.672
   PubMed Web of Science ®Google Scholar