Synaptic Growth and Transcriptional Regulation in Drosophila

  • Cynthia Barber
  • J. Troy Littleton


The elucidation of the underlying molecular mechanisms that allow learning and memory storage in the nervous system is one of the most exciting challenges in current neuroscience research. While memory storage in vertebrates can persist for a short time in the presence of mRNA transcription or protein translation blockers, these memories last for only a few hours and do not undergo consolidation into longer-term information storage. Physiological studies in the hippocampus have demonstrated that the late phases of long-term potentiation (LTP) depend on transcription and translation (kelleher, Govindarajan, Jung, Kang and Tonegawa, 2004; Kelleher, Govindarajan and Tonegawa, 2004). Transcription-dependent brain plasticity is also evident in invertebrates, as overexpression of a dominant-negative CREB (cAMP-responsive element binding protein) transgene is sufficient to block long-term memory storage in Drosophila (Yin, Wallach, Del Vecchio, Wilder, Zhou, Quinn and Tully 1994). Through a combination of genetic approaches using the Drosophila neuromuscular junction to study synaptic growth regulation, and genome-wide microarray studies in Drosophila mutants with altered neuronal activity, it has become clear that a critical target for transcriptional recoding during neuronal plasticity involves changes in synaptic wiring. Here we review both the mechanisms of activity-dependent transcriptional regulation in Drosophila, as well as how this regulation interfaces with the control of synaptic growth and function.


Synaptic Plasticity Mushroom Body Synaptic Structure Olfactory Learning Synaptic Growth 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aberle, H., Haghighi, A.P., Fetter, R.D., McCabe, B.D., Magalhaes, T.R. and Goodman C.S. (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33, 545–558.PubMedGoogle Scholar
  2. Adolfsen, B., Saraswati, S., Yoshihara, M. and Littleton, J.T. (2004) Synaptotagmins are Trafficked to Distinct Subcellular Domains Including the Postsynaptic Compartment. J. Cell. Biol. 166, 249–260.PubMedGoogle Scholar
  3. Andersen, R., Li, Y., Resseguie, M. and Brenman, J.E. (2005) Calcium/calmodulin-dependent protein kinase II alters structural plasticity and cytoskeletal dynamics in Drosophila. J. Neurosci. 25, 8878–8888.PubMedGoogle Scholar
  4. Ashley, J., Packard, M., Ataman, B. and Budnik, V. (2005) Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J. Neurosci. 25, 5943–5955.PubMedGoogle Scholar
  5. Ashraf, S.I., McLoon, A.L., Sclarsic, S.M., and Kunes S. (2006) Synaptic Protein Synthesis Associated with Memory Is Regulated by the RISC Pathway in Drosophila. Cell 124, 191–205.PubMedGoogle Scholar
  6. Bailey, C.H., Kaang, B.K., Chen, M., Martin, K.C., Lim, C.S., Casadio, A. and Kandel, E.R. (1997) Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18, 913–924.PubMedGoogle Scholar
  7. Bailey, C.H., and Chen, M. (1988) Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc. Natl. Acad. Sci. USA 85, 2373–2377.PubMedGoogle Scholar
  8. Baines, R.A., Seugnet, L., Thompson, A., Salvaterra, P.M. and Bate, M. (2002) Regulation of synaptic connectivity: levels of Fasciclin II influence synaptic growth in the Drosophila CNS. J. Neurosci. 22, 6587–6595.PubMedGoogle Scholar
  9. Ben-Ari, Y. and Represa, A. (1990) Brief Seizure Episodes Induce Long-Term Potentiation and Mossy Fibre Sprouting in the Hippocampus. Trends Neurosci 8, 312–318.Google Scholar
  10. Beumer, K., Matthies, H.J., Bradshaw, A. and Broadie, K. (2002) Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development 129, 3381–3391.PubMedGoogle Scholar
  11. Bito, H., Deisseroth, K. and Tsien, R.W. (1996) CREB Phosphorylation and Dephosphorylation: a Ca(2+) and Stimulus Duration-Dependent Switch for Hippocampal Gene Expression. Cell 87, 1203–1214.PubMedGoogle Scholar
  12. Brouillet, E., Trembleau, A., Galanaud, D., Volovitch, M., Bouillot, C., Valenza, C., Prochiantz, A. and Allinquant, B. (1999) The amyloid precursor protein interacts with Go heterotrimeric protein within a cell compartment specialized in signal transduction. J. Neurosci. 19, 1717–1727.PubMedGoogle Scholar
  13. Budnik, V., Zhong, Y. and Wu, C.F. (1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci. 10, 3754–3768.PubMedGoogle Scholar
  14. Chang, Q., and Balice-Gordon, R. (2000) highwire, rpm-1, and futsch: Balancing Synaptic Growth and Stability. Neuron 26, 287–290.PubMedGoogle Scholar
  15. Cheng, Y., Endo, K., Wu, K., Rodan, A.R., Heberlein, U. and Davis, R.L. (2001) Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105, 757–768.PubMedGoogle Scholar
  16. Chiang, A.S., Blum, A., Barditch, J., Chen, Y.H., Chiu, S.L., Regulski, M., Armstrong, J.D., Tully, T. and Dubnau, J. (2004) radish encodes a phospholipase-A2 and defines a neural circuit involved in anesthesia-resistant memory. Curr. Biol. 14, 263–272.PubMedGoogle Scholar
  17. Collins, C.A., Wairkar, Y.P., Johnson, S.L. and DiAntonio, A. (2006) Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51, 57–69.PubMedGoogle Scholar
  18. Curtis, J., and Finnkbeiner, S. (1999) Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J. Neurosci. Res. 58, 88–95.PubMedGoogle Scholar
  19. Dash, P.K., Hochner, B. and Kandel, E.R. (1990) Injection of the cAMP-Responsive Element into the Nucleus of Aplysia Sensory Neurons Blocks Long-Term Facilitation. Nature 345, 718–721.PubMedGoogle Scholar
  20. Davis, G. and Bezprozvanny, I. (2001) Maintaining the Stability of Neuronal Function: a Homeostatic Hypothesis. Annu. Rev. Physiol. 63, 847–869.PubMedGoogle Scholar
  21. Davis, G., Schuster, C. and Goodman, C. (1996) Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. III. CREB Is Necessary for Presynaptic Functional Plasticity. Neuron 17, 669–679.PubMedGoogle Scholar
  22. Davis, G., Schuster, C. and Goodman, C. (1997) Genetic Analysis of the Mechanisms Controlling Target Selection: Target-Derived Fasciclin II Regulates the Pattern of Synapse Formation. Neuron 19, 561–573.PubMedGoogle Scholar
  23. Desmond, N.L. and Levy, W.B. (1986) Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus. J. Comp. Neurol. 253, 466–475.PubMedGoogle Scholar
  24. DeZazzo, J., Sandstrom, D., de Belle, S., Velinzon, K., Smith, P., Grady, L., DelVecchio, M., Ramaswami, M. and Tully, T. (2000) nalyot, a mutation of the Drosophila myb-related Adf1 transcription factor, disrupts synapse formation and olfactory memory. Neuron 27, 145–158.PubMedGoogle Scholar
  25. DiAntonio, A., Haghighi, A.P., Portman, S.L., Lee, J.D., Amaranto, A.M. and Goodman, C.S. (2001) Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449–452.PubMedGoogle Scholar
  26. Dolmetsch, R.E., Pajvani, U., Fife, K., Spotts, J.M. and Greenberg, M.E. (2001) Signaling to the Nucleus by an L-type Calcium Channel-Calmodulin Complex Through the MAP Kinase Pathway. Science 294, 333–339.PubMedGoogle Scholar
  27. Dubnau, J., Chiang, A.S., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., Broger, C. and Tully, T. (2003) The staufen/pumilio Pathway Is Involved in Drosophila Long-Term Memory. Curr. Biol. 13, 286–296.PubMedGoogle Scholar
  28. Etter, P.D., Narayanan, R., Navratilova, Z., Patel, C., Bohmann, D., Jasper, H. and Ramaswami, M. (2005) Synaptic and genomic responses to JNK and AP-1 signaling in Drosophila neurons. BMC Neurosci. 6, 39.PubMedGoogle Scholar
  29. Feany, M.B. and Quinn, W.G. (1995) A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268.Google Scholar
  30. Ferguson, G.D., Anagnostaras, S.G., Silva, A.J. and Herschman, H.R. (2000) Deficits in Memory and Motor Performance in Synaptotagmin IV Mutant Mice. Proc. Natl. Acad. Sci. USA 97, 5598–5603.Google Scholar
  31. Ferguson, G.D., Herschman, H.R. and Storm, D.R. (2004) Reduced Anxiety and Depression-Like Behavior in Synaptotagmin IV (-/-) Mice. Neuropharmacol. 47, 604–611.Google Scholar
  32. Ferguson, G.D., Thomas, D.M., Elferink, L.A. and Herschman, H.R. (1999) Synthesis, Degradation and Subcellular Localization of Synaptotagmin IV, a Neuronal Immediate Early Gene Product. J. Neurochem. 72, 1821–1831.PubMedGoogle Scholar
  33. Ferguson, G.D., Wang, H., Herschman, H.R. and Storm, D.R. (2004) Altered Hoppocampal Short-Term Plasticity and Associative Memory in Synaptotagmin IV (-/-) Mice. Hippocampus 14, 964–974.Google Scholar
  34. Folkers E, Drain, P. and Quinn, W.G. (1993) Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl. Acad. Sci. USA 90, 8123–8127.PubMedGoogle Scholar
  35. Friedrich, A., Thomas, U. and Muller, U. (2004) Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J. Neurosci. 24, 4460–4468.PubMedGoogle Scholar
  36. Ganetzky, B. and Wu, C.F. (1986) Neurogenetics of Membrane Excitability in Drosophila. Annu. Rev. Genet. 20, 13–44.PubMedGoogle Scholar
  37. Garcia-Alonso, L., VanBerkum, M.F., Grenningloh, G., Schuster, C. and Goodman, C.S. (1995) Fasciclin II controls proneural gene expression in Drosophila. Proc. Natl. Acad. Sci. USA 92, 10501–10505.PubMedGoogle Scholar
  38. Glanzman, D.L., Kandel, E.R. and Schacher, S. (1990) Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249, 799–802.PubMedGoogle Scholar
  39. Grenningloh, G., Rehm, E.J. and Goodman, C.S. (1991) Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67, 45–57.PubMedGoogle Scholar
  40. Griffith, L.C., Lu, C.S. and Sun, X.X. (2003) CaMKII, an Enzyme on the Move: Regulation of Temporospatial Localization. Mol. Interven. 3, 386–403.Google Scholar
  41. Griffith, L.C., Verselis, L.M., Aitken, K.M., Kyriacou, C.P., Danho, W. and Greenspan, R.J. (1993) Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron 10, 501–509.PubMedGoogle Scholar
  42. Grotewiel, M.S., Beck, C.D., Wu, K.H., Zhu, X.R. and Davis, R.L. (1998) Integrin-mediated short-term memory in Drosophila. Nature 391, 455–460.PubMedGoogle Scholar
  43. Guan, Z., Saraswati, S., Adolfsen, B. and Littleton, J.T. (2005) Genome-Wide Transcriptional Changes Associated with Enhanced Activity in the Drosophila Nervous System. Neuron 48, 91–107.PubMedGoogle Scholar
  44. Hanson, P.I. and Schulman, H. (1992) Neuronal Ca2+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61, 559–601.PubMedGoogle Scholar
  45. Hebbar, S. and Fernandes, J.J. (2005) A role for Fas II in the stabilization of motor neuron branches during pruning in Drosophila. Dev. Biol. 285, 185–199.PubMedGoogle Scholar
  46. Hoeffer, C.A., Sanyal, S. and Ramaswami, M. (2003) Acute induction of conserved synaptic signaling pathways in Drosophila melanogaster. J. Neurosci. 23, 6362–6372.PubMedGoogle Scholar
  47. Huang, Y.Y., Li, X.C. and Kandel, E.R. (1994) cAMP Contributes to Mossy Fiber LTP by Initiating both a Covalently Mediated Early Phase and Macromolecular Synthesis-dependent Late Phase. Cell 79, 69–79.PubMedGoogle Scholar
  48. Hummel, T., Krukkert, K., Roos, J., Davis, G. and Klambt, C. (2000) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26, 357–370.PubMedGoogle Scholar
  49. Isabel, G., Pascual, A. and Preat, T. (2004) Exclusive Consolidated Memory Phases in Drosophila. Science 304, 1024–1027.PubMedGoogle Scholar
  50. Kaplan, W.D. and Trout, W.E. (1969) The Behavior of Four Neurological Mutants of Drosophila. Genetics 61, 399–409.PubMedGoogle Scholar
  51. Kelleher, R.J., Govindarajan, A. and Tonegawa, S. (2004) Translational Regulatory Mechanisms in Persistent Forms of Synaptic Plasticity. Neuron 44, 59–73.PubMedGoogle Scholar
  52. Kelleher, R.J., Govindarajan, A., Jung, H.Y., Kang, H. and Tonegawa, S. (2004) Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory. Cell 116, 467–479.PubMedGoogle Scholar
  53. Koh, Y.H., Popova, E., Thomas, U., Griffith, L.C. and Budnik, V. (1999) Regulation of DLG localization at synapses by CaMKII-dependent phosphorylation. Cell 98, 353–363.PubMedGoogle Scholar
  54. Koh, Y.H., Ruiz-Canada, C., Gorczyca, M. and Budnik, V. (2002) The Ras1-mitogen-activated protein kinase signal transduction pathway regulates synaptic plasticity through fasciclin II-mediated cell adhesion. J. Neurosci. 22, 2496–2504.PubMedGoogle Scholar
  55. Kuja-Panula, J., Kiiltomaki, M., Yamashiro, T., Rouhiainen, A. and Rauvala, H. (2003) AMIGO, a Transmembrane Protein Implicated in Axon Tract Development, Defines a Novel Protein Family with Leucine-Rich Repeats. J. Cell. Biol 160, 963–973.PubMedGoogle Scholar
  56. Li, W., Tully, T. and Kalderon, D. (1996) Effects of a conditional Drosophila PKA mutant on olfactory learning and memory. Learn. Mem. 2, 320–333.PubMedGoogle Scholar
  57. Lin, D.M. and Goodman, C.S. (1994) Ectopic and increased expression of fasciclin II alters motoneuron growth cone guidance. Neuron 13, 507–523.PubMedGoogle Scholar
  58. Lisman, J., Schulman, H. and Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175–190.PubMedGoogle Scholar
  59. Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M. and Liu, L. (2006) Nature 439, 551–556.Google Scholar
  60. Livingstone, M.S., Sziber, P.P. and Quinn, W.G. (1984) Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37, 205–215.PubMedGoogle Scholar
  61. MacLaren, C.M., Evans, T.A., Alvarado, D. and Duffy, J.B. (2004) Comparative Analysis of the Kekkon Molecules, Related Members of the LIG Superfamily. Dev. Genes Evol. 214, 360–366.PubMedGoogle Scholar
  62. Margulies, C., Tully, T. and Dubnau, J. (2005) Deconstructing Memory in Drosophila. Curr. Biol. 15, R700-R713.PubMedGoogle Scholar
  63. Marques, G., Bao, H., Haerry, T.E., Shimell, M.J., Duchek, P., Zhang, B. and O’Connor, M.B. (2002) The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33, 529–543.PubMedGoogle Scholar
  64. Marques, G., Haerry, T.E., Crotty, M.L., Xue, M., Zhang, B. and O’Connor, M.B. (2003) Retrograde Gbb signaling through the Bmp type 2 receptor wishful thinking regulates systemic FMRFa expression in Drosophila. Devolopment 130, 5457–5470.Google Scholar
  65. Martin, K.C., Michael, D., Rose, J.C., Barad, M., Casadio, A., Zhu, H. and Kandel, E.R. (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18, 899–912.PubMedGoogle Scholar
  66. McCabe, B.D., Hom, S., Aberle, H., Fetter, R.D., Marques, G., Haerry, T.E., Wan, H., O’Connor, M.B., Goodman, C.S. and Haghighi, A.P. (2004) Highwire Regulates Presynaptic BMP Signaling Essential for Synaptic Growth. Neuron 41, 891–905.PubMedGoogle Scholar
  67. McCabe, B.D., Marques, G., Haghighi, A.P., Fetter, R.D., Crotty, M.L., Haerry, T.E., Goodman, C.S. and O’Connor, M.B. (2003) The BMP Homolog Gbb Provides a Retrograde Signal that Regulates Synaptic Growth at the Drosophila Neuromuscular Junction. Neuron 39, 241–254.PubMedGoogle Scholar
  68. McGuire, S.E., Deshazer, M. and Davis, R.L. (2005) Thirty years of olfactory learning and memory research in Drosophila melanogaster. Progr. Neurobiol. 76, 328–347.Google Scholar
  69. Mehren, J.E. and Griffith, L.C. (2004) Calcium-independent calcium/calmodulin-dependent protein kinase II in the adult Drosophila CNS enhances the training of pheromonal cues. J. Neurosci. 24, 10584–10593.PubMedGoogle Scholar
  70. Menon, K.P., Sanyal, S., Habara, Y., Sanchez, R., Wharton, R.P., Ramaswami, M. and Zinn, K. (2004) The Translational Repressor Pumilio Regulates Presynaptic Morphology and Controls Postsynaptic Accumulation of Translation Factor eIF-4E. Neuron 44, 663–676.PubMedGoogle Scholar
  71. Michael, D., Martin, K.C., Seger, R., Ning, M.M., Baston, R. and Kandel, E.R. (1998) Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc. Natl. Acad. Sci. USA 95, 1864–1869.PubMedGoogle Scholar
  72. Murthy, V., Han, S., Beauchamp, R.L., Smith, N., Haddad, L.A., Ito, N. and Ramesh, V. (2004) Pam and its ortholog highwire interact with and may negatively regulate the TSC1.TSC2 complex. J. Biol. Chem. 279, 1351–1358.PubMedGoogle Scholar
  73. Nedivi, E., Hevroni, D., Naot, D., Israeli, D. and Citri, Y. (1993) Numerous Candidate Plasticity-Related Genes Revealed by Differential cDNA Cloning. Nature 363, 718–722.PubMedGoogle Scholar
  74. Nguyen, M., Park, S., Marques, G. and Arora, K. (1998) Interpretation of a BMP activity gradient in Drosophila embryos depends on synergistic signaling by two type I receptors, SAX and TKV. Cell 95, 495–506.PubMedGoogle Scholar
  75. Nishiki, T. and Augustine, G.J. (2004) Dual Roles of the C2B Domain of Synaptotagmin I in Synchronizing Ca2+-Dependent Neurotransmitter Release. J. Neurosci. 24, 8542–8550.PubMedGoogle Scholar
  76. Ono, T., Sekino-Suzuki, N., Kikkawa, Y., Yonekawa, H. and Kawashima, S. (2003) Alivin 1, a Novel Neuronal Activity-Dependent Gene, Inhibits Apoptosis and Promotes Survival of Cerebellar Granule Neurons. J. Neurosci. 23, 5887–5896.PubMedGoogle Scholar
  77. Peverali, F.A., Isaksson, A., Papavassiliou, A.G., Staszewski, L.M., Mlodzik, M. and Bohmann, D. (1996) Phosphorylation of Drosophila Jun by the MAP kinase rolled regulates photoreceptor differentiation. EMBO J 15, 3943–3950.PubMedGoogle Scholar
  78. Qian, Z., Gilbert, M.E., Colicos, M.A., Kandel, E.R. and Kuhl, D. (1993) Tissue-plasminogen Activator is Induced as an Immediate-Early Gene During Seizure, Kindling and Long-Term Potentiation. Nature 361, 453–457.PubMedGoogle Scholar
  79. Quinn, W.G., Sziber, P.P. and Booker, R. (1979) The Drosophila memory mutant amnesiac. Nature 277, 212–214.PubMedGoogle Scholar
  80. Roos, J., Hummel, T., Ng, N., Klambt, C. and Davis, G.W. (2000) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26, 371–382.PubMedGoogle Scholar
  81. Ruiz-Canada, C., Ashley, J., Moeckel-Cole, S., Drier, E., Yin, J. and Budnik, V. (2004) New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 42, 567–580.PubMedGoogle Scholar
  82. Sanyal, S., Kim, S.M. and Ramaswami, M. (2004) Retrograde Regulation in the CNS: Neuron-Specific Interpretations of TGF-beta Signaling. Neuron 41, 845–848.PubMedGoogle Scholar
  83. Sanyal, S., Sandstrom, D.J., Hoeffer, C.A. and Ramaswami, M. (2002) AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature 416, 870–874.PubMedGoogle Scholar
  84. Schuster, C., Davis, G., Fetter, R. and Goodman C.S. (1996) Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. II. Fasciclin II Controls Presynaptic Structural Plasticity. Neuron 17, 655–667.PubMedGoogle Scholar
  85. Schuster, C., Davis, G., Fetter, R. and Goodman, C.S. (1996) Genetic Dissection of Structural and Functional Components of Synaptic Plasticity. I. Fasciclin II Controls Synaptic Stabilization and Growth. Neuron 17, 641–654.PubMedGoogle Scholar
  86. Sigrist, S.J., Reiff, D.F., Thiel, P.R., Steinert, J.R. and Schuster, C.M. (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J. Neurosci. 23, 6546–6556.PubMedGoogle Scholar
  87. Sigrist, S.J., Thiel, P.R., Reiff, D.F., Lachance, P.E., Lasko, P., Schuster, C.M. (2000) Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature 405, 1062–1065.PubMedGoogle Scholar
  88. Skoulakis, E.M., Kalderon, D. and Davis, R.L. (1993) Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11, 197–208.PubMedGoogle Scholar
  89. Sontheimer, E.J. (2005) Assembly and function of RNA silencing complexes. Rev. Mol. Cell. Biol. 6, 127–138.Google Scholar
  90. Thomas, U., Kim, E., Kuhlendahl, S., Koh, Y.H., Gundelfinger, E.D., Sheng, M., Garner, C.C. and Budnik, V. (1997) Synaptic clustering of the cell adhesion molecule fasciclin II by discs-large and its role in the regulation of presynaptic structure. Neuron 19, 787–799.PubMedGoogle Scholar
  91. Titus, S.A., Warmke, J.W. and Ganetzky, B. (1997) The Drosophila erg K+ channel polypeptide is encoded by the seizure locus. J. Neurosci. 17, 875–881.PubMedGoogle Scholar
  92. Tully, T. and Quinn, W.G. (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. 157, 263–277.Google Scholar
  93. Turrigiano, G.G. and Nelson, S.B. (2004) Homeostatic Plasticity in the Developing Nervous System. Nat. Rev. Neurosci. 5, 97–107.PubMedGoogle Scholar
  94. Vician, L., Lim, I.K., Ferguson, G., Tocco, G., Baudry, M. and Herschman, H.R. (1995) Synaptotagmin IV is an Immediate Early Gene Induced by Depolarization in PC12 Cells and in Brain. Proc. Natl. Acad. Sci. 92, 2164–2168.PubMedGoogle Scholar
  95. Waddell, S. and Quinn, W.G. (2001) Fas-acting memory. Dev. Cell 1, 8–9.PubMedGoogle Scholar
  96. Wan, H.I., DiAntonio, A., Fetter, R.D., Bergstrom, K., Strauss, R. and Goodman, C.S. (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26, 313–329.PubMedGoogle Scholar
  97. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F. and Massague, J. (1994) Mechanism of activation of the TGF-beta receptor. Nature 370, 341–347.PubMedGoogle Scholar
  98. Wrana, J.L. and Attisano, L. (2000) The Smad Pathway. Cytokine Growth Fact. Rev. 11, 5–13.Google Scholar
  99. Wu, C., Wairkar, Y.P., Collins, C.A. and DiAntonio, A. (2005) Highwire function at the Drosophila neuromuscular junction, spatial, structural and temporal requirements. J. Neurosci. 25, 9557–9566.PubMedGoogle Scholar
  100. Ye, B., Petritsch, C., Clark, I.E., Gavis, E.R., Jan, L.Y. and Jan, Y.N. (2004) nanos and pumilio Are Essential for Dendrite Morphogenesis in Drosophila Peripheral Neurons. Curr. Biol. 14, 314–321.PubMedGoogle Scholar
  101. Yin, J.C., Wallach, J.S., Del Vecchio, M., Wilder, E.L., Zhou, H., Quinn, W.G. and Tully, T. (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49–58.PubMedGoogle Scholar
  102. Yin, J.C., Wallach, J.S., Wilder, E.L., Klingensmith, J., Dang, D., Perrimon, N., Zhou, H., Tully, T. and Quinn, W.G. (1995) A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol. Biol. Cell 15, 5123–5130.Google Scholar
  103. Yoshihara, M., Adolfsen, B., Galle, K.T. and Littleton, J.T. (2005) Retrograde Signaling by Syt 4 Induces Presynaptic Release and Synapse-Specific Growth. Science 310, 858–863.PubMedGoogle Scholar
  104. Yoshihara, M. and Littleton, J.T. (2002) Synaptotagmin I functions as a Calcium Sensor to Synchronize Neurotransmitter Release. Neuron 36, 897–908.PubMedGoogle Scholar
  105. Zhang, Y.Q., Bailey, A.M., Matthies, H.J., Renden, R.B., Smith, M.A., Speese, S.D., Rubin, G.M. and Broadie, K. (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107, 591–603.PubMedGoogle Scholar
  106. Zhong, Y., Budnik, V. and Wu C.F. (1992) Synaptic plasticity in Drosophila memory and hyperexcitable mutants, role of cAMP cascade. J. Neurosci. 12, 644–651.PubMedGoogle Scholar
  107. Zhong, Y. and Wu, C.F. (2004) Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J. Neurosci. 24, 1439–1445.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Cynthia Barber
  • J. Troy Littleton

There are no affiliations available

Personalised recommendations