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Research Article

Cyclic Adenosine Monophosphate Metabolism in Synaptic Growth, Strength, and Precision: Neural and Behavioral Phenotype-Specific Counterbalancing Effects between dnc Phosphodiesterase and rut Adenylyl Cyclase Mutations

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Pages 64-81 | Received 30 Oct 2011, Accepted 20 Dec 2011, Published online: 01 Mar 2012

REFERENCES

  • Aceves-Pina, E. O., & Quinn, W. G. (1979) Learning in normal and mutant Drosophila larvae. Science, 206, 93–96.
  • Asztalos, Z.,Arora, N., & Tully, T. (2007). Olfactory jump reflex habituation in Drosophila and effects of classical conditioning mutations. J Neurogenet, 21, 1–18.
  • Baines, R. A. (2003). Postsynaptic protein kinase A reduces neuronal excitability in response to increased synaptic excitation in the Drosophila CNS. J Neurosci, 23, 8664–8672.
  • Balling, A., Technau, G. M., & Heisenberg, M. (1987). Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet, 4, 65–73.
  • Bellen, HJ.,& Kiger, J. A., Jr. (1988). Maternal effects of general and regional specificity on embryos of Drosophila melanogaster caused by dunce and rutabaga mutant combinations. Roux Arch Dev Biol, 197, 258–268.
  • Berke, B., & Wu, C.-F. (2002). Regional calcium regulation within cultured Drosophila neurons: Effects of altered cAMP metabolism by the learning mutations dunce and rutabaga. J Neurosci, 22, 4437–4447.
  • Bhattacharya, A., Gu, G.-G., & Singh, S. (1999). Modulation of dihydripyridine-sensitive calcium channels in Drosophila by a cAMP-mediated pathway. J Neurobiol, 39, 491–500.
  • Bradacs, H., Cooper, R. L., Msghina, M., & Atwood, H. L. (1997). Differential physiology and morphology of phasic and tonic motor axons in a crayfish limb extensor muscle. J Exp Biol, 200, 677–691.
  • Brembs, B., & Plendl, W. (2008). Double dissociation of PKC and AC manipulations on operant and classical learning in Drosophila. Curr Biol, 18, 1168–1171.
  • Budnik, V., Zhong, Y., & Wu, C.-F. (1990). Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurobiol, 10, 3754–3768.
  • Byers, D., Davis, R. L., & Kiger, J. A., Jr. (1981). Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature, 289, 79–81.
  • Cann, M. J., & Levin, L. R. (2000). Restricted expression of a truncated adenylyl cyclase in the cephalic furrow of Drosophila melanogaster. Dev Genes Evol, 210, 34–40.
  • Chen, C.-N., Denome, S., & Davis, R. L. (1986). Molecular analysis of cDNA clonse and the corresponding genomic coding sequences of the Drosophila dunce + gene, the structural gene for cAMP phosphodiesterase. Proc Natl Acad Sci U S A, 83, 9313–9317.
  • Cheung, U., Atwood, H. L., & Zucker, R. S. (2006). Presynaptric effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J Neurobiol, 66, 273–280.
  • Cheung, U. S., Shayan, A. J., Boulianne, G. L., & Atwood, H. L. (1999). Drosophila larval neuromuscular junction's response to reduction of cAMP in the nervous system. J Neurobiol, 40, 1–13.
  • Corfas, G., & Dudai, Y. (1990a). Pharmacological evidence for the involvement of the cAMP cascade in sensory fatigue in Drosophila. J Comp Physiol A, 167, 437–440.
  • Corfas, G., & Dudai, Y. (1990b). Adaptation and fatigue of a mechanosensory neuron in wild-type Drosophila and memory mutants. J Neurosci, 10, 491–499.
  • Corfas, G., & Dudai, Y. (1991). Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging. Proc Natl Acad Sci USA, 88, 7252–7256.
  • Das, S., Sadanandappa, M. K., Dervan, A., Larkin, A., Lee, J. A., Sudhakaran, I. P., Priya, R., Heidari, R., Holohan, E. E., Pimentel, A., Gandhi, A., Ito, K., Sanyal, S., Wang, J. W., Rodrigues, V., & Ramaswami, M. (2011). Plasticity of local GABAergic interneurons drives olfactory habituation. Proc Natl Acad Sci USA, 108, E646-E654.
  • Davis, G. W., Schuster, C. M., & Goodman, C. S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron, 17, 669–679.
  • Davis, R. L. (2005). Olfactory memory formation in Drosophila: From molecular to systems neuroscience. Annu Rev Neurosci, 28, 275–302.
  • Davis, R. L., & Davidson, N. (1986). The memory gene dunc + encodes a remarkable set of RNAs with internal heterogeneity. Mol Cell Biol, 6, 1464–1470.
  • Davis, R. L., & Kiger, J. A., Jr. (1981). dunce mutants of Drosophila melanogaster: Mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol, 90, 101–107.
  • Day, J. P., Dow, J. A. T., Houslay, M. D., & Davies, S.-A. (2005). Cyclic nucleotide phosphodiesterases in Drosophila melanogaster. Biochem J, 388, 333–342.
  • Del Castillo, J., & Katz, B. (1954). Quantal components of the end-plate potential. J Physiol, 124, 560–573.
  • Delgado, R., Davis, R., Bono, M. R., Latorre, R., & Labarca, P. (1998). Outward currents in Drosophila larval neurons: dunce lacks a maintained outward current component downregulated by cAMP. J Neurosci, 18, 1399–1407.
  • Devaud, J.-M., Acebes, A., & Ferrús, A. (2001). Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila. J Neurosci, 21, 6274–6282.
  • Devaud, J.-M., Acebes, A., Ramaswami, M., & Ferrús, A. (2003). Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J Neurobiol, 56, 13–23.
  • Dévay, P., Pinter, M., Kiss, I., Farago, A., & Friedrich, P. (1989). Protein kinase C in larval brain of wild-type and dunce memory mutant Drosophila. J Neurogenet, 5, 119–126.
  • Dudai, Y. (1983). Mutations affect storage and use of memory differentially in Drosophila. Proc Natl Acad Sci USA, 80, 5445–5448.
  • Dudai, Y., Jan, Y.-N., Byers, D., Quinn, W. G., & Benzer, S. (1976). dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci USA, 73, 1684–1688.
  • Dudai, Y., Uzzan, A., & Zvi, S. (1983). Abnormal activity of adenylate cyclase in the Drosophila memory mutant rutabaga. Neurosci Lett, 42, 207–212.
  • Dudai, Y., & Zvi, S. (1984). Adenylate cyclase in the Drosophila memory mutant rutabaga displays an altered Ca2 + sensitivity. Neurosci Lett, 47, 119–124.
  • Duerr, J. S., & Quinn, W. G. (1982). Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc Natl Acad Sci USA, 79, 3646–3650.
  • Engel, J. E., & Wu, C.-F. (1996). Altered habituation of an identified escape circuit in Drosophila memory mutants. J Neurosci, 16, 3486–3499.
  • Engel, J. E., & Wu, C.-F. (2009). Neurogenetic approaches to habituation and dishabituation in Drosophila. Neurobiol Learn Mem, 92, 166–175.
  • Engel, J. E., Xie, X.-J., Sokolowski, M. B., & Wu, C.-F. (2000). A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila. Learn Mem, 7, 341–352.
  • Fatt, P., & Katz, B. (1952). Spontaneous subthreshold activity at motor nerve endings. J Physiol, 117, 109–128.
  • Feany, M. B. (1990). Rescue of the learning defect in dunce, a Drosophila learning mutant, by an allele of rutabaga, a second learning mutant. Proc Natl Acad Sci USA, 87, 2795–2799.
  • Feng, Y., Ueda, A., & Wu, C.-F. (2004). A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet, 18, 377–402.
  • Featherstone, D. E., Rushton, E. M., Hilderbrand-Chae, M., Phillips, A. M., Jackson, F. R., & Broadie, K. (2000). Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron, 27, 71–84.
  • Folkers, E. (1982). Visual learning and memory of Drosophila melanogaster wild type C-S and the mutants dunce, amnesiac, turnip and rutabaga. J Insect Physiol, 28, 535–539.
  • Gailey, D. A., Jackson, F. R., & Siegel, R. W. (1984). Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics, 106, 613–623.
  • Ganetzky, B., & Wu, C.-F. (1982a). Drosophila mutants with opposing effects on nerve excitability: Genetic and spatial interactions in repetitive firing. J Neurophysiol, 47, 501–514.
  • Ganetzky, B., & Wu, C.-F. (1982b). Indirect suppression involving behavioral mutants with altered nerve excitability in Drosophila melanogaster. Genetics, 100, 597–614.
  • Gong, Z.-F., Xia, S.-Z., Liu, L., Feng, C.-H., & Guo, A.-K. (1998). Operant visual learning and memory in Drosophila mutants dunce, amnesiac and radish. J Insect Physiol, 44, 1149–1158.
  • Griffith, L. C., & Ejima, A. (2009). Courtship learning in Drosophila melanogaster: Diverse plasticity of a reproductive behavior. Learn Mem, 16, 743–750.
  • Griffith, L. C., Wang, J., Zhong, Y., Wu, C.-F., & Greenspan, R. J. (1994). Calcium/calmodulin-dependent protein kinase II and potassium channel subunit Eag similarly affect plasticity in Drosophila. Proc Natl Acad Sci U S A, 91, 10044–10048.
  • Han, P.-L., Levin, L. R., Reed, R. R., & Davis, R. L. (1992). Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron, 9, 619–627.
  • Iourgenko, V., Kilot, B., Cann, M. J., & Levin, L. R. (1997). Cloning and characterization of Drosophila adenylyl cyclase homologous to mammalian type IX. Febs Lett, 413, 104–108.
  • Iourgenko, V., & Levin, L. R. (2000). A calcium-inhibited Drosophila adenylyl cyclase. Biochim Biophys Acta, 1495, 125–139.
  • Johannessen, M., & Moens, U. (2007). Multiple phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front Biosci, 12, 1814–1832.
  • Kauvar, L. M. (1982). Defective cyclic adenosine 3′:5′-monophosphate phosphodiesterase in the Drosophila memory mutant dunce. J Neurosci, 2, 1347–1358.
  • Kim, Y.-T., & Wu, C.-F. (1996). Reduced growth cone motility in cultured neurons from Drosophila memory mutants with a defective cAMP cascade. J Neurosci, 16, 5593–5602.
  • Kuromi, H., & Kidokoro, Y. (2000). Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron, 27, 133–143.
  • Larkin, A., Karak, S., Priya, R., Das, A., Ayyub, C., Ito, K., Rodrigues, V., & Ramaswami, M. (2010). Central synaptic mechanisms underlie short-term olfactory habituation in Drosophila larvae. Learn Mem, 17, 645–653.
  • Lee, J., Ueda, A., & Wu, C.-F. (2008). Pre- and post-synaptic mechanisms of synaptic strength homeostasis revealed by slowpoke and Shaker K + channel mutations in Drosophila. Neuroscience, 154, 1283–1296.
  • Levin, L. R., Han, P.-L., Hwang, P. M., Feinstein, P. G., Davis, R. L., & Reed, R. R. (1992). The Drosophila learning and memory gene rutabaga encodes a Ca2 + /calmodulin-responsive adenylyl cyclase. Cell, 68, 479–489.
  • Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M., & Liu, L. (2006). Distinct memory traces for two visual features in the Drosophila brain. Nature, 439, 551–556.
  • Livingstone, M. S., Sziber, P. P., & Quinn, W. G. (1984). Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell, 37, 205–215.
  • Mery, F., Belay, A. T., So, A. K.-C., Sokolowski, M. B., & Kawecki, T. J. (2007). Natural polymorphism affecting learning and memory in Drosophila. Proc Natl Acad Sci USA, 104, 13051–13055.
  • Mohler, D., & Carroll, A. (1984). Sex-linked female-sterile mutations in the Iowa collection. DIS, 60, 236–241.
  • Moore, M. S., DeZazzo, J., Luk, A. Y., Tully, T., Singh, C. M., & Heberlein, U. (1998). Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell, 93, 997–1007.
  • Nighorn, A., Healy, M. J., & Davis, R. L. (1991). The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron, 6, 455–467.
  • Peng, I.-F., Berke, B. A., Zhu, Y., Lee, W.-H., Chen, W., & Wu, C.-F. (2007). Temperature-dependent developmental plasticity of Drosophila neurons: Cell-autonomous roles of membrane excitability, Ca2 + influx, and cAMP signaling. J Neurosci, 27, 12611–12622.
  • Qiu, Y., Chen, C.-N., Malone, T., Richter, L., Beckendorf, S. K., & Davis, R. L. (1991). Characterization of the memory gene dunce of Drosophila melanogaster. J Mol Biol, 222, 553–565.
  • Renger, J. J., Ueda, A., Atwood, H. L., Govind, C. K., & Wu, C.-F. (2000). Role of cAMP cascade in synaptic stability and plasticity: Ultrastructural and physiological analysis of individual synaptic boutons in Drosophila memory mutants. J Neurosci, 20, 3980–3992.
  • Renger, J. J., Yao, W.-D., Sokolowski, M. B., & Wu, C.-F. (1999). Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. J Neurosci, 19, RC28.
  • Salz, H. K., Davis, R. L., & Kiger, J. A., Jr. (1982). Genetic analysis of chromomere 3D4 in Drosophila melanogaster: The dunce and sperm-amotile gene. Genetics, 100, 587–596.
  • Schuster, C. M., Davis, G. W., Fetter, R. D., & Goodman, C. S. (1996). Genetic dissection of structudal and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron, 17, 655–667.
  • Sigrist, S. J., Thiel, P. R., Reiff, D. F., Lachance, P. E. D., Lasko, P., & Schuster, G. M. (2000). Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature, 405, 1062–1065.
  • Song, H.-J., Ming, G.-L., & Poo, M.-m. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature, 388, 275–279.
  • Suzuki, K., Grinnell, A. D., & Kidokoro, Y. (2002). Hypertonicity-induced transmitter release at Drosophila neuromuscular junctions is partly mediated by integrins and cAMP/protein kinase A. J Physiol, 538, 103–119.
  • Tempel, B. L., Bonini, N., Dawson, D. R., & Quinn, W. G. (1983). Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci USA, 80, 1482–1486.
  • Tully, T., & Quinn, W. G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A, 157, 263–277.
  • Wustmann, G., Rein, K., Wolf, R., & Heisenberg, M. (1996). A new paradigm for operant conditioning of Drosophila melanogaster. J Comp Physiol A, 179, 429–436.
  • Yao, W.-D., Rusch, J., Poo, M.-m., & Wu, C.-F. (2000). Spontaneous acetylcholine secretion from developing growth cones of Drosophila central neurons in culture: Effects of cAMP-pathway mutations. J Neurosci, 20, 2626–2637.
  • Yao, W.-D., & Wu, C.-F. (2001). Distinct roles of CaMKII and PKA in regulation of firing patterns and K + currents in Drosophila neurons. J Neurophysiol, 85, 1384–1394.
  • Zars, T., Wolf, R., Davis, R., & Heisenberg, M. (2000). Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: In search of the engram. Learn Mem, 7, 18–31.
  • Zhao, M.-L., & Wu, C.-F. (1997). Alterations in frequency coding and activity dependence of excitability in cultured neurons of Drosophila memory mutants. J Neurosci, 17, 2187–2199.
  • Zhong, Y., Budnik, V., & Wu, C.-F. (1992). Synaptic plasticity in Drosophila memory and hyperexcitable mutants: Role of cAMP cascade. J Neurosci, 12, 644–651.
  • Zhong, Y., & Wu, C.-F. (1991). Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science, 251, 198–201.
  • Zhong, Y., & Wu, C.-F. (1993). Differential modulation of potassium currents by cAMP and its long-term and short-term effects: dunce and rutabaga mutants of Drosophila. J Neurogenet, 9, 15–27.
  • Zhong, Y., & Wu, C.-F. (2004). Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci, 24, 1439–1445.

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