cAMP Signals in Drosophila Motor Neurons Are Confined to Single Synaptic Boutons

Cell Reports

Volumn 17, Issue 5, 2016, Pages 1238-1246

  Maiellaro, Isabella ^a   Lohse, Martin J ^a,c   Kittel, Robert J ^b   Calebiro, Davide ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

active zone; cAMP; dunce; FRET; GPCR; octopamine; PDE; synaptic plasticity

Indexed keywords

CYCLIC AMP; FORSKOLIN; OCTOPAMINE RECEPTOR; PHOSPHODIESTERASE; RECEPTOR; UNCLASSIFIED DRUG; OCTOPAMINE;

ANIMAL CELL; ARTICLE; CELL BODY; CELL COMPARTMENTALIZATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; MOTONEURON; NERVE CELL PLASTICITY; NEUROMUSCULAR JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ANIMAL; AXON; DROSOPHILA MELANOGASTER; DRUG EFFECTS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IONTOPHORESIS; METABOLISM; NERVE ENDING;

ANIMALS; AXONS; CELL BODY; CYCLIC AMP; DROSOPHILA MELANOGASTER; FLUORESCENCE RESONANCE ENERGY TRANSFER; IONTOPHORESIS; MOTOR NEURONS; OCTOPAMINE; PHOSPHORIC DIESTER HYDROLASES; PRESYNAPTIC TERMINALS; SIGNAL TRANSDUCTION;

EID: 84994709509     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.09.090     Document Type: Article

References (41)

1. Bacskai, B.J., Hochner, B., Mahaut-Smith, M., Adams, S.R., Kaang, B.K., Kandel, E.R., Tsien, R.Y., Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260 (1993), 222–226.
2. Börner, S., Schwede, F., Schlipp, A., Berisha, F., Calebiro, D., Lohse, M.J., Nikolaev, V.O., FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat. Protoc. 6 (2011), 427–438.
3. Calebiro, D., Maiellaro, I., cAMP signaling microdomains and their observation by optical methods. Front. Cell. Neurosci., 8, 2014, 350.
4. Castro, L.R., Gervasi, N., Guiot, E., Cavellini, L., Nikolaev, V.O., Paupardin-Tritsch, D., Vincent, P., Type 4 phosphodiesterase plays different integrating roles in different cellular domains in pyramidal cortical neurons. J. Neurosci. 30 (2010), 6143–6151.
5. Collins, C.A., DiAntonio, A., Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 17 (2007), 35–42.
6. Conti, M., Mika, D., Richter, W., Cyclic AMP compartments and signaling specificity: role of cyclic nucleotide phosphodiesterases. J. Gen. Physiol. 143 (2014), 29–38.
7. Corbin, J.D., Sugden, P.H., Lincoln, T.M., Keely, S.L., Compartmentalization of adenosine 3′:5′-monophosphate and adenosine 3′:5′-monophosphate-dependent protein kinase in heart tissue. J. Biol. Chem. 252 (1977), 3854–3861.
8. Davis, R.L., Kiger, J.A. Jr., Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J. Cell Biol. 90 (1981), 101–107.
9. Ehmann, N., van de Linde, S., Alon, A., Ljaschenko, D., Keung, X.Z., Holm, T., Rings, A., DiAntonio, A., Hallermann, S., Ashery, U., et al. Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states. Nat. Commun., 5, 2014, 4650.
10. Frank, C.A., Homeostatic plasticity at the Drosophila neuromuscular junction. Neuropharmacology, 2013.
11. Gervasi, N., Tchénio, P., Preat, T., PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65 (2010), 516–529.
12. Griffith, L.C., Budnik, V., Plasticity and second messengers during synapse development. Int. Rev. Neurobiol. 75 (2006), 237–265.
13. Hempel, C.M., Vincent, P., Adams, S.R., Tsien, R.Y., Selverston, A.I., Spatio-temporal dynamics of cyclic AMP signals in an intact neural circuit. Nature 384 (1996), 166–169.
14. Hoang, B., Chiba, A., Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 229 (2001), 55–70.
15. Kahsai, L., Zars, T., Learning and memory in Drosophila: behavior, genetics, and neural systems. Int. Rev. Neurobiol. 99 (2011), 139–167.
16. Kandel, E.R., Dudai, Y., Mayford, M.R., The molecular and systems biology of memory. Cell 157 (2014), 163–186.
17. Koon, A.C., Ashley, J., Barria, R., DasGupta, S., Brain, R., Waddell, S., Alkema, M.J., Budnik, V., Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat. Neurosci. 14 (2011), 190–199.
18. Li, L., Gervasi, N., Girault, J.A., Dendritic geometry shapes neuronal cAMP signalling to the nucleus. Nat. Commun., 6, 2015, 6319.
19. Ljaschenko, D., Ehmann, N., Kittel, R.J., Hebbian plasticity guides maturation of glutamate receptor fields in vivo. Cell Rep. 3 (2013), 1407–1413.
20. Marrus, S.B., DiAntonio, A., Preferential localization of glutamate receptors opposite sites of high presynaptic release. Curr. Biol. 14 (2004), 924–931.
21. Melom, J.E., Akbergenova, Y., Gavornik, J.P., Littleton, J.T., Spontaneous and evoked release are independently regulated at individual active zones. J. Neurosci. 33 (2013), 17253–17263.
22. Nagarkar-Jaiswal, S., Lee, P.T., Campbell, M.E., Chen, K., Anguiano-Zarate, S., Gutierrez, M.C., Busby, T., Lin, W.W., He, Y., Schulze, K.L., et al. A library of MiMICs allows tagging of genes and reversible, spatial and temporal knockdown of proteins in Drosophila. eLife, 4, 2015, 4.
23. Neves, S.R., Tsokas, P., Sarkar, A., Grace, E.A., Rangamani, P., Taubenfeld, S.M., Alberini, C.M., Schaff, J.C., Blitzer, R.D., Moraru, I.I., Iyengar, R., Cell shape and negative links in regulatory motifs together control spatial information flow in signaling networks. Cell 133 (2008), 666–680.
24. Nicol, X., Hong, K.P., Spitzer, N.C., Spatial and temporal second messenger codes for growth cone turning. Proc. Natl. Acad. Sci. USA 108 (2011), 13776–13781.
25. Nicoll, R.A., Schmitz, D., Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6 (2005), 863–876.
26. Nikolaev, V.O., Bünemann, M., Hein, L., Hannawacker, A., Lohse, M.J., Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279 (2004), 37215–37218.
27. Olsen, D.P., Keshishian, H., Experimental methods for examining synaptic plasticity in Drosophila. Cold Spring Harb. Protoc. 2012 (2012), 162–173.
28. Paul, M.M., Pauli, M., Ehmann, N., Hallermann, S., Sauer, M., Kittel, R.J., Heckmann, M., Bruchpilot and Synaptotagmin collaborate to drive rapid glutamate release and active zone differentiation. Front. Cell. Neurosci., 9, 2015, 29.
29. Peled, E.S., Isacoff, E.Y., Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons. Nat. Neurosci. 14 (2011), 519–526.
30. Rich, T.C., Fagan, K.A., Tse, T.E., Schaack, J., Cooper, D.M., Karpen, J.W., A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc. Natl. Acad. Sci. USA 98 (2001), 13049–13054.
31. Sanyal, S., Genomic mapping and expression patterns of C380, OK6 and D42 enhancer trap lines in the larval nervous system of Drosophila. Gene Expr. Patterns 9 (2009), 371–380.
32. Sasaki, T., Matsuki, N., Ikegaya, Y., Targeted axon-attached recording with fluorescent patch-clamp pipettes in brain slices. Nat. Protoc. 7 (2012), 1228–1234.
33. Saucerman, J.J., Greenwald, E.C., Polanowska-Grabowska, R., Mechanisms of cyclic AMP compartmentation revealed by computational models. J. Gen. Physiol. 143 (2014), 39–48.
34. Schmid, A., Hallermann, S., Kittel, R.J., Khorramshahi, O., Frölich, A.M., Quentin, C., Rasse, T.M., Mertel, S., Heckmann, M., Sigrist, S.J., Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 11 (2008), 659–666.
35. Shafer, O.T., Kim, D.J., Dunbar-Yaffe, R., Nikolaev, V.O., Lohse, M.J., Taghert, P.H., Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58 (2008), 223–237.
36. Stewart, B.A., Atwood, H.L., Renger, J.J., Wang, J., Wu, C.F., Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 175 (1994), 179–191.
37. Tomchik, S.M., Davis, R.L., Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64 (2009), 510–521.
38. Wagh, D.A., Rasse, T.M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., Buchner, S., Dabauvalle, M.C., Schmidt, M., Qin, G., et al. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49 (2006), 833–844.
39. Zaccolo, M., Spatial control of cAMP signalling in health and disease. Curr. Opin. Pharmacol. 11 (2011), 649–655.
40. Zhong, Y., Wu, C.F., Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J. Neurosci. 24 (2004), 1439–1445.
41. Zhong, Y., Budnik, V., Wu, C.F., Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12 (1992), 644–651.