A neuropeptide signaling pathway regulates synaptic growth in Drosophila

Journal of Cell Biology

Volumn 196, Issue 4, 2012, Pages 529-543

  Chen, Xu ^a   Ganetzky, Barry ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DROSULFAKININ; NEUROPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE MUTATION; LEARNING; MEMORY; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PHENOTYPE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CLONING, MOLECULAR; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGY; FEMALE; IMMUNOENZYME TECHNIQUES; LARVA; MALE; MUTATION; NEUROMUSCULAR JUNCTION; NEUROPEPTIDES; OLIGOPEPTIDES; PRESYNAPTIC TERMINALS; RECEPTORS, CHOLECYSTOKININ; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84859966523     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201109044     Document Type: Article

References (38)

1. Adams, M.E., and M. O'Shea. 1983. Peptide cotransmitter at a neuromuscular junction. Science. 221:286-289. http://dx.doi.org/10.1126/science.6134339
2. Alberini, C.M. 2009. Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89:121-145. http://dx.doi.org/10.1152/physrev.00017.2008
3. Audsley, N., and R.J. Weaver. 2009. Neuropeptides associated with the regulation of feeding in insects. Gen. Comp. Endocrinol. 162:93-104. http:// dx.doi.org/10.1016/j.ygcen.2008.08.003
4. Benito, E., and A. Barco. 2010. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci. 33:230-240. http://dx.doi.org/10.1016/j.tins.2010.02.001
5. Cann, M.J., and L.R. Levin. 1998. Genetic characterization of adenylyl cyclase function. Adv. Second Messenger Phosphoprotein Res. 32:121-135.
6. Collins, C.A., and A. DiAntonio. 2007. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 17:35-42. http://dx.doi.org/10.1016/j.conb.2007.01.001
7. Collins, C.A., Y.P. Wairkar, S.L. Johnson, and A. DiAntonio. 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron. 51:57-69. http://dx.doi.org/10.1016/j.neuron.2006.05.026
8. Davis, G.W., C.M. Schuster, and C.S. Goodman. 1996. Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron. 17:669-679. http://dx.doi.org/10.1016/S0896-6273(00)80199-3
9. Davis, G.W., C.M. Schuster, and C.S. Goodman. 1997. Genetic analysis of the mechanisms controlling target selection: target-derived Fasciclin II regulates the pattern of synapse formation. Neuron. 19:561-573. http://dx.doi.org/10.1016/S0896-6273(00)80372-4
10. Featherstone, D.E., and K. Broadie. 2000. Surprises from Drosophila: genetic mechanisms of synaptic development and plasticity. Brain Res. Bull. 53:501-511. http://dx.doi.org/10.1016/S0361-9230(00)00383-X
11. Gilman, A.G. 1987. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56:615-649. http://dx.doi.org/10.1146/annurev.bi.56.070187.003151
12. Hewes, R.S., E.C. Snowdeal III, M. Saitoe, and P.H. Taghert. 1998. Functional redundancy of FMRFamide-related peptides at the Drosophila larval neuromuscular junction. J. Neurosci. 18:7138-7151.
13. Koon, A.C., J. Ashley, R. Barria, S. DasGupta, R. Brain, S. Waddell, M.J. Alkema, and V. Budnik. 2011. Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat. Neurosci. 14:190-199. http://dx.doi.org/10.1038/nn.2716
14. Levin, L.R., P.L. Han, P.M. Hwang, P.G. Feinstein, R.L. Davis, and R.R. Reed. 1992. The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell. 68:479-489. http:// dx.doi.org/10.1016/0092-8674(92)90185-F
15. Li, C., K. Kim, and L.S. Nelson. 1999. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res. 848:26-34. http://dx.doi.org/10.1016/S0006-8993(99)01972-1
16. Manseau, L., A. Baradaran, D. Brower, A. Budhu, F. Elefant, H. Phan, A.V. Philp, M. Yang, D. Glover, K. Kaiser, et al. 1997. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209:310-322. http://dx.doi.org/10.1002/(SICI)1097-0177(199707)209:3<310::AID-AJA6>3.0.CO;2-L
17. Martin, A.R. 1955. A further study of the statistical composition on the end-plate potential. J. Physiol. 130:114-122.
18. McCudden, C.R., M.D. Hains, R.J. Kimple, D.P. Siderovski, and F.S. Willard. 2005. G-protein signaling: back to the future. Cell. Mol. Life Sci. 62:551-577. http://dx.doi.org/10.1007/s00018-004-4462-3
19. Nässel, D.R. 2002. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog. Neurobiol. 68:1-84. http://dx.doi.org/10.1016/S0301-0082(02)00057-6
20. Nässel, D.R., and A.M. Winther. 2010. Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92:42-104. http://dx.doi.org/10.1016/j.pneurobio.2010.04.010
21. Neves, S.R., P.T. Ram, and R. Iyengar. 2002. G protein pathways. Science. 296:1636-1639. http://dx.doi.org/10.1126/science.1071550
22. Nichols, R. 1992. Isolation and expression of the Drosophila drosulfakinin neural peptide gene product, DSK-I. Mol. Cell. Neurosci. 3:342-347. http://dx.doi.org/10.1016/1044-7431(92)90031-V
23. Nichols, R. 2003. Signaling pathways and physiological functions of Drosophila melanogaster FMRFamide-related peptides. Annu. Rev. Entomol. 48: 485-503. http://dx.doi.org/10.1146/annurev.ento.48.091801.112525
24. Nichols, R. 2006. FMRFamide-related peptides and serotonin regulate Drosophila melanogaster heart rate: mechanisms and structure requirements. Peptides. 27:1130-1137. http://dx.doi.org/10.1016/j.peptides.2005.07.032
25. Perazzona, B., G. Isabel, T. Preat, and R.L. Davis. 2004. The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24:8823-8828. http://dx.doi.org/10.1523/JNEUROSCI.4542-03.2004
26. Petersen, S.A., R.D. Fetter, J.N. Noordermeer, C.S. Goodman, and A. DiAntonio. 1997. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron. 19:1237-1248. http://dx.doi.org/10.1016/S0896-6273(00)80415-8
27. Price, D.A., and M.J. Greenberg. 1977. Structure of a molluscan cardioexcitatory neuropeptide. Science. 197:670-671. http://dx.doi.org/10.1126/science.877582
28. Rathmayer, W., S. Djokaj, A. Gaydukov, and S. Kreissl. 2002. The neuromuscular junctions of the slow and the fast excitatory axon in the closer of thecrab Eriphia spinifrons are endowed with different Ca2+ channel types and allow neuron-specific modulation of transmitter release by two neuropeptides. J. Neurosci. 22:708-717.
29. Renden, R.B., and K. Broadie. 2003. Mutation and activation of Galpha s similarly alters pre- and postsynaptic mechanisms modulating neurotransmission. J. Neurophysiol. 89:2620-2638. http://dx.doi.org/10.1152/jn.01072.2002
30. Robb, S., and P. Evans. 1994. The modulatory effect of SchistoFLRFmide on heart and skeletal muscle in the locust Schistocerca gregaria. J. Exp. Biol. 197:437-442.
31. Schmidt, H., A. Stonkute, R. Jüttner, D. Koesling, A. Friebe, and F.G. Rathjen. 2009. C-type natriuretic peptide (CNP) is a bifurcation factor for sensory neurons. Proc. Natl. Acad. Sci. USA. 106:16847-16852. http://dx.doi.org/10.1073/pnas.0906571106
32. Schuster, C.M., G.W. Davis, R.D. Fetter, and C.S. Goodman. 1996a. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron. 17:641-654. http://dx.doi.org/10.1016/S0896-6273(00)80197-X
33. Schuster, C.M., G.W. Davis, R.D. Fetter, and C.S. Goodman. 1996b. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron. 17:655-667. http://dx.doi.org/10.1016/S0896-6273(00)80198-1
34. Stewart, B.A., H.L. Atwood, J.J. Renger, J. Wang, and C.F. Wu. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 175:179-191. http://dx.doi.org/10.1007/BF00215114
35. Tettamanti, M., J.D. Armstrong, K. Endo, M.Y. Yang, K. Furukubo-Tokunaga, K. Kaiser, and H. Reichert. 1997. Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev. Genes Evol. 207:242-252. http://dx.doi.org/10.1007/s004270050112
36. Wan, H.I., A. DiAntonio, R.D. Fetter, K. Bergstrom, R. Strauss, and C.S. Goodman. 2000. Highwire regulates synaptic growth in Drosophila. Neuron. 26:313-329. http://dx.doi.org/10.1016/S0896-6273(00)81166-6
37. Wolfgang, W.J., C. Clay, J. Parker, R. Delgado, P. Labarca, Y. Kidokoro, and M. Forte. 2004. Signaling through Gs alpha is required for the growth and function of neuromuscular synapses in Drosophila. Dev. Biol. 268:295-311. http://dx.doi.org/10.1016/j.ydbio.2004.01.007
38. Zhong, Y., V. Budnik, and C.F. Wu. 1992. Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12:644-651.