Synaptic transmission in neurons that express the Drosophila atypical soluble guanylyl cyclases, Gyc-89Da and Gyc-89Db, is necessary for the successful completion of larval and adult ecdysis

Journal of Experimental Biology

Volumn 211, Issue 10, 2008, Pages 1645-1656

  Morton, David B ^a   Stewart, Judith A ^a   Langlais, Kristofor K ^a   Clemens Grisham, Rachel A ^a   Vermehren, Anke ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; GUANYLATE CYCLASE; PRIMER DNA; TETANUS TOXIN;

ANIMAL; ARTICLE; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; DROSOPHILA MELANOGASTER; GENETICS; IN SITU HYBRIDIZATION; LARVA; METABOLISM; MOLECULAR CLONING; MOLTING; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; CLONING, MOLECULAR; DNA PRIMERS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GUANYLATE CYCLASE; IN SITU HYBRIDIZATION; LARVA; MICROSCOPY, CONFOCAL; MOLTING; RECEPTORS, CELL SURFACE; SYNAPTIC TRANSMISSION; TETANUS TOXIN;

DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 46949105729     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.014472     Document Type: Article

References (46)

1. Baines, R. A., Robinson, S. G., Fujioka, M., Jaynes, J. B. and Bate, M. (1999). Postsynaptic expression of tetanus toxin light chain blocks synaptogenesis in Drosophila. Curr. Biol. 9, 1267-1270.
2. Barolo, S., Carver, L. A. and Posakony, J. W. (2000). GFP and b-Galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. BioTechniques 29, 727-732.
3. Bodmer, R., Barbel, S., Shepard, S., Jack, J. W., Jan, L. Y. and Jan, Y. N. (1987). Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51, 293-307.
4. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
5. Broderick, K. E., Kean, L., Dow, J. A., Pyne, N. J. and Davies, S. A. (2004). Ectopic expression of bovine type 5 phosphodiesterase confers a renal phenotype in Drosophila. J. Biol. Chem. 279, 8159-8168.
6. Campos-Ortega, J. and Hartenstein, V. (1997). Embryonic Development of Drosophila melanogaster (2nd edn). Berlin: Springer-Verlag.
7. Clark, A. C., del Campo, M. L. and Ewer, J. (2004). Neuroendocrine control of larval ecdysis behavior in Drosophila: complex regulation by partially redundant neuropeptides. J. Neurosci. 24, 4283-4292.
8. Ewer, J. and Reynolds, S. (2002). Neuropeptide control of molting in insects. Horm. Brain Behav. 3, 1-92.
9. Gray, J. M., Karow, D. S., Lu, H., Chang, A. J., Chang, J. S., Ellis, R. E., Martietta, M. A. and Bargmann, C. I. (2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317-322.
10. Greenspan, R. J. (1997). Fly Pushing. Plainview: Cold Spring Harbor Laboratory Press.
11. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878.
12. Heimbeck, G., Bugnon, V., Gendre, N., Habelin, C. and Stocker, R. F. (1999). Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J. Neurosci. 19, 6599-6609.
13. Hewes, R. S., Park, D., Gauthier, S. A., Schaefer, A. and Taghert, P. H. (2003). The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130, 1771-1781.
14. Hiesinger, P. R., Reiter, C., Schau, H. and Fischbach, K. F. (1999). Neuropil pattern formation and regulation of cell adhesion molecules in Drosophila optic lobe development depends on synaptobrevin. J. Neurosci. 19, 7548-7556.
15. Horodyski, F. M., Ewer, J., Riddiford, L. M. and Truman, J. W. (1993). Isolation, characterization and expression of the eclosion hormone gene in Drosophila melanogaster. Eur. J. Biochem. 215, 221-228.
16. Kim, Y.-J., Spalovská-Valachová, I., Cho, K.-H., Zitnanova, I., Park, Y., Adams, M. E. and Žitnan, D. (2004). Corazonin receptor signaling in ecdysis initiation. Proc. Natl. Acad. Sci. USA 101, 6704-6709.
17. Kimura, K. and Truman, J. W. (1990). Postmetamorphic cell death in the nervous and muscular systems of Drosophila melanogaster. J. Neurosci. 10, 403-411.
18. Langlais, K. K., Stewart, J. A. and Morton, D. B. (2004). Preliminary characterization of two atypical sGC in the central and peripheral nervous system of Drosophila melanogaster. J. Exp. Biol. 207, 2323-2338.
19. Link, E., Edelman, L., Chou, J. H., Binz, T., Yamasaki, S., Eisel, U., Baumert, M., Südhof, T. C., Niemann, H. and Jahn, R. (1992). Tetanus toxin action: inhibition of neurotransmitter release linked to synaptobrevin proteolysis. Biochem. Biophys. Res. Commun. 189, 1017-1023.
20. Lucas, K. A., Pitari, G. M., Kazerounian, S., Ruiz-Stewart, I., Park, J., Schulz, S., Chepenik, K. P. and Waldman, S. A. (2000). Guanylyl cyclases and signaling by cyclic GMP. Pharmacol. Rev. 52, 375-413.
21. Martin, J. R., Keller, A. and Sweeney, S. T. (2002). Targeted expression of tetanus toxin: a new tool to study the neurobiology of behavior. Adv. Genet. 47, 1-47.
22. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory function in Drosophila. Science 302, 1765-1768.
23. McNabb, S. L., Baker, J. D., Agapite, J., Steller, H., Riddiford, L. M. and Truman, J. W. (1997). Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19, 813-823.
24. Meng, X., Wahlstrom, G., Immonen, T., Kolmer, M., Tirronen, M., Predel, R., Kalkkinen, N., Heino, T., Sariola, H. and Roos, C. (2002). The Drosophila hugin gene codes for myostimulatory and ecdysis-modifying neuropeptides. Mech. Dev. 117, 5-13.
25. Morton, D. B. (2004a). Invertebrates yield a plethora of atypical guanylyl cyclases. Mol. Neurol. 29, 97-115.
26. Morton, D. B. (2004b). Atypical sGCs in Drosophila can function as molecular oxygen sensors. J. Biol. Chem. 279, 50651-50653.
27. Morton, D. B. and Hudson, M. L. (2002). Cyclic GMP regulation and function in insects. Adv. Insect Physiol. 29, 1-54.
28. Morton, D. B. and Simpson, P. J. (2002). Cellular signaling in eclosion hormone action. J. Insect Physiol. 48, 1-13.
29. Morton, D. B., Langlais, K. K., Steward, J. A. and Vermehren, A. (2005a). Comparison of the properties of the five sGC subunits in Drosophila melanogaster. J. Insect Sci. 5, 12.
30. Morton, D. B., Langlais, K. K., Steward, J. A. and Vermehren, A. (2005b). Atypical sGCs in Drosophila as possible oxygen sensors. 2005 abstract viewer/itinerary planner, program 613.7. Washington, DC: Society for Neuroscience. http://www.stn.org/index.cfm?pagename=abstracts_ampublications.
31. O'Brien, M. A. and Taghert, P. H. (1998). A peritracheal neuropeptides system in insects: release of myomodulin-like peptides at ecdysis. J. Exp. Biol. 201, 193-209.
32. Osborne, K. A., Robichon, A., Burgess, E., Butland, S., Shaw, R. A., Coulthard, A., Pereira, H. S., Greenspan, R. J. and Sokolowski, M. B. (1997). Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834-836.
33. Park, D., Han, M., Kim, Y. C., Han, K. A. and Taghert, P. H. (2004). Ap-let neurons - a peptidergic circuit potentially controlling ecdysial behavior in Drosophila. Dev. Biol. 269, 95-108.
34. Park, J. H., Schroeder, A. J., Helfrich-Forster, C., Jackson, F. R. and Ewer, J. (2003). Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130, 2645-2656.
35. Park, Y., Filippov, V., Gill, S. S. and Adams, M. E. (2002). Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 129, 493-503.
36. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., DeLaurento, P. P., DasGupta, B. R. and Montecucco, C. (1992). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
37. Sharma, Y., Cheung, U., Larsen, E. W. and Eberl, D. F. (2002). PPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in Drosophila. Genesis 34, 115-118.
38. Stocker, R. F. (1994). The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26.
39. Sullivan, W., Ashburner, M. and Hawler, R. S. (2000). Drosophila Protocols. New York: Cold Spring Harbor Laboratory Press.
40. Sweeney, S. T., Kendal, B., Keane, J., Niemann, H. and O'Kane, C. J. (1995). Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral effects. Neuron 14, 341-351.
41. Truman, J. W., Taghert, P. H., Copenhaver, P. F., Tublitz, N. J. and Schwartz, L. M. (1981). Eclosion hormone may control all ecdyses in insects. Nature 291, 70-71.
42. Vermehren, A., Langlais, K. K. and Morton, D. B. (2006). Oxygen-sensitive guanylyl cyclases in insects and their potential roles in oxygen detection and in feeding behaviors. J. Insect Physiol. 52, 340-348.
43. Wingrove, J. A. and O'Farrell, P. H. (1999). Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105-114.
44. Yocum, R. R. and Johnston, M. (1984). Molecular cloning of the GAL80 gene from Saccharomyces cerevisiae and characterization of a gal80 deletion. Gene 32, 75-82.
45. Zdárek, J. and Friedman, S. (1986). Pupal ecdysis in flies: mechanisms of evagination of the head and expansion of the thoracic appendages. J. Insect Physiol. 32, 917-923.
46. Zeidler, M. P., Tan, C., Bellaiche, Y., Cherry, S., Hader, S., Gayko, U. and Perrimon, N. (2004). Temperature-sensitive control of protein activity by conditionally splicing inteins. Nat. Biotechnol. 22, 871-876.