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

Morton, David B.; Stewart, Judith; Langlais, Kristofor K.; Clemens-Grisham, Rachel; Vermehren, Anke

doi:10.1242/jeb.014472

Cited by 23 publications

(28 citation statements)

References 42 publications

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“…ND, not determined. 89Da and Gyc-89Db subunits are expressed extensively in the Drosophila nervous system, in both central and peripheral neurons (Langlais et al 2004;Morton et al 2008) (for a schematic see Figure 7A). There are relatively few cells that co-express both subunits.…”

Section: Discussionmentioning

confidence: 99%

“…background, which had to be kept over a MKRS balancer, with sufficient double homozygous flies eclosing for the rescue crosses. The transgenic GAL4 driver lines for Gyc-89Da and Gyc-89Db (Gyc-89Da GAL4 , Gyc-89Db GAL4 ) were generated by germline transformation as described earlier (Morton et al 2008).…”

Section: Methodsmentioning

confidence: 99%

“…We then used these fly lines in combination with the previously described Gyc-89Da and Gyc-89Db promoter-GAL4 lines (Morton et al 2008) to express either subunit in either subset of cells in all the different mutant backgrounds. To test the expression of Gyc-89Da and Gyc89Db driven by the GAL4-UAS system, we performed an RT-PCR analysis, which showed that the expression of both genes was restored in the different mutant backgrounds (Figure1B and Figure S1).…”

Section: Dbmentioning

confidence: 99%

“…To confirm that the increased time to respond to hypoxia was due to the loss of Gyc-89Da and Gyc-89Db we crossed GAL4 driver lines that drive expression in either the Gyc-89Da or Gyc-89Db cells (Langlais et al 2004;Morton et al 2008) with the UAS Gyc-89Da and UAS Gyc-89Db cDNA rescue lines into each of the three mutant backgrounds (see Table S3 for hypoxia escape response values of parental lines). On the basis of our previous data, the promoter regions used in the Gyc89Da GAL4 and Gyc-89Db GAL4 constructs drive expression in populations of neurons that are broadly nonoverlapping, with only a few sensory neurons observed that coexpress both Gyc-89Da and Gyc-89Db (Morton et al 2008).…”

Section: Dbmentioning

confidence: 99%

“…On the basis of our previous data, the promoter regions used in the Gyc89Da GAL4 and Gyc-89Db GAL4 constructs drive expression in populations of neurons that are broadly nonoverlapping, with only a few sensory neurons observed that coexpress both Gyc-89Da and Gyc-89Db (Morton et al 2008). The delayed hypoxia escape response seen in the single mutants was fully rescued for 0, 5, and 10% O 2 concentration by expressing either Gyc-89Da or Gyc89Db in either the Gyc-89Da or the Gyc-89Db neurons (Figure 2, B and C).…”

Section: Dbmentioning

confidence: 99%

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Behavioral Responses to Hypoxia in Drosophila Larvae Are Mediated by Atypical Soluble Guanylyl Cyclases

et al. 2010

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The three Drosophila atypical soluble guanylyl cyclases, Gyc-89Da, Gyc-89Db, and Gyc-88E, have been proposed to act as oxygen detectors mediating behavioral responses to hypoxia. Drosophila larvae mutant in any of these subunits were defective in their hypoxia escape response-a rapid cessation of feeding and withdrawal from their food. This response required cGMP and the cyclic nucleotide-gated ion channel, cng, but did not appear to be dependent on either of the cGMP-dependent protein kinases, dg1 and dg2. Specific activation of the Gyc-89Da neurons using channel rhodopsin showed that activation of these neurons was sufficient to trigger the escape behavior. The hypoxia escape response was restored by reintroducing either Gyc-89Da or Gyc-89Db into either Gyc-89Da or Gyc-89Db neurons in either mutation. This suggests that neurons that co-express both Gyc-89Da and Gyc-89Db subunits are primarily responsible for activating this behavior. These include sensory neurons that innervate the terminal sensory cones. Although the roles of Gyc-89Da and Gyc-89Db in the hypoxia escape behavior appeared to be identical, we also showed that changes in larval crawling behavior in response to either hypoxia or hyperoxia differed in their requirements for these two atypical sGCs, with responses to 15% oxygen requiring Gyc-89Da and responses to 19 and 25% requiring Gyc-89Db. For this behavior, the identity of the neurons appeared to be critical in determining the ability to respond appropriately.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Dbmentioning

confidence: 99%

Section: Dbmentioning

confidence: 99%

Section: Dbmentioning

confidence: 99%

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Behavioral Responses to Hypoxia in Drosophila Larvae Are Mediated by Atypical Soluble Guanylyl Cyclases

et al. 2010

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Neuronal Mechanisms of Oxygen Chemoreception: An Invertebrate Perspective

Janes

Syed

2012

Advances in Experimental Medicine and Biology

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Since the evolution of aerobic metabolism, cellular requirements for molecular oxygen have been the major driver for the development of sophisticated mechanisms underlying both invertebrate and vertebrate respiratory behaviour. Among the most important characteristics of respiration is its adaptability, which allows animals to maintain oxygen homeostasis over a wide range of environmental and metabolic conditions. In all animals, the respiratory behaviour is controlled by neural networks often termed respiratory central pattern generators (rCPG). While rCPG neurons are intrinsically capable of generating rhythmical outputs, the respiratory needs are generally "sensed" by either central or peripheral chemoreceptive neurons. The mechanisms by which chemoreceptors respond to changes in oxygen and modulate central respiratory control centers have been the focus of decades of research. However, our understanding of these mechanisms has been limited due to an inability to precisely locate oxygen chemoreceptor populations, combined with the overwhelming complexity of vertebrate neural circuits. Although mammalian models remain the gold standard for research in general, invertebrates do nevertheless offer greatly simplified neural networks that share fundamental similarities with vertebrates. The following review will provide evidence for the existence of oxygen chemoreceptors in many invertebrate groups and reveal the mechanisms by which these neurons may "perceive" environmental oxygen and drive central rCPG activity. For this, we will specifically highlight an invertebrate model, the pond snail Lymnaea stagnalis whose episodic respiratory behaviour resembles that of diving mammals. The rCPG neurons have been identified and fully characterized in this model both in vivo and in vitro. The Lymnaea respiratory network has also been reconstructed in vitro and the contributions of individual rCPG neurons towards rhythm generation characterized through direct intracellular recordings. We now provide evidence for the presence of genuine peripheral oxygen chemoreceptors in Lymnaea, and demonstrate that these neurons respond to hypoxia in a manner analogous to that of mammalian carotid bodies. These chemoreceptor cells not only drive the activity of the rCPG neurons but their synaptic connections also exhibit hypoxia-induced plasticity. The lessons learned from this model will likely reveal fundamental principles underlying both peripheral and central respiratory control mechanisms, which may be conserved in both invertebrate and vertebrate species.

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Drosophila gustatory preference behaviors require the atypical soluble guanylyl cyclases

et al. 2011

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The intracellular messenger cGMP has been suggested to play a role in taste signal transduction in both vertebrates and invertebrates. In the present study, we have examined the role of the Drosophila atypical soluble guanylyl cyclases (sGCs), Gyc-89Da and Gyc-89Db, in larval and adult gustatory preference behaviors. We showed that in larvae, sucrose attraction requires Gyc-89Db and caffeine avoidance requires Gyc-89Da. In adult flies, sucrose attraction is unaffected by mutations in either gene whereas avoidance of low concentrations of caffeine is eliminated by loss of either gene. Similar defective behaviors were observed when cGMP increases were prevented by the expression of a cGMP-specific phosphodiesterase. We also showed that both genes were expressed in gustatory receptor neurons (GRNs) in larval and adult gustatory organs, primarily in a non-overlapping pattern, with the exception of a small group of cells in the adult labellum. In addition, in adults, several cells co-expressed the bitter taste receptor, Gr66a, with either Gyc-89Da or Gyc-89Db. We also showed that the electrophysiological responses of a GRN to caffeine were significantly reduced in flies mutant for the atypical sGCs, suggesting that at least part of the adult behavioral defects were due to a reduced ability to detect caffeine.

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

Cited by 23 publications

References 42 publications

Behavioral Responses to Hypoxia in Drosophila Larvae Are Mediated by Atypical Soluble Guanylyl Cyclases

Behavioral Responses to Hypoxia in Drosophila Larvae Are Mediated by Atypical Soluble Guanylyl Cyclases

Neuronal Mechanisms of Oxygen Chemoreception: An Invertebrate Perspective

Drosophila gustatory preference behaviors require the atypical soluble guanylyl cyclases

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