Oxygen-sensitive guanylyl cyclases in insects and their potential roles in oxygen detection and in feeding behaviors

Vermehren, Anke; Langlais, Kristofor K.; Morton, David B.

doi:10.1016/j.jinsphys.2005.12.001

Cited by 28 publications

(32 citation statements)

References 43 publications

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“…Conventional sGCs are heme proteins that bind, and are regulated by NO and CO, but are unable to bind O 2 (Boon et al 2005). Recent studies have identified the atypical sGCs in C. elegans and Drosophila as likely molecular O 2 sensors that can bind and are regulated by O 2 (Gray et al 2004;Morton 2004b;Vermehren et al 2006;Huang et al 2007;Zimmer et al 2009). Results described here show that in Drosophila, like C. elegans, the atypical sGCs are required for behavioral responses to hypoxia.…”

Section: Discussionmentioning

confidence: 77%

“…The mammalian carotid body is a peripheral chemoreceptor that senses a number of blood-borne stimuli, including hypoxia and hypercapnia, transducing them into neural discharges that initiate a number of cardiorespiratory reflexes (Gonzalez et al 1994;Ló pez-Barneo et al 2008). Both long-term and short-term responses to hypoxia critically depend on the ability to detect decreases in O 2 supply; however, the molecular bases for O 2 -sensing systems have only recently begun to be identified (Gray et al 2004;Morton 2004b;Vermehren et al 2006). For example, within the carotid body, heme oxygenase-2 has been proposed as the O 2 sensor for the sensing of hypoxia in vertebrates (Kemp 2005;Ortega-Sá enz et al 2006).…”

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confidence: 99%

“…Transient expression of different combinations of the Drosophila atypical sGCs in COS-7 cells showed that Gyc-89Da and Gyc-89Db form obligate heterodimers with Gyc-88E, and are potently activated in the absence of O 2 , therefore suggesting a function as O 2 sensors (Morton 2004b;Vermehren et al 2006;Morton and Vermehren 2007). Gyc-88E is also active as a homodimer (Morton 2004b;Huang et al 2007), directly binds O 2 and is also activated by reduced O 2 (Huang et al 2007).…”

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

et al. 2010

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“…We have previously shown that the atypical sGC subunits, Gyc-88E, , are expressed in a subset of central and chemosensory peripheral neurons (Langlais et al, 2004;Morton et al, 2005a). Based on the expression pattern and biochemical properties of these subunits, we predicted that the sGCs formed from the atypical subunits would be involved in olfaction, gustation and/or oxygen sensation (Vermehren et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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

Morton

Stewart

Langlais

et al. 2008

Journal of Experimental Biology

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SUMMARY Insect ecdysis is a precisely coordinated series of behavioral and hormonal events that occur at the end of each molt. A great deal is known about the hormonal events that underlie this process, although less is known about the neuronal circuitry involved. In this study we identified two populations of neurons that are required for larval and adult ecdyses in the fruit fly, Drosophila melanogaster (Meigen). These neurons were identified by using the upstream region of two genes that code for atypical soluble guanylyl cyclases to drive tetanus toxin in the neurons that express these cyclases to block their synaptic activity. Expression of tetanus toxin in neurons that express Gyc-89Da blocked adult eclosion whereas expression of tetanus toxin in neurons that express Gyc-89Db prevented the initiation of the first larval ecdysis. Expression of tetanus toxin in the Gyc-89Da neurons also resulted in about 50% lethality just prior to pupariation; however, this was probably due to suffocation in the food as lethality was prevented by stopping the larvae from burrowing deep within the food. This result is consistent with our model that the atypical soluble guanylyl cyclases can act as molecular oxygen detectors. The expression pattern of these cyclases did not overlap with any of the neurons containing peptides known to regulate ecdysis and eclosion behaviors. By using the conditional expression of tetanus toxin we were also able to demonstrate that synaptic activity in the Gyc-89Da and Gyc-89Db neurons is required during early adult development for adult eclosion.

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“…There are five of these in Drosophila, two of which form an NO-binding heterodimer. 8 Morton reported that cGMP levels rise during hypoxia, and that larval mutants for one of the guanylyl cyclases displayed a slowed behavioral response to hypoxia. The NO-sensitive guanylyl cyclases are co-expressed in specific sensory neurons along the lateral wall and in the caudal sensilla; both places are exposed to atmospheric conditions.…”

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confidence: 99%

Life is a gas

Gibbs

Hoshizaki²

2008

Fly

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Oxygen-sensitive guanylyl cyclases in insects and their potential roles in oxygen detection and in feeding behaviors

Cited by 28 publications

References 43 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

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

Life is a gas

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