Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling

Department of Neurobiology, University of Massachusetts Medical School, Worcester, Massachusetts, USA.
Nature Neuroscience (Impact Factor: 16.1). 02/2011; 14(2):190-9. DOI: 10.1038/nn.2716
Source: PubMed


Adrenergic signaling has important roles in synaptic plasticity and metaplasticity. However, the underlying mechanisms of these functions remain poorly understood. We investigated the role of octopamine, the invertebrate counterpart of adrenaline and noradrenaline, in synaptic and behavioral plasticity in Drosophila. We found that an increase in locomotor speed induced by food deprivation was accompanied by an activity- and octopamine-dependent extension of octopaminergic arbors and that the formation and maintenance of these arbors required electrical activity. Growth of octopaminergic arbors was controlled by a cAMP- and CREB-dependent positive-feedback mechanism that required Octβ2R octopamine autoreceptors. Notably, this autoregulation was necessary for the locomotor response. In addition, octopamine neurons regulated the expansion of excitatory glutamatergic neuromuscular arbors through Octβ2Rs on glutamatergic motor neurons. Our results provide a mechanism for global regulation of excitatory synapses, presumably to maintain synaptic and behavioral plasticity in a dynamic range.

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Available from: Alex C Koon, Sep 30, 2015
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    • "Increased Octb2R expression supports a hormonal mechanism for increased foraging duration in infected free-flying bees, as synaptic growth associated with increased activity requires octopaminedependent extension of octopaminergic arbors. This results in the maintenance of increased locomotor activity , and requires an increase in Octb2R production within glutamatergic motor neurones (Koon et al., 2011). Although flight duration may have an independent hormonal driver, we cannot exclude the possibility that increased flight duration is instead the direct result of energetic stress: N. ceranae-infected bees stop more often and have significantly reduced homing ability (Wolf et al., 2014). "
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    ABSTRACT: Nosema ceranae, an emerging pathogen of the western honeybee (Apis mellifera), is implicated in recent pollinator losses and causes severe energetic stress. However, whether precocious foraging and accelerated behavioural maturation in infected bees are caused by the infection itself or via indirect energetic stress remains unknown. Using a combination of nutritional and infection treatments, we investigated how starvation and infection alters the regulation of adipokinetic hormone (AKH) and octopamine, two highly conserved physiological pathways that respond to energetic stress by mobilizing fat stores and increasing search activity for food. Although there was no response from AKH when bees were experimentally infected with N. ceranae or starved, supporting the notion that honeybees have lost this pathway, there were significant regulatory changes in the octopamine pathway. Significantly, we found no evidence of acute energetic stress being the only cause of symptoms associated with N. ceranae infection. Therefore, the parasite itself appears to alter regulatory components along a highly conserved physiological pathway in an infection-specific manner. This indicates that pathogen-induced behavioural alteration of chronically infected bees should not just be viewed as a coincidental short-term by-product of pathogenesis (acute energetic stress) and may be a result of a generalist manipulation strategy to obtain energy for reproduction. © 2015 The Royal Entomological Society.
    Insect Molecular Biology 09/2015; DOI:10.1111/imb.12190 · 2.59 Impact Factor
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    • "In insects, their roles are fulfilled by their invertebrate counterparts, octopamine and tyramine (Roeder 2005). The biogenic amine octopamine in insects, and other invertebrates, carries out many of the physiological roles such as aggression (Zhou et al. 2008), locomotion (Koon et al. 2011; Wu et al. 2012), olfactory learning and memory (Farooqui et al. 2003; Schwaerzel et al. 2003; Unoki et al. 2005; Mizunami et al. 2009), ovulation (Monastirioti et al. 1996; Monastirioti 2003), and innate immunity (Adamo 2010; Huang et al. 2012). "
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    ABSTRACT: The octopamine and tyramine, as the invertebrate counterparts of the vertebrate adrenergic transmitters, control and modulate many physiological and behavioral processes. Both molecules mediate their effects by binding to specific receptors belonging to the superfamily of G-protein-coupled receptors. So far, four families of octopamine and tyramine receptors have been reported. Here, we described the functional characterization of one putative octopamine/tyramine receptor gene from the rice stem borer, Chilo suppressalis. By a mechanism of alternative splicing, this receptor gene (CsOA3) encodes two molecularly distinct transcripts, CsOA3S and CsOA3L. CsOA3L differs from CsOA3S on account of the presence of an additional 30 amino acids within the third intracellular loop. When heterologously expressed, both receptors cause increases of intracellular Ca(2+) concentration. The short form, CsOA3S, was activated by both octopamine and tyramine, resulting in decreased intracellular cAMP levels ([cAMP]i ) in a dose-dependent manner, whereas dopamine and serotonin are not effective. However, CsOA3L did not show any impact on [cAMP]i . Studies with series of agonists and antagonists confirmed that CsOA3 has a different pharmacological profile from that of other octopamine receptor families. The CsOA3 is, to our knowledge, a novel family of insect octopamine receptors. Octopamine, the invertebrate counterpart of noradrenaline, modulates many physiological processes. Four families of octopamine/tyramine receptors have been reported. We found that a novel family of octopamine receptors, which encodes two transcripts by alternative splicing, couple with different second messenger pathways. It implicated that one octopamine receptor gene could play different functional roles by alternative splicing.
    Journal of Neurochemistry 11/2013; 129(1). DOI:10.1111/jnc.12526 · 4.28 Impact Factor
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    • "Intriguingly, it was recently discovered that these insulin-producing cells also produce the Drosophila homolog of cholecystokinin (CCK), known as Drosulfakinin (Dsk) (Söderberg et al. 2012), and in rodents levels of the satiation hormone CCK are correlated with aggression (Zwanzger et al. 2012). Furthermore, it has been reported that in Drosophila both octopamine and Dsk are involved in regulating muscle contractions necessary for the control of locomotory behavior (Koon et al. 2011; Chen and Ganetzky 2012; Chen et al. 2012), although it is not known if they interact. From these previous studies, we hypothesized that octopamine signaling could be modulating aggressiveness by regulating the expression of Dsk. "
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    ABSTRACT: In Drosophila the monoamine octopamine, through mechanisms that are not completely resolved, regulates both aggression and mating behavior. Interestingly, our study demonstrates that the Drosophila obesity-linked homologues Transcription factor AP-2 (TfAP-2, TFAP2B in humans) and Tiwaz (Twz, KCTD15 in humans) interact to modify male behavior by controlling the expression of Tyramine β-hydroxylase (Tbh) and Vesicular monanime transporter (Vmat), genes necessary for octopamine production and secretion. Furthermore, we reveal that octopamine in turn regulates aggression through the Drosophila cholecystokinin (CCK) satiation hormone homologue Drosulfakinin (Dsk). Finally, we establish that TfAP-2 is expressed in octopaminergic neurons known to control aggressive behaviour and that TfAP-2 requires functional Twz for its activity. We conclude that genetically manipulating the obesity-linked homologues TfAP-2 and Twz is sufficient to affect octopamine signalling, which in turn modulates Drosophila male behavior through the regulation of the satiation hormone Dsk.
    Genetics 10/2013; 196(1). DOI:10.1534/genetics.113.158402 · 5.96 Impact Factor
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