Tyramine and octopamine have opposite effects on the locomotion of <i>Drosophila</i> larvae

Saraswati, Sudipta; Fox, Lyle E.; Soll, David R.; Wu, Chun‐Fang

doi:10.1002/neu.10298

Cited by 197 publications

(193 citation statements)

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“…In the Drosophila larva, both TA and OA have been proposed to have opposing effects on locomotion, with OA stimulating and TA possibly inhibiting the CPG (Saraswati et al 2004;Fox et al 2006). We do not detect a decrease (or increase) in locomotion when either dVMAT mutant or WT larvae are fed TA.…”

Section: Discussionmentioning

confidence: 99%

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Chen

Lebestky

et al. 2013

Genetics

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To investigate the regulation of Drosophila melanogaster behavior by biogenic amines, we have exploited the broad requirement of the vesicular monoamine transporter (VMAT) for the vesicular storage and exocytotic release of all monoamine neurotransmitters. We used the Drosophila VMAT (dVMAT) null mutant to globally ablate exocytotic amine release and then restored DVMAT activity in either individual or multiple aminergic systems, using transgenic rescue techniques. We find that larval survival, larval locomotion, and female fertility rely predominantly on octopaminergic circuits with little apparent input from the vesicular release of serotonin or dopamine. In contrast, male courtship and fertility can be rescued by expressing DVMAT in octopaminergic or dopaminergic neurons, suggesting potentially redundant circuits. Rescue of major aspects of adult locomotion and startle behavior required octopamine, but a complementary role was observed for serotonin. Interestingly, adult circadian behavior could not be rescued by expression of DVMAT in a single subtype of aminergic neurons, but required at least two systems, suggesting the possibility of unexpected cooperative interactions. Further experiments using this model will help determine how multiple aminergic systems may contribute to the regulation of other behaviors. Our data also highlight potential differences between behaviors regulated by standard exocytotic release and those regulated by other mechanisms. BOTH invertebrate and mammalian behaviors undergo extensive regulation by monoamine neurotransmitters (reviewed in Joshua et al.

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Section: Discussionmentioning

confidence: 99%

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Chen

Lebestky

et al. 2013

Genetics

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“…Recent studies have demonstrated that tyramine and octopamine have antagonistic effects and suggest that behavioral regulation may depend on the balance of these two hormones (7,32). Thus, T␤M may be expected to function under k cat /K m conditions for all three substrates in vivo, making the enzyme exquisitely sensitive to small shifts in cellular conditions.…”

Section: Discussionmentioning

confidence: 99%

Mechanism of the Insect Enzyme, Tyramine β-Monooxygenase, Reveals Differences from the Mammalian Enzyme, Dopamine β-Monooxygenase

Hess

McGuirl

Klinman

2008

Journal of Biological Chemistry

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Tyramine ␤-monooxygenase (T␤M) catalyzes the synthesis of the neurotransmitter, octopamine, in insects. Kinetic and isotope effect studies have been carried out to determine the kinetic mechanism of T␤M for comparison with the homologous mammalian enzymes, dopamine ␤-monooxygenase and peptidylglycine ␣-hydroxylating monooxygenase. A new and distinctive feature of T␤M is very strong substrate inhibition that is dependent on the level of the co-substrate, O 2 , and reductant as well as substrate deuteration. This has led to a model in which tyramine can bind to either the Cu(I) or Cu(II) forms of T␤M, with substrate inhibition ameliorated at very high ascorbate levels. The rate of ascorbate reduction of the E-Cu(II) form of T␤M is also reduced at high tyramine, leading us to propose the existence of a binding site for ascorbate to this class of enzymes. These findings may be relevant to the control of octopamine production in insect cells.The copper hydroxylases are a unique class of enzymes that are found in eukaryotes and play a critical role in the biosynthesis of neurotransmitters and hormones. The most studied enzymes in this family are peptidylglycine ␣-hydroxylating monooxygenase (PHM) 3 and dopamine ␤-monooxygenase (D␤M) (1). PHM catalyzes the conversion of C-terminal glycine-extended peptides to their ␣-hydroxylated products, the first step in the amidation of peptide hormones, required for a range of biological activities (2). D␤M catalyzes the hydroxylation of dopamine to yield norepinephrine and, thus, is vital for the regulation of these neurotransmitters (3-5). More recently, a third member of this enzyme family was identified, tyramine ␤-monooxygenase (6). T␤M is the insect homolog of D␤M, sharing 39% identity and 55% similarity with the mammalian enzyme. T␤M similarly catalyzes the hydroxylation of tyramine at the ␤-carbon position (Scheme 1). Although tyramine plays no role in mammalian physiology, the product of T␤M, octopamine, has been shown to act as a neurotransmitter in invertebrates, regulating physiological functions such as neuromuscular transmission, behavioral development, and ovulation (7-9). One advantage to studies with T␤M is the much more facile expression system for this enzyme in relation to D␤M (10), which makes it possible to pursue structure/function relationships. In this paper, we report a detailed analysis of the kinetic behavior of the wild type T␤M, an essential first step in understanding this complex enzyme system.All three of the copper hydroxylases employ two noncoupled, mononuclear Cu centers for oxygenase activity, termed Cu M and Cu H . Structural information pertaining to the active site of the enzymes is derived primarily from the crystal structure for PHM and extended X-ray absorption fine structure studies with both D␤M and PHM (11-13). Each copper site assumes a unique coordination environment and a distinct mechanistic function. Cu M serves as the site of dioxygen binding and activation, whereas the Cu H site functions as an electron transfer site in the reac...

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“…TA-and OA-specific neurons, receptors, signaling pathways, and phenotypes have been described in both insects (Saudou et al, 1990) and nematodes . In insects, TA and OA have opposite effects on a variety of behaviors, including locomotion, excitatory junction potentials in muscle strips, and chloride ion conductance across Malpighian tubules in Drosophila (Nagaya et al, 2002;Blumenthal, 2003;Saraswati et al, 2003). In general, insect GPCRs with a preference for TA couple to a decrease in cAMP levels, whereas GPCRs with a preference for OA couple to an elevation in cAMP levels (Roeder, 2005).…”

Section: Figurementioning

confidence: 99%

Tyramine and Octopamine Independently Inhibit Serotonin-Stimulated Aversive Behaviors inCaenorhabditis elegansthrough Two Novel Amine Receptors

Wragg¹,

Hapiak²,

Miller³

et al. 2007

J. Neurosci.

115

146

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Biogenic amines modulate key behaviors in both vertebrates and invertebrates. In Caenorhabditis elegans, tyramine (TA) and octopamine (OA) inhibit aversive responses to 100%, but not dilute (30%) octanol. TA and OA also abolish food-and serotonin-dependent increases in responses to dilute octanol in wild-type but not tyra-3(ok325) and f14d12.6(ok371) null animals, respectively, suggesting that TA and OA modulated responses to dilute octanol are mediated by separate, previously uncharacterized, G-protein-coupled receptors. TA and OA are high-affinity ligands for TYRA-3 and F14D12.6, respectively, based on their pharmacological characterization after heterologous expression. f14d12.6::gfp is expressed in the ASHs, the neurons responsible for sensitivity to dilute octanol, and the sra-6-dependent expression of F14D12.6 in the ASHs is sufficient to rescue OA sensitivity in f14d12.6(ok371) null animals. In contrast, tyra-3::gfp appears not to be expressed in the ASHs, but instead in other neurons, including the dopaminergic CEP/ADEs. However, although dopamine (DA) also inhibits 5-HT-dependent responses to dilute octanol, TA still inhibits in dop-2; dop-1; dop-3 animals that do not respond to DA and cat-2(tm346) and Pdat-1::ICE animals that lack significant dopaminergic signaling, suggesting that DA is not an intermediate in TA inhibition. Finally, responses to TA and OA selectively desensitize after preexposure to the amines. Our data suggest that although tyraminergic and octopaminergic signaling yield identical phenotypes in these olfactory assays, they act independently through distinct receptors to modulate the ASH-mediated locomotory circuit and that C. elegans is a useful model to study the aminergic modulation of sensory-mediated locomotory behaviors.

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Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae

Cited by 197 publications

References 45 publications

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Mechanism of the Insect Enzyme, Tyramine β-Monooxygenase, Reveals Differences from the Mammalian Enzyme, Dopamine β-Monooxygenase

Tyramine and Octopamine Independently Inhibit Serotonin-Stimulated Aversive Behaviors inCaenorhabditis elegansthrough Two Novel Amine Receptors

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