Substrate regulation of serotonin and dopamine synthesis in Drosophila

Coleman, Chandra M.; Neckameyer, Wendi S.

doi:10.1007/s10158-004-0031-y

Cited by 30 publications

(22 citation statements)

References 40 publications

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“…It is not surprising that DTRH tryptophan hydroxylase activity is not inhibited by 5-HT since this is also observed with mammalian Tph2 prepared from rat homogenates (Johansen et al, 1991). The inhibition when assayed with dopamine points to another similarity between DTRH and mammalian tryptophan hydroxylase, and to another difference between the tryptophan hydroxylation of DTRH and that of DTPH, where no inhibition by 5-HT or dopamine is observed (Coleman and Neckameyer, 2004).…”

Section: Discussionmentioning

confidence: 97%

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Serotonin synthesis by two distinct enzymes inDrosophila melanogaster

Coleman

Neckameyer

2005

Arch. Insect Biochem. Physiol.

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Annotation of the sequenced Drosophila genome suggested the presence of an additional enzyme with extensive homology to mammalian tryptophan hydroxylase, which we have termed DTRH. In this work, we show that enzymatic analyses of the putative DTRH enzyme expressed in Escherichia coli confirm that it acts as a tryptophan hydroxylase but can also hydroxylate phenylalanine, in vitro. Building upon the knowledge gained from the work in mice and zebrafish, it is possible to hypothesize that DTRH may be primarily neuronal in function and expression, and DTPH, which has been previously shown to have phenylalanine hydroxylation as its primary role, may be the peripheral tryptophan hydroxylase in Drosophila. The experiments presented in this report also show that DTRH is similar to DTPH in that it exhibits differential hydroxylase activity based on substrate. When DTRH uses tryptophan as a substrate, substrate inhibition, catecholamine inhibition, and decreased tryptophan hydroxylase activity in the presence of serotonin synthesis inhibitors are observed. When DTRH uses phenylalanine as a substrate, end product inhibition, increased phenylalanine hydroxylase activity after phosphorylation by cAMP-dependent protein kinase, and a decrease in phenylalanine hydroxylase activity in the presence of the serotonin synthesis inhibitor, alpha-methyl-(DL)-tryptophan are observed. These experiments suggest that the presence of distinct tryptophan hydroxylase enzymes may be evolutionarily conserved and serve as an ancient mechanism to appropriately regulate the production of serotonin in its target tissues.

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Section: Discussionmentioning

confidence: 97%

“…DTPH exhibits differential hydroxylase activity based solely on substrate (Coleman and Neckameyer, 2004). When DTPH uses phenylalanine as a substrate, regulatory control is observed that is not seen when tryptophan is used as a substrate.…”

Section: May 2005mentioning

confidence: 88%

Serotonin synthesis by two distinct enzymes inDrosophila melanogaster

Coleman

Neckameyer

2005

Arch. Insect Biochem. Physiol.

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“…Behavioral phase state (P-sol) tyrosine synthesis and tryptophan hydroxylase for the synthesis of 5-hydrotryptophan (5-HTP), the precursor of serotonin (17). Except for a small but significant increase in the gregarious head tissue at the fourth stadium, little difference in henna expression was observed between the two phases in investigated tissues or stadia (Fig.…”

Section: Genome-wide Expression Identified the Catecholamine Metabolicmentioning

confidence: 99%

Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway

Guo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

167

249

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The migratory locust, Locusta migratoria, shows a striking phenotypic plasticity. It transitions between solitary and gregarious phases in response to population density changes. However, the molecular mechanism underlying the phase-dependent behavior changes remains elusive. Here we report a genome-wide gene expression profiling of gregarious and solitary nymphs at each stadium of the migratory locust, and we identified the most differentially expressed genes in the fourth stadium of the two phases. Bioinformatics analysis indicated that the catecholamine metabolic pathway was the most significant pathway up-regulated in the gregarious phase. We found pale, henna, and vat1, involved in dopamine biosynthesis and synaptic release, were critical target genes related to behavioral phase changes in the locusts. The roles of these genes in mediating behavioral changes in the gregarious individuals were confirmed by RNAi and pharmacological intervention. A single injection of dopamine or its agonist initiated gregarious behavior. Moreover, continuous and multiple injections of a dopamine agonist coupled with crowding resulted in more pronounced gregarious behavior. Our study thus provides insights into the relationships between genes and behavior in phase transition of this important pest species.microarray | RNA interference | polyphenism P henotypic plasticity associated with locust phase polyphenism arises when extrinsic factors induce alternative phenotypes in individuals with the same genetic background (1). Solitary locusts usually live in an isolated state, with their cryptic body color blending well into the surroundings (2). Population density is a substantial source of extrinsic factors that leads to the reversible transformation between solitary and gregarious phases. Under high population density, migratory locusts (Locusta migratoria) form large, fast-flying swarms that wreak havoc on local vegetation (3, 4). Gregarious locusts have a distinctive orange body color with dark patterns as nymphs. In addition, they are attracted to one another and exhibit collective social behavior (2).Behavior is one of the most obvious traits to examine to evaluate the phase state of the migratory locust (1-6). Although the neuronal circuitry responsible for processing and integrating phase-shifting cues is not clear, several neurochemicals have been implicated (1). For instance, the biogenic amine serotonin was found to be necessary and sufficient for inducing gregarious behavior in the desert locust, Schistocerca gregaria (7).The first step in identifying the mechanisms underlying phenotypic plasticity in locusts is to understand how behavior is regulated. A void in our understanding of the mechanism of the phenomena is the interaction of gene expression and environment in regulating phase change of the migratory locust (1). Because of the inherent complexity associated with phase transition, the full complement of behavioral and physiological changes is underwritten by genetic and epigenetic factors (8,9). In previous st...

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“…Our conclusion thus supports the hypothesis that specific TPH is present in arthropods generally, based on the phylogenetic analysis of the AAAH gene superfamily (Boularand et al 1998;Patton et al 1998). However, whether the PAH in all insects is similar to DTPH (the peripheral TPH in Drosophila) and serves the TPH function (Neckameyer and White 1992;Coleman and Neckameyer 2004) remains unknown. In other words, the question of whether these insects have also compartmentalized the neuronal and peripheral regulation of 5-HT by having two distinct enzymes, each specific for neuronal or peripheral synthesis, is still open.…”

Section: Presence Of Tph In the Brains Of Insectsmentioning

confidence: 99%

Immunohistochemical evidence for the presence of tryptophan hydroxylase in the brains of insects as revealed by sheep anti-tryptophan hydroxylase polyclonal antibody

et al. 2008

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Immediately following the discovery of tryptophan hydroxylase in Drosophila, we demonstrated the presence of tryptophan hydroxylase in the brain of the beetle Harmonia axyridis (Coleoptera: Coccinellidae). However, whether tryptophan hydroxylase is present in the brains of other insects is still a matter of discussion. In the current study, sheep anti-tryptophan hydroxylase polyclonal antibody has been applied to test for tryptophan hydroxylase immunoreactivity in a broader taxonomic range of insect brains, including holometabolous and hemimetabolous insects: one species each of Coleoptera, Hymenoptera, Diptera, and Blattaria, and two species of Lepidoptera. All species show consistent tryptophan hydroxylase immunoreactivity with distribution patterns matching that of serotonin. The immuno-positive results of such an antibody in brains from diverse orders of insects suggest that specific tryptophan hydroxylase responsible for central serotonin synthesis is probably present in the brains of all insects.

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Substrate regulation of serotonin and dopamine synthesis in Drosophila

Cited by 30 publications

References 40 publications

Serotonin synthesis by two distinct enzymes inDrosophila melanogaster

Serotonin synthesis by two distinct enzymes inDrosophila melanogaster

Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway

Immunohistochemical evidence for the presence of tryptophan hydroxylase in the brains of insects as revealed by sheep anti-tryptophan hydroxylase polyclonal antibody

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