Evidence for a possible neurotransmitter/neuromodulator role of tyramine on the locust oviducts

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Abstract

Visualization of the tyraminergic innervation of the oviducts was demonstrated by immunohistochemistry, and the presence of tyramine was confirmed using high-performance liquid chromatography coupled to electrochemical detection. Oviducts incubated in high-potassium saline released tyramine in a calcium-dependent manner. Stimulation of the oviducal nerves also resulted in tyramine release, suggesting that tyramine might function as a neurotransmitter/neuromodulator at the locust oviducts. Tyramine decreased the basal tension, and also attenuated proctolin-induced contractions in a dose-dependent manner over a range of doses between 10−7 and 10−4 M. Low concentrations of tyramine attenuated forskolin-stimulated cyclic AMP levels in a dose-dependent manner. This effect was not blocked by yohimbine. High concentrations of tyramine increased basal cyclic AMP levels of locust oviducts in a dose-dependent manner; however, the increases in cyclic AMP were only evident at the highest concentrations tested, 5×10−5 and 10−4 M tyramine. The tyramine-induced increase in cyclic AMP shared a similar pharmacological profile with the octopamine-induced increase in cyclic AMP. Tyramine increased the amplitude of excitatory junction potentials at low concentrations while hyperpolarizing the membrane potential by 2–5 mV. A further increase in the amplitude of the excitatory junction potentials and the occurrence of an active response was seen upon washing tyramine from the preparation. These results suggest that tyramine can activate at least three different endogenous receptors on the locust oviducts a putative tyramine receptor at low concentrations, a different tyramine receptor to inhibit muscle contraction, and an octopamine receptor at high concentrations.

Introduction

It earlier has been postulated that tyramine occurs in the nervous system of invertebrates because of its role as a biochemical precursor to the biogenic amine octopamine, a known neurotransmitter, neurohormone and neuromodulator in the invertebrate nervous system (see Roeder, 1999 for a recent review). However, a study characterizing the tyramine and octopamine content in locust tissues has suggested that tyramine may play an independent neuromodulatory role (Downer et al., 1993). This has been supported by the reports of cloned tyramine receptors in Drosophila, Apis, Bombyx and Locusta (Saudou et al., 1990, Vanden Broeck et al., 1995, Blenau et al., 2000, Ohta et al., 2003). These receptors are able to bind and respond to both tyramine and octopamine; however, they are capable of binding to lower doses of tyramine and only bind octopamine at higher doses (Saudou et al., 1990, Vanden Broeck et al., 1995, Von Nickisch-Rosenegk et al., 1996, Poels et al., 2001, Ohta et al., 2003). Pharmacologically, the tyramine receptors are distinct from the known octopamine receptors, in particular for their propensity to preferentially bind yohimbine, as opposed to other aminergic receptor antagonists (Saudou et al., 1990, Arakawa et al., 1990, Vanden Broeck et al., 1995, Poels et al., 2001). A separate study has revealed the presence of independent binding sites for tyramine and octopamine in the locust brain and revealed that the tyramine binding sites have a high affinity for yohimbine relative to the octopamine binding sites (Hiripi et al., 1994). A recently identified putative tyramine receptor from Caenorhabditis elegans is an exception and has a distinct pharmacological profile (Rex and Komuniecki, 2002). This receptor, like the insect tyramine receptors, is negatively coupled to adenylate cyclase; however, it does not preferentially bind yohimbine (Rex and Komuniecki, 2002).

The presence and physiological function of tyramine in the Drosophila Malpighian tubule has been suggested (Blumenthal, 2003). There is evidence for endogenous tyramine acting on a tyramine receptor, resulting in diuresis via an increase in chloride conductance in the tubules (Blumenthal, 2003). It has also been reported that tyramine functions as a neurotransmitter or neuromodulator in the olfactory system of the fruit fly, utilizing the Drosophila tyramine receptor as a mediator (Kutsukake et al., 2000). Tyramine is also implicated as a neuromodulator at neuromuscular junctions in the fruit fly (Nagaya et al., 2002). Tyramine might also act via octopamine receptors. For instance, in the foregut of Schistocerca gregaria, tyramine apparently antagonizes proctolin-induced contractions by activating octopamine receptors (Banner et al., 1990), although there is no evidence that tyramine works via octopamine receptors in vivo.

In various expression systems, the cloned tyramine receptors can negatively couple to adenylate cyclase, attenuating forskolin-induced increases in cyclic AMP levels (Saudou et al., 1990, Arakawa et al., 1990, Vanden Broeck et al., 1995, Blenau et al., 2000, Poels et al., 2001, Rex and Komuniecki, 2002). This differs from the majority of octopamine receptors which traditionally couple positively to adenylate cyclase, causing increases in cyclic AMP (see Roeder, 1999). Furthermore, the Drosophila and Locusta tyramine receptors lead to increases in intracellular calcium levels in various expression systems (Robb et al., 1994, Reale et al., 1997, Poels et al., 2001). This effect of the Drosophila tyramine receptor is sensitive to pertussis toxin (Robb et al., 1994, Reale et al., 1997).

The locust oviducts are a well studied model system with strong evidence that suggests that octopamine functions as a neurotransmitter via adenylate cyclase coupled octopamine-2 receptors to relax the locust oviduct muscle (Orchard and Lange, 1986, Orchard and Lange, 1988). Pharmacologically, the octopamine receptors on the locust oviducts are particularly sensitive to the aminergic receptor antagonists, phentolamine, gramine and metoclopramide, when testing the ability of these agents to antagonise octopamine-induced increases in cyclic AMP (Orchard and Lange, 1986). In contrast, cyproheptadine, phenoxybenzamine, and yohimbine are not very effective, while chlorpromazine is entirely ineffective (Orchard and Lange, 1986).

The present study, therefore, examines the presence and physiological effects of tyramine on the locust oviduct muscle. Physiological assays assessed the effects of tyramine on locust oviduct muscle. Immunohistochemistry and high-performance liquid chromatography coupled to electrochemical detection were used to confirm the presence and release of tyramine at the locust oviducts. Pharmacological agents were also employed to characterize the tyramine-activated receptors. This study lends further evidence for tyramine as a possible neurotransmitter/neuromodulator of an insect visceral muscle.

Section snippets

Animals

Adult female individuals of Locusta migratoria were obtained from a colony at the University of Toronto at Mississauga, Canada, raised on a 12 h light and 12 h dark regime at 30 °C and fed fresh wheat seedlings supplemented with bran. Adult female locusts were chosen because they have large muscular oviducts and the ovaries have undergone maturation.

Chemicals

The pentapeptide proctolin was purchased from Peninsula Laboratories (San Carlos, CA, USA), and was reconstituted in double-distilled water to

Results

Nerve processes containing tyramine-like immunoreactive material are present on the locust oviducts (Fig. 1B). The processes originate from at least two dorsal unpaired median (DUM) neurons in the posterior region of the seventh abdominal ganglion, of which the group of cells as a whole (Fig. 1A) send projections into all four segmental nerves. There are 6–8 tyramine-like immunoreactive DUM neurons in the group and at least two processes are present in each of the oviducal nerves (the nerves

Discussion

Tyramine is present throughout the locust nervous system and it has been suggested that tyramine is a putative neurotransmitter/neuromodulator in the locust (Downer et al., 1993). The locust oviducts contain tyramine and immunohistochemistry reveals that tyramine is localised in nerve processes lying on the oviducts, and appears to be released in a calcium-dependent manner in the presence of high-potassium saline and by electrical stimulation of the oviducal nerves. The restoration of tyramine

Acknowledgements

This work was supported by a Natural Sciences and Engineering Research Council of Canada research grant and post graduate fellowship to A.B. Lange and A. Donini, respectively. Special thanks to Vickie TeBrugge for her expertise with the confocal microscope.

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