Histamine directly gates a chloride channel in lobster olfactory receptor neurons.

Abstract

Biogenic amines mediate many types of intercellular communication in multicellular organisms. Heretofore, little direct evidence has indicated that biogenic amines produce intracellular responses other than by triggering the enzymatic production of second messengers. Our electrophysiological studies of lobster olfactory receptor neurons now reveal that one biogenic amine, histamine, can directly gate an ion channel. The channel responds to histamine concentrations of 1 ,xM or more, is permeable primarily to Cl-, is more active at depolarized potentials, and has a conductance of 44 pS in the American lobster and 66 pS in the Caribbean spiny lobster. The expression of this ligand-gated channel in olfactory receptor neurons implies that these neurons are targets of a regulatory or feedback process.Histamine (HA) is a putative neurotransmitter and important neuroregulatory compound in diverse species (1-4). The intracellular effector mechanisms mediating HA responses investigated to date involve biochemical second messengers (5-9). We recently discovered that application of HA to the somata of spiny lobster olfactory receptor neurons suppresses both spontaneous and odor-evoking spiking in these cells by rapidly activating a Cl-current (10). The rapid time course of this effect, as well as recent evidence that HA mediates fast synaptic transmission in arthropods (11-15) and molluscs (1, 16), raises the possibility that HA can also act by directly gating ion channels. We now provide evidence that lobster olfactory receptor neurons express a chloride channel that is directly gated by HA. Evidence is also provided to support the conclusion that this channel mediates the suppressive action of HA on lobster olfactory receptor neurons. MATERIALS AND METHODSAnimals. Adult specimens of the Caribbean spiny lobster Panulirus argus were collected in the Florida Keys and maintained in flowing seawater at 18°C-23°C. Similar specimens of the American lobster Homarus americanus were purchased from commercial suppliers in Woods Hole, MA, and were maintained in flowing seawater at 13°C-17°C.Patch-Clamp Recording. Olfactory receptor neurons were prepared for patch-clamp recording as described (17, 18). Briefly, olfactory organs were cut into hemicylindrical sections, exposing the clusters of receptor neuron somata. Sections from American lobsters were treated with collagenase (1 mg/ml; Sigma, type 1A) for 60 min followed by trypsin(1 mg/ml in Ca2+-free saline; Sigma, type IX) for another 20 min. Sections from spiny lobsters were treated with Lcysteine-activated papain (0.25 mg/ml; Sigma, type IV) for 20 min and then with trypsin for another 20 min. For whole-cell voltage-clamp recording, somata were isolated by drawing clusters of somata into a fire-polished glass pipette and expelling them into a recording dish, a process that severed the dendrite and any remaining axon from these bipolar neurons. Voltage-clamp and single-channel recording were performed by conventional patch-clamp methods with commercially available electron...

Histamine and Its Receptors Modulate Temperature-Preference Behaviors inDrosophila

“…Immunohistochemical studies indicated the presence of histamine in a variety of neuron types in the brain and optic lobes, as well as in the ganglia of the ventral nerve cord of several insect species (for review, see Nässel, 1999). In arthropods, it was reported that histamine increases chloride conductance (Claiborne and Selverston, 1984;Hardie, 1989;McClintock and Ache, 1989;Gisselmann et al, 2002) and that its receptors are members of the ligand-gated chloride channel family.…”

“…In invertebrates, histamine has various roles in neurotransmission in the brain, such as olfaction in crustaceans and photoreception in various arthropods (Hardie, 1989;McClintock and Ache, 1989;Stuart, 1999), as well as in mechanoreception (Melzig et al, 1996). The histaminergic system in the vertebrate CNS projects its neurites to most regions in the brain and plays a key role in the regulation of basic body functions.…”

Putative histamine‐gated chloride channel subunits of the insect visual system and thoracic ganglion

“…The receptors that transmit the effects of histamine within the visual system are members of the ligand-gated chloride channel family (Hardie 1989;McClintock and Ache 1989). Ligand-gated HA-channels are believed to be peculiar for arthropods, although electrophysiological evidence for the existence of these channels in vertebrates is available (Hatton and Yang 2001).…”

“…As in vertebrates, HA is also a transmitter in invertebrates. Both, olfaction in crustaceans (McClintock and Ache 1989) and mechanoreception in insects (Buchner et al 1993;Melzig et al 1996) are known to depend on histaminergic neurotransmission. Its most important role has HA in the arthropod visual system, where it is the neurotransmitter of all photoreceptor cells (Hardie 1987;Nässel et al 1988).…”

Dynamic representation of odours by oscillating neural assemblies

“…This suggests that the slow temporal patterns are shaped by mechanisms which are independent of the activation of this GABA receptor type. Other mechanisms include: other types of GABA receptors (note that GABAB receptors are not known in insects and that phaclophen, a GABAB receptor antagonist, had no effect on the temporal patterns; MacLeod & Laurent, in preparation); other neurotransmitters -such as histamine (McClintock & Ache, 1989), though cimetidine and pirylamine had effects only at very high concentrations; ionic pumps (though long-lasting hyperpolarizations do not always follow spike bursts; Laurent et al, 1996); nitric oxide (Müller & Buchner, 1993;Gelperin, 1994); temporal patterning of the antennal afferent input; and finally, complex dynamical behaviour of the highly interconnected antennal lobe circuits.…”