Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye: a comparative study

Skingsley, David R.; Laughlin, Simon B.; Hardie, Roger C.

doi:10.1007/bf01021581

Cited by 42 publications

(27 citation statements)

References 52 publications

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“…Histamine is known as a neurotransmitter in arthropod photoreceptors and histamine-activated chloride conductances, as well as single channels, have been reported in insect laminar neurons. The histamine sensitivity and pharmacology obtained with oocytes expressing HisCl1 and/or HisCl2 were similar to what has been reported for native histamine-activated chloride channels from insect laminar neurons (14,15). We propose that HisCl1 and HisCl2 are the molecular correlates of the histamine-gated chloride channels known to play a role in arthropod phototransduction.…”

Section: Discussionsupporting

confidence: 56%

“…However, the subunit composition of the native channel in laminar neurons is not known. Histamine dose-response curves in Drosophila laminar neurons were characterized by an EC 50 of 24 M (15), and EC 50 s ranging from 16 to 60 were found for four other insect species (14,15). In oocytes, the histamine sensitivity of HisCl2 homomultimers most closely matches that seen in native neurons, suggesting that HisCl2 is the major subunit expressed in these neurons.…”

Section: Discussionmentioning

confidence: 73%

“…The laminar neurons that are postsynaptic to insect photoreceptors respond to light with a rapid, chloride-mediated hyperpolarization that can be mimicked by application of histamine (6). These laminar neurons were isolated from optic lobes of several insect species, and the histamine receptor was characterized as a ligand-gated chloride channel (14,15). We report the first cloning of two histamine-gated ion channel subunits.…”

Section: From the Merck Research Laboratories Merck And Co Inc Rmentioning

confidence: 99%

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Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

Hirschberg

Yuan

et al. 2002

Journal of Biological Chemistry

156

151

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Histamine has been shown to play a role in arthropod vision; it is the major neurotransmitter of arthropod photoreceptors. Histamine-gated chloride channels have been identified in insect optic lobes. We report the first isolation of cDNA clones encoding histamine-gated chloride channel subunits from the fruit fly Drosophila melanogaster. The encoded proteins, HisCl1 and HisCl2, share 60% amino acid identity with each other. The closest structural homologue is the human glycine ␣3 receptor, which shares 45 and 43% amino acid identity respectively. Northern hybridization analysis suggested that hisCl1 and hisCl2 mRNAs are predominantly expressed in the insect eye. Oocytes injected with in vitro transcribed RNA, encoding either HisCl1 or HisCl2, produced substantial chloride currents in response to histamine but not in response to GABA, glycine, and glutamate. The histamine sensitivity was similar to that observed in insect laminar neurons. Histamine-activated currents were not blocked by picrotoxinin, fipronil, strychnine, or the H2 antagonist cimetidine. Co-injection of both hisCl1 and hisCl2 RNAs resulted in expression of a histamine-gated chloride channel with increased sensitivity to histamine, demonstrating coassembly of the subunits. The insecticide ivermectin reversibly activated homomeric HisCl1 channels and, more potently, HisCl1 and HisCl2 heteromeric channels.Histamine has been recognized for several years as the major neurotransmitter of arthropod photoreceptors (1, 2). In Drosophila, immunocytochemistry has shown high levels of histamine in photoreceptors and their synapses (2, 3). Further, histidine decarboxylase activity has been demonstrated in Drosophila photoreceptors, suggesting that histamine is synthesized in these cells (2). Drosophila mutants that are deficient in the hdc gene coding for histamine decarboxylase have been identified (4), and flies homozygous for the null mutation appear to be blind (5). Although light-dependent release of histamine from photoreceptors has not yet been demonstrated, exposure of the fly postsynaptic neuron to histamine mimics the effects of light (6).Phototransduction of invertebrates has been most extensively studied in insects, but histamine has been implicated as a neurotransmitter in photoreceptors of several other invertebrate species including barnacles and the horseshoe crab Limulus (7,8), whereas glycine and GABA 1 function as the inhibitory neurotransmitters in vertebrate phototransduction (9). Outside of phototransduction, histamine also appears to be the neurotransmitter in some mechanosensory neurons in Drosophila (10) and in lobster stomatogastric, cardiac, and olfactory neurons (11-13). To date, the molecular nature of the histamine receptor in these neurons is unknown. The laminar neurons that are postsynaptic to insect photoreceptors respond to light with a rapid, chloride-mediated hyperpolarization that can be mimicked by application of histamine (6). These laminar neurons were isolated from optic lobes of several insect species, and the hista...

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Section: Discussionsupporting

confidence: 56%

Section: Discussionmentioning

confidence: 73%

Section: From the Merck Research Laboratories Merck And Co Inc Rmentioning

confidence: 99%

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Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

Hirschberg

Yuan

et al. 2002

Journal of Biological Chemistry

156

151

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“…To rapidly characterize the conductance, its dose response function was measured using a 10-channel, rapid perfusion system, which allowed sequential application of six different histamine concentrations ([Ha]) separated by bath washes (see "Experimental Procedures") (23). The data were fitted to the Hill equation,…”

Section: Ort (Hcla)-encoded Histamine Receptor Subunitmentioning

confidence: 99%

“…The histamine-activated chloride conductance can be readily detected in wild-type fruit flies by whole-cell patch clamp recordings from the cell bodies of freshly dissociated laminar neurons, L1/L2 (2,23). To rapidly characterize the conductance, its dose response function was measured using a 10-channel, rapid perfusion system, which allowed sequential application of six different histamine concentrations ([Ha]) separated by bath washes (see "Experimental Procedures") (23).…”

Section: Ort (Hcla)-encoded Histamine Receptor Subunitmentioning

confidence: 99%

The Target of Drosophila Photoreceptor Synaptic Transmission Is a Histamine-gated Chloride Channel Encoded byort (hclA)

Gengs¹,

Leung²,

Skingsley³

et al. 2002

Journal of Biological Chemistry

116

133

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By screening Drosophila mutants that are potentially defective in synaptic transmission between photoreceptors and their target laminar neurons, L1/L2, (lack of electroretinogram on/off transients), we identified ort as a candidate gene encoding a histamine receptor subunit on L1/L2. We provide evidence that the ort gene corresponds to CG7411 (referred to as hclA), identified in the Drosophila genome data base, by P-element-mediated germ line rescue of the ort phenotype using cloned hclA cDNA and by showing that several ort mutants exhibit alterations in hclA regulatory or coding sequences and/or allele-dependent reductions in hclA transcript levels. Other workers have shown that hclA, when expressed in Xenopus oocytes, forms histamine-sensitive chloride channels. However, the connection between these chloride channels and photoreceptor synaptic transmission was not established. We show unequivocally that hclA-encoded channels are the channels required in photoreceptor synaptic transmission by 1) establishing the identity between hclA and ort and 2) showing that ort mutants are defective in photoreceptor synaptic transmission. Moreover, the present work shows that this function of the HCLA (ORT) protein is its native function in vivo.

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Histamine in the brain of insects: a review

Nässel

1999

Microsc. Res. Tech.

124

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Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye: a comparative study

Cited by 42 publications

References 52 publications

Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

The Target of Drosophila Photoreceptor Synaptic Transmission Is a Histamine-gated Chloride Channel Encoded byort (hclA)

Histamine in the brain of insects: a review

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