A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse

COMPARED with the variety of neuromodulatory agents acting through second messenger systems, the number of fast neurotran-smitters which directly activate ion channels is limited. Thus, synaptic receptors that act as ligand-gated ion channels have been firmly established only for acetylcholine, glycine, GABA and glutamate, with the first three of these belonging to the same molecular superfamily1. Recently, however, a possible addition to this list has been suggested as a result of evidence implicating histamine as the neurotransmitter released by a variety of arthropod photoreceptors2–7. Neurotransmission at this synapse has been studied extensively, particularly in the fly8–12. The post-synaptic elements, large monopolar cells, respond to light with a rapid, chloride-mediated hyperpolarization8,13,14 that can be mimicked by the application of histamine3. In this report I document some basic properties of the histamine receptors present on large monopolar cells isolated from blowfly optic lobes. The receptor is a ligand-gated chloride channel showing properties consistent with its presumed role of mediating neurotransmission at the photoreceptor synapse.

[1]  S B Laughlin,et al.  Synaptic limitations to contrast coding in the retina of the blowfly Calliphora , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  E Neher,et al.  A patch‐clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. , 1982, The Journal of physiology.

[3]  S. Shaw Early visual processing in insects. , 1984, The Journal of experimental biology.

[4]  Alan G. Hawkes,et al.  The Principles of the Stochastic Interpretation of Ion-Channel Mechanisms , 1983 .

[5]  Simon B. Laughlin,et al.  Form and function in retinal processing , 1987, Trends in Neurosciences.

[6]  Boschek Cb On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. , 1971 .

[7]  I A Meinertzhagen,et al.  An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly , 1982, The Journal of comparative neurology.

[8]  E. Neher,et al.  Single acetylcholine-activated channels show burst-kinetics in presence of desensitizing concentrations of agonist , 1980, Nature.

[9]  Hans Straka,et al.  Synaptic Chloride Channels Generating Hyperpolarizing On-Responses in Monopolar Neurones of the Blowfly Visual System , 1987 .

[10]  K L Magleby,et al.  The effect of voltage on the time course of end‐plate currents , 1972, The Journal of physiology.

[11]  P. Simmons,et al.  Evidence That Histamine is a Neurotransmitter of Photoreceptors in the Locust Ocellus , 1988 .

[12]  D. Sattelle,et al.  Dissociation and maintenance in vitro of neurones from adult cockroach (Periplaneta americana) and housefly (Musca domestica) , 1987, Journal of Neuroscience Methods.

[13]  L. Tuomisto,et al.  Distribution of histamine in the cockroach brain and visual system: An immunocytochemical and biochemical study , 1988, The Journal of comparative neurology.

[14]  P. Evans,et al.  Histamine in the Insect Nervous System: Distribution, Synthesis and Metabolism , 1983, Journal of neurochemistry.

[15]  R. Frizzell Cystic Fibrosis: a disease of ion channels? , 1987, Trends in Neurosciences.

[16]  B Sakmann,et al.  Fast events in single‐channel currents activated by acetylcholine and its analogues at the frog muscle end‐plate. , 1985, The Journal of physiology.

[17]  R. Hardie Effects of Antagonists on Putative Histamine Receptors in the First Visual Neuropile of the Housefly (Musca Domestica) , 1988 .

[18]  P. Seeburg,et al.  Molecular biology of the GABAA receptor: the receptor/channel superfamily , 1987, Trends in Neurosciences.