Multiple nicotinic acetylcholine receptor genes are expressed in goldfish retina and tectum

cDNAs encoding a novel nAChR structural subunit (GFn alpha-3) and a ligand-binding subunit (GF alpha-3) have been isolated from a goldfish retina cDNA library. The protein encoded by GFn alpha-3 shares 88% amino acid similarity with that encoded by GFn alpha-2, a structural subunit gene previously identified to be expressed in this system (Cauley et al., 1989). The ligand-binding subunit (GF alpha-3) is likely the goldfish homolog of the rat alpha-3 gene (Boulter et al., 1986). Northern blots and S1 protection experiments show that GFn alpha- 3 and GF alpha-3 genes are expressed in retina and brain. GFn alpha-3 identifies multiple RNAs differing in their 3′ untranslated regions. In situ hybridization analysis demonstrates GFn alpha-3, GFn alpha-2, and GF alpha-3 expression by cells of the retinal ganglion cell layer. Unlike GFn alpha-2 and GF alpha-3, GFn alpha-3 is expressed at highest levels by cells of the retina's inner nuclear layer. In the optic tectum, both GF alpha-3 and GFn alpha-3 genes are expressed by cells of the periventricular zone, as well as more superficial layers. These results suggest the presence of multiple nAChR systems in retina and tectum. In addition, they indicate that tectal nAChRs may arise from remote (ganglion cell) as well as local (tectal cell) synthesis.

[1]  H. Betz.  Characterization of the ol - bungarotoxin recep - tor in chick embryo retina , 2005 .

[2]  L. Swanson,et al.  Beta 3: a new member of nicotinic acetylcholine receptor gene family is expressed in brain. , 1989, The Journal of biological chemistry.

[3]  K. Isenberg,et al.  Cloning of a Putative Neuronal Nicotinic Acetylcholine Receptor Subunit , 1989, Journal of neurochemistry.

[4]  B. Agranoff,et al.  Identification of a novel nicotinic acetylcholine receptor structural subunit expressed in goldfish retina , 1989, The Journal of cell biology.

[5]  M. Kozak.  The scanning model for translation: an update , 1989, The Journal of cell biology.

[6]  J. Lindstrom,et al.  Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  B. Sakmann,et al.  Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance , 1988, Nature.

[8]  H. Karten,et al.  Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptors , 1988, Visual Neuroscience.

[9]  J P Changeux,et al.  Detection of the nicotinic acetylcholine receptor alpha‐subunit mRNA by in situ hybridization at neuromuscular junctions of 15‐day‐old chick striated muscles. , 1988, The EMBO journal.

[10]  P. Nef,et al.  Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. , 1988, The EMBO journal.

[11]  L. Swanson,et al.  Primary structure and expression of β2: A novel subunit of neuronal nicotinic acetylcholine receptors , 1988, Neuron.

[12]  D. Puro.  The Retina. An Approachable Part of the Brain , 1988 .

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

[14]  J. Henley,et al.  Two distinct (-)nicotine binding sites in goldfish brain. Identification and characterization of putative neuronal nicotinic acetylcholine receptor subtypes. , 1987, The Journal of biological chemistry.

[15]  T. Millar,et al.  Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells , 1987, Neuroscience Letters.

[16]  R. B. Langdon,et al.  Pharmacology of retinotectal transmission in the goldfish: effects of nicotinic ligands, strychnine, and kynurenic acid , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. B. Langdon,et al.  Antagonists of glutaminergic neurotransmission block retinotectal transmission in goldfish , 1986, Brain Research.

[18]  E. Gundelfinger,et al.  Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila , 1986, The EMBO journal.

[19]  J. Henley,et al.  Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. , 1986, Science.

[20]  A. Karlin,et al.  Acetylcholine receptor binding site contains a disulfide cross-link between adjacent half-cystinyl residues. , 1986, The Journal of biological chemistry.

[21]  D. A. Godfrey,et al.  Effect of enucleation on choline acetyltransferase activity in layers of goldfish optic tectum , 1986, Brain Research.

[22]  W. Stell,et al.  Putative cholinergic interneurons in the optic tectum of goldfish , 1986, Brain Research.

[23]  S. Easter,et al.  Retinal ganglion cells in goldfish: a qualitative classification into four morphological types, and a quantitative study of the development of one of them , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  W. Stell,et al.  Choline acetyltransferase immunoreactivity suggests that ganglion cells in the goldfish retina are not cholinergic , 1986, The Journal of comparative neurology.

[25]  J. Henley,et al.  Interaction of monoclonal antibodies to electroplaque acetylcholine receptors with the α-bungarotoxin binding site of goldfish brain , 1986, Brain Research.

[26]  P. Clarke,et al.  Autoradiographic evidence for nicotine receptors on nigrostriatal and mesolimbic dopaminergic neurons , 1985, Brain Research.

[27]  S. Heinemann,et al.  Isolation of a clone coding for the alpha-subunit of a mouse acetylcholine receptor , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  E. Gruberg,et al.  Nucleus isthmi provides most tectal choline acetyltransferase in the frogRana pipiens , 1985, Brain Research.

[29]  M. Busslinger,et al.  Transcription termination and 3′ processing: the end is in site! , 1985, Cell.

[30]  P. Clarke,et al.  Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-alpha-bungarotoxin , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R. Masland,et al.  The functions of acetylcholine in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[32]  D. Melton,et al.  Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. , 1984, Nucleic acids research.

[33]  R. Angerer,et al.  Detection of mrnas in sea urchin embryos by in situ hybridization using asymmetric RNA probes. , 1984, Developmental biology.

[34]  E. V. Famiglietti,et al.  On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells , 1983, Vision Research.

[35]  L. Butcher,et al.  Cholinergic projections from the basal forebrain to the frontal cortex: a combined fluorescent tracer and immunohistochemical analysis in the rat , 1983, Neuroscience Letters.

[36]  D Perlman,et al.  A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. , 1983, Journal of molecular biology.

[37]  Takashi Miyata,et al.  Primary structure of α-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence , 1982, Nature.

[38]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[39]  M. Ariel,et al.  Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells , 1982, The Journal of physiology.

[40]  J. Dowling,et al.  Inner plexiform circuits in the carp retina: Effects of cholinergic agonists, GABA, and substance P on the ganglion cells , 1982, Brain Research.

[41]  C. Zucker,et al.  Localization of synaptic and nonsynaptic nicotinic‐acetylcholine receptors in the goldfish retina , 1982, The Journal of comparative neurology.

[42]  B. Agranoff,et al.  Histological localization of binding sites of α-bungarotoxin and of antibodies specific to acetylcholine receptor in goldfish optic nerve and tectum , 1980, Brain Research.

[43]  John T. Schmidt,et al.  Electrophysiologic evidence that retinotectal synaptic transmission in the goldfish is nicotinic cholinergic , 1980, Brain Research.

[44]  W. Rutter,et al.  Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. , 1979, Biochemistry.

[45]  R H Masland,et al.  Autoradiographic identification of acetylcholine in the rabbit retina , 1979, The Journal of cell biology.

[46]  M. Kemel,et al.  Regulation of dopamine release by presynaptic nicotinic receptors in rat striatal slices: effect of nicotine in a low concentration. , 1979, Life sciences.

[47]  D. Bok,et al.  Electron microscopic localization of [125I]α-bungarotoxin binding sites in the outer plexiform layer of the goldfish retina , 1979, Journal of neurocytology.

[48]  K. Negishi,et al.  An electrophysiological study on the cholinergic system in the carp retina , 1978, Brain Research.

[49]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[50]  J. Patrick,et al.  Immunological distinction between acetylcholine receptor and the alpha-bungarotoxin-binding component on sympathetic neurons. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[51]  P Berg,et al.  Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. , 1977, Journal of molecular biology.

[52]  S. Yazulla,et al.  Radioautographic localization of125I α-bungarotoxin binding sites in the retinas of goldfish and turtle , 1976, Vision Research.

[53]  R H Masland,et al.  Responses to acetylcholine of ganglion cells in an isolated mammalian retina. , 1976, Journal of neurophysiology.

[54]  R. Masland,et al.  Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. , 1976, Journal of neurophysiology.

[55]  N. Proudfoot,et al.  3′ Non-coding region sequences in eukaryotic messenger RNA , 1976, Nature.

[56]  D. McDougal,et al.  THE DISTRIBUTION OF CHOLINE ACETYLTRANSFERASE ACTIVITY IN VERTEBRATE RETINA 1 , 1976, Journal of neurochemistry.

[57]  D. Fambrough.  Acetylcholine Receptors , 1974, The Journal of general physiology.

[58]  P. Leder,et al.  Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[59]  D. Pollen,et al.  Neurotransmission in central nervous tissue: a study of isolated rabbit retina. , 1969, Journal of neurophysiology.

[60]  C. Francis,et al.  Cholinesterase in the retina , 1953, The Journal of physiology.

[61]  P. Seeburg,et al.  Molecular biology of the GABA-A receptor - the receptor channel super-family , 1987 .

[62]  S. Heinemann,et al.  Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor α-subunit , 1986, Nature.

[63]  Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. , 1986, The EMBO journal.

[64]  R. Dale,et al.  A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. , 1985, Plasmid.

[65]  G von Heijne,et al.  Patterns of amino acids near signal-sequence cleavage sites. , 1983, European journal of biochemistry.

[66]  J P Changeux,et al.  The Acetylcholine Receptor: An Allosteric Membrane Protein , 1982 .

[67]  Changeux Jp,et al.  The acetylcholine receptor: an "allosteric" membrane protein. , 1979, Harvey lectures.

[68]  M. Neal.  CHAPTER 6 – ACETYLCHOLINE AS A RETINAL TRANSMITTER SUBSTANCE , 1976 .

[69]  Christus,et al.  A General Method Applicable to the Search for Similarities in the Amino Acid Sequence of Two Proteins , 2022 .

[70]  Ri-chi,et al.  Purification of Biologically Active Globin Messenger RNA by Chromatography on Oligothymidylic acid-Cellulose , 2022 .