A Tyramine-Gated Chloride Channel Coordinates Distinct Motor Programs of a Caenorhabditis elegans Escape Response

A key feature of escape responses is the fast translation of sensory information into a coordinated motor output. In C. elegans, anterior touch initiates a backward escape response in which lateral head movements are suppressed. Here, we show that tyramine inhibits head movements and forward locomotion through the activation of a tyramine-gated chloride channel, LGC-55. lgc-55 mutant animals have defects in reversal behavior and fail to suppress head oscillations in response to anterior touch. lgc-55 is expressed in neurons and muscle cells that receive direct synaptic inputs from tyraminergic motor neurons. Therefore, tyramine can act as a classical inhibitory neurotransmitter. Activation of LGC-55 by tyramine coordinates the output of two distinct motor programs, locomotion and head movements that are critical for a C. elegans escape response.

[1]  D. Faber,et al.  The Mauthner Cell Half a Century Later: A Neurobiological Model for Decision-Making? , 2005, Neuron.

[2]  M. O'Shea,et al.  Escape flight initiation in the fly , 2007, Journal of Comparative Physiology A.

[3]  M. Dickinson,et al.  Performance trade-offs in the flight initiation of Drosophila , 2008, Journal of Experimental Biology.

[4]  Beth Borowsky,et al.  Trace amines: Identification of a family of mammalian G protein-coupled receptors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[5]  W. N. Green,et al.  The Role of the Cystine Loop in Acetylcholine Receptor Assembly* , 1997, The Journal of Biological Chemistry.

[6]  G. Moulder,et al.  The Caenorhabditis elegans snf-11 gene encodes a sodium-dependent GABA transporter required for clearance of synaptic GABA. , 2006, Molecular biology of the cell.

[7]  E. M. Blumenthal.  Modulation of tyramine signaling by osmolality in an insect secretory epithelium. , 2005, American journal of physiology. Cell physiology.

[8]  J. Hirsh,et al.  Two Functional but Noncomplementing Drosophila Tyrosine Decarboxylase Genes , 2005, Journal of Biological Chemistry.

[9]  T. Utsumi,et al.  B96Bom encodes a Bombyx mori tyramine receptor negatively coupled to adenylate cyclase , 2003, Insect molecular biology.

[10]  L. Avery,et al.  LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. , 2003, Developmental biology.

[11]  Mark J Alkema,et al.  Tyramine Functions Independently of Octopamine in the Caenorhabditis elegans Nervous System , 2005, Neuron.

[12]  M. P. Nusbaum,et al.  A small-systems approach to motor pattern generation , 2002, Nature.

[13]  David H. Hall,et al.  C. elegans Atlas , 2008 .

[14]  R. Wyman,et al.  Motor outputs of giant nerve fiber in Drosophila. , 1980, Journal of neurophysiology.

[15]  M. Labouesse.  [Caenorhabditis elegans]. , 2003, Medecine sciences : M/S.

[16]  E. Borrelli,et al.  Cloning and characterization of a Drosophila tyramine receptor. , 1990, The EMBO journal.

[17]  Cori Bargmann,et al.  Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. , 1999, Genes & development.

[18]  Beibei Zhao,et al.  Reversal Frequency in Caenorhabditis elegans Represents an Integrated Response to the State of the Animal and Its Environment , 2003, The Journal of Neuroscience.

[19]  A. Baumann,et al.  Amtyr1: characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. , 2000, Journal of neurochemistry.

[20]  M. Chalfie,et al.  Green fluorescent protein as a marker for gene expression. , 1994, Science.

[21]  Tyramine excites rat subthalamic neurons in vitro by a dopamine-dependent mechanism , 2007, Neuropharmacology.

[22]  W. Paton.  Central and synaptic transmission in the nervous system; pharmacological aspects. , 1958, Annual review of physiology.

[23]  S. Brenner,et al.  The neural circuit for touch sensitivity in Caenorhabditis elegans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  A. Fire,et al.  Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. , 1993, Genetics.

[25]  N. A. Croll.  Components and patterns in the behaviour of the nematode Caenorhabditis elegans , 2009 .

[26]  H. Horvitz,et al.  The GABAergic nervous system of Caenorhabditis elegans , 1993, Nature.

[27]  Caenorhabditis Elegans Martinchalfieandjohnsulston.  Developmental Genetics of the Mechanosensory Neurons of Caenorhabditis elegans , 2003 .

[28]  Cori Bargmann,et al.  Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans , 2007, Nature Methods.

[29]  Andrew K. Jones,et al.  The cys-loop ligand-gated ion channel gene superfamily of the nematode, Caenorhabditis elegans , 2008, Invertebrate Neuroscience.

[30]  J. Changeux,et al.  Molecular tuning of fast gating in pentameric ligand-gated ion channels. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Patrick W. Hullett,et al.  BMC Genomics BioMed Central Methodology article Rapid single nucleotide polymorphism mapping in C. elegans , 2005 .

[32]  A. V. Maricq,et al.  Action potentials contribute to neuronal signaling in C. elegans , 2008, Nature Neuroscience.

[33]  T. Roeder,et al.  Tyramine and octopamine: antagonistic modulators of behavior and metabolism. , 2003, Archives of insect biochemistry and physiology.

[34]  J. Kaplan,et al.  Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor , 1995, Nature.

[35]  E. Jorgensen,et al.  The Caenorhabditis elegans unc-49 Locus Encodes Multiple Subunits of a Heteromultimeric GABA Receptor , 1999, The Journal of Neuroscience.

[36]  Monica Driscoll,et al.  Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor , 1995, Nature.

[37]  George G. Lunt,et al.  Evolutionary history of the ligand-gated ion-channel superfamily of receptors , 1995, Trends in Neurosciences.

[38]  A. Karlin,et al.  Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins , 1995, Neuron.

[39]  Hong Yang,et al.  Primate Trace Amine Receptor 1 Modulation by the Dopamine Transporter , 2005, Journal of Pharmacology and Experimental Therapeutics.

[40]  D. Coates,et al.  Metabolism and inactivation of neurotransmitters in nematodes , 1996, Parasitology.

[41]  B. Brembs,et al.  Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels , 2007, The Journal of Neuroscience.

[42]  M. J. Allen,et al.  Making an escape: development and function of the Drosophila giant fibre system. , 2006, Seminars in cell & developmental biology.

[43]  M. Monastirioti,et al.  Characterization of Drosophila Tyramine β-HydroxylaseGene and Isolation of Mutant Flies Lacking Octopamine , 1996, The Journal of Neuroscience.

[44]  E. Marder,et al.  Central pattern generators and the control of rhythmic movements , 2001, Current Biology.

[45]  A. V. Maricq,et al.  Electrophysiological analysis of neuronal and muscle function in C. elegans. , 2006, Methods in molecular biology.

[46]  R. Komuniecki,et al.  Characterization of a tyramine receptor from Caenorhabditis elegans , 2002, Journal of Neurochemistry.

[47]  P. Komuniecki,et al.  Tyramine and Octopamine Independently Inhibit Serotonin-Stimulated Aversive Behaviors in Caenorhabditis elegans through Two Novel Amine Receptors , 2007, The Journal of Neuroscience.

[48]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  A. V. Maricq,et al.  Neuronal Control of Locomotion in C. elegans Is Modified by a Dominant Mutation in the GLR-1 Ionotropic Glutamate Receptor , 1999, Neuron.

[50]  W. Gish,et al.  Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map , 2001, Nature Genetics.

[51]  D. H. Edwards,et al.  Metamodulation of the Crayfish Escape Circuit , 2003, Brain, Behavior and Evolution.

[52]  O. Hobert,et al.  A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. , 2001, Development.

[53]  P. A. Getting,et al.  Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit , 1994, Nature.

[54]  R. Thorn,et al.  Carnivorous Mushrooms , 1984, Science.

[55]  Cori Bargmann,et al.  Erratum: Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor (Nature (1995) 378 (78-81)) , 1996 .

[56]  C. Elliott,et al.  Distance and force production during jumping in wild-type and mutant Drosophila melanogaster , 2004, Journal of Experimental Biology.

[57]  Robert J. Hobson,et al.  TYRA‐2 (F01E11.5): a Caenorhabditis elegans tyramine receptor expressed in the MC and NSM pharyngeal neurons , 2005, Journal of neurochemistry.

[58]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[59]  M. M. Alam,et al.  Nematode destroying fungi. , 1990 .

[60]  W. Weber,et al.  Ion currents of Xenopus laevis oocytes: state of the art. , 1999, Biochimica et biophysica acta.

[61]  H. Betz.  Ligand-gated ion channels in the brain: The amino acid receptor superfamily , 1990, Neuron.

[62]  N. Munakata.  [Genetics of Caenorhabditis elegans]. , 1989, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[63]  R. Tsien,et al.  Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein , 2004, Nature Biotechnology.

[64]  Cori Bargmann,et al.  A circuit for navigation in Caenorhabditis elegans , 2005 .

[65]  F. Schweizer,et al.  Synapses , 2022, European Lisp Symposium.

[66]  J. Phillis,et al.  Iontophoretic studies of some trace amines in the mammalian CNS , 1979, Brain Research.

[67]  D. Ish-Horowicz,et al.  MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C . elegans , 2000 .

[68]  J. Bacon,et al.  Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.