Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans

Humans and other animals can sense temperature changes as small as 0.1 °C. How animals achieve such exquisite sensitivity is poorly understood. By recording from the C. elegans thermosensory neurons AFD in vivo, we found that cooling closes and warming opens ion channels. We found that AFD thermosensitivity, which exceeds that of most biological processes by many orders of magnitude, is achieved by nonlinear signal amplification. Mutations in genes encoding subunits of a cyclic guanosine monophosphate (cGMP)-gated ion channel (tax-4 and tax-2) and transmembrane guanylate cyclases (gcy-8, gcy-18 and gcy-23) eliminated both cooling- and warming-activated thermoreceptor currents, indicating that a cGMP-mediated pathway links variations in temperature to changes in ionic currents. The resemblance of C. elegans thermosensation to vertebrate photosensation and the sequence similarity between TAX-4 and TAX-2 and subunits of the rod phototransduction channel raise the possibility that nematode thermosensation and vertebrate vision are linked by conserved evolution.

[1]  J D Hardy,et al.  STUDIES IN TEMPERATURE SENSATION. III. THE SENSITIVITY OF THE BODY TO HEAT AND THE SPATIAL SUMMATION OF THE END ORGAN RESPONSES. , 1937, The Journal of clinical investigation.

[2]  T. Bullock,et al.  Properties of an infra‐red receptor , 1956, The Journal of physiology.

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

[4]  D. Kenshalo,et al.  Spatial summation on the forehead, forearm, and back produced by radiant and conducted heat. , 1967, Journal of comparative and physiological psychology.

[5]  S. Ward,et al.  Electron microscopical reconstruction of the anterior sensory anatomy of the nematode caenorhabditis elegans , 1975, The Journal of comparative neurology.

[6]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[7]  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.

[8]  J. N. Thomson,et al.  Mutant sensory cilia in the nematode Caenorhabditis elegans. , 1986, Developmental biology.

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

[10]  T. Lamb,et al.  Amplification and kinetics of the activation steps in phototransduction. , 1993, Biochimica et biophysica acta.

[11]  Cori Bargmann,et al.  Odorant-selective genes and neurons mediate olfaction in C. elegans , 1993, Cell.

[12]  P. Fisher,et al.  The role of cGMP in photosensory and thermosensory transduction in Dictyostelium discoideum. , 1994, Microbiology.

[13]  I. Mori,et al.  Neural regulation of thermotaxis in Caenorhabditis elegans , 1995, Nature.

[14]  Cori Bargmann,et al.  A Putative Cyclic Nucleotide–Gated Channel Is Required for Sensory Development and Function in C. elegans , 1996, Neuron.

[15]  Ikue Mori,et al.  Mutations in a Cyclic Nucleotide–Gated Channel Lead to Abnormal Thermosensation and Chemosensation in C. elegans , 1996, Neuron.

[16]  V. Torre,et al.  Single-channel properties of ionic channels gated by cyclic nucleotides. , 1997, Biophysical journal.

[17]  E. Stefani,et al.  Fast inactivation of Shaker K+ channels is highly temperature dependent , 1997, Experimental Brain Research.

[18]  S. Lockery,et al.  Active Currents Regulate Sensitivity and Dynamic Range in C. elegans Neurons , 1998, Neuron.

[19]  I. Mori.  Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. , 1999, Annual review of genetics.

[20]  Cori Bargmann,et al.  Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells , 1999, Brain Research.

[21]  Cori Bargmann,et al.  Lateral Signaling Mediated by Axon Contact and Calcium Entry Regulates Asymmetric Odorant Receptor Expression in C. elegans , 1999, Cell.

[22]  R. Orkand,et al.  Temperature coefficient of membrane currents induced by noxious heat in sensory neurones in the rat , 1999, The Journal of physiology.

[23]  Yuji Kohara,et al.  The LIM Homeobox Gene ceh-14 Confers Thermosensory Function to the AFD Neurons in Caenorhabditis elegans , 2000, Neuron.

[24]  S. Lockery,et al.  Pressure polishing: a method for re-shaping patch pipettes during fire polishing , 2000, Journal of Neuroscience Methods.

[25]  B. Hille,et al.  Ionic channels of excitable membranes , 2001 .

[26]  Aravinthan D. T. Samuel,et al.  Thermotaxis in Caenorhabditis elegans Analyzed by Measuring Responses to Defined Thermal Stimuli , 2002, The Journal of Neuroscience.

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

[28]  Beiying Liu,et al.  Thermodynamics of heat activation of single capsaicin ion channels VR1. , 2003, Biophysical journal.

[29]  Aravinthan D. T. Samuel,et al.  Identification of Thermosensory and Olfactory Neuron-Specific Genes via Expression Profiling of Single Neuron Types , 2004, Current Biology.

[30]  A. Patapoutian.  Faculty Opinions recommendation of Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. , 2004 .

[31]  Koutarou D. Kimura,et al.  The C. elegans Thermosensory Neuron AFD Responds to Warming , 2004, Current Biology.

[32]  R. Latorre,et al.  Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Koutarou D. Kimura,et al.  Genetic Control of Temperature Preference in the Nematode Caenorhabditis elegans , 2005, Genetics.

[34]  M. Chalfie,et al.  The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals , 2005, Nature Neuroscience.

[35]  Damon A. Clark,et al.  The AFD Sensory Neurons Encode Multiple Functions Underlying Thermotactic Behavior in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[36]  Damon A. Clark,et al.  Sensorimotor control during isothermal tracking in Caenorhabditis elegans , 2006, Journal of Experimental Biology.

[37]  Aravinthan D. T. Samuel,et al.  The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation , 2006, BMC Neuroscience.

[38]  Hitoshi Inada,et al.  Identification of Guanylyl Cyclases That Function in Thermosensory Neurons of Caenorhabditis elegans , 2006, Genetics.

[39]  Damon A. Clark,et al.  A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans , 2006, Nature Neuroscience.

[40]  A. Patapoutian,et al.  Trp ion channels and temperature sensation. , 2006, Annual review of neuroscience.

[41]  Koutarou D. Kimura,et al.  Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. , 2006, Genes & development.

[42]  Steven J. M. Jones,et al.  The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. , 2007, Genes & development.

[43]  Damon A. Clark,et al.  Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients , 2007, The Journal of Neuroscience.

[44]  J. D. Bronson,et al.  The Function of Guanylate Cyclase 1 and Guanylate Cyclase 2 in Rod and Cone Photoreceptors* , 2007, Journal of Biological Chemistry.

[45]  Aravinthan D. T. Samuel,et al.  Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans , 2007, Journal of Experimental Biology.

[46]  Koutarou D. Kimura,et al.  Temperature Sensing by an Olfactory Neuron in a Circuit Controlling Behavior of C. elegans , 2008, Science.