Temperature, oxygen, and salt-sensing neurons in C. elegans are carbon dioxide sensors that control avoidance behavior

Neuron

Volumn 69, Issue 6, 2011, Pages 1099-1113

  Bretscher, Andrew Jonathan ^a   Kodama Namba, Eiji ^a   Busch, Karl Emanuel ^a   Murphy, Robin Joseph ^a   Soltesz, Zoltan ^a   Laurent, Patrick ^a   de Bono, Mario ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CARBON DIOXIDE; CYCLIC AMP; GUANYLATE CYCLASE; ION CHANNEL; OXYGEN; SODIUM CHLORIDE;

ANIMAL CELL; ARTICLE; AVOIDANCE BEHAVIOR; BODY FLUID; BODY TEMPERATURE; CAENORHABDITIS ELEGANS; CHANNEL GATING; CONTROLLED STUDY; GAS EXCHANGE; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; THERMORECEPTOR;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CALCIUM; CARBON DIOXIDE; HOMEOSTASIS; ION CHANNEL GATING; MOTOR ACTIVITY; OXYGEN; SENSORY RECEPTOR CELLS; SODIUM CHLORIDE;

EID: 79952763288     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.02.023     Document Type: Article

References (68)

1. Bargmann C.I., Horvitz H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 1991, 7:729-742.
2. Boon E.M., Marletta M.A. Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins. Curr. Opin. Chem. Biol. 2005, 9:441-446.
3. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
4. Bretscher A.J., Busch K.E., de Bono M. A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2008, 105:8044-8049.
5. Buchanan G.F., Richerson G.B. Central serotonin neurons are required for arousal to CO2. Proc. Natl. Acad. Sci. USA 2010, 107:16354-16359.
6. Buckler K.J., Williams B.A., Honore E. An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J. Physiol. 2000, 525:135-142.
7. Bustami H.P., Harrison J.F., Hustert R. Evidence for oxygen and carbon dioxide receptors in insect CNS influencing ventilation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 133:595-604.
8. Cammer W.B., Brion L.P. Carbonic anhydrase in the nervous system. EXS 2000, 90:475-489.
9. Chandrashekar J., Yarmolinsky D., von Buchholtz L., Oka Y., Sly W., Ryba N.J., Zuker C.S. The taste of carbonation. Science 2009, 326:443-445.
10. Clark D.A., Biron D., Sengupta P., Samuel A.D. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J. Neurosci. 2006, 26:7444-7451.
11. Clark D.A., Gabel C.V., Gabel H., Samuel A.D. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J. Neurosci. 2007, 27:6083-6090.
12. Coates E.L., Wells C.M., Smith R.P. Identification of carbonic anhydrase activity in bullfrog olfactory receptor neurons: histochemical localization and role in CO2 chemoreception. J. Comp. Physiol. A 1998, 182:163-174.
13. Coates J.C., de Bono M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 2002, 419:925-929.
14. Coburn C.M., Bargmann C.I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 1996, 17:695-706.
15. Colosimo M.E., Brown A., Mukhopadhyay S., Gabel C., Lanjuin A.E., Samuel A.D., Sengupta P. Identification of thermosensory and olfactory neuron-specific genes via expression profiling of single neuron types. Curr. Biol. 2004, 14:2245-2251.
16. Conradt B., Horvitz H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 1998, 93:519-529.
17. de Bono M., Bargmann C.I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 1998, 94:679-689.
18. Dusenbery D.B., Sheridan R.E., Russell R.L. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics 1975, 80:297-309.
19. Fasseas M.K., Tsikou D., Flemetakis E., Katinakis P. Molecular and biochemical analysis of the beta class carbonic anhydrases in Caenorhabditis elegans. Mol. Biol. Rep. 2010, 37:2941-2950.
20. Faucher C., Forstreuter M., Hilker M., de Bruyne M. Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J. Exp. Biol. 2006, 209:2739-2748.
21. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 2003, 26:239-266.
22. Fischler W., Kong P., Marella S., Scott K. The detection of carbonation by the Drosophila gustatory system. Nature 2007, 448:1054-1057.
23. Gray J.M., Karow D.S., Lu H., Chang A.J., Chang J.S., Ellis R.E., Marletta M.A., Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 2004, 430:317-322.
24. Hallem E.A., Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2008, 105:8038-8043.
25. Hedgecock E.M., Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1975, 72:4061-4065.
26. Hetz S.K., Bradley T.J. Insects breathe discontinuously to avoid oxygen toxicity. Nature 2005, 433:516-519.
27. Hilliard M.A., Apicella A.J., Kerr R., Suzuki H., Bazzicalupo P., Schafer W.R. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J. 2005, 24:63-72.
28. Hobert O., Johnston R.J.J., Chang S. Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat. Rev. Neurosci. 2002, 3:629-640.
29. Hu J., Zhong C., Ding C., Chi Q., Walz A., Mombaerts P., Matsunami H., Luo M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 2007, 317:953-957.
30. Inada H., Ito H., Satterlee J., Sengupta P., Matsumoto K., Mori I. Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 2006, 172:2239-2252.
31. Jiang C., Rojas A., Wang R., Wang X. CO2 central chemosensitivity: why are there so many sensing molecules?. Respir. Physiol. Neurobiol. 2005, 145:115-126.
32. Jones W.D., Cayirlioglu P., Kadow I.G., Vosshall L.B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 2007, 445:86-90.
33. Kerr R.A., Schafer W.R. Intracellular Ca2+ imaging in C. elegans. Methods Mol. Biol. 2006, 351:253-264.
34. Kimura K.D., Miyawaki A., Matsumoto K., Mori I. The C. elegans thermosensory neuron AFD responds to warming. Curr. Biol. 2004, 14:1291-1295.
35. Kindt K.S., Quast K.B., Giles A.C., De S., Hendrey D., Nicastro I., Rankin C.H., Schafer W.R. Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 2007, 55:662-676.
36. Komatsu H., Mori I., Rhee J.S., Akaike N., Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 1996, 17:707-718.
37. Kwon J.Y., Dahanukar A., Weiss L.A., Carlson J.R. The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. USA 2007, 104:3574-3578.
38. Lahiri S., Forster R.E. CO2/H+ sensing: peripheral and central chemoreception. Int. J. Biochem. Cell Biol. 2003, 35:1413-1435.
39. Lehmann F.O., Heymann N. Unconventional mechanisms control cyclic respiratory gas release in flying Drosophila. J. Exp. Biol. 2005, 208:3645-3654.
40. L'Etoile N.D., Coburn C.M., Eastham J., Kistler A., Gallegos G., Bargmann C.I. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 2002, 36:1079-1089.
41. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
42. Ortiz C.O., Etchberger J.F., Posy S.L., Frokjaer-Jensen C., Lockery S., Honig B., Hobert O. Searching for neuronal left/right asymmetry: genomewide analysis of nematode receptor-type guanylyl cyclases. Genetics 2006, 173:131-149.
43. Ortiz C.O., Faumont S., Takayama J., Ahmed H.K., Goldsmith A.D., Pocock R., McCormick K.E., Kunimoto H., Iino Y., Lockery S., Hobert O. Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases. Curr. Biol. 2009, 19:996-1004.
44. Persson A., Gross E., Laurent P., Busch K.E., Bretes H., de Bono M. Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans. Nature 2009, 458:1030-1033.
45. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat. Rev. Neurosci. 2004, 5:449-461.
46. Richerson G.B., Wang W., Hodges M.R., Dohle C.I., Diez-Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp. Physiol. 2005, 90:259-266.
47. Richmond J.E., Davis W.S., Jorgensen E.M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 1999, 2:959-964.
48. Ridderstrale Y., Hanson M. Histochemical study of the distribution of carbonic anhydrase in the cat brain. Acta Physiol. Scand. 1985, 124:557-564.
49. Satterlee J.S., Ryu W.S., Sengupta P. The CMK-1 CaMKI and the TAX-4 cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans. Curr. Biol. 2004, 14:62-68.
50. Satterlee J.S., Sasakura H., Kuhara A., Berkeley M., Mori I., Sengupta P. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 2001, 31:943-956.
51. Sawin E.R., Ranganathan R., Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619-631.
52. Sharabi K., Hurwitz A., Simon A.J., Beitel G.J., Morimoto R.I., Rechavi G., Sznajder J.I., Gruenbaum Y. Elevated CO2 levels affect development, motility, and fertility and extend life span in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2009, 106:4024-4029.
53. Speese S., Petrie M., Schuske K., Ailion M., Ann K., Iwasaki K., Jorgensen E.M., Martin T.F. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J. Neurosci. 2007, 27:6150-6162.
54. Suh G.S., Wong A.M., Hergarden A.C., Wang J.W., Simon A.F., Benzer S., Axel R., Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behavior in Drosophila. Nature 2004, 431:854-859.
55. Suh G.S., Ben-Tabou de Leon S., Tanimoto H., Fiala A., Benzer S., Anderson D.J. Light activation of an innate olfactory avoidance response in Drosophila. Curr. Biol. 2007, 17:905-908.
56. Sun L., Wang H., Hu J., Han J., Matsunami H., Luo M. Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate. Proc. Natl. Acad. Sci. USA 2009, 106:2041-2046.
57. Suzuki H., Thiele T.R., Faumont S., Ezcurra M., Lockery S.R., Schafer W.R. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 2008, 454:114-117.
58. Syrjänen L., Tolvanen M., Hilvo M., Olatubosun A., Innocenti A., Scozzafava A., Leppiniemi J., Niederhauser B., Hytonen V.P., Gorr T.A., et al. Characterization of the first beta-class carbonic anhydrase from an arthropod (Drosophila melanogaster) and phylogenetic analysis of beta-class carbonic anhydrases in invertebrates. BMC Biochem. 2010, 11:28.
59. Turner S.L., Ray A. Modification of CO2 avoidance behavior in Drosophila by inhibitory odorants. Nature 2009, 461:277-281.
60. Vosshall L.B., Stocker R.F. Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 2007, 30:505-533.
61. Wang W., Bradley S.R., Richerson G.B. Quantification of the response of rat medullary raphe neurones to independent changes in pHo and pCO2. J. Physiol. 2002, 540:951-970.
62. Ward S., Thomson N., White J.G., Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 1975, 160:313-337.
63. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1986, 314:1-340.
64. Williams R.H., Jensen L.T., Verkhratsky A., Fugger L., Burdakov D. Control of hypothalamic orexin neurons by acid and CO2. Proc. Natl. Acad. Sci. USA 2007, 104:10685-10690.
65. Young J.M., Waters H., Dong C., Fulle H.J., Liman E.R. Degeneration of the olfactory guanylyl cyclase D gene during primate evolution. PLoS ONE 2007, 2:e884.
66. Yu S., Avery L., Baude E., Garbers D.L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl. Acad. Sci. USA 1997, 94:3384-3387.
67. Ziemann A.E., Allen J.E., Dahdaleh N.S., Drebot I.I., Coryell M.W., Wunsch A.M., Lynch C.M., Faraci F.M., Howard M.A.R., Welsh M.J., Wemmie J.A. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 2009, 139:1012-1021.
68. Zimmer M., Gray J.M., Pokala N., Chang A.J., Karow D.S., Marletta M.A., Hudson M.L., Morton D.B., Chronis N., Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 2009, 61:865-879.