Hypoxia activates a latent circuit for processing gustatory information in C. elegans

Nature Neuroscience

Volumn 13, Issue 5, 2010, Pages 610-614

  Pocock, Roger ^a   Hobert, Oliver ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1; METABOTROPIC RECEPTOR; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; SEROTONIN; SEROTONIN 7 RECEPTOR;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CHEMOSENSITIVITY; CHEMOTAXIS; CONTROLLED STUDY; FLP 21 GENE; GENE; GENE MUTATION; HYPOXIA; IMMUNOFLUORESCENCE; MOTONEURON; NONHUMAN; NPR 1 GENE; PRIORITY JOURNAL; PROMOTER REGION; SENSORY NERVE CELL; SEROTONIN RELEASE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOXIA; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHEMOTACTIC FACTORS; DISEASE MODELS, ANIMAL; FEEDING BEHAVIOR; FMRFAMIDE; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; MEMBRANE TRANSPORT MODULATORS; MOVEMENT; MUTATION; NERVE NET; NEURONS; PHARYNX; RECEPTORS, NEUROPEPTIDE Y; SEROTONIN; TRANSCRIPTION FACTORS; TRYPTOPHAN HYDROXYLASE; UP-REGULATION;

EID: 77951667748     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2537     Document Type: Article

References (43)

1. Joels, M. & Baram, T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 10, 459-466 (2009).
2. de Kloet, E.R., Joels, M. & Holsboer, F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475 (2005).
3. McEwen, B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904 (2007).
4. Chaouloff, F. Serotonin, stress and corticoids. J. Psychopharmacol. 14, 139-151 (2000).
5. Liang, B. et al. Serotonin targets the DAF-16/FOXO signaling pathway to modulate stress responses. Cell Metab. 4, 429-440 (2006).
6. Zhang, Y., Lu, H. & Bargmann, C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179-184 (2005).
7. Chang, A.J. et al. A distributed chemosensory circuit for oxygen preference in C. elegans. PLoS Biol. 4, e274 (2006).
8. Hukema, R.K., Rademakers, S. & Jansen, G. Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine and glutamate. Learn. Mem. 15, 829-836 (2008).
9. Pocock, R. & Hobert, O. Oxygen levels affect axon guidance and neuronal migration in Caenorhabditis elegans. Nat. Neurosci. 11, 894-900 (2008).
10. Sze, J.Y. et al. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403, 560-564 (2000).
11. Semenza, G.L. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med. 7, 345-350 (2001).
12. Epstein, A.C. et al. C. elegans EGL-9 and mammalian homologs defne a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54 (2001).
13. Bishop, T. et al. Genetic analysis of pathways regulated by the von Hippel-Lindau tumor suppressor in Caenorhabditis elegans. PLoS Biol. 2, e289 (2004).
14. Shen, C. et al. Roles of the HIF-1 hypoxia-inducible factor during hypoxia response in Caenorhabditis elegans. J. Biol. Chem. 280, 20580-20588 (2005).
15. Semenza, G.L. et al. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271, 32529-32537 (1996).
16. Rahman, M.S. & Thomas, P. Molecular cloning, characterization and expression of two tryptophan hydroxylase (TPH-1 and TPH-2) genes in the hypothalamus of Atlantic croaker: down-regulation after chronic exposure to hypoxia. Neuroscience 158, 751-765 (2009).
17. Poncet, L. et al. Activity of tryptophan hydroxylase and content of indolamines in discrete brain regions after a long-term hypoxic exposure in the rat. Brain Res. 765, 122-128 (1997).
18. Bargmann, C.I. & Horvitz, H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729-742 (1991).
19. Uchida, O. et al. The C. elegans che-1 gene encodes a zinc fnger transcription factor required for specifcation of the ASE chemosensory neurons. Development 130, 1215-1224 (2003).
20. Hobson, R.J. et al. SER-7, a Caenorhabditis elegans 5-HT7-like receptor, is essential for the 5-HT stimulation of pharyngeal pumping and egg laying. Genetics 172, 159-169 (2006).
21. Hapiak, V.M. et al. Dual excitatory and inhibitory serotonergic inputs modulate egg laying in Caenorhabditis elegans. Genetics 181, 153-163 (2009).
22. 7-like receptor expressed in the Caenorhabditis elegans M4 pharyngeal motorneuron. J. Neurochem. 87, 22-29 (2003).
23. Ray, P., Schnabel, R. & Okkema, P.G. Behavioral and synaptic defects in C. elegans lacking the NK-2 homeobox gene ceh-28. Dev. Neurobiol. 68, 421-433 (2008).
24. Mehta, R. et al. Proteasomal regulation of the hypoxic response modulates aging in C. elegans. Science 324, 1196-1198 (2009).
25. Avery, L. & Horvitz, H.R. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3, 473-485 (1989).
26. Albertson, D.G. & Thomson, J.N. The pharynx of Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 275, 299-325 (1976).
27. Kim, K. & Li, C. Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. J. Comp. Neurol. 475, 540-550 (2004).
28. Rogers, C. et al. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat. Neurosci. 6, 1178-1185 (2003).
29. Gloria-Soria, A. & Azevedo, R.B. npr-1 regulates foraging and dispersal strategies in Caenorhabditis elegans. Curr. Biol. 18, 1694-1699 (2008).
30. de Bono, M. & Bargmann, C.I. Natural variation in a neuropeptide Y receptor homolog modifes social behavior and food response in C. elegans. Cell 94, 679-689 (1998).
31. Coates, J.C. & de Bono, M. Antagonistic pathways in neurons exposed to body fuid regulate social feeding in Caenorhabditis elegans. Nature 419, 925-929 (2002).
32. Hukema, R.K. et al. Antagonistic sensory cues generate gustatory plasticity in Caenorhabditis elegans. EMBO J. 25, 312-325 (2006).
33. Cheung, B.H. et al. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr. Biol. 15, 905-917 (2005).
34. Pierce-Shimomura, J.T., Morse, T.M. & Lockery, S.R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci. 19, 9557-9569 (1999).
35. Chang, A.J. & Bargmann, C.I. Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105, 7321-7326 (2008).
36. Poncet, L. et al. Alteration in central and peripheral substance P-and neuropeptide Y-like immunoreactivity after chronic hypoxia in the rat. Brain Res. 733, 64-72 (1996).
37. Saraf-Reinach, T.R. et al. The lin-11 LIM homeobox gene specifes olfactory and chemosensory neuron fates in C. elegans. Development 128, 3269-3281 (2001).
38. Sagasti, A. et al. Alternative olfactory neuron fates are specifed by the LIM homeobox gene lim-4. Genes Dev. 13, 1794-1806 (1999).
39. Aspöck, G., Ruvkun, G. & Burglin, T.R. The Caenorhabditis elegans ems class homeobox gene ceh-2 is required for M3 pharynx motoneuron function. Development 130, 3369-3378 (2003).
40. Macosko, E.Z. et al. A hub-and-spoke circuit drives pheromone attraction and social behavior in C. elegans. Nature 458, 1171-1175 (2009).
41. Bargmann, C.I. & Horvitz, H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729-742 (1991).
42. Sze, J.Y. et al. Food and metabolic signaling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403, 560-564 (2000).
43. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71 (1974).