Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans

Nature Communications

Volumn 5, Issue , 2014, Pages

  Ohta, Akane ^a   Ujisawa, Tomoyo ^a   Sonoda, Satoru ^a   Kuhara, Atsushi ^a  

^a KONAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; CYSTEINE PROTEINASE; ENDONUCLEASE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANYLATE CYCLASE; HEAT SHOCK TRANSCRIPTION FACTOR 1; INSULIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHODIESTERASE I; PROTEIN KINASE C; SYNAPTOBREVIN; SYNAPTOTAGMIN; TRANSFORMING GROWTH FACTOR BETA; CAENORHABDITIS ELEGANS PROTEIN; PHEROMONE;

BIOCHEMISTRY; COLD TOLERANCE; ENZYME ACTIVITY; HABITUATION; INSULATION; NEMATODE; NEUROLOGY; PHEROMONE; PHYSIOLOGY; PROTEIN;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; COLD; COLD HABITUATION; COLD TOLERANCE; CONTROLLED STUDY; ECTOPIC EXPRESSION; EPISTASIS; GENE EXPRESSION; GENETIC ANALYSIS; HABITUATION; INSULIN RELEASE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY; ADAPTATION; ANIMAL; COLD SHOCK RESPONSE; GENE EXPRESSION REGULATION; GENETICS; INTESTINE; LIGHT; METABOLISM; MUTATION; NERVE CELL; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALIA; CAENORHABDITIS ELEGANS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; COLD TEMPERATURE; COLD-SHOCK RESPONSE; GENE EXPRESSION REGULATION; INSULIN; INTESTINES; LIGHT; MUTATION; NEURONS; PHEROMONES; SIGNAL TRANSDUCTION;

EID: 84925294037     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5412     Document Type: Article

References (46)

1. Murray, P., Hayward, S. A., Govan, G. G., Gracey, A. Y. & Cossins, A. R. An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 104, 5489-5494 (2007).
2. Savory, F. R., Sait, S. M. & Hope, I. A. DAF-16 and Delta9 desaturase genes promote cold tolerance in long-lived Caenorhabditis elegans age-1 mutants. Plos One 6, e24550 (2011).
3. Hall, D. H. & Hedgecock, E. M. Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65, 837-847 (1991).
4. Otsuka, A. J. et al. The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron 6, 113-122 (1991).
5. Mori, I. & Ohshima, Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344-348 (1995).
6. Kuhara, A. et al. Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science 320, 803-807 (2008).
7. Ohta, A. & Kuhara, A. Molecular mechanism for trimeric G protein-coupled thermosensation and synaptic regulation in the temperature response circuit of Caenorhabditis elegans. Neurosci. Res. 76, 119-124 (2013).
8. Kuhara, A., Inada, H., Katsura, I. & Mori, I. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 33, 751-763 (2002).
9. Kuhara, A. & Mori, I. Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. J. Neurosci. 26, 9355-9364 (2006).
10. Haycraft, C. J., Schafer, J. C., Zhang, Q., Taulman, P. D. & Yoder, B. K. Identification of CHE-13, a novel intraflagellar transport protein required for cilia formation. Exp. Cell. Res. 284, 251-263 (2003).
11. Perkins, L. A., Hedgecock, E. M., Thomson, J. N. & Culotti, J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456-487 (1986).
12. Collet, J., Spike, C. A., Lundquist, E. A., Shaw, J. E. & Herman, R. K. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics 148, 187-200 (1998).
13. Deane, J. A., Cole, D. G., Seeley, E. S., Diener, D. R. & Rosenbaum, J. L. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 11, 1586-1590 (2001).
14. 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 17, 707-718 (1996).
15. Liu, J. et al. C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat. Neurosci. 13, 715-722 (2010).
16. Miyawaki, A. et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887 (1997).
17. Kuhara, A., Ohnishi, N., Shimowada, T. & Mori, I. Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans. Nat. Commun. 2, 355 (2011).
18. Larsen, P. L. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 90, 8905-8909 (1993).
19. Vanfleteren, J. R. Oxidative stress and ageing in Caenorhabditis elegans. Biochem. J. 292 Pt 2, 605-608 (1993).
20. Murakami, S. & Johnson, T. E. A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143, 1207-1218 (1996).
21. Barsyte, D., Lovejoy, D. A. & Lithgow, G. J. Longevity and heavy metal resistance in daf-2 and age-1 long-lived mutants of Caenorhabditis elegans. FASEB J. 15, 627-634 (2001).
22. Garsin, D. A. et al. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300, 1921 (2003).
23. Lamitina, S. T. & Strange, K. Transcriptional targets of DAF-16 insulin signaling pathway protect C. elegans from extreme hypertonic stress. American journal of physiology. Cell Physiol. 288, C467-C474 (2005).
24. Cornils, A., Gloeck, M., Chen, Z., Zhang, Y. & Alcedo, J. Specific insulin-like peptides encode sensory information to regulate distinct developmental processes. Development 138, 1183-1193 (2011).
25. Li, W., Kennedy, S. G. & Ruvkun, G. daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev. 17, 844-858 (2003).
26. Kodama, E. et al. Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev. 20, 2955-2960 (2006).
27. Ishihara, T. et al. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109, 639-649 (2002).
28. Kimura, K. D., Tissenbaum, H. A., Liu, Y. & Ruvkun, G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946 (1997).
29. Malone, E. A., Inoue, T. & Thomas, J. H. Genetic analysis of the roles of daf-28 and age-1 in regulating Caenorhabditis elegans dauer formation. Genetics 143, 1193-1205 (1996).
30. Pierce, S. B. et al. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev. 15, 672-686 (2001).
31. Fielenbach, N. & Antebi, A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 22, 2149-2165 (2008).
32. Wolkow, C. A., Kimura, K. D., Lee, M. S. & Ruvkun, G. Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290, 147-150 (2000).
33. Xiao, R. et al. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806-817 (2013).
34. Sugi, T., Nishida, Y. & Mori, I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat. Neurosci. 14, 984-992 (2011).
35. Hirotsu, T., Saeki, S., Yamamoto, M. & Iino, Y. The Ras-MAPK pathway is important for olfaction in Caenorhabditis elegans. Nature 404, 289-293 (2000).
36. Miranda-Vizuete, A. et al. Lifespan decrease in a Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons. FEBS Lett. 580, 484-490 (2006).
37. Tanizawa, Y. et al. Inositol monophosphatase regulates localization of synaptic components and behavior in the mature nervous system of C. elegans. Genes Dev. 20, 3296-3310 (2006).
38. Ohnishi, N., Kuhara, A., Nakamura, F., Okochi, Y. & Mori, I. Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO J. 30, 1376-1388 (2011).
39. Ogura, K., Shirakawa, M., Barnes, T. M., Hekimi, S. & Ohshima, Y. The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes Dev. 11, 1801-1811 (1997).
40. Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970 (1991).
41. Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970 (1991).
42. Fraser, A. G. et al. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330 (2000).
43. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. & Ahringer, J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002 (2001).
44. Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 (1998).
45. Kennedy, S., Wang, D. & Ruvkun, G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427, 645-649 (2004).
46. Henderson, S. T. & Johnson, T. E. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11, 1975-1980 (2001).