The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans

Neuron

Volumn 36, Issue 6, 2002, Pages 1079-1089

  L'Etoile, Noelle D ^a,b,c   Coburn, Cara M ^a,d   Eastham, Jeffery ^c   Kistler, Amy ^a   Gallegos, Gloriana ^b,c   Bargmann, Cornelia I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Morrison and Foerster LLP   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR;

ADAPTATION; ARTICLE; BETA CHAIN; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENZYME ACTIVITY; MUTATION; NERVE CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OLFACTORY NERVE; OLFACTORY RECEPTOR; PHOSPHORYLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SMELLING;

EID: 0037137698     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(02)01066-8     Document Type: Article

References (50)

1. Bargmann C.I., Mori I. Chemotaxis and thermotaxis. Riddle D.L., Blumenthal T., Meyer B.J., Priess J.R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 717-737.pp.
2. Bargmann C.I., Hartwieg E., Horvitz H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 74:1993;515-527.
3. Bear M.F., Linden D.J. The mechanisms and meaning of long-term synaptic depression in the mammalian brain. Cowan W.M., Sudhof T.C., Stevens C.F. Synapses. 2001;The Johns Hopkins University Press, Baltimore. 455-517.pp.
4. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics. 155:2000;85-104.
5. Bradley J., Reuter D., Frings S. Facilitation of calmodulin-mediated odor adaptation by cAMP-gated channel subunits. Science. 294:2001;2176-2178.
6. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 77:1974;71-94.
7. Chen T.Y., Yau K.W. Direct modulation by Ca(2+)-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature. 368:1994;545-548.
8. Coburn C.M., Bargmann C.I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 17:1996;695-706.
9. Coburn C.M., Mori I., Oshima Y., Bargmann C.I. A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans. a distinct pathway for maintenance of sensory axon structure Development. 125:1998;249-258.
10. Colbert H.A., Bargmann C.I. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron. 14:1995;803-812.
11. Colbert H.A., Bargmann C.I. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn. Mem. 4:1997;179-191.
12. Dalton P. Psychophysical and behavioral characteristics of olfactory adaptation. Chem. Senses. 25:2000;487-492.
13. Daniels S.A., Ailion M., Thomas J.H., Sengupta P. egl-4 acts through a transforming growth factor-beta/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues. Genetics. 156:2000;123-141.
14. Davare M.A., Avdonin V., Hall D.D., Peden E.M., Burette A., Weinberg R.J., Horne M.C., Hoshi T., Hell J.W. A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. Science. 293:2001;98-101.
15. Fujiwara M., Sengupta P., McIntire S.L. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron. 36:2002;1091-1102. this issue,
16. Gu T., Orita S., Han M. Caenorhabditis elegans SUR-5, a novel but conserved protein negatively regulates LET-60 ras activity during vulva induction. Mol. Cell. Bio. 18:1998;4556-4564.
17. Gudi T., Lohmann S.M., Pilz R.B. Regulation of gene expression by cyclic GMP-dependent protein kinase requires nuclear translocation of the kinase. identification of a nuclear localization signal Mol. Cell. Biol. 17:1997;5244-5254.
18. Huber A., Sander P., Gobert A., Bahner M., Hermann R., Paulsen R. The transient receptor potential protein (Trp), a putative store-operated Ca2+ channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J. 15:1996;7036-7045.
19. 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. 17:1996;707-718.
20. Komatsu H., Jin Y.H., L'Etoile N., Mori I., Bargmann C.I., Akaike N., Ohshima Y. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821:1999;160-168.
21. Kuhara A., Inada H., Katsura I., Mori I. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron. 33:2002;751-763.
22. Kramer R.H., Molokanova E. Modulation of cyclic-nucleotide-gated channels and regulation of vertebrate phototransduction. J. Exp. Biol. 204:2001;2921-2931.
23. L'Etoile N.D., Bargmann C.I. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron. 25:2000;575-586.
24. Mello C., Fire A. DNA transformation. Methods Cell Biol. 48:1995;451-482.
25. Munger S.D., Lane A.P., Zhong H., Leinders-Zufall T., Yau K.W., Zufall F., Reed R.R. Central role of the CNGA4 channel subunit in Ca2+-calmodulin-dependent odor adaptation. Science. 294:2001;2172-2175.
26. Osborne K.A., Robichon A., Burgess E., Butland S., Shaw R.A., Coulthard A., Pereira H.S., Greenspan R.J., Sokolowski M.B. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science. 277:1997;834-836.
27. Peckol E.L., Troemel E.R., Bargmann C.I. Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 98:2001;11032-11038.
28. Pierce-Shimomura J.T., Morse T.M., Lockery S.R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci. 19:1999;9557-9569.
29. Pugh E.N. Jr., Nikonov S., Lamb T.D. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr. Opin. Neurobiol. 9:1999;410-418.
30. Riddle D.L., Albert P.S. Genetic and environmental regulation of dauer larva development. Riddle D.L., Blumenthal T., Meyer B.J., Priess J.R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 739-768.pp.
31. Roayaie K., Crump J.G., Sagasti A., Bargmann C.I. The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron. 20:1998;55-67.
32. Robertson H.M. Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. Genome Res. 8:1998;449-463.
33. Robertson H.M. The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. Genome Res. 10:2000;192-203.
34. Saeki S., Yamamoto M., Iino Y. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J. Exp. Biol. 204:2001;1757-1764.
35. Schackwitz W.S., Inoue T., Thomas J.H. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron. 17:1996;719-728.
36. Sengupta P., Chou J.H., Bargmann C.I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 84:1996;899-909.
37. Stansberry J., Baude E.J., Taylor M.K., Chen P.J., Jin S.W., Ellis R.E., Uhler M.D. A cGMP-dependent protein kinase is implicated in wild-type motility in C. elegans. J. Neurochem. 76:2001;1177-1187.
38. Stringham E.G., Dixon D.K., Jones D., Candido E.P. Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell. 3:1992;221-233.
39. Sulston, J., and Hodgkin, J. (1988). Methods. The nematode Caenorhabditis elegans. W.B. Wood and the community of C. elegans researchers, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press) pp. 587-606.
40. Trent C., Tsuing N., Horvitz H.R. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics. 104:1983;619-647.
41. Troemel, E.R. (1999). Chemosensory Receptors in Caenorhabditis elegans. Ph.D. thesis, the University of California, San Francisco, San Francisco, California.
42. Troemel E.R., Chou J.H., Dwyer N.D., Colbert H.A., Bargmann C.I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 83:1995;207-218.
43. Tsunoda S., Sierralta J., Sun Y., Bodner R., Suzuki E., Becker A., Socolich M., Zuker C.S. A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature. 388:1997;243-249.
44. Wes P.D., Bargmann C.I. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature. 410:2001;698-701.
45. White J.G., Southgate E., Thomson J.N., Brenner F.R.S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314:1986;1-340.
46. Wingrove J.A., O'Farrell P.H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell. 98:1999;105-114.
47. 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. 94:1997;3384-3387.
48. Zheng J., Knighton D.R., ten Eyck L.F., Karlsson R., Xuong N., Taylor S.S., Sowadski J.M. Crystal structure of the catalytic subunit of camp-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry. 32:1993;2154-2161.
49. Zufall F., Leinders-Zufall T. Identification of a long-lasting form of odor adaptation that depends on the carbon monoxide/cGMP second-messenger system. J. Neurosci. 17:1997;2703-2712.
50. Zufall F., Leinders-Zufall T. The cellular and molecular basis of odor adaptation. Chem. Senses. 25:2000;473-481.