Nuclear entry of a cGMP-dependent kinase converts transient into long-lasting olfactory adaptation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 13, 2010, Pages 6016-6021

  Lee, Jin I ^a,e   O'Halloran, Damien M ^a   Eastham Anderson, Jeffery ^a,f   Juang, Bi Tzen ^a   Kaye, Julia A ^a,g   Hamilton, O Scott ^a   Lesch, Bluma ^b   Goga, Andrei ^c   L'Etoile, Noelle D ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Fred Hutchinson Cancer Research Center   (United States)

^f GENENTECH INC   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Integration; Memory; Neuron; Plasticity; Signaling

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE EGL 4; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CHEMOTAXIS; CORRELATION ANALYSIS; EVOLUTIONARY ADAPTATION; LONG TERM EXPOSURE; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; SENSOR; SENSORY NERVE CELL; SMELLING;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION; GENES, HELMINTH; MODELS, NEUROLOGICAL; ODORS; OLFACTORY RECEPTOR NEURONS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SMELL;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 77950530977     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1000866107     Document Type: Article

References (38)

1. Burns ME, Arshavsky VY (2005) Beyond counting photons: Trials and trends in vertebrate visual transduction. Neuron 48:387-401.
2. Fain GL (2006) Why photoreceptors die (and why they don't). Bioessays 28:344-354.
3. Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-527. (Pubitemid 23244617)
4. Colbert HA, Bargmann CI (1995) Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803-812.
5. Hirotsu T, Iino Y (2005) Neural circuit-dependent odor adaptation in C. elegans is regulated by the Ras-MAPK pathway. Genes Cells 10:517-530. (Pubitemid 40867484)
6. Matsuki M, Kunitomo H, Iino Y (2006) Goalpha regulates olfactory adaptation by antagonizing Gqalpha-DAG signaling in Caenorhabditis elegans. Proc Natl Acad Sci USA 103:1112-1117.
7. White JG, Southgate E, Thomson JN, Brenner S (1986) The nervous system of the nematode, Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340.
8. Sengupta P, Chou JH, Bargmann CI (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84:899-909. (Pubitemid 26106859)
9. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-218.
10. Birnby DA, et al. (2000) A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans. Genetics 155:85-104.
11. Coburn CM, Bargmann CI (1996) A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17:695-706.
12. Komatsu H, Mori I, Rhee JS, Akaike N, Ohshima Y (1996) Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17:707-718. (Pubitemid 26365349)
13. L'Etoile ND, Bargmann CI (2000) Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25:575-586.
14. Chalasani SH, et al. (2007) Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450:63-70. (Pubitemid 350070575)
15. Hirotsu T, Saeki S, Yamamoto M, Iino Y (2000) The Ras-MAPK pathway is important for olfaction in Caenorhabditis elegans. Nature 404:289-293. (Pubitemid 30163546)
16. Yamada K, Hirotsu T, Matsuki M, Kunitomo H, Iino Y (2009) GPC-1, a G protein gamma-subunit, regulates olfactory adaptation in Caenorhabditis elegans. Genetics 181:1347-1357.
17. L'Etoile ND, et al. (2002) The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36:1079-1089.
18. Colbert HA, Bargmann CI (1997) Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn Mem 4:179-191.
19. Tsunozaki M, Chalasani SH, Bargmann CI (2008) A behavioral switch: cGMP and PKC signaling in olfactory neurons reverses odor preference in C. elegans. Neuron 59:959-971.
20. Palmitessa A, et al. (2005) Caenorhabditus elegans arrestin regulates neural G protein signaling and olfactory adaptation and recovery. J Biol Chem 280:24649-24662. (Pubitemid 40934554)
21. Miyahara K, Suzuki N, Ishihara T, Tsuchiya E, Katsura I (2004) TBX2/TBX3 transcriptional factor homologue controls olfactory adaptation in Caenorhabditis elegans. J Neurobiol 58:392-402. (Pubitemid 38199126)
22. Ikeda DD, et al. (2008) CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc Natl Acad Sci USA 105:5260-5265.
23. Kaye JA, Rose NC, Goldsworthy B, Goga A, L'Etoile ND (2009) A 3'UTR pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron 61:57-70.
24. O'Halloran DM, Altshuler-Kyelin S, Lee JI, L'Etoile ND (2009) Regulators of AWC-mediated olfactory plasticity in Caeorhabditis elegans. PLoS Genet, 5:1000761 Available at: http://www.plosgenetics.org/article/info%3Adoi%2F10. 1371%2Fjournal.pgen.1000761, Accessed December 5, 2009.
25. Eastham-Anderson JR (2004) Nuclear translocation of EGL-4, a cGMP dependant (i.e. dependent) protein kinase, in response to odorant adaptation in C. elegans. Master's thesis (University of California, Davis, CA).
26. Roayaie K, Crump JG, Sagasti A, Bargmann CI (1998) The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20:55-67. (Pubitemid 28078349)
27. Troemel ER, Sagasti A, Bargmann CI (1999) Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99:387-398.
28. Wes PD, Bargmann CI (2001) C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410:698-701.
29. Reed RB, et al. (1996) Fast and slow cyclic nucleotide-dissociation sites in cAMP-dependent protein kinase are transposed in type Ibeta cGMP-dependent protein kinase. J Biol Chem 271:17570-17575.
30. Stansberry J, et al. (2001) A cGMP-dependent protein kinase is implicated in wild-type motility in C. elegans. J Neurochem 76:1177-1187. (Pubitemid 32167391)
31. Francis SH, Corbin JD (1994) Structure and function of cyclic nucleotide-dependent protein kinases. Annu Rev Physiol 56:237-272. (Pubitemid 24111861)
32. Gudi T, Lohmann SM, Pilz RB (1997) 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 17:5244-5254. (Pubitemid 27357623)
33. Daniels SA, Ailion M, Thomas JH, Sengupta P (2000) 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 156:123-141.
34. Lu YF, Kandel ER, Hawkins RD (1999) Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus. J Neurosci 19:10250-10261.
35. Gudi T, Casteel DE, Vinson C, Boss GR, Pilz RB (2000) NO activation of fos promoter elements requires nuclear translocation of G-kinase I and CREB phosphorylation but is independent of MAP kinase activation. Oncogene 19:6324-6333. (Pubitemid 32641846)
36. Lesch BJ, Gehrke AR, Bulyk ML, Bargmann CI (2009) Transcriptional regulation and stabilization of left-right neuronal identity in C. elegans. Genes Dev 23:345-358.
37. Lans H, Rademakers S, JansenG (2004) A network of stimulatory and inhibitory Galphasubunits regulates olfaction in Caenorhabditis elegans. Genetics 167:1677-1687. (Pubitemid 39265905)
38. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.