A Behavioral Switch: cGMP and PKC Signaling in Olfactory Neurons Reverses Odor Preference in C. elegans

Tsunozaki, Makoto; Chalasani, Sreekanth H.; Bargmann, Cornelia I.

doi:10.1016/j.neuron.2008.07.038

Cited by 133 publications

(201 citation statements)

References 65 publications

(98 reference statements)

Supporting

Mentioning

190

Contrasting

Order By: Relevance

“…8). It has also been reported that a single olfactory neuron can switch from attraction to repulsion towards lower concentrations of an attractive odorant 32 . Hence, a mechanism different from the labelled-line theory might also contribute to the regulation of the olfactory preference switch depending on the odour concentration.…”

Section: Discussionmentioning

confidence: 98%

Odour concentration-dependent olfactory preference change in C. elegans

et al. 2012

View full text Add to dashboard Cite

Section: Discussionmentioning

confidence: 98%

Odour concentration-dependent olfactory preference change in C. elegans

et al. 2012

View full text Add to dashboard Cite

“…To determine the level at which EGL-4 affects AWC's response to the adapting stimulus itself, we turned to the paradigm of butanone exposure-induced butanone repulsion (19). Briefly, prolonged (120 min) butanone exposures cause starving animals to be repulsed from butanone.…”

Section: Gfp-egl-4( Nls)mentioning

confidence: 99%

“…When starvation is coupled with 120 min of odor exposure, a new repulsive behavior is evoked (19). In this phase, the AWC neuron allows the animal to respond to butanone, but it switches from directing forward movement to initiating backward movement in response to the odor (19).…”

mentioning

confidence: 99%

See 1 more Smart Citation

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

Lee

O'Halloran

Eastham-Anderson

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

To navigate a complex and changing environment, an animal's sensory neurons must continually adapt to persistent cues while remaining responsive to novel stimuli. Long-term exposure to an inherently attractive odor causes Caenorhabditis elegans to ignore that odor, a process termed odor adaptation. Odor adaptation is likely to begin within the sensory neuron, because it requires factors that act within these cells at the time of odor exposure. The process by which an olfactory sensory neuron makes a decisive shift over time from a receptive state to a lasting unresponsive one remains obscure. In C. elegans, adaptation to odors sensed by the AWC pair of olfactory neurons requires the cGMP-dependent protein kinase EGL-4. Using a fully functional, GFP-tagged EGL-4, we show here that prolonged odor exposure sends EGL-4 into the nucleus of the stimulated AWC neuron. This odor-induced nuclear translocation correlates temporally with the stable dampening of chemotaxis that is indicative of long-term adaptation. Long-term adaptation requires cGMP binding residues as well as an active EGL-4 kinase. We show here that EGL-4 nuclear accumulation is both necessary and sufficient to induce longlasting odor adaptation. After it is in the AWC nucleus, EGL-4 decreases the animal's responsiveness to AWC-sensed odors by acting downstream of the primary sensory transduction. Thus, the EGL-4 protein kinase acts as a sensor that integrates odor signaling over time, and its nuclear translocation is an instructive switch that allows the animal to ignore persistent odors.neuron | plasticity | signaling | memory | integration S ensory neurons, the entry point for information about an animal's external environment, must both respond to relevant stimuli and dampen their response as a consequence of prolonged stimulation. This dampening or adaptation is thought to be a protective consequence of prolonged stimulation, because indeed, adaptation protects mammalian photoreceptors from stimulationinduced degeneration (1, 2). The cellular, molecular, and temporal controls that allow sensory neurons to switch from being responsive to refractory to a given stimulus are examined herein. The Caenorhabditis elegans AWC sensory neuronal pair can sense (3) and adapt (4) to inherently attractive odors, and although both sensory and interneurons within the olfactory circuit adapt to persistent stimulation (5, 6), this focus will be on the events that instruct long-lasting adaptation within the sensory neuron.The AWC neurons (3, 7) are postulated to express at least 20 different odor-responsive G protein-coupled receptors (8, 9), use cGMP as a second messenger (10-13), and hyperpolarize in response to odor (14). Odor adaptation begins within 10 min of odor exposure, and there is a mild decrease in the animal's attraction to the odor accompanied by an increase in phosphorylated MAP kinase in AWC (5, 15) that requires the G protein gamma, GPC-1 (16). After 30 min of exposure, attraction decreases further as the animal enters a phase of short-term adaptation...

show abstract

“…AWC ON and AWC OFF neurons have similar morphologies but different functions and patterns of gene expression (Troemel et al 1999). AWC ON senses the odor butanone, expresses the G protein-coupled receptor gene str-2, and can promote either attractive or repulsive behaviors based on modulatory inputs from a guanylate cyclase (Troemel et al 1999;Wes and Bargmann 2001;Tsunozaki et al 2008). The contralateral neuron, AWC OFF , senses the odor 2,3-pentanedione, expresses the G protein-coupled receptor gene srsx-3, and has only been observed to mediate attractive behaviors (Wes and Bargmann 2001;Bauer Huang et al 2007).…”

mentioning

confidence: 99%

Transcriptional regulation and stabilization of left–right neuronal identity in C. elegans

Lesch

Gehrke²,

Bulyk³

et al. 2009

Genes Dev.

Self Cite

View full text Add to dashboard Cite

At discrete points in development, transient signals are transformed into long-lasting cell fates. For example, the asymmetric identities of two Caenorhabditis elegans olfactory neurons called AWC ON and AWC OFF are specified by an embryonic signaling pathway, but maintained throughout the life of an animal. Here we show that the DNAbinding protein NSY-7 acts to convert a transient, partially differentiated state into a stable AWC ON identity. Expression of an AWC ON marker is initiated in nsy-7 loss-of-function mutants, but subsequently lost, so that most adult animals have two AWC OFF neurons and no AWC ON neurons. nsy-7 encodes a protein with distant similarity to a homeodomain. It is expressed in AWC ON , and is an early transcriptional target of the embryonic signaling pathway that specifies AWC ON and AWC OFF ; its expression anticipates future AWC asymmetry. The NSY-7 protein binds a specific optimal DNA sequence that was identified through a complete biochemical survey of 8-mer DNA sequences. This sequence is present in the promoter of an AWC OFF marker and essential for its asymmetric expression. An 11-base-pair (bp) sequence required for AWC OFF expression has two activities: One region activates expression in both AWCs, and the overlapping NSY-7-binding site inhibits expression in AWC ON . Our results suggest that NSY-7 responds to transient embryonic signaling by repressing AWC OFF genes in AWC ON , thus acting as a transcriptional selector for a randomly specified neuronal identity.[Keywords: Homeodomain; olfactory development; transcriptional maintenance; transcriptional repression; activitydependent gene expression; cGMP-dependent protein kinase] Supplemental material is available at http://www.genesdev.org.

show abstract

A Behavioral Switch: cGMP and PKC Signaling in Olfactory Neurons Reverses Odor Preference in C. elegans

Cited by 133 publications

References 65 publications

Odour concentration-dependent olfactory preference change in C. elegans

Odour concentration-dependent olfactory preference change in C. elegans

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

Transcriptional regulation and stabilization of left–right neuronal identity in C. elegans

Contact Info

Product

Resources

About