In vivo calcium imaging of OFF-responding ASK chemosensory neurons in C. elegans

Wakabayashi, Tokumitsu; Kimura, Yukihiro; Ohba, Yusuke; Adachi, Ryota; Satoh, Yuichi; Shingai, Ryuzo

doi:10.1016/j.bbagen.2009.03.032

Cited by 29 publications

(28 citation statements)

References 33 publications

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“…Desensitization may also enable processes such as novelty detection, acute protection from overstimulation, or sharpening of response dynamics for efficient downstream processing (Wark et al, 2007). Interestingly, desensitization is observed in other C. elegans sensory neurons whose calcium levels increase with stimulation, like AWA, but is less prominent in sensory neurons whose calcium levels decrease with stimulation, like AWC (Chalasani et al, 2007; Hilliard et al, 2004; Suzuki et al, 2008; Wakabayashi et al, 2009). The depolarizing regime of sensory processing may preferentially encode stimulus change over stimulus level, and may help explain why AWA and AWC, which detect similar and even overlapping attractive odors, have distinct sensory transduction properties.…”

Section: Discussionmentioning

confidence: 99%

A Circuit for Gradient Climbing in C. elegans Chemotaxis

Larsch¹,

Flavell²,

Liu³

et al. 2015

Cell Reports

128

195

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Animals have a remarkable ability to track dynamic sensory information. For example, the nematode Caenorhabditis elegans can locate a diacetyl odor source across a 100,000-fold concentration range. Here, we relate neuronal properties, circuit implementation, and behavioral strategies underlying this robust navigation. Diacetyl responses in AWA olfactory neurons are concentration- and history-dependent; AWA integrates over time at low odor concentrations, but as concentrations rise it desensitizes rapidly through a process requiring cilia transport. After desensitization, AWA retains sensitivity to small odor increases. The downstream AIA interneuron amplifies weak odor inputs and desensitizes further, resulting in a stereotyped response to odor increases over three orders of magnitude. The AWA-AIA circuit drives asymmetric behavioral responses to odor increases that facilitate gradient climbing. The adaptation-based circuit motif embodied by AWA and AIA shares computational properties with bacterial chemotaxis and the vertebrate retina, each providing a solution for maintaining sensitivity across a dynamic range.

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Section: Discussionmentioning

confidence: 99%

A Circuit for Gradient Climbing in C. elegans Chemotaxis

Larsch¹,

Flavell²,

Liu³

et al. 2015

Cell Reports

128

195

View full text Add to dashboard Cite

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“…The AWB and ASK amphid chemosensory neurons ( Figure 1A) respond largely to volatile and aqueous compounds, including lipophilic pheromones, respectively (Bargmann and Horvitz 1991;Troemel et al 1997;Kim et al 2009;Macosko et al 2009;Wakabayashi et al 2009). We and others previously showed that the AWB neurons express a subset of predicted GPCRs encoded by the C. elegans genome (Troemel et al 1995;Colosimo et al 2004;Nokes et al 2009;C.…”

Section: Resultsmentioning

confidence: 99%

Diverse Cell Type-Specific Mechanisms Localize G Protein-Coupled Receptors to Caenorhabditis elegans Sensory Cilia

Brear

Yoon

Wojtyniak³

et al. 2014

Genetics

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The localization of signaling molecules such as G protein-coupled receptors (GPCRs) to primary cilia is essential for correct signal transduction. Detailed studies over the past decade have begun to elucidate the diverse sequences and trafficking mechanisms that sort and transport GPCRs to the ciliary compartment. However, a systematic analysis of the pathways required for ciliary targeting of multiple GPCRs in different cell types in vivo has not been reported. Here we describe the sequences and proteins required to localize GPCRs to the cilia of the AWB and ASK sensory neuron types in Caenorhabditis elegans. We find that GPCRs expressed in AWB or ASK utilize conserved and novel sequences for ciliary localization, and that the requirement for a ciliary targeting sequence in a given GPCR is different in different neuron types. Consistent with the presence of multiple ciliary targeting sequences, we identify diverse proteins required for ciliary localization of individual GPCRs in AWB and ASK. In particular, we show that the TUB-1 Tubby protein is required for ciliary localization of a subset of GPCRs, implying that defects in GPCR localization may be causal to the metabolic phenotypes of tub-1 mutants. Together, our results describe a remarkable complexity of mechanisms that act in a protein-and cellspecific manner to localize GPCRs to cilia, and suggest that this diversity allows for precise regulation of GPCR-mediated signaling as a function of external and internal context. SIGNALING molecules must be precisely localized to specific subcellular domains to optimize detection and transduction of external stimuli. G protein-coupled receptors (GPCRs) comprise a large family of transmembrane signaling proteins that directly bind and transduce a range of cues including photons, odorants, neurotransmitters, and peptides (Pierce et al. 2002;Kato and Touhara 2009;Demaria and Ngai 2010;Sung and Chuang 2010;Chamero et al. 2012;Frooninckx et al. 2012;Montell 2012;Bathgate et al. 2013). Regulation of GPCR function, including regulation of membrane targeting and trafficking to specific subcellular regions, is a major contributor to the tuning of signaling efficacy and fidelity (e.g., Deretic et al. 1995;Ango et al. 2000;Xia et al. 2003;Esseltine et al. 2012;. However, much remains to be understood regarding the mechanisms by which GPCR trafficking and membrane localization are regulated.GPCR-mediated signal transduction in many cellular contexts requires these proteins to be localized to specialized microtubule-based primary cilia. For example, in photoreceptors and olfactory neurons, efficient sensory signal transduction is mediated via localization of rhodopsin and olfactory receptors, together with other signaling molecules, to photoreceptor outer segments and olfactory neuron cilia, respectively (Insinna and Besharse 2008;Berbari et al. 2009;Pifferi et al. 2010;Deretic and Wang 2012). Receptors in the Hedgehog (Hh) morphogen signaling pathway such as the Smoothened and Patched transmembrane proteins, and the G...

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“…Previous work has shown that ablating the AWC and ASK neurons partially disrupts the stimulatory effect of food on egg-laying (62). Ca 2+ imaging suggests that food-associated cues inhibit the AWC and ASK neurons (47). Perhaps the CO 2 -evoked Ca 2+ increases we observed in these same neurons antagonize the effects of food on ASK and AWC neurons, thereby inhibiting egg-laying.…”

Section: Resultsmentioning

confidence: 85%

“…cGMP channel subunits encoded by the tax-4 and tax-2 genes are expressed in four of the CO 2 -responsive neurons we have identified here: ASJ, ASK, AWC, and ASG. The previously studied sensory responses mediated by these neurons [e.g., ASJ responses to light (46); ASK responses to pheromones and food (45,47); and AWC responses to odors (48,49)] are disrupted in tax-2 or tax-4 mutants. Do CO 2 responses in these neurons also depend on these cGMP channels?…”

Section: Resultsmentioning

confidence: 99%

Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

Fenk

Bono

2015

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

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Carbon dioxide (CO 2 ) gradients are ubiquitous and provide animals with information about their environment, such as the potential presence of prey or predators. The nematode Caenorhabditis elegans avoids elevated CO 2 , and previous work identified three neuron pairs called "BAG," "AFD," and "ASE" that respond to CO 2 stimuli. Using in vivo Ca 2+ imaging and behavioral analysis, we show that C. elegans can detect CO 2 independently of these sensory pathways. Many of the C. elegans sensory neurons we examined, including the AWC olfactory neurons, the ASJ and ASK gustatory neurons, and the ASH and ADL nociceptors, respond to a rise in CO 2 with a rise in Ca 2+ . In contrast, glial sheath cells harboring the sensory endings of C. elegans' major chemosensory neurons exhibit strong and sustained decreases in Ca 2+ in response to high CO 2 . Some of these CO 2 responses appear to be cell intrinsic. Worms therefore may couple detection of CO 2 to that of other cues at the earliest stages of sensory processing. We show that C. elegans persistently suppresses oviposition at high CO 2 . Hermaphrodite-specific neurons (HSNs), the executive neurons driving egg-laying, are tonically inhibited when CO 2 is elevated. CO 2 modulates the egg-laying system partly through the AWC olfactory neurons: High CO 2 tonically activates AWC by a cGMP-dependent mechanism, and AWC output inhibits the HSNs. Our work shows that CO 2 is a more complex sensory cue for C. elegans than previously thought, both in terms of behavior and neural circuitry.neural circuit | behavioral choice | olfactory system | oviposition | glia M ost living matter creates temporal or spatial gradients of carbon dioxide (CO 2 ). Animals across phylogeny use such gradients to help detect food, conspecifics, or predators (1, 2). The ubiquity of CO 2 suggests that the ecologically relevant information it communicates will depend on the dynamics of the CO 2 stimulus and on context. CO 2 -responsive excitable cells have been identified in mammals (3), arthropods (4), and nematodes (5, 6). However, the number of CO 2 -responsive neurons that are functional in vivo, how they are embedded in neural circuits, and how they shape behavior is unclear.CO 2 crosses membranes readily and dissolves to generate CO 2 (aq), H + , and HCO 3 − . Many proteins whose activity is modified by CO 2 or its solvation products have been identified. pH changes can modulate G protein-coupled receptors (7), Ca 2+ -activated K + channels (8), inwardly rectifying K + channels (9), two pore domain K + channels (10), transient receptor potential (TRP) channels (11, 12), acid-sensing ion channels (ASICs) (13,14), and Pyk2 and ErbB1/2 kinases (15). HCO 3 − modulates soluble adenylate cyclase (16) and transmembrane guanylate cyclases (17); and CO 2 (aq) has been proposed to regulate transmembrane guanylate cyclases (18) and connexin 26 (19) directly. Cells expressing any of these proteins potentially could transduce changes in CO 2 /H + , raising the question: Do animals use a few specific sensory channe...

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In vivo calcium imaging of OFF-responding ASK chemosensory neurons in C. elegans

Cited by 29 publications

References 33 publications

A Circuit for Gradient Climbing in C. elegans Chemotaxis

A Circuit for Gradient Climbing in C. elegans Chemotaxis

Diverse Cell Type-Specific Mechanisms Localize G Protein-Coupled Receptors to Caenorhabditis elegans Sensory Cilia

Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

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In vivo calcium imaging of OFF-responding ASK chemosensory neurons in C. elegans

Cited by 29 publications

References 33 publications

A Circuit for Gradient Climbing in C. elegans Chemotaxis

A Circuit for Gradient Climbing in C. elegans Chemotaxis

Diverse Cell Type-Specific Mechanisms Localize G Protein-Coupled Receptors to Caenorhabditis elegans Sensory Cilia

Environmental CO 2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

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Resources

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Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity