GPC-1, a G Protein γ-Subunit, Regulates Olfactory Adaptation in <i>Caenorhabditis elegans</i>

Yamada, Koji; Hirotsu, Takaaki; Matsuki, Masahiro; Kunitomo, Hirofumi; Iino, Yuichi

doi:10.1534/genetics.108.099002

Cited by 25 publications

(21 citation statements)

References 45 publications

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“…GPB-2 is similar to the novel vertebrate G␤ 5 subunit (52)(53)(54)(55). GPC-1 is expressed in a subset of sensory neurons and is required for response to quinine, as well as adaptation to a variety of attractants and repellents (56,57), whereas no sensory function has been reported for GPC-2 (58).…”

Section: Rh Domain-mediated Interactions Are Not Required For Ce-grk-mentioning

confidence: 99%

Structural Domains Required for Caenorhabditis elegans G Protein-coupled Receptor Kinase 2 (GRK-2) Function in Vivo

Wood

Wang

Benovic

et al. 2012

Journal of Biological Chemistry

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Background: GRKs phosphorylate activated GPCRs to terminate signaling. Results: Disrupting residues required for GPCR phosphorylation and G␤␥ and phospholipid binding eliminated Ce-GRK-2 chemosensory function. Conclusion: These interactions are required for Ce-GRK-2 function in vivo and support a recently proposed universal model for GRK activation. Significance: This is the first study to systematically determine the residues required for GRK function in live animals.

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Section: Rh Domain-mediated Interactions Are Not Required For Ce-grk-mentioning

confidence: 99%

Structural Domains Required for Caenorhabditis elegans G Protein-coupled Receptor Kinase 2 (GRK-2) Function in Vivo

Wood

Wang

Benovic

et al. 2012

Journal of Biological Chemistry

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“…Gene and protein expression data for solitary chemosensory cells (SCCs) in the gut and the respiratory tract as well as for the putative glucose-sensing hypothalamic neurons, which express taste receptor T1R1, T1R2, and T1R3, also indicates the presence of a similar Gβγ-mediated activation of the PLC pathway (Bezencon et al, 2007; Lin et al, 2008; Ren et al, 2009; Krasteva et al, 2011). In invertebrates, Gγ 1 has been implicated in the detection of sugar by Drosophila taste neurons, and GPC-1, one of the Gγ subunit homologs in C.elegans , has been implicated in taste (Jansen et al, 2002) and olfactory adaptation (Yamada et al, 2009). These accumulating evidences clearly demonstrate the important role of Gβγ subunits in chemical sensing.…”

Section: Introductionmentioning

confidence: 99%

Expression profile of G-protein βγ subunit gene transcripts in the mouse olfactory sensory epithelia

Sathyanesan¹,

Feijoo²,

Mehta³

et al. 2013

Front. Cell. Neurosci.

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Heterotrimeric G-proteins mediate a variety of cellular functions, including signal transduction in sensory neurons of the olfactory system. Whereas the Gα subunits in these neurons are well characterized, the gene transcript expression profile of Gβγ subunits is largely missing. Here we report our comprehensive expression analysis to identify Gβ and Gγ subunit gene transcripts in the mouse main olfactory epithelium (MOE) and the vomeronasal organ (VNO). Our reverse transcriptase PCR (RT-PCR) and realtime qPCR analyses of all known Gβ (β1,2,3,4,5) and Gγ (γ1,2,2t,3,4,5,7,8,10,11,12,13) subunits indicate presence of multiple Gβ and Gγ subunit gene transcripts in the MOE and the VNO at various expression levels. These results are supported by our RNA in situ hybridization (RISH) experiments, which reveal the expression patterns of two Gβ subunits and four Gγ subunits in the MOE as well as one Gβ and four Gγ subunits in the VNO. Using double-probe fluorescence RISH and line intensity scan analysis of the RISH signals of two dominant Gβγ subunits, we show that Gγ13 is expressed in mature olfactory sensory neurons (OSNs), while Gβ1 is present in both mature and immature OSNs. Interestingly, we also found Gβ1 to be the dominant Gβ subunit in the VNO and present throughout the sensory epithelium. In contrast, we found diverse expression of Gγ subunit gene transcripts with Gγ2, Gγ3, and Gγ13 in the Gαi2-expressing neuronal population, while Gγ8 is expressed in both layers. Further, we determined the expression of these Gβγ gene transcripts in three post-natal developmental stages (p0, 7, and 14) and found their cell-type specific expression remains largely unchanged, except the transient expression of Gγ2 in a single basal layer of cells in the MOE during P7 and P14. Taken together, our comprehensive expression analyses reveal cell-type specific gene expression of multiple Gβ and Gγ in sensory neurons of the olfactory system.

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“…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 that requires the protein kinase (PKG) EGL-4 and a consensus PKG phosphorylation site within the C terminus of the cGMP-gated channel β-subunit, TAX-2 (17).…”

mentioning

confidence: 99%

“…Genetic analysis has produced a list of factors required for adaptation (4,6,16,17,(20)(21)(22)(23)(24); however, the process by which these factors promote adaptation is unknown. To understand how adaptation proceeds in the AWC neuron, we complemented genetic methods with cell biological techniques.…”

mentioning

confidence: 99%

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.

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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...

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GPC-1, a G Protein γ-Subunit, Regulates Olfactory Adaptation in Caenorhabditis elegans

Cited by 25 publications

References 45 publications

Structural Domains Required for Caenorhabditis elegans G Protein-coupled Receptor Kinase 2 (GRK-2) Function in Vivo

Structural Domains Required for Caenorhabditis elegans G Protein-coupled Receptor Kinase 2 (GRK-2) Function in Vivo

Expression profile of G-protein βγ subunit gene transcripts in the mouse olfactory sensory epithelia

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

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