The Gα Protein ODR-3 Mediates Olfactory and Nociceptive Function and Controls Cilium Morphogenesis in C. elegans Olfactory Neurons

Roayaie, Kayvan; Crump, J. Gage; Sagasti, Alvaro; Bargmann, Cornelia I.

doi:10.1016/s0896-6273(00)80434-1

Cited by 297 publications

(318 citation statements)

References 59 publications

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“…Additionally, the gene of odr-3 is involved in cilium morphogenesis in olfactory neurons, and its amount determined the extent of cilium outgrowth in AWA and AWC neurons. For example, it has been proposed that ODR-3 expression defined the unique fan-like extension of the AWC olfactory cilia (29). Thus it is reasonable for us to speculate that the ODR-3's function for maintaining the AWC cilium structure should be partially responsible for the deficiency to sense 2-heptanone besides its potential role in transducing the signal.…”

Section: Discussionmentioning

confidence: 99%

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

Zhang

Zhao

Chen

et al. 2016

Journal of Biological Chemistry

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The nematode Caenorhabditis elegans exhibits behavioral responses to a wide range of odorants associated with food and pathogens. A previous study described a Trojan Horse-like strategy of pathogenesis whereby the bacterium Bacillus nematocida B16 emits the volatile organic compound 2-heptanone to trap C. elegans for successful infection. Here, we further explored the receptor for 2-heptanone as well as the pathway involved in signal transduction in C. elegans. Our experiments showed that 2-heptanone sensing depended on the function of AWC neurons and a GPCR encoded by str-2. Consistent with the above observation, the HEK293 cells expressing STR-2 on their surfaces showed a transient elevation in intracellular Ca 2؉ levels after 2-heptanone applications. After combining the assays of RNA interference and gene mutants, we also identified the G␣ subunits and their downstream components in the olfactory signal cascade that are necessary for responding to 2-heptanone, including G␣ subunits of egl-30 and gpa-3, phospholipase C of plc-1and egl-8, and the calcium channel of cmk-1 and cal-1. Our work demonstrates for the first time that an integrated signaling pathway for 2-heptanone response in C. elegans involves recognition by GPCR STR-2, activation by G␣ subunits of egl-30/gpa-3 and transfer to the PLC pathway, indicating that a potentially novel olfactory pathway exists in AWC neurons. Meanwhile, since 2-heptanone, a metabolite from the pathogenic bacterium B. nematocida B16, can be sensed by C. elegans and thus strongly attract its host, our current work also suggested coevolution between the pathogenic microorganism and the chemosensory system in C. elegans.

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Section: Discussionmentioning

confidence: 99%

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

Zhang

Zhao

Chen

et al. 2016

Journal of Biological Chemistry

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“…The promoters of odr-3, gpa-13, and odr-1 drive the expression in AWC neurons and some other neurons (10,19,31,32). When goa-1 was expressed in AWC chemosensory neurons of goa-1(n1134) mutants using these promoters, goa-1(n1134) mutants were partially rescued for adaptation (Fig.…”

Section: Goa-1 Acts In Awc Chemosensory Neurons For Olfactory Adaptatmentioning

confidence: 95%

G _o α regulates olfactory adaptation by antagonizing G _q α-DAG signaling in Caenorhabditis elegans

Matsuki

Kunitomo

Iino

2006

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

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The heterotrimeric G protein Go is abundantly expressed in the mammalian nervous system and modulates neural activities in response to various ligands. However, G o's functions in living animals are less well understood. Here, we demonstrate that GOA-1 G o␣ has a fundamental role in olfactory adaptation in Caenorhabditis elegans. Impairment of GOA-1 G o␣ function and excessive activation of EGL-30 G q␣ cause a defect in adaptation to AWC-sensed odorants. These pathways antagonistically modulate olfactory adaptation in AWC chemosensory neurons. Wild-type animals treated with phorbol esters and double-mutant animals of diacylglycerol (DAG) kinases, dgk-3; dgk-1, also have a defect in adaptation, suggesting that elevated DAG signals disrupt normal adaptation. Constitutively active GOA-1 can suppress the adaptation defect of dgk-3; dgk-1 double mutants, whereas it fails to suppress the adaptation defect of animals with constitutively active EGL-30, implying that GOA-1 acts upstream of EGL-30 in olfactory adaptation. Our results suggest that down-regulation of EGL-30 -DAG signaling by GOA-1 underlies olfactory adaptation and plasticity of chemotaxis.chemotaxis ͉ G protein T he olfactory sensory system can endow animals with abilities to detect food sources and mates and, in some cases, to avoid harmful chemicals and predators. Sensitivity to an odor stimulus can be appropriately adjusted by previous experience, allowing the sensory system to adapt to changeable environments. In mammals, olfactory adaptation (habituation) is known to occur throughout the odorant sensory pathway; for example, olfactory receptor neurons (1), secondary interneurons (2), and primary and higher-order olfactory cortices (3). These adaptation mechanisms appear to allow animals to increase the range of concentrations of odor that can be sensed and to discriminate among multiple odors.The nematode Caenorhabditis elegans has only 302 neurons, and a variety of behaviors have been observed. Of these, olfactory behavior is relatively well studied. Volatile odorants are mainly sensed by five pairs of sensory neurons, AWA, AWB, AWC, ADL, and ASH (4-6), of which AWA and AWC chemosensory neurons mediate attraction behavior (4). In this response, olfactory adaptation has also been observed (7). Animals lacking OSM-9 TRPV channel (7, 8), EGL-4 cGMPdependent protein kinase (9) or animals overexpressing ODR-1 guanylyl cyclase (10) exhibited defects in olfactory adaptation to AWC-sensed odorants. By contrast, animals with mutated tax-6, which encodes calcineurin, exhibited hyperadaptation (11), suggesting that Ca 2ϩ and cGMP signaling cascades participate in olfactory adaptation. Moreover, ARR-1 arrestin (12), TBX-2 T-box transcription factor (13), and the Ras-MAPK pathway (14) are also known to act in olfactory adaptation, illustrating that olfactory adaptation in C. elegans is modulated by complicated mechanisms consisting of multiple signaling cascades and control of gene expression.In general, neural activities are modulated by many types of ligands th...

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“…A G␣ protein named ODR-3 is expressed in ASH neurons and is required for all behaviors that require OSM-9 and OCR-2 ( Fig. 2D) (98). Genetic and biochemical studies have also demonstrated a role for long-chain polyunsaturated fatty acids upstream from Ca 2ϩ transients in ASH neurons (47).…”

Section: R178 Salt and Water Homeostasis In C Elegansmentioning

confidence: 99%

Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

Choe

2013

American Journal of Physiology-Regulatory, Integrative and Comp

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Choe KP. Physiological and molecular mechanisms of salt and water homeostasis in the nematode Caenorhabditis elegans. Am J Physiol Regul Integr Comp Physiol 305: R175-R186, 2013. First published June 5, 2013 doi:10.1152/ajpregu.00109.2013.-Intracellular salt and water homeostasis is essential for all cellular life. Extracellular salt and water homeostasis is also important for multicellular organisms. Many fundamental mechanisms of compensation for osmotic perturbations are well defined and conserved. Alternatively, molecular mechanisms of detecting salt and water imbalances and regulating compensatory responses are generally poorly defined for animals. Throughout the last century, researchers studying vertebrates and vertebrate cells made critical contributions to our understanding of osmoregulation, especially mechanisms of salt and water transport and organic osmolyte accumulation. Researchers have more recently started using invertebrate model organisms with defined genomes and well-established methods of genetic manipulation to begin defining the genes and integrated regulatory networks that respond to osmotic stress. The nematode Caenorhabditis elegans is well suited to these studies. Here, I introduce osmoregulatory mechanisms in this model, discuss experimental advantages and limitations, and review important findings. Key discoveries include defining genetic mechanisms of osmolarity sensing in neurons, identifying protein damage as a sensor and principle determinant of hypertonic stress resistance, and identification of a putative sensor for hypertonic stress associated with the extracellular matrix. Many of these processes and pathways are conserved and, therefore, provide new insights into salt and water homeostasis in other animals, including mammals. osmoregulation; cell volume; ion; organic osmolyte; protein homeostasis; model organism SALT AND WATER HOMEOSTASIS is a fundamental requirement for metazoan life. Ion and water transport mechanisms that compensate for changes in composition and volume of intracellular and extracellular compartments have been generally well defined using vertebrate cell and in vivo models (38). Alternatively, the upstream molecular mechanisms that animal cells use to sense deviations in salt and water balance and regulate compensatory responses are still poorly characterized (20). Studies in brewer's yeast demonstrate that osmotic signal detection and transduction within a single eukaryotic cell can be highly complex with numerous components, acting in parallel pathways, that often cross-talk with other processes (40,55). Osmotic signal detection and transduction are likely to be even more complex in metazoans, which require homeostasis of both the extracellular and intracellular compartments and integration of responses between cells. Genetics is an extremely powerful approach for identifying and characterizing genes and proteins that function in complex biological processes but has been underutilized in the field of osmosensing and signal transduction in metazoans. In...

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The Gα Protein ODR-3 Mediates Olfactory and Nociceptive Function and Controls Cilium Morphogenesis in C. elegans Olfactory Neurons

Cited by 297 publications

References 59 publications

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

G _o α regulates olfactory adaptation by antagonizing G _q α-DAG signaling in Caenorhabditis elegans

Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

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The Gα Protein ODR-3 Mediates Olfactory and Nociceptive Function and Controls Cilium Morphogenesis in C. elegans Olfactory Neurons

Cited by 297 publications

References 59 publications

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

The Signaling Pathway of Caenorhabditis elegans Mediates Chemotaxis Response to the Attractant 2-Heptanone in a Trojan Horse-like Pathogenesis

G o α regulates olfactory adaptation by antagonizing G q α-DAG signaling in Caenorhabditis elegans

Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

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G _o α regulates olfactory adaptation by antagonizing G _q α-DAG signaling in Caenorhabditis elegans