Chemosensory Neurons Function in Parallel to Mediate a Pheromone Response in C. elegans

Schackwitz, Wendy; Inoué, Takao; Thomas, James H.

doi:10.1016/s0896-6273(00)80203-2

Cited by 299 publications

(350 citation statements)

References 32 publications

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“…In the dauer formation assay, the fraction is incorporated into a minimal agar plate, onto which 50-100 eggs are laid and allowed to develop in the presence of a small amount of Escherichia coli food over the course of 3-4 d (6). Although the genetics of dauer formation and recovery are similar, some differences have been identified, such as the role of specific amphid chemosensory neurons (20) and certain G proteins (47) in the dauer formation and recovery processes. Thus, although it is likely that the small molecules that control dauer formation and recovery are similar, there may be differences between them.…”

Section: Resultsmentioning

confidence: 99%

“…Epistasis analysis has enabled these genes to be ordered into signaling pathways (8,(14)(15)(16). Currently, it is thought that the dauer pheromone is detected by exposed sensory neurons in the head of the worm (17)(18)(19)(20)(21) and signals through multiple signaling pathways, including the TGF␤ pathway (20,(22)(23)(24) and the insulin/insulin-like growth factor-1 (IGF-1) pathway (25)(26)(27)(28)(29). These pathways converge on the nuclear hormone receptor DAF-12, which acts downstream of most Daf genes and which is expressed in many tissues that undergo remodeling during dauer formation (30).…”

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confidence: 99%

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A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components

Butcher

Ragains

Kim

et al. 2008

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

145

172

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In the model organism Caenorhabditis elegans, the dauer pheromone is the primary cue for entry into the developmentally arrested, dauer larval stage. The dauer is specialized for survival under harsh environmental conditions and is considered ''nonaging'' because larvae that exit dauer have a normal life span. C. elegans constitutively secretes the dauer pheromone into its environment, enabling it to sense its population density. Several components of the dauer pheromone have been identified as derivatives of the dideoxy sugar ascarylose, but additional unidentified components of the dauer pheromone contribute to its activity. Here, we show that an ascaroside with a 3-hydroxypropionate side chain is a highly potent component of the dauer pheromone that acts synergistically with previously identified components. Furthermore, we show that the active dauer pheromone components that are produced by C. elegans vary depending on cultivation conditions. Identifying the active components of the dauer pheromone, the conditions under which they are produced, and their mechanisms of action will greatly extend our understanding of how chemosensory cues from the environment can influence such fundamental processes as development, metabolism, and aging in nematodes and in higher organisms.ascaroside ͉ natural product structure elucidation

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components

Butcher

Ragains

Kim

et al. 2008

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

145

172

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“…By soaking gcs1ϻgfp lines in DiI, a dye that fills amphid sensory neurons (Herman and Hedgecock 1990), we determined that two GCS-1ϻGFP-expressing cells located adjacent to the posterior pharynx correspond to the ASI chemosensory neurons (Fig. 2C,D), which prevent constitutive entry into the dauer diapause state (Ren et al 1996;Schackwitz et al 1996). GCS-1ϻGFP expression was also apparent anteriorly and posteriorly in the intestine ( Fig.…”

Section: Constitutive and Inducible Phase II Detoxification Gene Actimentioning

confidence: 99%

SKN-1 linksC. elegansmesendodermal specification to a conserved oxidative stress response

An¹,

Blackwell²

2003

Genes Dev.

664

877

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During the earliest stages of Caenorhabditis elegans embryogenesis, the transcription factor SKN-1 initiates development of the digestive system and other mesendodermal tissues. Postembryonic SKN-1 functions have not been elucidated. SKN-1 binds to DNA through a unique mechanism, but is distantly related to basic leucine-zipper proteins that orchestrate the major oxidative stress response in vertebrates and yeast. Here we show that despite its distinct mode of target gene recognition, SKN-1 functions similarly to resist oxidative stress in C. elegans. During postembryonic stages, SKN-1 regulates a key Phase II detoxification gene through constitutive and stress-inducible mechanisms in the ASI chemosensory neurons and intestine, respectively. SKN-1 is present in ASI nuclei under normal conditions, and accumulates in intestinal nuclei in response to oxidative stress. skn-1 mutants are sensitive to oxidative stress and have shortened lifespans. SKN-1 represents a connection between developmental specification of the digestive system and one of its most basic functions, resistance to oxidative and xenobiotic stress. This oxidative stress response thus appears to be both widely conserved and ancient, suggesting that the mesendodermal specification role of SKN-1 was predated by its function in these detoxification mechanisms.

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“…3). daf-7 was reported to be expressed specifically in the amphid neurons ASI (32,33), and expression of daf-7 specifically in ASI neurons rescued the defect in CO 2 avoidance of daf-7 mutants (Fig. S5B).…”

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confidence: 90%

Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

Hallem

Spencer

McWhirter

et al. 2010

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

121

173

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CO 2 is both a critical regulator of animal physiology and an important sensory cue for many animals for host detection, food location, and mate finding. The free-living soil nematode Caenorhabditis elegans shows CO 2 avoidance behavior, which requires a pair of ciliated sensory neurons, the BAG neurons. Using in vivo calcium imaging, we show that CO 2 specifically activates the BAG neurons and that the CO 2 -sensing function of BAG neurons requires TAX-2/ TAX-4 cyclic nucleotide-gated ion channels and the receptor-type guanylate cyclase GCY-9. Our results delineate a molecular pathway for CO 2 sensing and suggest that activation of a receptor-type guanylate cyclase is an evolutionarily conserved mechanism by which animals detect environmental CO 2 .guanylyl cyclase | olfaction | transcriptional profiling | regulator of G protein signaling | chemosensation T he ability to detect and respond to changing concentrations of environmental CO 2 is widespread among animals and plays a critical role in locating food, finding hosts and mates, and avoiding danger (1-4). CO 2 exposure can also have profound physiological effects, including altered respiration, motility, fecundity, and emotional state (5-7). CO 2 is sensed as an aversive cue by many free-living animals, including humans (3,6,8,9). By contrast, many parasites and disease vectors are attracted to CO 2 , which serves as a sensory cue for host location (1, 10).Nematodes constitute a large and highly diverse phylum that includes both free-living and parasitic species. Many parasitic nematodes, including some of the most devastating human-and plant-parasitic nematodes, are attracted to CO 2 . By contrast, adults of the free-living species Caenorhabditis elegans are repelled by CO 2 (11-14). CO 2 avoidance by C. elegans requires a pair of head neurons called the BAG neurons (13), which also mediate responses to decreases in ambient oxygen levels (15). Whether the BAG neurons directly sense CO 2 is not known, and the signaling pathways that mediate CO 2 detection are poorly understood.We show here that environmental CO 2 specifically activates the BAG neurons and not other neurons that drive avoidance behavior, suggesting that the BAG neurons are primary sensory neurons that detect CO 2 . Prolonged CO 2 exposure causes desensitization of avoidance behavior and the BAG neurons themselves, indicating that behavioral adaptation to CO 2 occurs at the level of the BAG neurons. In addition, we show that the CO 2 -evoked activity of the BAG neurons requires a cGMP signaling pathway consisting of the receptor guanylate cyclase GCY-9 and the cGMP-gated cation channel TAX-2/TAX-4. Insects detect CO 2 using a pair of gustatory receptors (16, 17), whereas some mammals detect CO 2 using the receptor-type guanylate cyclase, guanylate cyclase D (GC-D), and soluble adenylate cyclase (18)(19)(20). Our results show that the mechanism of CO 2 detection in C. elegans more closely resembles that of mammals than insects and suggest an evolutionarily ancient role for receptor-type guanyl...

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Chemosensory Neurons Function in Parallel to Mediate a Pheromone Response in C. elegans

Cited by 299 publications

References 32 publications

A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components

A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components

SKN-1 linksC. elegansmesendodermal specification to a conserved oxidative stress response

Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

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