Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases

Zimmer, Manuel; Gray, Jesse; Pokala, Navin; Chang, Andy J.; Karow, David S.; Marletta, Michael A.; Hudson, Martin L.; Morton, David B.; Chronis, Nikos; Bargmann, Cornelia I.

doi:10.1016/j.neuron.2009.02.013

Cited by 267 publications

(463 citation statements)

References 54 publications

(104 reference statements)

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“…We also tested whether two BAG neuron-specific guanylate cyclases, gcy-31 and gcy-33, are required for CO 2 -evoked BAG neuron activity. gcy-31 and gcy-33 encode soluble guanylate cyclases that are required for BAG neuron responses to acute hypoxia (15). We found that the BAG neurons of gcy-33; gcy-31 double mutants showed normal CO 2 -evoked activity and that gcy-33; gcy-31 mutants had normal behavioral responses to CO 2 .…”

mentioning

confidence: 79%

“…By contrast, adults of the free-living species Caenorhabditis elegans are repelled by CO 2 (11)(12)(13)(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.…”

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confidence: 99%

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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.

118

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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mentioning

confidence: 79%

mentioning

confidence: 99%

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.

118

173

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“…The regulation of bordering and clumping behaviours by oxygen was analysed by performing the above assay in a custom-fabricated Plexiglas chamber [25]. In our assays, the air pressure remained always constant when oxygen concentration was manipulated.…”

Section: (B) Behavioural Assaysmentioning

confidence: 99%

“…B 283: 20152263 to attractive stimuli [29]. Wild isolates, like CB4856 from Hawaii, respond to the aversive stimuli induced by shifts in oxygen concentration from 20% to 21% with increased rates of V-turns, whereas the solitary N2 strain does not modify its V-turn rate in response to these shifts [21,25]. To explore whether a similar pattern exists in P. pacificus, we analysed the V-turn rate of RSB001 and RS2333 under varying oxygen levels (see Methods).…”

Section: (B) Natural Variation In Clumping and Bordering Inmentioning

confidence: 99%

Oxygen-induced social behaviours inPristionchus pacificushave a distinct evolutionary history and genetic regulation fromCaenorhabditis elegans

et al. 2016

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Wild isolates of the nematode Caenorhabditis elegans perform social behaviours, namely clumping and bordering, to avoid hyperoxia under laboratory conditions. In contrast, the laboratory reference strain N2 has acquired a solitary behaviour in the laboratory, related to a gain-of-function variant in the neuropeptide Y-like receptor NPR-1. Here, we study the evolution and natural variation of clumping and bordering behaviours in Pristionchus pacificus nematodes in a natural context, using strains collected from 22 to 2400 metres above sea level on La Réunion Island. Through the analysis of 106 wild isolates, we show that the majority of strains display a solitary behaviour similar to C. elegans N2, whereas social behaviours are predominantly seen in strains that inhabit high-altitude locations. We show experimentally that P. pacificus social strains perform clumping and bordering to avoid hyperoxic conditions in the laboratory, suggesting that social strains may have adapted to or evolved a preference for the lower relative oxygen levels available at high altitude in nature. In contrast to C. elegans, clumping and bordering in P. pacificus do not correlate with locomotive behaviours in response to changes in oxygen conditions. Furthermore, QTL analysis indicates clumping and bordering to represent complex quantitative traits. Thus, clumping and bordering behaviours represent an example of phenotypic convergence with a different evolutionary history and distinct genetic control in both nematode species.

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“…GLB-5 modulates the same O 2 sensing neurons as NPR-1 (AQR, PQR, and URX), which also express GCY-35 and GCY-36, subunits of soluble guanylate cyclases that also act as oxygen sensors (25,(30)(31)(32)(33). When the O 2 concentration rises, soluble guanylate cyclases are activated and cause an increase in the cGMP level, resulting in a depolarization of these neurons by cGMP-mediated gating of an ion channel that contains the TAX-4 subunit (15,27,34). It was proposed that GLB-5 acts as a signaling molecule, inhibiting neuronal activation when the O 2 concentration drops below 21% (15).…”

Section: Glb-5mentioning

confidence: 99%

Globins in Caenorhabditis elegans

et al. 2011

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SummaryExtensive in silico search of the genome of Caenorhabditis elegans revealed the presence of 33 genes coding for globins that are all transcribed. These globins are very diverse in gene and protein structure and are localized in a variety of cells, mostly neurons. The large number of C. elegans globin genes is assumed to be the result of multiple evolutionary duplication and radiation events. Processes of subfunctionalization and diversification probably led to their cell-specific expression patterns and fixation into the genome. To date, four globins (GLB-1, GLB-5, GLB-6, and GLB-26) have been partially characterized physicochemically, and the crystallographic structure of two of them (GLB-1 and GLB-6) was solved. In this article, a three-dimensional model was designed for the other two globins (GLB-5 and GLB-26), and overlays of the globins were constructed to highlight the structural diversity among them. It is clear that although they all share the globin fold, small variations in the three-dimensional structure have major implications on their ligand-binding properties and possibly their function. We also review here all the information available so far on the globin family of C. elegans and suggest potential functions.

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Neurons Detect Increases and Decreases in Oxygen Levels Using Distinct Guanylate Cyclases

Cited by 267 publications

References 54 publications

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

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

Oxygen-induced social behaviours inPristionchus pacificushave a distinct evolutionary history and genetic regulation fromCaenorhabditis elegans

Globins in Caenorhabditis elegans

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