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• W1973464749 abstract "Oxygen (O2) and carbon dioxide (CO2) levels vary in different environments and locally fluctuate during respiration and photosynthesis. Recent studies in diverse animals have identified sensory neurons that detect these external variations and direct a variety of behaviors. Detection allows animals to stay within a preferred environment as well as identify potential food or dangers. The complexity of sensation is reflected in the fact that neurons compartmentalize detection into increases, decreases, and short-range and long-range cues. Animals also adjust their responses to these prevalent signals in the context of other cues, allowing for flexible behaviors. In general, the molecular mechanisms for detection suggest that sensory neurons adopted ancient strategies for cellular detection and coupled them to brain activity and behavior. This review highlights the multiple strategies that animals use to extract information about their environment from variations in O2 and CO2. Oxygen (O2) and carbon dioxide (CO2) levels vary in different environments and locally fluctuate during respiration and photosynthesis. Recent studies in diverse animals have identified sensory neurons that detect these external variations and direct a variety of behaviors. Detection allows animals to stay within a preferred environment as well as identify potential food or dangers. The complexity of sensation is reflected in the fact that neurons compartmentalize detection into increases, decreases, and short-range and long-range cues. Animals also adjust their responses to these prevalent signals in the context of other cues, allowing for flexible behaviors. In general, the molecular mechanisms for detection suggest that sensory neurons adopted ancient strategies for cellular detection and coupled them to brain activity and behavior. This review highlights the multiple strategies that animals use to extract information about their environment from variations in O2 and CO2. Oxygen (O2) and carbon dioxide (CO2) are the substrates and products for maintaining life on earth. Because these two gases are essential, organisms have evolved sophisticated homeostatic mechanisms to ensure that appropriate internal concentrations are maintained. For example, if a jogger runs up a hill, arterial chemoreceptors in the carotid body sense a rapid reduction of O2 in the bloodstream and elicit panting to increase O2 intake (Gonzalez et al., 1992Gonzalez C. Almaraz L. Obeso A. Rigual R. Oxygen and acid chemoreception in the carotid body chemoreceptors.Trends Neurosci. 1992; 15: 146-153Abstract Full Text PDF PubMed Scopus (164) Google Scholar). In addition to internal monitoring of O2 and CO2, it has become increasingly clear that animals also monitor external concentrations and use this information to direct a variety of behaviors. In the atmosphere, O2 levels are 21% and CO2 levels are a trace 0.038%. However, in subterrestrial and aquatic environments, the concentrations of these substances vary enormously. Animals that live in these environments monitor external concentrations as a homeostatic mechanism to stay within a preferred concentration range that meets their metabolic needs. Fish gills have specialized chemoreceptor cells that sense variations in O2 or CO2 in the environment (Jonz et al., 2004Jonz M.G. Fearon I.M. Nurse C.A. Neuroepithelial oxygen chemoreceptors of the zebrafish gill.J. Physiol. 2004; 560: 737-752Crossref PubMed Scopus (141) Google Scholar, Qin et al., 2010Qin Z. Lewis J.E. Perry S.F. Zebrafish (Danio rerio) gill neuroepithelial cells are sensitive chemoreceptors for environmental CO2.J. Physiol. 2010; 588: 861-872Crossref PubMed Scopus (77) Google Scholar). Indeed, the size and shape of a school of fish may be a trade-off between access to oxygen-rich water at peripheral edges of the school and safety from predators in the middle (Brierley and Cox, 2010Brierley A.S. Cox M.J. Shapes of krill swarms and fish schools emerge as aggregation members avoid predators and access oxygen.Curr. Biol. 2010; 20: 1758-1762Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). Soil dwellers such as the nematode Caenorhabditis elegans also have sensory neurons that detect variations in O2 and CO2, allowing them to stay within their preferred environment (Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar, Cheung et al., 2005Cheung B.H. Cohen M. Rogers C. Albayram O. de Bono M. Experience-dependent modulation of C. elegans behavior by ambient oxygen.Curr. Biol. 2005; 15: 905-917Abstract Full Text Full Text PDF PubMed Scopus (142) Google Scholar, Bretscher et al., 2008Bretscher A.J. Busch K.E. de Bono M. A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8044-8049Crossref PubMed Scopus (111) Google Scholar, Hallem and Sternberg, 2008Hallem E.A. Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8038-8043Crossref PubMed Scopus (130) Google Scholar, Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). Even animals that live in enclosed spaces may monitor ambient concentrations. When CO2 levels in the hive increase by ∼1%–2%, honeybees exhibit fanning behavior to ventilate the nest in order to maintain a low CO2 environment (Seeley, 1974Seeley T.D. Atmospheric carbon dioxide regulation in honey-bee (Apis mellifera) colonies.J. Insect Physiol. 1974; 20: 2301-2305Crossref PubMed Scopus (86) Google Scholar). CO2 emitted during respiration may also serve as a secreted chemical signal that other animals detect. In this way, CO2 may act as a chemosensory signal that alerts animals to potential food, predators, or danger. Blood-feeding insects such as mosquitoes, black flies, and tsetse flies are attracted to CO2 and use this signal to hone in on their human hosts (Gibson and Torr, 1999Gibson G. Torr S.J. Visual and olfactory responses of haematophagous Diptera to host stimuli.Med. Vet. Entomol. 1999; 13: 2-23Crossref PubMed Scopus (233) Google Scholar). The hawkmoth, Manduca Sexta, prefers flowers that emit a high level of CO2, suggesting that CO2 acts as a proximal signal for nectar (Guerenstein et al., 2004Guerenstein P.G. Yepez E.A. Van Haren J. Williams D.G. Hildebrand J.G. Floral CO(2) emission may indicate food abundance to nectar-feeding moths.Naturwissenschaften. 2004; 91: 329-333Crossref PubMed Scopus (59) Google Scholar, Thom et al., 2004Thom C. Guerenstein P.G. Mechaber W.L. Hildebrand J.G. Floral CO2 reveals flower profitability to moths.J. Chem. Ecol. 2004; 30: 1285-1288Crossref PubMed Scopus (94) Google Scholar). CO2 increases can also signal avoidance, as CO2 emitted by Drosophila upon stress acts as a signal for other Drosophila to flee (Suh et al., 2004Suh G.S. Wong A.M. Hergarden A.C. Wang J.W. Simon A.F. Benzer S. Axel R. Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila.Nature. 2004; 431: 854-859Crossref PubMed Scopus (393) Google Scholar). How do animals detect and respond to varying concentrations of O2 and CO2 in their environment? Recent studies of the model organisms C. elegans, Drosophila melanogaster and mice have begun to elucidate the neural and molecular bases of detection. In all cases, detection occurs in specialized sensory cells; in Drosophila and mice, subsets of olfactory and gustatory neurons respond specifically to CO2. In most cases, these neurons respond to discrete features in their environment, such as increases or decreases in O2 or short-range or long-range cues. Detection can lead to attraction or avoidance behavior, and these behaviors are plastic. Plasticity may be especially important to allow animals to interpret the rather nonspecific signals of O2 and CO2 in the context of their complex sensory world. The molecular underpinnings of detection are beginning to be elucidated, highlighting similarities across organisms and commonalities with ancient cellular mechanisms of detection. The nematode C. elegans lives in the soil. O2 levels in this environment vary from 1%–21%, depending on depth from the surface as well as soil properties such as compaction, aeration, and drainage (Anderson and Ultsch, 1987Anderson J.F. Ultsch G.R. Respiratory gas concentrations in the microhabitats of some Florida arthropods.Comp. Biochem. Physiol. 1987; 88A: 585-588Crossref Scopus (39) Google Scholar). C. elegans show a behavioral preference for 5%–10% O2 levels and avoid higher and lower concentrations (Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar). This preferred O2 setpoint may reflect a compromise between the metabolic needs of the animal (favoring high O2) and oxidative stress (favoring low O2) (Lee and Atkinson, 1977Lee D.L. Atkinson H.J. Physiology of nematodes. Columbia University Press, New York1977Google Scholar). The study of C. elegans O2 sensation has provided a framework for understanding how animals monitor gas levels to select a preferred environment. Recent progress has been made elucidating the neural and molecular bases for hyperoxia avoidance. Two pairs of neurons, URX and BAG, play critical roles in sensing O2 (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar) (Figure 1). URX is a pair of unciliated sensory neurons whose dendrites extend toward the tip of the nose (White et al., 1986White J.G. Southgate E. Thomson J.N. Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1986; 314: 1-340Crossref PubMed Google Scholar). BAG neurons have bag-like dendrites that extend near the lateral lips (Perkins et al., 1986Perkins L.A. Hedgecock E.M. Thomson J.N. Culotti J.G. Mutant sensory cilia in the nematode Caenorhabditis elegans.Dev. Biol. 1986; 117: 456-487Crossref PubMed Scopus (642) Google Scholar, White et al., 1986White J.G. Southgate E. Thomson J.N. Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1986; 314: 1-340Crossref PubMed Google Scholar). Both URX and BAG neurons respond to changes in O2 in the environment but have different response properties and are associated with different behaviors. URX neurons depolarize in response to O2 increases, responding best to upshifts between 10%–12% to 15%–20% O2 (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). These neurons are essential for the aggregation behavior that C. elegans displays in response to high O2 and aerotaxis responses to O2 increases (Coates and de Bono, 2002Coates J.C. de Bono M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans.Nature. 2002; 419: 925-929Crossref PubMed Scopus (142) Google Scholar, Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar, Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). The BAG neurons, in contrast, respond to decreases in O2 levels, depolarizing upon downshifts to preferred concentrations (5%) (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). These neurons mediate aerotaxis response to O2 downshifts (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). Soluble guanylate cyclases are expressed in the O2-sensing neurons and mediate recognition. C. elegans have seven atypical, β-like, soluble GCs (Morton, 2004bMorton D.B. Invertebrates yield a plethora of atypical guanylyl cyclases.Mol. Neurobiol. 2004; 29: 97-116Crossref PubMed Google Scholar), four of which have been shown to participate in hyperoxic avoidance. gcy-35 and gcy-36 are expressed in URX and together mediate responses to O2 increases (Cheung et al., 2004Cheung B.H. Arellano-Carbajal F. Rybicki I. de Bono M. Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior.Curr. Biol. 2004; 14: 1105-1111Abstract Full Text Full Text PDF PubMed Scopus (109) Google Scholar, Cheung et al., 2005Cheung B.H. Cohen M. Rogers C. Albayram O. de Bono M. Experience-dependent modulation of C. elegans behavior by ambient oxygen.Curr. Biol. 2005; 15: 905-917Abstract Full Text Full Text PDF PubMed Scopus (142) Google Scholar, Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar, Chang et al., 2006Chang A.J. Chronis N. Karow D.S. Marletta M.A. Bargmann C.I. A distributed chemosensory circuit for oxygen preference in C. elegans.PLoS Biol. 2006; 4: e274Crossref PubMed Scopus (146) Google Scholar). gcy-31 and gcy-33 are required in BAG neurons for responses to O2 decreases (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar) (Figure 1). Guanylate cyclases are gas sensors that contain a heme-binding domain fused to a cyclase enzymatic domain that converts GTP to cGMP (Boon and Marletta, 2005Boon E.M. Marletta M.A. Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins.Curr. Opin. Chem. Biol. 2005; 9: 441-446Crossref PubMed Scopus (87) Google Scholar). For canonical GCs, the heme-binding domain selectively binds the reactive gas nitric oxide and excludes O2; a small change in the binding pocket of GCY-35 alters the ligand selectivity such that the heme binds O2 (Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar). How do O2 increases activate URX while decreases activate BAG? For URX, the model is that GCY-35 and GCY-36 sense an increase in O2, activating the cyclase leading to cGMP production, the opening of cyclic nucleotide-gated (CNG) ion channels (TAX-2/TAX-4), and cell depolarization (Coates and de Bono, 2002Coates J.C. de Bono M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans.Nature. 2002; 419: 925-929Crossref PubMed Scopus (142) Google Scholar, Cheung et al., 2004Cheung B.H. Arellano-Carbajal F. Rybicki I. de Bono M. Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior.Curr. Biol. 2004; 14: 1105-1111Abstract Full Text Full Text PDF PubMed Scopus (109) Google Scholar, Gray et al., 2004Gray J.M. Karow D.S. Lu H. Chang A.J. Chang J.S. Ellis R.E. Marletta M.A. Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue.Nature. 2004; 430: 317-322Crossref PubMed Scopus (396) Google Scholar, Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). For BAG, GCY-31 and GCY-33 are activated by a decrease in O2, triggering cyclase activity (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). Thus, the cyclases themselves are thought to show opposite responses to O2, with GCY-35/36 activated and GCY-31/33 inhibited by O2 increases. This model predicts that responses to increased and decreased O2 are the property of the cyclase not the neuron. Consistent with this, placing GCY-35 and GCY-36 in BAG neurons (in a gcy-31, gcy-33 double mutant background) causes these neurons to respond to O2 upshifts rather than downshifts (Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). Interestingly, Drosophila also contains three atypical guanylate cyclases that participate in O2-mediated behaviors: Gyc-89Da, Gyc-89Db, and Gyc-88E. Gyc88E clusters in a phylogenetic tree with C. elegans GCY-31 and Gyc-89Da/b cluster with GCY-33 (Morton, 2004bMorton D.B. Invertebrates yield a plethora of atypical guanylyl cyclases.Mol. Neurobiol. 2004; 29: 97-116Crossref PubMed Google Scholar, Zimmer et al., 2009Zimmer M. Gray J.M. Pokala N. Chang A.J. Karow D.S. Marletta M.A. Hudson M.L. Morton D.B. Chronis N. Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases.Neuron. 2009; 61: 865-879Abstract Full Text Full Text PDF PubMed Scopus (174) Google Scholar). Gyc-88E can act as a homodimer or as a heterodimer in conjunction with Gyc-89Da or Gyc-89Db, all of which increase cyclase activity under anoxic conditions (Morton, 2004aMorton D.B. Atypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors.J. Biol. Chem. 2004; 279: 50651-50653Crossref PubMed Scopus (46) Google Scholar). Purified Gyc-88E binds O2, and cyclase activity is inhibited as O2 increases (Huang et al., 2007Huang S.H. Rio D.C. Marletta M.A. Ligand binding and inhibition of an oxygen-sensitive soluble guanylate cyclase, Gyc-88E, from Drosophila.Biochemistry. 2007; 46: 15115-15122Crossref PubMed Scopus (25) Google Scholar). This argues that these cyclases are activated in the absence of O2, similar to the model for GCY-31 and GCY-33. Behaviorally, Drosophila larvae avoid hypoxic conditions (Wingrove and O'Farrell, 1999Wingrove J.A. O'Farrell P.H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila.Cell. 1999; 98: 105-114Abstract Full Text Full Text PDF PubMed Scopus (207) Google Scholar). When there is a decrease in O2 levels, larvae leave the food and wander. Mutants in any of the three Gycs reduce wandering under hypoxic conditions (Vermehren-Schmaedick et al., 2010Vermehren-Schmaedick A. Ainsley J.A. Johnson W.A. Davies S.A. Morton D.B. Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases.Genetics. 2010; 186: 183-196Crossref PubMed Scopus (39) Google Scholar). When larvae are exposed to hyperoxic or hypoxic environments, they decrease stops and turns, suggesting escape behavior. Mutants in gyc-89Da do not show this decrease to hypoxia (11%–16% O2) and gyc-89Db mutants do not show this decrease to mild hypoxia (18%–20%) or hyperoxia (22%–30%) (Vermehren-Schmaedick et al., 2010Vermehren-Schmaedick A. Ainsley J.A. Johnson W.A. Davies S.A. Morton D.B. Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases.Genetics. 2010; 186: 183-196Crossref PubMed Scopus (39) Google Scholar). Thus, different Gycs sense different O2 environments. A common theme emerging from the studies of O2 sensation in C. elegans and Drosophila is that sensory cells respond to selective features of O2 in the environment. For C. elegans, one set of O2-sensing neurons responds to O2 increases and the other to O2 decreases in hyperoxic environments. For Drosophila, one set is necessary for hyperoxic avoidance, the other for hypoxic avoidance. These animals do not have a single class of O2-sensing neuron that responds best to a preferred concentration; instead, they have different sets of neurons to monitor changing concentrations or values above and below the preferred setpoint. The finding that animals use different receptors and cells tuned to different O2 concentrations is reminiscent to what is seen in mammalian thermosensation where different transient receptor potential ion channels respond best to different temperature ranges (Jordt et al., 2003Jordt S.E. McKemy D.D. Julius D. Lessons from peppers and peppermint: The molecular logic of thermosensation.Curr. Opin. Neurobiol. 2003; 13: 487-492Crossref PubMed Scopus (266) Google Scholar). By having some channels tuned for cool environments and others tuned for hot environments, animals can identify their preferred temperature and avoid thermal extremes. A similar strategy in O2 sensing may allow animals to resolve small variations in their environment and optimize their responses to changing conditions. In addition to monitoring atmospheric gases to maintain favorable environments, animals use long-range and short-range variations to extract information about predators, hosts, and food. CO2 detection may be useful to stay within a low CO2 environment or to detect a specific signal. In many cases, the biological relevance of CO2 detection is unknown, as all plants and animals emit CO2 during respiration. C. elegans show acute avoidance to CO2, avoiding levels as low as 0.5%–1% above ambient concentrations (Bretscher et al., 2008Bretscher A.J. Busch K.E. de Bono M. A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8044-8049Crossref PubMed Scopus (111) Google Scholar, Hallem and Sternberg, 2008Hallem E.A. Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8038-8043Crossref PubMed Scopus (130) Google Scholar). This avoidance is greatly reduced when BAG neurons are ablated (Hallem and Sternberg, 2008Hallem E.A. Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8038-8043Crossref PubMed Scopus (130) Google Scholar), arguing that the neurons that sense O2 decreases also sense CO2 increases. Avoidance requires the TAX-4 CNG channel (Bretscher et al., 2008Bretscher A.J. Busch K.E. de Bono M. A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8044-8049Crossref PubMed Scopus (111) Google Scholar, Hallem and Sternberg, 2008Hallem E.A. Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8038-8043Crossref PubMed Scopus (130) Google Scholar) but does not require GCY-31/33 (Hallem and Sternberg, 2008Hallem E.A. Sternberg P.W. Acute carbon dioxide avoidance in Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA. 2008; 105: 8038-8043Crossref PubMed Scopus (130) Google Scholar). Thus, CO2 sensing and O2 sensing may be partially mediated by BAG neurons through activation of the same CNG channels but different receptor mechanisms. The molecular sensors for CO2 detection in C. elegans are unknown. Mammals also sense CO2 in the environment. Recent studies of mammalian CO2 detection have provided insight into cellular and molecular mechanisms of detection. In mammals, CO2 is sensed by both the olfactory system and the gustatory system, demonstrating an unexpected complexity in detection (Figure 2). Although CO2 concentrations up to 30% are odorless to humans (Shusterman and Avila, 2003Shusterman D. Avila P.C. Real-time monitoring of nasal mucosal pH during carbon dioxide stimulation: Implications for stimulus dynamics.Chem. Senses. 2003; 28: 595-601Crossref PubMed Scopus (41) Google Scholar), mice smell CO2 and show innate avoidance at around 0.2% (Hu et al., 2007Hu J. Zhong C. Ding C. Chi Q. Walz A. Mombaerts P. Matsunami H. Luo M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse.Science. 2007; 317: 953-957Crossref PubMed Scopus (181) Google Scholar). Olfactory neurons have been identified that depolarize in response to CO2, with a detection threshold of 0.1%, consistent with the behavioral threshold (Hu et al., 2007Hu J. Zhong C. Ding C. Chi Q. Walz A. Mombaerts P. Matsunami H. Luo M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse.Science. 2007; 317: 953-957Crossref PubMed Scopus (181) Google Scholar). The olfactory neurons in mouse that respond to CO2 are different from most olfactory neurons. First, whereas most olfactory neurons express members of the odorant receptor family, an olfactory-specific G protein called Golf and adenylate cyclase, the CO2-sensing neurons express a unique complement of signaling molecules involved in CO2 detection (Fulle et al., 1995Fulle H.J. Vassar R. Foster D.C. Yang R.B. Axel R. Garbers D.L. A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons.Proc. Natl. Acad. Sci. USA. 1995; 92: 3571-3575Crossref PubMed Scopus (225) Google Scholar, Juilfs et al., 1997Juilfs D.M. Fulle H.J. Zhao A.Z. Houslay M.D. Garbers D.L. Beavo J.A. A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway.Proc. Natl. Acad. Sci. USA. 1997; 94: 3388-3395Crossref PubMed Scopus (260) Google Scholar, Meyer et al., 2000Meyer M.R. Angele A. Kremmer E. Kaupp U.B. Muller F. A cGMP-signaling pathway in a subset of olfactory sensory neurons.Proc. Natl. Acad. Sci. USA. 2000; 97: 10595-10600Crossref PubMed Scopus (131) Google Scholar, Hu et al., 2007Hu J. Zhong C. Ding C. Chi Q. Walz A. Mombaerts P. Matsunami H. Luo M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse.Science. 2007; 317: 953-957Crossref PubMed Scopus (181) Google Scholar). Second, these neurons show unusual axonal projection patterns in the first relay the olfactory bulb (Juilfs et al., 1997Juilfs D.M. Fulle H.J. Zhao A.Z. Houslay M.D. Garbers D.L. Beavo J.A. A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway.Proc. Natl. Acad. Sci. USA. 1997; 94: 3388-3395Crossref PubMed Scopus (260) Google Scholar). In general, olfactory neurons that express the same receptor project to a single glomerulus; CO2-sensing olfactory neurons target a string of caudal glomeruli called necklace glomeruli that are anatomically segregated from other olfactory projections. These differences suggest the CO2 detection system forms a distinct subsystem of the main olfactory system. The molecules specifically expressed in CO2 neurons provide insight into CO2 detection (Figure 2). A soluble carbonic anhydrase (CAII) and a receptor guanylate cyclase (GC-D) may couple CO2 detection to the production of the second messenger cGMP and cell depolarization (Fulle et al., 1995Fulle H.J. Vassar R. Foster D.C. Yang R.B. Axel R. Garbers D.L. A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons.Proc. Natl. Acad. Sci. USA. 1995; 92: 3571-3575Crossref PubMed Scopus (225) Google Scholar, Juilfs et al., 1997Juilfs D.M. Fulle H.J. Zhao A.Z. Houslay M.D. Garbers D.L. Beavo J.A. A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway.Proc. Natl. Acad. Sci. USA. 1997; 94: 3388-3395Crossref PubMed Scopus (260) Google Scholar, Hu et al., 2007Hu J. Zhong C. Ding C. Chi Q. Walz A. Mombaerts P. Matsunami H. Luo M. Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse.Science. 2007; 317: 953-957Crossref PubMed Scopus (181" @default.
• W1973464749 created "2016-06-24" @default.
• W1973464749 creator A5000276142 @default.
• W1973464749 date "2011-01-01" @default.
• W1973464749 modified "2023-10-11" @default.
• W1973464749 title "Out of Thin Air: Sensory Detection of Oxygen and Carbon Dioxide" @default.
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• W1973464749 doi "https://doi.org/10.1016/j.neuron.2010.12.018" @default.
• W1973464749 hasPubMedCentralId "https://www.ncbi.nlm.nih.gov/pmc/articles/3038919" @default.
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