The neurobiology of sensing respiratory gases for the control of animal behavior
Dengke K. MA, Niels RINGSTAD
The neurobiology of sensing respiratory gases for the control of animal behavior
Aerobic metabolism is fundamental for almost all animal life. Cellular consumption of oxygen (O2) and production of carbon dioxide (CO2) signal metabolic states and physiologic stresses. These respiratory gases are also detected as environmental cues that can signal external food quality and the presence of prey, predators and mates. In both contexts, animal nervous systems are endowed with mechanisms for sensing O2/CO2 to trigger appropriate behaviors and maintain homeostasis of internal O2/CO2. Although different animal species show different behavioral responses to O2/CO2, some underlying molecular mechanisms and pathways that function in the detection of respiratory gases are fundamentally similar and evolutionarily conserved. Studies of Caenorhabditis elegans and Drosophila melanogaster have identified roles for cyclic nucleotide signaling and the hypoxia inducible factor (HIF) transcriptional pathway in mediating behavioral responses to respiratory gases. Understanding how simple invertebrate nervous systems detect respiratory gases to control behavior might reveal general principles common to nematodes, insects and vertebrates that function in the molecular sensing of respiratory gases and the neural control of animal behaviors.
oxygen / carbon dioxide / C. elegans / Drosophila / respiratory gases / animal behaviors
[1] |
Anderson J F, Ultsch G R (1987). Respiratory gas concentrations in the microhabitats of some Florida arthropods. Comp Biochem Physiol Part A Physiol, 88(3): 585-588
CrossRef
Google scholar
|
[2] |
Bargmann C I, Hartwieg E, Horvitz H R (1993). Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell, 74(3): 515-527
CrossRef
Pubmed
Google scholar
|
[3] |
Bickler P E, Donohoe P H (2002). Adaptive responses of vertebrate neurons to hypoxia. J Exp Biol, 205(Pt 23): 3579-3586
Pubmed
|
[4] |
Brandt J P, Aziz-Zaman S, Juozaityte V, Martinez-Velazquez L A, Petersen J G, Pocock R, Ringstad N (2012). A single gene target of an ETS-family transcription factor determines neuronal CO2-chemosensitivity. PLoS ONE, (In press)
|
[5] |
Bretscher A J, Busch K E, de Bono M (2008). A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc Natl Acad Sci USA, 105(23): 8044-8049
CrossRef
Pubmed
Google scholar
|
[6] |
Chandrashekar J, Yarmolinsky D, von Buchholtz L, Oka Y, Sly W, Ryba N J, Zuker C S (2009). The taste of carbonation. Science, 326(5951): 443-445
CrossRef
Pubmed
Google scholar
|
[7] |
Chang A J, Bargmann C I (2008). Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans. Proc Natl Acad Sci USA, 105(20): 7321-7326
CrossRef
Pubmed
Google scholar
|
[8] |
Ehrismann D, Flashman E, Genn D N, Mathioudakis N, Hewitson K S, Ratcliffe P J, Schofield C J (2007). Studies on the activity of the hypoxia-inducible-factor hydroxylases using an oxygen consumption assay. Biochem J, 401(1): 227-234
CrossRef
Pubmed
Google scholar
|
[9] |
Epstein A C, Gleadle J M, McNeill L A, Hewitson K S, O’Rourke J, Mole D R, Mukherji M, Metzen E, Wilson M I, Dhanda A, Tian Y M, Masson N, Hamilton D L, Jaakkola P, Barstead R, Hodgkin J, Maxwell P H, Pugh C W, Schofield C J, Ratcliffe P J (2001). C. elegansEGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell, 107(1): 43-54
CrossRef
Pubmed
Google scholar
|
[10] |
Félix M A, Braendle C (2010). The natural history of Caenorhabditis elegans. Curr Biol, 20(22): R965-R969
CrossRef
Pubmed
Google scholar
|
[11] |
Fischler W, Kong P, Marella S, Scott K (2007). The detection of carbonation by the Drosophila gustatory system. Nature, 448(7157): 1054-1057
CrossRef
Pubmed
Google scholar
|
[12] |
Gourine A V, Kasymov V, Marina N, Tang F, Figueiredo M F, Lane S, Teschemacher A G, Spyer K M, Deisseroth K, Kasparov S (2010). Astrocytes control breathing through pH-dependent release of ATP. Science, 329(5991): 571-575
CrossRef
Pubmed
Google scholar
|
[13] |
Gourine A V, Llaudet E, Dale N, Spyer K M (2005). ATP is a mediator of chemosensory transduction in the central nervous system. Nature, 436(7047): 108-111
CrossRef
Pubmed
Google scholar
|
[14] |
Gray J M, Karow D S, Lu H, Chang A J, Chang J S, Ellis R E, Marletta M A, Bargmann C I (2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature, 430(6997): 317-322
CrossRef
Pubmed
Google scholar
|
[15] |
Guerenstein P G, Hildebrand J G (2008). Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol, 53(1): 161-178
CrossRef
Pubmed
Google scholar
|
[16] |
Guillermin M L, Castelletto M L, Hallem E A (2011). Differentiation of carbon dioxide-sensing neurons in Caenorhabditis elegans requires the ETS-5 transcription factor. Genetics, 189(4): 1327-1339
CrossRef
Pubmed
Google scholar
|
[17] |
Guo D, Zhang J J, Huang X Y (2009). Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry, 48(20): 4417-4422
CrossRef
Pubmed
Google scholar
|
[18] |
Hallem E A, Spencer W C, McWhirter R D, Zeller G, Henz S R, Rätsch G, Miller D M 3rd, Horvitz H R, Sternberg P W, Ringstad N (2011). Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proc Natl Acad Sci USA, 108(1): 254-259
CrossRef
Pubmed
Google scholar
|
[19] |
Hallem E A, Sternberg P W (2008). Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci USA, 105(23): 8038-8043
CrossRef
Pubmed
Google scholar
|
[20] |
Hendricks T, Francis N, Fyodorov D, Deneris E S (1999). The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci, 19(23): 10348-10356
Pubmed
|
[21] |
Hodges M R, Tattersall G J, Harris M B, McEvoy S D, Richerson D N, Deneris E S, Johnson R L, Chen Z F, Richerson G B (2008). Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci, 28(10): 2495-2505
CrossRef
Pubmed
Google scholar
|
[22] |
Hu J, Zhong C, Ding C, Chi Q, Walz A, Mombaerts P, Matsunami H, Luo M (2007). Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science, 317(5840): 953-957
CrossRef
Pubmed
Google scholar
|
[23] |
Huang S H, Rio D C, Marletta M A (2007). Ligand binding and inhibition of an oxygen-sensitive soluble guanylate cyclase, Gyc-88E, from Drosophila. Biochemistry, 46(51): 15115-15122
CrossRef
Pubmed
Google scholar
|
[24] |
Jones W D, Cayirlioglu P, Kadow I G, Vosshall L B (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature, 445(7123): 86-90
CrossRef
Pubmed
Google scholar
|
[25] |
Kimura H (2010). Hydrogen sulfide: from brain to gut. Antioxid Redox Signal, 12(9): 1111-1123
CrossRef
Pubmed
Google scholar
|
[26] |
Klein D F (1993). False suffocation alarms, spontaneous panics, and related conditions. An integrative hypothesis. Arch Gen Psychiatry, 50(4): 306-317
CrossRef
Pubmed
Google scholar
|
[27] |
Lenton T M T (2003). The Coupled Evolution of Life and Atmospheric Oxygen. Amsterdam: Elsevier Science
|
[28] |
Li Q, Sun B, Wang X, Jin Z, Zhou Y, Dong L, Jiang L H, Rong W (2010). A crucial role for hydrogen sulfide in oxygen sensing via modulating large conductance calcium-activated potassium channels. Antioxid Redox Signal, 12(10): 1179-1189
CrossRef
Pubmed
Google scholar
|
[29] |
Loenarz C, Coleman M L, Boleininger A, Schierwater B, Holland P W, Ratcliffe P J, Schofield C J (2011). The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep, 12(1): 63-70
CrossRef
Pubmed
Google scholar
|
[30] |
Luo M, Sun L, Hu J (2009). Neural detection of gases—carbon dioxide, oxygen—in vertebrates and invertebrates. Curr Opin Neurobiol, 19(4): 354-361
CrossRef
Pubmed
Google scholar
|
[31] |
Ma D K, Vozdek R, Bhatla N, Horvitz H R (2012). CYSL-1 Interacts with the O2-sensing Hydroxylase EGL-9 to Promote H2S-modulated Hypoxia-induced behavioral plasticity in C. elegans. Neuron, 73(5): 925-940
CrossRef
Google scholar
|
[32] |
Maina J N (1998). The Gas Exchangers: Structure, Function, and Evolution of the Respiratory Processes. Berlin: Springer
|
[33] |
McGrath P T, Rockman M V, Zimmer M, Jang H, Macosko E Z, Kruglyak L, Bargmann C I (2009). Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron, 61(5): 692-699
CrossRef
Pubmed
Google scholar
|
[34] |
Morton D B (2004). Atypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors. J Biol Chem, 279(49): 50651-50653
CrossRef
Pubmed
Google scholar
|
[35] |
Morton D B (2011). Behavioral responses to hypoxia and hyperoxia in Drosophila larvae: molecular and neuronal sensors. Fly (Austin), 5(2): 119-125
Pubmed
|
[36] |
Olson K R (2011a). Hydrogen sulfide is an oxygen sensor in the carotid body. Respir Physiol Neurobiol, 179(2-3): 103-110
CrossRef
Pubmed
Google scholar
|
[37] |
Olson K R (2011b). The therapeutic potential of hydrogen sulfide: separating hype from hope. Am J Physiol Regul Integr Comp Physiol, 301(20): R297-R312
CrossRef
Pubmed
Google scholar
|
[38] |
Olson K R, Dombkowski R A, Russell M J, Doellman M M, Head S K, Whitfield N L, Madden J A (2006). Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J Exp Biol, 209(Pt 20): 4011-4023
CrossRef
Pubmed
Google scholar
|
[39] |
Olson K R, Whitfield N L (2010). Hydrogen sulfide and oxygen sensing in the cardiovascular system. Antioxid Redox Signal, 12(10): 1219-1234
CrossRef
Pubmed
Google scholar
|
[40] |
Padilla P A, Nystul T G, Zager R A, Johnson A C, Roth M B (2002). Dephosphorylation of cell cycle-regulated proteins correlates with anoxia-induced suspended animation in Caenorhabditis elegans. Mol Biol Cell, 13(5): 1473-1483
CrossRef
Pubmed
Google scholar
|
[41] |
Papp L A, Klein D F, Gorman J M (1993). Carbon dioxide hypersensitivity, hyperventilation, and panic disorder. Am J Psychiatry, 150(8): 1149-1157
Pubmed
|
[42] |
Peng Y J, Nanduri J, Raghuraman G, Souvannakitti D, Gadalla M M, Kumar G K, Snyder S H, Prabhakar N R (2010). H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci USA, 107(23): 10719-10724
CrossRef
Pubmed
Google scholar
|
[43] |
Persson A, Gross E, Laurent P, Busch K E, Bretes H, de Bono M (2009). Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans. Nature, 458(7241): 1030-1033
CrossRef
Pubmed
Google scholar
|
[44] |
Pocock R, Hobert O (2010). Hypoxia activates a latent circuit for processing gustatory information in C. elegans. Nat Neurosci, 13(5): 610-614
CrossRef
Pubmed
Google scholar
|
[45] |
Potter L R (2011). Guanylyl cyclase structure, function and regulation. Cell Signal, 23(12): 1921-1926
CrossRef
Pubmed
Google scholar
|
[46] |
Powell-Coffman J A (2010). Hypoxia signaling and resistance in C. elegans. Trends Endocrinol Metab, 21(7): 435-440
CrossRef
Pubmed
Google scholar
|
[47] |
Prabhakar N R (2005). O2 sensing at the mammalian carotid body: why multiple O2 sensors and multiple transmitters? Exp Physiol, 91(1): 17-23
CrossRef
Pubmed
Google scholar
|
[48] |
Quaegebeur A, Carmeliet P (2010). Oxygen sensing: a common crossroad in cancer and neurodegeneration. Curr Top Microbiol Immunol, 345: 71-103
CrossRef
Pubmed
Google scholar
|
[49] |
Ray R S, Corcoran A E, Brust R D, Kim J C, Richerson G B, Nattie E, Dymecki S M (2011). Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science, 333(6042): 637-642
CrossRef
Pubmed
Google scholar
|
[50] |
Richerson G B (2004). Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci, 5(6): 449-461
CrossRef
Pubmed
Google scholar
|
[51] |
Scott K (2011). Out of thin air: sensory detection of oxygen and carbon dioxide. Neuron, 69(2): 194-202
CrossRef
Pubmed
Google scholar
|
[52] |
Semenza G L (2011a). Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta, 1813(7): 1263-1268
CrossRef
Pubmed
Google scholar
|
[53] |
Semenza G L (2011b). Oxygen sensing, homeostasis, and disease. N Engl J Med, 365(6): 537-547
CrossRef
Pubmed
Google scholar
|
[54] |
Singh S, Padovani D, Leslie R A, Chiku T, Banerjee R (2009). Relative contributions of cystathionine beta-synthase and gamma-cystathionase to H2S biogenesis via alternative trans-sulfuration reactions. J Biol Chem, 284(33): 22457-22466
CrossRef
Pubmed
Google scholar
|
[55] |
Spyer K M (2009). To breathe or not to breathe? That is the question. Exp Physiol, 94(1): 1-10
CrossRef
Pubmed
Google scholar
|
[56] |
Suh G S, Wong A M, Hergarden A C, Wang J W, Simon A F, Benzer S, Axel R, Anderson D J (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature, 431(7010): 854-859
CrossRef
Pubmed
Google scholar
|
[57] |
Sun L, Wang H, Hu J, Han J, Matsunami H, Luo M (2009). Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate. Proc Natl Acad Sci USA, 106(6): 2041-2046
CrossRef
Pubmed
Google scholar
|
[58] |
Teppema L J, Dahan A (2010). The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiol Rev, 90(2): 675-754
CrossRef
Pubmed
Google scholar
|
[59] |
Vermehren-Schmaedick A, Ainsley J A, Johnson W A, Davies S A, Morton D B (2010). Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics, 186(1): 183-196
CrossRef
Pubmed
Google scholar
|
[60] |
Vozdek R, Hnizda A, Krijt J, Kostrouchova M, Kozich V (2012). Novel structural arrangement of nematode cystathionine beta-synthases: characterization of Caenorhabditis elegans CBS-1. Biochem J, Available online 13 Jan 2012
|
[61] |
Ward J P (2008). Oxygen sensors in context. Biochim Biophys Acta, 1777(1): 1-14
CrossRef
Pubmed
Google scholar
|
[62] |
Yu S, Avery L, Baude E, Garbers D L (1997). Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci USA, 94(7): 3384-3387
CrossRef
Pubmed
Google scholar
|
[63] |
Ziemann A E, Allen J E, Dahdaleh N S, Drebot I I, Coryell M W, Wunsch A M, Lynch C M, Faraci F M, Howard M A 3rd, Welsh M J, Wemmie J A (2009). The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell, 139(5): 1012-1021
CrossRef
Pubmed
Google scholar
|
[64] |
ZimmerM, GrayJ M, PokalaN, ChangA J, KarowD S, MarlettaM A, HudsonM L, MortonD B, ChronisN, BargmannC I(2009). Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron, 61(6): 865-879
CrossRef
Pubmed
Google scholar
|
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