Carbon dioxide-sensing in organisms and its implications for human disease

Cellular and Molecular Life Sciences

Volumn 71, Issue 5, 2014, Pages 831-845

  Cummins, Eoin P ^a   Selfridge, Andrew C ^a   Sporn, Peter H ^b   Sznajder, Jacob I ^b   Taylor, Cormac T ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Carbon dioxide (CO2); Hypercapnia; Immune regulation; NF kappaB; Physiological gases

Indexed keywords

ADAPTATION, BIOLOGICAL; ADENYLATE CYCLASE; ANIMALS; AQUAPORINS; CARBON DIOXIDE; CARBONIC ANHYDRASES; CHEMORECEPTOR CELLS; CONNEXINS; HUMANS; INFECTION; INFLAMMATION; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; RESPIRATION; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84893845005     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1470-6     Document Type: Review

References (135)

1. Taylor CT, McElwain JC (2010) Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. Physiology (Bethesda) 25(5):272-279
2. Monastersky R (2013) Global carbon dioxide levels near worrisome milestone. Nature 497(7447):13-14
3. Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30(4):393-402
4. Lopez-Barneo J et al (2008) Carotid body oxygen sensing. Eur Respir J Off J Eur Soc Clin Respir Physiol 32(5):1386-1398
5. Poulos T (2006) Soluble guanylate cyclase. Curr Opin Struct Biol 16(6):736-743
6. Cooper GM (2000) The cell: a molecular approach, 2nd edn. In: Transport of small molecules. Sinauer Associates, Sunderland
7. 2channels? J Exp Zool A Ecol Genet Physiol 313(9):618-621
8. Missner A et al (2008) Carbon dioxide transport through membranes. J Biol Chem 283(37):25340-25347
9. Hachez C, Chaumont F (2010) Aquaporins: a family of highly regulated multifunctional channels. Adv Exp Med Biol 679:1-17
10. 3selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci USA 106(13):5406-5411
11. 2pore with physiological functions. Nature 425(6959):734-737
12. 2permeability of Xenopus oocytes. Am J Physiol 274 (2 Pt 1):C543-C548
13. Yang B et al (2000) Carbon dioxide permeability of aquaporin-1 measured in erythrocytes and lung of aquaporin-1 null mice and in reconstituted proteoliposomes. J Biol Chem 275(4):2686-2692
14. 2channels. Chemphyschem Eur J Chem Phys Phys Chem 12(5):1017-1019
15. Kaplan A, Lieman-Hurwitz J, Tchernov D (2004) Resolving the biological role of the Rhesus (Rh) proteins of red blood cells with the aid of a green alga. Proc Natl Acad Sci USA 101(20):7497-7498
16. Soupene E et al (2002) Rhesus expression in a green alga is regulated by CO (2). Proc Natl Acad Sci USA 99(11):7769-7773
17. Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212 (Pt 15):2303-2312
18. 2channels. Transfus Clin Biol 13 (1-2):103-110
19. 2. Biophys J 73(2):798-806
20. Dean JB et al (2002) Role of gap junctions in CO (2) chemoreception and respiratory control. Am J Physiol Lung Cell Mol Physiol 283(4):L665-L670
21. Solomon IC et al (2001) Localization of connexin26 and connexin32 in putative CO (2)-chemosensitive brainstem regions in rat. Respir Physiol 129 (1-2):101-121
22. 2-dependent opening of connexin 26 and related beta connexins. J Physiol 588 (Pt 20):3921-3931
23. 2responsive regulon in Bordetella. PLoS ONE 7(10):e47635
24. Skinner JA et al (2004) Bordetella type III secretion and adenylate cyclase toxin synergize to drive dendritic cells into a semimature state. J Immunol 173(3):1934-1940
25. 2-bicarbonate and aerobic atmospheres. PLoS ONE 4(3):e4904
26. Bongiorni C et al (2008) Dual promoters control expression of the Bacillus anthracis virulence factor AtxA. J Bacteriol 190(19):6483-6492
27. Gohar M et al (2008) The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3(7):e2793
28. Gilmore RD Jr, Mbow ML, Stevenson B (2001) Analysis of Borrelia burgdorferi gene expression during life cycle phases of the tick vector Ixodes scapularis. Microbes Infect 3(10):799-808
29. 2levels. J Bacteriol 189(2):437-445
30. Shimamura T, Watanabe S, Sasaki S (1985) Enhancement of enterotoxin production by carbon dioxide in Vibrio cholerae. Infect Immun 49(2):455-456
31. Abuaita BH, Withey JH (2009) Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 77(9):4111-4120
32. Lotlikar S et al (2013) Three functional β-carbonic anhydrases in P. aeruginosa PAO1. Role in survival in ambient air. Microbiology (Reading, England) (in press)
33. Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59(7):1615-1624
34. 2-controlled stomatal movements in guard cells. Nat Cell Biol 12(1):87-93
35. 2signal transduction in guard cell. EMBO J 30(8):1645-1658
36. 2mmon sense. Science 327(5963):275-276
37. 2+ signaling. Annu Rev Plant Biol 61:561-591
38. Young J et al (2006) CO (2) signaling in guard cells: calcium sensitivity response modulation, a Ca (2+)-independent phase, and CO (2) insensitivity of the gca2 mutant. Proc Natl Acad Sci USA 103(19):7506-7511
39. 2sensing in the human fungal pathogen Candida albicans. Mol Biol Cell 23(14):2692-2701
40. Hall RA et al (2010) CO (2) acts as a signalling molecule in populations of the fungal pathogen Candida albicans. PLoS Pathog 6(11):e1001193
41. Kadosh D, Johnson AD (2001) Rfg1, a protein related to the Saccharomyces cerevisiae hypoxic regulator Rox1, controls filamentous growth and virulence in Candida albicans. Mol Cell Biol 21(7):2496-2505
42. Allen AM, King RD (1978) Occlusion, carbon dioxide, and fungal skin infections. Lancet 1(8060):360-362
43. Huang G et al (2009) CO (2) regulates white-to-opaque switching in Candida albicans. Curr Biol 19(4):330-334
44. 2through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5(1):103-111
45. 2sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr Biol 15(22):2013-2020
46. Granger DL, Perfect JR, Durack DT (1985) Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. J Clin Invest 76(2):508-516
47. Zaragoza O, Fries BC, Casadevall A (2003) Induction of capsule growth in Cryptococcus neoformans by mammalian serum and CO (2). Infect Immun 71(11):6155-6164
48. Ravi S et al (2009) Biofilm formation by Cryptococcus neoformans under distinct environmental conditions. Mycopathologia 167(6):307-314
49. 2sensing in fungi and beyond. Curr Opin Microbiol 9(6):572-578
50. Elleuche S, Poggeler S (2010) Carbonic anhydrases in fungi. Microbiology 156 (Pt 1):23-29
51. 2sensing with cAMP signaling and virulence. Curr Biol 15(22):2021-2026
52. Hallem EA, Sternberg PW (2008) Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci USA 105(23):8038-8043
53. Guillermin ML, Castelletto ML, Hallem EA (2011) Differentiation of carbon dioxide-sensing neurons in Caenorhabditis elegans requires the ETS-5 transcription factor. Genetics 189(4):1327-1339
54. Hallem E et al (2011) Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proc Natl Acad Sci USA 108(1):254-259
55. Hallem E et al (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21(5):377-383
56. Bretscher A et al (2011) Temperature, oxygen, and salt-sensing neurons in C. elegans are carbon dioxide sensors that control avoidance behavior. Neuron 69(6):1099-1113
57. 2levels affect development, motility, and fertility and extend life span in Caenorhabditis elegans. Proc Natl Acad Sci USA 106(10):4024-4029
58. Stange G, Stowe S (1999) Carbon-dioxide sensing structures in terrestrial arthropods. Microsc Res Tech 47(6):416-427
59. Jones WD et al (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445(7123):86-90
60. Dekker T, Geier M, Cardé R (2005) Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 208 (Pt 15):2963-2972
61. 2-sensing neurons disorients mosquitoes. Nature 474(7349):87-91
62. Robertson HM, Kent LB (2009) Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J Insect Sci 9:19
63. Suh G et al (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431(7010):854-859
64. Wasserman S, Salomon A, Frye M (2013) Drosophila tracks carbon dioxide in flight. Curr Biol 23 (Pt 4):301-306
65. Suver M, Mamiya A, Dickinson M (2012) Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr Biol 22(24):2294-2302
66. 2suppresses specific Drosophila innate immune responses and resistance to bacterial infection. Proc Natl Acad Sci USA 106(44):18710-18715
67. Roelofs J, Van Haastert P (2002) Deducing the origin of soluble adenylyl cyclase, a gene lost in multiple lineages. Mol Biol Evol 19(12):2239-2246
68. Perry S, Abdallah S (2012) Mechanisms and consequences of carbon dioxide sensing in fish. Respir Physiol Neurobiol 184(3):309-315
69. 2. J Physiol 588 (Pt 5):861-872
70. 2levels on coral reef fishes: what hope for the future? J Exp Biol 215 (Pt 22):3865-3873
71. 2chemosensitivity-towards a better understanding of mechanism. J Physiol 589 (Pt 23):5561-5579
72. 2during eupneic breathing. Adv Exp Med Biol 605:322-326
73. Nattie E, Forster H (2010) Special issue on central chemoreception. Foreword. Respir Physiol Neurobiol 173(3):193-194
74. Blain G et al (2010) Peripheral chemoreceptors determine the respiratory sensitivity of central chemoreceptors to CO (2). J Physiol 588 (Pt 13):2455-2471
75. Haldane J, Priestley J (1905) The regulation of the lung-ventilation. J Physiol 32 (3-4):225-266
76. Ramanantsoa N et al (2011) Breathing without CO (2) chemosensitivity in conditional Phox2b mutants. J Neurosci Off J Soc Neurosci 31(36):12880-12888
77. 2levels impair alveolar epithelial function independently of pH. PLoS One 2 (Pt 11):e1238
78. 2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na, K-ATPase endocytosis. J Clin Investig 118(2):752-762
79. Welch L et al (2010) Extracellular signal-regulated kinase (ERK) participates in the hypercapnia-induced Na, K-ATPase downregulation. FEBS Lett 584(18):3985-3989
80. 2-induced epithelial dysfunction. PLoS One 7(10):e46696
81. 2levels. Am J Respir Cell Mol Biol 48 (Pt 5):626-634
82. Chen J et al (2008) Carbonic anhydrase II and alveolar fluid reabsorption during hypercapnia. Am J Respir Cell Mol Biol 38(1):32-37
83. 2by an olfactory subsystem in the mouse. Science 317(5840):953-957
84. 2neurons is activated by bicarbonate. Proc Natl Acad Sci USA 106(6):2041-2046
85. Chandrashekar J et al (2009) The taste of carbonation. Science (N Y) 326(5951):443-445
86. 2levels cause mitochondrial dysfunction and impair cell proliferation. J Biol Chem 286 (Pt 43):37067-37076
87. O'Toole D et al (2009) Hypercapnic acidosis attenuates pulmonary epithelial wound repair by an NF-kappaB-dependent mechanism. Thorax 64(11):976-982
88. Jaitovich A D L, Welch L, Gusorava GA, Sznajder JI (2012) Role of AMP-activated protein kinase (AMPK) in hypercapniainduced muscle atrophy. Am J Respir Crit Care Med 185:A2013
89. West MA et al (1997) Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgery. Ann Surg 226(2):179-190
90. 2on LPS-induced cytokine responses in rat alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 289(1):L96-L103
91. 2selectively inhibits interleukin-6 and tumor necrosis factor expression and decreases phagocytosis in the macrophage. FASEB J 24(7):2178-2190
92. Hayden MS, Ghosh S (2012) NF-kappaB, the first quartercentury: remarkable progress and outstanding questions. Genes Dev 26(3):203-234
93. Takeshita K et al (2003) Hypercapnic acidosis attenuates endotoxininduced nuclear factor-[kappa]B activation. Am J Respir Cell Mol Biol 29(1):124-132
94. Abolhassani M et al (2009) Carbon dioxide inhalation causes pulmonary inflammation. Am J Physiol Lung Cell Mol Physiol 296(4):L657-L665
95. Li AM et al (2010) Effects of therapeutic hypercapnia on inflammation and apoptosis after hepatic ischemia.reperfusion injury in rats. Chin Med J (Engl) 123(16):2254-2258
96. 2sensing and signaling. J Biol Chem 287(17):14004-14011
97. 2sensing to innate immunity and inflammation in mammalian cells. J Immunol 185(7):4439-4445
98. Taylor CT, Cummins EP (2011) Regulation of gene expression by carbon dioxide. J Physiol 589 (Pt 4):797-803
99. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148(3):399-408
100. Greer SN et al (2012) The updated biology of hypoxia-inducible factor. EMBO J 31(11):2448-2460
101. Broccard AF et al (2001) Protective effects of hypercapnic acidosis on ventilator-induced lung injury. Am J Respir Crit Care Med 164(5):802-806
102. Sinclair SE et al (2002) Hypercapnic acidosis is protective in an in vivo model of ventilator-induced lung injury. Am J Respir Crit Care Med 166(3):403-408
103. Laffey JG et al (2004) Hypercapnic acidosis attenuates endotoxininduced acute lung injury. Am J Respir Crit Care Med 169(1):46-56
104. O'Croinin DF et al (2005) Hypercapnic acidosis does not modulate the severity of bacterial pneumonia-induced lung injury. Crit Care Med 33(11):2606-2612
105. O'Croinin DF et al (2008) Sustained hypercapnic acidosis during pulmonary infection increases bacterial load and worsens lung injury. Crit Care Med 36(7):2128-2135
106. Chonghaile MN et al (2008) Hypercapnic acidosis attenuates lung injury induced by established bacterial pneumonia. Anesthesiology 109(5):837-848
107. Nichol AD et al (2009) Infection-induced lung injury is worsened after renal buffering of hypercapnic acidosis. Crit Care Med 37(11):2953-2961
108. Ni Chonghaile M et al (2008) Hypercapnic acidosis attenuates severe acute bacterial pneumonia-induced lung injury by a neutrophil-independent mechanism. Crit Care Med 36(12):3135-3144
109. Gates KL et al (2013) Hypercapnia impairs lung neutrophil function and increases mortality in murine Pseudomonas Pneumonia. Am J Respir Cell Mol Biol (in press)
110. Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74(1):1-20
111. Lindskog S, Coleman J (1973) The catalytic mechanism of carbonic anhydrase. Proc Natl Acad Sci USA 70(9):2505-2508
112. Aggarwal M et al (2013) Structural annotation of human carbonic anhydrases. J Enzyme Inhib Med Chem 28(2):267-277
113. Kamenetsky M et al (2006) Molecular details of cAMP generation in mammalian cells: a tale of two systems. J Mol Biol 362(4):623-639
114. Gehring C (2010) Adenyl cyclases and cAMP in plant signaling. past and present. Cell Commun Signal 8:15
115. Sassone-Corsi P (2012) The cyclic AMP pathway. Cold Spring Harb Perspect Biol 4 (Pt 12):a011148
116. Cook Z, Gray M, Cann M (2012) Elevated carbon dioxide blunts mammalian cAMP signaling dependent on inositol 1, 4, 5-triphosphate receptor-mediated Ca2+ release. J Biol Chem 287(31):26291-26301
117. Townsend P et al (2009) Stimulation of mammalian G-proteinresponsive adenylyl cyclases by carbon dioxide. J Biol Chem 284(2):784-791
118. Buck J, Levin L (2011) Physiological sensing of carbon dioxide/bicarbonate/pH via cyclic nucleotide signaling. Sensors (Basel, Switzerland) 11(2):2112-2128
119. Chen Y et al (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science (N Y) 289(5479):625-628
120. Moser KM, Shibel EM, Beamon AJ (1973) Acute respiratory failure in obstructive lung disease. Long-term survival after treatment in an intensive care unit. JAMA 225(7):705-707
121. Martin TR, Lewis SW, Albert RK (1982) The prognosis of patients with chronic obstructive pulmonary disease after hospitalization for acute respiratory failure. Chest 82(3):310-314
122. Goel A, Pinckney RG, Littenberg B (2003) APACHE II predicts long-term survival in COPD patients admitted to a general medical ward. J Gen Intern Med 18(10):824-830
123. Groenewegen KH, Schols AM, Wouters EF (2003) Mortality and mortality-related factors after hospitalization for acute exacerbation of COPD. Chest 124(2):459-467
124. Sin DD, Man SF, Marrie TJ (2005) Arterial carbon dioxide tension on admission as a marker of in-hospital mortality in communityacquired pneumonia. Am J Med 118(2):145-150
125. Laserna E et al (2012) Hypocapnia and hypercapnia are predictors for ICU admission and mortality in hospitalized patients with community-acquired pneumonia. Chest 142(5):1193-1199
126. Belkin RA et al (2006) Risk factors for death of patients with cystic fibrosis awaiting lung transplantation. Am J Respir Crit Care Med 173(6):659-666
127. Dreyfuss D et al (1988) High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Respir Dis 137(5):1159-1164
128. Corbridge TC et al (1990) Adverse effects of large tidal volume and low PEEP in canine acid aspiration. Am Rev Respir Dis 142(2):311-315
129. Amato MB et al (1998) Effect of a protective-ventilation strategy on mortality in the acute respiratory distress syndrome. N Engl J Med 338(6):347-354
130. ARDSnet (2000) Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 342(18):1301-1308
131. Laffey JG, Kavanagh BP (1999) Carbon dioxide and the critically ill-too little of a good thing? Lancet 354(9186):1283-1286
132. Curley GF, Laffey JG, Kavanagh BP (2013) CrossTalk proposal: there is added benefit to providing permissive hypercapnia in the treatment of ARDS. J Physiol 591 (Pt 11):2763-2765
133. Curley GF, Laffey JG, Kavanagh BP (2013) Rebuttal from Gerard F. Curley, John G. Laffey and Brian P. Kavanagh. J Physiol 591 (Pt 11):2771-2772
134. Beitler JR, Hubmayr RD, Malhotra A (2013) CrossTalk opposing view: there is not added benefit to providing permissive hypercapnia in the treatment of ARDS. J Physiol 591 (Pt 11):2767-2769
135. Beitler JR, Hubmayr RD, Malhotra A (2013) Rebuttal from Jeremy R. Beitler, Rolf D. Hubmayr and Atul Malhotra. J Physiol 591 (Pt 11):2773