A revisit to O2 sensing and transduction in the carotid body chemoreceptors in the context of reactive oxygen species biology

Respiratory Physiology and Neurobiology

Volumn 174, Issue 3, 2010, Pages 317-330

  Gonzalez, C ^a   Agapito, M T ^a   Rocher, A ^a   Gomez Nino A ^a   Rigual, R ^a   Castaneda J ^a   Conde, S V ^a   Obeso, A ^a  

^a UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

Oxygen sensing; Sensor; Transducer; Transduction

Indexed keywords

ACETYLCYSTEINE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; POTASSIUM CHANNEL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; ROTENONE; SMALL INTERFERING RNA; SODIUM AZIDE; OXYGEN;

ADRENAL MEDULLA; BIOSYNTHESIS; CAROTID BODY CHEMORECEPTOR; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; CHROMAFFIN CELL; ELECTRON TRANSPORT; HUMAN; HYPOXIA; KIDNEY; LUNG ARTERY; MITOCHONDRION; NEUROTRANSMISSION; NONHUMAN; OXIDATION REDUCTION REACTION; OXYGEN SENSING; OXYGEN TENSION; POTASSIUM CURRENT; PRIORITY JOURNAL; REVIEW; SENSOR; ANIMAL; CAROTID BODY; CHEMORECEPTOR; CYTOLOGY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CAROTID BODY; CHEMORECEPTOR CELLS; HUMANS; OXYGEN; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 78449293812     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2010.09.002     Document Type: Review

References (137)

1. 2. Pflügers Arch. 1971, 329:136-155.
2. Acker H., Lübbers D.W. Relationship between local flow, tissue PO2, and total flow of the cat carotid body. Chemoreception in the Carotid Body 1977, 271-276. Springer-Verlag, Berlin. H. Acker, S. Fidone, D. Pallot, C. Eyzaguirre, D.W. Lübbers, R.W. Torrance (Eds.).
3. Agapito M.T., Sanz-Alfayate G., Gomez-Niño A., Gonzalez C., Obeso A. General redox environment and carotid body chemoreceptor function. Am. J. Physiol. Cell Physiol. 2009, 296:C620-C631.
4. Aldieri E., Riganti C., Polimeni M., Gazzano E., Lussiana C., Campia I., Ghigo D. Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr. Drug Metab. 2008, 9:686-696.
5. 3H]dopamine from the cat carotid body in vitro. J. Physiol. 1986, 379:293-307.
6. 2+] in the endoplasmic reticulum with aequorin. Cell Calcium 2002, 32:251-260.
7. 2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7944-7949.
8. 2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am. J. Physiol. Heart Circ. Physiol. 2008, 294(February (2)):H570-H578.
9. Armitage M.E., Wingler K., Schmidt H.H. Translating the oxidative stress hypothesis into the clinic: NOX versus NOS. J. Mol. Med. 2009, 87:1071-1076.
10. Basuroy S., Bhattacharya S., Leffler C.W., Parfenova H. Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-alpha in cerebral vascular endothelial cells. Am. J. Physiol. Cell Physiol. 2009, 296:C422-432.
11. Biscoe T.J., Purves M.J., Sampson S.R. The frequency of nerve impulses in single carotid body chemoreceptor afferent fibres recorded in vivo with intact circulation. J. Physiol. 1970, 208:121-131.
12. Borowsky I.W., Collins R.C. Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities. J. Comp. Neurol. 1989, 15(288):401-413.
13. Brazier S.P., Telezhkin V., Mears R., Müller C.T., Riccardi D., Kemp P.J. Cysteine residues in the C-terminal tail of the human BK(Ca)alpha subunit are important for channel sensitivity to carbon monoxide. Adv. Exp. Med. Biol. 2009, 648:49-56.
14. Brown D.I., Griendling K.K. Nox proteins in signal transduction. Free. Radic. Biol. Med. 2009, 47:1239-1253.
15. Buckler K.J. A novel oxygen-sensitive potassium current in rat carotid body type I cells. J. Physiol. 1997, 498:649-662.
16. Cantó C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
17. Carreras M.C., Poderoso J.J. Mitochondrial nitric oxide in the signaling of cell integrated responses. Am. J. Physiol. Cell Physiol. 2007, 292:C1569-1580.
18. Chandel N.S., Schumacker P.T. Cellular oxygen sensing by mitochondria: old questions, new insight. J. Appl. Physiol. 2000, 88:1880-1889.
19. Chandel N.S., McClintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., Schumacker P.T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 2000, 275:25130-25138.
20. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11715-11720.
21. Coburn R.F., Forman H.J. Carbon monoxide toxicity. Handbook of Physiology, Section 3. Respiratory System, Vol. 4. Gas Exchange 1987, 439-456. Am. Physiol. Soc., Bethesda, MD. L.E. Farhi, S.M. Tenney (Eds.).
22. Cogolludo A., Moreno L., Frazziano G., Moral-Sanz J., Menendez C., Castañeda J., González C., Villamor E., Perez-Vizcaino F. Activation of neutral sphingomyelinase is involved in acute hypoxic pulmonary vasoconstriction. Cardiovasc. Res. 2009, 82:296-302.
23. Conde S.V., Monteiro E.C., Obeso A., Gonzalez C. Adenosine in peripheral chemoreception: new insights into a historically overlooked molecule - invited article. Adv. Exp. Med. Biol. 2009, 648:145-159.
24. Cross A.R., Jones O.T. Enzymic mechanisms of superoxide production. Biochim. Biophys. Acta 1991, 1057:281-298.
25. 2 sensing. Adv. Exp. Med. Biol. 2009, 648:427-438.
26. Cellular and Molecular Biology of Airway Chemoreceptors 1997, 1-33. Springer, NY. E. Cutz (Ed.).
27. Daiber A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 2010, [Epub ahead of print].
28. Dallas M.L., Scragg J.L., Wyatt C.N., Ross F., Hardie D.G., Evans A.M., Peers C. Modulation of O(2) sensitive K (+) channels by AMP-activated protein kinase. Adv. Exp. Med. Biol. 2009, 648:57-63.
29. D'Autréaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell. Biol. 2007, 8:813-824.
30. + channels essential for carotid body chemo-transduction?. Respir. Physiol. 1997, 110:211-218.
31. Dvorakova M., Hohler B., Vollerthun R., Fischbach T., Kummer W. Macrophages: a major source of cytochrome b558 in the rat carotid body. Brain Res. 2000, 852:349-354.
32. Erecińska M., Wilson D.F. Regulation of cellular energy metabolism. J. Membr. Biol. 1982, 70:1-14.
33. Evans A.M., Mustard K.J., Wyatt C.N., Peers C., Dipp M., Kumar P., Kinnear N.P., Hardie D.G. Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells?. J. Biol. Chem. 2005, 280:41504-41511.
34. Evans M.A., Ward J.P. Hypoxic pulmonary vasoconstriction. Adv. Exp. Med. Biol. 2009, 648:351-360.
35. Fidone S.J., González C. Initiation and control of chemoreceptor activity in the carotid body. Handbook of Physiology. The Respiratory System 1986, 247-312. Amer. Physiol. Soc, Bethesda, MD. A.P. Fishman (Ed.).
36. Fisher A.B. Redox signaling across cell membranes. Antioxid. Redox Signal. 2009, 11:1349-1356.
37. Frazziano, G., Moreno L., Moral-Sanz J., Menendez C., Escolano L., González C., Villamor E., Cogolludo A., Perez-Vizcaino F., submitted. Neutral sphingomyelinase, NADPH oxidase and reactive oxygen species. Role in acute hypoxic pulmonary vasoconstriction.
38. 2 tension. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:2927-2930.
39. Gomez-Niño A., Obeso A., Baranda J.A., Santo-Domingo J., Lopez-Lopez J.R., Gonzalez C. MaxiK potassium channels in the function of chemoreceptor cells of the rat carotid body. Am. J. Physiol. Cell Physiol. 2009, 297:C715-722.
40. Gomez-Niño A., Agapito M.T., Obeso A., Gonzalez C. Effects of mitochondrial poisons on glutathione redox potential and carotid body chemoreceptor activity. Respir. Physiol. Neurobiol. 2009, 165:104-111.
41. Gonzalez C., Almaraz L., Obeso A., Rigual R. Oxygen and acid chemoreception in the carotid body chemoreceptors. Trends Neurosci. 1992, 15:146-153.
42. Gonzalez C., Sanz-Alfayate G., Agapito M.T., Gomez-Nino A., Rocher A., Obeso A. Significance of ROS in oxygen sensing in cell systems with sensitivity to physiological hypoxia. Respir. Physiol. Neurobiol. 2002, 132:17-41.
43. Gonzalez C., Sanz-Alfayate G., Obeso A., Agapito M.T. Role of glutathione redox state in oxygen sensing by carotid body chemoreceptor cells. Methods Enzymol. 2004, 381:40-71.
44. Gonzalez C., Sanz-Alyayate G., Agapito M.T., Obeso A. Effects of reducing agents on glutathione metabolism and the function of carotid body chemoreceptor cells. Biol. Chem. 2004, 385:265-274.
45. Gonzalez C., Agapito M.T., Rocher A., Gonzalez-Martin M.C., Vega-Agapito V., Gomez-Niño A., Rigual R., Castañeda J., Obeso A. Chemoreception in the context of the general biology of ROS. Respir. Physiol. Neurobiol. 2007, 157:30-44.
46. Gonzalez C., Vaquero L.M., López-López J.R., Pérez-García M.T. Oxygen-sensitive potassium channels in chemoreceptor cell physiology: making a virtue of necessity. Ann. N. Y. Acad. Sci. 2009, 1177:82-88.
47. Gonzalez C. Sensitivity to physiologic hypoxia. Oxygen regulation of ion channels and gene expression 1998, 321-336. Futura Publishing Co. Inc., Armonk, NY. J. Lopez-Barneo, E.K. Weir (Eds.).
48. Gonzalez C., Almaraz L., Obeso A., Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev. 1994, 74:829-898.
49. Grundfest H. The general electrophysiology of input membrane in the electrogenic excitable cells. Handbook of Sensory Physiology, Vol. I Principles of Receptor Physiology 1971, 135-165. Springer Verlag, Berlin. W.R. Loewenstein (Ed.).
50. Guarani V., Potente M. SIRT1 - a metabolic sensor that controls blood vessel growth. Curr. Opin. Pharmacol. 2010, 10:139-145.
51. Guzy R.D., Schumacker P.T. Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 2006, 91:807-819.
52. Halperin M.L., Cheema-Dhadli S., Lin S.H., Kamel K.S. Properties permitting the renal cortex to be the oxygen sensor for the release of erythropoietin: clinical implications. Clin. J. Am. Soc. Nephrol. 2006, 1:1049-1053.
53. Hardie D.G. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int. J. Obes. (Lond.) 2008, 32(Suppl. 4):S7-12.
54. Hardie D.G., Salt I.P., Hawley S.A., Davies S.P. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem. J. 1999, 338(Pt 3):717-722.
55. He L., Chen J., Dinger B., Sanders K., Sundar K., Hoidal J., Fidone S. Characteristics of carotid body chemosensitivity in NADPH oxidase-deficient mice. Am. J. Physiol. Cell Physiol. 2002, 282:C27-33.
56. He L., Liu X., Chen J., Dinger B., Stensaas L., Fidone S. Modulation of chronic hypoxia-induced chemoreceptor hypersensitivity by NADPH oxidase subunits in rat carotid body. J. Appl. Physiol. 2010, 108:1304-1310.
57. phox gene-deletion on reactive oxygen species (ROS) production and oxygen sensing in mouse carotid body chemoreceptor cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2005, 289:916-924.
58. Iizuka T., Kanegasaki S., Makino R., Tanaka T., Ishimura Y. Studies on neutrophil b-type cytochrome are situ by low temperature absorption spectroscopy. J. Biol. Chem. 1985, 260:12049-12053.
59. Iturriaga R., Alcayaga J. Neurotransmission in the carotid body: transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Res. Brain Res. Rev. 2004, 47:46-53.
60. Iturriaga R., Alcayaga J., Gonzalez C. Neurotransmitters in carotid body function: the case of dopamine. Adv. Exp. Med. Biol. 2009, 648:137-143.
61. Jelic S., Le Jemtel T.H. Inflammation, oxidative stress, and the vascular endothelium in obstructive sleep apnea. Trends Cardiovasc. Med. 2008, 18:253-260.
62. Kahn B.B., Alquier T., Carling D., Hardie D.G. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005, 1:15-25.
63. Kemp P.J., Peers C., Lewis A. Oxygen sensing by human recombinant large conductance, calcium-activated potassium channels. Regulation by acute hypoxia. Adv. Exp. Med. Biol. 2003, 536:209-215.
64. Kim D., Cavanaugh E.J., Kim I., Carroll J.L. Heteromeric TASK-1/TASK-3 is the major oxygen-sensitive background K+ channel in rat carotid body glomus cells. J. Physiol. 2009, 587:2963-2975.
65. Kummer W., Acker H. Immunohistochemical demonstration of four subunits of neutrophil NAD(P)H oxidase in type I cells of carotid body. J. Appl. Physiol. 1995, 78:1904-1909.
66. Kääb S., Miguel-Velado E., López-López J.R., Pérez-García M.T. Down regulation of Kv3.4 channels by chronic hypoxia increases acute oxygen sensitivity in rabbit carotid body. J. Physiol. 2005, 566(Pt 2):395-408.
67. Lahiri S., Iturriaga R., Mokashi A., Ray D.K., Chugh D. CO reveals dual mechanisms of chemoreception in the cat carotid body. Res. Physiol. 1993, 94:227-240.
68. Lassègue B., Griendling K.K. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 2010, 30:653-661.
69. Lee Y.M., Kim B.J., Chun Y.S., So I., Choi H., Kim M.S., Park J.W. NOX4 as an oxygen sensor to regulate TASK-1 activity. Cell Signal. 2006, 18:499-507.
70. Lewis A., Peers C., Ashford M.L., Kemp P.J. Hypoxia inhibits human recombinant large conductance, Ca(2+)-activated K(+) (maxi-K) channels by a mechanism which is membrane delimited and Ca(2+) sensitive. J. Physiol. 2002, 540:771-780.
71. + current modulated by PO2 in type I chemoreceptor cells. Science 1988, 241:580-582.
72. + current inhibition by low oxygen in chemoreceptors cells of adult rabbit carotid body. Effects of carbon monoxide. FEBS Lett. 1992, 299:251-254.
73. McCartney C.E., McClafferty H., Huibant J.M., Rowan E.G., Shipston M.J., Rowe I.C. A cysteine-rich motif confers hypoxia sensitivity to mammalian large conductance voltage- and Ca-activated K (BK) channel alpha-subunits. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17870-21786.
74. Michelakis E.D., Hampl V., Nsair A., Wu X., Harry G., Haromy A., Gurtu R., Archer S.L. Diversity in mitochondrial function explains differences in vascular oxygen sensing. Circ. Res. 2002, 90:1307-1315.
75. 2+ transients that modulate secretion. Nat. Cell Biol. 2000, 2:57-61.
76. Moudgil R., Michelakis E.D., Archer S.L. Hypoxic pulmonary vasoconstriction. J. Appl. Physiol. 2005, 98:390-403.
77. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
78. Nakahira K., Kim H.P., Geng X.H., Nakao A., Wang X., Murase N., Drain P.F., Wang X., Sasidhar M., Nabel E.G., Takahashi T., Lukacs N.W., Ryter S.W., Morita K., Choi A.M. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J. Exp. Med. 2006, 203:2377-2389.
79. Nielsen A.M., Bisgard G.E., Vidruk E.H. Carotid chemoreceptor activity during acute and sustained hypoxia in goats. J. Appl. Physiol. 1988, 65:1796-1802.
80. Nohl H., Gille L., Staniek K. Intracellular generation of reactive oxygen species by mitochondria. Biochem. Pharmacol. 2005, 69:719-723.
81. Oakley F.D., Abbott D., Li Q., Engelhardt J.F. Signaling components of redox active endosomes: the redoxosomes. Antioxid. Redox Signal. 2009, 11:1313-1333.
82. Obeso A., Almaraz L., Gonzalez C. Correlation between adenosine triphosphate levels, dopamine release and electrical activity in the carotid body: support for the metabolic hypothesis of chemoreception. Brain Res. 1985, 348:64-68.
83. Obeso A., Gonzalez C., Dinger B., Fidone S. Metabolic activation of carotid body glomus cells by hypoxia. J. Appl. Physiol. 1989, 67:484-487.
84. 2 on glucose uptake in the rabbit carotid body. J. Appl. Physiol. 1993, 74:2387-2393.
85. Obeso A., Rocher A., Herreros B., Gonzalez C. Oxygen consumption and energy metabolism of the carotid body. The Carotid Body Chemoreceptors 1997, 31-45. Springer-Verlag, NY. C. Gonzalez (Ed.).
86. Ortega-Sáenz P., Levitsky K.L., Marcos-Almaraz M.T., Bonilla-Henao V., Pascual A., López-Barneo J. Carotid body chemosensory responses in mice deficient of TASK channels. J. Gen. Physiol. 2010, 135(April 4):379-392.
87. Osipenko O.N., Tate R.J., Gurney A.M. Potential role for kv3. 1b channels as oxygen sensors. Circ. Res. 2000, 86:534-540.
88. Pardal R., Ludewig U., Garcia-Hirschfeld J., Lopez-Barneo J. Secretory responses of intact glomus cells in thin slices of rat carotid body to hypoxia and tetraethylammonium. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2361-2366.
89. + channels. Am. J. Physiol. Cell Physiol. 2009, 297:C855-864.
90. Parkos C.A., Dinauer M.C., Walker L.E., Allen R.A., Jesaitis A.J., Orkin S.H. Primary structure and unique expression of the 22-kilodalton light chain of human neutrophil cytochrome b. Proc. Natl. Acad. Sci. U.S.A. 1988, 15:3319-3323.
91. Paulsen C.E., Carroll K.S. Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem. Biol. 2010, 5:47-62.
92. Peers C., Wyatt C.N. The role of maxiK channels in carotid body chemotransduction. Respir. Physiol. Neurobiol. 2007, 157:75-82.
93. Peng Y.J., Nanduri J., Yuan G., Wang N., Deneris E., Pendyala S., Natarajan V., Kumar G.K., Prabhakar N.R. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J. Neurosci. 2009, 29:4903-4910.
94. Perez-Garcia M.T., Lopez-Lopez J.R., Gonzalez C. Kvbeta1.2 subunit coexpression in HEK293 cells confers O2 sensitivity to kv4.2 but not to Shaker channels. J. Gen. Physiol. 1999, 113:897-907.
95. Rathore R., Zheng Y.M., Niu C.F., Liu Q.H., Korde A., Ho Y.S., Wang Y.X. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic. Biol. Med. 2008, 45:1223-1231.
96. Rathore R., Zheng Y.M., Li X.Q., Wang Q.S., Liu Q.H., Ginnan R., Singer H.A., Ho Y.S., Wang Y.X. Mitochondrial ROS-PKCepsilon signaling axis is uniquely involved in hypoxic increase in [Ca2+]i in pulmonary artery smooth muscle cells. Biochem. Biophys. Res. Commun. 2006, 351:784-790.
97. Reeve H.L., Michelakis E., Nelson D.P., Weir E.K., Archer S.L. Alterations in a redox oxygen sensing mechanism in chronic hypoxia. J. Appl. Physiol. 2001, 90:2249-2256.
98. Rico A.J., Prieto-Lloret J., Gonzalez C., Rigual R. Hypoxia and acidosis increase the secretion of catecholamines in the neonatal rat adrenal medulla: an in vitro study. Am. J. Physiol. Cell Physiol. 2005, 289:C1417-C1425.
99. Ridge J.W. Hypoxia and the energy charge of the cerebral adenylate pool. Biochem. J. 1972, 127:351-355.
100. + channels of rat chemoreceptor cells by a membrane-restricted and CO-sensitive mechanism. Circ. Res. 2001, 89:430-436.
101. Roepstorff C., Thiele M., Hillig T., Pilegaard H., Richter E.A., Wojtaszewski J.F., Kiens B. Higher skeletal muscle alpha2AMPK activation and lower energy charge and fat oxidation in men than in women during submaximal exercise. J. Physiol. 2006, 574:125-138.
102. Roy A., Rozanov C., Mokashi A., Daudu P., Al-mehdi A.B., Shams H., Lahiri S. Mice lacking in gp91 phox subunit of NAD(P)H oxidase showed glomus cell [Ca(2+)](i) and respiratory responses to hypoxia. Brain Res. 2000, 872:188-193.
103. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., Lan F., Ido Y. AMPK and SIRT1: a long-standing partnership?. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E751-E760.
104. Rumsey W.L., Iturriaga R., Spergel D., Lahiri S., Wilson D.F. Optical measurements of the dependence of chemoreception on oxygen pressure in the cat carotid body. Am. J. Physiol. 1991, 261:C614-C622.
105. Rumsey W.L., Lahiri S., Iturriaga R., Mokashi A., Spergel D., Wilson D.F. Optical measurements of oxygen and electrical measurements of oxygen chemoreception in the cat carotid body. Adv. Exp. Med. Biol. 1992, 317:387-395.
106. Sanchez D., López-López J.R., Pérez-García M.T., Sanz-Alfayate G., Obeso A., Ganfornina M.D., Gonzalez C. Molecular identification of Kvalpha subunits that contribute to the oxygen-sensitive K(+) current of chemoreceptor cells of the rabbit carotid body. J. Physiol. 2002, 542:369-382.
107. Sanders K.A., Sundar K.M., He L., Dinger B., Fidone S., Hoidal J.R. Role of components of the phagocytic NADPH oxidase in oxygen sensing. J. Appl. Physiol. 2002, 93:1357-1364.
108. Santodomingo J., Vay L., Camacho M., Hernández-Sanmiguel E., Fonteriz R.I., Lobatón C.D., Montero M., Moreno A., Alvarez J. Calcium dynamics in bovine adrenal medulla chromaffin cell secretory granules. Eur. J. Neurosci. 2008, 28:1265-1274.
109. Sanz-Alfayate G., Obeso A., Agapito M.T., Gonzalez C. Reduced to oxidized glutathione ratios and oxygen sensing in calf and rabbit carotid body chemoreceptor cells. J. Physiol. 2001, 537:209-220.
110. - and NO: how far can either radical, or any specific reaction product, transmit a message under in vivo conditions?. Chem. Biol. Interact. 1994, 90:35-45.
111. Seidler F.J., Slotkin T.A. Adrenomedullary function in the neonatal rat: responses to acute hypoxia. J. Physiol. 1985, 358:1-16.
112. Sekiguchi F., Seo M., Sunano S. Contraction of arterial smooth muscle of normotensive and spontaneously hypertensive rats by manganese(III) tetrakis(1-methyl-4-pyridyl)porphyrin (MnTMPyP). J. Pharmacol. Sci. 2003, 92:163-165.
113. Steinberg G.R., Kemp B.E. AMPK in health and disease. Physiol. Rev. 2009, 89:1025-1078.
114. Streit B.R., Blanc B., Lukat-Rodgers G.S., Rodgers K.R., DuBois J.L. How active-site protonation state influences the reactivity and ligation of the heme in chlorite dismutase. J. Am. Chem. Soc. 2010, 132:5711-5724.
115. Tamayo L., López-López J.R., Castañeda J., González C. Carbon monoxide inhibits hypoxic pulmonary vasoconstriction in rats by a cGMP-independent mechanism. Pflugers Arch. 1997, 434:698-704.
116. Taylor C.T. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem. J. 2008, 409:19-26.
117. Ushio-Fukai M. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid. Redox Signal. 2009, 11:1289-1299.
118. Verna A., Talib N., Roumy M., Pradet A. Effects of metabolic inhibitors and hypoxia on the ATP, ADP and AMP content of the rabbit carotid body in vitro: the metabolic hypothesis in question. Neurosci. Lett. 1990, 116:156-161.
119. Wang Y.X., Zheng Y.M. ROS-dependent signaling mechanisms for hypoxic Ca(2+) responses in pulmonary artery myocytes. Antioxid. Redox Signal. 2010, 12:611-623.
120. Ward J.P. Oxygen sensors in context. Biochim. Biophys. Acta 2008, 1777:1-14.
121. Waypa G.B., Schumacker P.T. Oxygen sensing in hypoxic pulmonary vasoconstriction: using new tools to answer an age-old question. Exp. Physiol. 2008, 93:133-138.
122. Waypa G.B., Chandel N.S., Schumacker P.T. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ. Res. 2001, 88:1259-1266.
123. Waypa G.B., Marks J.D., Guzy R., Mungai P.T., Schriewer J., Dokic D., Schumacker P.T. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ. Res. 2010, 106:526-535.
124. Waypa G.B., Schumacker P.T. Hypoxic pulmonary vasoconstriction: redox events in oxygen sensing. J. Appl. Physiol. 2005, 98:404-414.
125. Waypa G.B., Schumacker P.T. Role for mitochondrial reactive oxygen species in hypoxic pulmonary vasoconstriction. Novartis Found. Symp. 2006, 272:176-192.
126. Weir E.K., Archer S.L. The mechanism of acute hypoxic pulmonary vasoconstriction: the tale of two channels. FASEB J. 1995, 9:183-189.
127. Weissmann N., Zeller S., Schäfer R.U., Turowski C., Ay M., Quanz K., Ghofrani H.A., Schermuly R.T., Fink L., Seeger W., Grimminger F. Impact of mitochondria and NADPH oxidases on acute and sustained hypoxic pulmonary vasoconstriction. Am. J. Respir. Cell Mol. Biol. 2006, 34:505-513.
128. Westermann M., Leutbecher H., Meyer H.W. Membrane structure of caveolae and isolated caveolin-rich vesicles. Histochem. Cell Biol. 1999, 111:71-81.
129. 2 in the carotid body of the cat. Morphology and Mechanisms of Chemoreceptors 1976, 91-102. Navchetan Press, Delhi. A.S. Paintal (Ed.).
130. 2 of the carotid body. Physiology of the Peripheral Arterial Chemoreceptors 1983, 117-132. Elsevier, Amsterdam. H. Acker, R.G. O'Regan (Eds.).
131. Williams S.E., Brazier S.P., Baban N., Telezhkin V., Müller C.T., Riccardi D., Kemp P.J. A structural motif in the C-terminal tail of slo1 confers carbon monoxide sensitivity to human BK Ca channels. Pflugers Arch. 2008, 456:561-572.
132. Williams S.E., Wootton P., Mason H.S., Bould J., Iles D.E., Riccardi D., Peers C., Kemp P.J. Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel. Science 2004, 306:2093-2097.
133. Woods A., Johnstone S.R., Dickerson K., Leiper F.C., Fryer L.G., Neumann D., Schlattner U., Wallimann T., Carlson M., Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 2003, 13:2004-2008.
134. Wu W., Platoshyn O., Firth A.L., Yuan J.X. Hypoxia divergently regulates production of reactive oxygen species in human pulmonary and coronary artery smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 293:L952-L959.
135. Wyatt C.N., Mustard K.J., Pearson S.A., Dallas M.L., Atkinson L., Kumar P., Peers C., Hardie D.G., Evans A.M. AMP-activated protein kinase mediates carotid body excitation by hypoxia. J. Biol. Chem. 2007, 282:8092-8098.
136. + currents in carotid body chemoreceptor cells from normoxic and chronically hypoxic rats and their roles in hypoxic chemotransduction. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:295-299.
137. Yu J.H., Kim K.H., Kim D.G., Kim H. Diphenyleneiodonium suppresses apoptosis in cerulein-stimulated pancreatic acinar cells. Int. J. Biochem. Cell Biol. 2007, 39:2063-2075.