Cellular and molecular mechanisms of O2 sensing

High Altitude: Human Adaptation to Hypoxia

Volumn 9781461487722, Issue , 2014, Pages 1-22

  Schumacker, Paul T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84929665015     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-8772-2_1     Document Type: Chapter

References (117)

1. Leung DW, Cachianes G, Kuang WJ, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246(4935):1306-9.
2. May D, Gilon D, Djonov V, et al. Transgenic system for conditional induction and rescue of chronic myocardial hibernation provides insights into genomic programs of hibernation. Proc Natl Acad Sci USA. 2008;105(1):282-7.
3. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380(6573):439-42.
4. Hardie DG, Hawley SA, Scott JW. AMP-activated protein kinase-development of the energy sensor concept. J Physiol. 2006;574(Pt 1):7-15.
5. Semenza GL. Involvement of hypoxia-inducible factor 1 in pulmonary pathophysiology. Chest. 2005;128(6):592S-4.
6. Voter WA, Gayeski TE. Determination of myoglobin saturation of frozen specimens using a reflecting cryospectrophotometer. Am J Physiol. 1995;269 (4 Pt 2):H1328-41.
7. Gayeski TE, Honig CR. Intracellular PO2 in individual cardiac myocytes in dogs, cats, rabbits, ferrets, and rats. Am J Physiol. 1991;260:H522-31.
8. Gayeski TE, Honig CR. Intracellular PO2 in long axis of individual fibers in working dog gracilis muscle. Am J Physiol. 1988;254:H1179-86.
9. Gayeski TE, Honig CR. O2 gradients from sarcolemma to cell interior in red muscle at maximal VO2. Am J Physiol. 1986;251:H789-99.
10. Honig CR, Gayeski TE. Comparison of intracellular PO2 and conditions for blood-tissue O2 transport in heart and working red skeletal muscle. Adv Exp Med Biol. 1987;215:309-21.
11. Gayeski TE, Connett RJ, Honig CR. Minimum intracellular PO2 for maximum cytochrome turnover in red muscle in situ. Am J Physiol. 1987;252:H906-15.
12. Clark Jr A, Clark PA, Connett RJ, et al. How large is the drop in PO2 between cytosol and mitochondrion? Am J Physiol. 1987;252:C583-7.
13. Takahashi E, Endoh H, Xu ZL, et al. Direct estimation of intracellular PO2 gradients in a single cardiomyocyte of the rat. Adv Exp Med Biol. 1998;454: 409-13.
14. Takahashi E, Sato K, Endoh H, et al. Direct observation of radial intracellular PO2 gradients in a single cardiomyocyte of the rat. Am J Physiol. 1998;275 (1 Pt 2):H225-33.
15. Jones DP, Mason HS. Gradients of O 2 concentration in hepatocytes. J Biol Chem. 1978;253:4874-80.
16. Goldwasser E, Jacobson LO, Fried W, et al. Studies on erythropoiesis. V. The effect of cobalt on the production of erythropoietin. Blood. 1958;13:55-60.
17. Goldberg MA, Glass GA, Cunningham JM, et al. The regulated expression of erythropoietin by two human hepatoma cell lines. Proc Natl Acad Sci USA. 1987;84(22):7972-6.
18. Goldberg MA, Dunning SP, Bunn HF. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science. 1988;242: 1412-5.
19. Fandrey J, Bunn HF. In vivo and in vitro regulation of erythropoietin mRNA: measurement by competitive polymerase chain reaction. Blood. 1993;81(3): 617-23.
20. Horiguchi H, Bunn HF. Erythropoietin induction in Hep3B cells is not affected by inhibition of heme biosynthesis. Biochim Biophys Acta Mol Cell Res. 2000;1495(3):231-6.
21. Babior BM. The leukocyte NADPH oxidase. Isr Med Assoc J. 2002;4(11):1023-4.
22. Babior BM, Lambeth JD, Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys. 2002;397(2): 342-4.
23. Wolin MS, Ahmad M, Gao Q, et al. Cytosolic NAD(P)H regulation of redox signaling and vascular oxygen sensing. Antioxid Redox Signal. 2007;9(6): 671-8.
24. Muller G, Morawietz H. NAD(P)H oxidase and endothelial dysfunction. Horm Metab Res. 2009;41(2): 152-8.
25. 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(5):1904-9.
26. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P) H oxidase-role in cardiovascular biology and disease. Circ Res. 2000;86(5):494-501.
27. Babior BM. The NADPH oxidase of endothelial cells. IUBMB Life. 2000;50(4-5):267-9.
28. Archer SL, Reeve HL, Michelakis E, et al. O 2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase. Proc Natl Acad Sci USA. 1999;96:7944-9.
29. Weissmann N, Zeller S, Schafer RU, et al. Impact of mitochondria and NADPH oxidases on acute and sustained hypoxic pulmonary vasoconstriction. Am J Respir Cell Mol Biol. 2006;34(4):505-13.
30. Ganfornina MD, Lopez-Barneo J. Single K + channels in membrane patches of arterial chemoreceptor cells are modulated by O 2 tension. Proc Natl Acad Sci USA. 1991;88(7):2927-30.
31. Ganfornina MD, Lopez-Barneo J. Potassium channel types in arterial chemoreceptor cells and their selective modulation by oxygen. J Gen Physiol. 1992;100(3):401-26.
32. Peers C. Hypoxic suppression of K+ currents in type I carotid body cells: selective effect on the Ca2(+)- activated K+ current. Neurosci Lett. 1990;119(2): 253-6.
33. Wyatt CN, Peers C. Ca(2+)-activated K+ channels in isolated type I cells of the neonatal rat carotid body. J Physiol. 1995;483(Pt 3):559-65.
34. Perez-Garcia MT, Colinas O, Miguel-Velado E, et al. Characterization of the Kv channels of mouse carotid body chemoreceptor cells and their role in oxygen sensing. J Physiol (Lond ). 2004;557(2):457-71.
35. Weir EK, Lopez-Barneo J, Buckler KJ, et al. Mechanisms of disease-acute oxygen-sensing mechanisms. N Engl J Med. 2005;353(19):2042-55.
36. Williams SEJ, Wootton P, Mason HS, et al. Hemoxygenase-2 is an oxygen sensor for a calciumsensitive potassium channel. Science. 2004;306 (5704):2093-7.
37. Ortega-Saenz P, Pascual A, Gomez-Diaz R, et al. Acute oxygen sensing in heme oxygenase-2 null mice. J Gen Physiol. 2006;128(4):405-11.
38. Semenza GL, Roth PH, Fang H-M, et al. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem. 1994;269:23757-63.
39. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992;12(12):5447-54.
40. Semenza GL, Nejfelt MK, Chi SM, et al. Hypoxiainducible nuclear factors bind to an enhancer element located 3' to the human erythropoietin gene. Proc Natl Acad Sci USA. 1991;88(13):5680-4.
41. Maxwell PH, Pugh CW, Ratcliffe PJ. Inducible operation of the erythropoietin 3' enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. Proc Natl Acad Sci USA. 1993;90:2423-7.
42. Marx J. How cells endure low oxygen. Science. 2004;303:1454-6.
43. Iyer NV, Kotch LE, Agani F, et al. Cellular and developmental control of O2 homeostasis by hypoxia- inducible factor 1 alpha. Genes Dev. 1998;12(2):149-62.
44. Maltepe E, Schmidt JV, Baunoch D, et al. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature. 1997;386(6623):403-7.
45. Maltepe E, Simon MC. Oxygen, genes, and development: an analysis of the role of hypoxic gene regulation during murine vascular development. J Mol Med. 1998;76(6):391-401.
46. Wang GL, Jiang B-H, Rue EA, et al. Hypoxiainducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O 2 tension. Proc Natl Acad Sci USA. 1995;92:5510-4.
47. Jiang BH, Semenza GL, Bauer C, et al. Hypoxiainducible factor 1 levels vary exponentially over a physiologically relevant range of O 2 tension. Am J Physiol. 1996;271(4 Pt 1):C1172-80.
48. Huang LE, Gu J, Schau M, et al. Regulation of hypoxia-inducible factor 1α is mediated by an O 2 - dependent degradation domain via the ubiquitinproteasome pathway. Proc Natl Acad Sci USA. 1998;95(14):7987-92.
49. Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxiainducible factors for oxygen-dependent proteolysis. Nature. 1999;399(6733):271-5.
50. Semenza GL. HIF-1, O2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell. 2001;107(1):1-3.
51. Takeda K, Ho VC, Takeda H, et al. Placental but not heart defects are associated with elevated hypoxiainducible factor alpha levels in mice lacking prolyl hydroxylase domain protein. Mol Cell Biol. 2006;26(22):8336-46.
52. Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001;292(5516):468-72.
53. Ivan M, Kondo K, Yang H, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001; 292(5516):464-8.
54. Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF- 1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394(6692):485-90.
55. Mole DR, Maxwell PH, Pugh CW, et al. Regulation of HIF by the von Hippel-Lindau tumour suppressor: implications for cellular oxygen sensing. IUBMB Life. 2001;52(1-2):43-7.
56. Lando D, Peet DJ, Whelan DA, et al. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science. 2002;295(5556):858-61.
57. Lando D, Peet DJ, Gorman JJ, et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002;16(12):1466-71.
58. Masson N, Singleton RS, Sekirnik R, et al. The FIH hydroxylase is a cellular peroxide sensor that modulates HIF transcriptional activity. EMBO Rep. 2012;13(3):251-7.
59. Hagen T, Taylor CT, Lam F, et al. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science. 2003;302(5652):1975-8.
60. Cassina A, Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys. 1996;328(2):309-16.
61. Castello PR, David PS, McClure T, et al. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 2006;3(4):277-87.
62. Poyton RO, Castello PR, Ball KA, et al. Mitochondria and hypoxic signaling: a new view. Ann N Y Acad Sci. 2009;1177:48-56.
63. Kadenbach B, Barth J, Akgun R, et al. Regulation of mitochondrial energy generation in health and disease. Biochim Biophys Acta. 1995;1271:103-9.
64. Kadenbach B, Stroh A, Ungibauer M, et al. Isozymes of cytochrome-c oxidase: characterization and isolation from different tissues. Methods Enzymol. 1986;126:32-45.
65. Huttemann M, Kadenbach B, Grossman LI. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene. 2001;267(1):111-23.
66. Brunori M, Wilson MT. Electron transfer and proton pumping in cytochrome oxidase. Biochimie. 1995;77:668-76.
67. Mills E, Jobsis FF. Mitochondrial respiratory chain of carotid body and chemoreceptor response to changes in oxygen tension. J Neurophysiol. 1972;35(4):405-28.
68. Nair PK, Buerk DG, Whalen WJ, et al. Two cytochrome oxygen consumption model and mechanism for carotid body chemoreception. Adv Exp Med Biol. 1986;200:293-300.
69. Nair PK, Buerk DG, Whalen WJ. Cat carotid body oxygen metabolism and chemoreception described by a two-cytochrome model. Am J Physiol. 1986;250(2 Pt 2):H202-7.
70. Buerk DG, Nair PK, Whalen WJ. Two-cytochrome metabolic model for carotid body PtiO2 and chemosensitivity changes after hemorrhage. J Appl Physiol. 1989;67(1):60-8.
71. Eyzaguirre C, Zapata P. Perspectives in carotid body research. J Appl Physiol. 1984;57(4):931-57.
72. Cooper CE. The steady-state kinetics of cytochrome c oxidation by cytochrome oxidase. Biochim Biophys Acta. 1990;1017:187-203.
73. Joels N, Neil E. The action of high tensions of carbon monoxide on the carotid chemoreceptors. Arch Int Pharm Ther. 1962;130:528-34.
74. Lahiri S, Iturriaga R, Mokashi A, et al. CO reveals dual mechanisms of O2 chemoreception in the cat carotid body. Respir Physiol. 1993;94(2):227-40.
75. Lahiri S. Chromophores in O2 chemoreception: the carotid body model. News Physiol Sci. 1994;9: 161-5.
76. Jensen PK. Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-tranport particles. Biochim Biophys Acta. 1966;122:157-66.
77. Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J. 1972;128(3):617-30.
78. Ambrosio G, Zweier JL, Duilio C, et al. Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem. 1993;268(25):18532-41.
79. Becker LB, Vanden Hoek TL, Shao ZH, et al. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol. 1999;277(6 Pt 2):H2240-6.
80. Di Lisa F, Menabo R, Canton M, et al. The role of mitochondria in the salvage and the injury of the ischemic myocardium. Biochim Biophys Acta. 1998;1366(1-2):69-78.
81. Ferrari R. The role of mitochondria in ischemic heart disease. J Cardiovasc Pharmacol. 1996;28 Suppl 1:S1-10.
82. Turrens JF, Beconi M, Barilla J, et al. Mitochondrial generation of oxygen radicals during reoxygenation of ischemic tissues. Free Radic Res Commun. 1991;12-13(Pt 2):681-9.
83. Vanden Hoek TL, Li C, Shao Z, et al. Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J Mol Cell Cardiol. 1997;29:2571-83.
84. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem. 1981;256(21):10986-92.
85. Shimada H, Hirai K, Simamura E, et al. Mitochondrial NADH-quinone oxidoreductase of the outer membrane is responsible for paraquat cytotoxicity in rat livers. Arch Biochem Biophys. 1998;351(1):75-81.
86. Boveris A, Cadenas E. Mitochondrial production of hydrogen peroxide regulation by nitric oxide and the role of ubisemiquinone. IUBMB Life. 2000;50(4-5): 245-50.
87. Chandel NS, Maltepe E, Goldwasser E, et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA. 1998;95:11715-20.
88. Chandel NS, Schumacker PT. Cellular oxygen sensing by mitochondria: old questions, new insight. J Appl Physiol. 2000;88(5):1880-9.
89. Jones DP, Shan X, Park Y. Coordinated multisite regulation of cellular energy metabolism. Annu Rev Nutr. 1992;12:327-43.
90. Turrens JF, Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J. 1980;191:421-7.
91. Votyakova TV, Reynolds IJ. DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem. 2001;79(2):266-77.
92. Genova ML, Ventura B, Giuliano G, et al. The site of production of superoxide radical in mitochondrial Complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett. 2001;505(3):364-8.
93. Li Y, Trush MA. Diphenyleneiodonium, an NAD(P) H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Biophys Res Commun. 1998;253(2):295-9.
94. Misra HP, Fridovich I. The univalent reduction of oxygen by reduced flavins and quinones. J Biol Chem. 1972;247:188-92.
95. Turrens JF, Alexandre A, Lehninger AL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys. 1985;237:408-14.
96. Garcia-Ruiz C, Colell A, Morales A, et al. Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-kappa B: studies with isolated mitochondria and rat hepatocytes. Mol Pharmacol. 1995;48(5):825-34.
97. Kwong LK, Sohal RS. Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys. 1998;350:118-26.
98. Garcia-Ruiz C, Colell A, Mari M, et al. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J Biol Chem. 1997;272(17):11369-77.
99. Quillet-Mary A, Jaffrezou JP, Mansat V, et al. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J Biol Chem. 1997;272(34):21388-95.
100. Gille L, Nohl H. The ubiquinol/bc1 redox couple regulates mitochondrial oxygen radical formation. Arch Biochem Biophys. 2001;388(1):34-8.
101. Zhang L, Yu LD, Yu CA. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J Biol Chem. 1998;273(51):33972-6.
102. Guzy RD, Hoyos B, Robin E, et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005;1(6):401-8.
103. Mansfield KD, Guzy RD, Pan Y, et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIFalpha activation. Cell Metab. 2005;1(6):393-9.
104. Waypa GB, Marks JD, Guzy R, et al. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res. 2010;106(3): 526-35.
105. Remington SJ. Fluorescent proteins: maturation, photochemistry and photophysics. Curr Opin Struct Biol. 2006;16(6):714-21.
106. Hanson GT, Aggeler R, Oglesbee D, et al. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem. 2004;279(13):13044-53.
107. Waypa GB, Guzy R, Mungai PT, et al. Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells. Circ Res. 2006;99(9): 970-8.
108. Waypa GB, Marks JD, Mack MM, et al. Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ Res. 2002;91(8):719-26.
109. Waypa GB, Chandel NS, Schumacker PT. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ Res. 2001; 88(12):1259-66.
110. Jung HJ, Shim JS, Lee J, et al. Terpestacin inhibits tumor angiogenesis by targeting UQCRB of mitochondrial complex III and suppressing hypoxiainduced reactive oxygen species production and cellular oxygen sensing. J Biol Chem. 2010;285(15):11584-95.
111. King MP, Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 1989;246:500-3.
112. Vaux EC, Metzen E, Yeates KM, et al. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood. 2001;98(2):296-302.
113. Chandel NS, McClintock DS, Feliciano CE, et al. Reactive oxygen species generated at mitochondrial Complex III stabilize HIF-1-alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130-8.
114. Gusarova GA, Dada LA, Kelly AM, et al. Alpha1- AMP- activated protein kinase regulates hypoxiainduced Na, K-ATPase endocytosis via direct phosphorylation of protein kinase C zeta. Mol Cell Biol. 2009;29(13):3455-64.
115. Emerling BM, Weinberg F, Snyder C, et al. Hypoxic activation of AMPK is dependent on mitochondrial ROS but independent of an increase in AMP/ATP ratio. Free Radic Biol Med. 2009;46(10):1386-91.
116. Mungai PT, Waypa GB, Jairaman A, et al. Hypoxia triggers AMPK activation through ROS-mediated activation of CRAC channels. Mol Cell Biol. 2011;31(17):3531-45.
117. Guzy RD, Schumacker PT. Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol. 2006;91(5):807-19.