Oxygen sensing and homeostasis

Physiology

Volumn 30, Issue 5, 2015, Pages 340-348

  Prabhakar, Nanduri R ^a   Semenza, Gregg L ^b  

^a University of Chicago   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

ADAPTIVE BEHAVIOR; ANIMAL; BREATHING; CAROTID BODY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HOMEOSTASIS; HUMAN; HYPOXIA; LUNG; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; CAROTID BODY; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; HYPOXIA; LUNG; OXYGEN; RESPIRATION; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84940866922     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00022.2015     Document Type: Review

References (96)

1. Barnett S, Mulligan E, Wagerle LC, Lahiri S. Measurement of carotid body blood flow in cats by use of radioactive microspheres. J Appl Physiol 65: 2484-2489, 1988.
2. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, Mazure NM. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29: 2570-2581, 2009.
3. Bernhardt WM, Wiesener MS, Scigalla P, Chou J, Schmieder RE, Günzler V, Eckardt KU. Inhibition of prolyl hydroxylases increases erythropoietin production in ESRD. J Am Soc Nephrol 21: 2151-2156, 2010.
4. Biscoe TJ, Bradley GW, Purves MJ. The relation between carotid body chemoreceptor discharge, carotid sinus pressure and carotid body venous flow. J Physiol 208: 99-120, 1970.
5. Black AM, McCloskey DI, Torrance RW. The responses of carotid body chemoreceptors in the cat to sudden changes of hypercapnic and hypoxic stimuli. Respir Physiol 13: 36-49, 1971.
6. Buckler KJ. Effects of exogenous hydrogen sulphide on calcium signalling, background (TASK) K channel activity and mitochondrial function in chemoreceptor cells. Pflügers Arch 463: 743-754, 2012.
7. Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab 10: 273-284, 2009.
8. Clarke JA, de Burgh Daly M, Ead HW. Dimensions and volume of the carotid body in the adult cat, and their relation to the specific blood flow through the organ. A histological and morphometric study. Acta Anat (Basel) 126: 84-86, 1986.
9. De Burgh Daly M, Lambertsen CJ, Schweitzer A. Observations on the volume of blood flow and oxygen utilization of the carotid body in the cat. J Physiol 125: 67-89, 1954.
10. De Castro F. Sur la structure et l’innervation de la glande intercarotidienne (glomus caroticum) de l’homme et des mammiferes et sur un nouveau systeme de l’innervation autonome du nerf glossopharyngien. Trav Lab Rech Biol 24: 365-432, 1926.
11. Dempsey JA, Forster HV. Mediation of ventilatory adaptations. Physiol Rev 62: 262-346, 1982.
12. Duan LJ, Takeda K, Fong GH. Hematological, hepatic, and retinal phenotypes in mice deficient for prolyl hydroxylase domain proteins in the liver. Am J Pathol 184: 1240-1250, 2014.
13. Eschbach JW, Egrie JC, Downing MR, Browne JK, Adamson JW. Correction of the anemia of end-stage renal disease with recombinant human erythropoietin. Results of a combined phase I and II clinical trial. N Engl J Med 316: 73-78, 1987.
14. Eyzaguirre C, Lewin J. Effect of different oxygen tensions on the carotid body in vitro. J Physiol 159: 238-250, 1961.
15. Fidone SJ, Gonzalez C. Initiation and control of chemoreceptor activity in the carotid body. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. 2, pt. 1, chapt. 9, p. 247-312.
16. Fitzgerald RS, Lahiri S. Reflex responses to carotid/aortic body stimulation. In: Handbook of Physiology The Respiratory System Control of Breathing. Bethesda, MD: American Physiological Society., 1986, sect. 3, vol. 2, pt. 1, chapt. 10, p. 313-362.
17. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129: 111-122, 2007.
18. Gilkes DM, Semenza GL, Wirtz D. Hypoxia and the extracellular matrix: drivers of tumour metastasis. Nat Rev Cancer 14: 430-439, 2014.
19. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol 23: 359-369, 2003.
20. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74: 829-898, 1994.
21. Hackenbeck T, Knaup KX, Schietke R, Schödel J, Willam C, Wu X, Warnecke C, Eckardt KU, Wiesener MS. HIF-1 or HIF-2 induction is sufficient to achieve cell cycle arrest in NIH3T3 mouse fibroblasts independent from hypoxia. Cell Cycle 8: 1386-1395, 2009.
22. Hackett PH, Roach RC, Schoene RB, Harrison GL, Mills WJ Jr. Abnormal control of ventilation in high-altitude pulmonary edema. J Appl Physiol 64: 1268-1272, 1988.
23. Hayward LF, Castellanos M, Noah C. Cardiorespiratory variability following repeat acute hypoxia in the conscious SHR versus two normotensive rat strains. Auton Neurosci 171: 58-65, 2012.
24. Heymans J, Heymans C. Sur les modifications directes et sur la regulationreflexede l’activitie du centre respiratory de la tete isolee du chien. Arch Int Pharmacodyn Ther 33: 273-372, 1927.
25. Hodges MR, Forster HV, Papanek PE, Dwinell MR, Hogan GE. Ventilatory phenotypes among four strains of adult rats. J Appl Physiol 93: 974-983, 2002.
26. Hohenhaus E, Paul A, McCullough RE, Kucherer H, Bartsch P. Ventilatory and pulmonary vascular response to hypoxia and susceptibility to high altitude pulmonary oedema. Eur Respir J 8: 1825-1833, 1995.
27. Hornbein TF, Griffo ZJ, Roos A. Quantitation of chemoreceptor activity: interrelation of hypoxia and hypercapnia. J Neurophysiol 24: 561-568, 1961.
28. Hubbi M, Kshitiz E, Gilkes DM, Rey S, Wong CC, Luo W, Kim DH, Dang CV, Levchenko A, Semenza GL. A nontranscriptional role for HIF-1+ as a direct inhibitor of DNA replication. Sci Signal 6: ra10, 2013.
29. Hubbi ME, Luo W, Baek JH, Semenza GL. MCM proteins are negative regulators of hypoxia-inducible factor 1. Mol Cell 42: 700-712, 2011.
30. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol Rev 72: 449-489, 1992.
31. Jiang X, Sung YK, Tian W, Qian J, Semenza GL, Nicolls MR. Graft microvascular disease in solid organ transplantation. J Mol Med 92: 797-810, 2014.
32. Julius D, Nathans J. Signaling by sensory receptors. Cold Spring Harb Perspect Biol 4: a005991, 2012.
33. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177-185, 2006.
34. Kline DD, Peng YJ, Manalo DJ, Semenza GL, Prabhakar NR. Defective carotid body function and impaired ventilatory responses to chronic hypoxia in mice partially deficient for hypoxiainducible factor 1 alpha. Proc Natl Acad Sci USA 99: 821-826, 2002.
35. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23: 1949-1956, 2004.
36. Koury MJ. Abnormal erythropoiesis and the pathophysiology of chronic anemia. Blood Rev 28: 49-66, 2014.
37. Kumar P, Prabhakar NR. Peripheral chemoreceptors: function and plasticity of the carotid body. Comp Physiol 2: 141-219, 2012.
38. Kwast KE, Burke PV, Poyton RO. Oxygen sensing and the transcriptional regulation of oxygen-responsive genes in yeast. J Exp Biol 201: 1177-1195, 1998.
39. Lahiri S, Ehleben W, Acker H. Chemoreceptor discharges and cytochrome redox changes of the rat carotid body: role of heme ligands. Proc Natl Acad Sci USA 96: 9427-9432, 1999.
40. Li Q, Sun B, Wang X, Jin Z, Zhou Y, Dong L, Jiang LH, Rong W. A crucial role for hydrogen sulfide in oxygen sensing via modulating large conductance calcium-activated potassium channels. Antioxid Redox Signal 12: 1179-1189, 2010.
41. Luo W, Chang R, Zhong J, Pandey A, Semenza GL. Histone demethylase JMJD2C is a coactivator for hypoxia-inducible factor 1 that is required for breast cancer progression. Proc Natl Acad Sci USA 109: 3367-3376, 2012.
42. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517-554, 1997.
43. Makarenko VV, Nanduri J, Raghuraman G, Fox AP, Gadalla MM, Kumar GK, Snyder SH, Prabhakar NR. Endogenous H2S is required for hypoxic sensing by carotid body glomus cells. Am J Physiol Cell Physiol 303: C916-C923, 2012.
44. Makarenko VV, Peng YJ, Yuan G, Fox AP, Kumar GK, Nanduri J, Prabhakar NR. CaV3.2 T-type Ca2+ channels in H2S-mediated hypoxic response of the carotid body. Am J Physiol Cell Physiol 308: C146-C154, 2015.
45. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105: 659-669, 2005.
46. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J Clin Invest 119: 1159-1166, 2009.
47. McCoubrey WK, Huang TJ, Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 272: 12568-12574, 1997.
48. Minamishima YA, Kaelin WG. Reactivation of hepatic EPO synthesis in mice after PHD loss. Science 329: 407, 2010.
49. Mkrtchian S, Kahlin J, Ebberyd A, Gonzalez C, Sanchez D, Balbir A, Kostuk EW, Shirahata M, Fagerlund MJ, Eriksson LI. The human carotid body transcriptome with focus on oxygen sensing and inflammation: a comparative analysis. J Physiol 590: 3807-3819, 2012.
50. Moya EA, Alcayaga J, Iturriaga R. NO modulation of carotid body chemoreception in health and disease. Respir Physiol Neurobiol 184: 158-164, 2012.
51. Nurse CA. Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp Physiol 95: 657-667, 2010.
52. Ortega-Saenz P, Pascual A, Gomez-Diaz R, Lopez-Barneo J. Acute oxygen sensing in heme oxygenase-2 null mice. J Gen Physiol 128: 405-411, 2006.
53. Paliege A, Rosenberger C, Bondke A, Sciesielski L, Shina A, Heyman SN, Flippin LA, Arend M, Klaus SJ, Bachmann S. Hypoxia-inducible factor-2alpha-expressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. Kidney Int 77: 312-318, 2010.
54. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3: 187-197, 2006.
55. Paton JF, Sobotka PA, Fudim M, Engelman ZJ, Hart EC, McBryde FD, Abdala AP, Marina N, Gourine AV, Lobo M, Patel N, Burchell A, Ratcliffe L, Nightingale A. The carotid body as a therapeutic target for the treatment of sympathetically mediated diseases. Hypertension 61: 5-13, 2013.
56. Peng YJ, Nanduri J, Raghuraman G, Souvannakitti D, Gadalla MM, Kumar GK, Snyder SH, Prabhakar NR. H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci USA 107: 10719-10724, 2010.
57. Peng YJ, Makarenko VV, Nanduri J, Vasavda C, Raghuraman G, Yuan G, Gadalla MM, Kumar GK, Snyder SH, Prabhakar NR. Inherent variations in CO-H2S-mediated carotid body O2 sensing mediate hypertension and pulmonary edema. Proc Natl Acad Sci USA 111: 1174-1179, 2014.
58. Pflüger E. Ueber die Ursache der Athembewegungen, sowie der Dyspnoë und Apnoë. Pflügers Arch Gesamte Physiol Meschen Tiere 1: 61-106, 1868.
59. Prabhakar NR. Sensing hypoxia: physiology, genetics and epigenetics. J Physiol 591: 2245-2257, 2013.
60. Prabhakar NR, Dinerman JL, Agani FH, Snyder SH. Carbon monoxide: a role in carotid body chemoreception. Proc Natl Acad Sci USA 92: 1994-1997, 1995.
61. Prabhakar NR, Kumar GK, Chang CH, Agani FH, Haxhiu MA. Nitric oxide in the sensory function of the carotid body. Brain Res 625: 16-22, 1993.
62. Prabhakar NR, Peers C. Gasotransmitter regulation of ion channels: a key step in O2 sensing by the carotid body. Physiology 29: 49-57, 2014.
63. Prabhakar NR, Semenza GL. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev 92: 967-1003, 2012.
64. Przybylski J. Do arterial chemoreceptors play a role in the pathogenesis of hypertension? Med Hypotheses 7: 127-131, 1981.
65. Rey S, Luo W, Shimoda LA, Semenza GL. Metabolic reprogramming by HIF-1 promotes the survival of bone marrow-derived angiogenic cells in ischemic tissue. Blood 117: 4988-4998, 2011.
66. Rey S, Semenza GL. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86: 236-242, 2010.
67. Safran M, Kim WY, O’Connell F, Flippin L, Günzler V, Horner JW, Depinho RA, Kaelin WG. Mouse model for noninvasive imaging of HIF prolyl hydroxylase activity: assessment of an oral agent that stimulates erythropoietin production. Proc Natl Acad Sci USA 103: 105-110, 2006.
68. Schultz HD, Li YL. Carotid body function in heart failure. Respir Physiol Neurobiol 157: 171-185, 2007.
69. Scortegagna M, Ding K, Zhang Q, Oktay Y, Bennett MJ, Bennett M, Shelton JM, Richardson JA, Moe O, Garcia JA. HIF-2alpha regulates murine hematopoietic development in an erythropoietin-dependent manner. Blood 105: 3133-3140, 2005.
70. Semenza G, Prabhakar N. Neural regulation of hypoxia-inducible factors and redox state drives the pathogenesis of hypertension in a rodent model of sleep apnea. J Appl Physiol. In press
71. Semenza GL. Hypoxia-inducible factor 1 and cardiovascular disease. Annu Rev Physiol 76: 39-56, 2014.
72. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408, 2012.
73. Semenza GL. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood 114: 2015-2019, 2009.
74. Semenza GL. Oxygen homeostasis. Wiley Interdiscip Rev Syst Biol Med 2: 336-361, 2010.
75. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537, 1996.
76. 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 12: 5447-5454, 1992.
77. Shah YM, Matsubara T, Ito S, Yim SH, Gonzalez FJ. Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab 9: 152-164, 2009.
78. Shimoda LA, Laurie SS. HIF and pulmonary vascular responses to hypoxia. J Appl Physiol 116: 867-874, 2014.
79. Smith ML, Niedermaier ON, Hardy SM, Decker MJ, Strohl KP. Role of hypoxemia in sleep apneainduced sympathoexcitation. J Auton Nerv Syst 56: 184-190, 1996.
80. Spivak JL. The biology and clinical applications of recombinant erythropoietin. Semin Oncol 25: 7-11, 1998.
81. Streller T, Huckstorf C, Pfeiffer C, Acker H. Unusual cytochrome a592 with low PO2 affinity correlates as putative oxygen sensor with rat carotid body chemoreceptor discharge. FASEB J 16: 1277-1279, 2002.
82. Strohl KP, Thomas AJ, St Jean P, Schlenker EH, Koletsky RJ, Schork NJ. Ventilation and metabolism among rat strains. J Appl Physiol 82: 317-323, 1997.
83. Takeda K, Aguila HL, Parikh NS, Li X, Lamothe K, Duan LJ, Takeda H, Lee FS, Fong GH. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood 111: 3229-3235, 2008.
84. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, Suda T. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7: 391-402, 2010.
85. Telezhkin V, Brazier SP, Cayzac SH, Wilkinson WJ, Riccardi D, Kemp PJ. Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels. Respir Physiol Neurobiol 172: 169-178, 2010.
86. Trzebski A, Tafil M, Zoltwski M, Przybylski J. Central and peripheral chemosensitivity in early essential hypertension in man. In: Central Neurone Environment and the Control Systems of Breathing and Circulation, edited by Schlaefke ME, Koepchen HP, See W. New York: Springer-Verlag, 1983, p. 204-213.
87. Uniacke J, Holterman CE, Lachance G, Franovic A, Jacob MD, Fabian MR, Payette J, Holcik M, Pause A, Lee S. An oxygen-regulated switch in the protein synthesis machinery. Nature 486: 126-129, 2012.
88. Vidruk EH, Olson EB, Ling L, Mitchell GS. Responses of single-unit carotid body chemoreceptors in adult rats. J Physiol 531: 165-170, 2001.
89. Von Euler U, Liljestrand G, Zotterman Y. The excitation mechanism of the chemoreceptors of the carotid body. Scand Arch Physiol 83: 132-152, 1939.
90. Weil JV. Variation in human ventilatory controlgenetic influence on the hypoxic ventilatory response. Respir Physiol Neurobiol 135: 239-246, 2003.
91. West JB. Oxygen sensing. High Alt Med Biol 13: 67, 2012.
92. Wu CY, Tsai YP, Wu MZ, Teng SC, Wu KJ. Epigenetic reprogramming and post-transcriptional regulation during the epithelial-mesenchymal transition. Trends Genet 28: 454-463, 2012.
93. Xia X, Lemieux ME, Li W, Carroll JS, Brown M, Liu XS, Kung AL. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc Natl Acad Sci USA 106: 4260-4265, 2009.
94. Yoon D, Ponka P, Prchal JT. Hypoxia and hematopoiesis. Am J Physiol Cell Physiol 300: C1215-C1222, 2011.
95. Yuan G, Vasavda C, Peng YJ, Makarenko VV, Raghuraman G, Nanduri J, Gadalla MM, Semenza GL, Kumar GK, Snyder SH, Prabhakar NR. Protein kinase G-regulated production of H2S governs oxygen sensing. Sci Signal 8: ra37, 2015.
96. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283: 10892-10903, 2008.