Hypoxia signaling during acute lung injury

Journal of Applied Physiology

Volumn 119, Issue 10, 2015, Pages 1157-1163

  Vohwinkel, Christine U ^a,b   Hoegl, Sandra ^a,c   Eltzschig, Holger K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b University of Colorado Denver and Children s Hospital Colorado   (United States)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Acute lung injury; Acute respiratory distress syndrome; Carbohydrate metabolism; Glycolysis; HIF1A; Hypoxia; Hypoxia inducible factor; Inflammation; LPS; Lung protection; Mechanical ventilation; Sepsis

Indexed keywords

AUTACOID; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ACUTE LUNG INJURY; ANIMAL; HUMAN; HYPOXIA; LUNG; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACUTE LUNG INJURY; ANIMALS; HUMANS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION MEDIATORS; LUNG; SIGNAL TRANSDUCTION;

EID: 84947236790     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00226.2015     Document Type: Review

References (73)

1. Anonymous. 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: 1301-1308, 2000.
2. Aggarwal NR, D'Alessio FR, Eto Y, Chau E, Avalos C, Waickman AT, Garibaldi BT, Mock JR, Files DC, Sidhaye V, Polotsky VY, Powell J, Horton M, King LS. Macrophage A2A adenosinergic receptor modulates oxygen-induced augmentation of murine lung injury. Am J Respir Cell Mol Biol 48: 635-646, 2013.
3. Ahmad A, Ahmad S, Glover L, Miller SM, Shannon JM, Guo X, Franklin WA, Bridges JP, Schaack JB, Colgan SP, White CW. Adenosine A2A receptor is a unique angiogenic target of HIF-2alpha in pulmonary endothelial cells. Proc Natl Acad Sci USA 106: 10684-10689, 2009.
4. Anderson MR. Update on pediatric acute respiratory distress syndrome. Respir Care 48: 261-276, 2003.
5. Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet 2: 319-323, 1967.
6. Beloncle F, Lorente JA, Esteban A, Brochard L. Update in acute lung injury and mechanical ventilation 2013. Am J Respir Crit Care Med 189: 1187-1193, 2014.
7. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, Lamy M, Legall JR, Morris A, Spragg R. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 149: 818-824, 1994.
8. Bernhardt WM, Wiesener MS, Scigalla P, Chou J, Schmieder RE, Gunzler V, Eckardt KU. Inhibition of prolyl hydroxylases increases erythropoietin production in ESRD. J Am Soc Nephrol 21: 2151-2156, 2010.
9. Campbell EL, Bruyninckx WJ, Kelly CJ, Glover LE, McNamee EN, Bowers BE, Bayless AJ, Scully M, Saeedi BJ, Golden-Mason L, Ehrentraut SF, Curtis VF, Burgess A, Garvey JF, Sorensen A, Nemenoff R, Jedlicka P, Taylor CT, Kominsky DJ, Colgan SP. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity 40: 66-77, 2014.
10. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490, 1998.
11. Clambey ET, McNamee EN, Westrich JA, Glover LE, Campbell EL, Jedlicka P, de Zoeten EF, Cambier JC, Stenmark KR, Colgan SP, Eltzschig HK. Hypoxia-inducible factor-1alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci USA 109: E2784-E2793, 2012.
12. Colgan SP, Eltzschig HK. Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu Rev Physiol 74: 153-175, 2012.
13. Colgan SP, Taylor CT. Hypoxia: an alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol 7: 281-287, 2010.
14. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS. HIF-1alpha is essential for myeloid cellmediated inflammation. Cell 112: 645-657, 2003.
15. Csoka B, Nemeth ZH, Rosenberger P, Eltzschig HK, Spolarics Z, Pacher P, Selmeczy Z, Koscso B, Himer L, Vizi ES, Blackburn MR, Deitch EA, Hasko G. A2B adenosine receptors protect against sepsisinduced mortality by dampening excessive inflammation. J Immunol 185: 542-550, 2010.
16. Cummins EP, Seeballuck F, Keely SJ, Mangan NE, Callanan JJ, Fallon PG, Taylor CT. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134: 156-165, 2008.
17. De Backer D, Creteur J, Zhang H, Norrenberg M, Vincent JL. Lactate production by the lungs in acute lung injury. Am J Respir Crit Care Med 156: 1099-1104, 1997.
18. Eckle T, Brodsky K, Bonney M, Packard T, Han J, Borchers CH, Mariani TJ, Kominsky DJ, Mittelbronn M, Eltzschig HK. HIF1A reduces acute lung injury by optimizing carbohydrate metabolism in the alveolar epithelium. PLoS Biol 11: e1001665, 2013.
19. Eckle T, Fullbier L, Grenz A, Eltzschig HK. Usefulness of pressurecontrolled ventilation at high inspiratory pressures to induce acute lung injury in mice. Am J Physiol Lung Cell Mol Physiol 295: L718-L724, 2008.
20. Eckle T, Fullbier L, Wehrmann M, Khoury J, Mittelbronn M, Ibla J, Rosenberger P, Eltzschig HK. Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J Immunol 178: 8127-8137, 2007.
21. Eckle T, Grenz A, Laucher S, Eltzschig HK. A2B adenosine receptor signaling attenuates acute lung injury by enhancing alveolar fluid clearance in mice. J Clin Invest 118: 3301-3315, 2008.
22. Eckle T, Hughes K, Ehrentraut H, Brodsky KS, Rosenberger P, Choi DS, Ravid K, Weng T, Xia Y, Blackburn MR, Eltzschig HK. Crosstalk between the equilibrative nucleoside transporter ENT2 and alveolar Adora2b adenosine receptors dampens acute lung injury. FASEB J 27: 3078-3089, 2013.
23. Eckle T, Kewley EM, Brodsky KS, Tak E, Bonney S, Gobel M, Anderson D, Glover LE, Riegel AK, Colgan SP, Eltzschig HK. Identification of hypoxia-inducible factor HIF-1A as transcriptional regulator of the A2B adenosine receptor during acute lung injury. J Immunol 192: 1249-1256, 2014.
24. Eltzschig HK, Abdulla P, Hoffman E, Hamilton KE, Daniels D, Schonfeld C, Loffler M, Reyes G, Duszenko M, Karhausen J, Robinson A, Westerman KA, Coe IR, Colgan SP. HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J Exp Med 202: 1493-1505, 2005.
25. Eltzschig HK, Bonney SK, Eckle T. Attenuating myocardial ischemia by targeting A2B adenosine receptors. Trends Mol Med 19: 345-354, 2013.
26. Eltzschig HK, Bratton DL, Colgan SP. Targeting hypoxia signalling for the treatment of ischaemic and inflammatory diseases. Nat Rev Drug Discov 13: 852-869, 2014.
27. Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med 364: 656-665, 2011.
28. Eltzschig HK, Collard CD. Vascular ischaemia and reperfusion injury. Br Med Bull 70: 71-86, 2004.
29. Eltzschig HK, Eckle T. Ischemia and reperfusion-from mechanism to translation. Nat Med 17: 1391-1401, 2011.
30. Eltzschig HK, Sitkovsky MV, Robson SC. Purinergic signaling during inflammation. N Engl J Med 367: 2322-2333, 2012.
31. Erickson SE, Martin GS, Davis JL, Matthay MA, Eisner MD. Recent trends in acute lung injury mortality: 1996-2005. Crit Care Med 37: 1574-1579, 2009.
32. Flight MH. Deal watch: AstraZeneca bets on FibroGen's anaemia drug. Nat Rev Drug Discov 12: 730, 2013.
33. Frohlich S, Murphy N, Ryan D, Boylan JF. Acute respiratory distress syndrome: current concepts and future directions. Anaesth Intensive Care 41: 463-472, 2013.
34. Guerin C, Reignier J, Richard JC, Beuret P, Gacouin A, Boulain T, Mercier E, Badet M, Mercat A, Baudin O, Clavel M, Chatellier D, Jaber S, Rosselli S, Mancebo J, Sirodot M, Hilbert G, Bengler C, Richecoeur J, Gainnier M, Bayle F, Bourdin G, Leray V, Girard R, Baboi L, Ayzac L. Prone positioning in severe acute respiratory distress syndrome. N Engl J Med 368: 2159-2168, 2013.
35. Han S, Mallampalli RK. The acute respiratory distress syndrome: from mechanism to translation. J Immunol 194: 855-860, 2015.
36. Hartmann H, Eltzschig HK, Wurz H, Hantke K, Rakin A, Yazdi AS, Matteoli G, Bohn E, Autenrieth IB, Karhausen J, Neumann D, Colgan SP, Kempf VA. Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores. Gastroenterology 134: 756-767, 2008.
37. Herridge MS, Tansey CM, Matte A, Tomlinson G, Diaz-Granados N, Cooper A, Guest CB, Mazer CD, Mehta S, Stewart TE, Kudlow P, Cook D, Slutsky AS, Cheung AM. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med 364: 1293-1304, 2011.
38. Idzko M, Ferrari D, Eltzschig HK. Nucleotide signalling during inflammation. Nature 509: 310-317, 2014.
39. Idzko M, Ferrari D, Riegel AK, Eltzschig HK. Extracellular nucleotide and nucleoside signaling in vascular and blood disease. Blood 124: 1029-1037, 2014.
40. Johnson ML, Emhoff CA, Horning MA, Brooks GA. Transpulmonary lactate shuttle. Am J Physiol Regul Integr Comp Physiol 302: R143-R149, 2012.
41. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402, 2008.
42. Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, Haase VH. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 114: 1098-1106, 2004.
43. Koivunen P, Hirsila M, Remes AM, Hassinen IE, Kivirikko KI, Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 282: 4524-4532, 2007.
44. Koivunen P, Lee S, Duncan CG, Lopez G, Lu G, Ramkissoon S, Losman JA, Joensuu P, Bergmann U, Gross S, Travins J, Weiss S, Looper R, Ligon KL, Verhaak RG, Yan H, Kaelin WG Jr. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature 483: 484-488, 2012.
45. Kong T, Westerman KA, Faigle M, Eltzschig HK, Colgan SP. HIFdependent induction of adenosine A2B receptor in hypoxia. FASEB J 20: 2242-2250, 2006.
46. Macdougall IC. New anemia therapies: translating novel strategies from bench to bedside. Am J Kidney Dis 59: 444-451, 2012.
47. 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.
48. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol 44: 725-738, 2011.
49. Morote-Garcia JC, Rosenberger P, Kuhlicke J, Eltzschig HK. HIF-1-dependent repression of adenosine kinase attenuates hypoxia-induced vascular leak. Blood 111: 5571-5580, 2008.
50. Nowak-Machen M, Schmelzle M, Hanidziar D, Junger W, Exley M, Otterbein L, Wu Y, Csizmadia E, Doherty G, Sitkovsky M, Robson SC. Pulmonary natural killer T cells play an essential role in mediating hyperoxic acute lung injury. Am J Respir Cell Mol Biol 48: 601-609, 2013.
51. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414: 916-920, 2001.
52. Peyssonnaux C, Cejudo-Martin P, Doedens A, Zinkernagel AS, Johnson RS, Nizet V. Cutting edge: essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J Immunol 178: 7516-7519, 2007.
53. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, Camporota L, Slutsky AS. Acute respiratory distress syndrome: the Berlin Definition. JAMA 307: 2526-2533, 2012.
54. Routsi C, Bardouniotou H, Delivoria-Ioannidou V, Kazi D, Roussos C, Zakynthinos S. Pulmonary lactate release in patients with acute lung injury is not attributable to lung tissue hypoxia. Crit Care Med 27: 2469-2473, 1999.
55. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 353: 1685-1693, 2005.
56. Ryan HE, Lo J, Johnson RS. HIF-1alpha is required for solid tumor formation and embryonic vascularization. EMBO J 17: 3005-3015, 1998.
57. Safran M, Kim WY, O'Connell F, Flippin L, Gunzler V, Horner JW, Depinho RA, Kaelin WG Jr. 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.
58. Samanta D, Gilkes DM, Chaturvedi P, Xiang L, Semenza GL. Hypoxia-inducible factors are required for chemotherapy resistance of breast cancer stem cells. Proc Natl Acad Sci USA 111: E5429-E5438, 2014.
59. Schingnitz U, Hartmann K, Macmanus CF, Eckle T, Zug S, Colgan SP, Eltzschig HK. Signaling through the A2B adenosine receptor dampens endotoxin-induced acute lung injury. J Immunol 184: 5271-5279, 2010.
60. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, Simon MC, Thompson CB, Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7: 77-85, 2005.
61. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29: 625-634, 2009.
62. Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763, 1994.
63. Stapleton RD, Wang BM, Hudson LD, Rubenfeld GD, Caldwell ES, Steinberg KP. Causes and timing of death in patients with ARDS. Chest 128: 525-532, 2005.
64. Sternberg N, Hamilton D. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J Mol Biol 150: 467-486, 1981.
65. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, Eltzschig HK, Hansen KR, Thompson LF, Colgan SP. Ecto-5=-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110: 993-1002, 2002.
66. Tambuwala MM, Cummins EP, Lenihan CR, Kiss J, Stauch M, Scholz CC, Fraisl P, Lasitschka F, Mollenhauer M, Saunders SP, Maxwell PH, Carmeliet P, Fallon PG, Schneider M, Taylor CT. Loss of prolyl hydroxylase-1 protects against colitis through reduced epithelial cell apoptosis and increased barrier function. Gastroenterology 139: 2093-2101, 2010.
67. Taylor CT, McElwain JC. Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. Physiology (Bethesda) 25: 272-279, 2010.
68. Thiel M, Chouker A, Ohta A, Jackson E, Caldwell C, Smith P, Lukashev D, Bittmann I, Sitkovsky MV. Oxygenation inhibits the physiological tissue-protecting mechanism and thereby exacerbates acute inflammatory lung injury. PLoS Biol 3: e174, 2005.
69. Vadasz I, Brochard L. Update in acute lung injury and mechanical ventilation 2011. Am J Respir Crit Care Med 186: 17-23, 2012.
70. Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, Cramer T, Sobolewski A, Condliffe AM, Cowburn AS, Johnson N, Chilvers ER. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J Exp Med 201: 105-115, 2005.
71. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
72. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005: re12, 2005.
73. Yu AY, Shimoda LA, Iyer NV, Huso DL, Sun X, McWilliams R, Beaty T, Sham JS, Wiener CM, Sylvester JT, Semenza GL. Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1alpha. J Clin Invest 103: 691-696, 1999.