Methemoglobin-induced signaling and chemokine responses in human alveolar epithelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 1, 2014, Pages

  Mumby, Sharon ^a   Ramakrishnan, Latha ^a   Evans, Timothy W ^a   Griffiths, Mark J D ^a   Quinlan, Gregory J ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Alveolar epithelial cells; Cytokines; Methemoglobin

Indexed keywords

ANTIOXIDANT; AZIDE BOUND METHEMOGLOBIN; FERRIC CITRATE; FERRIC ION; FERRITIN; FERROUS SULFATE; HEMIN; HEMOGLOBIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; IRON CHELATING AGENT; IRON SALT; MESSENGER RNA; METHEMOGLOBIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; OXYHEMOGLOBIN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL ISOLATION; CELL LYSATE; CELL PROLIFERATION; CELL RESPIRATION; CELL VIABILITY; CONCENTRATION RESPONSE; CYTOKINE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SILENCING; HEAVY CHAIN; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOTHESIS; LIGHT CHAIN; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS EPITHELIUM; LUNG PARENCHYMA; LUNG SLICE; MTT ASSAY; OXIDATIVE STRESS; PNEUMONIA; PRIMARY CELL CULTURE; PRIMARY CULTURE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84891543976     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00066.2013     Document Type: Article

References (54)

1. Adamzik M, Hamburger T, Petrat F, Peters J, de Groot H, Hartmann M. Free hemoglobin concentration in severe sepsis: methods of measurement and prediction of outcome. Crit Care 16: R125, 2012.
2. Alayash AI, Patel RP, Cashon RE. Redox reactions of hemoglobin and myoglobin: biological and toxicological implications. Antioxid Redox Signal 3: 313-327, 2001.
3. Antoniades HN, Neville-Golden J, Galanopoulos T, Kradin RL, Valente AJ, Graves DT. Expression of monocyte chemoattractant protein 1 mRNA in human idiopathic pulmonary fibrosis. Proc Natl Acad Sci USA 89: 5371-5375, 1992.
4. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 90: 9285-9289, 1993.
5. Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Jacob HS, Eaton JW, Balla G. Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and dies) in an iron-rich environment. Antioxid Redox Signal 9: 2119-2137, 2007.
6. Bastarache JA, Sebag SC, Clune JK, Grove BS, Lawson WE, Janz DR, Roberts LJ 2nd, Dworski R, Mackman N, Ware LB. Low levels of tissue factor lead to alveolar haemorrhage, potentiating murine acute lung injury and oxidative stress. Thorax 67: 1032-1039, 2012.
7. Bodet C, Chandad F, Grenier D. Hemoglobin and LPS act in synergy to amplify the inflammatory response. J Dent Res 86: 878-882, 2007.
8. Brandenburg K, Garidel P, Andra J, Jurgens G, Muller M, Blume A, Koch MH, Levin J. Cross-linked hemoglobin converts endotoxically inactive pentaacyl endotoxins into a physiologically active conformation. J Biol Chem 278: 47660-47669, 2003.
9. Carrillo EH, Gordon LE, Richardson JD, Polk HC Jr. Free hemoglobin enhances tumor necrosis factor-alpha production in isolated human monocytes. J Trauma 52: 449-452, 2002.
10. Chavko M, Adeeb S, Ahlers ST, McCarron RM. Attenuation of pulmonary inflammation after exposure to blast overpressure by N-acetylcysteine amide. Shock 32: 325-331, 2009.
11. Chen-Roetling J, Li Z, Chen M, Awe OO, Regan RF. Heme oxygenase activity and hemoglobin neurotoxicity are attenuated by inhibitors of the MEK/ERK pathway. Neuropharmacology 56: 922-928, 2009.
12. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, Horii T, Akira S. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201: 19-25, 2005.
13. Cosgrove S, Chotirmall SH, Greene CM, McElvaney NG. Pulmonary proteases in the cystic fibrosis lung induce interleukin 8 expression from bronchial epithelial cells via a heme/meprin/epidermal growth factor receptor/Toll-like receptor pathway. J Biol Chem 286: 7692-7704, 2011.
14. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134-L147, 1990.
15. Donnelly SC, Strieter RM, Kunkel SL, Walz A, Robertson CR, Carter DC, Grant IS, Pollok AJ, Haslett C. Interleukin-8 and development of adult respiratory distress syndrome in at-risk patient groups. Lancet 341: 643-647, 1993.
16. Elssner A, Jaumann F, Dobmann S, Behr J, Schwaiblmair M, Reichenspurner H, Furst H, Briegel J, Vogelmeier C. Elevated levels of interleukin-8 and transforming growth factor-beta in bronchoalveolar lavage fluid from patients with bronchiolitis obliterans syndrome: proinflammatory role of bronchial epithelial cells. Munich Lung Transplant Group. Transplantation 70: 362-367, 2000.
17. Feng L, Zhou X, Su LX, Feng D, Jia YH, Xie LX. Clinical significance of soluble hemoglobin scavenger receptor CD163 (sCD163) in sepsis, a prospective study. PLoS One 7: e38400, 2012.
18. Figueiredo RT, Fernandez PL, Mourao-Sa DS, Porto BN, Dutra FF, Alves LS, Oliveira MF, Oliveira PL, Graca-Souza AV, Bozza MT. Characterization of heme as activator of Toll-like receptor 4. J Biol Chem 282: 20221-20229, 2007.
19. Ghio AJ, Richards JH, Crissman KM, Carter JD. Iron disequilibrium in the rat lung after instilled blood. Chest 118: 814-823, 2000.
20. Gow AJ, Luchsinger BP, Pawloski JR, Singel DJ, Stamler JS. The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci USA 96: 9027-9032, 1999.
21. Graca-Souza AV, Arruda MA, de Freitas MS, Barja-Fidalgo C, Oliveira PL. Neutrophil activation by heme: implications for inflammatory processes. Blood 99: 4160-4165, 2002.
22. Griffith JW, Sun T, McIntosh MT, Bucala R. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208-5220, 2009.
23. Halliwell B, Gutteridge J. Free Radicals in Biology and Medicine. New York: Oxford University Press, 2007.
24. Huang FP, Xi G, Keep RF, Hua Y, Nemoianu A, Hoff JT. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J Neurosurg 96: 287-293, 2002.
25. Janz DR, Bastarache JA, Peterson JF, Sills G, Wickersham N, May AK, Roberts LJ 2nd, Ware LB. Association between cell-free hemoglobin, acetaminophen, and mortality in patients with sepsis: an observational study. Crit Care Med 41: 784-790, 2013.
26. Jurgens G, Muller M, Koch MH, Brandenburg K. Interaction of hemoglobin with enterobacterial lipopolysaccharide and lipid A. Physicochemical characterization and biological activity. Eur J Biochem 268: 4233-4242, 2001.
27. Kaca W, Roth RI, Levin J. Hemoglobin, a newly recognized lipopolysaccharide (LPS)-binding protein that enhances LPS biological activity. J Biol Chem 269: 25078-25084, 1994.
28. Lagan AL, Melley DD, Evans TW, Quinlan GJ. Pathogenesis of the systemic inflammatory syndrome and acute lung injury: role of iron mobilization and decompartmentalization. Am J Physiol Lung Cell Mol Physiol 294: L161-L174, 2008.
29. Lin M, Rippe RA, Niemela O, Brittenham G, Tsukamoto H. Role of iron in NF-κB activation and cytokine gene expression by rat hepatic macrophages. Am J Physiol Gastrointest Liver Physiol 272: G1355-G1364, 1997.
30. Lisk C, Kominsky D, Ehrentraut S, Bonaventura J, Nuss R, Hassell K, Nozik-Grayck E, Irwin DC. Hemoglobin-induced endothelial cell permeability is controlled, in part, via a myeloid differentiation primary response gene-88-dependent signaling mechanism. Am J Respir Cell Mol Biol 49: 619-626, 2013.
31. Liu X, Spolarics Z. Methemoglobin is a potent activator of endothelial cells by stimulating IL-6 and IL-8 production and E-selectin membrane expression. Am J Physiol Cell Physiol 285: C1036-C1046, 2003.
32. Lu H, Shi JX, Zhang DM, Shen J, Lin YX, Hang CH, Yin HX. Hemolysate-induced expression of intercellular adhesion molecule-1 and monocyte chemoattractant protein-1 expression in cultured brain microvascular endothelial cells via through ROS-dependent NF-κB pathways. Cell Mol Neurobiol 29: 87-95, 2009.
33. Lumadue JA, Lanzkron SM, Kennedy SD, Kuhl DT, Kickler TS. Cytokine induction of platelet activation. Am J Clin Pathol 106: 795-798, 1996.
34. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 122: 2731-2740, 2012.
35. McFaul SJ, Bowman PD, Villa VM, Gutierrez-Ibanez MJ, Johnson M, Smith D. Hemoglobin stimulates mononuclear leukocytes to release interleukin-8 and tumor necrosis factor alpha. Blood 84: 3175-3181, 1994.
36. Miller EJ, Cohen AB, Nagao S, Griffith D, Maunder RJ, Martin TR, Weiner-Kronish JP, Sticherling M, Christophers E, Matthay MA. Elevated levels of NAP-1/interleukin-8 are present in the airspaces of patients with the adult respiratory distress syndrome and are associated with increased mortality. Am Rev Respir Dis 146: 427-432, 1992.
37. Misra HP, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem 247: 6960-6962, 1972.
38. Muller JM, Rupec RA, Baeuerle PA. Study of gene regulation by NF-κB and AP-1 in response to reactive oxygen intermediates. Methods 11: 301-312, 1997.
39. Natarajan R, Fisher BJ, Fowler AA 3rd. Hypoxia inducible factor-1 modulates hemin-induced IL-8 secretion in microvascular endothelium. Microvasc Res 73: 163-172, 2007.
40. Quinlan GJ, Evans TW, Gutteridge JM. Iron and the redox status of the lungs. Free Radic Biol Med 33: 1306-1313, 2002.
41. Reeder BJ, Wilson MT. Hemoglobin and myoglobin associated oxidative stress: from molecular mechanisms to disease states. Curr Med Chem 12: 2741-2751, 2005.
42. Reiter CD, Wang X, Tanus-Santos JE, Hogg N, Cannon RO 3rd, Schechter AN, Gladwin MT. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med 8: 1383-1389, 2002.
43. Roth RI. Hemoglobin enhances the production of tissue factor by endothelial cells in response to bacterial endotoxin. Blood 83: 2860-2865, 1994.
44. Schulz C, Farkas L, Wolf K, Kratzel K, Eissner G, Pfeifer M. Differences in LPS-induced activation of bronchial epithelial cells (BEAS-2B) and type II-like pneumocytes (A-549). Scand J Immunol 56: 294-302, 2002.
45. Sekine Y, Yasufuku K, Heidler KM, Cummings OW, Van Rooijen N, Fujisawa T, Brown J, Wilkes DS. Monocyte chemoattractant protein-1 and RANTES are chemotactic for graft infiltrating lymphocytes during acute lung allograft rejection. Am J Respir Cell Mol Biol 23: 719-726, 2000.
46. Shiu YT, Udden MM, McIntire LV. Perfusion with sickle erythrocytes up-regulates ICAM-1 and VCAM-1 gene expression in cultured human endothelial cells. Blood 95: 3232-3241, 2000.
47. Silva G, Jeney V, Chora A, Larsen R, Balla J, Soares MP. Oxidized hemoglobin is an endogenous proinflammatory agonist that targets vascular endothelial cells. J Biol Chem 284: 29582-29595, 2009.
48. Smith KR, Veranth JM, Hu AA, Lighty JS, Aust AE. Interleukin-8 levels in human lung epithelial cells are increased in response to coal fly ash and vary with the bioavailability of iron, as a function of particle size and source of coal. Chem Res Toxicol 13: 118-125, 2000.
49. Solomon SB, Wang D, Sun J, Kanias T, Feng J, Helms CC, Solomon MA, Alimchandani M, Quezado M, Gladwin MT, Kim-Shapiro DB, Klein HG, Natanson C. Mortality increases after massive exchange transfusion with older stored blood in canines with experimental pneumonia. Blood 121: 1663-1672, 2013.
50. Suzuki YJ, Forman HJ, Sevanian A. Oxidants as stimulators of signal transduction. Free Radic Biol Med 22: 269-285, 1997.
51. Thorley AJ, Grandolfo D, Lim E, Goldstraw P, Young A, Tetley TD. Innate immune responses to bacterial ligands in the peripheral human lung-role of alveolar epithelial TLR expression and signalling. PLoS One 6: e21827, 2011.
52. Tsemakhovich VA, Bamm VV, Shaklai M, Shaklai N. Vascular damage by unstable hemoglobins: the role of heme-depleted globin. Arch Biochem Biophys 436: 307-315, 2005.
53. Xiong S, She H, Takeuchi H, Han B, Engelhardt JF, Barton CH, Zandi E, Giulivi C, Tsukamoto H. Signaling role of intracellular iron in NF-κB activation. J Biol Chem 278: 17646-17654, 2003.
54. Yang F, Haile DJ, Berger FG, Herbert DC, Van Beveren E, Ghio AJ. Haptoglobin reduces lung injury associated with exposure to blood. Am J Physiol Lung Cell Mol Physiol 284: L402-L409, 2003.