The iron cycle and oxidative stress in the lung

Free Radical Biology and Medicine

Volumn 36, Issue 7, 2004, Pages 850-857

  Turi, Jennifer L ^a   Yang, Funmei ^b   Garrick, Michael D ^c   Piantadosi, Claude A ^a   Ghio, Andrew J ^d,e  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^e Human Studies Facility   (United States)

Author keywords

Free radicals; Lung; Membrane transporters; Metals

Indexed keywords

FERRITIN; IRON; LACTOFERRIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; TRANSFERRIN; TRANSFERRIN RECEPTOR;

BRONCHUS; CELL TRANSPORT; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL TRACT; HUMAN; IRON OVERLOAD; IRON STORAGE; IRON TRANSPORT; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG FLUID; MUCOCILIARY CLEARANCE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RETICULOENDOTHELIAL SYSTEM; REVIEW;

EPITHELIAL CELLS; HUMANS; IRON; IRON-BINDING PROTEINS; LUNG; MACROPHAGES; NEUTROPHILS; OXIDATIVE STRESS;

EID: 1542395642     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2003.12.008     Document Type: Review

References (77)

1. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18:1995;321-336.
2. Ghio A.J., Kennedy T.P., Whorton A.R., Crumbliss A.L., Hatch G.E., Hoidal J.R. Role of surface complexed iron in oxidant generation and lung inflammation induced by silicates. Am. J. Physiol. 263(5 Pt 1):1992;L511-L518.
3. Schroeder W.H., Dobson M., Kane D.M., Johnson N.D. Toxic trace elements associated with airborne particulate matter: a review. Japca. 37:1987;1267-1285.
4. Nriagu J.O., Pacyna J.M. Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature. 333:1988;134-139.
5. Ward C.G., Bullen J.J., Rogers H.J. Iron and infection: new developments and their implications. J. Trauma. 41:1996;356-364.
6. Mateos F., Brock J.H., Perez-Arellano J.L. Iron metabolism in the lower respiratory tract. Thorax. 53:1998;594-600.
7. Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., Vercellotti G.M. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267:1992;18148-18153.
8. Olakanmi O., McGowan S.E., Hayek M.B., Britigan B.E. Iron sequestration by macrophages decreases the potential for extracellular hydroxyl radical formation. J. Clin. Invest. 91:1993;889-899.
9. Balla J., Nath K.A., Balla G., Juckett M.B., Jacob H.S., Vercellotti G.M. Endothelial cell heme oxygenase and ferritin induction in rat lung by hemoglobin in vivo. Am. J. Physiol. 268(2 Pt 1):1995;L321-L327.
10. Cozzi A., Santambrogio P., Levi S., Arosio P. Iron detoxifying activity of ferritin: effects of H and L human apoferritins on lipid peroxidation in vitro. FEBS Lett. 277:1990;119-122.
11. Ghio A.J., Carter J.D., Richards J.H., Brighton L.E., Lay J.C., Devlin R.B. Disruption of normal iron homeostasis after bronchial instillation of an iron-containing particle. Am. J. Physiol. 274(3 Pt 1):1998;L396-L403.
12. Rouault T.A., Hentze M.W., Caughman S.W., Harford J.B., Klausner R.D. Binding of a cytosolic protein to the iron-responsive element of human ferritin messenger RNA. Science. 241:1988;1207-1210.
13. Basilion J.P., Rouault T.A., Massinople C.M., Klausner R.D., Burgess W.H. The iron-responsive element-binding protein: localization of the RNA-binding site to the aconitase active-site cleft. Proc. Natl. Acad. Sci. USA. 91:1994;574-578.
14. Beinert H., Kennedy M.C. Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J. 7:1993;1442-1449.
15. Haile D.J., Rouault T.A., Harford J.B., Kennedy M.C., Blondin G.A., Beinert H., Klausner R.D. Cellular regulation of the iron-responsive element binding protein: disassembly of the cubane iron-sulfur cluster results in high-affinity RNA binding. Proc. Natl. Acad. Sci. USA. 89:1992;11735-11739.
16. Kaptain S., Downey W.E., Tang C., Philpott C., Haile D., Orloff D.G., Harford J.B., Rouault T.A., Klausner R.D. A regulated RNA binding protein also possesses aconitase activity. Proc. Natl. Acad. Sci. USA. 88:1991;10109-10113.
17. Kennedy M.C., Mende-Mueller L., Blondin G.A., Beinert H. Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc. Natl. Acad. Sci. USA. 89:1992;11730-11734.
18. Leibold E.A., Munro H.N. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy - and light-subunit mRNAs. Proc. Natl. Acad. Sci. USA. 85:1988;2171-2175.
19. Watts R.N., Ponka P., Richardson D.R. Effects of nitrogen monoxide and carbon monoxide on molecular and cellular iron metabolism: mirror-image effector molecules that target iron. Biochem. J. 369(Pt 3):2003;429-440.
20. Cairo G., Recalcati S., Pietrangelo A., Minotti G. The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage. Free Radic. Biol. Med. 32:2002;1237-1243.
21. Kim S., Ponka P. Role of nitric oxide in cellular iron metabolism. Biometals. 16:2003;125-135.
22. Aisen P., Listowsky I. Iron transport and storage proteins. Annu. Rev. Biochem. 49:1980;357-393.
23. Thorstensen K., Romslo I. The role of transferrin in the mechanism of cellular iron uptake. Biochem. J. 271:1990;1-9.
24. Birgens H.S., Kristensen L.O., Borregaard N., Karle H., Hansen N.E. Lactoferrin-mediated transfer of iron to intracellular ferritin in human monocytes. Eur. J. Haematol. 41:1988;52-57.
25. Markowetz B., Van Snick J.L., Masson P.L. Binding and ingestion of human lactoferrin by mouse alveolar macrophages. Thorax. 34:1979;209-212.
26. van Snick J.L., Markowetz B., Masson P.L. The ingestion and digestion of human lactoferrin by mouse peritoneal macrophages and the transfer of its iron into ferritin. J. Exp. Med. 146:1977;817-827.
27. Breuer W., Epsztejn S., Cabantchik Z.I. Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J. Biol. Chem. 270:1995;24209-24215.
28. Breuer W., Greenberg E., Cabantchik Z.I. Newly delivered transferrin iron and oxidative cell injury. FEBS Lett. 403:1997;213-219.
29. Yang F., Coalson J.J., Bobb H.H., Carter J.D., Banu J., Ghio A.J. Resistance of hypotransferrinemic mice to hyperoxia-induced lung injury. Am. J. Physiol. 277(6 Pt 1):1999;L1214-L1223.
30. Ghio A.J., Carter J.D., Richards J.H., Crissman K.M., Bobb H.H., Yang F. Diminished injury in hypotransferrinemic mice after exposure to a metal-rich particle. Am. J. Physiol. Lung Cell Mol. Physiol. 278:2000;L1051-L1061.
31. Leibold E.A., Guo B. Iron-dependent regulation of ferritin and transferrin receptor expression by the iron-responsive element binding protein. Annu. Rev. Nutr. 12:1992;345-368.
32. Theil E.C., McKenzie R.A., Sierzputowska-Gracz H. Structure and function of IREs, the noncoding mRNA sequences regulating synthesis of ferritin, transferrin receptor and (erythroid) 5-aminolevulinate synthase. Adv. Exp. Med. Biol. 356:1994;111-118.
33. Ghio A.J., Carter J.D., Samet J.M., Reed W., Quay J., Dailey L.A., Richards J.H., Devlin R.B. Metal-dependent expression of ferritin and lactoferrin by respiratory epithelial cells. Am. J. Physiol. 274(5 Pt 1):1998;L728-L736.
34. Upton R.L., Chen Y., Mumby S., Gutteridge J.M., Anning P.B., Nicholson A.G., Evans T.W., Quinlan G.J. Variable tissue expression of transferrin receptors: relevance to acute respiratory distress syndrome. Eur. Respir. J. 22:2003;335-341.
35. Iyer S., Lonnerdal B. Lactoferrin, lactoferrin receptors and iron metabolism. Eur. J. Clin. Nutr. 47:1993;232-241.
36. Lonnerdal B., Iyer S. Lactoferrin: molecular structure and biological function. Annu. Rev. Nutr. 15:1995;93-110.
37. Sanchez L., Calvo M., Brock J.H. Biological role of lactoferrin. Arch. Dis. Child. 67:1992;657-661.
38. Ghio A.J., Carter J.D., Dailey L.A., Devlin R.B., Samet J.M. Respiratory epithelial cells demonstrate lactoferrin receptors that increase after metal exposure. Am. J. Physiol. 276(6 Pt 1):1999;L933-L940.
39. Cakmak I., Vandewetering D.A.M., Marschner H., Bienfait H.F. Involvement of superoxide radical in extracellular ferric reduction by iron-deficient bean roots. Plant Physiol. 85:1987;310-314.
40. de la Guardia M.D., Alcantara E. Ferric chelate reduction by sunflower (Helianthus annuus L) leaves: influence of light, oxygen, iron-deficiency and leaf age. J. Exp. Bot. 47:1996;669-675.
41. Buckhout T.J., Bell P.F., Luster D.G., Chaney R.L. Iron-stress induced redox activity in tomato (Lycopersicum-esculentum mill) is localized on the plasma-membrane. Plant Physiol. 90:1989;151-156.
42. Cross A.R., Jones O.T. Enzymic mechanisms of superoxide production. Biochim. Biophys. Acta. 1057:1991;281-298.
43. Lesuisse E., Casteras-Simon M., Labbe P. Evidence for the Saccharomyces cerevisiae ferrireductase system being a multicomponent electron transport chain. J. Biol. Chem. 271:1996;13578-13583.
44. McKie A.T., Barrow D., Latunde-Dada G.O., Rolfs A., Sager G., Mudaly E., Mudaly M., Richardson C., Barlow D., Bomford A., Peters T.J., Raja K.B., Shirali S., Hediger M.A., Farzaneh F., Simpson R.J. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science. 291:2001;1755-1759.
45. Turi J.L., Wang X., Piantadosi C.A., McKie A.T., Ghio A.J. Dcytb is present in the lung and may mediate superoxide dependent iron transport. Am. J. Respir. Crit. Care Med. 167:2003;A130.
46. Alper S.L. The band 3-related anion exchanger (AE) gene family. Annu. Rev. Physiol. 53:1991;549-564.
47. Kontos H.A., Wei E.P. Superoxide production in experimental brain injury. J. Neurosurg. 64:1986;803-807.
48. Lynch R.E., Fridovich I. Permeation of the erythrocyte stroma by superoxide radical. J. Biol. Chem. 253:1978;4697-4699.
49. Ghio A.J., Nozik-Grayck E., Turi J., Jaspers I., Mercatante D.R., Kole R., Piantadosi C.A. Superoxide-dependent iron uptake: a new role for anion exchange protein 2. Am. J. Respir. Cell Mol. Biol. 29:2003;653-660.
50. Vidal S., Belouchi A.M., Cellier M., Beatty B., Gros P. Cloning and characterization of a second human NRAMP gene on chromosome 12q13. Mamm. Genome. 6:1995;224-230.
51. Lee P.L., Gelbart T., West C., Halloran C., Beutler E. The human Nramp2 gene: characterization of the gene structure, alternative splicing, promoter region and polymorphisms. Blood Cells Mol. Dis. 24:1998;199-215.
52. Fleming M.D., Romano M.A., Su M.A., Garrick L.M., Garrick M.D., Andrews N.C. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc. Natl. Acad. Sci. USA. 95:1998;1148-1153.
53. Lash A., Saleem A. Iron metabolism and its regulation: a review. Ann. Clin. Lab. Sci. 25:1995;20-30.
54. Wang X., Ghio A.J., Yang F., Dolan K.G., Garrick M.D., Piantadosi C.A. Iron uptake and Nramp2/DMT1/DCT1 in human bronchial epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 282:2002;L987-L995.
55. Trinder D., Oates P.S., Thomas C., Sadleir J., Morgan E.H. Localisation of divalent metal transporter 1 (DMT1) to the microvillus membrane of rat duodenal enterocytes in iron deficiency, but to hepatocytes in iron overload. Gut. 46:2000;270-276.
56. Goetz D.H., Holmes M.A., Borregaard N., Bluhm M.E., Raymond K.N., Strong R.K. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell. 10:2002;1033-1043.
57. Yang J., Goetz D., Li J.Y., Wang W., Mori K., Setlik D., Du T., Erdjument-Bromage H., Tempst P., Strong R., Barasch J. An iron delivery pathway mediated by a lipocalin. Mol. Cell. 10:2002;1045-1056.
58. Friedl A., Stoesz S.P., Buckley P., Gould M.N. Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues: cell type-specific pattern of expression. Histochem. J. 31:1999;433-441.
59. Wesselius L.J., Nelson M.E., Skikne B.S. Increased release of ferritin and iron by iron-loaded alveolar macrophages in cigarette smokers. Am. J. Respir. Crit. Care Med. 150:1994;690-695.
60. Ghio A.J., Carter J.D., Samet J.M., Quay J., Wortman I.A., Richards J.H., Kennedy T.P., Devlin R.B. Ferritin expression after in vitro exposures of human alveolar macrophages to silica is iron-dependent. Am. J. Respir. Cell Mol. Biol. 17:1997;533-540.
61. McLemore T.L., Mace M.L. Jr., Roggli V., Marshall M.V., Lawrence E.C., Wilson R.K., Martin R.R., Brinkley B.R., Greenberg S.D. Asbestos body phagocytosis by human free alveolar macrophages. Cancer Lett. 9:1980;85-93.
62. Iancu T.C., Lichterman L., Neustein H.B. Hepatic sinusoidal cells in iron overload: ultrastructural observations. Isr. J. Med. Sci. 14:1978;1191-1201.
63. Abboud S., Haile D.J. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275:2000;19906-19912.
64. McKie A.T., Marciani P., Rolfs A., Brennan K., Wehr K., Barrow D., Miret S., Bomford A., Peters T.J., Farzaneh F., Hediger M.A., Hentze M.W., Simpson R.J. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell. 5:2000;299-309.
65. Yang F., Wang X., Haile D.J., Piantadosi C.A., Ghio A.J. Iron increases expression of iron-export protein MTP1 in lung cells. Am. J. Physiol. Lung Cell Mol. Physiol. 283:2002;L932-L939.
66. Vulpe C.D., Kuo Y.M., Murphy T.L., Cowley L., Askwith C., Libina N., Gitschier J., Anderson G.J. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat. Genet. 21:1999;195-199.
67. Cellier M., Prive G., Belouchi A., Kwan T., Rodrigues V., Chia W., Gros P. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. USA. 92:1995;10089-10093.
68. Gruenheid S., Cellier M., Vidal S., Gros P. Identification and characterization of a second mouse Nramp gene. Genomics. 25:1995;514-525.
69. Skamene E. The Bcg gene story. Immunobiology. 191:1994;451-460.
70. Vidal S.M., Malo D., Vogan K., Skamene E., Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell. 73:1993;469-485.
71. Van Snick J.L., Masson P.L. The binding of human lactoferrin to mouse peritoneal cells. J. Exp. Med. 144:1976;1568-1580.
72. Hamilton T.A., Gray P.W., Adams D.O. Expression of the transferrin receptor on murine peritoneal macrophages is modulated by in vitro treatment with interferon gamma. Cell. Immunol. 89:1984;478-488.
73. Laskey J., Webb I., Schulman H.M., Ponka P. Evidence that transferrin supports cell proliferation by supplying iron for DNA synthesis. Exp. Cell Res. 176:1988;87-95.
74. Sibille J.C., Kondo H., Aisen P. Interactions between isolated hepatocytes and Kupffer cells in iron metabolism: a possible role for ferritin as an iron carrier protein. Hepatology. 8:1988;296-301.
75. Molloy A.L., Winterbourn C.C. Release of iron from phagocytosed Escherichia coli and uptake by neutrophil lactoferrin. Blood. 75:1990;984-989.
76. Birgens H.S. The biological significance of lactoferrin in haematology. Scand. J. Haematol. 33:1984;225-230.
77. Birgens H.S., Hansen N.E., Karle H., Kristensen L.O. Receptor binding of lactoferrin by human monocytes. Br. J. Haematol. 54:1983;383-391.