Sustained submicromolar H2O2 levels induce hepcidin via signal transducer and activator of transcription 3 (STAT3)

Journal of Biological Chemistry

Volumn 287, Issue 44, 2012, Pages 37472-37482

  Millonig, Gunda ^a   Ganzleben, Ingo ^a   Peccerella, Teresa ^a   Casanovas, Guillem ^a   Brodziak Jarosz, Lidia ^b   Breitkopf Heinlein, Katja ^a   Dick, Tobias P ^b   Seitz, Helmut Karl ^a   Muckenthaler, Martina U ^a   Mueller, Sebastian ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRACELLULAR; HEPCIDIN; INTRACELLULAR IRON; IRON METABOLISM; LIVER CELLS; SIGNAL TRANSDUCERS; UP-REGULATION;

IRON; PATHOLOGY;

ENZYME ACTIVITY;

ACETYLCYSTEINE; ANTIMYCIN A1; BONE MORPHOGENETIC PROTEIN 6; CATALASE; GLUCOSE OXIDASE; GLYCOPROTEIN GP 130; HEPCIDIN; HYDROGEN PEROXIDE; JANUS KINASE 1; JANUS KINASE 2; RECOMBINANT INTERLEUKIN 6; ROTENONE; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; ANTIMICROBIAL CATIONIC PEPTIDE; AUTACOID; BMP6 PROTEIN, HUMAN; INTERLEUKIN 6; SCAVENGER; STAT3 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME RELEASE; GENE OVEREXPRESSION; HEPATOMA CELL; HUMAN; HUMAN CELL; IRON METABOLISM; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROMOTER REGION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ACETYLCYSTEINE; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; BONE MORPHOGENETIC PROTEIN 6; CELL LINE, TUMOR; FREE RADICAL SCAVENGERS; HUMANS; HYDROGEN PEROXIDE; INFLAMMATION MEDIATORS; INTERLEUKIN-6; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84868258078     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.358911     Document Type: Article

References (48)

1. Cartwright, G. E., and Lauretsen, M. A. (1946) The anemia associated with chronic infection. Science 103, 72
2. Ganz, T. (2002) The role of hepcidin in iron sequestration during infections and in the pathogenesis of anemia of chronic disease. Isr. Med. Assoc. J. 4, 1043-1045
3. Nemeth, E., Valore, E. V., Territo, M., Schiller, G., Lichtenstein, A., and Ganz, T. (2003) Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101, 2461-2463
4. Nicolas, G., Bennoun, M., Porteu, A., Mativet, S., Beaumont, C., Grandchamp, B., Sirito, M., Sawadogo, M., Kahn, A., and Vaulont, S. (2002) Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc. Natl. Acad. Sci. U.S.A. 99, 4596-4601
5. Nemeth, E., Tuttle, M. S., Powelson, J., Vaughn, M. B., Donovan, A., Ward, D. M., Ganz, T., and Kaplan, J. (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306, 2090-2093
6. Nemeth, E., Rivera, S., Gabayan, V., Keller, C., Taudorf, S., Pedersen, B. K., and Ganz, T. (2004) IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 113, 1271-1276
7. Roy, C. N., Custodio, A. O., de Graaf, J., Schneider, S., Akpan, I., Montross, L. K., Sanchez, M., Gaudino, A., Hentze, M. W., Andrews, N. C., and Muckenthaler, M. U. (2004) An Hfe-dependent pathway mediates hyposideremia in response to lipopolysaccharide-induced inflammation in mice. Nat. Genet. 36, 481-485
8. Verga Falzacappa, M. V., Vujic Spasic, M., Kessler, R., Stolte, J., Hentze, M. W., and Muckenthaler, M. U. (2007) STAT3 mediates hepatic hepcidin expression and its inflammatory stimulation. Blood 109, 353-358
9. Truksa, J., Lee, P., and Beutler, E. (2007) The role of STAT, AP-1, E-box and TIEG motifs in the regulation of hepcidin by IL-6 and BMP-9. Lessons from human HAMP and murine Hamp1 and Hamp2 gene promoters. Blood Cells Mol. Dis. 39, 255-262
10. Island, M. L., Fatih, N., Leroyer, P., Brissot, P., and Loreal, O. GATA-4 transcription factor regulates hepatic hepcidin expression. Biochem. J. 437, 477-482
11. Bagu, E. T., and Santos, M. M. Friend of GATA suppresses the GATAinduced transcription of hepcidin in hepatocytes through a GATA-regulatory element in the HAMP promoter. J. Mol. Endocrinol. 47, 299-313
12. Casanovas, G., Mleczko-Sanecka, K., Altamura, S., Hentze, M. W., and Muckenthaler, M. U. (2009) Bone morphogenetic protein (BMP)-responsive elements located in the proximal and distal hepcidin promoter are critical for its response to HJV/BMP/SMAD. J. Mol. Med. 87, 471-480
13. Klebanoff, S. J. (1988) Phagocytic cells. Products of oxygen metabolism. in Inflammation: Basic Principles and Clinical Correlates (Snyderman, R., ed) pp. 391-444, Raven Press, New York
14. Geiszt, M., and Leto, T. L. (2004) The Nox family of NAD(P)H oxidases. Host defense and beyond. J. Biol. Chem. 279, 51715-51718
15. Mueller, S., and Arnhold, J. (1995) Fast and sensitive chemiluminescence determination of H2O2 concentration in stimulated human neutrophils. J. Biolumin. Chemilumin. 10, 229-237
16. Hentze, M. W., Muckenthaler, M. U., and Andrews, N. C. (2004) Balancing acts. Molecular control of mammalian iron metabolism. Cell 117, 285-297
17. Martins, E. A., Robalinho, R. L., and Meneghini, R. (1995) Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Arch. Biochem. Biophys. 316, 128-134
18. Pantopoulos, K., and Hentze, M. W. (1995) Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J. 14, 2917-2924
19. Andriopoulos, B., Hegedüsch, S., Mangin, J., Riedel, H. D., Hebling, U., Wang, J., Pantopoulos, K., and Mueller, S. (2007) Sustained hydrogen peroxide induces iron uptake by transferrin receptor-1 independent of the iron regulatory protein/iron-responsive element network. J. Biol. Chem. 282, 20301-20308
20. Harrison-Findik, D. D., Schafer, D., Klein, E., Timchenko, N. A., Kulaksiz, H., Clemens, D., Fein, E., Andriopoulos, B., Pantopoulos, K., and Gollan, J. (2006) Alcohol metabolism-mediated oxidative stress down-regulates hepcidin transcription and leads to increased duodenal iron transporter expression. J. Biol. Chem. 281, 22974-22982
21. Miura, K., Taura, K., Kodama, Y., Schnabl, B., and Brenner, D. A. (2008) Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology 48, 1420-1429
22. Mueller, S., Millonig, G., and Waite, G. N. (2009) The GOX/CAT system. A novel enzymatic method to independently control hydrogen peroxide and hypoxia in cell culture. Adv. Med. Sci. 54, 121-135
23. Mütze, S., Hebling, U., Stremmel, W., Wang, J., Arnhold, J., Pantopoulos, K., and Mueller, S. (2003) Myeloperoxidase-derived hypochlorous acid antagonizes the oxidative stress-mediated activation of iron regulatory protein 1. J. Biol. Chem. 278, 40542-40549
24. Mueller, S., Pantopoulos, K., Hübner, C. A., Stremmel, W., and Hentze, M. W. (2001) IRP1 activation by extracellular oxidative stress in the perfused rat liver. J. Biol. Chem. 276, 23192-23196
25. Mueller, S. (2000) Sensitive and nonenzymatic measurement of hydrogen peroxide in biological systems. Free Radic. Biol. Med. 29, 410-415
26. Mueller, S., Riedel, H. D., and Stremmel, W. (1997) Determination of catalase activity at physiological hydrogen peroxide concentrations. Anal. Biochem. 245, 55-60
27. Millonig, G., Hegedüsch, S., Becker, L., Seitz, H. K., Schuppan, D., and Mueller, S. (2009) Hypoxia-inducible factor 1 α under rapid enzymatic hypoxia. Cells sense decrements of oxygen but not hypoxia per se. Free Radic. Biol. Med. 46, 182-191
28. Miller, E. W., Tulyathan, O., Isacoff, E. Y., and Chang, C. J. (2007) Molecular imaging of hydrogen peroxide produced for cell signaling. Nat. Chem. Biol. 3, 263-267
29. Verga Falzacappa, M. V., Casanovas, G., Hentze, M. W., and Muckenthaler, M. U. (2008) A bone morphogenetic protein (BMP)-responsive element in the hepcidin promoter controls HFE2-mediated hepatic hepcidin expression and its response to IL-6 in cultured cells. J. Mol. Med. 86, 531-540
30. Franke, K., Curth, K., Lenart, J., Knochenhauer, D., and Kietzmann, T. (2004) Enhanced plasminogen activator inhibitor-1 expression in transgenic mice with hepatocyte-specific overexpression of superoxide dismutase or glutathione peroxidase. Antioxid. Redox Signal. 6, 721-728
31. BelAiba, R. S., Djordjevic, T., Bonello, S., Flügel, D., Hess, J., Kietzmann, T., and Görlach, A. (2004) Redox-sensitive regulation of the HIF pathway under non-hypoxic conditions in pulmonary artery smooth muscle cells. Biol. Chem. 385, 249-257
32. Murray, P. J. (2007) The JAK-STAT signaling pathway. Input and output integration. J. Immunol. 178, 2623-2629
33. Guschin, D., Rogers, N., Briscoe, J., Witthuhn, B., Watling, D., Horn, F., Pellegrini, S., Yasukawa, K., Heinrich, P., and Stark, G. R. (1995) A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J. 14, 1421-1429
34. Loschen, G., Flohé, L., and Chance, B. (1971) Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett. 18, 261-264
35. Boveris, A., Oshino, R., Erecińska, M., and Chance, B. (1971) Reduction of mitochondrial components by durohydroquinone. Biochim. Biophys. Acta 245, 1-16
36. Moritz, R. L., Hall, N. E., Connolly, L. M., and Simpson, R. J. (2001) Determination of the disulfide structure and N-glycosylation sites of the extracellular domain of the human signal transducer gp130. J. Biol. Chem. 276, 8244-8253
37. Test, S. T., and Weiss, S. J. (1984) Quantitative and temporal characterization of the extracellular H2O2 pool generated by human neutrophils. J. Biol. Chem. 259, 399-405
38. de Oliveira-Marques, V., Cyrne, L., Marinho, H. S., and Antunes, F. (2007) A quantitative study of NF-κB activation by H2O2. Relevance in inflammation and synergy with TNF-α. J. Immunol. 178, 3893-3902
39. Nishina, S., Hino, K., Korenaga, M., Vecchi, C., Pietrangelo, A., Mizukami, Y., Furutani, T., Sakai, A., Okuda, M., Hidaka, I., Okita, K., and Sakaida, I. (2008) Hepatitis C virus-induced reactive oxygen species raise hepatic iron level in mice by reducing hepcidin transcription. Gastroenterology 134, 226-23
40. Courselaud, B., Pigeon, C., Inoue, Y., Inoue, J., Gonzalez, F. J., Leroyer, P., Gilot, D., Boudjema, K., Guguen-Guillouzo, C., Brissot, P., Loréal, O., and Ilyin, G. (2002) C/EBPβ regulates hepatic transcription of hepcidin, an antimicrobial peptide and regulator of iron metabolism. Cross-talk between C/EBP pathway and iron metabolism. J. Biol. Chem. 277, 41163-41170
41. Devary, Y., Gottlieb, R. A., Lau, L. F., and Karin, M. (1991) Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol. Cell. Biol. 11, 2804-2811
42. Mueller, S., and Pantopoulos, K. (2002) Activation of iron regulatory protein-1 (IRP1) by oxidative stress. Methods Enzymol. 348, 324-337
43. Schieffer, B., Luchtefeld, M., Braun, S., Hilfiker, A., Hilfiker-Kleiner, D., and Drexler, H. (2000) Role of NAD(P)H oxidase in angiotensin II-induced JAK/STAT signaling and cytokine induction. Circ. Res. 87, 1195-1201
44. Moirand, R., Mortaji, A. M., Loréal, O., Paillard, F., Brissot, P., and Deugnier, Y. (1997) A new syndrome of liver iron overload with normal transferrin saturation. Lancet 349, 95-97
45. Riva, A., Trombini, P., Mariani, R., Salvioni, A., Coletti, S., Bonfadini, S., Paolini, V., Pozzi, M., Facchetti, R., Bovo, G., and Piperno, A. (2008) Revaluation of clinical and histological criteria for diagnosis of dysmetabolic iron overload syndrome. World J. Gastroenterol. 14, 4745-4752
46. Livingston, J. N., Gurny, P. A., and Lockwood, D. H. (1977) Insulin-like effects of polyamines in fat cells. Mediation by H2O2 formation. J. Biol. Chem. 252, 560-562
47. Ikemura, M., Nishikawa, M., Hyoudou, K., Kobayashi, Y., Yamashita, F., and Hashida, M. (2010) Improvement of insulin resistance by removal of systemic hydrogen peroxide by PEGylated catalase in obese mice. Mol. Pharm. 7, 2069-2076
48. Litwin, J. A., Völkl, A.,Müller-Höcker, J., Hashimoto, T., and Fahimi, H. D. (1987) Immunocytochemical localization of peroxisomal enzymes in human liver biopsies. Am J Pathol 128, 141-150