Iron-mediated oxidative stress plays an essential role in ferritin-induced cell death

Free Radical Biology and Medicine

Volumn 48, Issue 10, 2010, Pages 1347-1357

  Bresgen, Nikolaus ^a   Jaksch, Heidi ^a   Lacher, Heide ^a   Ohlenschläger, Ingo ^a   Uchida, Koji ^b   Eckl, Peter M ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Ferritin; Free radicals; Hydroxynonenal; Iron; Lipid peroxidation; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; FAS ANTIGEN; FERRITIN; FERROUS ION; IRON; PROTEIN P53; TROLOX C;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CONTROLLED STUDY; DNA DAMAGE; ENDOCYTOSIS; FEMALE; FENTON REACTION; IRON CHELATION; LIPID PEROXIDATION; LIVER CELL; LYSOSOME; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; RAT; UPREGULATION;

ALDEHYDES; ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHROMANS; DEFEROXAMINE; FEMALE; FERRITINS; FREE RADICAL SCAVENGERS; HEPATOCYTES; IRON; IRON CHELATING AGENTS; LIPID PEROXIDATION; OXIDATIVE STRESS; RATS; RATS, INBRED F344;

RATTUS;

EID: 77951939586     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.02.019     Document Type: Article

References (73)

1. Harrison P.M., Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1996, 1275:161-203.
2. Levi S., Santambrogio P., Cozzi A., Rovida E., Corsi B., Tamborini E., Spada S., Albertini A., Arosio P. The role of the L-chain in ferritin iron incorporation: studies of homo and heteropolymers. J. Mol. Biol. 1994, 238:649-654.
3. Sammarco M.C., Ditch S., Banerjee A., Grabczyk E. Ferritin L and H subunits are differentially regulated on a post-transcriptional level. J. Biol. Chem. 2008, 283:4578-4587.
4. 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. 1990, 277:119-122.
5. Zhao G., Arosio P., Chasteen N.D. Iron(II) and hydrogen peroxide detoxification by human H-chain ferritin: an EPR spin-trapping study. Biochemistry 2006, 45:3429-3436.
6. Berberat P.O., Katori M., Kaczmarek E., Anselmo D., Lassman C., Ke B., Shen X., Busuttil R.W., Yamashita K., Csizmadia E., Tyagi S., Otterbein L.E., Brouard S., Tobiasch E., Bach F.H., Kupiec-Weglinski J.W., Soares M.P. Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury. FASEB J. 2003, 17:1724-1726.
7. Ghosh S., Hevi S., Chuck S.L. Regulated secretion of glycosylated human ferritin from hepatocytes. Blood 2004, 103:2369-2376.
8. Sirota L., Kupfer B., Moroz C. Placental isoferritin as a physiological downregulator of cellular immunoreactivity during pregnancy. Clin. Exp. Immunol. 1989, 77:257-262.
9. Hann H.W., Kim C.Y., London W.T., Blumberg B.S. Increased serum ferritin in chronic liver disease: a risk factor for primary hepatocellular carcinoma. Int. J. Cancer 1989, 43:376-379.
10. You S.A., Wang Q. Ferritin in atherosclerosis. Clin. Chim. Acta 2005, 357:1-16.
11. Recalcati S., Invernizzi P., Arosio P., Cairo G. New functions for an iron storage protein: the role of ferritin in immunity and autoimmunity. J. Autoimmun. 2008, 30:84-89.
12. Zandman-Goddard G., Shoenfeld Y. Ferritin in autoimmune diseases. Autoimmun. Rev. 2007, 6:457-463.
13. Koc M., Taysi S., Sezen O., Bakan N. Levels of some acute-phase proteins in the serum of patients with cancer during radiotherapy. Biol. Pharm. Bull. 2003, 26:1494-1497.
14. Bresgen N., Ohlenschlager I., Wacht N., Afazel S., Ladurner G., Eckl P.M. Ferritin and FasL (CD95L) mediate density dependent apoptosis in primary rat hepatocytes. J. Cell. Physiol 2008, 217:800-808.
15. Gray C.P., Arosio P., Hersey P. Association of increased levels of heavy-chain ferritin with increased CD4+ CD25+ regulatory T-cell levels in patients with melanoma. Clin. Cancer Res. 2003, 9:2551-2559.
16. Miyata Y., Koga S., Nishikido M., Hayashi T., Kanetake H. Relationship between serum ferritin levels and tumour status in patients with renal cell carcinoma. BJU Int. 2001, 88:974-977.
17. Riley R.D., Heney D., Jones D.R., Sutton A.J., Lambert P.C., Abrams K.R., Young B., Wailoo A.J., Burchill S.A. A systematic review of molecular and biological tumor markers in neuroblastoma. Clin. Cancer Res. 2004, 10:4-12.
18. Tran T.N., Eubanks S.K., Schaffer K.J., Zhou C.Y., Linder M.C. Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 1997, 90:4979-4986.
19. Gray C.P., Franco A.V., Arosio P., Hersey P. Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int. J. Cancer 2001, 92:843-850.
20. Fisher J., Devraj K., Ingram J., Slagle-Webb B., Madhankumar A.B., Liu X., Klinger M., Simpson I.A., Connor J.R. Ferritin: a novel mechanism for delivery of iron to the brain and other organs. Am. J. Physiol., Cell Physiol. 2007, 293:C641-C649.
21. Broxmeyer H., Bognacki J., Dorner M., de Sousa M. Identification of leukemia-associated inhibitory activity as acidic isoferritins: a regulatory role for acidic isoferritins in the production of granulocytes and macrophages. J. Exp. Med. 1981, 153:1426-1444.
22. Moroz C., Traub L., Maymon R., Zahalka M.A. PLIF, a novel human ferritin subunit from placenta with immunosuppressive activity. J. Biol. Chem. 2002, 277:12901-12905.
23. Bresgen N., Ohlenschlager I., Fiedler B., Wacht N., Zach S., Dunkelmann B., Arosio P., Kuffner E., Lottspeich F., Eckl P.M. Ferritin-a mediator of apoptosis?. J. Cell. Physiol. 2007, 212:157-164.
24. Moroz C., Grunspan A., Zahalka M.A., Traub L., Kodman Y., Yaniv I. Treatment of human bone marrow with recombinant placenta immunoregulator ferritin results in myelopoiesis and T-cell suppression through modulation of the cytokine-chemokine networks. Exp. Hematol. 2006, 34:159-166.
25. Zahalka M.A., Barak V., Traub L., Moroz C. PLIF induces IL-10 production in monocytes: a calmodulin-p38 mitogen-activated protein kinase-dependent pathway. FASEB J. 2003, 17:955-957.
26. Ruddell R.G., Hoang-Le D., Barwood J.M., Rutherford P.S., Piva T.J., Watters D.J., Santambrogio P., Arosio P., Ramm G.A. Ferritin functions as a proinflammatory cytokine via iron-independent protein kinase C zeta/nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 2009, 49:887-900.
27. Chen T.T., Li L., Chung D.H., Allen C.D.C., Torti S.V., Torti F.M., Cyster J.G., Chen C.Y., Brodsky F.M., Niemi E.C., Nakamura M.C., Seaman W.E., Daws M.R. TIM-2 is expressed on B cells and in liver and kidney and is a receptor for H-ferritin endocytosis. J. Exp. Med. 2005, 202:955-965.
28. Moss D., Hibbs A.R., Stenzel D., Powell L.W., Halliday J.W. The endocytic pathway for H-ferritin established in live MOLT-4 cells by laser scanning confocal microscopy. Br. J. Haematol. 1994, 88:746-753.
29. Moss D., Powell L.W., Arosio P., Halliday J.W. Effect of cell proliferation on H-ferritin receptor expression in human T lymphoid (MOLT-4) cells. J. Lab. Clin. Med. 1992, 120:239-243.
30. Fargion S., Cappellini M.D., Fracanzani A.L., De Feo T.M., Levi S., Arosio P., Fiorelli G. Binding and suppressive activity of human recombinant ferritins on erythroid cells. Am. J. Hematol. 1992, 39:264-268.
31. Kroemer G., Jaattela M. Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 2005, 5:886-897.
32. Nilsson E., Ghassemifar R., Brunk U.T. Lysosomal heterogeneity between and within cells with respect to resistance against oxidative stress. Histochem. J. 1997, 29:857-865.
33. Persson H.L., Yu Z., Tirosh O., Eaton J.W., Brunk U.T. Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radic. Biol. Med. 2003, 34:1295-1305.
34. Yu Z., Persson H.L., Eaton J.W., Brunk U.T. Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic. Biol. Med. 2003, 34:1243-1252.
35. Kurz T., Terman A., Gustafsson B., Brunk U. Lysosomes in iron metabolism, ageing and apoptosis. Histochem. Cell Biol. 2008, 129:389-406.
36. Boya P., Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27:6434-6451.
37. Guicciardi M.E., Leist M., Gores G.J. Lysosomes in cell death. Oncogene 2004, 23:2881-2890.
38. Toyokuni S., Miyake N., Hiai H., Hagiwara M., Kawakishi S., Osawa T., Uchida K. The monoclonal antibody specific for the 4-hydroxy-2-nonenal histidine adduct. FEBS Lett. 1995, 359:189-191.
39. Michalopoulos G., Cianciulli H.D., Novotny A.R., Kligerman A.D., Strom S.C., Jirtle R.L. Liver regeneration studies with rat hepatocytes in primary culture. Cancer Res. 1982, 42:4673-4682.
40. Bresgen N., Rolinek R., Hochleitner E., Lottspeich F., Eckl P.M. Induction of apoptosis by a hepatocyte conditioned medium. J. Cell Physiol. 2004, 198:452-460.
41. Huerta S., Goulet E.J., Huerta-Yepez S., Livingston E.H. Screening and detection of apoptosis. J. Surg. Res. 2007, 139:143-156.
42. Wyllie A.H., Kerr J.F., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 1980, 68:251-306.
43. Hashimoto M., Sibata T., Wasada H., Toyokuni S., Uchida K. Structural basis of protein-bound endogenous aldehydes: chemical and immunochemical characterizations of configurational isomers of a 4-hydroxy-2-nonenal-histidine adduct. J. Biol. Chem. 2003, 278:5044-5051.
44. Garty B., Kaminsky E., Moroz C. The immunosuppressive human placental ferritin subunit p43 is produced by activated CD4+ lymphocytes. Clin. Diagn. Lab. Immunol. 1995, 2:225-226.
45. Moroz C., Kupfer B., Twig S., Parhami-Seren B. Preparation and characterization of monoclonal antibodies specific to placenta ferritin. Clin. Chim. Acta 1985, 148:111-118.
46. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11:81-128.
47. Uchida K., Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc. Natl. Acad. Sci. USA 1992, 89:4544-4548.
48. Sodum R.S., Chung F.L. 1,N2-Ethenodeoxyguanosine as a potential marker for DNA adduct formation by trans-4-hydroxy-2-nonenal. Cancer Res. 1988, 48:320-323.
49. Eckl P.M., Raffelsberger I. The primary rat hepatocyte micronucleus assay: general features. Mutat. Res. 1997, 392:117-124.
50. Lu Z., Nie G., Li Y., Soe-Lin S., Tao Y., Cao Y., Zhang Z., Liu N., Ponka P., Zhao B. Overexpression of mitochondrial ferritin sensitizes cells to oxidative stress via an iron-mediated mechanism. Antioxid. Redox Signal. 2009, 11:1791-1803.
51. Tenopoulou M., Kurz T., Doulias P.T., Galaris D., Brunk U.T. Does the calcein-AM method assay the total cellular 'labile iron pool' or only a fraction of it?. Biochem. J. 2007, 403:261-266.
52. Tenopoulou M., Doulias P.T., Barbouti A., Brunk U., Galaris D. Role of compartmentalized redox-active iron in hydrogen peroxide-induced DNA damage and apoptosis. Biochem. J. 2005, 387:703-710.
53. Moss D., Fargion S., Fracanzani A.L., Levi S., Cappellini M.D., Arosio P., Powell L.W., Halliday J.W. Functional roles of the ferritin receptors of human liver, hepatoma, lymphoid and erythroid cells. J. Inorg. Biochem. 1992, 47:219-227.
54. Kidane T.Z., Sauble E., Linder M.C. Release of iron from ferritin requires lysosomal activity. Am. J. Physiol., Cell Physiol. 2006, 291:C445-C455.
55. Kalgaonkar S., Lonnerdal B. Receptor-mediated uptake of ferritin-bound iron by human intestinal Caco-2 cells. J. Nutr. Biochem. 2009, 20:304-311.
56. Meyron-Holtz E.G., Fibach E., Gelvan D., Konijn A.M. Binding and uptake of exogenous isoferritins by cultured human erythroid precursor cells. Br. J. Haematol. 1994, 86:635-641.
57. Broxmeyer H., Williams D., Geissler K., Hangoc G., Cooper S., Bicknell D., Levi S., Arosio P. Suppressive effects in vivo of purified recombinant human H-subunit (acidic) ferritin on murine myelopoiesis. Blood 1989, 73:74-79.
58. Fargion S., Fracanzani A., Brando B., Arosio P., Levi S., Fiorelli G. Specific binding sites for H-ferritin on human lymphocytes: modulation during cellular proliferation and potential implication in cell growth control. Blood 1991, 78:1056-1061.
59. Doulias P.T., Christoforidis S., Brunk U.T., Galaris D. Endosomal and lysosomal effects of desferrioxamine: protection of HeLa cells from hydrogen peroxide-induced DNA damage and induction of cell-cycle arrest. Free Radic. Biol. Med. 2003, 35:719-728.
60. Radisky D.C., Kaplan J. Iron in cytosolic ferritin can be recycled through lysosomal degradation in human fibroblasts. Biochem. J. 1998, 336(Pt. 1):201-205.
61. Wen Y., Leake D.S. Low density lipoprotein undergoes oxidation within lysosomes in cells. Circ. Res. 2007, 100:1337-1343.
62. Eckl P.M., Ortner A., Esterbauer H. Genotoxic properties of 4-hydroxyalkenals and analogous aldehydes. Mutat. Res./Fundam. Mol. Mech. Mutagen. 1993, 290:183-192.
63. Erster S., Mihara M., Kim R.H., Petrenko O., Moll U.M. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol. Cell. Biol. 2004, 24:6728-6741.
64. Awasthi Y.C., Sharma R., Sharma A., Yadav S., Singhal S.S., Chaudhary P., Awasthi S. Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Radic. Biol. Med. 2008, 45:111-118.
65. Ethier C., Raymond V.A., Musallam L., Houle R., Bilodeau M. Antiapoptotic effect of EGF on mouse hepatocytes associated with downregulation of proapoptotic Bid protein. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G298-G308.
66. Bailly-Maitre B., de Sousa G., Boulukos K., Gugenheim J., Rahmani R. Dexamethasone inhibits spontaneous apoptosis in primary cultures of human and rat hepatocytes via Bcl-2 and Bcl-xL induction. Cell Death Differ. 2001, 8:279-288.
67. Musallam L., Ethier C., Haddad P.S., Bilodeau M. Role of EGF receptor tyrosine kinase activity in antiapoptotic effect of EGF on mouse hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280:G1360-G1369.
68. Feldstein A.E., Werneburg N.W., Li Z., Bronk S.F., Gores G.J. Bax inhibition protects against free fatty acid-induced lysosomal permeabilization. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290:G1339-G1346.
69. Poli G., Schaur R.J., Siems W.G., Leonarduzzi G. 4-Hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med. Res. Rev. 2008, 28:569-631.
70. Barrera G., Pizzimenti S., Dianzani M.U. Lipid peroxidation: control of cell proliferation, cell differentiation and cell death. Mol. Aspects Med. 2008, 29:1-8.
71. Liu W., Akhand A.A., Kato M., Yokoyama I., Miyata T., Kurokawa K., Uchida K., Nakashima I. 4-Hydroxynonenal triggers an epidermal growth factor receptor-linked signal pathway for growth inhibition. J. Cell Sci. 1999, 112(Pt. 14):2409-2417.
72. Ji C., Kozak K.R., Marnett L.J. IkappaB kinase, a molecular target for inhibition by 4-hydroxy-2-nonenal. J. Biol. Chem. 2001, 276:18223-18228.
73. Page S., Fischer C., Baumgartner B., Haas M., Kreusel U., Loidl G., Hayn M., Ziegler-Heitbrock H.W., Neumeier D., Brand K. 4-Hydroxynonenal prevents NF-kappaB activation and tumor necrosis factor expression by inhibiting IkappaB phosphorylation and subsequent proteolysis. J. Biol. Chem. 1999, 274:11611-11618.