2,3,7,8-Tetrachlorodibenzo-p-dioxin impairs iron homeostasis by modulating iron-related proteins expression and increasing the labile iron pool in mammalian cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 5, 2011, Pages 704-712

  Santamaria, Rita ^a   Fiorito, Filomena ^a   Irace, Carlo ^a   De Martino, Luisa ^a   Maffettone, Carmen ^a   Granato, Giovanna Elvira ^a   Di Pascale, Antonio ^a   Iovane, Valentina ^a   Pagnini, Ugo ^a   Colonna, Alfredo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin; Iron metabolism; Iron regulatory proteins; Iron related proteins; Labile iron pool

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CD71 ANTIGEN; FERRITIN; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; COW; DOWN REGULATION; FEMALE; GEL MOBILITY SHIFT ASSAY; HOMEOSTASIS; IRON METABOLISM; KIDNEY CELL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA BINDING; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CATION TRANSPORT PROTEINS; CATTLE; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; FERRITINS; GENE EXPRESSION REGULATION; HOMEOSTASIS; IRON; IRON-REGULATORY PROTEINS; MAMMALS; RECEPTORS, TRANSFERRIN; RNA, MESSENGER; TETRACHLORODIBENZODIOXIN;

BOVINAE; MAMMALIA;

EID: 79955666963     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.02.003     Document Type: Article

References (59)

1. Beard J. Iron deficiency alters brain development and functioning. J. Nutr. 2003, 133:1468S-1472S.
2. Nelson S.K., McCord J.M. Iron, oxygen radicals, and disease. Adv. Mol. Cell. Biol. 1998, 25:157-183.
3. Toyokuni S. Iron-induced carcinogenesis: the role of redox regulation. Free Radic. Biol. Med. 1996, 20:553-566.
4. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., Ganz T., Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306:2090-2093.
5. Nemeth E., Ganz T. The role of hepcidin in iron metabolism. Acta Haematol. 2009, 122:78-86.
6. Hentze M.W., Muckenthaler M.U., Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell 2004, 117:285-297.
7. Pantopoulos K. Iron metabolism and the IRE/IRP regulatory system: an update. Ann. N. Y. Acad. Sci. 2004, 1012:1-13.
8. Rouault T.A. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2006, 2:406-414.
9. Muckenthaler M.U., Galy B., Hentze M.W. Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu. Rev. Nutr. 2008, 28:197-213.
10. Wallander M.L., Leibold E.A., Eisenstein R.S. Molecular control of vertebrate iron homeostasis by iron regulatory proteins. Biochim. Biophys. Acta 2006, 1763:668-689.
11. Fishman J.B., Rubin J.B., Handrahan J.V., Connor J.R., Fine R.E. Receptor mediated transcytosis of transferrin across the blood-brain barrier. J. Neurosci. Res. 1987, 18:299-304.
12. Mims M.P., Prchal J.T. Divalent metal transporter 1. Hematology 2005, 10:339-345.
13. Aziz N., Munro H.N. Iron regulates ferritin mRNA translation through a segment of its 5' untranslated region. Proc. Natl Acad. Sci. USA 1987, 84:8478-8482.
14. 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 1992, 89:11730-11734.
15. Salahudeen A.A., Thompson J.W., Ruiz J.C., Ma H.W., Kinch L.N., Li Q., Grishin N.V., Bruick R.K. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 2009, 326:722-726.
16. Vashisht A.A., Zumbrennen K.B., Huang X., Powers D.N., Durazo A., Sun D., Bhaskaran N., Persson A., Uhlen M., Sangfelt O., Spruck C., Leibold E.A., Wohlschlegel J.A. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 2009, 326:718-721.
17. Pantopoulos K., Mueller S., Atzberger A., Ansorge W., Stremmel W., Hentze M.W. Differences in the regulation of iron regulatory protein-1 (IRP1) by extra- and intra-cellular oxidative stress. J. Biol. Chem. 1997, 272:9802-9808.
18. Drapier J.C., Hirling H., Wietzerbin J., Kaldy P., Kühn L.C. Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 1993, 12:3643-3649.
19. Brown N.M., Anderson S.A., Steffen D.W., Carpenter T.B., Kennedy M.C., Walden W.E., Eisenstein R.S. Novel role of phosphorylation in Fe-S cluster stability revealed by Phosphomimetic mutation at Ser-138 of iron regulatory protein 1. Proc. Natl Acad. Sci. USA 1998, 95:15235-15240.
20. Meyron-Holtz E.G., Ghosh M.C., Rouault T.A. Mammalian tissue oxygen levels modulate iron-regulatory protein activities in vivo. Science 2004, 306:2087-2090.
21. Irace C., Scorziello A., Maffettone C., Pignataro G., Matrone C., Adornetto A., Santamaria R., Annunziato L., Colonna A. Divergent modulation of iron regulatory proteins and ferritin biosynthesis by hypoxia/reoxygenation in neurons and glial cells. J. Neurochem. 2005, 95:1321-1331.
22. Maffettone C., De Martino L., Irace C., Santamaria R., Pagnini U., Iovane G., Colonna A. Expression of iron-related proteins during infection by bovine herpes virus type-1. J. Cell. Biochem. 2008, 104:213-223.
23. Mattace Raso G., Irace C., Esposito E., Maffettone C., Iacono A., Di Pascale A., Santamaria R., Colonna A., Meli R. Ovariectomy and estrogen treatment modulate iron metabolism in rat adipose tissue. Biochem. Pharmacol. 2009, 78:1001-1007.
24. Festa M., Colonna A., Pietropaolo C., Ruffo A. Oxalomalate, a competitive inhibitor of aconitase, modulates the RNA-binding activity of iron-regulatory proteins. Biochem. J. 2000, 348:315-320.
25. Santamaria R., Irace C., Festa M., Maffettone C., Colonna A. Induction of ferritin expression by oxalomalate. Biochim. Biophys. Acta 2004, 1691:151-159.
26. Santamaria R., Bevilacqua M.A., Maffettone C., Irace C., Iovine B., Colonna A. Induction of H-ferritin synthesis by oxalomalate is regulated at both the transcriptional and post-transcriptional levels. Biochim. Biophys. Acta 2006, 1763:815-822.
27. Schecter A., Birnbaum L., Ryan J.J., Constable J.D. Dioxins: an overview. Environ. Res. 2006, 101:419-428.
28. Santelli F., Boscaino F., Cautela D., Castaldo D., Malorni A. Determination of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzo-p-furans (PCDFs) and polychlorinated biphenyls (PCBs) in buffalo milk and mozzarella cheese. Eur. Food Res. Technol. 2006, 223:51-56.
29. Diletti G., Torreti L., De Massis M.R., Migliorati G., Scortichini G. A case of milk contamination by PCDD/Fs in Italy: analytical levels and contamination source identification. Organohalogen Compouds 2003, 64:1-4.
30. Mandal P.K. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. B 2005, 175:221-230.
31. Knerr S., Schrenk D. Carcinogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in experimental models. Mol. Nutr. Food Res. 2006, 50:897-907.
32. Pohjanvirta R., Tuomisto J. Short-term toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in laboratory animals: effects, mechanisms, and animal models. Pharmacol. Rev. 1994, 46:483-549.
33. Consonni D., Pesatori A.C., Zocchetti C., Sindaco R., D'Oro L.C., Rubagotti M., Bertazzi P.A. Mortality in a population exposed to dioxin after the Seveso, Italy, accident in 1976: 25years of follow-up. Am. J. Epidemiol. 2008, 167:847-858.
34. Mocarelli P., Gerthoux P.M., Patterson D.G., Milani S., Limonta G., Bertona M., Signorini S., Tramacere P., Colombo L., Crespi C., Brambilla P., Sarto C., Carreri V., Sampson E.J., Turner W.E., Needham L.L. Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environ. Health Perspect. 2008, 116:70-77.
35. Bock K.W., Köhle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem. Pharmacol. 2006, 72:393-404.
36. Ray S., Swanson H.I. Activation of the aryl hydrocarbon receptor by TCDD inhibits senescence: a tumor promoting event?. Biochem. Pharmacol. 2009, 77:681-688.
37. Ohtake F., Baba A., Takada I., Okada M., Iwasaki K., Miki H., Takahashi S., Kouzmenko A., Nohara K., Chiba T., Fujii-Kuriyama Y., Kato S. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 2007, 446:562-566.
38. Bock K.W., Köhle C. The mammalian aryl hydrocarbon (Ah) receptor: from mediator of dioxin toxicity toward physiological functions in skin and liver. Biol. Chem. 2009, 390:1225-1235.
39. al-Bayati Z.A., Wahba Z.Z., Stohs S.J. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-induced alterations in lipid peroxidation, enzymes, and divalent cations in rat testis. Xenobiotica 1988, 18:1281-1289.
40. Wahba Z.Z., al-Bayati Z.A., Stohs S.J. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the hepatic distribution of iron, copper, zinc, and magnesium in rats. J. Biochem. Toxicol. 1988, 3:121-129.
41. Smith A.G., Clothier B., Robinson S., Scullion M.J., Carthew P., Edwards R., Luo J., Lim C.K., Toledano M. Interaction between iron metabolism and 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice with variants of the Ahr gene: a hepatic oxidative mechanism. Mol. Pharmacol. 1998, 53:52-61.
42. Davies R., Clothier B., Robinson S.W., Edwards R.E., Greaves P., Luo J., Gant T.W., Chernova T., Smith A.G. Essential role of the AH receptor in the dysfunction of heme metabolism induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chem. Res. Toxicol. 2008, 21:330-340.
43. Fiorito F., Pagnini U., De Martino L., Montagnaro S., Ciarcia R., Florio S., Pacilio M., Fucito A., Rossi A., Iovane G., Giordano A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases bovine herpesvirus type-1 (BHV-1) replication in Madin-Darby Bovine Kidney (MDBK) cells in vitro. J. Cell. Biochem. 2008, 103:221-233.
44. Fiorito F., Marfè G., De Blasio E., Granato G.E., Tafani M., De Martino L., Montagnaro S., Florio S., Pagnini U. 2,3,7,8-Tetrachlorodibenzo-p-dioxin regulates bovine herpesvirus type 1 induced apoptosis by modulating Bcl-2 family members. Apoptosis 2008, 13:1243-1252.
45. Fiorito F., Marfè G., Granato G.E., Ciarcia R., De Blasio E., Tafani M., Florio S., De Martino L., Muzi G., Pagnini U., Giordano A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin modifies expression and nuclear/cytosolic localization of bovine herpesvirus 1 immediate-early protein (bICP0) during infection. J. Cell. Biochem. 2010, 111(2):333-342.
46. Festa M., Ricciardelli G., Mele G., Pietropaolo C., Ruffo A., Colonna A. Overexpression of H ferritin and up-regulation of iron regulatory protein genes during differentiation of 3T3-L1 pre-adipocytes. J. Biol. Chem. 2000, 275:36708-36712.
47. Breuer W., Epsztejn S., Millgram P., Cabantchik Z.I. Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am. J. Physiol. 1995, 268:1354-1361.
48. Bouton C., Hirling H., Drapier J.C. Redox modulation of iron regulatory proteins by peroxynitrite. J. Biol. Chem. 1997, 272:19969-19975.
49. Sharma N., Butterworth J., Cooper B.T., Tselepis C., Iqbal T.H. The emerging role of the liver in iron metabolism. Am. J. Gastroenterol. 2005, 100:201-206.
50. Gore A.C., Heindel J.J., Zoeller R.T. Endocrinology 2006, 147:S1-S3.
51. Safe S., Wormke M., Samudio I. Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary Gland Biol. Neoplasia 2000, 5:295-306.
52. Safe S., Wormke M. Inhibitory aryl hydrocarbon receptor-estrogen receptor alpha cross-talk and mechanisms of action. Chem. Res. Toxicol. 2003, 16:807-816.
53. Swedenborg E., Pongratz I. AhR and ARNT modulate ER signaling. Toxicology 2010, 268:132-138.
54. Zhang D., Meyron-Holtz E., Rouault T.A. Renal iron metabolism: transferrin iron delivery and the role of iron regulatory proteins. J. Am. Soc. Nephrol. 2007, 18:401-406.
55. Meyron-Holtz E.G., Ghosh M.C., Iwai K., LaVaute T., Brazzolotto X., Berger U.V., Land W., Ollivierre-Wilson H., Grinberg A., Love P., Rouault T.A. Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J. 2004, 23:386-395.
56. Kruszewski M. Labile iron pool: the main determinant of cellular response to oxidative stress. Mutat. Res. 2003, 531:81-92.
57. Portier C.J. Endocrine dismodulation and cancer. Neuro Endocrinol. Lett. 2002, 23:43-47.
58. Toyokuni S. Role of iron in carcinogenesis: cancer as a ferrotoxic disease. Cancer Sci. 2009, 100:9-16.
59. Maffettone C., Chen G., Drozdov I., Ouzounis C., Pantopoulos K. Tumorigenic properties of iron regulatory protein 2 (IRP2) mediated by its specific 73-amino acids insert. PLoS ONE 2010, 5(4):e10163.