Differing expression of genes involved in non-transferrin iron transport across plasma membrane in various cell types under iron deficiency and excess

Molecular and Cellular Biochemistry

Volumn 321, Issue 1-2, 2009, Pages 123-133

  Balusikova, Kamila ^a   Neubauerova, Jitka ^a   Dostalikova Cimburova, Marketa ^a   Horak, Jiri ^a   Kovar, Jan ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Ceruloplasmin; Dcytb; DMT1; Ferroportin; Hephaestin; Non transferrin iron transport

Indexed keywords

CELL MEMBRANE PROTEIN; CERULOPLASMIN; FERRIC CITRATE; FERROPORTIN; HEPHAESTIN; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PROTEIN DCYTB; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE TRANSPORT; CELL STRAIN CACO 2; CELL STRAIN HEPG2; CELL STRAIN K 562; CELL TYPE; CONTROLLED STUDY; CORRELATION FUNCTION; GENE EXPRESSION; HUMAN; HUMAN CELL; INCUBATION TIME; IRON DEFICIENCY; IRON OVERLOAD; IRON TRANSPORT; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE; CELL MEMBRANE; CERULOPLASMIN; CULTURE MEDIA; CYTOCHROME B GROUP; GENE EXPRESSION; HUMANS; IRON; MEMBRANE PROTEINS; OXIDOREDUCTASES; TRANSFERRIN;

EID: 58249136810     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-008-9926-y     Document Type: Article

References (54)

1. Hentze MW, Kuhn LC (1996) Molecular control of vertebrate iron metabolism: MRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93:8175-8182. doi: 10.1073/pnas.93.16.8175
2. Anderson GJ, Darshan D, Wilkins SJ, Frazer DM (2007) Regulation of systemic iron homeostasis: How the body responds to changes in iron demand. Biometals 20:665-674. doi: 10.1007/s10534-006-9030-2
3. Fleming MD, Trenor CCIII, Su MA, Foernzler D, Beier DR, Dietrich WF et al (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16:383-386
4. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF et al (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482-488. doi: 10.1038/41343
5. McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, Mudaly E et al (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291:1755-1759. doi: 10.1126/science.1057206
6. Latunde-Dada GO, Simpson RJ, McKie AT (2008) Duodenal cytochrome B expression stimulates iron uptake by human intestinal epithelial cells. J Nutr 138:991-995
7. Wyman S, Simpson RJ, McKie AT, Sharp PA (2008) Dcytb (Cybrd1) functions as both a ferric and a cupric reductase in vitro. FEBS Lett 582:1901-1906. doi: 10.1016/j.febslet.2008.05.010
8. Gunshin H, Starr CN, Direnzo C, Fleming MD, Jin J, Greer EL et al (2005) Cybrd1 (duodenal cytochrome b) is not necessary for dietary iron absorption in mice. Blood 106:2879-2883. doi: 10.1182/blood-2005-02-0716
9. Abboud S, Haile DJ (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem 275:19906-19912. doi: 10.1074/jbc.M000713200
10. Donovan A, Brownlie A, Zhou Y, Shepard J, Pratt SJ, Moynihan J et al (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403:776-781. doi: 10.1038/ 35001596
11. McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, Barrow D et al (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell 5:299-309. doi: 10.1016/S1097-2765(00)80425-6
12. Vulpe CD, Kuo YM, Murphy TL, Cowley L, Askwith C, Libina N et al (1999) Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat Genet 21:195-199. doi: 10.1038/5979
13. Andrews NC (1999) Disorders of iron metabolism. N Engl J Med 341:1986-1995. doi: 10.1056/NEJM199912233412607
14. Fleming RE, Migas MC, Holden CC, Waheed A, Britton RS, Tomatsu S et al (2000) Transferrin receptor 2: Continued expression in mouse liver in the face of iron overload and in hereditary hemochromatosis. Proc Natl Acad Sci USA 97:2214-2219. doi: 10.1073/pnas.040548097
15. Ohgami RS, Campagna DR, Greer EL, Antiochos B, McDonald A, Chen J et al (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat Genet 37:1264-1269. doi: 10.1038/ng1658
16. Dunn LL, Rahmanto YS, Richardson DR (2007) Iron uptake and metabolism in the new millennium. Trends Cell Biol 17:93-100. doi: 10.1016/ j.tcb.2006.12.003
17. Hellman NE, Gitlin JD (2002) Ceruloplasmin metabolism and function. Annu Rev Nutr 22:439-458. doi: 10.1146/annurev.nutr.22.012502.114457
18. McKie AT, Barlow DJ (2004) The SLC40 basolateral iron transporter family (IREG1/ferroportin/MTP1). Pflugers Arch 447:801-806. doi: 10.1007/ s00424-003-1102-3
19. Cianetti L, Segnalini P, Calzolari A, Morsilli O, Felicetti F, Ramoni C et al (2005) Expression of alternative transcripts of ferroportin-1 during human erythroid differentiation. Haematologica 90:1595-1606
20. Klausner RD, Rouault TA, Harford JB (1993) Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72:19-28. doi: 10.1016/ 0092-8674(93)90046-S
21. Schumann K, Moret R, Kunzle H, Kuhn LC (1999) Iron regulatory protein as an endogenous sensor of iron in rat intestinal mucosa Possible implications for the regulation of iron absorption. Eur J Biochem 260:362-372. doi: 10.1046/j.1432-1327.1999.00155.x
22. Oates PS, Trinder D, Morgan EH (2000) Gastrointestinal function, divalent metal transporter-1 expression and intestinal iron absorption. Pflugers Arch 440:496-502
23. Kovar J, Kuhn LC, Richardson V, Seiser C, Kriegerbeckova K, Musilkova J (1997) The inability of cells to grow in low iron correlates with increasing activity of their iron regulatory protein (IRP). In Vitro Cell Dev Biol 33:633-639. doi: 10.1007/s11626-997-0114-2
24. Nunez MT, Nunez-Millacura C, Tapia V, Munoz P, Mazariegos D, Arredondo M et al (2003) Iron-activated iron uptake: A positive feedback loop mediated by iron regulatory protein 1. Biometals 16:83-90. doi: 10.1023/ A:1020743405347
25. Inman RS, Wessling-Resnick M (1993) Characterization of transferrin-independent iron transport in K562 cells Unique properties provide evidence for multiple pathways of iron uptake. J Biol Chem 268:8521-8528
26. Baker E, Baker SM, Morgan EH (1998) Characterisation of non-transferrin-bound iron (ferric citrate) uptake by rat hepatocytes in culture. Biochim Biophys Acta 1380:21-30
27. Musilkova J, Kriegerbeckova K, Krusek J, Kovar J (1998) Specific binding to plasma membrane is the first step in the uptake of non-transferrin iron by cultured cells. Biochim Biophys Acta 1369:103-108. doi: 10.1016/ S0005-2736(97)00214-9
28. Musilkova J, Kovar J (2001) Additive stimulatory effect of extracellular calcium and potassium on non-transferrin ferric iron uptake by HeLa and K562 cells. Biochim Biophys Acta 1514:117-126. doi: 10.1016/ S0005-2736(01)00367-4
29. Kovar J, Neubauerova J, Cimburova M, Truksa J, Balusikova K, Horak J (2006) Stimulation of non-transferrin iron uptake by iron deprivation in K562 cells. Blood Cells Mol Dis 37:95-99. doi: 10.1016/j.bcmd.2006.06.004
30. Grootveld M, Bell JD, Halliwell B, Aruoma OI, Bomford A, Sadler PJ (1989) Non-transferrin-bound iron in plasma or serum from patients with idiopathic hemochromatosis Characterization by high performance liquid chromatography and nuclear magnetic resonance spectroscopy. J Biol Chem 264:4417-4722
31. Kovar J, Franek F (1989) Growth-stimulating effect of transferrin on a hybridoma cell line: Relation to transferrin iron-transporting function. Exp Cell Res 182:358-369. doi: 10.1016/0014-4827(89)90241-3
32. Zoller H, Koch RO, Theurl I, Obrist P, Pietrangelo A, Montosi G et al (2001) Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 120:1412-1419. doi: 10.1053/gast.2001.24033
33. Zoller H, Theurl I, Koch RO, McKie AT, Vogel W, Weiss G (2003) Duodenal cytochrome b and hephaestin expression in patients with iron deficiency and hemochromatosis. Gastroenterology 125:746-754. doi: 10.1016/ S0016-5085(03)01063-1
34. Truksa J, Kovar J, Valenta T, Ehrlichova M, Polak J, Naumann PW (2003) Iron deprivation induces apoptosis independently of p53 in human and murine tumour cells. Cell Prolif 36:199-213. doi: 10.1046/ j.1365-2184.2003.00280.x
35. Martini LA, Tchack L, Wood RJ (2002) Iron treatment downregulates DMT1 and IREG1 mRNA expression in Caco-2 cells. J Nutr 132:693-696
36. Zoller H, Theurl I, Koch R, Kaser A, Weiss G (2002) Mechanisms of iron mediated regulation of the duodenal iron transporters divalent metal transporter 1 and ferroportin 1. Blood Cells Mol Dis 29:488-497. doi: 10.1006/bcmd.2002.0587
37. Wessling-Resnick M (2006) Iron imports. III. Transfer of iron from the mucosa into circulation. Am J Physiol Gastrointest Liver Physiol 290:G1-G6. doi: 10.1152/ajpgi.00415.2005
38. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM et al (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306:2090-2093. doi: 10.1126/ science.1104742
39. Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M (2005) Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc Natl Acad Sci USA 102:1324-1328. doi: 10.1073/pnas.0409409102
40. Gleeson F, Ryan E, Barrett S, Russell J, Kelleher B, Crowe J (2005) Duodenal Dcytb and hephaestin mRNA expression are not significantly modulated by variations in body iron homeostasis. Blood Cells Mol Dis 35:303-308. doi: 10.1016/j.bcmd.2005.06.005
41. Theurl I, Ludwiczek S, Eller F, Seifert M, Artner E, Brunner P et al (2005) Pathways for the regulation of body iron homeostasis in response to experimental iron overload. J Hepatol 43:711-719. doi: 10.1016/ j.jhep.2005.03.030
42. Aldred AR, Grimes A, Schreiber G, Mercer JF (1987) Rat ceruloplasmin. Molecular cloning and gene expression in liver, choroid plexus, yolk sac, placenta, and testis. J Biol Chem 262:2875-2878
43. Fleming RE, Gitlin JD (1990) Primary structure of rat ceruloplasmin and analysis of tissue-specific gene expression during development. J Biol Chem 265:7701-7707
44. Klomp LW, Farhangrazi ZS, Dugan LL, Gitlin JD (1996) Ceruloplasmin gene expression in the murine central nervous system. J Clin Invest 98:207-215. doi: 10.1172/JCI118768
45. Lockhart PJ, Mercer JF (1999) Cloning and expression analysis of the sheep ceruloplasmin cDNA. Gene 236:251-257. doi: 10.1016/ S0378-1119(99)00276-0
46. Tabuchi M, Tanaka N, Nishida-Kitayama J, Ohno H, Kishi F (2002) Alternative splicing regulates the subcellular localization of divalent metal transporter 1 isoforms. Mol Biol Cell 13:4371-4387. doi: 10.1091/ mbc.E02-03-0165
47. Kato J, Kobune M, Ohkubo S, Fujikawa K, Tanaka M, Takimoto R et al (2007) Iron/IRP-1-dependent regulation of mRNA expression for transferrin receptor, DMT1 and ferritin during human erythroid differentiation. Exp Hematol 35:879-887. doi: 10.1016/ j.exphem.2007.03.005
48. Viatte L, Lesbordes-Brion JC, Lou DQ, Bennoun M, Nicolas G, Kahn A et al (2005) Deregulation of proteins involved in iron metabolism in hepcidin-deficient mice. Blood 105:4861-4864. doi: 10.1182/ blood-2004-12-4608
49. Mukhopadhyay CK, Attieh ZK, Fox PL (1998) Role of ceruloplasmin in cellular iron uptake. Science 279:714-717. doi: 10.1126/ science.279.5351.714
50. Canonne-Hergaux F, Gruenheid S, Ponka P, Gros P (1999) Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93:4406-4417
51. Hubert N, Hentze MW (2002) Previously uncharacterized isoforms of divalent metal transporter (DMT)-1: Implications for regulation and cellular function. Proc Natl Acad Sci USA 99:12345-12350. doi: 10.1073/ pnas.192423399
52. Jacolot S, Ferec C, Mura C (2008) Iron responses in hepatic, intestinal and macrophage/monocyte cell lines under different culture conditions. Blood Cells Mol Dis 41:100-108. doi: 10.1016/j.bcmd.2008.01.006
53. Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T (2003) Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101:2461-2463. doi: 10.1182/ blood-2002-10-3235
54. Montosi G, Corradini E, Garuti C, Barelli S, Recalcati S, Cairo G et al (2005) Kupffer cells and macrophages are not required for hepatic hepcidin activation during iron overload. Hepatology 41:545-552. doi: 10.1002/hep.20620