The role of iron regulatory proteins in the control of iron metabolism in mammals

Biotechnologia

Volumn 92, Issue 1, 2011, Pages 66-75

  Styś, Agnieszka ^a   Starzyński, Rafał R ^a   Lipiński, Paweł ^a  

^a INSTITUTE OF GENETICS AND ANIMAL BREEDING   (Poland)

Author keywords

IRE; Iron homeostasis; Iron regulatory; IRP

Indexed keywords

MAMMALIA; MUS;

EID: 79959406739     PISSN: 08607796     EISSN: None     Source Type: Journal    
DOI: 10.5114/bta.2011.46518     Document Type: Article

References (74)

1. Andrews N.C. (2008) Forging a field: the golden age of iron biology. Blood 112: 219-230.
2. Arosio P., Levi S. (2010) Cytosolic and mitochondrial ferritins in the regulation of cellular iron homeostasis and oxidative damage. Biochim. Biophys. Acta. 1800: 783-792.
3. Bartosz G. (2003) Druga twarz tlenu, Wydawnictwo Naukowe PWN, Warszawa.
4. Binder R., Horowitz J.A., Basilion J.P., Koeller D.M., Klausner R.D., Harford J.B. (1994) Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3' UTR and does not involve poly(A) tail shortening. EMBO J. 13: 1969-1980.
5. Bouton C., Chauveau M.J., Lazereg S., Drapier J.C. (2002) Recycling of RNA binding iron regulatory protein 1 into an aconitase after nitric oxide removal depends on mitochondrial ATP. J. Biol. Chem. 277: 31220-31227.
6. Bouton C., Drapier J.C. (2003) Iron regulatory proteins as NO signal transducers. Sci STKE. 182: pe17.
7. Bouton C., Oliveira L., Drapier J.C. (1998) Converse modulation of IRP1 and IRP2 by immunological stimuli in murine RAW 264.7 macrophages. J. Biol. Chem. 273: 9403-9408.
8. Bouton C., Raveau M., Drapier J.C. (1996) Modulation of iron regulatory protein functions. Further insights into the role of nitrogen-and oxygen-derived reactive species. J. Biol. Chem. 271: 2300-2306.
9. Brazzolotto X., Gaillard J., Pantopoulos K., Hentze M.W., Moulis J.M. (1999) Human cytoplasmic aconitase (Iron regulatory protein 1) is converted into its [3Fe-4S] form by hydrogen peroxide in vitro but is not activated for iron-responsive element binding. J. Biol. Chem. 274: 21625-21630.
10. Dandekar T., Stripecke R., Gray N.K., Goossen B., Constable A., Johansson H.E., Hentze M.W. (1991) Identification of a novel iron-responsive element in murine and human erythroid delta-aminolevulinic acid synthase mRNA. EMBO J. 10: 1903-1909.
11. Drapier J.C., Hirling H., Wietzerbin J., Kaldy P., Kühn L.C. (1993) Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 12: 3643-3649.
12. Dupuy J., Darnault C., Brazzolotto X., Kühn L.C., Moulis J.M., Volbeda A., Fontecilla-Camps J.C. (2005) Crystallization and preliminary X-ray diffraction data for the aconitase form of human iron-regulatory protein 1. Acta Crystallogr. F: Struct. Biol. Cryst. Commun. 61: 482-485.
13. Feelders R.A., Kuiper-Kramer E.P., van Eijk H.G. (1999) Structure, function and clinical significance of transferrin receptors. Clin. Chem. Lab. Med. 37: 1-10.
14. Galy B., Ferring D., Benesova M., Benes V., Hentze M.W. (2004) Targeted mutagenesis of the murine IRP1 and IRP2 genes reveals context-dependent RNA processing differences in vivo. RNA J10: 1019-1025.
15. Galy B., Ferring D., Hentze M.W. (2005) Generation of conditional alleles of the murine Iron Regulatory Protein (IRP)-1 and-2 genes. Genesis 43: 181-188.
16. Galy B., Ferring-Appel D., Kaden S., Gröne H.J., Hentze M.W. (2008) Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab. 7: 79-85.
17. Galy B., Ferring-Appel D., Sauer S.W., Kaden S., Lyoumi S., Puy H., Kölker S., Gröne H.J., Hentze M.W. (2010) Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab. 12: 194-201.
18. Ganz T. (2005) Cellular iron: ferroportin is the only way out. Cell Metab. 1: 155-157.
19. Gardner P.R., Raineri I., Epstein L.B., White C.W. (1995) Superoxide radical and iron modulate aconitase activity in mammalian cells. J. Biol. Chem. 270: 13399-13405.
20. Gunshin H., Mackenzie B., Berger U.V., Gunshin Y., Romero M.F., Boron W.F., Nussberger S., Gollan J.L., Hediger M.A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
21. Guo B., Brown F.M., Phillips J.D., Yu Y., Leibold E.A. (1995) Characterization and expression of iron regulatory protein 2 (IRP2). Presence of multiple IRP2 transcripts regulated by intracellular iron levels. J. Biol. Chem. 270: 16529-16535.
22. Guo B., Yu Y., Leibold E.A. (1994) Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem. 269: 24252-24260.
23. Hanson E.S., Rawlins M.L., Leibold E.A. (2003) Oxygen and iron regulation of iron regulatory protein 2. J. Biol. Chem. 278: 40337-40342.
24. Henderson B.R., Menotti E., Bonnard C., Kühn L.C. (1994) Optimal sequence and structure of iron-responsive elements. Selection of RNA stem-loops with high affinity for iron regulatory factor. J. Biol. Chem. 269: 17481-17489.
25. Hentze M.W., Muckenthaler M.U., Galy B., Camaschella C. (2010) Two to tango: regulation of Mammalian iron metabolism. Cell. 142: 24-38.
26. Hirling H., Henderson B.R., Kühn L.C. (1994) Mutational analysis of the [4Fe-4S]-cluster converting iron regulatory factor from its RNA-binding form to cytoplasmic aconitase. EMBO J. 13: 453-461.
27. Ishikawa H., Kato M., Hori H., Ishimori K., Kirisako T., Tokunaga F., Iwai K. (2005) Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. Mol. Cell. 19: 171-181.
28. Kakhlon O., Cabantchik Z.I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes(1). Free Radic. Biol. Med. 33: 1037-1046.
29. Kim S., Wing S.S., Ponka P. (2004) S-nitrosylation of IRP2 regulates its stability via the ubiquitin-proteasome pathway. Mol. Cell Biol. 24: 330-337.
30. Kohler S.A., Henderson B.R., Kühn L.C. (1995) Succinate dehydrogenase b mRNA of Drosophila melanogaster has a functional iron-responsive element in its 5'-untranslated region. J. Biol. Chem. 270: 30781-30786.
31. Kruszewski M. (2003) Labile iron pool: the main determinant of cellular response to oxidative stress. Mutat. Res. 531: 81-92.
32. LaVaute T., Smith S., Cooperman S., Iwai K., Land W., Meyron-Holtz E., Drake S.K., Miller G., Abu-Asab M., Tsokos M. et al. (2001) Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nat. Genet. 27: 209-214.
33. Leibold E.A., Munro H.N. (1988) 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: 2171-2175.
34. Lipiński P., Drapier J.C., Oliveira L., Retmańska H., Sochanowicz B., Kruszewski M. (2000) Intracellular iron status as a hallmark of mammalian cell susceptibility to oxidative stress: a study of L5178Y mouse lymphoma cell lines differentially sensitive to H2O2. Blood 95: 2960-2966.
35. Lipiński P., Starzyński R.R. (2006) The role of iron regulatory proteins (IRPs) in the regulation of systemic iron homeostasis: lessons from studies on IRP1 and IRP2 knock out mice. Postepy Hig. Med. Dosw. 60: 322-330.
36. Lipiński P., Starzyński R.R., Drapier J.C., Bouton C., Bartłomiejczyk T., Sochanowicz B., Smuda E., Gajkowska A., Kruszewski M. (2005) Induction of iron regulatory protein 1 RNAbinding activity by nitric oxide is associated with a concomitant increase in the labile iron pool: implications for DNA damage. Biochem. Biophys. Res. Commun. 327: 349-355.
37. Lipiński P., Starzyński R.R., Styś A., Straciło M. (2010) Iron homeostasis, a defense mechanism in oxidative stress. Post. Biochem. 56: 305-316.
38. Martins E.A., Robalinho R.L., Meneghini R. (1995) Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Acta Biochem. Biophys, 316: 128-134.
39. 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. et al. (2004) Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J. 23: 386-395.
40. Muckenthaler M.U., Galy B., Hentze M.W. (2008) Systemic iron homeostasis and the iron-responsive element/ironregulatory protein (IRE/IRP) regulatory network. Ann. Rev. Nut. 28: 197-213.
41. Muckenthaler M., Gray N.K., Hentze M.W. (1998) IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell 2: 383-388.
42. Mueller S., Pantopoulos K., Hübner C.A., Stremmel W., Hentze M.W. (2001) IRP1 activation by extracellular oxidative stress in the perfused rat liver. J. Biol. Chem. 76: 23192-23196.
43. Mulero V., Brock J.H. (1999) Regulation of iron metabolism in murine J774 macrophages: role of nitric oxide-dependent and-independent pathways following activation with gamma interferon and lipopolysaccharide. Blood 94: 2383-2389.
44. Mullner E.W., Kuhn L.C. (1988) A stem-loop in the 3' untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell 53: 815-825.
45. Nagy A. (2000) Cre recombinase: the universal reagent for genome tailoring. Genesis. 26: 99-109.
46. Oliveira L., Drapier J.C. (2000) Down-regulation of iron regulatory protein 1 gene expression by nitric oxide. Proc. Natl Acad. Sci. USA 97: 6550-6555.
47. Pantopoulos K., Hentze M.W. (1995) Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J., 14: 2917-2924.
48. Pantopoulos K., Mueller S., Atzberger A., Ansorge W., Stremmel W., Hentze M.W. (1997) Differences in the regulation of iron regulatory protein-1 (IRP-1) by extra-and intracellular oxidative stress. J. Biol. Chem. 272: 9802-9808.
49. Phillips J.D., Kinikini D.V., Yu Y., Guo B., Leibold E.A. (1996) Differential regulation of IRP1 and IRP2 by nitric oxide in rat hepatoma cells. Blood 87: 2983-2992.
50. Radisky D.C., Kaplan J. (1998) Iron in cystolic ferritin can be recycled through lysosomal degradation in human fibroblasts. Biochem. J. 15: 201-205.
51. Recalcati S., Taramelli D., Conte D., Cairo G. (1998) Nitric oxide-mediated induction of ferritin synthesis in J774 macrophages by inflammatory cytokines: role of selective iron regulatory protein-2 downregulation. Blood 91: 1059-1066.
52. Rouault T.A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2: 406-414.
53. Salahudeen A.A., Thompson J.W., Ruiz J.C., Ma H.W., Kinch L.N., Li Q., Grishin N.V., Bruick R.K. (2009) An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326: 722-726.
54. Samaniego F., Chin J., Iwai K., Rouault T.A., Klausner R.D. (1994) Molecular characterization of a second iron-responsive element binding protein, iron regulatory protein 2. Structure, function, and post-translational regulation. J. Biol. Chem. 269: 30904-30910.
55. Schalinske K.L., Blemings K.P., Steffen D.W., Chen O.S., Eisenstein R.S. (1997) Iron regulatory protein 1 is not required for the modulation of ferritin and transferrin receptor expression by iron in a murine pro-B lymphocyte cell line. Proc. Nat. Acad. Sci. USA 94: 10681-10686.
56. Shi H., Bencze K.Z., Stemmler T.L., Philpott C.C. (2008) A cytosolic iron chaperone that delivers iron to ferritin. Science 320: 1207-1210.
57. rd et al. (2004) Severity of neurodegeneration correlates with compromise of iron metabolism in mice with iron regulatory protein deficiencies. Ann. N. Y. Acad. Sci. 1012: 65-83.
58. Smith S.R., Ghosh M.C., Ollivierre-Wilson H., Hang Tong W., Rouault T.A. (2006) Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development. Blood Cells Mol. Dis. 36: 283-287.
59. Soum E., Drapier J.C. (2003) Nitric oxide and peroxynitrite promote complete disruption of the [4Fe-4S] cluster of recombinant human iron regulatory protein 1. J. Biol. Inorg. Chem. 8: 226-232.
60. Starzyński R.R., Lipiński P., Drapier J.C., Diet A., Smuda E., Bartlomiejczyk T., Gralak M.A., Kruszewski M. (2005) Down-regulation of iron regulatory protein 1 activities and expression in superoxide dismutase 1 knock-out mice is not associated with alterations in iron metabolism. J. Biol. Chem. 280: 4207-4212.
61. Starzyński R.R., Gonçalves A.S., Muzeau F., Tyrolczyk Z., Smuda E., Drapier J.C., Beaumont C., Lipiński P. (2006) STAT5 proteins are involved in down-regulation of iron regulatory protein 1 gene expression by nitric oxide. Biochem. J. 400: 367-375.
62. th 2010: 17.
63. Torti F.M., Torti S.V. (2002) Regulation of ferritin genes and protein. Blood 99: 3505-3516.
64. Tsuji Y., Ayaki H., Whitman S.P., Morrow C., Torti S.V., Torti F.M. (2000) Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol. Cell Biol. 20: 5818-5827.
65. Vashisht A.A., Zumbrennen K.B., Huang X., Powers D.N., Durazo A., Sun D., Bhaskaran N., Persson A., Uhlen M., Sangfelt O. et al. 2009. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 326: 718-721.
66. Viatte L., Vaulont S. (2009) Hepcidin, the iron watcher. Biochimie. 91: 1223-1228.
67. Volz K. (2008) The functional duality of iron regulatory protein 1. Curr. Opin. Struct. Biol. 18: 106-111.
68. Wallander M.L., Leibold E.A., Eisenstein R.S. (2006) Molecular control of vertebrate iron homeostasis by iron regulatory proteins. Biochim. Biophys. Acta. 1763: 668-689.
69. Wang J., Chen G., Pantopoulos K. (2005) Nitric oxide inhibits the degradation of IRP2. Mol. Cell Biol. 25: 1347-1353.
70. Watts R.N., Ponka P., Richardson D.R. (2003) Effects of nitrogen monoxide and carbon monoxide on molecular and cellular iron metabolism: mirror-image effector molecules that target iron. Biochem J. 369: 429-440.
71. Weinberg E.D. (1997) The Lactobacillus anomaly: total iron abstinence. Perspect. Biol. Med. 40: 578-583.
72. Weiss G., Goossen B., Doppler W., Fuchs D., Pantopoulos K., Werner-Felmayer G., Wachter H., Hentze M.W. (1993) Translational regulation via iron-responsive elements by the nitric oxide/NO-synthase pathway. EMBO J. 12: 3651-3657.
73. Ye H., Rouault T.A. (2010) Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry 49: 4945-4456.
74. Zheng L., Kennedy M.C., Blondin G.A., Beinert H., Zalkin H. (1992) Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Arch. Biochem. Biophys. 299: 356-360.