Heme metabolism as an integral part of iron homeostasis;Metabolizm hemu jako integralny element homeostazy zelaza

Postepy Higieny i Medycyny Doswiadczalnej

Volumn 68, Issue , 2014, Pages 557-570

  Lipiński, Pawel ^a   Starzyński, Rafal R ^a   Stys̈, Agnieszka ^a   Gajowiak, Anna ^a   Staroń, Robert ^a  

^a Instytutu Genetyki i Hodowli Zwierz t PAN w Jastrzebcu   (Poland)

Author keywords

Erythroblast; Erythrophagocytosis; Ferroportin; Heme; Heme oxygenase; IRE; Iron; IRP

Indexed keywords

CATION TRANSPORT PROTEIN; FERROCHELATASE; HEME; HEME OXYGENASE 1; HEPCIDIN; IRON; METAL TRANSPORTING PROTEIN 1;

ANIMAL; BIOSYNTHESIS; ERYTHROCYTE; HEMOLYSIS; HOMEOSTASIS; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; CATION TRANSPORT PROTEINS; ERYTHROCYTES; FERROCHELATASE; HEME; HEME OXYGENASE-1; HEMOLYSIS; HEPCIDINS; HOMEOSTASIS; HUMANS; IRON;

EID: 84920574777     PISSN: 00325449     EISSN: 17322693     Source Type: Journal    
DOI: 10.5604/17322693.1102284     Document Type: Review

References (112)

1. Anderson G.J., Frazer D.M., McKie A.T., Vulpe C.D., Smith A.: Mechanisms of haem and non-haem iron absorption: Lessons from inherited disorders of iron metabolism. Biometals, 2005; 18: 339-348
2. Andrews N.C.: The iron transporter DMT1. Int. J. Biochem. Cell Biol., 1999; 31: 991-994
3. Auriac A., Willemetz A., Canonne-Hergaux F.: Lipid raft-dependent endocytosis: A new route for hepcidin-mediated regulation of ferroportin in macrophages. Haematologica, 2010; 95: 1269-1277
4. Beaumont C.: Multiple regulatory mechanisms act in concert to control ferroportin expression and heme iron recycling by macrophages. Haematologica, 2010; 95: 1233-1236
5. Bowman S.E., Bren K.L.: The chemistry and biochemistry of heme c: Functional bases for covalent attachment. Nat. Prod. Rep., 2008; 25: 1118-1130
6. Camaschella C., Campanella A., De Falco L., Boschetto L., Merlini R., Silvestri L., Levi S., Iolascon A.: The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload. Blood, 2007; 110: 1353-1358
7. Chiabrando D., Marro S., Mercurio S., Giorgi C., Petrillo S., Vinchi F., Fiorito V., Fagoonee S., Camporeale A., Turco E., Merlo G.R, Silengo L., Altruda F, Pinton P., Tolosano E.: The mitochondrial heme exporter FLVCR1b mediates erythroid differentiation. J. Clin. Invest., 2012; 122: 4569-4579
8. Clark S.F.: Iron deficiency anemia: Diagnosis and management. Curr. Opin. Gastroenterol., 2009, 25: 122-128
9. Cooperman S.S., Meyron-Holtz E.G., Olivierre-Wilson H., Ghosh M.C., McConnell J.P., Rouault T.A.: Microcytic anemia, erythropoietic protoporphyria, and neurodegeneration in mice with targeted deletion of iron-regulatory protein 2. Blood, 2005; 106: 1084-1091
10. Cox T.C., Bawden M.J., Martin A., May B.K.: Human erythroid 5-Aminolevulinate synthase: Promoter analysis and identification of an iron-responsive element in the mRNA. EMBO J., 1991; 10: 1891-1902
11. Crooks D.R., Ghosh M.C., Haller R.G., Tong W.H., Rouault T.A.: Posttranslational stability of the heme biosynthetic enzyme ferrochelatase is dependent on iron availability and intact iron-sulfur cluster assembly machinery. Blood, 2010; 115: 860-869
12. Dandekar T., Stripecke R., Gray N.K., Goossen B., Constable A., Johansson H.E., Hentze M.W.: Identification of a novel iron-responsive element in murine and human erythroid delta-Aminolevulinic acid synthase mRNA. EMBO J., 1991; 10: 903-909
13. Davis M.R., Shawron K.M., Rendina E., Peterson S.K., Lucas E.A., Smith B.J., Clarke S.L.: Hypoxia inducible factor-2 α is translationally repressed in response to dietary iron deficiency in Sprague-Dawley rats. J. Nutr., 2011; 141: 1590-1596
14. De Domenico I., Ward D.M., Langelier C., Vaughn M.B., Nemeth E., Sundquist W.I., Ganz T., Musci G., Kaplan J.: The molecular mechanism of hepcidin-mediated ferroportin down-regulation. Mol. Biol. Cell, 2007; 18: 2569-2578
15. Delaby C., Pilard N., Hetet G., Driss F., Grandchamp B., Beaumont C., Canonne-Hergaux F.: A physiological model to study iron recycling in macrophages. Exp. Cell Res., 2005; 310: 43-53
16. Delaby C., Pilard N., Puy H., Canonne-Hergaux F.: Sequential regulation of ferroportin expression after erythrophagocytosis in murine macrophages: Early mRNA induction by haem, followed by iron-dependent protein expression. Biochem. J., 2008; 411: 123-131
17. Delaby C., Rondeau C., Pouzet C., Willemetz A., Pilard N., Desjardins M., Canonne-Hergaux F.: Subcellular localization of iron and heme metabolism related proteins at early stages of erythrophagocytosis. PLoS One, 2012; 7: E42199
18. Desuzinges-Mandon E., Arnaud O., Martinez L., Huché F., Di Pietro A., Falson P.: ABCG2 transports and transfers heme to albumin through its large extracellular loop. J. Biol. Chem., 2010; 285: 33123-33133
19. Epstein A.C., Gleadle J.M., McNeill L.A., Hewitson K.S., O'Rourke J., Mole D.R., Mukherji M., Metzen E., Wilson M.I., Dhanda A., Tian Y.M., Masson N., Hamilton D.L., Jaakkola P., Barstead R. I wsp.: C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell, 2001; 107: 43-54
20. Fleming M.D., Romano M.A., Su M.A., Garrick L.M., Garrick M.D., Andrews N.C.: Nramp2 is mutated in the anemic Belgrade (b) rat: Evidence of a role for Nramp2 in endosomal iron transport. Proc. Natl. Acad. Sci. USA, 1998; 95: 1148-1153
21. Folgueras A.R., de Lara F.M., Pendás A.M., Garabaya C., Rodríguez F., Astudillo A., Bernal T., Cabanillas R., López-Otín C., Velasco G.: Membrane-bound serine protease matriptase-2 (Tmprss6) is an essential regulator of iron homeostasis. Blood, 2008; 112: 2539-2545
22. French C.E., Bell J.M., Ward F.B.: Diversity and distribution of hemerythrin-like proteins in prokaryotes. FEMS Microbiol. Lett., 2008; 279: 131-145
23. Furuyama K., Kaneko K., Vargas P.D.: Heme as a magnificent molecule with multiple missions: Heme determines its own fate and governs cellular homeostasis. Tohoku J. Exp. Med., 2007; 213: 1-16
24. Galy B., Ferring D., Minana B., Bell O., Janser H.G., Muckenthaler M., Schumann K., Hentze M.W.: Altered body iron distribution and microcytosis in mice deficient in iron regulatory protein 2 (IRP2). Blood, 2005; 106: 2580-2589
25. Galy B., Ferring-Appel D., Becker C., Gretz N., Gröne H.J., Schümann K., Hentze M.W.: Iron regulatory proteins control a mucosal block to intestinal iron absorption. Cell Rep., 2013; 3: 844-857
26. Galy B., Ferring-Appel D., Kaden S., Gröne H.J., Hentze M.W.: Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab., 2008; 7: 79-85
27. Galy B., Ferring-Appel D., Sauer S.W., Kaden S., Lyoumi S., Puy H., Kölker S., Gröne H.J., Hentze M.W.: Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab., 2010, 12: 194-201
28. Ganz T.: Cellular iron: Ferroportin is the only way out. Cell Metab., 2005; 1: 155-157
29. Ganz T., Nemeth E.: Hepcidin and iron homeostasis. Biochim. Biophys. Acta, 2012; 1823: 1434-1443
30. Gonzalez-Rosendo G., Polo J., Rodriguez-Jerez J.J., Puga-Diaz R., Reyes-Navarrete E.G., Quintero-Gutierrez A.G.: Bioavailability of a heme-iron concentrate product added to chocolate biscuit filling in adolescent girls living in a rural area of Mexico. J. Food Sci., 2010; 75: H73-H78
31. Gottlieb Y., Truman M., Cohen L.A., Leichtmann-Bardoogo Y., Meyron-Holtz E.G.: Endoplasmic reticulum anchored heme-oxygenase 1 faces the cytosol. Haematologica, 2012; 97: 1489-1493
32. Gozzelino R., Andrade B.B., Larsen R., Luz N.F., Vanoaica L., Seixas E., CoutinhoA., Cardoso S., Rebelo S., Poli M., Barral-Netto M., Darshan D., Kühn L.C., Soares M.P.: Metabolic adaptation to tissue iron overload confers tolerance to malaria. Cell Host Microbe, 2012; 12: 693-704
33. Gozzelino R., Soares M.P.: Heme sensitization to TNF-mediated programmed cell death. Adv. Exp. Med. Biol., 2011; 691: 211-219
34. Guo B., Yu Y., Leibold E.A.: Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem., 1994; 269: 24252-24260
35. Harrison P.M., Arosio P.: The ferritins: Molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta, 1996; 1275: 161-203
36. Hentze M.W., Muckenthaler M.U., Galy B., Camaschella C.: Two to tango: Regulation of mammalian iron metabolism. Cell, 2010; 142: 24-38
37. Hira S., Tomita T., Matsui T., Igarashi K., Ikeda-Saito M.: Bach1, a heme-dependent transcription factor, reveals presence of multiple heme binding sites with distinct coordination structure. IUBMB Life, 2007; 59: 542-551
38. Hvidberg V., Maniecki M.B., Jacobsen C., Højrup P., Møller H.J., Moestrup S.K.: Identification of the receptor scavenging hemopexin-heme complexes. Blood, 2005; 106: 2572-2579
39. Kakhlon O., Cabantchik Z.I.: The labile iron pool: Characterization, measurement, and participation in cellular processes. Free Radic. Biol. Med., 2002; 33: 1037-1046
40. Kakhlon O., Gruenbaum Y., Cabantchik Z.I.: Repression of ferritin expression increases the labile iron pool, oxidative stress, and short term growth of human erythroleukemia cells. Blood, 2001; 97: 2863-2871
41. Keel S.B., Doty R.T., Yang Z., Quigley J.G., Chen J., Knoblaugh S., Kingsley P.D., De Domenico I., Vaughn M.B., Kaplan J., Palis J., Abkowitz J.L.: A heme export protein is required for red blood cell differentiation and iron homeostasis. Science, 2008; 319: 825-828
42. Khan A.A., Quigley J.G.: Control of intracellular heme levels: Heme transporters and heme oxygenases. Biochim. Biophys. Acta, 2011; 1813: 668-682
43. Khan A.A., Quigley J.G.: Heme and FLVCR-related transporter families SLC48 and SLC49. Mol. Aspects Med., 2013; 34: 669-682
44. Kikuchi G., Yoshida T., Noguchi M.: Heme oxygenase and heme degradation. Biochem. Biophys. Res. Commun., 2005; 338: 558-567
45. Knutson M., Wessling-Resnick M.: Iron metabolism in the reticuloendothelial system. Crit. Rev. Biochem. Mol. Biol., 2003; 38: 61-88
46. Knutson M.D., Oukka M., Koss L.M., Aydemir F., Wessling-Resnick M.: Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc. Natl. Acad. Sci. USA, 2005; 102: 1324-1328
47. Konijn A.M., Glickstein H., Vaisman B., Meyron-Holtz E.G., Slotki I.N., Cabantchik Z.I.: The cellular labile iron pool and intracellular ferritin K562 cells. Blood, 1999; 94: 2128-2134
48. Kovtunovych G., Eckhaus M.A., Ghosh M.C., Ollivierre-Wilson H., Rouault T.: Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: Effects on macrophage viability and tissue iron distribution. Blood, 2010; 116: 6054-6062
49. Kruszewski M.: Labile iron pool: The main determinant of cellular response to oxidative stress. Mutat. Res., 2003; 531: 81-92
50. Le Blanc S., Garrick M.D., Arredondo M.: Heme carrier protein 1 transports heme and is involved in heme-Fe metabolism. Am. J. Physiol. Cell Physiol., 2012; 302: C1780-C1785
51. Lill R., Hoffmann B., Molik S., Pierik A.J., Rietzschel N., Stehling O., Uzarska M.A., Webert H., Wilbrecht C., Mühlenhoff U.: The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim. Biophys. Acta, 2012; 1823: 1491-1508
52. Lin Y.W., Wang J.: Structure and function of heme proteins in non-native states: A mini-review, J. Inorg. Biochem., 2013; 129: 162-171
53. Lipiński P., Starzyński R.R., Stys̈ A., Stracilo M.: Iron homeostasis, a defense mechanism in oxidative stress. Postępy Biochem., 2010; 56: 305-316
54. Liu Z.G., Hsu H., Goeddel D.V., Karin M.: Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell, 1996; 87: 565-576
55. Mangum C.P.: Oxygen transport in invertebrates. Am. J. Physiol., 1985; 248: R505-R514
56. Marques L., Auriac A., Willemetz A., Banha J., Silva B., Canonne-Hergaux F., Costa L.: Immune cells and hepatocytes express glycosylphosphatidylinositol-Anchored ceruloplasmin at their cell surface. Blood Cells Mol. Dis., 2012; 48: 110-120
57. Mastrogiannaki M., Matak P., Keith B., Simon M.C., Vaulont S., Peyssonnaux C.: HIF-2α, but not HIF-1α, promotes iron absorption in mice. J. Clin. Invest., 2009; 119: 1159-1166
58. Mastrogiannaki M., Matak P., Peyssonnaux C.: The gut in iron homeostasis: Role of HIF-2 under normal and pathological conditions. Blood, 2013; 122: 885-892
59. McKie A.T., Barrow D., Latunde-Dada G.O., Rolfs A., Sager G., Mudaly E., Mudaly M., Richardson C., Barlow D., Bomford A., Peters T.J., Raja K.B., Shirali S., Hediger M.A., Farzaneh F., Simpson R.J.: An iron regulated ferric reductase associated with the absorption of dietary iron. Science, 2001; 291: 1755-1759
60. McKie A.T., Marciani P., Rolfs A., Brennan K., Wehr K., Barrow D., Miret S., Bomford A., Peters T.J., Farzaneh F., Hediger M.A., Hentze M.W., Simpson R.J.: A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell., 2000; 5: 299-309
61. 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
62. Mueller S.: Iron regulatory protein 1 as a sensor of reactive oxygen species. Biofactors, 2005; 24: 171-181
63. 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
64. Ohgami R.S., Campagna D.R., Greer E.L., Antiochos B., McDonald A., Chen J., Sharp J.J., Fujiwara Y., Barker J.E., Fleming M.D.: Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat. Genet., 2005; 37: 1264-1269
65. Paoli M., Marles-Wright J., Smith A.: Structure-function relationships in heme-proteins. DNA Cell Biol., 2002; 21: 271-280
66. Parfenova H, Leffler C.W.: Cerebroprotective functions of HO-2. Curr. Pharm. Des., 2008; 14: 443-453
67. Petrat F., de Groot H., Rauen U.: Subcellular distribution of chelatable iron: A laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem. J., 2001; 356: 61-69
68. Pham C.G., Bubici C., Zazzeroni F., Papa S., Jones J., Alvarez K., Jayawardena S., De Smaele E., Cong R., Beaumont C., Torti F.M., Torti S.V., Franzoso G.: Ferritin heavy chain upregulation by NF-κB inhibits TNFα-induced apoptosis by suppressing reactive oxygen species. Cell, 2004; 119: 529-542
69. Picard V., Epsztejn S., Santambrogio P., Cabantchik Z.I., Beaumont C.: Role of ferritin in the control of the labile iron pool in murine erythroleukemia cells. J. Biol. Chem., 1998; 273: 15382-15386
70. Pietrangelo A.: Hereditary hemochromatosis: Pathogenesis, diagnosis, and treatment. Gastroenterology, 2010; 139: 393-408
71. Ponka P.: Cell biology of heme. Am. J. Med. Sci., 1999; 318: 241-256
72. Ponka P., Lok C.N.: The transferrin receptor: Role in health and disease. Int. J. Biochem. Cell Biol., 1999; 31: 1111-1137
73. Poss K.D., Tonegawa S.: Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. USA, 1997; 94: 10919-10924
74. Quigley J.G., Yang Z., Worthington M.T., Phillips J.D., Sabo K.M., Sabath D.E., Berg C.L., Sassa S., Wood B.L., Abkowitz J.L.: Identification of a human heme exporter that is essential for erythropoiesis. Cell, 2004; 118: 757-766
75. Quintero-Gutierrez A.G., Gonzalez-Rosendo G., Sanchez-Munoz J., Polo-Pozo J., Rodriguez-Jerez J.J.: Bioavailability of heme iron in biscuit filling using piglets as an animal model for humans. Int. J. Biol. Sci., 2008; 4: 58-62
76. Rajagopal A., Rao A.U., Amigo J., Tian M., Upadhyay S.K., Hall C., Uhm S., Mathew M.K., Fleming M.D., Paw B.H., Krause M., Hamza I.: Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins. Nature, 2008; 453: 1127-1131
77. Rouault T.A.: The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol., 2006; 2: 406-414
78. Rouhier N., Couturier J., Johnson M.K., Jacquot J.P.: Glutaredoxins: Roles in iron homeostasis. Trends. Biochem. Sci., 2010; 35: 43-52
79. 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
80. Sanchez M., Galy B., Muckenthaler M.U., Hentze M.W.: Iron-regulatory proteins limit hypoxia-inducible factor-2alpha expression in iron deficiency. Nat. Struct. Mol. Biol., 2007; 14: 420-426
81. Sassa S.: Why heme needs to be degraded to iron, biliverdin IXα, and carbon monoxide? Antioxid. Redox Signal., 2004; 6: 819-824
82. Shah Y.M., Matsubara T., Ito S., Yim S.H., Gonzalez F.J.: Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab., 2009; 9: 152-164
83. Shaw G.C., Cope J.J., Li L., Corson K., Hersey C., Ackermann G.E., Gwynn B., Lambert A.J., Wingert R.A., Traver D., Trede N.S., Barut B.A., Zhou Y., Minet E., Donovan A. i wsp.: Mitoferrin is essential for erythroid iron assimilation. Nature, 2006; 440: 96-100
84. Shayeghi M., Latunde-Dada G.O., Oakhill J.S., Laftah A.H., Takeuchi K., Halliday N., Khan Y., Warley A., McCann F.E., Hider R.C., Frazer D.M., Anderson G.J., Vulpe C.D., Simpson R.J., McKie A.T.: Identification of an intestinal heme transporter. Cell, 2005; 122: 789-801
85. Shi H., Bencze K.Z., Stemmler T.L., Philpott C.C.: A cytosolic iron chaperone that delivers iron to ferritin. Science, 2008; 320: 1207-1210
86. Sikorska K., Bielawski K.P., Romanowski T., Stalke P.: Hemochromatoza dziedziczna -najczęstsza choroba genetyczna czlowieka. Postępy Hig. Med. Dos̈w., 2006; 60: 667-676
87. Smith A., Rish K.R., Lovelace R., Hackney J.F., Helston R.M.: Role for copper in the cellular and regulatory effects of heme-hemopexin. Biometals, 2009; 22: 421-437
88. Soe-Lin S., Apte S.S, Andriopoulos B.Jr, Andrews M.C., Schranzhofer M., Kahawita T., Garcia-Santos D., Ponka P.: Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo. Proc. Natl. Acad. Sci. USA, 2009; 106: 5960-5965
89. Starzyński R.R., Canonne-Hergaux F., Lenartowicz M., Krzeptowski W., Willemetz A., Stys̈ A., Bierla J., Pietrzak P., Dziaman T., Lipiński P.: Ferroportin expression in haem oxygenase 1-deficient mice. Biochem. J., 2013; 449: 69-78
90. Starzyński R.R., Lipiński P.: IRP1, bialko kontrolujące homeostazę zelaza komórkach ssaków: Regulacja jego aktywnos̈ci przez jony zelaza i tlenek azotu. Postępy Biol. Kom., 2003; 30: 497-514
91. Stys̈ A., Galy B., Starzyński R.R., Smuda E., Drapier J.C., Lipiński P., Bouton C.: Iron regulatory protein 1 outcompetes iron regulatory protein 2 in regulating cellular iron homeostasis in response to nitric oxide. J. Biol. Chem., 2011; 286: 22846-22854
92. Sun C.C., Vaja V., Babitt J.L., Lin H.Y.: Targeting the hepcidin-ferroportin axis to develop new treatment strategies for anemia of chronic disease and anemia of inflammation. Am. J. Hematol., 2012; 87: 392-400
93. Suzuki H., Tashiro S., Hira S., Sun J., Yamazaki C., Zenke Y., Ikeda-Saito M., Yoshida M., Igarashi K.: Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J., 2004; 23: 2544-2553
94. Tanno T., Bhanu N.V., Oneal P.A., Goh S.H., Staker P., Lee Y.T., Moroney J.W, Reed C.H., Luban N.L., Wang R.H., Eling T.E., Childs R., Ganz T., Leitman S.F., Fucharoen S., Miller J.L.: High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nat. Med., 2007; 13: 1096-1101
95. Tanno T., Porayette P., Sripichai O., Noh S.J., Byrnes C., Bhupatiraju A., Lee Y.T., Goodnough J.B., Harandi O., Ganz T., Paulson R.F., Miller J.L.: Identification of TWSG1 as a second novel erythroid regulator of hepcidin expression in murine and human cells. Blood, 2009; 114: 181-186
96. Tolosano E., Fagoonee S., Morello N., Vinchi F., Fiorito V.: Heme scavenging and the other facets of hemopexin. Antioxid. Redox Signal., 2010; 12: 305-320
97. Tolosano E., Hirsch E., Patrucco E., Camaschella C., Navone R., Silengo L., Altruda F.: Defective recovery and severe renal damage after acute hemolysis in hemopexin-deficient mice. Blood, 1999; 94: 3906-3914
98. 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
99. Viatte L., Vaulont S.: Hepcidin, the iron watcher. Biochimie, 2009; 91: 1223-1228
100. Vinchi F., Gastaldi S., Silengo L., Altruda F., Tolosano E.: Hemopexin prevents endothelial damage and liver congestion in a mouse model of heme overload. Am. J. Pathol., 2008; 173: 289-299
101. Volz K.: The functional duality of iron regulatory protein 1. Curr. Opin. Struct. Biol., 2008; 18: 106-111
102. Vulpe C.D., Kuo Y.M., Murphy T.L., Cowley L., Askwith C., Libina N., Gitschier J., Anderson G.J.: Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat. Genet., 1999; 21: 195-199
103. Walker F.A.: Models of the bis-histidine-ligated electron-Transferring cytochromes. Comparative geometric and electronic structure of low-spin ferro-And ferrihemes. Chem. Rev., 2004; 104: 589-615
104. Wang X.M., Kim H.P., Nakahira K., Ryter S.W., Choi A.M.: The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 si gnaling by regulating the interaction of TLR4 with caveolin-1. J. Immunol., 2009; 182: 3809-3818
105. West A.R., Oates P.S.: Subcellular location of heme oxygenase 1 and 2 and divalent metal transporter 1 in relation to endocytotic markers during heme iron absorption. J. Gastroenterol. Hepatol., 2008; 23: 150-158
106. White K.N., Conesa C., Sánchez L., Amini M., Farnaud S., Lorvoralak C., Evans R.W.: The transfer of iron between ceruloplasmin and transferrins. Biochim. Biophys. Acta, 2012; 1820: 411-416
107. Yang Z., Philips J.D., Doty R.T., Giraudi P., Ostrow J.D., Tiribelli C., Smith A., Abkowitz J.L.: Kinetics and specificity of feline leukemia virus subgroup C receptor (FLVCR) export function and its dependence on hemopexin. J. Biol. Chem., 2010, 285: 28874-28882
108. Ye H., Jeong S.Y., Ghosh M.C., Kovtunovych G., Silvestri L., Ortillo D., Uchida N., Tisdale J., Camaschella C., Rouault T.A.: Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts. J. Clin. Invest., 2010; 120: 1749-1761
109. Ye H., Rouault T.A.: Erythropoiesis and iron-sulfur cluster biogenesis. Adv. Hematol., 2010; 2010: 1-8
110. Young M.F., Griffin I., Pressman E., McIntyre A.W., Cooper E., McNanley T., Harris Z.L., Westerman M., O'Brien K.O.: Utilization of iron from an animal-based iron source is greater than that of ferrous sulfate in pregnant and nonpregnant women. J. Nutr., 2010; 140: 2162-2166
111. Zhang D.L., Hughes R.M., Ollivierre-Wilson H., Ghosh M.C., Rouault T.A.: A ferroportin transcript that lacks an iron-responsive element enables duodenal and erythroid precursor cells to evade translational repression. Cell Metab., 2009; 9: 461-473
112. Zhang D.L., Senecal T., Ghosh M.C., Ollivierre-Wilson H., Tu T., Rouault T.A.: Hepcidin regulates ferroportin expression and intracellular iron homeostasis of erythroblasts. Blood, 2011; 118: 2868-2877