Macrophages and iron trafficking at the birth and death of red cells

Blood

Volumn 125, Issue 19, 2015, Pages 2893-2897

  Korolnek, Tamara ^a   Hamza, Iqbal ^a  

^a University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEME; IRON;

ARTICLE; BIRTH; CELL DEATH; CELL MIGRATION; DEATH; ERYTHROCYTE; ERYTHROID CELL; ERYTHROPHAGOCYTOSIS; ERYTHROPOIESIS; HOMEOSTASIS; HUMAN; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CYTOLOGY; METABOLISM;

ANIMALS; ERYTHROCYTES; HOMEOSTASIS; HUMANS; IRON; MACROPHAGES;

EID: 84929186045     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-567776     Document Type: Article

References (74)

1. Aisen P, Enns C, Wessling-Resnick M. Chemistry and biology of eukaryotic iron metabolism. Int J Biochem Cell Biol. 2001; 33(10):940-959.
2. Papanikolaou G, Pantopoulos K. Iron metabolism and toxicity. Toxicol Appl Pharmacol. 2005;202(2):199-211.
3. Gkouvatsos K, Papanikolaou G, Pantopoulos K. Regulation of iron transport and the role of transferrin. Biochim Biophys Acta. 2012;1820(3):188-202.
4. Palis J. Primitive and definitive erythropoiesis in mammals. Front Physiol. 2014;5:3.
5. Bessis M. [Erythroblastic island, functional unity of bone marrow] [in French]. Rev Hematol. 1958;13(1):8-11.
6. An X, Mohandas N. Erythroblastic islands, terminal erythroid differentiation and reticulocyte maturation. Int J Hematol. 2011;93(2):139-143.
7. de Back DZ, Kostova EB, van Kraaij M, van den Berg TK, van Bruggen R. Of macrophages and red blood cells; a complex love story. Front Physiol. 2014;5:9.
8. Liu XS, Li XH, Wang Y, et al. Disruption of palladin leads to defects in definitive erythropoiesis by interfering with erythroblastic island formation in mouse fetal liver. Blood. 2007;110(3):870-876.
9. Sadahira Y, Yoshino T, Monobe Y. Very late activation antigen 4-vascular cell adhesion molecule 1 interaction is involved in the formation of erythroblastic islands. JExpMed.1995;181(1):411-415.
10. Soni S, Bala S, Gwynn B, Sahr KE, Peters LL, Hanspal M. Absence of erythroblast macrophage protein (Emp) leads to failure of erythroblast nuclear extrusion. J Biol Chem. 2006;281(29): 20181-20189.
11. Kusakabe M, Hasegawa K, Hamada M, et al. c-Maf plays a crucial role for the definitive erythropoiesis that accompanies erythroblastic island formation in the fetal liver. Blood. 2011; 118(5):1374-1385.
12. Hirsch E, Iglesias A, Potocnik AJ, Hartmann U, Fässler R. Impaired migration but not differentiation of haematopoietic stem cells in the absence of beta1 integrins. Nature. 1996; 380(6570):171-175.
13. Ulyanova T, Jiang Y, Padilla S, Nakamoto B, Papayannopoulou T. Combinatorial and distinct roles of a? and a? integrins in stress erythropoiesis in mice. Blood. 2011;117(3):975-985.
14. Ulyanova T, Padilla SM, Papayannopoulou T. Stage-specific functional roles of integrins in murine erythropoiesis. Exp Hematol. 2014;42(5): 404-409.e4.
15. Chow A, Huggins M, Ahmed J, et al. CD169+ macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat Med. 2013;19(4):429-436.
16. Ramos P, Casu C, Gardenghi S, et al. Macrophages support pathological erythropoiesis in polycythemia vera and b-thalassemia. Nat Med. 2013;19(4):437-445.
17. da Silva Lima F, Rogero MM, Ramos MC, Borelli P, Fock RA. Modulation of the nuclear factor-kappa B (NF-kB) signalling pathway by glutamine in peritoneal macrophages of a murine model of protein malnutrition. Eur J Nutr. 2013;52(4):1343-1351.
18. Jacobsen RN, Forristal CE, Raggatt LJ, et al. Mobilization with granulocyte colony-stimulating factor blocks medullar erythropoiesis by depleting F4/80(1)VCAM1(1)CD169(1)ER-HR3(1)Ly6G(1) erythroid island macrophages in the mouse. Exp Hematol. 2014;42(7):547-561.e4.
19. Juarez JG, Harun N, Thien M, et al. Sphingosine-1-phosphate facilitates trafficking of hematopoietic stem cells and their mobilization by CXCR4 antagonists in mice. Blood. 2012;119(3):707-716.
20. Walsh RJ, Thomas ED, Chow SK, Fluharty RG, Finch CA. Iron Metabolism. Heme Synthesis in Vitro by Immature Erythrocytes. Science. 1949; 110(2859):396-398.
21. Jandl JH, Inman JK, Simmons RL, Allen DW. Transfer of iron from serum iron-binding protein to human reticulocytes. J Clin Invest. 1959; 38(1, Part 1):161-185.
22. Allen DW, Jandl JH. Kinetics of intracellular iron in rabbit reticulocytes. Blood. 1960;15:71-81.
23. Jandl JH, Katz JH. The plasma-to-cell cycle of transferrin in iron utilization. Trans Assoc Am Physicians. 1961;74:72-76.
24. Jandl JH, Katz JH. The plasma-to-cell cycle of transferrin. J Clin Invest. 1963;42:314-326.
25. Paoletti C, Durand M, Gosse C, Boiron M. [Absence of consummation of siderophilin during hemoglobin synthesis in vitro] [in French]. Rev Fr Etud Clin Biol. 1958;3(3):259-261.
26. Richardson DR, Ponka P. The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta. 1997;1331(1):1-40.
27. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. Two to tango: regulation of Mammalian iron metabolism. Cell. 2010;142(1):24-38.
28. Bartnikas TB. Known and potential roles of transferrin in iron biology. Biometals. 2012;25(4):677-686.
29. Levy JE, Jin O, Fujiwara Y, Kuo F, Andrews NC. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat Genet. 1999;21(4):396-399.
30. Li JY, Paragas N, Ned RM, et al. Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev Cell. 2009;16(1):35-46.
31. Beutler E, Gelbart T, Lee P, Trevino R, Fernandez MA, Fairbanks VF. Molecular characterization of a case of atransferrinemia. Blood. 2000;96(13):4071-4074.
32. Asada-Senju M, Maeda T, Sakata T, Hayashi A, Suzuki T. Molecular analysis of the transferrin gene in a patient with hereditary hypotransferrinemia. J Hum Genet. 2002;47(7):355-359.
33. Knisely AS, Gelbart T, Beutler E. Molecular characterization of a third case of human atransferrinemia. Blood. 2004;104(8):2607.
34. Aslan D, Crain K, Beutler E. A new case of human atransferrinemia with a previously undescribed mutation in the transferrin gene. Acta Haematol. 2007;118(4):244-247.
35. Chen C, Wen S, Tan X. Molecular analysis of a novel case of congenital atransferrinemia. Acta Haematol. 2009;122(1):27-28.
36. Bernstein SE. Hereditary hypotransferrinemia with hemosiderosis, a murine disorder resembling human atransferrinemia. J Lab Clin Med. 1987; 110(6):690-705.
37. Huggenvik JI, Craven CM, Idzerda RL, Bernstein S, Kaplan J, McKnight GS. A splicing defect in the mouse transferrin gene leads to congenital atransferrinemia. Blood. 1989;74(1):482-486.
38. Trenor CC III, Campagna DR, Sellers VM, Andrews NC, Fleming MD. The molecular defect in hypotransferrinemic mice. Blood. 2000;96(3): 1113-1118.
39. Policard A, Bessis M. Micropinocytosis and rhopheocytosis. Nature. 1962;194:110-111.
40. Leimberg JM, Konijn AM, Fibach E. Developing human erythroid cells grown in transferrin-free medium utilize iron originating from extracellular ferritin. Am J Hematol. 2003;73(3):211-212.
41. Leimberg MJ, Prus E, Konijn AM, Fibach E. Macrophages function as a ferritin iron source for cultured human erythroid precursors. J Cell Biochem. 2008;103(4):1211-1218.
42. Nicolas G, Bennoun M, Devaux I, et al. Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci USA. 2001; 98(15):8780-8785.
43. Park CH, Valore EV, Waring AJ, Ganz T. Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem. 2001; 276(11):7806-7810.
44. Pigeon C, Ilyin G, Courselaud B, et al. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem. 2001;276(11):7811-7819.
45. Nemeth E, Tuttle MS, Powelson J, et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004;306(5704):2090-2093.
46. Kautz L, Jung G, Valore EV, Rivella S, Nemeth E, Ganz T. Identification of erythroferrone as an erythroid regulator of iron metabolism. Nat Genet. 2014;46(7):678-684.
47. Campbell MR, Karaca M, Adamski KN, Chorley BN, Wang X, Bell DA. Novel hematopoietic target genes in the NRF2-mediated transcriptional pathway. Oxid Med Cell Longev. 2013;2013:120305.
48. Keel SB, Doty RT, Yang Z, et al. A heme export protein is required for red blood cell differentiation and iron homeostasis. Science. 2008;319(5864):825-828.
49. Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M. Iron release from macrophages after erythrophagocytosis is upregulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc Natl Acad Sci USA. 2005;102(5):1324-1328.
50. Quigley JG, Yang Z, Worthington MT, et al. Identification of a human heme exporter that is essential for erythropoiesis. Cell. 2004;118(6): 757-766.
51. Vinchi F, Ingoglia G, Chiabrando D, et al. Heme exporter FLVCR1a regulates heme synthesis and degradation and controls activity of cytochromes P450. Gastroenterology. 2014;146(5):1325-1338.
52. Bratosin D, Mazurier J, Tissier JP, et al. Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie. 1998;80(2):173-195.
53. Knutson M, Wessling-Resnick M. Iron metabolism in the reticuloendothelial system. Crit Rev Biochem Mol Biol. 2003;38(1):61-88.
54. Beaumont C, Delaby C. Recycling iron in normal and pathological states. Semin Hematol. 2009; 46(4):328-338.
55. Ganz T. Macrophages and systemic iron homeostasis. J Innate Immun. 2012;4(5-6):446-453.
56. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA. 1997;94(20):10919-10924.
57. Kovtunovych G, Eckhaus MA, Ghosh MC, Ollivierre-Wilson H, Rouault TA. Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: effects on macrophage viability and tissue iron distribution. Blood. 2010;116(26): 6054-6062.
58. Yachie A, Niida Y, Wada T, et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103(1):129-135.
59. Kawashima A, Oda Y, Yachie A, Koizumi S, Nakanishi I. Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol. 2002;33(1):125-130.
60. Radhakrishnan N, Yadav SP, Sachdeva A, et al. Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J Pediatr Hematol Oncol. 2011;33(1):74-78.
61. Beaumont C, Canonne-Hergaux F. [Erythrophagocytosis and recycling of heme iron in normal and pathological conditions; regulation by hepcidin] [in French]. Transfus Clin Biol. 2005; 12(2):123-130.
62. Yoshida T, Sato M. Posttranslational and direct integration of heme oxygenase into microsomes. Biochem Biophys Res Commun. 1989;163(2): 1086-1092.
63. Gottlieb Y, Truman M, Cohen LA, Leichtmann-Bardoogo Y, Meyron-Holtz EG. Endoplasmic reticulum anchored heme-oxygenase 1 faces the cytosol. Haematologica. 2012;97(10):1489-1493.
64. Liu Y, Ortiz de Montellano PR. Reaction intermediates and single turnover rate constants for the oxidation of heme by human heme oxygenase-1. J Biol Chem. 2000;275(8): 5297-5307.
65. Maines MD, Ewing JF, Huang TJ, Panahian N. Nuclear localization of biliverdin reductase in the rat kidney: response to nephrotoxins that induce heme oxygenase-1. J Pharmacol Exp Ther. 2001; 296(3):1091-1097.
66. Reed JR, Huber WJ III, Backes WL. Human heme oxygenase-1 efficiently catabolizes heme in the absence of biliverdin reductase. Drug Metab Dispos. 2010;38(11):2060-2066.
67. Delaby C, Rondeau C, Pouzet C, et al. Subcellular localization of iron and heme metabolism related proteins at early stages of erythrophagocytosis. PLoS ONE. 2012;7(7): e42199.
68. WhiteC,YuanX,SchmidtPJ,etal.HRG1 is essential for heme transport from the phagolysosome of macrophages during erythrophagocytosis. Cell Metab. 2013;17(2):261-270.
69. Rajagopal A, Rao AU, Amigo J, et al. Haem homeostasis is regulated by the conserved and concerted functions of HRG-1 proteins. Nature. 2008;453(7198):1127-1131.
70. Korolnek T, Hamza I. Like iron in the blood of the people: the requirement for heme trafficking in iron metabolism. Front Pharmacol. 2014;5:126.
71. Rao AU, Carta LK, Lesuisse E, Hamza I. Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci USA. 2005;102(12):4270-4275.
72. Korolnek T, Zhang J, Beardsley S, Scheffer GL, Hamza I. Control of metazoan heme homeostasis by a conserved multidrug resistance protein. Cell Metab. 2014;19(6):1008-1019.
73. Kohyama M, Ise W, Edelson BT, et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature. 2009;457(7227):318-321.
74. Haldar M, Kohyama M, So AY, et al. Hememediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell. 2014;156(6):1223-1234.