Binding and uptake of H-ferritin are mediated by human transferrin receptor-1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 8, 2010, Pages 3505-3510

  Li, Li ^a   Fang, Celia J ^a,b   Ryan, James C ^a,b   Niemi, Eréne C ^b   Lebrón, José A ^c,f   Björkman, Pamela J ^c   Arase, Hisashi ^d   Torti, Frank M ^e   Torti, Suzy V ^e   Nakamura, Mary C ^a,b   Seaman, William E ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d OSAKA UNIVERSITY   (Japan)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

^f MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Endocytosis; Ferritin; HFE; Iron; Receptors

Indexed keywords

CD71 ANTIGEN; FERRITIN; H FERRITIN; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CELL LINE; CELL SURFACE; CELL TYPE; ENDOCYTOSIS; ENDOSOME; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; LYSOSOME; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; RETICULOCYTE; T LYMPHOCYTE;

ANTIGENS, CD; APOFERRITINS; B-LYMPHOCYTES; CELL LINE; CLONING, MOLECULAR; ENDOSOMES; HUMANS; LYSOSOMES; PROTEIN BINDING; RECEPTORS, TRANSFERRIN; T-LYMPHOCYTES; TRANSFERRIN;

EID: 77649268711     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0913192107     Document Type: Article

References (43)

1. Theil EC (1987) Ferritin: Structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu Rev Biochem 56:289-315.
2. Ganz T (2008) Iron homeostasis: Fitting the puzzle pieces together. Cell Metab 7: 288-290.
3. MacKenzie EL, Iwasaki K, Tsuji Y (2008) Intracellular iron transport and storage: From molecular mechanisms to health implications. Antioxid Redox Signal 10:997-1030.
4. Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1-14.
5. Torti FM, Torti SV (2002) Regulation of ferritin genes and protein. Blood 99: 3505-3516.
6. Arosio P, Levi S (2002) Ferritin, iron homeostasis, and oxidative damage. Free Radic Biol Med 33:457-463.
7. Harrison PM, Arosio P (1996) The ferritins: Molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275:161-203.
8. Levi S, et al. (1988) Mechanism of ferritin iron uptake: Activity of the H-chain and deletion mapping of the ferro-oxidase site. A study of iron uptake and ferro-oxidase activity of human liver, recombinant H-chain ferritins, and of two H-chain deletion mutants. J Biol Chem 263:18086-18092.
9. Ford GC, et al. (1984) Ferritin: Design and formation of an iron-storage molecule. Philos Trans R Soc Lond B Biol Sci 304:551-565.
10. Liao QK, Kong PA, Gao J, Li FY, Qian ZM (2001) Expression of ferritin receptor in placental microvilli membrane in pregnant women with different iron status at midterm gestation. Eur J Clin Nutr 55:651-656.
11. Meyron-Holtz EG, Fibach E, Gelvan D, Konijn AM (1994) Binding and uptake of exogenous isoferritins by cultured human erythroid precursor cells. Br J Haematol 86: 635-641.
12. Fargion S, et al. (1988) Characteristics and expression of binding sites specific for ferritin H-chain on human cell lines. Blood 71:753-757.
13. Moss D, Powell LW, Arosio P, Halliday JW (1992) Characterization of the ferritin receptors of human T lymphoid (MOLT-4) cells. J Lab Clin Med 119:273-279.
14. Bretscher MS, Thomson JN (1983) Distribution of ferritin receptors and coated pits on giant HeLa cells. EMBO J 2:599-603.
15. Takami M, et al. (1986) Human placental ferritin receptor. Biochim Biophys Acta 884: 31-38.
16. Fargion S, et al. (1991) Specific binding sites for H-ferritin on human lymphocytes: Modulation during cellular proliferation and potential implication in cell growth control. Blood 78:1056-1061.
17. Moss D, et al. (1992) Functional roles of the ferritin receptors of human liver, hepatoma, lymphoid and erythroid cells. J Inorg Biochem 47:219-227.
18. Gelvan D, Fibach E, Meyron-Holtz EG, Konijn AM (1996) Ferritin uptake by human erythroid precursors is a regulated iron uptake pathway. Blood 88:3200-3207.
19. Leimberg MJ, Prus E, Konijn AM, Fibach E (2008) Macrophages function as a ferritin iron source for cultured human erythroid precursors. J Cell Biochem 103:1211-1218.
20. Leimberg JM, Konijn AM, Fibach E (2003) Developing human erythroid cells grown in transferrin-free medium utilize iron originating from extracellular ferritin. Am J Hematol 73:211-212.
21. Chen TT, et al. (2005) TIM-2 is expressed on B cells and in liver and kidney and is a receptor for H-ferritin endocytosis. J Exp Med 202:955-965.
22. Todorich B, Zhang X, Slagle-Webb B, Seaman WE, Connor JR (2008) Tim-2 is the receptor for H-ferritin on oligodendrocytes. J Neurochem 107:1495-1505.
23. Kuchroo VK, Umetsu DT, DeKruyff RH, Freeman GJ (2003) The TIM gene family: Emerging roles in immunity and disease. Nat Rev Immunol 3:454-462.
24. McGraw TE, Greenfield L, Maxfield FR (1987) Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J Cell Biol 105:207-214.
25. Lebrón JA (1999) Biochemical and biophysical characterization of the hemochromatosis protein HFE and its interaction with the transferrin receptor. PhD thesis (California Institute of Technology, Pasadena, CA).
26. Giannetti AM, Björkman PJ (2004) HFE and transferrin directly compete for transferrin receptor in solution and at the cell surface. J Biol Chem 279:25866-25875.
27. Mattia E, Rao K, Shapiro DS, Sussman HH, Klausner RD (1984) Biosynthetic regulation of the human transferrin receptor by desferrioxamine in K562 cells. J Biol Chem 259: 2689-2692.
28. Meyron-Holtz EG, et al. (1999) Regulation of intracellular iron metabolism in human erythroid precursors by internalized extracellular ferritin. Blood 94:3205-3211.
29. Vaisman B, Fibach E, Konijn AM (1997) Utilization of intracellular ferritin iron for hemoglobin synthesis in developing human erythroid precursors. Blood 90:831-838.
30. Kidane TZ, Sauble E, Linder MC (2006) Release of iron from ferritin requires lysosomal activity. Am J Physiol Cell Physiol 291:C445-C455.
31. De Domenico I, Ward DM, Kaplan J (2009) Specific iron chelators determine the route of ferritin degradation. Blood 12:4546-4551.
32. Kwok JC, Richardson DR (2004) Examination of the mechanism(s) involved in doxorubicin-mediated iron accumulation in ferritin: Studies using metabolic inhibitors, protein synthesis inhibitors, and lysosomotropic agents. Mol Pharmacol 65:181-195.
33. Tsunoo H, Sussman HH (1983) Characterization of transferrin binding and specificity of the placental transferrin receptor. Arch Biochem Biophys 225:42-54.
34. Feder JN, et al. (1998) The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc Natl Acad Sci USA 95:1472-1477.
35. Li JY, et al. (2009) Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev Cell 16:35-46.
36. Jiang Y, Oliver P, Davies KE, Platt N (2006) Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem 281:11834-11845.
37. Li R, Luo C, Mines M, Zhang J, Fan GH (2006) Chemokine CXCL12 induces binding of ferritin heavy chain to the chemokine receptor CXCR4, alters CXCR4 signaling, and induces phosphorylation and nuclear translocation of ferritin heavy chain. J Biol Chem 281:37616-37627.
38. Pham CG, et al. (2004) Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 119:529-542.
39. Ohgami RS, et al. (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat Genet 37:1264-1269.
40. Sendamarai AK, Ohgami RS, Fleming MD, Lawrence CM (2008) Structure of the membrane proximal oxidoreductase domain of human Steap3, the dominant ferrireductase of the erythroid transferrin cycle. Proc Natl Acad Sci USA 105: 7410-7415.
41. Arase H, Saito T, Phillips JH, Lanier LL (2001) Cutting edge: The mouse NK cell-associated antigen recognized by DX5 monoclonal antibody is CD49b (alpha 2 integrin, very late antigen-2). J Immunol 167:1141-1144.
42. Rucker P, Torti FM, Torti SV (1997) Recombinant ferritin: Modulation of subunit stoichiometry in bacterial expression systems. Protein Eng 10:967-973.
43. Lebrón JA, et al. (1998) Crystal structure of the hemochromatosis protein HFE and characterization of its interaction with transferrin receptor. Cell 93:111-123.