The transferrin receptor: The cellular iron gate

Metallomics

Volumn 9, Issue 10, 2017, Pages 1367-1375

  Gammella, Elena ^a   Buratti, Paolo ^a   Cairo, Gaetano ^a   Recalcati, Stefania ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CELL PROLIFERATION; MOLECULAR BIOLOGY;

CELLULAR IRONS; CLATHRIN-DEPENDENT ENDOCYTOSIS; IRON HOMEOSTASIS; MOLECULAR REGULATION; MULTIPLE LEVELS; PROLIFERATING CELLS; RATE-LIMITING STEPS; TRANSFERRIN RECEPTORS;

IRON;

CD71 ANTIGEN; CLATHRIN; IRON; IRON REGULATORY FACTOR; TRANSFERRIN RECEPTOR; TRANSFERRIN RECEPTOR 2; TRANSFERRIN;

CELL GROWTH; CELL PROLIFERATION; CELL SURFACE; ENDOCYTOSIS; ENDOSOME; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; HOMEOSTASIS; IRON HOMEOSTASIS; IRON METABOLISM; IRON OVERLOAD; IRON RESPONSIVE ELEMENT; IRON STORAGE; IRON TRANSPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REVIEW; TISSUE SPECIFICITY; ANIMAL; HUMAN; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; ENDOCYTOSIS; HOMEOSTASIS; HUMANS; IRON; RECEPTORS, TRANSFERRIN; TRANSFERRIN;

EID: 85029859796     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c7mt00143f     Document Type: Review

References (88)

1. V. D. Paul R. Lill Biogenesis of cytosolic and nuclear iron-sulfur proteins and their role in genome stability Biochim. Biophys. Acta. 2015 1853 1528 1539
2. R. Gozzelino P. Arosio The importance of iron in pathophysiologic conditions Front. Pharmacol. 2015 6 26
3. D. L. Zhang M. C. Ghosh T. A. Rouault The physiological functions of iron regulatory proteins in iron homeostasis-an update Front. Pharmacol. 2014 5 124
4. G. Cairo F. Bernuzzi S. Recalcati A precious metal: Iron, an essential nutrient for all cells Genes Nutr. 2006 1 25 39
5. V. G. Sankaran M. J. Weiss Anemia: progress in molecular mechanisms and therapies Nat. Med. 2015 21 221 230
6. R. Gozzelino M. P. Soares Coupling heme and iron metabolism via ferritin H chain Antioxid Redox Signal 2014 20 1754 1769
7. A. Pietrangelo Hereditary hemochromatosis: pathogenesis, diagnosis, and treatment Gastroenterology 2010 139 393 408
8. L. W. Powell R. C. Seckington Y. Deugnier Haemochromatosis Lancet 2016 388 706 716
9. M. U. Muckenthaler S. Rivella M. W. Hentze B. Galy A Red Carpet for Iron Metabolism Cell 2017 168 344 361
10. N. C. Andrews P. J. Schmidt Iron homeostasis Annu. Rev. Physiol. 2007 69 69 85
11. I. De Domenico D. McVey Ward J. Kaplan Regulation of iron acquisition and storage: consequences for iron-linked disorders Nat. Rev. Mol. Cell Biol. 2008 9 72 81
12. T. Ganz Hepcidin and iron regulation, 10 years later Blood 2011 117 4425 4433
13. M. W. Hentze M. U. Muckenthaler B. Galy C. Camaschella Two to tango: regulation of Mammalian iron metabolism Cell 2010 142 24 38
14. P. Ponka C. N. Lok The transferrin receptor: role in health and disease Int. J. Biochem. Cell Biol. 1999 31 1111 1137
15. J. Wang K. Pantopoulos Regulation of cellular iron metabolism Biochem. J. 2011 434 365 381
16. L. Li C. J. Fang J. C. Ryan E. C. Niemi J. A. Lebrón P. J. Björkman H. Arase F. M. Torti S. V. Torti M. C. Nakamura W. E. Seaman Binding and uptake of H-ferritin are mediated by human transferrin receptor-1 Proc. Natl. Acad. Sci. U. S. A. 2010 107 3505 3510
17. Z. I. Cabantchik Labile iron in cells and body fluids: physiology, pathology, and pharmacology Front. Pharmacol. 2014 5 45
18. C. M. Lawrence S. Ray M. Babyonyshev R. Galluser D. W. Borhani S. C. Harrison Crystal structure of the ectodomain of human transferrin receptor Science 1999 286 779 782
19. M. J. Bennett J. A. Lebrón P. J. Bjorkman Crystal structure of the hereditary haemochromatosis protein HFE complexed with transferrin receptor Nature 2000 403 46 53
20. Y. Cheng O. Zak P. Aisen S. C. Harrison T. Walz Structure of the human transferrin receptor-transferrin complex Cell 2004 116 565 576
21. G. Papanikolaou K. Pantopoulos Systemic iron homeostasis and erythropoiesis IUBMB Life 2017 69 399 413
22. K. Gkouvatsos G. Papanikolaou K. Pantopoulos Regulation of iron transport and the role of transferrin Biochim. Biophys. Acta. 2012 1820 188 202
23. J. P. Liuzzi F. Aydemir H. Nam M. D. Knutson R. J. Cousins Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells Proc. Natl. Acad. Sci. U. S. A. 2006 103 13612 13617
24. S. Jenkitkasemwong C. Y. Wang R. Coffey W. Zhang A. Chan T. Biel J. S. Kim S. Hojyo T. Fukada M. D. Knutson SLC39A14 Is Required for the Development of Hepatocellular Iron Overload in Murine Models of Hereditary Hemochromatosis Cell Metab. 2015 22 138 150
25. M. U. Muckenthaler B. Galy M. W. Hentze Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network Annu. Rev. Nutr. 2008 28 197 213
26. S. Recalcati G. Minotti G. Cairo Iron regulatory proteins: from molecular mechanisms to drug development Antioxid Redox Signal 2010 13 1593 1616
27. E. W. Müllner L. C. Kühn A stem-loop in the 3′ untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm Cell 1988 53 815 825
28. M. Yoshinaga Y. Nakatsuka A. Vandenbon D. Ori T. Uehata T. Tsujimura Y. Suzuki T. Mino O. Takeuchi Regnase-1 Maintains Iron Homeostasis via the Degradation of Transferrin Receptor 1 and Prolyl-Hydroxylase-Domain-Containing Protein 3 mRNAs Cell Rep. 2017 19 1614 1630
29. G. Cairo S. Recalcati Iron-regulatory proteins: molecular biology and pathophysiological implications Expert Rev. Mol. Med. 2007 9 1 13
30. M. Bayeva A. Khechaduri S. Puig H. C. Chang S. Patial P. J. Blackshear H. Ardehali mTOR regulates cellular iron homeostasis through tristetraprolin Cell Metab. 2012 16 645 657
31. S. Patial D. J. Stumpo W. S. Young J. M. Ward G. P. Flake P. J. Blackshear Effects of Combined Tristetraprolin/Tumor Necrosis Factor Receptor Deficiency on the Splenic Transcriptome Mol. Cell Biol. 2016 36 1395 1411
32. Z. A. Knight S. F. Schmidt K. Birsoy K. Tan J. M. Friedman A critical role for mTORC1 in erythropoiesis and anemia Elife 2014 3 e01913
33. C. Truillet J. T. Cunningham M. F. Parker L. T. Huynh C. S. Conn D. Ruggero J. S. Lewis M. J. Evans Noninvasive Measurement of mTORC1 Signaling with (89)Zr-Transferrin Clin. Cancer Res. 2017 23 3045 3052
34. M. Laplante D. M. Sabatini mTOR signaling in growth control and disease Cell 2012 149 274 293
35. M. Bayeva H. C. Chang R. Wu H. Ardehali When less is more: novel mechanisms of iron conservation Trends Endocrinol. Metab. 2013 24 569 577
36. M. Castoldi M. U. Muckenthaler Regulation of iron homeostasis by microRNAs Cell Mol. Life Sci. 2012 69 3945 3952
37. D. G. Schaar D. J. Medina D. F. Moore R. K. Strair Y. Ting miR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation Exp. Hematol. 2009 37 245 255
38. I. Kindrat V. Tryndyak A. de Conti S. Shpyleva T. K. Mudalige T. Kobets A. M. Erstenyuk F. A. Beland I. P. Pogribny MicroRNA-152-mediated dysregulation of hepatic transferrin receptor 1 in liver carcinogenesis Oncotarget 2016 7 1276 1287
39. L. Tacchini L. Bianchi A. Bernelli-Zazzera G. Cairo Transferrin receptor induction by hypoxia. HIF-1-mediated transcriptional activation and cell-specific post-transcriptional regulation J. Biol. Chem. 1999 274 24142 24146
40. C. N. Lok P. Ponka Identification of a hypoxia response element in the transferrin receptor gene J. Biol. Chem. 1999 274 24147 24152
41. S. Recalcati E. Gammella G. Cairo New perspectives on the molecular basis of the interaction between oxygen homeostasis and iron metabolism Hypoxia (Auckl) 2015 3 93 103
42. R. J. Simpson A. T. McKie Iron and oxygen sensing: a tale of 2 interacting elements? Metallomics 2015 7 223 231
43. L. Bianchi L. Tacchini G. Cairo HIF-1-mediated activation of transferrin receptor gene transcription by iron chelation Nucleic Acids Res. 1999 27 4223 4227
44. L. Tacchini D. Fusar Poli A. Bernelli-Zazzera G. Cairo Transferrin receptor gene expression and transferrin-bound iron uptake are increased during postischemic rat liver reperfusion Hepatology 2002 36 103 111
45. K. A. O'Donnell D. Yu K. I. Zeller J. W. Kim F. Racke A. Thomas-Tikhonenko C. V. Dang Activation of transferrin receptor 1 by c-Myc enhances cellular proliferation and tumorigenesis Mol. Cell. Biol. 2006 26 2373 2386
46. K. J. Wu A. Polack R. Dalla-Favera Coordinated regulation of iron-controlling genes, H-ferritin and IRP2, by c-MYC Science 1999 283 676 679
47. B. Ning G. Liu Y. Liu X. Su G. J. Anderson X. Zheng Y. Chang M. Guo Y. Zhao G. Nie 5-aza-2′-deoxycytidine activates iron uptake and heme biosynthesis by increasing c-Myc nuclear localization and binding to the E-boxes of transferrin receptor 1 (TfR1) and ferrochelatase (Fech) genes J. Biol. Chem. 2011 286 37196 37206
48. B. M. Zhu S. K. McLaughlin R. Na J. Liu Y. Cui C. Martin A. Kimura G. W. Robinson N. C. Andrews L. Hennighausen Hematopoietic-specific Stat5-null mice display microcytic hypochromic anemia associated with reduced transferrin receptor gene expression Blood 2008 112 2071 2080
49. M. A. Kerenyi F. Grebien H. Gehart M. Schifrer M. Artaker B. Kovacic H. Beug R. Moriggl E. W. Müllner Stat5 regulates cellular iron uptake of erythroid cells via IRP-2 and TfR-1 Blood 2008 112 3878 3888
50. F. Okazaki N. Matsunaga H. Okazaki H. Azuma K. Hamamura A. Tsuruta Y. Tsurudome T. Ogino Y. Hara T. Suzuki K. Hyodo H. Ishihara H. Kikuchi H. To H. Aramaki S. Koyanagi S. Ohdo Circadian Clock in a Mouse Colon Tumor Regulates Intracellular Iron Levels to Promote Tumor Progression J. Biol. Chem. 2016 291 7017 7028
51. E. Bourseau-Guilmain A. Griveau J. P. Benoit E. Garcion The importance of the stem cell marker prominin-1/CD133 in the uptake of transferrin and in iron metabolism in human colon cancer Caco-2 cells PLoS One 2011 6 e25515
52. H. Cao B. Schroeder J. Chen M. B. Schott M. A. McNiven The Endocytic Fate of the Transferrin Receptor Is Regulated by c-Abl Kinase J. Biol. Chem. 2016 291 16424 16437
53. B. Wang J. Zhang F. Song M. Tian B. Shi H. Jiang W. Xu H. Wang M. Zhou X. Pan J. Gu S. Yang L. Jiang Z. Li EGFR regulates iron homeostasis to promote cancer growth through redistribution of transferrin receptor 1 Cancer Lett. 2016 381 331 340
54. R. Beydoun M. A. Hamood D. M. Gomez Zubieta K. C. Kondapalli Na(+)/H(+) Exchanger 9 Regulates Iron Mobilization at the Blood-Brain Barrier in Response to Iron Starvation J. Biol. Chem. 2017 292 4293 4301
55. R. Tachiyama D. Ishikawa M. Matsumoto K. I. Nakayama T. Yoshimori S. Yokota M. Himeno Y. Tanaka H. Fujita Proteome of ubiquitin/MVB pathway: possible involvement of iron-induced ubiquitylation of transferrin receptor in lysosomal degradation Genes Cells 2011 16 448 466
56. H. Fujita Y. Iwabu K. Tokunaga Y. Tanaka Membrane-associated RING-CH (MARCH) 8 mediates the ubiquitination and lysosomal degradation of the transferrin receptor J. Cell Sci. 2013 126 2798 2809
57. H. Li T. Choesang W. Bao H. Chen M. Feola D. Garcia-Santos J. Li S. Sun A. Follenzi P. Pham J. Liu J. Zhang P. Ponka X. An N. Mohandas R. E. Fleming S. Rivella G. Li Y. Z. Ginzburg Decreasing TfR1 expression reverses anemia and hepcidin suppression in β-thalassemic mice Blood 2017 129 1514 1526
58. G. Cairo A. Pietrangelo Transferrin receptor gene expression during rat liver regeneration. Evidence for post-transcriptional regulation by iron regulatory factorB, a second iron-responsive element-binding protein J. Biol. Chem. 1994 269 6405 6409
59. Y. Yu Z. Kovacevic D. R. Richardson Tuning cell cycle regulation with an iron key Cell Cycle 2007 6 1982 1994
60. T. R. Daniels T. Delgado J. A. Rodriguez G. Helguera M. L. Penichet The transferrin receptor part I: Biology and targeting with cytotoxic antibodies for the treatment of cancer Clin. Immunol. 2006 121 144 158
61. A. C. Chen A. Donovan R. Ned-Sykes N. C. Andrews Noncanonical role of transferrin receptor 1 is essential for intestinal homeostasis Proc. Natl. Acad. Sci. U. S. A. 2015 112 11714 11719
62. H. Drakesmith A. Prentice Viral infection and iron metabolism Nat. Rev. Microbiol. 2008 6 541 552
63. S. R. Radoshitzky J. Abraham C. F. Spiropoulou J. H. Kuhn D. Nguyen W. Li J. Nagel P. J. Schmidt J. H. Nunberg N. C. Andrews M. Farzan H. Choe Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses Nature 2007 446 92 96
64. J. S. Parker W. J. Murphy D. Wang S. J. O'Brien C. R. Parrish Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells J. Virol. 2001 75 3896 3902
65. S. R. Ross J. J. Schofield C. J. Farr M. Bucan Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus Proc. Natl. Acad. Sci. U. S. A. 2002 99 12386 12390
66. D. N. Martin S. L. Uprichard Identification of transferrin receptor 1 as a hepatitis C virus entry factor Proc. Natl. Acad. Sci. U. S. A. 2013 110 10777 10782
67. G. Y. Lui Z. Kovacevic V. Richardson A. M. Merlot D. S. Kalinowski D. R. Richardson Targeting cancer by binding iron: dissecting cellular signaling pathways Oncotarget 2015 6 18748 18779
68. J. R. Tejedor P. Papasaikas J. Valcárcel Genome-wide identification of Fas/CD95 alternative splicing regulators reveals links with iron homeostasis Mol. Cell 2015 57 23 38
69. J. D. Mancias L. Pontano Vaites S. Nissim D. E. Biancur A. J. Kim X. Wang Y. Liu W. Goessling A. C. Kimmelman J. W. Harper Ferritinophagy via NCOA4 is required for erythropoiesis and is regulated by iron dependent HERC2-mediated proteolysis Elife 2015 4
70. R. Bellelli G. Federico A. Matte D. Colecchia A. Iolascon M. Chiariello M. Santoro L. De Franceschi F. Carlomagno NCOA4 Deficiency Impairs Systemic Iron Homeostasis Cell Rep. 2016 14 411 421
71. S. V. Torti F. M. Torti Iron and cancer: more ore to be mined Nat. Rev. Cancer 2013 13 342 355
72. S. Radulescu M. J. Brookes P. Salgueiro R. A. Ridgway E. McGhee K. Anderson S. J. Ford D. H. Stones T. H. Iqbal C. Tselepis O. J. Sansom Luminal iron levels govern intestinal tumorigenesis after Apc loss in vivo Cell Rep. 2012 2 270 282
73. A. Alberghini S. Recalcati L. Tacchini P. Santambrogio A. Campanella G. Cairo Loss of the von Hippel Lindau tumor suppressor disrupts iron homeostasis in renal carcinoma cells J. Biol. Chem. 2005 280 30120 30128
74. R. Taetle J. Castagnola J. Mendelsohn Mechanisms of growth inhibition by anti-transferrin receptor monoclonal antibodies Cancer Res. 1986 46 1759 1763
75. R. Crépin A. L. Goenaga B. Jullienne H. Bougherara C. Legay K. Benihoud J. D. Marks M. A. Poul Development of human single-chain antibodies to the transferrin receptor that effectively antagonize the growth of leukemias and lymphomas Cancer Res. 2010 70 5497 5506
76. T. R. Daniels T. Delgado G. Helguera M. L. Penichet The transferrin receptor part II: targeted delivery of therapeutic agents into cancer cells Clin. Immunol. 2006 121 159 176
77. J. E. Levy O. Jin Y. Fujiwara F. Kuo N. C. Andrews Transferrin receptor is necessary for development of erythrocytes and the nervous system Nat. Genet. 1999 21 396 399
78. H. H. Jabara S. E. Boyden J. Chou N. Ramesh M. J. Massaad H. Benson W. Bainter D. Fraulino F. Rahimov C. Sieff Z. J. Liu S. H. Alshemmari B. K. Al-Ramadi H. Al-Dhekri R. Arnaout M. Abu-Shukair A. Vatsayan E. Silver S. Ahuja E. G. Davies M. Sola-Visner T. K. Ohsumi N. C. Andrews L. D. Notarangelo M. D. Fleming W. Al-Herz L. M. Kunkel R. S. Geha A missense mutation in TFRC, encoding transferrin receptor 1, causes combined immunodeficiency Nat. Genet. 2016 48 74 78
79. W. Xu T. Barrientos L. Mao H. A. Rockman A. A. Sauve N. C. Andrews Lethal Cardiomyopathy in Mice Lacking Transferrin Receptor in the Heart Cell Rep. 2015 13 533 545
80. T. Barrientos I. Laothamatas T. R. Koves E. J. Soderblom M. Bryan M. A. Moseley D. M. Muoio N. C. Andrews Metabolic Catastrophe in Mice Lacking Transferrin Receptor in Muscle EBioMedicine 2015 2 1705 1717
81. P. Matak A. Matak S. Moustafa D. K. Aryal E. J. Benner W. Wetsel N. C. Andrews Disrupted iron homeostasis causes dopaminergic neurodegeneration in mice Proc. Natl. Acad. Sci. U. S. A. 2016 113 3428 3435
82. T. A. Rouault Iron metabolism in the CNS: implications for neurodegenerative diseases Nat. Rev. Neurosci. 2013 14 551 564
83. D. Senyilmaz S. Virtue X. Xu C. Y. Tan J. L. Griffin A. K. Miller A. Vidal-Puig A. A. Teleman Regulation of mitochondrial morphology and function by stearoylation of TFR1 Nature 2015 525 124 128
84. C. Camaschella A. Pagani A. Nai L. Silvestri The mutual control of iron and erythropoiesis Int. J. Lab Hematol. 2016 38 suppl 1 20 26
85. A. Nai M. R. Lidonnici M. Rausa G. Mandelli A. Pagani L. Silvestri G. Ferrari C. Camaschella The second transferrin receptor regulates red blood cell production in mice Blood 2015 125 1170 1179
86. H. Kawabata T. Nakamaki P. Ikonomi R. D. Smith R. S. Germain H. P. Koeffler Expression of transferrin receptor 2 in normal and neoplastic hematopoietic cells Blood 2001 98 2714 2719
87. S. Matsuo M. Ogawa M. U. Muckenthaler Y. Mizui S. Sasaki T. Fujimura M. Takizawa N. Ariga H. Ozaki M. Sakaguchi F. J. Gonzalez Y. Inoue Hepatocyte Nuclear Factor 4α Controls Iron Metabolism and Regulates Transferrin Receptor 2 in Mouse Liver J. Biol. Chem. 2015 290 30855 30865
88. J. Chen J. Wang K. R. Meyers C. A. Enns Transferrin-directed internalization and cycling of transferrin receptor 2 Traffic 2009 10 1488 1501