Crossing the iron gate: Why and how transferrin receptors mediate viral entry

Annual Review of Nutrition

Volumn 38, Issue , 2018, Pages 431-458

  Wessling Resnick, Marianne ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

infection; innate immunity; iron; mTOR; receptor mediated endocytosis

Indexed keywords

CD71 ANTIGEN; IRON; TRANSFERRIN; TRANSFERRIN RECEPTOR; TRANSFERRIN RECEPTOR 2;

ALPHAVIRUS; CANINE PARVOVIRUS; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; FELINE PANLEUKOPENIA VIRUS; GENE THERAPY; HEPATITIS C VIRUS; HUMAN; HUMAN ADENOVIRUS C; IRON DEFICIENCY; IRON HOMEOSTASIS; IRON OVERLOAD; MINK ENTERITIS VIRUS; MOUSE MAMMARY TUMOR VIRUS; NEW WORLD ARENAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECYCLING; REVIEW; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES DIFFERENCE; VIRUS ENTRY; VIRUS INFECTION; ANIMAL; INNATE IMMUNITY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; HUMANS; IMMUNITY, INNATE; IRON; RECEPTORS, TRANSFERRIN; TRANSFERRIN; VIRUS INTERNALIZATION;

EID: 85052241847     PISSN: 01999885     EISSN: 15454312     Source Type: Book Series    
DOI: 10.1146/annurev-nutr-082117-051749     Document Type: Review

References (180)

1. Abraham J,Corbett KD, Farzan M, Choe H, Harrison SC. 2010. Structural basis for receptor recognition by NewWorld hemorrhagic fever arenaviruses. Nat. Struct. Mol. Biol. 17:438-44
2. Ajioka RS, Kaplan J. 1986. Intracellular pools of transferrin receptors result from constitutive internalization of unoccupied receptors. PNAS 83:6445-49
3. AlkhouriN, Lawitz E, Poordad F. 2017. Novel treatments for chronic hepatitis C: closing the remaining gaps. Curr. Opin. Pharmacol. 37:107-11
4. Andrews NC. 2008. Forging a field: the golden age of iron biology. Blood 112:219-30
5. Armitage AE, StaceyAR, Giannoulatou E, Marshall E, Sturges P, et al. 2014. Distinct patterns of hepcidin and iron regulation during HIV-1, HBV, and HCV infections. PNAS 111:12187-92
6. Asano T, KomatsuM, Yamaguchi-Iwai Y, Ishikawa F,MizushimaN, Iwai K. 2011. Distinct mechanisms of ferritin delivery to lysosomes in iron-depleted and iron-replete cells. Mol. Cell. Biol. 31:2040-52
7. Babitt JL, Huang FW, WrightingDM, Xia Y, Sidis Y, et al. 2006. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat. Genet. 38:531-39
8. Barrientos T, Laothamatas I, Koves TR, Soderblom EJ, Bryan M, et al. 2015. Metabolic catastrophe in mice lacking transferrin receptor in muscle. EBioMedicine 2:1705-17
9. Bartnikas TB. 2012. Known and potential roles of transferrin in iron biology. BioMetals 25:677-86
10. Batista A, Millan J, Mittelbrunn M, Sanchez-Madrid F, Alonso MA. 2004. Recruitment of transferrin receptor to immunological synapse in response to TCR engagement. J. Immunol. 172:6709-14
11. Bayeva M, Khechaduri A, Puig S, Chang HC, Patial S, et al. 2012. mTOR regulates cellular iron homeostasis through tristetraprolin. Cell Metab. 16:645-57
12. Beck MA. 2007. Selenium and Vitamin E status: impact on viral pathogenicity. J. Nutr. 137:1338-40
13. Beck MA, Handy J, Levander OA. 2004. Host nutritional status: the neglected virulence factor. Trends Microbiol. 12:417-23
14. Bellelli R, Federico G, Matte A, Colecchia D, Iolascon A, et al. 2016.NCOA4deficiency impairs systemic iron homeostasis. Cell Rep. 14:411-21
15. Boshuizen M, van der Ploeg K, von Bonsdorff L, Biemond BJ, Zeerleder SS, et al. 2017. Therapeutic use of transferrin to modulate anemia and conditions of iron toxicity. Blood Rev. 31:400-5
16. Bowden TA,Crispin M, Graham SC,Harvey DJ, Grimes JM, et al. 2009. Unusualmolecular architecture of the Machupo virus attachment glycoprotein. J. Virol. 83:8259-65
17. Buchkovich NJ, Yu Y, Zampieri CA, Alwine JC. 2008. The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K-Akt-mTOR signalling pathway. Nat. Rev. Microbiol. 6:266-75
18. Byrne SL, Buckett PD, Kim J, Luo F, Sanford J, et al. 2013. Ferristatin II promotes degradation of transferrin receptor-1 in vitro and in vivo. PLOS ONE 8:e70199
19. Camaschella C. 2015. Iron-deficiency anemia. N. Engl. J. Med. 373:485-86
20. Camaschella C, Roetto A, Cali A, Gobbi M Garozzo G, et al. 2000. The gene TFR2 is mutated in a new type of haemochromatosis mapping to 7q22. Nat. Genet. 25:14-15
21. Cao H, Chen J, Krueger EW, McNiven MA. 2010. Src-mediated phosphorylation of dynamin and cortactin regulates the "constitutive" endocytosis of transferrin. Mol. Cell. Biol. 30:781-92
22. Castilla V, Mersich SE. 1996. Low-pH-induced fusion of Vero cells infected with Junin virus. Arch. Virol. 141:1307-17
23. Chen AC, Donovan A, Ned-Sykes R, Andrews NC. 2015. Noncanonical role of transferrin receptor 1 is essential for intestinal homeostasis. PNAS 112:11714-19
24. Chen C, Garcia-Santos D, Ishikawa Y, Seguin A, Li L, et al. 2013. Snx3 regulates recycling of the transferrin receptor and iron assimilation. Cell Metab. 17:343-52
25. Chen J, ChloupkovaM, Gao J, Chapman-Arvedson TL, Enns CA. 2007. HFE modulates transferrin receptor 2 levels in hepatoma cells via interactions that differ from transferrin receptor 1-HFE interactions. J. Biol. Chem. 282:36862-70
26. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. 1999. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621-25
27. Chua AC, Herbison CE, Drake SF, Graham RM, Olynyk JK, Trinder D. 2008. The role of Hfe in transferrin-bound iron uptake by hepatocytes. Hepatology 47:1737-44
28. Coffin JM. 2013. Virions at the gates: receptors and the host-virus arms race. PLOS Biol. 11:e1001574
29. Collawn JF, Lai A, Domingo D, Fitch M, Hatton S, Trowbridge IS. 1993. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis. J. Biol. Chem. 268:21686-92
30. Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422:37-44
31. Cullen PJ. 2008. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat. Rev. Mol. Cell Biol. 9:574-82
32. Cureton DK, Harbison CE, Cocucci E, Parrish CR, Kirchhausen T. 2012. Limited transferrin receptor clustering allows rapid diffusion of canine parvovirus into clathrin endocytic structures. J. Virol. 86:5330-40
33. D'Alessio F, Hentze MW, Muckenthaler MU. 2012. The hemochromatosis proteins HFE, TfR2, and HJV form a membrane-associated protein complex for hepcidin regulation. J. Hepatol. 57:1052-60
34. Dale JC, Burritt MF, Zinsmeister AR. 2002. Diurnal variation of serum iron, iron-binding capacity, transferrin saturation, and ferritin levels. Am. J. Clin. Pathol. 117:802-8
35. Dauner K, Eid W, Raghupathy R, Presley JF, Zha X. 2017. mTOR complex 1 activity is required to maintain the canonical endocytic recycling pathway against lysosomal delivery. J. Biol. Chem. 292:5737-47
36. Dautry-Varsat A, Ciechanover A, Lodish HF. 1983. pH and the recycling of transferrin during receptormediated endocytosis. PNAS 80:2258-62
37. Demogines A, Abraham J, Choe H, Farzan M, Sawyer SL. 2013. Dual host-virus arms races shape an essential housekeeping protein. PLOS Biol. 11:e1001571
38. Bisceglie AM, Axiotis CA, Hoofnagle JH, Bacon BR. 1992. Measurements of iron status in patients with chronic hepatitis. Gastroenterology 102:2108-13
39. Paolo G, Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-57
40. Dibble CC, Manning BD. 2013. Signal integration bymTORC1 coordinates nutrient input with biosynthetic output. Nat. Cell Biol. 15:555-64
41. DowdleWE,Nyfeler B, Nagel J,EllingRA, Liu S, et al. 2014. SelectiveVPS34 inhibitor blocks autophagy and uncovers a role for NCOA4 in ferritin degradation and iron homeostasis in vivo. Nat. Cell Biol. 16:1069-79
42. Drakesmith H, Chen N, Ledermann H, Screaton G, Townsend A, Xu XN. 2005. HIV-1 Nef downregulates the hemochromatosis proteinHFE,manipulating cellular iron homeostasis. PNAS 102:11017-22
43. Drakesmith H, Prentice AM. 2012. Hepcidin and the iron-infection axis. Science 338:768-72
44. Eckenroth BE, Steere AN, Chasteen ND, Everse SJ, Mason AB. 2011. How the binding of human transferrin primes the transferrin receptor potentiating iron release at endosomal pH. PNAS 108:13089-94
45. Eggers CT, Schafer JC, Goldenring JR, Taylor SS. 2009. D-AKAP2 interacts with Rab4 and Rab11 through its RGS domains and regulates transferrin receptor recycling. J. Biol. Chem. 284:32869-80
46. Ehrlich M, BollW,Van Oijen A,Hariharan R, Chandran K, et al. 2004. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591-605
47. Ekiz C, Agaoglu L, Karakas Z, Gurel N, Yalcin I. 2005. The effect of iron deficiency anemia on the function of the immune system. Hematol. J. 5:579-83
48. Farci P, Shimoda A, Coiana A,Diaz G, PeddisG, et al. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339-44
49. Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, et al. 1996. A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat. Genet. 13:399-408
50. Fillebeen C, Pantopoulos K. 2013. Hepatitis C virus infection causes iron deficiency in Huh7.5.1 cells. PLOS ONE 8:e83307
51. Fleming RE, Ahmann JR,Migas MC,Waheed A, Koeffler HP, et al. 2002. Targeted mutagenesis of the murine transferrin receptor-2 gene produces hemochromatosis. PNAS 99:10653-58
52. Foster JL, Garcia JV. 2008. HIV-1 Nef: at the crossroads. Retrovirology 5:84
53. Frazer DM, Anderson GJ. 2014. The regulation of iron transport. BioFactors 40:206-14
54. Freeze HH. 2013. Understanding human glycosylation disorders: Biochemistry leads the charge. J. Biol. Chem. 288:6936-45
55. Fujita H, Iwabu Y, Tokunaga K, Tanaka Y. 2013. Membrane-associated RING-CH (MARCH) 8 mediates the ubiquitination and lysosomal degradation of the transferrin receptor. J. Cell Sci. 126:2798-809
56. Fujita N, Sugimoto R, Takeo M, Urawa N, Mifuji R, et al. 2007. Hepcidin expression in the liver: relatively low level in patients with chronic hepatitis C. Mol. Med. 13:97-104
57. Fujita N, Sugimoto R, Urawa N, Araki J, Mifuji R, et al. 2007. Hepatic iron accumulation is associated with disease progression and resistance to interferon/ribavirin combination therapy in chronic hepatitis C. J. Gastroenterol. Hepatol. 22:1886-93
58. Fujita N, Takei Y. 2007. Iron, hepatitis C virus, and hepatocellular carcinoma: Iron reduction preaches the gospel for chronic hepatitis C. J. Gastroenterol. 42:923-26
59. Galvez T, TeruelMN, HeoWD, Jones JT, Kim ML, et al. 2007. siRNA screen of the human signaling proteome identifies the PtdIns(3,4,5)P3-mTOR signaling pathway as a primary regulator of transferrin uptake. Genome Biol. 8:R142
60. Ganz T. 2013. Systemic iron homeostasis. Physiol. Rev. 93:1721-41
61. Gao J, Chen J, Kramer M, Tsukamoto H, Zhang AS, Enns CA. 2009. Interaction of the hereditary hemochromatosis protein HFE with transferrin receptor 2 is required for transferrin-induced hepcidin expression. Cell Metab. 9:217-27
62. Garrick MD,Garrick LM. 2007. Loss of rapid transferrin receptor recycling due to amutation in Sec15l1 in hbd mice. Biochim. Biophys. Acta 1773:105-8
63. Gaudin R, Kirchhausen T. 2015. Superinfection exclusion is absent during acute Junin virus infection of Vero and A549 cells. Sci. Rep. 5:15990
64. Giannetti AM, Bjorkman PJ. 2004. HFE and transferrin directly compete for transferrin receptor in solution and at the cell surface. J. Biol. Chem. 279:25866-75
65. Giannetti AM, Snow PM, Zak O, Bjorkman PJ. 2003. Mechanism for multiple ligand recognition by the human transferrin receptor. PLOS Biol. 1:e51
66. Girelli D, Trombini P, Busti F, CampostriniN, SandriM, et al. 2011. A time course of hepcidin response to iron challenge in patients with HFE and TFR2 hemochromatosis. Haematologica 96:500-6
67. Girones N, Davis RJ. 1989. Comparison of the kinetics of cycling of the transferrin receptor in the presence or absence of bound diferric transferrin. Biochem. J. 264:35-46
68. Gkouvatsos K, Papanikolaou G, Pantopoulos K. 2012. Regulation of iron transport and the role of transferrin. Biochim. Biophys. Acta 1820:188-202
69. Goodman LB, Lyi SM, Johnson NC, Cifuente JO, Hafenstein SL, Parrish CR. 2010. Binding site on the transferrin receptor for the parvovirus capsid and effects of altered affinity on cell uptake and infection. J. Virol. 84:4969-78
70. Goswami T, Andrews NC. 2006. Hereditary hemochromatosis protein, HFE, interaction with transferrin receptor 2 suggests a molecular mechanism for mammalian iron sensing. J. Biol. Chem. 281:28494-98
71. Guan P, Wang N. 2014. Mammalian target of rapamycin coordinates iron metabolism with iron-sulfur cluster assembly enzyme and tristetraprolin. Nutrition 30:968-74
72. Hafenstein S, Palermo LM, Kostyuchenko VA, Xiao C, Morais MC, et al. 2007. Asymmetric binding of transferrin receptor to parvovirus capsids. PNAS 104:6585-89
73. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A, et al. 2009. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 41:1088-93
74. Helguera G, Jemielity S, Abraham J, Cordo SM, Martinez MG, et al. 2012. An antibody recognizing the apical domain of human transferrin receptor 1 efficiently inhibits the entry of allNewWorld hemorrhagic fever arenaviruses. J. Virol. 86:4024-28
75. Hentze MW, Muckenthaler MU, Andrews NC. 2004. Balancing acts: molecular control of mammalian iron metabolism. Cell 117:285-97
76. Horonchik L, Wessling-Resnick M. 2008. The small-molecule iron transport inhibitor ferristatin/ NSC306711 promotes degradation of the transferrin receptor. Chem. Biol. 15:647-53
77. Hueffer K, Parker JS, Weichert WS, Geisel RE, Sgro JY, Parrish CR. 2003. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J. Virol. 77:1718-26
78. Iacopetta BJ, Morgan EH, Yeoh GC. 1982. Transferrin receptors and iron uptake during erythroid cell development. Biochim. Biophys. Acta 687:204-10
79. Isanaka S, Mugusi F, Urassa W, Willett WC, Bosch RJ, et al. 2012. Iron deficiency and anemia predict mortality in patients with tuberculosis. J. Nutr. 142:350-57
80. Ishikawa Y,Maeda M, Pasham M, Aguet F, Tacheva-Grigorova SK, et al. 2015. Role of the clathrin adaptor PICALM in normal hematopoiesis and polycythemia vera pathophysiology. Haematologica 100:439-51
81. Jabara HH, Boyden SE, Chou J, Ramesh N, Massaad MJ, et al. 2016. A missense mutation in TFRC, encoding transferrin receptor 1, causes combined immunodeficiency. Nat. Genet. 48:74-78
82. Jain A, Chasoo G, Singh SK, Saxena AK, Jain SK. 2011. Transferrin-appended PEGylated nanoparticles for temozolomide delivery to brain: in vitro characterisation. J. Microencapsul. 28:21-28
83. Johannes L, Wunder C. 2011. Retrograde transport: Two (or more) roads diverged in an endosomal tree? Traffic 12:956-62
84. Johnson MB, Enns CA. 2004. Diferric transferrin regulates transferrin receptor 2 protein stability. Blood 104:4287-93
85. Joung I, Harber G, Gerecke KM, Carroll SL, Collawn JF, Engler JA. 2005. Improved gene delivery into neuroglial cells using a fiber-modified adenovirus vector. Biochem. Biophys. Res. Commun. 328:1182-87
86. Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB, et al. 2012. Evolutionary reconstructions of the transferrin receptor of caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLOS Pathog. 8:e1002666
87. Kaito M. 2007. Molecular mechanism of iron metabolism and overload in chronic hepatitis C. J. Gastroenterol. 42:96-99
88. KawabataH,TongX, KawanamiT,Wano Y,Hirose Y, et al. 2004. Analyses for binding of the transferrin family of proteins to the transferrin receptor. Br. J. Haematol. 127:464-73
89. Kawabata H, Yang R, Hirama T, Vuong PT, Kawano S, et al. 1999. Molecular cloning of transferrin receptor 2: a new member of the transferrin receptor-like family. J. Biol. Chem. 274:20826-32
90. Kenneth NS, Mudie S, Naron S, Rocha S. 2013. TfR1 interacts with the IKK complex and is involved in IKK-NF-kB signalling. Biochem. J. 449:275-84
91. Kielian M, Chanel-Vos C, Liao M. 2010. Alphavirus entry and membrane fusion. Viruses 2:796-825
92. Kirchhausen T, Owen D, Harrison SC. 2014. Molecular structure, function, and dynamics of clathrinmediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6:a016725
93. Klausner RD, Ashwell G, van Renswoude J, Harford JB, Bridges KR. 1983. Binding of apotransferrin to K562 cells: explanation of the transferrin cycle. PNAS 80:2263-66
94. Koppensteiner H, Hohne K, Gondim MV,Gobert FX,WidderM, et al. 2014. Lentiviral Nef suppresses iron uptake in a strain specific manner through inhibition of Transferrin endocytosis. Retrovirology 11:1
95. Kupka R, Msamanga GI, Mugusi F, Petraro P, Hunter DJ, Fawzi WW. 2007. Iron status is an important cause of anemia in HIV-infected Tanzanian women but is not related to accelerated HIV disease progression. J. Nutr. 137:2317-23
96. Lambert LA. 2012. Molecular evolution of the transferrin family and associated receptors. Biochim. Biophys. Acta 1820:244-55
97. Lawrence CM, Ray S, Babyonyshev M, Galluser R, Borhani DW, Harrison SC. 1999. Crystal structure of the ectodomain of human transferrin receptor. Science 286:779-82
98. Lei R, Zhang K, Liu K, Shao X, Ding Z, et al. 2016. Transferrin receptor facilitates TGF-βand BMP signaling activation to control craniofacial morphogenesis. Cell Death Dis. 7:e2282
99. Leverence R, Mason AB, Kaltashov IA. 2010. Noncanonical interactions between serum transferrin and transferrin receptor evaluated with electrospray ionization mass spectrometry. PNAS 107:8123-28
100. Levy JE, JinO, Fujiwara Y,Kuo F, AndrewsNC. 1999. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 21:396-99
101. Li L, Fang CJ, Ryan JC, Niemi EC, Lebron JA, et al. 2010. Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. PNAS 107:3505-10
102. Lim JE, Jin O, Bennett C, Morgan K, Wang F, et al. 2005. A mutation in Sec15l1 causes anemia in hemoglobin deficit (hbd) mice. Nat. Genet. 37:1270-73
103. Lucas M, Gershlick DC, VidaurrazagaA,Rojas AL, Bonifacino JS, Hierro A. 2016. Structural mechanism for cargo recognition by the retromer complex. Cell 167:1623-35
104. Luck AN, Mason AB. 2012. Transferrin-mediated cellular iron delivery. Curr. Top. Membr. 69:3-35
105. Luck AN, Mason AB. 2013. Structure and dynamics of drug carriers and their interaction with cellular receptors: focus on serum transferrin. Adv. Drug Deliv. Rev. 65:1012-19
106. Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC. 2014. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509:105-9
107. Martin DN, Uprichard SL. 2013. Identification of transferrin receptor 1 as a hepatitis C virus entry factor. PNAS 110:10777-82
108. Martys JL, Wjasow C, Gangi DM, Kielian MC, McGraw TE, Backer JM. 1996. Wortmannin-sensitive trafficking pathways in Chinese hamster ovary cells: differential effects on endocytosis and lysosomal sorting. J. Biol. Chem. 271:10953-62
109. Mason AL, Gilady SY, Mackey JR. 2011. Mouse mammary tumor virus in human breast cancer: red herring or smoking gun? Am. J. Pathol. 179:1588-90
110. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5:121-32
111. Maxson ME, Grinstein S. 2014. The vacuolar-type H+-ATPase at a glance-more than a proton pump. J. Cell Sci. 127:4987-93
112. Mayle KM, Le AM, Kamei DT. 2012. The intracellular trafficking pathway of transferrin. Biochim. Biophys. Acta 1820:264-81
113. McClellandA,KuhnLC, Ruddle FH. 1984. The human transferrin receptor gene: genomic organization, and the complete primary structure of the receptor deduced from a cDNA sequence. Cell 39:267-74
114. 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. 105:207-14
115. Motley A, Bright NA, Seaman MN, Robinson MS. 2003. Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162:909-18
116. Moura IC, Arcos-Fajardo M, Sadaka C, Leroy V, Benhamou M, et al. 2004. Glycosylation and size of IgA1 are essential for interaction with mesangial transferrin receptor in IgA nephropathy. J. Am. Soc. Nephrol. 15:622-34
117. Moura IC, Centelles MN, Arcos-Fajardo M, Malheiros DM, Collawn JF, et al. 2001. Identification of the transferrin receptor as a novel immunoglobulin (Ig)A1 receptor and its enhanced expression on mesangial cells in IgA nephropathy. J. Exp. Med. 194:417-25
118. MuckenthalerMU, Rivella S, HentzeMW,Galy B. 2017. A red carpet for iron metabolism. Cell 168:344-61
119. Nai A, Lidonnici MR, Rausa M, Mandelli G, Pagani A, et al. 2015. The second transferrin receptor regulates red blood cell production in mice. Blood 125:1170-79
120. Ned RM, Swat W, Andrews NC. 2003. Transferrin receptor 1 is differentially required in lymphocyte development. Blood 102:3711-18
121. Nekhai S, Kumari N, Dhawan S. 2013. Role of cellular iron and oxygen in the regulation of HIV-1 infection. Future Virol. 8:301-11
122. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, et al. 2004. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306:2090-93
123. Nunberg JH, York J. 2012. The curious case of arenavirus entry, and its inhibition. Viruses 4:83-101
124. Oppenheimer SJ. 2001. Iron and its relation to immunity and infectious disease. J. Nutr. 131:616S-33S
125. Palermo LM, Hueffer K, Parrish CR. 2003. Residues in the apical domain of the feline and canine transferrin receptors control host-specific binding and cell infection of canine and feline parvoviruses. J. Virol. 77:8915-23
126. Park GS, Best SM, Bloom ME. 2005. Two mink parvoviruses use different cellular receptors for entry into CRFK cells. Virology 340:1-9
127. Parker JS,MurphyWJ, Wang D, O'Brien SJ, Parrish CR. 2001. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75:3896-902
128. Peng YY, Uprichard J. 2017. Ferritin and iron studies in anaemia and chronic disease. Ann. Clin. Biochem. 54:43-48
129. Philpott CC, RyuMS. 2014. Special delivery: distributing iron in the cytosol of mammalian cells. Front. Pharmacol. 5:173
130. Radoshitzky SR, Abraham J, Spiropoulou CF, Kuhn JH, Nguyen D, et al. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96
131. Radoshitzky SR, Kuhn JH, Spiropoulou CF, Albarino CG, Nguyen DP, et al. 2008. Receptor determinants of zoonotic transmission of NewWorld hemorrhagic fever arenaviruses. PNAS 105:2664-69
132. Recalcati S,Gammella E, Buratti P, CairoG. 2017. Molecular regulation of cellular iron balance. IUBMB Life 69:389-98
133. Robb AD, Ericsson M, Wessling-Resnick M. 2004. Transferrin receptor 2 mediates a biphasic pattern of transferrin uptake associated with ligand delivery to multivesicular bodies. Am. J. Physiol. Cell Physiol. 287:C1769-75
134. Robb AD, Wessling-Resnick M. 2004. Regulation of transferrin receptor 2 protein levels by transferrin. Blood 104:4294-99
135. Rose PP, Hanna SL, Spiridigliozzi A, Wannissorn N, Beiting DP, et al. 2011. Natural resistance-associated macrophage protein is a cellular receptor for Sindbis virus in both insect and mammalian hosts. Cell Host Microbe 10:97-104
136. Ross SR, Schofield JJ, Farr CJ, Bucan M. 2002. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. PNAS 99:12386-90
137. Rutledge EA, Enns CA. 1996. Cleavage of the transferrin receptor is influenced by the composition of the O-linked carbohydrate at position 104. J. Cell. Physiol. 168:284-93
138. RyuMS, ZhangD, ProtchenkoO, Shakoury-ElizehM, Philpott CC. 2017. PCBP1 andNCOA4regulate erythroid iron storage and heme biosynthesis. J. Clin. Investig. 127:1786-97
139. Salmeron A, Borroto A, Fresno M, Crumpton MJ,Ley SC, Alarcon B. 1995. Transferrin receptor induces tyrosine phosphorylation in T cells and is physically associated with the TCR zeta-chain. J. Immunol. 154:1675-83
140. Sarute N, Ross SR. 2017. NewWorld arenavirus biology. Annu. Rev. Virol. 4:141-58
141. Senyilmaz D, Virtue S, Xu X, Tan CY, Griffin JL, et al. 2015. Regulation of mitochondrial morphology and function by stearoylation of TFR1. Nature 525:124-28
142. Sheftel AD, Mason AB, Ponka P. 2012. The long history of iron in the Universe and in health and disease. Biochim. Biophys. Acta 1820:161-87
143. Sheftel AD, Zhang AS, Brown C, Shirihai OS, Ponka P. 2007. Direct interorganellar transfer of iron from endosome to mitochondrion. Blood 110:125-32
144. Shi H, Bencze KZ, Stemmler TL, Philpott CC. 2008. A cytosolic iron chaperone that delivers iron to ferritin. Science 320:1207-10
145. Shu ST, Emert-Sedlak LA, Smithgall TE. 2017. Cell-based fluorescence complementation reveals a role forHIV-1 Nef protein dimerization in AP-2 adaptor recruitment andCD4co-receptor down-regulation. J. Biol. Chem. 292:2670-78
146. Spiro DJ, Boll W, Kirchhausen T, Wessling-Resnick M. 1996. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell 7:355-67
147. Steere AN, Chasteen ND, Miller BF, Smith VC, MacGillivray RT, Mason AB. 2012. Structure-based mutagenesis reveals critical residues in the transferrin receptor participating in the mechanism of pHinduced release of iron from human serum transferrin. Biochemistry 51:2113-21
148. Stiles KM, Kielian M. 2011. Alphavirus entry: NRAMP leads the way. Cell Host Microbe 10:92-93
149. Sun JZ, Wang J, Wang S, Yuan D, Li Z, et al. 2014. MicroRNA miR-320a and miR-140 inhibit mink enteritis virus infection by repression of its receptor, feline transferrin receptor. Virol. J. 11:210
150. Tachiyama R, Ishikawa D, Matsumoto M, Nakayama KI, Yoshimori T, et al. 2011. Proteome of ubiquitin/ MVB pathway: possible involvement of iron-induced ubiquitylation of transferrin receptor in lysosomal degradation. Genes Cells 16:448-66
151. TerBush DR, Maurice T, Roth D, Novick P. 1996. The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15:6483-94
152. Touret N, Furuya W, Forbes J, Gros P, Grinstein S. 2003. Dynamic traffic through the recycling compartment couples the metal transporter Nramp2 (DMT1) with the transferrin receptor. J. Biol. Chem. 278:25548-57
153. Traer CJ, Rutherford AC, Palmer KJ,Wassmer T, Oakley J, et al. 2007. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9:1370-80
154. Trenor CC 3rd, Campagna DR, Sellers VM, Andrews NC, Fleming MD. 2000. The molecular defect in hypotransferrinemic mice. Blood 96:1113-18
155. Vogt TM, Blackwell AD, Giannetti AM, Bjorkman PJ, Enns CA. 2003. Heterotypic interactions between transferrin receptor and transferrin receptor. Blood 101:2008-14
156. Wallace DF, Summerville L, Subramaniam VN. 2007. Targeted disruption of the hepatic transferrin receptor 2 gene in mice leads to iron overload. Gastroenterology 132:301-10
157. Wandinger-Ness A, Zerial M. 2014. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb. Perspect. Biol. 6:a022616
158. Wang E, Albritton L, Ross SR. 2006. Identification of the segments of the mouse transferrin receptor 1 required for mouse mammary tumor virus infection. J. Biol. Chem. 281:10243-49
159. Wang E, Obeng-AdjeiN, YingQ,Meertens L, Dragic T, et al. 2008. Mouse mammary tumor virus uses mouse but not human transferrin receptor 1 to reach a low pH compartment and infect cells. Virology 381:230-40
160. Watts C. 1985. Rapid endocytosis of the transferrin receptor in the absence of bound transferrin. J. Cell Biol. 100:633-37
161. Weinberg ED. 1996. Iron withholding: a defense against viral infections. BioMetals 9:393-99
162. Weiss G, Carver PL. 2017. Role of divalent metals in infectious disease susceptibility and outcome. Clin. Microbiol. Infect. 24:16-23
163. Wen J, Pan S, Liang S, Zhong Z, He Y, et al. 2013. Soluble form of canine transferrin receptor inhibits canine parvovirus infection in vitro and in vivo. BioMed Res. Int. 2013:172479
164. Wessling-Resnick M. 2010. Iron homeostasis and the inflammatory response. Annu. Rev. Nutr. 30:105-22
165. Wessling-Resnick M. 2015. Nramp1 and other transporters involved in metal withholding during infection. J. Biol. Chem. 290:18984-90
166. West AP Jr., Bennett MJ, Sellers VM, Andrews NC, Enns CA, Bjorkman PJ. 2000. Comparison of the interactions of transferrin receptor and transferrin receptor 2 with transferrin and the hereditary hemochromatosis protein HFE. J. Biol. Chem. 275:38135-38
167. White RA, Boydston LA, Brookshier TR, McNulty SG, Nsumu NN, et al. 2005. Iron metabolism mutant hbd mice have a deletion in Sec15l1, which has homology to a yeast gene for vesicle docking. Genomics 86:668-73
168. Worthen CA, Enns CA. 2014. The role of hepatic transferrin receptor 2 in the regulation of iron homeostasis in the body. Front. Pharmacol. 5:34
169. Xia H, Anderson B,Mao Q, Davidson BL. 2000. Recombinant human adenovirus: Targeting to the human transferrin receptor improves gene transfer to brain microcapillary endothelium. J. Virol. 74:11359-66
170. Xu W, Barrientos T, Mao L, Rockman HA, Sauve AA, Andrews NC. 2015. Lethal cardiomyopathy in mice lacking transferrin receptor in the heart. Cell Rep. 13:533-45
171. Yanatori I, Yasui Y, Tabuchi M, Kishi F. 2014. Chaperone protein involved in transmembrane transport of iron. Biochem. J. 462:25-37
172. Yang B, Hoe MH, Black P, Hunt RC. 1993. Role of oligosaccharides in the processing and function of human transferrin receptors: effect of the loss of the three N-glycosyl oligosaccharides individually or together. J. Biol. Chem. 268:7435-41
173. Yang FM, FriedrichsWE, Buchanan JM,Herbert DC,Weaker FJ, et al. 1990. Tissue specific expression of mouse transferrin during development and aging. Mech. Ageing Dev. 56:187-97
174. Zapata JC, Salvato MS. 2013. Arenavirus variations due to host-specific adaptation. Viruses 5:241-78
175. Zeltina A,Krumm SA, Sahin M, Struwe WB,Harlos K, et al. 2017. Convergent immunological solutions to Argentine hemorrhagic fever virus neutralization. PNAS 114:7031-36
176. Zhang AS, Sheftel AD, Ponka P. 2005. Intracellular kinetics of iron in reticulocytes: evidence for endosome involvement in iron targeting to mitochondria. Blood 105:368-75
177. Zhang AS, Xiong S, Tsukamoto H, Enns CA. 2004. Localization of iron metabolism-related mRNAs in rat liver indicate that HFE is expressed predominantly in hepatocytes. Blood 103:1509-14
178. Zhao N, Enns CA. 2013. N-linked glycosylation is required for transferrin-induced stabilization of transferrin receptor 2, but not for transferrin binding or trafficking to the cell surface. Biochemistry 52:3310-19
179. Zong M, Fofana I, Choe H. 2014. Human and host species transferrin receptor 1 use byNorth American arenaviruses. J. Virol. 88:9418-28
180. Zumerle S,Mathieu JR, Delga S, Heinis M, Viatte L, et al. 2014. Targeted disruption of hepcidin in the liver recapitulates the hemochromatotic phenotype. Blood 123:3646-50