Ferristatin II Promotes Degradation of Transferrin Receptor-1 In Vitro and In Vivo

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Byrne, Shaina L ^a   Buckett, Peter D ^a   Kim, Jonghan ^a   Luo, Flora ^a   Sanford, Jack ^a   Chen, Juxing ^b   Enns, Caroline ^b   Wessling Resnick, Marianne ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CD71 ANTIGEN; CLATHRIN; FERRISTATIN II; GLYCINE; HEME; HEPCIDIN; IRON 59; LIGAND; LIVER PROTEIN; MUTANT PROTEIN; NYSTATIN; PROTEIN INHIBITOR; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; ENDOCYTOSIS; GENE EXPRESSION; HEPCIDIN GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE ABSORPTION; IRON BLOOD LEVEL; IRON STORAGE; IRON TRANSPORT; LIGAND BINDING; LIPID RAFT; MALE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; RECEPTOR BINDING; RECEPTOR BLOCKING; RECEPTOR DOWN REGULATION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; BRAIN MAPPING; CASE-CONTROL STUDIES; CELL PHYSIOLOGICAL PHENOMENA; FEMALE; FLUORODEOXYGLUCOSE F18; FOLLOW-UP STUDIES; GLUCOSE; HUMANS; LONGITUDINAL STUDIES; MALE; MICE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NEURAL NETWORKS (COMPUTER); NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY; RATS;

EID: 84880730276     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070199     Document Type: Article

References (82)

1. Aisen P, Listowsky I, (1980) Iron transport and storage proteins. Annu Rev Biochem 49: 357-393.
2. Lederman HM, Cohen A, Lee JW, Freedman MH, Gelfand EW, (1984) Deferoxamine: a reversible S-phase inhibitor of human lymphocyte proliferation. Blood 64: 748-753.
3. Seligman PA, Schleicher RB, Siriwardana G, Domenico J, Gelfand EW, (1993) Effects of agents that inhibit cellular iron incorporation on bladder cancer cell proliferation. Blood 82: 1608-1617.
4. Noulsri E, Richardson DR, Lerdwana S, Fucharoen S, Yamagishi T, et al. (2009) Antitumor activity and mechanism of action of the iron chelator, Dp44mT, against leukemic cells. Am J Hematol 84: 170-176.
5. Ciechanover A, Schwartz AL, Lodish HF, (1983) The asialoglycoprotein receptor internalizes and recycles independently of the transferrin and insulin receptors. Cell 32: 267-275.
6. van Renswoude J, Bridges KR, Harford JB, Klausner RD, (1982) Receptor-mediated endocytosis of transferrin and the uptake of Fe in K562 cells: identification of a nonlysosomal acidic compartment. Proc Natl Acad Sci U S A 79: 6186-6190.
7. Ohgami RS, Campagna DR, Greer EL, Antiochos B, McDonald A, et al. (2005) Identification of a ferrireductase required for efficient transferrin-dependent iron uptake in erythroid cells. Nat Genet 37: 1264-1269.
8. Lambe T, Simpson RJ, Dawson S, Bouriez-Jones T, Crockford TL, et al. (2009) Identification of a Steap3 endosomal targeting motif essential for normal iron metabolism. Blood 113: 1805-1808.
9. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, et al. (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci U S A 95: 1148-1153.
10. Zhao N, Gao J, Enns CA, Knutson MD, (2010) ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J Biol Chem 285: 32141-32150.
11. Dong XP, Cheng X, Mills E, Delling M, Wang F, et al. (2008) The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 455: 992-996.
12. Dautry-Varsat A, Ciechanover A, Lodish HF, (1983) pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci U S A 80: 2258-2262.
13. Klausner RD, Van Renswoude J, Ashwell G, Kempf C, Schechter AN, et al. (1983) Receptor-mediated endocytosis of transferrin in K562 cells. J Biol Chem 258: 4715-4724.
14. Herbison CE, Thorstensen K, Chua AC, Graham RM, Leedman P, et al. (2009) The role of transferrin receptor 1 and 2 in transferrin-bound iron uptake in human hepatoma cells. Am J Physiol Cell Physiol 297: C1567-1575.
15. Ciechanover A, Schwartz AL, Dautry-Varsat A, Lodish HF, (1983) Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J Biol Chem 258: 9681-9689.
16. Beardmore J, Howell KE, Miller K, Hopkins CR, (1987) Isolation of an endocytic compartment from A431 cells using a density modification procedure employing a receptor-specific monoclonal antibody complexed with colloidal gold. J Cell Sci 87 (Pt 4): 495-506.
17. Zuk PA, Elferink LA, (2000) Rab15 differentially regulates early endocytic trafficking. J Biol Chem 275: 26754-26764.
18. McMahon HT, Boucrot E, (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533.
19. McGraw TE, Maxfield FR, (1990) Human transferrin receptor internalization is partially dependent upon an aromatic amino acid on the cytoplasmic domain. Cell Regul 1: 369-377.
20. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, et al. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269: 1872-1875.
21. Pytowski B, Judge TW, McGraw TE, (1995) An internalization motif is created in the cytoplasmic domain of the transferrin receptor by substitution of a tyrosine at the first position of a predicted tight turn. J Biol Chem 270: 9067-9073.
22. Hinshaw JE, Schmid SL, (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374: 190-192.
23. Sweitzer SM, Hinshaw JE, (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93: 1021-1029.
24. Babitt JL, Huang FW, Wrighting DM, Xia Y, Sidis Y, et al. (2006) Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet 38: 531-539.
25. 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.
26. Camaschella C, Roetto A, Cali A, De 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.
27. Montosi G, Donovan A, Totaro A, Garuti C, Pignatti E, et al. (2001) Autosomal-dominant hemochromatosis is associated with a mutation in the ferroportin (SLC11A3) gene. J Clin Invest 108: 619-623.
28. Roetto A, Papanikolaou G, Politou M, Alberti F, Girelli D, et al. (2003) Mutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosis. Nat Genet 33: 21-22.
29. Papanikolaou G, Samuels ME, Ludwig EH, MacDonald ML, Franchini PL, et al. (2004) Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis. Nat Genet 36: 77-82.
30. Gao J, Chen J, De Domenico I, Koeller DM, Harding CO, et al. (2010) Hepatocyte-targeted HFE and TFR2 control hepcidin expression in mice. Blood 115: 3374-3381.
31. Schmidt PJ, Toran PT, Giannetti AM, Bjorkman PJ, Andrews NC, (2008) The transferrin receptor modulates Hfe-dependent regulation of hepcidin expression. Cell Metab 7: 205-214.
32. Gao J, Chen J, Kramer M, Tsukamoto H, Zhang AS, et al. (2009) Interaction of the hereditary hemochromatosis protein HFE with transferrin receptor 2 is required for transferrin-induced hepcidin expression. Cell Metab 9: 217-227.
33. Schmidt PJ, Andrews NC, Fleming MD, (2010) Hepcidin induction by transgenic overexpression of Hfe does not require the Hfe cytoplasmic tail, but does require hemojuvelin. Blood 116: 5679-5687.
34. Vujic Spasic M, Kiss J, Herrmann T, Galy B, Martinache S, et al. (2008) Hfe acts in hepatocytes to prevent hemochromatosis. Cell Metab 7: 173-178.
35. 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: 2090-2093.
36. Canonne-Hergaux F, Donovan A, Delaby C, Wang HJ, Gros P, (2006) Comparative studies of duodenal and macrophage ferroportin proteins. Am J Physiol Gastrointest Liver Physiol 290: G156-163.
37. Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI, et al. (2005) The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab 1: 191-200.
38. Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, et al. (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276: 7811-7819.
39. Weinstein DA, Roy CN, Fleming MD, Loda MF, Wolfsdorf JI, et al. (2002) Inappropriate expression of hepcidin is associated with iron refractory anemia: implications for the anemia of chronic disease. Blood 100: 3776-3781.
40. Bridle KR, Frazer DM, Wilkins SJ, Dixon JL, Purdie DM, et al. (2003) Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis. Lancet 361: 669-673.
41. Nemeth E, Roetto A, Garozzo G, Ganz T, Camaschella C, (2005) Hepcidin is decreased in TFR2 hemochromatosis. Blood 105: 1803-1806.
42. Byrne SL, Krishnamurthy D, Wessling-Resnick M, (2013) Pharmacology of iron transport. Annu Rev Pharmacol Toxicol 53: 17-36.
43. Brown JX, Buckett PD, Wessling-Resnick M, (2004) Identification of small molecule inhibitors that distinguish between non-transferrin bound iron uptake and transferrin-mediated iron transport. Chem Biol 11: 407-416.
44. Horonchik L, Wessling-Resnick M, (2008) The small-molecule iron transport inhibitor ferristatin/NSC306711 promotes degradation of the transferrin receptor. Chem Biol 15: 647-653.
45. Buckett PD, Wessling-Resnick M, (2009) Small molecule inhibitors of divalent metal transporter-1. Am J Physiol Gastrointest Liver Physiol 296: G798-804.
46. 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.
47. Chen J, Chloupkova M, 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: 36862-36870.
48. Warren RA, Green FA, Enns CA, (1997) Saturation of the endocytic pathway for the transferrin receptor does not affect the endocytosis of the epidermal growth factor receptor. J Biol Chem 272: 2116-2121.
49. Heilig E, Molina R, Donaghey T, Brain JD, Wessling-Resnick M, (2005) Pharmacokinetics of pulmonary manganese absorption: evidence for increased susceptibility to manganese loading in iron-deficient rats. Am J Physiol Lung Cell Mol Physiol 288: L887-893.
50. Kim J, Molina RM, Donaghey TC, Buckett PD, Brain JD, et al. (2011) Influence of DMT1 and iron status on inflammatory responses in the lung. Am J Physiol Lung Cell Mol Physiol 300: L659-665.
51. Feder JN, Penny DM, Irrinki A, Lee VK, Lebron JA, et al. (1998) The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc Natl Acad Sci U S A 95: 1472-1477.
52. Gross CN, Irrinki A, Feder JN, Enns CA, (1998) Co-trafficking of HFE, a nonclassical major histocompatibility complex class I protein, with the transferrin receptor implies a role in intracellular iron regulation. J Biol Chem 273: 22068-22074.
53. 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: 28494-28498.
54. Parton RG, Richards AA, (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4: 724-738.
55. Brown DA, (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21: 430-439.
56. Watts C, (1985) Rapid endocytosis of the transferrin receptor in the absence of bound transferrin. J Cell Biol 100: 633-637.
57. Stein BS, Sussman HH, (1986) Demonstration of two distinct transferrin receptor recycling pathways and transferrin-independent receptor internalization in K562 cells. J Biol Chem 261: 10319-10331.
58. 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.
59. Dubljevic V, Sali A, Goding JW, (1999) A conserved RGD (Arg-Gly-Asp) motif in the transferrin receptor is required for binding to transferrin. Biochem J 341 (Pt 1): 11-14.
60. West AP, Giannetti AM, Herr AB, Bennett MJ, Nangiana JS, et al. (2001) Mutational analysis of the transferrin receptor reveals overlapping HFE and transferrin binding sites. J Mol Biol 313: 385-397.
61. Bos RP, Groenen MA, Theuws JL, Leijdekkers CM, Henderson PT, (1984) Metabolism of benzidine-based dyes and the appearance of mutagenic metabolites in urine of rats after oral or intraperitoneal administration. Toxicology 31: 271-282.
62. Richardson DR, Ponka P, (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 1331: 1-40.
63. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, et al. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102: 2760-2765.
64. Blot V, McGraw TE, (2006) GLUT4 is internalized by a cholesterol-dependent nystatin-sensitive mechanism inhibited by insulin. Embo J 25: 5648-5658.
65. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL, (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421.
66. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, et al. (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 96: 6775-6780.
67. Auriac A, Willemetz A, Canonne-Hergaux F, (2010) Lipid raft-dependent endocytosis: a new route for hepcidin-mediated regulation of ferroportin in macrophages. Haematologica 95: 1269-1277.
68. Bourseau-Guilmain E, Griveau A, Benoit JP, Garcion E, (2011) 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 6: e25515.
69. Ganz T, (2007) Molecular control of iron transport. J Am Soc Nephrol 18: 394-400.
70. Finberg KE, Heeney MM, Campagna DR, Aydinok Y, Pearson HA, et al. (2008) Mutations in TMPRSS6 cause iron-refractory iron deficiency anemia (IRIDA). Nat Genet 40: 569-571.
71. Du X, She E, Gelbart T, Truksa J, Lee P, et al. (2008) The serine protease TMPRSS6 is required to sense iron deficiency. Science 320: 1088-1092.
72. Fleming MD, Trenor CC 3rd, Su MA, Foernzler D, Beier DR, et al (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16: 383-386.
73. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, et al. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
74. Brasse-Lagnel C, Karim Z, Letteron P, Bekri S, Bado A, et al. (2011) Intestinal DMT1 cotransporter is down-regulated by hepcidin via proteasome internalization and degradation. Gastroenterology 140: 1261-1271 e1261.
75. Sun CC, Vaja V, Babitt JL, Lin HY, (2012) Targeting the hepcidin-ferroportin axis to develop new treatment strategies for anemia of chronic disease and anemia of inflammation. Am J Hematol 87: 392-400.
76. Preza GC, Ruchala P, Pinon R, Ramos E, Qiao B, et al. (2011) Minihepcidins are rationally designed small peptides that mimic hepcidin activity in mice and may be useful for the treatment of iron overload. J Clin Invest 121: 4880-4888.
77. Ramos E, Ruchala P, Goodnough JB, Kautz L, Preza GC, et al. (2012) Minihepcidins prevent iron overload in a hepcidin-deficient mouse model of severe hemochromatosis. Blood 120: 3829-3836.
78. Theurl I, Schroll A, Sonnweber T, Nairz M, Theurl M, et al. (2011) Pharmacologic inhibition of hepcidin expression reverses anemia of chronic inflammation in rats. Blood 118: 4977-4984.
79. Babitt JL, Huang FW, Xia Y, Sidis Y, Andrews NC, et al. (2007) Modulation of bone morphogenetic protein signaling in vivo regulates systemic iron balance. J Clin Invest 117: 1933-1939.
80. Song SN, Tomosugi N, Kawabata H, Ishikawa T, Nishikawa T, et al. (2010) Down-regulation of hepcidin resulting from long-term treatment with an anti-IL-6 receptor antibody (tocilizumab) improves anemia of inflammation in multicentric Castleman disease. Blood 116: 3627-3634.
81. Fatih N, Camberlein E, Island ML, Corlu A, Abgueguen E, et al. (2010) Natural and synthetic STAT3 inhibitors reduce hepcidin expression in differentiated mouse hepatocytes expressing the active phosphorylated STAT3 form. J Mol Med (Berl) 88: 477-486.
82. Ba Q, Zhou N, Duan J, Chen T, Hao M, et al. (2012) Dihydroartemisinin exerts its anticancer activity through depleting cellular iron via transferrin receptor-1. PLoS One 7: e42703.