Mobilization of stored iron in mammals: A review

Nutrients

Volumn 5, Issue 10, 2013, Pages 4022-4050

  Linder, Maria C ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Autophagy; DMT1; Erythrocyte iron recycling; Erythropoietin; Ferritin; Ferroportin; Hepcidin; Iron mobilization; Iron stores; Lysosomes; Proteasome

Indexed keywords

5 AMINOLEVULINATE SYNTHASE; CATHEPSIN B; CATHEPSIN L; FERRITIN; FERROPORTIN; LACTACYSTIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PROTEASOME; RETICULOCYTE DELTA AMINO LEVULINATE SYNTHASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; UNCLASSIFIED DRUG;

ALKALIZATION; AUTOPHAGY; CHEMICAL REACTION; DETOXIFICATION; ERYTHROPOIESIS; HUMAN; IRON ABSORPTION; IRON KINETICS; IRON STORAGE; IRON TRANSPORT; LYSOSOME; MACROAUTOPHAGY; MICROAUTOPHAGY; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; REVIEW; SOLUBILIZATION; UBIQUITINATION;

MAMMALIA;

ANIMALS; FERRITINS; HEMOGLOBINS; HUMANS; IRON, DIETARY; LIVER; LYSOSOMES; MAMMALS; PROTEASOME ENDOPEPTIDASE COMPLEX; SPLEEN;

EID: 84885919083     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu5104022     Document Type: Review

References (137)

1. Linder, M.C. Nutrition and Metabolism of Trace Elements. In Nutritional Biochemistry and Metabolism, 2nd ed.; Linder, M.C., Ed.; Elsevier/Appleton-Lange: New York, NY, USA, 1991; pp. 215-276.
2. LeBlanc, S.; Barrick, M.D.; Arredondo, M. Heme carrier protein 1 transports heme and is involved in heme iron metabolism. Am. J. Physiol. Cell Physiol. 2012, 302, C1780-C1785.
3. Theil, E.C.; Chen, H.; Miranda, C.; Janser, H.; Elsenhans, B.; Nunez, M.T.; Pizarro, F.; Schumann, K. Absorption of iron from ferritin is independent of heme iron and ferrous salts in women and rat intestinal segments. J. Nutr. 2012, 142, 478-483.
4. Schaer, D.J.; Buehler, P.W.; Alayashi, A.; Belcher, J.D.; Vercellotti, G.M. Hemolysis and free hemoglobin revisited: Exploring hemoglobin and hemin scavengers as a novel class of therapeutic proteins. Blood 2013, 121, 1276-1284.
5. Wang, J.; Pantopoulos, K. Regulation of cellular iron metabolism. Biochem. J. 2011, 434, 365-381.
6. Muckenthaler, M.U.; Galy, B.; Hentze, M. Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu. Rev. Nutr. 2008, 28, 197-213.
7. Clegg, G.A.; Fitton, J.E.; Harrison, P.M.; Treffry, A. Ferritin: Molecular structure and iron storage mechanisms. Prog. Biophys. Mol. Biol. 1980, 36, 56-86.
8. Harrison, P.M.; Hoy, T.G.; Macara, I.G.; Hoare, R.J. Ferritin iron uptake and release. Structure-function relationships. Biochem. J. 1974, 143, 445-451.
9. Linder, M.C.; Kakavandi, H.R.; Miller, P.; Nagel, G.N. Dissociation of ferritins. Arch. Biochem. Biophys. 1989, 269, 485-496.
10. Linder, M.C.; Goode, C.A.; Gonzalez, R.; Gottschling, C.; Gray, J.; Nagel, G.N. Heart tissue contains small and large aggregates of ferritin subunits. Arch. Biochem. Biophys. 1989, 273, 34-41.
11. Linder, M.C.; Nagel, G.N.; Roboz, M.; Hungerford, D., Jr. Heart cells contain a ferritin larger and more asymmetric than ferritins of other mammalian tissues. J. Biol. Chem. 1981, 256, 9104-9111.
12. Vulimiri, L.; Linder, M.C.; Munro, H.N.; Catsimpoolas, N. Structural features of rat cardiac ferritins. Biochim. Biophys. Acta 1977, 491, 67-75.
13. Andrews, S.; Robinson, A.K.; Rodriguez-Quinones, F. Bacterial iron homeostasis. FEMS Microbiol. Rev. 2003, 27, 215-237.
14. Macedo, S.; Romao, C.V.; Mitchell, E.; Matias, P.M.; Liu, M.Y.; Xavier, A.V.; LeGall, J.; Teixeira, M.; Lindley, P.; Carrondo, M.A. The nature of the di-iron site in the bacterioferritin from Desulfovibrio desulfuricans. Nat. Struct. Biol. 2003, 10, 285-290.
15. Theil, E.C. Iron, ferritin, and nutrition. Annu. Rev. Nutr. 2004, 24, 327-343.
16. Campbell, C.H.; Ismail, R.; Linder, M.C. Ferritin mRNA is found on bound as well as free polyribosomes in rat heart. Arch. Biochem. Biophys. 1989, 273, 89-98.
17. Linder, M.C.; Madani, N.; Middleton, R.; Miremadi, A.; Cairo, G.; Tacchini, L.; Schiaffonati, L.; Rappocciolo, E. Ferritin synthesis on polyribosomes attached to the endoplasmic reticulum. J. Inorg. Biochem. 1992, 47, 229-240.
18. Tran, T.N.; Eubanks, S.; Zhou, C.Y.J.; Linder, M.C. Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 1997, 90, 4979-4986.
19. Levi, S.; Corsi, B.; Bosisio, M.; Invernizzi, R.; Volz, A.; Sanford, D.; Arosio, P.; Drysdale, J. A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 2001, 276, 24437-24440.
20. Richardson, D.R.; Lane, D.J.R.; Becker, E.M.; Huang, M.L.-H.; Whitnall, M.; Rahmanto, Y.S.; Sheftel, A.D.; Ponka, P. Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc. Natl. Acad. Sci. USA 2010, 107, 10775-10782.
21. Theil, E.C.; Liu, X.S.; Tosha, T. Gated pores in the ferritin protein nanocage. Inorg. Chim. Acta 2008, 361, 868-874.
22. Liu, X.; Theil, E.C. Ferritins: Dynamic management of biological iron and oxygen chemistry. Acc. Chem. Res. 2005, 38, 167-175.
23. Vulimiri, L.; Catsimpoolas, N.; Griffith, A.L.; Linder, M.C.; Munro, H.N. Size and charge heterogeneity of rat tissue ferritins. Biochim. Biophys. Acta 1975, 412, 148-156.
24. Vulimiri, L.; Linder, M.C.; Munro, H.N. Sex difference in the distribution and iron responsiveness of rat cardiac and skeletal muscle ferritins. Biochim. Biophys. Acta 1977, 497, 280-287.
25. Linder, M.C.; Moor, J.R.; Munro, H.N.; Morris, H.P. Structural differences in ferritins from normal and malignant rat tissues. Biochim. Biophys. Acta 1975, 386, 409-421.
26. Linder, M.C.; Wright, K.; Madara, J. Concentration, structure and iron-saturation of ferritins from normal human lung and lung tumors with graded histopathology. Enzyme 1982, 27, 189-198.
27. Linder, M.C.; Munro, H.N. Metabolic and chemical features of ferritin, a series of iron inducible tissue proteins. Am. J. Pathol. 1973, 72, 263-282.
28. Liu, X.; Jin, W.; Theil, E.C. Opening protein pores with chaotropes enhances Fe reduction and chelation of Fe from the ferritin biomineral. Proc. Natl. Acad. Sci. USA 2003, 100, 3653-3658.
29. May, C.A.; Grady, J.K.; Laue, T.M.; Poli, M.; Arosio, P.; Chasteen, N.D. The sedimentation properties of ferritins. New insights and analysis of methods of nanoparticle preparation. Biochim. Biophys. Acta 2010, 1800, 858-870.
30. Munro, H.N.; Linder, M.C. Ferritin: Structure, biosynthesis, and role in iron metabolism. Physiol. Rev. 1978, 58, 317-396.
31. Theil, E.C. Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry. Curr. Opin. Chem. Biol. 2011, 15, 304-311.
32. Toussaint, L.; Bertrand, L.; Hue, L.; Crichton, R.R.; Declercq, J.P. High resolution E-ray structures of human apoferritin H chains mutants correlates with their activity and metal binding sites. J. Mol. Biol. 2007, 365, 440-452.
33. Philpott, C.C. Coming into view: Eukaryotic iron chaperones and intracellular iron delivery. J. Biol. Chem. 2012, 2878, 13518-13523.
34. Shi, H.; Bencze, K.Z.; Stemmler, T.L.; Philpott, C.C. A cytosolic iron chaperone that delivers iron to ferritin. Science 2008, 320, 1207-1210.
35. Nam, H.; Wang, C.Y.; Zhang, L.; Zhang, W.; Hojyo, S.; Fukada, T.; Knutson, M.D. ZIP14 and DMT1 in the liver, pancreas, and heart are differentially regulated by iron deficiency and overload: Implications for tissue iron uptake in iron-related disorders. Haematologica 2013, 98, 1049-1057.
36. Kahlon, O.; Cabantchik, Z.I. The labile iron pool: Characterization, measurement, and participation in cellular processes (1). Free Radic. Biol. Med. 2002, 33, 1037-1046.
37. Ward, D.M.; Kaplan, J. Ferroportin-mediated iron transport: Expression and regulation. Biochim. Biophys. Acta 2012, 1823, 1426-1433.
38. Lane, D.J.R.; Chikhani, S.; Richardson, V.; Richardson, D.R. Transferrin iron uptake is stimulated by ascorbate via an intracellular reductive mechanism. Biochem. Biophys. Acta 2013, 1833, 1527-1541.
39. Arosio, P.; Ingrassia, R.; Cavadini, P. Ferritins: A family of molecules for iron storage, antioxidation and more. Biochim. Biophys. Acta 2009, 1790, 589-599.
40. Torti, F.M.; Torti, S.V. Regulation of ferritin genes and protein. Blood 2002, 99, 3505-3516.
41. Tsuji, Y. JunD activates transcription of human ferritin H gene through an antioxidant defense element during oxidative stress. Oncogene 2005, 24, 7567-7578.
42. Truty, J.; Malpe, R.; Linder, M.C. Iron prevents ferritin turnover in hepatic cells. J. Biol. Chem. 2001, 276, 48775-48780.
43. Kidane, T.Z.; Sauble, E.; Linder, M.C. Release of iron from ferritin requires lysosomal activity. Am. J. Physiol. Cell Physiol. 2006, 291, C445-C455.
44. Linder, M.C.; Zerounian, N.A.; Moriya, M.; Malpe, R. Iron and copper homeostasis and intestinal absorption, using the Caco2 cell model system. BioMetals 2003, 16, 145-160.
45. Moriya, M.; Linder, M.C. Vesicular transport and apotransferrin in intestinal iron absorption, as shown in the Caco2 cell model. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G301-G309.
46. Dailey, H.A.; Meissner, P.N. Erythroid heme biosynthesis and its disorders. Cold Spring Harb. Perspect. Med. 2013, 3, doi: 10.1101/cshperspect.a011676.
47. Bridges, K.R.; Hoffman, K.E. The effects of ascorbic acid on the intracellular metabolism of iron and ferritin. J. Biol. Chem. 1986, 261, 14273-14277.
48. Asano, T.; Komatsu, M.; Yamaguchi-Iwai, Y.; Ishikawa, F.; Mizushima, N.; Iwai, K. Distinct mechanisms of ferritin delivery to lysosomes in iron-depleted and iron-replete cells. Mol. Cell. Biol. 2011, 31, 2040-2052.
49. Faa, G.; Terlizzo, M.; Gerosa, C.; Congiu, T.; Angelucci, E. Patterns of iron distribution in liver cells in β-thalassemia studied in X-ray microanalysis. Haematologica 2002, 87, 479-484.
50. Garner, G.; Roberg, K.; Brunk, U.T. Endogenous ferritin protects cells with iron-laden lysosomes against oxidative stress. Free Radic. Res. 1998, 29, 103-114.
51. Houghton, P.B.; James, E.M.; Williams, W.J.; Henderson, W.J. The fine structure of dense lysosomes isolated from rat spleen. Beitr. Pathol. 1976, 157, 244-250.
52. Persson, H.L.; Nilsson, K.J.; Brunk, U.T. Novel cellular defenses against iron and oxidation: Ferritin and autophagocytosis preserve lysosomal stability in airway epithelium. Redox Rep. 2001, 6, 57-63.
53. Kurz, T.; Eaton, J.W.; Brunk, U.T. The role of lysosomes in iron metabolism and recycling. Int. J. Biochem. Cell Biol. 2011, 43, 1686-1697.
54. Droga-Mazovec, G.; Bojic, L.; Petelin, A.; Ivanova, S.; Romih, R.; Repnik, U.; Salvesen, G.S.; Stoka, V.; Turk, V.; Turk, B. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues. J. Biol. Chem. 2008, 283, 19140-19150.
55. Schafer, F.Q.; Buettner, G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30, 1191-1212.
56. Terman, A.; Kurz, T.; Navratil, M.; Arriaga, E.; Brunk, U. Mitochondrial turnover and aging of long-lived postmitotic cells: The mitochondrial-lysosomal axis theory of aging. Antioxid. Redox Signal. 2010, 12, 503-535.
57. Klionsky, D.J.; Cuervo, A.M.; Dunn, W.A., Jr.; Levine, B.; van der Klei, I.; Seglen, P.O. How shall I eat thee? Autophagy 2007, 3, 413-416.
58. Park, C.; Cuervo, A.M. Selective autophagy: Talking with the UPS. Cell. Biochem. Biophys. 2013, 67, 3-13.
59. Mehlhase, J.; Sandig, G.; Pantopoulos, K.; Grune, T. Oxidation-induced ferritin turnover in microglial cells: Role of proteasome. Free Radic. Biol. Med. 2005, 38, 276-285.
60. Bridges, K.R. Ascorbic acid inhibits lysosomal autophagy of ferritin. J. Biol. Chem. 1987, 262, 14773-14778.
61. Hoffman, K.E.; Yanelli, K.; Bridges, K.R. Ascorbic acid and iron metabolism: Alterations in lysosomal function. Am. J. Clin. Nutr. 1991, 54, 1188S-1192S.
62. Roberts, S.; Bomford, A. Ferritin iron kinetics and protein turnover in K562 cells. J. Biol. Chem. 1988, 263, 19181-19187.
63. Vaisman, B.; Fibach, E.; Konijn, A.M. Utilization of intracellular ferritin iron for hemoglobin synthesis in developing human erythroid precursors. Blood 1997, 90, 831-838.
64. Radisky, D.C.; Kaplan, J. Iron in cytosolic ferritin can be recycled through lysosomal degradation in human fibroblasts. Biochem. J. 1998, 336, 201-205.
65. Ollinger, K.; Roberg, K. Nutrient deprivation of cultured rat hepatocytes increases the desferrioxamine-available iron pool and augments the sensitivity to hydrogen peroxide. J. Biol. Chem. 1997, 272, 23707-23711.
66. Larson, J.A.; Howie, H.L.; So, M. Neisseria meningitidis accelerates ferritin degradation in host epithelial cells to yield an essential iron source. Mol. Microbiol. 2004, 53, 807-820.
67. Kwok, J.C.; Richardson, D.R. Examination of the mechanisms involved in doxorubicin-mediated iron accumulation in ferritin: Studies using metabolic inhibitors, protein synthesis inhibitors, and lysosomotropic agents. Mol. Pharmacol. 2004, 65, 81-195.
68. Zhang, Y.; Mikhael, M.; Xu, D.; Li, Y.; Soe-Lin, S.; Ning, B.; Li, W.; Nie, G.; Zhao, Y.; Ponka, P. Lysosomal proteolysis is the primary degradation pathway for cytosolic ferritin and cytosolic ferritin degradation is necessary for iron exit. Antioxid. Redox Signal. 2010, 13, 999-1009.
69. Kurz, T.; Gustafsson, B.; Brunk, U.T. Cell sensitivity to oxidative stress is influenced by ferritin autophagy. Free Radic. Biol. Med. 2011, 50, 1647-1658.
70. Sulzer, D.; Mosharov, E.; Talloczy, Z.; Zucca, F.A.; Simon, J.D.; Zecca, L. Neuronal pigmented autophagic vacuoles: Lipofuscin, neuromelanin, and ceroid as macroautophagic responses during aging and disease. J. Neurochem. 2008, 106, 24-36.
71. Ghosh, M.; Carlsson, F.; Laskar, A.; Yuan, X.-M.; Li, W. Lysosomal membtane permeabilization causes oxidative stress and ferritin induction in macrophages. FEBS Lett. 2011, 585, 623-629.
72. Kurz, T.; Terman, A.; Gustafsson, B.; Brunk, U.T. Lysosomes in iron metabolism, ageing and apoptosis. Histochem. Cell Biol. 2008, 129, 389-406.
73. Andrews, G.K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem. Pharmacol. 2000, 59, 95-104.
74. Ruttkay-Nedecky, B.; Nejdl, L.; Gumulec, J.; Zitka, O.; Masarik, M.; Eckschlager, T.; Stiborova, M.; Adam, V.; Kizek, R. The role of metallothionein in oxidative stress. Int. J. Mol. Sci. 2013, 14, 6044-6066.
75. Doulias, P.T.; Kotoglou, P.; Tenopoulou, M.; Keramisanou, D.; Tzavaras, T.; Brunk, U.T.; Galaris, D.; Angelidis, C. Involvement of heat shock protein-70 in the mechanism of hydrogen peroxide-induced DNA damage: The role of lysosomes and iron. Free Radic. Biol. Med. 2007, 42, 567-577.
76. Kurz, T.; Brunk, U.T. Autophagy of HSP70 and chelation of lysosomal iron in a non-redox active form. Autophagy 2009, 5, 93-95.
77. Baird, S.K.; Kurz, T.; Brunk, U.T. Metallothionein protects against oxidative stress-induced lysosomal destabilization. Biochem. J. 2006, 394, 275-283.
78. Garner, G.; Li, W.; Roberg, K.; Brunk, U.T. On the cytoprotective role of ferritin in macrophages and its ability to enhance lysosomal stability. Free Radic. Res. 1997, 27, 487-500.
79. Epsztejn, S.; Glickstein, H.; Picard, V.; Slotki, I.N.; Breuer, W.; Beaumont, C.; Cabantchik, Z.I. H-Ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood 1999, 94, 3593-3603.
80. Orino, K.; Tsuji, Y.; Torti, F.M.; Torti, S.V. Adenovirus E1A blocks oxidant-dependent ferritin induction and sensitizes cells to pro-oxidant cytotoxicity. FEBS Lett. 1999, 462, 334-338.
81. Li, W.; Yang, Q.; Mao, Z. Chaperone-mediated autophagy: Machinery, regulation and biological consequences. Cell. Mol. Life Sci. 2011, 68, 749-763.
82. Cuervo, A.M. Autophagy: Many paths to the same end. Mol. Cell. Biochem. 2004, 263, 55-72.
83. Mizushima, N. Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 2004, 36, 2491-2502.
84. Fuqua, B.K.; Vulpe, C.D.; Anderson, G.J. Intestinal iron absorption. J. Trace Elem. Med. Biol. 2012, 26, 115-119.
85. Kettern, N.; Dreiseidler, M.; Tawo, R.; Hohfeld, J. Chaperone-assisted degradation: Multiple paths to destruction. Biol. Chem. 2010, 391, 481-489.
86. Kaushik, S.; Cuervo, A.M. Autophagy as a cell-repair mechanism: Activation of chaperone-mediated autophagy during oxidative stress. Mol. Aspects Med. 2006, 27, 444-454.
87. Massey, A.; Kiffin, R.; Cuervo, A.M. Pathophysiology of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 2004, 36, 2420-2434.
88. Gamerdinger, M.; Carra, A.; Behl, C. Emerging roles of molecular chaperones and co-chaperones in sselective autophagy: Focus on BAG proteins. J. Mol. Med. 2011, 89, 1175-1182.
89. Kirkin, V.; McEwan, D.G.; Novak, I.; Didik, I. A role for ubiquitin in selective autophagy. Mol. Cell 2009, 34, 259-269.
90. Grune, T.; Jung, T.; Merker, K.; Davies, K.J. Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofusion, ceroid, and "aggresomes" during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 2004, 36, 2519-2530.
91. De Domenico, I.; Ward, D.M.; Kaplan, J. Specific iron chelators determine the route of ferritin degradation. Blood 2009, 114, 4546-4551.
92. Seglen, P.O.; Gordon, P.B. 3-Methyl adenine: Specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 1982, 79, 1889-1892.
93. Wu, Y.-T.; Tan, W.-L.; Shui, G.; Bauvy, C.; Huang, Q.; Wenk, M.R.; Ong, C.-N.; Codogno, P.; Shen, H.-M. Dual role of 3methyladenine in modulation of autophagy via different temporal patterns of inhibition on Class I and III phosphoinositide 3-kinase. J. Biol. Chem. 2010, 285, 10850-10861.
94. Williams, A.; Jahreiss, L.; Sarkar, S.; Saiki, S.; Menzies, F.M.; Ravikumar, B.; Rubinsztein, D.C. Aggregate-prone proteins are cleared from the cytosol by autophagy: Therapeutic implications. Curr. Top. Dev. Biol. 2006, 76, 89-101.
95. Harrison, P.M.; Gregory, D.W. Evidence for the existence of stable "aggregates" in horse ferritin and apoferritin. J. Mol. Biol. 1965, 14, 626-629.
96. Lee, S.S.C.; Richter, G.W. The monomers and oligomers of ferritin and apoferritin: Association and dissociation. Biochemistry 1967, 15, 65-70.
97. Williams, M.A.; Harrison, P.M. Electron microscopic and chemical studies of oligomers of ferritin. Biochem. J. 1968, 110, 265-280.
98. Welch, K.D.; Reilly, C.A.; Aust, S.D. The role of cysteine residues in the oxidation of ferritin. Free Radic. Biol. Med. 2001, 33, 399-408.
99. Welch, K.D.; van Eden, M.E.; Aust, S.D. Modification of ferritin during iron loading. Free Radic. Biol. Med. 2001, 31, 999-1006.
100. Hasan, M.R.; Morishima, D.; Tomita, K.; Katsuki, M.; Kotani, S. Identification of a 250 kDa putative microtubule-associated protein as bovine ferritin: Evidence for ferritin-microtubule interaction. FEBS J. 2005, 272, 822-831.
101. Hasan, M.R.; Koikawa, S.; Kotani, S.; Miyamoto, S.; Nakagawa, H. Ferritin forms dynamic oligomers to associate with microtubules in vivo: Implication for the role of microtubules in iron metabolism. Exp. Cell Res. 2006, 312, 1950-1960.
102. Rechsteiner, M.; Rogers, S.W. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 1996, 21, 267-271.
103. Adams, J. The proteasome: Structure, function, and role in the cell. Cancer Treat. Rev. 2003, 29, S3-S9.
104. Shringarpure, R.; Grune, T.; Mehlhase, J.; Davies, K.J.A. Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J. Biol. Chem. 2003, 278, 311-318.
105. Rock, K.L.; Gramm, C.; Rothstein, L.; Clark, K.; Stein, R.; Dick, L.; Hwang, D.; Goldberg, A.L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994, 78, 761-771.
106. Rudeck, M.; Volk, T.; Sitte, N.; Grune, T. Ferritin oxidation in vitro: Implication of iron release and degradation by the 20S proteasome. IUBMB Life 2000, 49, 451-456.
107. De Domenico, I.; Vaughn, M.B.; Li, L.; Bagley, D.; Musci, G.; Ward, D.M.; Kaplan, J. Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J. 2006, 25, 5396-5404.
108. Lloyd, J.B.; Cable, H.; Rice-Evans, C. Evidence that desferrioxamine cannot enter cells by passive diffusion. Biochem. Pharmacol. 1991, 41, 1361-1363.
109. Tosha, T.; Behera, R.K.; Ng, H.L.; Bhattahali, O.; Alber, T.; Theil, E. Ferritin protein nanocage ion channels: Gating by N-terminal extensions. J. Biol. Chem. 2012, 287, 13016-13025.
110. Jin, W.; Takagi, H.; Pancorbo, B.; Theil, E.C. Opening the ferritin pore for iron release by mutation of conserved amino acids at interhelix and loop sites. Biochemistry 2001, 40, 7525-7532.
111. Takagi, H.; Shi, D.; Ha, Y.; Allewell, N.M.; Theil, E.C. Localized unfolding at the junction of three ferritin subunits. A mechanism for iron release? J. Biol. Chem. 1998, 273, 18685-18688.
112. Liu, X.S.; Patterson, L.D.; Miller, M.J.; Theil, E.C. Peptides selected for the protein nanocage pores change the rate of iron recovery from the ferritin mineral. J. Biol. Chem. 2007, 282, 31821-31825.
113. Nguyen, T.; Linder, M.C. California State University, Fullerton, CA, USA. Unpublished work, 2010.
114. Morgan, J.; La, A.; Nguyen, T.; Sauble, E.; Gonzalez, A.; Nguyen, A.; Linder, M.C. Release of Iron from Cellular Iron Stores in Lysosomes: Potential Involvement of Divalent Metal Transporter 1 (DMT1) and Common Metabolites. In Proceedings of the Metals at EB 2012, San Diego, CA, USA, 21-25 April 2012.
115. Harris, D.C.; Aisen, P. Facilitation of Fe(II) autoxidation by Fe(III) complexing agents. Biochim. Biophys. Acta 1973, 329, 156-158.
116. Gray, L.A.; Kidane, T.Z.; Nguyen, A.; Akagi, S.; Petrasek, K.; Chu, Y.-L.; Nguyen, T.; Cabrera, A.; Kantardjieff, K.; Mason, A.Z. et al. Copper proteins and ferroxidases in human plasma in that of wild type and ceruloplasmin knockout mice. Biochem. J. 2009, 419, 237-245.
117. Chen, H.; Attieh, Z.K.; Syed, B.A.; Kuo, Y.M.; Stevens, V.; Fuqua, B.K.; Anderson, H.S.; Naylor, C.E.; Evans, R.W.; Gambling, L. et al. Identification of zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J. Nutr. 2010, 140, 1728-1735.
118. Sauble, E.N. Mechanisms of Ferritin Degradation in Lysosomes. Master's Thesis, California State University, June 2007.
119. Gruenheid, S.; Pinner, E.; Desjardins, M.; Gros, P. Natural resistance to infection with intracellular pathogens: The Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 1997, 185, 717-730.
120. Forbes, J.R.; Gros, P. Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 2003, 102, 1884-1892.
121. Soe-Lin, S.; Apte, S.S.; Andriopoulos, B., Jr.; Andrews, M.C.; Schranzhofer, M.; Kahawita, T.; Garcia-Santos, D.; Ponka, P. Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo. Proc. Natl. Acad. Sci. USA 2009, 106, 5960-5965.
122. Soe-Lin, S.; Apte, S.S.; Mikhael, M.R.; Kayembe, L.K.; Nie, G.; Ponka, P. Both Nramp1 and DMT1 are necessary for efficient macrophage iron recycling. Exp. Hematol. 2010, 38, 609-617.
123. Sun, M.; Goldin, E.; Stahl, S.; Falardeau, J.L.; Kennedy, J.C.; Acierno, J.S., Jr.; Bove, C.; Kaneski, C.R.; Nagle, J.; Bromley, M.C. et al. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum. Mol. Genet. 2000, 9, 2471-2478.
124. Venkatachalam, K.; Hofmann, I.; Monteil, C. Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1. J. Biol. Chem. 2006, 281, 17517-17527.
125. Dong, X.P.; Cheng, X.; Mills, E.; Delling, M.; Wang, F.; Kurz, T.; Xu, H. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 2008, 455, 992-996.
126. Eichelsdoerfer, J.L.; Evans, J.A.; Slaugenhaupt, S.A.; Cuajungco, M.P. Zinc dyshomeostasis is linked with the loss of mucolipidosis IV-associated TRPML1 ion channel. J. Biol. Chem. 2010, 285, 34304-34308.
127. Wang, C.Y.; Jenkitkasemwong, S.; Duarte, S.; Sparkman, B.K.; Mackenzie, B.; Knutson, M.D. ZIP8 is an iron and zinc transporter whose cell-surface expression is up-regulated by cellular iron loading. J. Biol. Chem. 2012, 287, 34032-34043.
128. Mikhael, M.; Sheftel, A.D.; Ponka, P. Ferritin does not donate its iron for haem synthesis in macrophages. Biochem. J. 2010, 429, 463-471.
129. Devireddy, L.R.; Hart, D.O.; Goetz, D.H.; Green, M.R. A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 2010, 141, 1006-1017.
130. Donovan, A.; Lima, C.A.; Pinkus, J.L.; Pinkus, G.S.; Zon, L.I.; Robine, S.; Andrews, N.C. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 2005, 1, 191-200.
131. Zhang, A.; Zhang, F.; An, P.; Guo, X.; Shen, Y.; Tao, Y.; Wu, Q.; Zhang, Y.; Yu, Y.; Ning, B.; et al. Ferroportin 1 deficiency in mouse macrophages impairs iron homeostasis and inflammatory responses. Blood 2011, 118, 1912-1922.
132. Alvarez-Hernandez, X.; Smith, M.; Glass, J. The effect of apotransferrin on iron release from Caco2 cells, an intestinal epithelial cell line. Blood 1998, 91, 3974-3979.
133. Ma, Y.; Specian, R.D.; Yeh, K.Y.; Yeh, M.; Rodriguez-Paris, J.; Glass, J. The transcytosis of divalent metal transporter 1 and apo-transferrin during iron uptake in intestinal epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283, G965-G974.
134. Nunez, M.T.; Nunez-Millacura, C.; Beltran, M.; Tapia, V.; Alvarez-Hernandez, X. Apotransferrin and holotransferrin undergo different endocytic cycles in intestinal epithelia (Caco2) cells. J. Biol. Chem. 1997, 272, 19425-19428.
135. Nemeth, E.; Ganz, T. Regulation of iron metabolism by hepcidin. Annu. Rev. Nutr. 2007, 26, 323-342.
136. Sow, F.B.; Florence, W.C.; Satoskar, A.R.; Schlesinger, L.S.; Zwilling, B.S.; Lafuse, W.P. Expression and localization of hepcidin in macrophages: A role in host defense against tuberculosis. J. Leukoc. Biol. 2007, 82, 934-945.
137. Delaby, C.; Rondeau, C.; Pouzet, C.; Willemetz, A.; Pilard, N.; Canonne-Hergaux, F. Subcellular localization of iron and heme metabolism related proteins at early stages of erythropoiesis. PLoS One 2012, 7, e42199.