Molecular mediators governing iron-copper interactions

Annual Review of Nutrition

Volumn 34, Issue , 2014, Pages 95-116

  Gulec, Sukru ^a   Collins, James F ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Ceruloplasmin, hephaestin; Copper transporting ATPase1; Divalent metal ion transporter 1; Ferroportin 1; Intestine; Liver

Indexed keywords

COPPER; IRON; CATION TRANSPORT PROTEIN; IRON INTAKE; ISOPROTEIN;

ARTICLE; ERYTHROID CELL; HOMEOSTASIS; HUMAN; INTESTINE ABSORPTION; IRON ABSORPTION; IRON INTAKE; LIVER; MACROPHAGE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CHEMISTRY; INTESTINE MUCOSA; METABOLISM; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; COPPER; ERYTHROID CELLS; HOMEOSTASIS; HUMANS; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; IRON, DIETARY; LIVER; MACROPHAGES; MODELS, BIOLOGICAL; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

EID: 84904635716     PISSN: 01999885     EISSN: 15454312     Source Type: Book Series    
DOI: 10.1146/annurev-nutr-071812-161215     Document Type: Article

References (121)

1. Aigner E, Theurl I, Haufe H, Seifert M, Hohla F, et al. 2008. Copper availability contributes to iron perturbations in human nonalcoholic fatty liver disease. Gastroenterology 135:680-88
2. Arredondo M, MendiburoMJ, Flores S, Singleton ST, Garrick MD. 2014. Mouse divalent metal transporter 1 is a copper transporter in HEK293 cells. Biometals 27:115-23
3. Arredondo M, Munoz P, Mura CV, Nunez MT. 2003. DMT1, a physiologically relevant apical Cu1+ transporter of intestinal cells. Am. J. Physiol. Cell Physiol. 284:C1525-30
4. Broderius M, Mostad E, Prohaska JR. 2012. Suppressed hepcidin expression correlates with hypotransferrinemia in copper-deficient rat pups but not dams. Genes Nutr. 7:405-14
5. Broderius M, Mostad E, Wendroth K, Prohaska JR. 2010. Levels of plasma ceruloplasmin protein are markedly lower following dietary copper deficiency in rodents. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 151:473-79
6. BrubakerC, Sturgeon P. 1956. Copper deficiency in infants; a syndrome characterized by hypocupremia, iron deficiency anemia, and hypoproteinemia. AMA J. Dis. Child. 92:254-65
7. Casareno RL,Waggoner D, Gitlin JD. 1998. The copper chaperone CCS directly interacts with copper/zinc superoxide dismutase. J. Biol. Chem. 273:23625-28
8. Chen H, Attieh ZK, Syed BA, Kuo YM, Stevens V, et al. 2010. Identification of zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J. Nutr. 140:1728-35
9. Chen H, Huang G, Su T, Gao H, Attieh ZK, et al. 2006. Decreased hephaestin activity in the intestine of copper-deficient mice causes systemic iron deficiency. J. Nutr. 136:1236-41
10. Cherukuri S, Potla R, Sarkar J, Nurko S, Harris ZL, Fox PL. 2005. Unexpected role of ceruloplasmin in intestinal iron absorption. Cell Metab. 2:309-19
11. Chloupkova M, Zhang AS, Enns CA. 2010. Stoichiometries of transferrin receptors 1 and 2 in human liver. Blood Cells Mol. Dis. 44:28-33
12. Choi J, Masaratana P, Latunde-Dada GO, Arno M, Simpson RJ, McKie AT. 2012. Duodenal reductase activity and spleen iron stores are reduced and erythropoiesis is abnormal in Dcytb knockout mice exposed to hypoxic conditions. J. Nutr. 142:1929-34
13. Chung J, Prohaska JR, Wessling-Resnick M. 2004. Ferroportin-1 is not upregulated in copper-deficient mice. J. Nutr. 134:517-21
14. Collins JF. 2006. Gene chip analyses reveal differential genetic responses to iron deficiency in rat duodenum and jejunum. Biol. Res. 39:25-37
15. Collins JF, Franck CA,Kowdley KV,Ghishan FK. 2005. Identification of differentially expressed genes in response to dietary iron deprivation in rat duodenum. Am. J. Physiol.Gastrointest. Liver Physiol. 288:G964- 71
16. Collins JF, Hu Z, Ranganathan PN, Feng D, Garrick LM, et al. 2008. Induction of arachidonate 12- lipoxygenase (Alox15) in intestine of iron-deficient rats correlates with the production of biologically active lipid mediators. Am. J. Physiol. Gastrointest. Liver Physiol. 294:G948-62
17. Collins JF, Prohaska JR, Knutson MD. 2010. Metabolic crossroads of iron and copper. Nutr. Rev. 68:133-47
18. Donovan A, Lima CA, Pinkus JL, PinkusGS, Zon LI, et al. 2005. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 1:191-200
19. Dupic F, Fruchon S, Bensaid M, Loreal O, Brissot P, et al. 2002. Duodenal mRNA expression of iron related genes in response to iron loading and iron deficiency in four strains of mice. Gut 51:648-53
20. Ece A, Uyanik BS, Iscan A, Ertan P, Yigitoglu MR. 1997. Increased serum copper and decreased serum zinc levels in children with iron deficiency anemia. Biol. Trace Elem. Res. 59:31-39
21. El-Shobaki FA, RummelW. 1979. Binding of copper to mucosal transferrin and inhibition of intestinal iron absorption in rats. Res. Exp. Med. 174:187-95
22. Evans GW. 1973. Copper homeostasis in the mammalian system. Physiol. Rev. 53:535-70
23. Feng W, Ye F, XueW, Zhou Z,Kang YJ. 2009. Copper regulation of hypoxia-inducible factor-1 activity. Mol. Pharmacol. 75:174-82
24. Fox PL. 2003. The copper-iron chronicles: the story of an intimate relationship. Biometals 16:9-40
25. Gao J, Zhao N, Knutson MD, Enns CA. 2008. The hereditary hemochromatosis protein, HFE, inhibits iron uptake via down-regulation of Zip14 in HepG2 cells. J. Biol. Chem. 283:21462-68
26. Garrick MD, Gniecko K, Liu Y, Cohan DS, Garrick LM. 1993. Transferrin and the transferrin cycle in Belgrade rat reticulocytes. J. Biol. Chem. 268:14867-74
27. Gauss GH, Kleven MD, Sendamarai AK, Fleming MD, Lawrence CM. 2013. The crystal structure of six-transmembrane epithelial antigen of the prostate 4 (Steap4), a ferri/cuprireductase, suggests a novel interdomain flavin-binding site. J. Biol. Chem. 288:20668-82
28. Gitlin JD, Schroeder JJ, Lee-Ambrose LM, Cousins RJ. 1992. Mechanisms of caeruloplasmin biosynthesis in normal and copper-deficient rats. Biochem. J. 282:835-39
29. Goodman JR, Dalman PR. 1969. Role of copper in iron localization in developing erythrocytes. Blood 34:747-53
30. Graham RM, Chua AC, Herbison CE, Olynyk JK, Trinder D. 2007. Liver iron transport. World J. Gastroenterol. 13:4725-36
31. Gulec S, Collins JF. 2013. Investigation of iron metabolism in mice expressing a mutantMenke's copper transporting ATPase (Atp7a) protein with diminished activity (Brindled; MoBr/y. PLoS ONE 8:e66010
32. Gulec S, Collins JF. 2014. Silencing the Menkes copper-transporting ATPase (Atp7a) gene in rat intestinal epithelial (IEC-6) cells increases iron flux via transcriptional induction of ferroportin 1 (Fpn1). J. Nutr. 144:12-19
33. Gunshin H, Fujiwara Y, Custodio AO, Direnzo C, Robine S, Andrews NC. 2005. Slc11a2 is required for intestinal iron absorption and erythropoiesis but dispensable in placenta and liver. J. Clin. Investig. 115:1258-66
34. GunshinH,Mackenzie B, Berger UV,Gunshin Y, Romero MF, et al. 1997. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482-88
35. Gunshin H, Starr CN, Direnzo C, Fleming MD, Jin J, et al. 2005. Cybrd1 (duodenal cytochrome b) is not necessary for dietary iron absorption in mice. Blood 106:2879-83
36. Gupta A, Lutsenko S. 2009. Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Med. Chem. 1:1125-42
37. Han O, Kim EY. 2007. Colocalization of ferroportin-1 with hephaestin on the basolateral membrane of human intestinal absorptive cells. J. Cell Biochem. 101:1000-10
38. Han O, Wessling-Resnick M. 2002. Copper repletion enhances apical iron uptake and transepithelial iron transport by Caco-2 cells. Am. J. Physiol. Gastrointest. Liver Physiol. 282:G527-33
39. Harris ZL, Durley AP,Man TK, Gitlin JD. 1999. Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux. Proc. Natl. Acad. Sci. USA 96:10812-17
40. Harris ZL, Takahashi Y, Miyajima H, Serizawa M, MacGillivray RT, Gitlin JD. 1995. Aceruloplasminemia: molecular characterization of this disorder of iron metabolism. Proc. Natl. Acad. Sci. USA 92:2539-43
41. Hart EB, Steenbock H,Waddell J, Elvehjem CA. 1928. Iron in nutrition. VII. Copper as a supplement to iron for hemoglobin building in the rat. J. Biol. Chem. 77:797-812
42. Hayashi H, Hattori A, Tatsumi Y, Hayashi K, Katano Y, et al. 2013. Various copper and iron overload patterns in the livers of patients withWilson disease and idiopathic copper toxicosis. Med. Mol. Morphol. 46:133-40
43. Hellman NE, Gitlin JD. 2002. Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22:439-58
44. Hu Z, Gulec S, Collins JF. 2010. Cross-species comparison of genomewide gene expression profiles reveals induction of hypoxia-inducible factor-responsive genes in iron-deprived intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 299:C930-38
45. Illing AC, Shawki A, Cunningham CL, Mackenzie B. 2012. Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J. Biol. Chem. 287:30485-96
46. Iwa nska S, Strusi nska D. 1978. Copper metabolism in different states of erythropoiesis activity. Acta Physiol. Pol. 29:465-74
47. Jenkitkasemwong S, Broderius M, Nam H, Prohaska JR, Knutson MD. 2010. Anemic copper-deficient rats, but not mice, display low hepcidin expression and high ferroportin levels. J. Nutr. 140:723-30
48. Jiang L, Garrick MD, Garrick LM, Zhao L, Collins JF. 2013. Divalent metal transporter 1 (Dmt1) mediates copper transport in the duodenum of iron-deficient rats and when overexpressed in irondeprived HEK-293 cells. J. Nutr. 143:1927-33
49. 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
50. Kelly EJ, Palmiter RD. 1996. A murine model of Menkes disease reveals a physiological function of metallothionein. Nat. Genet. 13:219-22
51. Kim BE, Turski ML, Nose Y, Casad M, Rockman HA, Thiele DJ. 2010. Cardiac copper deficiency activates a systemic signaling mechanism that communicates with the copper acquisition and storage organs. Cell Metab. 11:353-63
52. Kim H, Son HY, Bailey SM, Lee J. 2009. Deletion of hepatic Ctr1 reveals its function in copper acquisition and compensatory mechanisms for copper homeostasis. Am. J. Physiol. Gastrointest. Liver Physiol. 296:G356-64
53. Knutson M, Wessling-Resnick M. 2003. Iron metabolism in the reticuloendothelial system. Crit. Rev. Biochem. Mol. Biol. 38:61-88
54. Knutson MD. 2007. Steap proteins: implications for iron and copper metabolism. Nutr. Rev. 65:335-40
55. Kono S. 2013. Aceruloplasminemia: an update. Int. Rev. Neurobiol. 110:125-51
56. Konz T, Alonso-Garc?a J, Montes-Bay on M, Sanz-Medel A. 2013. Comparison of copper labeling followed by liquid chromatography-inductively coupled plasma mass spectrometry and immunochemical assays for serum hepcidin-25 determination. Anal. Chim. Acta 799:1-7
57. Laftah AH, Latunde-Dada GO, Fakih S, Hider RC, Simpson RJ, McKie AT. 2009. Haem and folate transport by proton-coupled folate transporter/haem carrier protein 1 (SLC46A1). Br. J.Nutr. 101:1150-56
58. LambeT, Simpson RJ,Dawson S, Bouriez-JonesT, Crockford TL, et al. 2009. Identification of a Steap3 endosomal targeting motif essential for normal iron metabolism. Blood 113:1805-8
59. Larin D, Mekios C, Das K, Ross B, Yang AS, Gilliam TC. 1999. Characterization of the interaction between the Wilson and Menkes disease proteins and the cytoplasmic copper chaperone, HAH1p. J. Biol. Chem. 274:28497-504
60. Latunde-Dada GO, Xiang L, Simpson RJ, McKie AT. 2011. Duodenal cytochrome b (Cybrd 1) and HIF-2?expression during acute hypoxic exposure in mice. Eur. J. Nutr. 50:699-704
61. Lee GR, Nacht S, Lukens JN, Cartwright GE. 1968. Iron metabolism in copper-deficient swine. J. Clin. Investig. 47:2058-69
62. Lespagnol A, Duflaut D, Beekman C, Blanc L, Fiucci G, et al. 2008. Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3- null mice. Cell Death Differ. 15:1723-33
63. Linder MC, Zerounian NR, Moriya M, Malpe R. 2003. Iron and copper homeostasis and intestinal absorption using the Caco2 cell model. Biometals 16:145-60
64. Liuzzi JP, Aydemir F, Nam H, Knutson MD, Cousins RJ. 2006. Zip14 (Slc39a14) mediates nontransferrin- bound iron uptake into cells. Proc. Natl. Acad. Sci. USA 103:13612-17
65. Maine GN, Burstein E. 2007. COMMD proteins: COMMing to the scene. Cell Mol. Life Sci. 64:1997-2005
66. Maine GN, Mao X, Muller PA, Komarck CM, Klomp LW, Burstein E. 2009. COMMD1 expression is controlled by critical residues that determine XIAP binding. Biochem. J. 417:601-9
67. Maisetta G, Petruzzelli R, Brancatisano FL, Esin S, Vitali A, et al. 2010. Antimicrobial activity of human hepcidin 20 and 25 against clinically relevant bacterial strains: effect of copper and acidic pH. Peptides 31:1995-2002
68. Martin F, Linden T, Katschinski DM, Oehme F, Flamme I, et al. 2005. Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation. Blood 105:4613-19
69. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C. 2009. HIF-2?, but not HIF-1?, promotes iron absorption in mice. J. Clin. Investig. 119:1159-66
70. Matak P, Zumerle S, Mastrogiannaki M, El Balkhi S, Delga S, et al. 2013. Copper deficiency leads to anemia, duodenal hypoxia, upregulation of HIF-2?and altered expression of iron absorption genes in mice. PLoS ONE 8:e59538
71. McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, et al. 2001. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291:1755-59
72. Mostad EJ, Prohaska JR. 2011. Glycosylphosphatidylinositol-linked ceruloplasmin is expressed in multiple rodent organs and is lower following dietary copper deficiency. Exp. Biol. Med. 236:298-308
73. Mukhopadhyay CK, Mazumder B, Fox PL. 2000. Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. J. Biol. Chem. 275:21048-54
74. 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
75. Nose Y, Kim BE, Thiele DJ. 2006. Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metab. 4:235-44
76. Nose Y, Rees EM, Thiele DJ. 2006. Structure of the Ctr1 copper transPORE'ter reveals novel architecture. Trends Biochem. Sci. 31:604-7
77. 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. 37:1264-69
78. Ohgami RS,CampagnaDR, McDonald A, FlemingMD. 2006. The Steap proteins aremetalloreductases. Blood 108:1388-94
79. Osaki S, Johnson DA, Frieden E. 1971. The mobilization of iron from the perfused mammalian liver by a serum copper enzyme, ferroxidase I. J. Biol. Chem. 246:3018-23
80. Owen CA Jr. 1973. Effects of iron on copper metabolism and copper on iron metabolism in rats. Am. J. Physiol. 224:514-18
81. Palumaa P, Kangur L, Voronova A, Sillard R. 2004. Metal-binding mechanism of Cox17, a copper chaperone for cytochrome c oxidase. Biochem. J. 382:307-14
82. Pan Y,Mansfield KD, Bertozzi CC, Rudenko V, Chan DA, et al. 2007. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol. Cell. Biol. 27:912-25
83. Patel BN, David S. 1997. A novel glycosylphosphatidylinositol-anchored form of ceruloplasmin is expressed by mammalian astrocytes. J. Biol. Chem. 272:20185-90
84. Pelucchi S,Mariani R, Calza S, Fracanzani AL, Modignani GL, et al. 2012. CYBRD1 as a modifier gene that modulates iron phenotype in HFE p.C282Y homozygous patients. Haematologica 97:1818-25
85. Petris MJ, Mercer JF, Culvenor JG, Lockhart P, Gleeson PA, Camakaris J. 1996. Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J. 15:6084-95
86. Pollack S, George JN, Reba RC, Kaufman RM, Crosby WH. 1965. The absorption of nonferrous metals in iron deficiency. J. Clin. Investig. 44:1470-73
87. Pourvali K, Matak P, Latunde-Dada GO, Solomou S, Mastrogiannaki M, et al. 2012. Basal expression of copper transporter 1 in intestinal epithelial cells is regulated by hypoxia-inducible factor 2?. FEBS Lett. 586:2423-27
88. Prohaska JR. 2011. Impact of copper limitation on expression and function of multicopper oxidases (ferroxidases). Adv. Nutr. 2:89-95
89. Prohaska JR, Broderius M. 2012. Copper deficiency has minimal impact on ferroportin expression or function. Biometals 25:633-42
90. Pyatskowit JW, Prohaska JR. 2008. Copper deficient rats and mice both develop anemia but only rats have lower plasma and brain iron levels. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 147:316-23
91. Qiu A, Jansen M, Sakaris A, Min SH, Chattopadhyay S, et al. 2006. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127:917-28
92. Qiu L, Ding X, Zhang Z, Kang YJ. 2012. Copper is required for cobalt-induced transcriptional activity of hypoxia-inducible factor-1. J. Pharmacol. Exp. Ther. 342:561-67
93. Ranganathan PN, Lu Y, Fuqua BK, Collins JF. 2012. Discovery of a cytosolic/soluble ferroxidase in rodent enterocytes. Proc. Natl. Acad. Sci. USA 109:3564-69
94. Ranganathan PN, Lu Y, Fuqua BK, Collins JF. 2012. Immunoreactive hephaestin and ferroxidase activity are present in the cytosolic fraction of rat enterocytes. Biometals 25:687-95
95. Ranganathan PN, Lu Y, Jiang L, Kim C, Collins JF. 2011. Serum ceruloplasmin protein expression and activity increases in iron-deficient rats and is further enhanced by higher dietary copper intake. Blood 118:3146-53
96. Ravia JJ, Stephen RM, Ghishan FK, Collins JF. 2005. Menkes copper ATPase (Atp7a) is a novel metalresponsive gene in rat duodenum, and immunoreactive protein is present on brush-border and basolateral membrane domains. J. Biol. Chem. 280:36221-27
97. Reeves PG, DeMars LC. 2004. Copper deficiency reduces iron absorption and biological half-life in male rats. J. Nutr. 134:1953-57
98. Reeves PG, DeMars LC. 2005. Repletion of copper-deficient rats with dietary copper restores duodenal hephaestin protein and iron absorption. Exp. Biol. Med. 230:320-25
99. Reeves PG, DeMars LC. 2006. Signs of iron deficiency in copper-deficient rats are not affected by iron supplements administered by diet or by injection. J. Nutr. Biochem. 17:635-42
100. Reeves PG, DeMars LC, Johnson WT, Lukaski HC. 2005. Dietary copper deficiency reduces iron absorption and duodenal enterocyte hephaestin protein in male and female rats. J. Nutr. 135:92-98
101. Roelofsen H, Wolters H, Van Luyn MJ, Miura N, Kuipers F, Vonk RJ. 2000. Copper-induced apical trafficking of ATP7B in polarized hepatoma cells provides a mechanism for biliary copper excretion. Gastroenterology 119:782-93
102. Shah YM, Matsubara T, Ito S, Yim SH, Gonzalez FJ. 2009. Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab. 9:152-64
103. Shaw GC, Cope JJ, Li L, Corson K, Hersey C, et al. 2006. Mitoferrin is essential for erythroid iron assimilation. Nature 440:96-100
104. Singh NP, Medeiros DM. 1984. Effect of copper deficiency and sodium intake upon liver lipid and mineral composition in the rat. Biol. Trace Elem. Res. 6:423-29
105. SourkesTL, Lloyd K, BirnbaumH. 1968. Inverse relationship of hepatic copper and iron concentrations in rats fed deficient diets. Can. J. Biochem. 46:267-71
106. Taylor M, Qu A, Anderson ER, Matsubara T, Martin A, et al. 2011. Hypoxia-inducible factor-2? mediates the adaptive increase of intestinal ferroportin during iron deficiency in mice. Gastroenterology 140:2044-55
107. Thackeray EW, Sanderson SO, Fox JC, Kumar N. 2011. Hepatic iron overload or cirrhosis may occur in acquired copper deficiency and is likely mediated by hypoceruloplasminemia. J. Clin. Gastroenterol. 45:153-58
108. Tselepis C, Ford SJ, McKie AT, Vogel W, Zoller H, et al. 2010. Characterization of the transitionmetal- binding properties of hepcidin. Biochem. J. 427:289-96
109. Vulpe CD, Kuo YM, Murphy TL, Cowley L, Askwith C, et al. 1999. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat. Genet. 21:195-99
110. Wang B, Dong D, Kang YJ. 2013. Copper chaperone for superoxide dismutase-1 transfers copper to mitochondria but does not affect cytochrome c oxidase activity. Exp. Biol. Med. 238:1017-23
111. Wang CY, Knutson MD. 2013. Hepatocyte divalent metal-ion transporter-1 is dispensable for hepatic iron accumulation and non-transferrin-bound iron uptake in mice. Hepatology 58:788-98
112. Wee NK, Weinstein DC, Fraser ST, Assinder SJ. 2013. The mammalian copper transporters CTR1 and CTR2 and their roles in development and disease. Int. J. Biochem. Cell Biol. 45:960-63
113. White C, Kambe T, Fulcher YG, Sachdev SW, Bush AI, et al. 2009. Copper transport into the secretory pathway is regulated by oxygen in macrophages. J. Cell Sci. 122:1315-21
114. Williams DM, Kennedy FS, Green BG. 1983. Hepatic iron accumulation in copper-deficient rats. Br. J. Nutr. 50:653-60
115. Williams DM, Loukopoulos D, Lee GR, Cartwright GE. 1976. Role of copper in mitochondrial iron metabolism. Blood 48:77-85
116. Wyman S, Simpson RJ, McKie AT, Sharp PA. 2008. Dctyb (Cybrd1) functions as both a ferric and a cupric reductase in vitro. FEBS Lett. 582:1901-6
117. Xie L, Collins JF. 2011. Transcriptional regulation of the Menkes copper ATPase (Atp7a) gene by hypoxia-inducible factor (HIF2?) in intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 300:C1298- 305
118. Xie L, Collins JF. 2013. Transcription factors Sp1 and Hif2? mediate induction of the coppertransporting ATPase (Atp7a) gene in intestinal epithelial cells during hypoxia. J. Biol. Chem. 288:23943-52
119. Yeh KY, Yeh M, Mims L, Glass J. 2009. Iron feeding induces ferroportin 1 and hephaestin migration and interaction in rat duodenal epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 296:G55-65
120. Zhang B, Georgiev O, Hagmann M, Gunes C, Cramer M, et al. 2003. Activity of metal-responsive transcription factor 1 by toxic heavy metals and H2O2 in vitro is modulated by metallothionein. Mol. Cell. Biol. 23:8471-85
121. Zoller H, Koch RO, Theurl I, Obrist P, Pietrangelo A, et al. 2001. Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 120:1412-19