Decreased hephaestin activity in the intestine of Copper-deficient mice causes systemic iron deficiency

Journal of Nutrition

Volumn 136, Issue 5, 2006, Pages 1236-1241

  Chen, Huijun ^a   Huang, Gang ^a   Su, Trent ^a   Gao, Hua ^a   Attieh, Zouhair K ^a,b   McKie, Andrew T ^c   Anderson, Gregory J ^d   Vulpe, Chris D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Ceruloplasmin; Copper; Ferroportin1; Hephaestin; Iron

Indexed keywords

CERULOPLASMIN; COPPER; FERRITIN; FERROPORTIN 1; HEPCIDIN; HEPHAESTIN; IRON; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL CULTURE; COLON ADENOCARCINOMA; COPPER DEFICIENCY; COPPER METABOLISM; HUMAN; HUMAN CELL; IRON DEFICIENCY; IRON METABOLISM; LABOR INDUCTION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TISSUE CULTURE;

ANIMALIA; MAMMALIA;

EID: 33646386896     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/136.5.1236     Document Type: Article

References (59)

1. Fox PL. The copper-iron chronicles: the story of an intimate relationship. Biometals. 2003;16:9-40.
2. Lee GR, Nacht S, Lukens JN, Cartwright GE. Iron metabolism in copper-deficient swine. J Clin Invest. 1968;47:2058-69.
3. Hart EB, Steenbock H, Waddell J, Elvehjem CA. Iron in nutrition. VII. Copper as a supplement to iron for hemoglobin building in the rat. J Biol Chem. 1928;77:797-812.
4. Danks DM. Copper deficiency in humans. Ciba Found Symp. 1980;79:209-25.
5. Petrak J, Vyoral D. Hephaestin - a ferroxidase of cellular iron export. Int J Biochem Cell Biol. 2005;37:1173-8.
6. Garrick MD, Nunez MT, Olivares M, Harris ED. Parallels and contrasts between iron and copper metabolism. Biometals. 2003;16:1-8.
7. Hellman NE, Kono S, Miyajima H, Gitlin JD. Biochemical analysis of a missense mutation in aceruloplasminemia. J Biol Chem. 2002;277:1375-80.
8. Anderson GJ, Vulpe CD. Regulation of intestinal iron transport. In: Templeton DM, editor. Molecular and cellular iron transport. New York: Marcel Dekker; 2002. p. 559-96.
9. Harris ZL, Takahashi Y, Miyajima H, Serizawa M, MacGillivray RT, Gitlin JD. Aceruloplasminemia: molecular characterization of this disorder of iron metabolism. Proc Natl Acad Sci U S A. 1995;92:2539-43.
10. Harris ZL, Durley AP, Man TK, Gitlin JD. Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux. Proc Natl Acad Sci U S A. 1999;96:10812-7.
11. Vulpe CD, Kuo YM, Murphy TL, Cowley L, Askwith C, Libina N, Gitschier J, Anderson GJ. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat Genet. 1999;21:195-9.
12. Chen H, Attieh ZK, Su T, Syed BA, Gao H, Alaeddine RM, Fox TC, Usta J, Naylor CE, et al. Hephaestin is a ferroxidase that maintains partial activity in sex-linked anemia mice. Blood. 2004;103:3933-9.
13. Li L, Vulpe CD, Kaplan J. Functional studies of hephaestin in yeast: evidence for multicopper oxidase activity in the endocytic pathway. Biochem J. 2003;375:793-8.
14. Abboud S, Haile DJ. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem. 2000;275:19906-12.
15. McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, Barrow D, Miret S, Bomford A, Peters TJ, et al. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell. 2000;5:299-309.
16. Donovan A, Brownlie A, Zhou Y, Shepard J, Pratt SJ, Moynihan J, Paw BH, Drejer A, Barut B, et al. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature. 2000;403:776-81.
17. Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, Brissot P, Loreal O. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem. 2001;276:7811-9.
18. Nicolas G, Bennoun M, Devaux I, Beaumont C, Grandchamp B, Kahn A, Vaulont S. Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci U S A. 2001;98:8780-5.
19. Frazer DM, Wilkins SJ, Becker EM, Vulpe CD, McKie AT, Trinder D, Anderson GJ. Hepcidin expression inversely correlates with the expression of duodenal iron transporters and iron absorption in rats. Gastroenterology. 2002;123:835-44.
20. Frazer DM, Inglis HR, Wilkins SJ, Millard KN, Steele TM, McLaren GD, McKie AT, Vulpe CD, Anderson GJ. Delayed hepcidin response explains the lag period in iron absorption following a stimulus to increase erythropoiesis. Gut. 2004;53:1509-15.
21. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004;306:2090-3.
22. Yamaji S, Sharp P, Ramesh B, Srai SK. Inhibition of iron transport across human intestinal epithelial cells by hepcidin. Blood. 2004;104:2178-80.
23. Nittis T, Gitlin JD. Role of copper in the proteosome-mediated degradation of the multicopper oxidase hephaestin. J Biol Chem. 2004;279:25696-702.
24. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993;123:1939-51.
25. Chen H, Su T, Attieh ZK, Fox TC, McKie AT, Anderson GJ, Vulpe CD. Systemic regulation of Hephaestin and Ireg1 revealed in studies of genetic and nutritional iron deficiency. Blood. 2003;102:1893-9.
26. Huston WM, Jennings MP, McEwan AG. The multicopper oxidase of Pseudomonas aeruginosa is a ferroxidase with a central role in iron acquisition. Mol Microbiol. 2002;45:1741-50.
27. De Freitas J, Wintz H, Kim JH, Poynton H, Fox T, Vulpe C. Yeast, a model organism for iron and copper metabolism studies. Biometals. 2003;16:185-97.
28. La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Gohre V, Moseley JL, Kropat J, Merchant S. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot Cell. 2002;1:736-57.
29. Kosman DJ. FET3P, ceruloplasmin, and the role of copper in iron metabolism. Adv Protein Chem. 2002;60:221-69.
30. Nittis T, Gitlin JD. The copper-iron connection: hereditary aceruloplasminemia. Semin Hematol. 2002;39:282-9.
31. Yuan DS, Stearman R, Dancis A, Dunn T, Beeler T, Klausner RD. The Menkes Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc Natl Acad Sci USA. 1995;92:2632-6.
32. Yuan DS, Dancis A, Klausner RD. Restriction of copper export in Saccharomyces cerevisae to a late golgi or post-golgi compartment in the secretory pathway. J Biol Chem. 1997;272:25787-93.
33. Eisenstein RS. Discovery of the ceruloplasmin homologue hephaestin: new insight into the copper/iron connection. Nutr Rev. 2000;58:22-6.
34. Miyajima H, Takahashi Y, Kono S. Aceruloplasminemia, an inherited disorder of iron metabolism. Biometals. 2003;16:205-13.
35. Hellman NE, Kono S, Miyajima H, Gitlin JD. Biochemical analysis of a missense mutation in aceruloplasminemia. J Biol Chem. 2002;277:1375-80.
36. Harris ZL, Klomp LW, Gitlin JD. Aceruloplasminemia: an inherited neurodegenerative disease with impairment of iron homeostasis. Am J Clin Nutr. 1998;67:972S-7.
37. Prohaska JR. Repletion of copper-deficient mice and brindled mice with copper or iron. J Nutr. 1984;114:422-30.
38. Reeves PG, DeMars LC. Copper deficiency reduces iron absorption and biological half-life in male rats. J Nutr. 2004;134:1953-7.
39. Osaki S, Johnson DA. Mobilization of liver iron by ferroxidase (ceruloplasmin). J Biol Chem. 1969;244:5757-8.
40. Roeser HP, Lee GR, Nacht S, Cartwright GE. The role of ceruloplasmin in iron metabolism. J Clin Invest. 1970;49:2408-17.
41. Osaki S, Johnson DA, Frieden E. The mobilization of iron from the perfused mammalian liver by a serum copper enzyme, ferroxidase I. J Biol Chem. 1971;246:3018-23.
42. McArdle HJ, Mercer JF, Sargeson AM, Danks DM. Effects of cellular copper content on copper uptake and metallothionein and ceruloplasmin mRNA levels in mouse hepatocytes. J Nutr. 1990;120:1370-5.
43. Mercer JF, Grimes A, Danks DM, Rauch H. Hepatic ceruloplasmin gene expression is unaltered in the toxic milk mouse. J Nutr. 1991;121:894-9.
44. Laftah AH, Ramesh B, Simpson RJ, Solanky N, Bahram S, Schumann K, Debnam ES, Srai SK. Effect of hepcidin on intestinal iron absorption in mice. Blood. 2004;103:3940-4.
45. Reeves PG, Demars LC. Repletion of copper-deficient rats with dietary copper restores duodenal hephaestin protein and iron absorption. Exp Biol Med (Maywood). 2005;230:320-5.
46. Reeves PG, Demars LC, Johnson WT, Lukaski HC. Dietary copper deficiency reduces iron absorption and duodenal enterocyte hephaestin protein in male and female rats. J Nutr. 2005;135:92-8.
47. Thomas C, Oates PS. Copper deficiency increases iron absorption in the rat. Am J Physiol Gastrointest Liver Physiol. 2003;285:G789-95.
48. Culotta VC, Klomp LW, Strain J, Casareno RL, Krems B, Gitlin JD. The copper chaperone for superoxide dismutase. J Biol Chem. 1997;272:23469-72.
49. Petris MJ, Strausak D, Mercer JF. The Menkes copper transporter is required for the activation of tyrosinase. Hum Mol Genet. 2000;9:2845-51.
50. Wittung-Stafshede P. Role of cofactors in protein folding. Acc Chem Res. 2002;35:201-8.
51. Hellman NE, Gitlin JD. Ceruloplasmin metabolism and function. Annu Rev Nutr. 2002;22:439-58.
52. Holtzman NA, Gaumnitz BM. Studies on the rate of release and turnover of ceruloplasmin and apoceruloplasmin in rat plasma. J Biol Chem. 1970;245:2354-8.
53. Holtzman NA, Gaumnitz BM. Identification of an apoceruloplasmin-like substance in the plasma of copper-deficient rats. J Biol Chem. 1970;245:2350-3.
54. Hellman NE, Kono S, Mancini GM, Hoogeboom AJ, De Jong GJ, Gitlin JD. Mechanisms of copper incorporation into human ceruloplasmin. J Biol Chem. 2002;277:46632-8.
55. Spritz RA, Ho L, Furumura M, Hearing VJ Jr. Mutational analysis of copper binding by human tyrosinase. J Invest Dermatol. 1997;109:207-12.
56. Syed BA, Beaumont NJ, Patel A, Naylor CE, Bayele HK, Joannou CL, Rowe PSN, Evans RW, Srai SKS. Analysis of the human hephaestin gene and protein: comparative modelling of the N-terminus ecto-domain based upon ceruloplasmin. Protein Eng. 2002;15:205-14.
57. Kostova Z, Wolf DH. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 2003;22:2309-17.
58. Bertinato J, Iskandar M, L'Abbé MR. Copper deficiency induces the upregulation of the copper chaperone for Cu/Zn superoxide dismutase in weanling male rats. J Nutr. 2003;133:28-31.
59. Zhu Z, Labbé S, Peña MM, Thiele DJ. Copper differentially regulates the activity and degradation of yeast Mac1 transcription factor. J Biol Chem. 1998;273:1277-80.