Immune cells and hepatocytes express glycosylphosphatidylinositol-anchored ceruloplasmin at their cell surface

Blood Cells, Molecules, and Diseases

Volumn 48, Issue 2, 2012, Pages 110-120

  Marques, Liliana ^a,b   Auriac, Anne ^c,d   Willemetz, Alexandra ^c   Banha, João ^a,b   Silva, Bruno ^a   Canonne Hergaux, François ^c,d   Costa, Luciana ^a,b  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^d INSERM   (France)

Author keywords

Ferroportin; GPI ceruloplasmin; Hepatocytes; Immune cells; Iron metabolism; Lipid raft

Indexed keywords

CERULOPLASMIN; FERROPORTIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED CERULOPLASMIN; IRON; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN HEPG2; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; LIPID RAFT; LIVER CELL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE; CELLS, CULTURED; CERULOPLASMIN; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEPATOCYTES; HUMANS; IRON; ISOENZYMES; LYMPHOCYTES; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; MONOCYTES;

EID: 84856370491     PISSN: 10799796     EISSN: 10960961     Source Type: Journal    
DOI: 10.1016/j.bcmd.2011.11.005     Document Type: Article

References (57)

1. Bielli P., Calabrese L. Structure to function relationships in ceruloplasmin: a 'moonlighting' protein. Cell. Mol. Life Sci. 2002, 59:1413-1427.
2. Shukla N., Maher J., Masters J., Angelini G.D., Jeremy J.Y. Does oxidative stress change ceruloplasmin from a protective to a vasculopathic factor?. Atherosclerosis 2006, 187:238-250.
3. Gitlin J.D. Transcriptional regulation of ceruloplasmin gene expression during inflammation. J. Biol. Chem. 1988, 263:6281-6287.
4. Gutteridge J.M., Winyard P.G., Blake D.R., et al. The behaviour of caeruloplasmin in stored human extracellular fluids in relation to ferroxidase II activity, lipid peroxidation and phenanthroline-detectable copper. Biochem. J. 1985, 230:517-523.
5. Fox P.L., Mukhopadhyay C., Ehrenwald E. Structure, oxidant activity, and cardiovascular mechanisms of human ceruloplasmin. Life Sci. 1995, 56:1749-1758.
6. Osaki S. Kinetic studies of ferrous ion oxidation with crystalline human ferroxidase (ceruloplasmin). J. Biol. Chem. 1966, 241:5053-5059.
7. Harris Z.L., Durley A.P., Man T.K., Gitlin J.D. Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10812-10817.
8. Jeong S.Y., David S. Glycosylphosphatidylinositol-anchored ceruloplasmin is required for iron efflux from cells in the central nervous system. J. Biol. Chem. 2003, 278:27144-27148.
9. De Domenico I., Ward D.M., di Patti M.C., et al. Ferroxidase activity is required for the stability of cell surface ferroportin in cells expressing GPI-ceruloplasmin. EMBO J. 2007, 26:2823-2831.
10. Di Patti M.C., Maio N., Rizzo G., et al. Dominant mutants of ceruloplasmin impair the copper loading machinery in aceruloplasminemia. J. Biol. Chem. 2009, 284:4545-4554.
11. Osaki S., Johnson D.A. Mobilization of liver iron by ferroxidase (ceruloplasmin). J. Biol. Chem. 1969, 244:5757-5758.
12. Harris Z.L. Aceruloplasminemia. J. Neurol. Sci. 2003, 207:108-109.
13. Attieh Z.K., Mukhopadhyay C.K., Seshadri V., Tripoulas N.A., Fox P.L. Ceruloplasmin ferroxidase activity stimulates cellular iron uptake by a trivalent cation-specific transport mechanism. J. Biol. Chem. 1999, 274:1116-1123.
14. Mukhopadhyay C.K., Attieh Z.K., Fox P.L. Role of ceruloplasmin in cellular iron uptake. Science 1998, 279:714-717.
15. Qian Z.M., Ke Y. Rethinking the role of ceruloplasmin in brain iron metabolism. Brain Res. Brain Res. Rev. 2001, 35:287-294.
16. Patel B.N., Dunn R.J., David S. Alternative RNA splicing generates a glycosylphosphatidylinositol-anchored form of ceruloplasmin in mammalian brain. J. Biol. Chem. 2000, 275:4305-4310.
17. Hellman N.E., Kono S., Miyajima H., Gitlin J.D. Biochemical analysis of a missense mutation in aceruloplasminemia. J. Biol. Chem. 2002, 277:1375-1380.
18. Hellman N.E., Gitlin J.D. Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 2002, 22:439-458.
19. Cousins R.J. Absorption, transport, and hepatic metabolism of copper and zinc: special reference to metallothionein and ceruloplasmin. Physiol. Rev. 1985, 65:238-309.
20. Aldred A.R., Grimes A., Schreiber G., Mercer J.F. Rat ceruloplasmin. Molecular cloning and gene expression in liver, choroid plexus, yolk sac, placenta, and testis. J. Biol. Chem. 1987, 262:2875-2878.
21. Yang F.M., Friedrichs W.E., Cupples R.L., et al. Human ceruloplasmin. Tissue-specific expression of transcripts produced by alternative splicing. J. Biol. Chem. 1990, 265:10780-10785.
22. Patel B.N., David S. A novel glycosylphosphatidylinositol-anchored form of ceruloplasmin is expressed by mammalian astrocytes. J. Biol. Chem. 1997, 272:20185-20190.
23. Patel B.N., Dunn R.J., Jeong S.Y., et al. Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury. J. Neurosci. 2002, 22:6578-6586.
24. Abboud S., Haile D. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 2000, 275:19906-19912.
25. Donovan A., Brownlie A., Zhou Y., et al. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 2000, 403:776-781.
26. McKie A.T., Marciani P., Rolfs A., 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.
27. Canonne-Hergaux F., Donovan A., Delaby C., Wang H.J., Gros P. Comparative studies of duodenal and macrophage ferroportin proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290:G156-G163.
28. Di Patti M., Maio N., Rizzo G., et al. Dominant mutants of ceruloplasmin impair the copper loading machinery in aceruloplasminemia. J. Biol. Chem. 2009, 284:4545-4554.
29. Pan Y., Katula K., Failla M.L. Expression of ceruloplasmin gene in human and rat lymphocytes. Biochim. Biophys. Acta 1996, 1307:233-238.
30. Mazumder B., Mukhopadhyay C.K., Prok A., Cathcart M.K., Fox P.L. Induction of ceruloplasmin synthesis by IFN-gamma in human monocytic cells. J. Immunol. 1997, 159:1938-1944.
31. Fleming R.E., Whitman I.P., Gitlin J.D. Induction of ceruloplasmin gene expression in rat lung during inflammation and hyperoxia. Am. J. Physiol. 1991, 260:L68-L74.
32. Banha J., Marques L., Oliveira R., et al. Ceruloplasmin expression by human peripheral blood lymphocytes: a new link between immunity and iron metabolism. Free Radic. Biol. Med. 2008, 44:483-492.
33. Delaby C., Pilard N., Hetet G., et al. A physiological model to study iron recycling in macrophages. Exp. Cell Res. 2005, 310:43-53.
34. Auriac A., Willemetz A., Canonne-Hergaux F. Lipid raft-dependent endocytosis: a new route for hepcidin-mediated regulation of ferroportin in macrophages. Haematologica 2010, 95:1269-1277.
35. Delaby C., Pilard N., Goncalves A.S., Beaumont C., Canonne-Hergaux F. Presence of the iron exporter ferroportin at the plasma membrane of macrophages is enhanced by iron loading and down-regulated by hepcidin. Blood 2005, 106:3979-3984.
36. Sato M., Gitlin J.D. Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J. Biol. Chem. 1991, 266:5128-5134.
37. Sarkar J., Seshadri V., Tripoulas N.A., Ketterer M.E., Fox P.L. Role of ceruloplasmin in macrophage iron efflux during hypoxia. J. Biol. Chem. 2003, 278:44018-44024.
38. Orso E., Werner T., Wolf Z., et al. Ezetimib influences the expression of raft-associated antigens in human monocytes. Cytom. A 2006, 69:206-208.
39. Fortna R.R., Watson H.A., Nyquist S.E. Glycosyl phosphatidylinositol-anchored ceruloplasmin is expressed by rat Sertoli cells and is concentrated in detergent-insoluble membrane fractions. Biol. Reprod. 1999, 61:1042-1049.
40. Salzer J.L., Lovejoy L., Linder M.C., Rosen C. Ran-2, a glial lineage marker, is a GPI-anchored form of ceruloplasmin. J. Neurosci. Res. 1998, 54:147-157.
41. Mostad E.J., Prohaska J.R. GPI-Ceruloplasmin is expressed in multiple rodent organs and is markedly lower in spleen following dietary copper deficiency. Exp. Biol. Med. 2011, 236:298-308.
42. Schmitz G., Orso E. CD14 signalling in lipid rafts: new ligands and co-receptors. Curr. Opin. Lipidol. 2002, 13:513-521.
43. Deshmukh V.K., Raman P.H., Dhuley J.N., Naik S.R. Role of ceruloplasmin in inflammation: increased serum ceruloplasmin levels during inflammatory conditions and its possible relationship with anti-inflammatory agents. Pharmacol. Res. Commun. 1985, 17:633-642.
44. Ehrenwald E., Fox P.L. Role of endogenous ceruloplasmin in low density lipoprotein oxidation by human U937 monocytic cells. J. Clin. Invest. 1996, 97:884-890.
45. Fox P.L., Mazumder B., Ehrenwald E., Mukhopadhyay C.K. Ceruloplasmin and cardiovascular disease. Free Radic. Biol. Med. 2000, 28:1735-1744.
46. Ali H., Haribabu B., Richardson R.M., Snyderman R. Mechanisms of inflammation and leukocyte activation. Med. Clin. North Am. 1997, 81:1-28.
47. Owen C.A. Leukocyte cell surface proteinases: regulation of expression, functions, and mechanisms of surface localization. Int. J. Biochem. Cell Biol. 2008, 40:1246-1272.
48. De Sousa M. Immune cell functions in iron overload. Clin. Exp. Immunol. 1989, 75:1-6.
49. De Sousa M., Smithyman A., Tan C. Suggested models of ecotaxopathy in lymphoreticular malignancy. A role for iron-binding proteins in the control of lymphoid cell migration. Am. J. Pathol. 1978, 90:497-520.
50. Pinto J.P., Dias V., Zoller H., et al. Hepcidin messenger RNA expression in human lymphocytes. Immunology 2010, 130:217-230.
51. Zhang A.S., Xiong S., Tsukamoto H., Enns C.A. Localization of iron metabolism-related mRNAs in rat liver indicate that HFE is expressed predominantly in hepatocytes. Blood 2004, 103:1509-1514.
52. Chen H., Attieh Z.K., Syed B.A., 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.
53. Duce J.A., Tsatsanis A., Cater M.A., et al. Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 2010, 142:857-867.
54. Asare G.A., Mossanda K.S., Kew M.C., et al. Hepatocellular carcinoma caused by iron overload: a possible mechanism of direct hepatocarcinogenicity. Toxicology 2006, 219:41-52.
55. Jacolot S., Ferec C., Mura C. Iron responses in hepatic, intestinal and macrophage/monocyte cell lines under different culture conditions. Blood Cells Mol. Dis. 2008, 41:100-108.
56. Ramey G., Deschemin J.C., Durel B., et al. Hepcidin targets ferroportin for degradation in hepatocytes. Haematologica 2010, 95:501-504.
57. Pinnix Z.K., Miller L.D., Wang W., et al. Ferroportin and iron regulation in breast cancer progression and prognosis. Sci Transl. Med 2010, 2:43ra56.