Human macrophage ferroportin biology and the basis for the ferroportin disease

Hepatology

Volumn 65, Issue 5, 2017, Pages 1512-1525

  Sabelli, Manuela ^a   Montosi, Giuliana ^a   Garuti, Cinzia ^a   Caleffi, Angela ^a   Oliveto, Stefania ^b   Biffo, Stefano ^b,c   Pietrangelo, Antonello ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b INGM   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FERROPORTIN 1; HEPCIDIN; CATION TRANSPORT PROTEIN; HAMP PROTEIN, HUMAN; IRON; METAL TRANSPORTING PROTEIN 1;

ANIMAL CELL; ARTICLE; BLOOD DONOR; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GEL FILTRATION; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; IRON BLOOD LEVEL; MACROPHAGE; MDCK CELL LINE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TURNOVER TIME; WESTERN BLOTTING; ANIMAL; CASE CONTROL STUDY; DEFICIENCY; METABOLISM; MOUSE;

ANIMALS; CASE-CONTROL STUDIES; CATION TRANSPORT PROTEINS; HEP G2 CELLS; HEPCIDINS; HUMANS; IRON; MACROPHAGES; MICE;

EID: 85016497543     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.29007     Document Type: Article

References (50)

1. Drakesmith H, Nemeth E, Ganz T. Ironing out Ferroportin. Cell Metab 2015;22:777-787.
2. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004;306:2090-2093.
3. Rice AE, Mendez MJ, Hokanson CA, Rees DC, Bjorkman PJ. Investigation of the biophysical and cell biological properties of ferroportin, a multipass integral membrane protein iron exporter. J Mol Biol 2009;386:717-732.
4. Canonne-Hergaux F, Donovan A, Delaby C, Wang HJ, Gros P. Comparative studies of duodenal and macrophage ferroportin proteins. Am J Physiol Gastrointest Liver Physiol 2006;290:G156-G163.
5. Schimanski LM, Drakesmith H, Merryweather-Clarke AT, Viprakasit V, Edwards JP, Sweetland E, et al. In vitro functional analysis of human ferroportin (FPN) and hemochromatosis-associated FPN mutations. Blood 2005;105:4096-4102.
6. Drakesmith H, Schimanski LM, Ormerod E, Merryweather-Clarke AT, Viprakasit V, Edwards JP, et al. Resistance to hepcidin is conferred by hemochromatosis-associated mutations of ferroportin. Blood 2005;106:1092-1097.
7. Liu XB, Yang F, Haile DJ. Functional consequences of ferroportin 1 mutations. Blood Cells Mol Dis 2005;35:33-46.
8. De Domenico I, Ward DM, Musci G, Kaplan J. Evidence for the multimeric structure of ferroportin. Blood 2007;109:2205-2209.
9. Wallace DF, Harris JM, Subramaniam VN. Functional analysis and theoretical modeling of ferroportin reveals clustering of mutations according to phenotype. Am J Physiol Cell Physiol 2010;298:C75-C84.
10. Le Gac G, Ka C, Joubrel R, Gourlaouen I, Lehn P, Mornon JP, et al. Structure-function analysis of the human ferroportin iron exporter (SLC40A1): effect of hemochromatosis type 4 disease mutations and identification of critical residues. Hum Mutat 2013;34:1371-1380.
11. Bonaccorsi di Patti MC, Polticelli F, Cece G, Cutone A, Felici F, Persichini T, Musci G. A structural model of human ferroportin and of its iron binding site. FEBS J 2014;281:2851-2860.
12. Praschberger R, Schranz M, Griffiths WJ, Baumgartner N, Hermann M, Lomas DJ, et al. Impact of D181V and A69T on the function of ferroportin as an iron export pump and hepcidin receptor. Biochim Biophys Acta 2014;1842:1406-1412.
13. Taniguchi R, Kato HE, Font J, Deshpande CN, Wada M, Ito K, et al. Outward- and inward-facing structures of a putative bacterial transition-metal transporter with homology to ferroportin. Nat Commun 2015;6:8545.
14. Pietrangelo A. The ferroportin disease. Blood Cells Mol Dis 2004;32:131-138.
15. Pietrangelo A, Montosi G, Totaro A, Garuti C, Conte D, Cassanelli S, et al. Hereditary hemochromatosis in adults without pathogenic mutations in the hemochromatosis gene [see comments]. N Engl J Med 1999;341:725-732.
16. Montosi G, Donovan A, Totaro A, Garuti C, Pignatti E, Cassanelli S, et al. Autosomal-dominant hemochromatosis is associated with a mutation in the ferroportin (SLC11A3) gene. J Clin Invest 2001;108:619-623.
17. Njajou OT, Vaessen N, Joosse M, Berghuis B, van Dongen JW, Breuning MH, et al. A mutation in SLC11A3 is associated with autosomal dominant hemochromatosis. Nat Genet 2001;28:213-214.
18. Wallace DF, Clark RM, Harley HA, Subramaniam VN. Autosomal dominant iron overload due to a novel mutation of ferroportin1 associated with parenchymal iron loading and cirrhosis. J Hepatol 2004;40:710-713.
19. Sham RL, Phatak PD, West C, Lee P, Andrews C, Beutler E. Autosomal dominant hereditary hemochromatosis associated with a novel ferroportin mutation and unique clinical features. Blood Cells Mol Dis 2005;34:157-161.
20. McGregor JA, Shayeghi M, Vulpe CD, Anderson GJ, Pietrangelo A, Simpson RJ, McKie AT. Impaired iron transport activity of ferroportin 1 in hereditary iron overload. J Membr Biol 2005;206:3-7.
21. De Domenico I, Ward DM, Nemeth E, Vaughn MB, Musci G, Ganz T, Kaplan J. The molecular basis of ferroportin-linked hemochromatosis. Proc Natl Acad Sci U S A 2005;102:8955-8960.
22. De Domenico I, McVey Ward D, Nemeth E, Ganz T, Corradini E, Ferrara F, et al. Molecular and clinical correlates in iron overload associated with mutations in ferroportin. Haematologica 2006;91:1092-1095.
23. De Domenico I, Ward DM, Langelier C, Vaughn MB, Nemeth E, Sundquist WI, et al. The molecular mechanism of hepcidin-mediated ferroportin down-regulation. Mol Biol Cell 2007;18:2569-2578.
24. Mayr R, Janecke AR, Schranz M, Griffiths WJ, Vogel W, Pietrangelo A, Zoller H. Ferroportin disease: a systematic meta-analysis of clinical and molecular findings. J Hepatol 2010;53:941-949.
25. Griffiths WJ, Mayr R, McFarlane I, Hermann M, Halsall DJ, Zoller H, Cox TM. Clinical presentation and molecular pathophysiology of autosomal dominant hemochromatosis caused by a novel ferroportin mutation. Hepatology 2010;51:788-795.
26. Mayr R, Griffiths WJ, Hermann M, McFarlane I, Halsall DJ, Finkenstedt A, et al. Identification of mutations in SLC40A1 that affect ferroportin function and phenotype of human ferroportin iron overload. Gastroenterology 2011;140:2056-2063, 2063.e1.
27. Pietrangelo A, Caleffi A, Corradini E. Non-HFE hepatic iron overload. Sem Liv Dis 2011;31:302-318.
28. Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI, Robine S, Andrews NC. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab 2005;1:191-200.
29. Zohn IE, De Domenico I, Pollock A, Ward DM, Goodman JF, Liang X, et al. The flatiron mutation in mouse ferroportin acts as a dominant negative to cause ferroportin disease. Blood 2007;109:4174-4180.
30. Goncalves AS, Muzeau F, Blaybel R, Hetet G, Driss F, Delaby C, et al. Wild-type and mutant ferroportins do not form oligomers in transfected cells. Biochem J 2006;396:265-275.
31. Schimanski LM, Drakesmith H, Talbott C, Horne K, James JR, Davis SJ, et al. Ferroportin: lack of evidence for multimers. Blood Cells Mol Dis 2008;40:360-369.
32. Pignatti E, Mascheroni L, Sabelli M, Barelli S, Biffo S, Pietrangelo A. Ferroportin is a monomer in vivo in mice. Blood Cells Mol Dis 2006;36:26-32.
33. Montosi G, Paglia P, Garuti C, Guzman CA, Bastin JM, Colombo MP, Pietrangelo A. Wild-type HFE protein normalizes transferrin iron accumulation in macrophages from subjects with hereditary hemochromatosis. Blood 2000;96:1125-1129.
34. Kagan JC, Su T, Horng T, Chow A, Akira S, Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat Immunol 2008;9:361-368.
35. Schaer DJ, Boretti FS, Schoedon G, Schaffner A. Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br J Haematol 2002;119:239-243.
36. Delaby C, Pilard N, Goncalves AS, 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.
37. Park EK, Jung HS, Yang HI, Yoo MC, Kim C, Kim KS. Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm Res 2007;56:45-50.
38. Abboud S, Haile DJ. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem 2000;275:19906-19912.
39. Miluzio A, Beugnet A, Grosso S, Brina D, Mancino M, Campaner S, et al. Impairment of cytoplasmic eIF6 activity restricts lymphomagenesis and tumor progression without affecting normal growth. Cancer Cell 2011; 19:765-775.
40. Thomas TC, McNamee MG. Purification of membrane proteins. Guide to protein purification. In: Deutscher MF, ed. Methods in Enzymology Series 182. San Diego, CA: Academic; 1990:499-520.
41. Mahler HC, Friess W, Grauschopf U, Kiese S. Protein aggregation: pathways, induction factors and analysis. J Pharm Sci 2009;98:2909-2934.
42. Delaby C, Pilard N, Puy H, Canonne-Hergaux F. Sequential regulation of ferroportin expression after erythrophagocytosis in murine macrophages: early mRNA induction by haem, followed by iron-dependent protein expression. Biochem J 2008;411:123-131.
43. Pietrangelo A. Hemochromatosis: 15 years since hepcidin. Gastroenterology 2015;149:1240-1251.
44. Wallace DF, Pedersen P, Dixon JL, Stephenson P, Searle JW, Powell LW, Subramaniam VN. Novel mutation in ferroportin1 is associated with autosomal dominant hemochromatosis. Blood 2002;100:692-694.
45. Zoller H, McFarlane I, Theurl I, Stadlmann S, Nemeth E, Oxley D, et al. Primary iron overload with inappropriate hepcidin expression in V162del ferroportin disease. Hepatology 2005;42:466-472.
46. Subramaniam VN, Wallace DF, Dixon JL, Fletcher LM, Crawford DH. Ferroportin disease due to the A77D mutation in Australia. Gut 2005;54:1048-1049.
47. Pietrangelo A, Corradini E, Ferrara F, Vegetti A, De Jong G, Luca Abbati G, et al. Magnetic resonance imaging to identify classic and nonclassic forms of ferroportin disease. Blood Cells Mol Dis 2006;37:192-196.
48. Lim FL, Dooley JS, Roques AW, Grellier L, Dhillon AP, Walker AP. Hepatic iron concentration, fibrosis and response to venesection associated with the A77D and V162del “loss of function” mutations in ferroportin disease. Blood Cells Mol Dis 2008;40:328-333.
49. McDonald CJ, Wallace DF, Ostini L, Bell SJ, Demediuk B, Subramaniam VN. G80S-linked ferroportin disease: classical ferroportin disease in an Asian family and reclassification of the mutant as iron transport defective. J Hepatol 2011;54:538-544.
50. Wolff F, Bailly B, Gulbis B, Cotton F. Monitoring of hepcidin levels in a patient with G80S-linked ferroportin disease undergoing iron depletion by phlebotomy. Clin Chim Acta 2014;430:20-21.