Repression of repulsive guidance molecule C during inflammation is independent of Hfe and involves tumor necrosis factor-α

American Journal of Pathology

Volumn 170, Issue 2, 2007, Pages 497-504

  Constante, Marco ^a   Wang, Dongmei ^a   Raymond, Valérie Ann ^b   Bilodeau, Marc ^b   Santos, Manuela M ^a,c  

^a NOTRE DAME HOSPITAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOJUVELIN; HEPCIDIN; HFE PROTEIN; INTERLEUKIN 6; IRON; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; ANTIMICROBIAL CATIONIC PEPTIDE; HFE PROTEIN, MOUSE; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; MUSCLE PROTEIN; RGMC PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; DRUG EFFECT; GENETICS; HEMOCHROMATOSIS; HUMAN; METABOLISM;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; DOWN-REGULATION; HEMOCHROMATOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INFLAMMATION; INTERLEUKIN-6; IRON; LIPOPOLYSACCHARIDES; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33947531436     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.060437     Document Type: Article

References (60)

1. Pietrangelo A: Iron, oxidative stress and liver fibrogenesis. J Hepatol 1998, 28:8-13
2. Wood JC, Enriquez C, Ghugre N, Otto-Duessel M, Aguilar M, Nelson MD, Moats REX, Coates TD: Physiology and pathophysiology of iron cardiomyopathy in thalassemia. Ann NY Acad Sci 2005, 1054:386-395
3. Parkkila S, Parkkila AK, Waheed A, Britton RS, Zhou XY, Fleming RE, Tomatsu S, Bacon BR, Sly WS: Cell surface expression of HFE protein in epithelial cells, macrophages, and monocytes. Haematologica 2000, 85:340-345
4. Parkkila S, Waheed A, Britton RS, Feder JN, Tsuchihashi Z, Schatzman RC, Bacon BR, Sly WS: Immunohistochemistry of HLA-H, the protein defective in patients with hereditary hemochromatosis, reveals unique pattern of expression in gastrointestinal tract. Proc Natl Acad Sci USA 1997, 94:2534-2539
5. Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, Basava A, Dormishian F, Domingo R, Ellis MC, Fullan A, Hinton LM, Jones NL, Kimmel BE, Kronmal GS, Lauer P, Lee VK, Loeb DB, Mapa FA, McClelland E, Meyer NC, Mintier GA, Moeller N, Moore T, Morikang E, Prass CE, Quintana L, Starnes SM, Schatzman RC, Brunke KJ, Drayna DT, Risch NJ, Bacon BR, Wolff RK: A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet 1996, 13:399-408
6. Feder JN, Tsuchihashi Z, Irrinki A, Lee VK, Mapa FA, Morikang E, Prass CE, Starnes SM, Wolff RK, Parkkila S, Sly WS, Schatzman RC: The hemochromatosis founder mutation in HLA-H disrupts beta2-microglobulin interaction and cell surface expression. J Biol Chem 1997, 272:14025-14028
7. Santos M, Schilham MW, Rademakers LH, Marx JJ, de Sousa M, Clevers H: Defective iron homeostasis in beta 2-microglobulin knockout mice recapitulates hereditary hemochromatosis in man. J Exp Med 1996, 184:1975-1985
8. Ajioka RS, Levy JE, Andrews NC, Kushner JP: Regulation of iron absorption in Hfe mutant mice. Blood 2002, 100:1465-1469
9. Levy JE, Montross LK, Cohen DE, Fleming MD, Andrews NC: The C282Y mutation causing hereditary hemochromatosis does not produce a null allele. Blood 1999, 94:9-11
10. Feder JN, Penny DM, Irrinki A, Lee VK, Lebron JA, Watson N, Tsuchihashi Z, Sigal E, Bjorkman PJ, Schatzman RC: The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc Natl Acad Sci USA 1998, 95:1472-1477
11. Salter-Cid L, Brunmark A, Li Y, Leturcq D, Peterson PA, Jackson MR, Yang Y: Transferrin receptor is negatively modulated by the hemochromatosis protein HFE: implications for cellular iron homeostasis. Proc Natl Acad Sci USA 1999, 96:5434-5439
12. Camaschella C, Roetto A, De Gobbi M: Juvenile hemochromatosis. Semin Hematol 2002, 39:242-248
13. Roetto A, Papanikolaou G, Politou M, Alberti F, Girelli D, Christakis J, Loukopoulos D, Camaschella C: Mutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosis. Nat Genet 2003, 33:21-22
14. Papanikolaou G, Samuels ME, Ludwig EH, MacDonald ML, Franchini PL, Dube MP, Andres L, MacFarlane J, Sakellaropoulos N, Politou M, Nemeth E, Thompson J, Risler JK, Zaborowska C, Babakaiff R, Radomski CC, Pape TD, Davidas O, Christakis J, Brissot P, Lockitch G, Ganz T, Hayden MR, Goldberg YP: Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis. Nat Genet 2004, 36:77-82
15. 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, 276:7811-7819
16. Park CH, Valore EV, Waring AJ, Ganz T: Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 2001, 276:7806-7810
17. Krause A, Neitz S, Magert H-J, Schulz A, Forssmann W-G, Schulz-Knappe P, Adermann K: LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett 2000, 480:147-150
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 USA 2001, 98:8780-8785
19. Nicolas G, Bennoun M, Porteu A, Mativet S, Beaumont C. Grandchamp B, Sirito M, Sawadogo M, Kahn A, Vaulont S: Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc Natl Acad Sci USA 2002, 99:4596-4601
20. Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S: The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 2002, 110:1037-1044
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, 306:2090-2093
22. Niederkofler V, Salie R, Arber S: Hemojuvelin is essential for dietary iron sensing, and its mutation leads to severe iron overload. J Clin Invest 2005, 115:2180-2186
23. Monnier PP, Sierra A, Macchi P, Deitinghoff L, Andersen JS, Mann M, Flad M, Hornberger MR, Stahl B, Bonhoeffer F, Mueller BK: RGM is a repulsive guidance molecule for retinal axons. Nature 2002, 419:392-395
24. Huang FW, Pinkus JL, Pinkus GS, Fleming MD, Andrews NC: A mouse model of juvenile hemochromatosis. J Clin Invest 2005, 115:2187-2191
25. Bridle KR, Frazer DM, Wilkins SJ, Dixon JL, Purdie DM, Crawford DH, Subramaniam VN, Powell LW, Anderson GJ, Ramm GA: Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis. Lancet 2003, 361:669-673
26. Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, Knutson MD, Ganz T, Cousins RJ: Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci USA 2005, 102:6843-6848
27. Li N, Choudhuri S, Cherrington NJ, Klaassen CD: Down-regulation of mouse organic anion-transporting polypeptide 4 (Oatp4; Oatp1b2; Slc21a10) mRNA by lipopolysaccharide through the toll-like receptor 4 (TLR4). Drug Metab Dispos 2004, 32:1265-1271
28. Camenisch TD, Koller BH, Earp HS, Matsushima GK: A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide- induced endotoxic shock. J Immunol 1999, 162:3498-3503
29. Kirchgessner TG, Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS: Tumor necrosis factor-alpha contributes to obesity-related hyperleptinemia by regulating leptin release from adipocytes. J Clin Invest 1997, 100:2777-2782
30. de Coupade C, Ajuebor MN, Russo-Marie F, Perretti M, Solito E: Cytokine modulation of liver annexin 1 expression during experimental endotoxemia. Am J Pathol 2001, 159:1435-1443
31. Makui H, Soares RJ, Jiang W, Constante M, Santos MM: Contribution of Hfe expression in macrophages to the regulation of hepatic hepcidin levels and iron loading. Blood 2005, 106:2189-2195
32. Musallam L, Ethier C, Haddad PS, Bilodeau M: Role of EGF receptor tyrosine kinase activity in antiapoptotic effect of EGF on mouse hepatocytes. Am J Physiol 2001, 280:G1360-G1369
33. Miranda CJ, Makui H, Andrews NC, Santos MM: Contributions of beta2-microglobulin-dependent molecules and lymphocytes to iron regulation: insights from HfeRag1(-/-) and beta2mRag1(-/-) double knock-out mice. Blood 2004, 103:2847-2849
34. Mazur A, Feillet-Coudray C, Romier B, Bayle D, Gueux E, Ruivard M, Coudray C, Rayssiguier Y: Dietary iron regulates hepatic hepcidin 1 and 2 mRNAs in mice. Metabolism 2003, 52:1229-1231
35. Constante M, Jiang W, Wang D, Raymond V-A, Bilodeau M, Santos MM: Distinct requirements for Hfe in basal and induced hepcidin levels in iron overload and inflammation. Am J Physiol 2006, 291:G229-G237
36. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S: Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999, 162:3749-3752
37. Dupic F, Fruchon S, Bensaid M, Loreal O, Brissot P, Borot N, Roth MP, Coppin H: Duodenal mRNA expression of iron related genes in response to iron loading and iron deficiency in four strains of mice. Gut 2002, 51:648-653
38. Beutler B, Krochin N, Milsark IW, Luedke C, Cerami A: Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science 1986, 232:977-980
39. Mengozzi M, Sironi M, Gadina M, Ghezzi P: Reversal of defective IL-6 production in lipopolysaccharide-tolerant mice by phorbol myristate acetate. J Immunol 1991, 147:899-902
40. Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, Ganz T: IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 2004, 113:1271-1276
41. Kobune M, Kohgo Y, Kato J, Miyazaki E, Niitsu Y: Interleukin-6 enhances hepatic transferrin uptake and ferritin expression in rats. Hepatology 1994, 19:1468-1475
42. Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T: Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 2003, 101:2461-2463
43. Lee P, Peng H, Gelbart T, Beutler E: The IL-6- and lipopolysaccharide- induced transcription of hepcidin in HFE-, transferrin receptor 2-, and beta 2-microglobulin-deficient hepatocytes. Proc Natl Acad Sci USA 2004, 101:9263-9265
44. Krijt J, Vokurka M, Chang KT, Necas E: Expression of Rgmc, the murine ortholog of hemojuvelin gene, is modulated by development and inflammation, but not by iron status or erythropoietin. Blood 2004, 104:4308-4310
45. Theurl I, Ludwiczek S, Eller P, Seifert M, Artner E, Brunner P, Weiss G: Pathways for the regulation of body iron homeostasis in response to experimental iron overload. J Hepatol 2005, 43:711-719
46. Pietrangelo A: Hereditary hemochromatosis - a new look at an old disease. N Engl J Med 2004, 350:2383-2397
47. Lin L, Goldberg YP, Ganz T: Competitive regulation of hepcidin mRNA by soluble and cell-associated hemojuvelin. Blood 2005, 106:2884-2889
48. Ahmad KA, Ahmann JR, Migas MC, Waheed A, Britton RS, Bacon BR, Sly WS, Fleming RE: Decreased liver hepcidin expression in the Hfe knockout mouse. Blood Cells Mol Dis 2002, 29:361-366
49. Muckenthaler M, Roy CN, Custodio AO, Minana B, deGraaf J, Montross LK, Andrews NC, Hentze MW: Regulatory defects in liver and intestine implicate abnormal hepcidin and Cybrd1 expression in mouse hemochromatosis. Nat Genet 2003, 34:102-107
50. Gehrke SG, Herrmann T, Kulaksiz H, Merle U, Bents K, Kaiser I, Riedel HD, Stremmel W: Iron stores modulate hepatic hepcidin expression by an HFE-independent pathway. Digestion 2005, 72:25-32
51. Roy CN, Andrews NC: Anemia of inflammation: the hepcidin link. Curr Opin Hematol 2005, 12:107-111
52. Tanaka T, Araki E, Nitta K, Tateno M: Recombinant human tumor necrosis factor depresses serum iron in mice. J Biol Response Mod 1987, 6:484-488
53. Alvarez-Hernandez X, Liceaga J, McKay IC, Brock JH: Induction of hypoferremia and modulation of macrophage iron metabolism by tumor necrosis factor. Lab Invest 1989, 61:319-322
54. Laftah AH, Sharma N, Brookes MJ, McKie AT, Simpson RJ, Iqbal TH, Tselepis C: Tumour necrosis factor alpha causes hypoferraemia and reduced intestinal iron absorption in mice. Biochem J 2006, 397:61-67
55. Ludwiczek S, Aigner E, Theurl I, Weiss G: Cytokine-mediated regulation of iron transport in human monocytic cells. Blood 2003, 101:4148-4154
56. Nanami M, Ookawara T, Otaki Y, Ito K, Moriguchi R, Miyagawa K, Hasuike Y, Izumi M, Eguchi H, Suzuki K, Nakanishi T: Tumor necrosis factor-|alpha)-induced iron sequestration and oxidative stress in human endothelial cells. Arterioscler Thromb Vasc Biol 2005, 25:2495-2501
57. Zetterstrom M, Sundgren-Andersson AK, Ostlund P, Bartfai T: Delineation of the proinflammatory cytokine cascade in fever induction. Ann NY Acad Sci 1998, 856:48-52
58. Nelson ME, Wald TC, Bailey K, Wesselius LJ: Intrapulmonary cytokine accumulation following BAL and the role of endotoxin contamination. Chest 1999, 115:151-157
59. Fattori E, Cappelletti M, Costa P, Sellitto C, Cantoni L, Carelli M, Faggioni R, Fantuzzi G, Ghezzi P, Poll V: Defective inflammatory response in interleukin 6-deficient mice. J Exp Med 1994, 180:1243-1250
60. Lee P, Peng H, Gelbart T, Wang L, Beutler E: Regulation of hepcidin transcription by interleukin-1 and interleukin-6. Proc Natl Acad Sci USA 2005, 102:1906-1910