Expression and localization of hepcidin in macrophages: A role in host defense against tuberculosis

Journal of Leukocyte Biology

Volumn 82, Issue 4, 2007, Pages 934-945

  Sow, Fatoumata B ^a   Florence, William C ^a   Satoskar, Abhay R ^a   Schlesinger, Larry S ^a   Zwilling, Bruce S ^a   Lafuse, William P ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Antimicrobial peptides; Cytokines; Innate immunity

Indexed keywords

FERROPORTIN 1; GAMMA INTERFERON; HEPCIDIN; IRON; MESSENGER RNA;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; B LYMPHOCYTE; CHEMOLUMINESCENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HOMEOSTASIS; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VITRO STUDY; IRON ABSORPTION; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; TUBERCULOSIS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; IMMUNITY, NATURAL; INTERFERON TYPE II; INTESTINAL ABSORPTION; IRON; IRON CHELATING AGENTS; IRON OVERLOAD; LIVER; MICE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOMES; RNA, MESSENGER; TUBERCULOSIS;

CORYNEBACTERINEAE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 34848888911     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0407216     Document Type: Article

References (52)

1. Schlesinger, L. S. (2004) Phagocytosis and Toll-like receptors in tuberculosis. In Tuberculosis, 2nd edition (W. M. Rom, S. M. Garay, eds.), Philadelphia, PA, USA, Lippincott, Williams, and Wilkins, 203-204.
2. Fenton, M. J., Riley, L. W., Schlesinger, L. S. (2004) Receptor-mediated recognition of Mycobacterium tuberculosis by host cells. In Tuberculosis and Tubercle Bacillus (S. T. Cole, K. D. Eisenach, D. N. McMurray, W R. Jacobs, eds.), Herndon, VA, USA, American Society for Microbiology, 405-426.
3. Flynn, J. L., Chan, J. (2001) Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-119.
4. Collins, H. L., Kaufmann, S. H. E. (2001) The many faces of host response to tuberculosis. Immunology 103, 1-9.
5. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K., Stewart, T. A., Bloom, B. R. (1993) An essential role for interferon γ in resistance in Mycobacterium tuberculosis infection. J. Exp. Med. 178, 2249-2254.
6. Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G., Orme, I. M. (1993) Disseminated tuberculosis in interferon γ disrupted mice. J. Exp. Med. 178, 2243-2247.
7. MacMicking, J., Xie, Q-W., Nathan, C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350.
8. Schaible, U. E., Strugill-Koszycki, S., Schlesinger, P. H., Russell, D. G. (1998) Cytokine activation leads to acidification and increases maturation of Mycobacterim avium-containing phagosomes in murine macrophages. J. Immunol. 160, 1290-1296.
9. Via, L. E., Fratti, R. A., McFalone, M., Pagen-Ramos, E., Deretic, D., Deretic, V. (1998) Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905.
10. Crichton, R. R., Wilmet, S., Legssyer, R., Ward, R. J. (2002) Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J. Inorg. Biochem. 91, 9-18.
11. Asp169. J. Leukoc. Biol. 66, 113-119.
12. Taetle, R., Honeysett, J. M. (1988) γ-Interferon modulates human monocyte/macrophage transferrin receptor expression. Blood 71, 1590-1595.
13. Byrd, T. F., Horwitz, M. A. (1993) Regulation of transferrin receptor expression and ferritin content in human mononuclear phagocytes. Coordinate upregulation by iron transferrin and downregulation by interferon-γ. J. Clin. Invest. 91, 969-976.
14. Mulero, V., Block, J. H. (1999) Regulation of iron metabolism in murine J774 macrophages: role of nitric oxide-dependent and -independent pathways following activation with γ interferon and lipopolysaccharide. Blood 94, 2383-2389.
15. Zhong, W., Lafuse, W. P., Zwilling, B. S. (2001) Infection with Mycobacterium avium differentially regulates the expression of iron transport protein mRNA in murine peritoneal macrophages. Infect. Immun. 69, 6618-6624.
16. Gold, B., Rodriguez, G. M., Marras, M. P., Pentecost, M., Smith, I. (2001) The Mycobacterium tuberculosis IdeR is a dual functional regulator and controls transcription of genes involved in iron acquisition, iron storage, and survival in macrophages. Mol. Microbiol. 42, 851-865.
17. De Voss, J. J., Rutter, K., Schroeder, B. G., Barry III, C. E. (1999) Iron acquisition and metabolism by mycobacteria. J. Bacteriol. 181, 4443-4451.
18. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D., Nathan, C., Schoolnik, G. K. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198, 693-704.
19. Timm, J., Post, F. A., Bekker, L. G., Walther, G. B., Wainwright, C. H., Manganelli, R., Chan, W. T., Tsenova, L., Gold, B., Smith, I., Kaplan, G., McKinney, J. D. (2003) Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronicle infected mice and tuberculosis patients. Proc. Natl. Acad. Sci. USA 100, 14321-14326.
20. Hancock, R. E., Diamond, G. (2000) The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol. 8, 402-410.
21. Krause, A., Neitz, S., Magert, H. J., Schulz, A., Forssmann, W. G., Schulz-Knappe, P., Adermann, K. (2000) LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity. FEBS Lett. 480, 147-150.
22. Park, C. H., Valore, E. V., Waring, A. J., Ganz, T. (2001) Hepcidin: a urinary antimicrobial peptide synthesized in the liver. J. Biol. Chem. 276, 7806-7810.
23. Laftah, A. H., Ramesh, B., Simpson, R. J., Solanky, N., Bahram, S., Schumann, K., Debnam, E. S., Srai, S. K. S. (2004) Effect of hepcidin on intestinal iron absorption in mice. Blood 103, 3940-3944.
24. Yamaji, S., Sharp, P., Ramesh, B., Srai, S. K. S. (2004) Inhibition of iron transport across human intestinal epithelial cells by hepcidin. Blood 104, 2178-2180.
25. Knutson, M. D., Oukka, M., Koss, L. M., Aydemir, F., Wessling-Resnick, M. (2005) Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc. Natl. Acad. Sci. USA 102, 1324-1328.
26. Nemeth, E., Tuttle, M. S., Powelson, J., Vaughn, M. B., Donovan, A., McVey Ward, D., Gantz, T., Kaplan, J. (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306, 2090-2093.
27. Nicolas, G., Bennoun, M., Devaux, I., Beaumont, C., Grandchamp, B., Kahn, A., Vaulont, S. (2001) Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc. Natl. Acad. Sci. USA 98, 8780-8785.
28. Nicolas, G., Bennoun, M., Porteu, A., Mativet, S., Beaumont, C., Grandchamp, B., Sirito, M., Sawadogo, M., Kahn, A., Vaulont, S. (2002) Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc. Natl. Acad. Sci. USA 99, 4596-4601.
29. Nemeth, E., Rivera, S., Gabayan, V., Keller, C., Taudorf, S., Pedersen, B. K., Ganz, T. (2004) IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 113, 1271-1276.
30. Nemeth, E., Valore, E. V., Territo, M., Schiller, G., Lichtenstein, A., Ganz, T. (2003) Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 101, 2461-2463.
31. Lee, P., Peng, H., Gelbart, T., Wang, L., Beutler, E. (2005) Regulation of hepcidin transcription by interleukin-1 and interleukin-6. Proc. Natl. Acad. Sci. USA 102, 1906-1910.
32. Anderson, G. J., Frazer, D. M., Wilkins, S. J., Becker, E. M., Millard, K. N., Murphy, T. L., McKie, A. T., Vulpe, C. D. (2002) Relationship between intestinal iron-transporter expression, hepatic hepcidin levels and the control of iron absorption. Biochem. Soc. Trans. 30, 724-726.
33. Nicolas, G., Ghauvet, C., Viatte, L., Danan, J. L., Biggard, X., Devaux, I., Beaumont, C., Kahn, A., Vaulont, S. (2002) The gene that codes for hepcidin, an iron regulatory hormone, is regulated by anemia, hypoxia, and inflammation. J. Clin. Invest. 110, 1037-1044.
34. Pigeon, C., Ilyin, G., Courselaud, B., Leroyer, P., Turlin, B., Brissot, P., Loreal, O. (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J. Biol. Chem. 276, 7811-7819.
35. Peyssonnaux, C., Zinkernagel, A. S., Datta, V., Lauth, X., Johnson, R. S., Nizet, V. (2006) TLR-4 dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood 107, 3727-3732.
36. Schlesinger, L. S. (1993) Macrophage phagocytosis of virulent but not attenuated strains is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150, 2920-2930.
37. -ΔΔCt method. Methods 25, 402-408.
38. Ferguson, J. S., Voelker, D. R., Ufnar, J. A., Dawson, A. J., Schlesinger, L. S. (2002) Surfactant protein D inhibition of human macrophage uptake of Mycobacterium tuberculosis is independent of bacterial agglutination. J. Immunol. 168, 1309-1314.
39. Fleming, R. E., Sly, W. S. (2001) Hepcidin: a putative iron regulatory hormone relative to hereditary hemochromatosis and the anemia of chronic disease. Proc. Natl. Acad. Sci. USA 98, 8160-8162.
40. Roy, C. N., Custodio, A. O., deGraaf, J., Schneider, S., Akpan, I., Montross, L. K., Sanchez, M., Gaudino, A., Hentze, M. W., Andrews, N. C., Muckenthaler, M. U. (2004) An Hfe-dependent pathway mediates hyposidermia in response to lipopolysaccharide-induced inflammation in mice. Nat. Genet. 36, 481-485.
41. Liu, X. B., Nguyen, N. H., Marquess, K. D., Yang, F., Haile, D. J. (2005) Regulation of hepcidin and ferroportin expression by lipopolysaccharide in splenic macrophages. Blood Cells Mol. Dis. 35, 47-56.
42. Nguyen, N-B., Callaghan, K. D., Ghio, A. J., Haile, D. J., Yang, F. (2006) Hepcidin expression and iron transport in alveolar macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L417-L425.
43. Dlaska, M., Weiss, G. (1999) Central role of transcription factor NF-IL6 for cytokines and iron-mediated regulation of murine inducible nitric oxide synthase expression. J. Immunol. 162, 6171-6177.
44. Boelaert, J. R., Vandecasteele, S. J., Appelberg, R., Gordeuk, V. R. (2007) The effect of the host's iron status on tuberculosis. J. Infect. Dis. 195, 1745-1753.
45. Nicolas, G., Viatte, L., Bennoun, M., Beaumont, C., Kahn, A., Vaulont, S. (2002) Hepcidin, a new iron regulatory peptide. Blood Cells Mol. Dis. 29, 327-335.
46. Olakanmi, O., Schlesinger, L. S., Ahmed, A., Britigan, B. E. (2002) Intraphagosomal Mycobacterium tuberculosis acquires iron from both extracellular transferrin and intracellular iron pools. Impact of interferon-γ and hemochromatosis. J. Biol. Chem. 277, 49727-49734.
47. Olakanmi, O., Schlesinger, L. S., Ahmed, A., Britigan, B. E. (2004) The nature of extracellular iron influences iron acquisition by Mycobacterium tuberculosis. Infect. Immun. 72, 2022-2028.
48. Ganz, T. (2003) Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 102, 783-788.
49. Weinstein, D. A., Roy, C. N., Fleming, M. D., Loda, M. F., Wolfsdorf, J. I., Andrews, N. C. (2002) Inappropriate expression of hepcidin is associated with iron refractory anemia: implications for the anemia of chronic disease. Blood 100, 3776-3781.
50. Goldenberg, A. S. (1996) Haematological abnormalities and mycobacterial infections. In Tuberculosis (W. N. Rome, S. Garay, eds,), Boston, MA, USA, Little Brown and Company, 645-652.
51. Gangaidzo, I. T., Moyo, V. M., Mvundura, E., Aggrey, G., Murphree, N. L., Khumalo, H., Saungweme, T., Kasvosve, I., Gomo, Z. A. R., Rouault, T., Boelaert, J. R., Gordeuk, V. R. (2001) Association of pulmonary tuberculosis with increased dietary iron. J. Infect. Dis. 184, 936-939.
52. Lounis, N., Truffot-Pernot, C., Grosset, J., Grodeuk, V. R., Boelaert, J. R. (2001) Iron and Mycobacterium tuberculosis infection. J. Clin. Virol. 20, 123-126.