Mycobacterium tuberculosis components stimulate production of the antimicrobial peptide hepcidin

Tuberculosis

Volumn 91, Issue 4, 2011, Pages 314-321

  Sow, Fatoumata B ^a   Nandakumar, Subhadra ^a   Velu, Vijayakumar ^b   Kellar, Kathryn L ^c   Schlesinger, Larry S ^d   Amara, Rama R ^b   Lafuse, William P ^d   Shinnick, Thomas M ^a   Sable, Suraj B ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b EMORY UNIVERSITY   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Dendritic cells; Epithelial cells; Innate immunity; Mycobacteria; Tuberculosis

Indexed keywords

BACTERIAL PROTEIN; BCG VACCINE; GAMMA INTERFERON; GLYCOPROTEIN P 15095; HEPCIDIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LIPOARABINOMANNAN; LIPOPHOSPHOGLYCAN; MANNOSE; MESSENGER RNA; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLMYOINOSITOL MANNOSIDE; TOLL LIKE RECEPTOR 4 AGONIST; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; MYELOID DENDRITIC CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; FEMALE; FLOW CYTOMETRY; IMMUNITY, INNATE; INTERFERON-GAMMA; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; MYCOBACTERIUM TUBERCULOSIS; RNA, MESSENGER; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUBERCULOSIS, PULMONARY;

EID: 79960272634     PISSN: 14729792     EISSN: 1873281X     Source Type: Journal    
DOI: 10.1016/j.tube.2011.03.003     Document Type: Article

References (54)

1. WHO Tuberculosis (fact sheet number 104, March 2010) 2010
2. A.M. Cooper Cell-mediated immune responses in tuberculosis Annu Rev Immunol 27 2009 393 422
3. R. Teitelbaum, W. Schubert, L. Gunther, Y. Kress, F. Macaluso, and J.W. Pollard The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium Tuberculosis Immun 10 1999 641 650 (Pubitemid 29302917)
4. L.E. Bermudez, F.J. Sangari, P. Kolonoski, M. Petrofsky, and J. Goodman The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells Infect Immun 70 2002 140 146 (Pubitemid 34028610)
5. P.S. Hiemstra Epithelial antimicrobial peptides and proteins: their role in host defence and inflammation Paediatr Respir Rev 2 2001 306 310 (Pubitemid 34467147)
6. J. Ashitani, H. Mukae, T. Hiratsuka, M. Nakazato, K. Kumamoto, and S. Matsukura Elevated levels of alpha-defensins in plasma and BAL fluid of patients with active pulmonary tuberculosis Chest 121 2002 519 526 (Pubitemid 34132993)
7. S. Sharma, I. Verma, and G.K. Khuller Therapeutic potential of human neutrophil peptide 1 against experimental tuberculosis Antimicrob Agents Chemother 45 2001 639 640 (Pubitemid 32105312)
8. A. Krause, S. Neitz, H.J. Magert, A. Schulz, W.G. Forssmann, and P. Schulz-Knappe LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity FEBS Lett 480 2000 147 150
9. C.H. Park, E.V. Valore, A.J. Waring, and T. Ganz Hepcidin, a urinary antimicrobial peptide synthesized in the liver J Biol Chem 276 2001 7806 7810
10. F.B. Sow, W.C. Florence, A.R. Satoskar, L.S. Schlesinger, B.S. Zwilling, and W.P. Lafuse Expression and localization of hepcidin in macrophages: a role in host defense against tuberculosis J Leukoc Biol 82 2007 934 945 (Pubitemid 47511054)
11. A.H. Laftah, B. Ramesh, R.J. Simpson, N. Solanky, S. Bahram, and K. Schumann Effect of hepcidin on intestinal iron absorption in mice Blood 103 2004 3940 3944 (Pubitemid 38596316)
12. M.D. Knutson, M. Oukka, L.M. Koss, F. Aydemir, and M. Wessling-Resnick Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin Proc Natl Acad Sci U S A 102 2005 1324 1328 (Pubitemid 40209169)
13. E. Nemeth, M.S. Tuttle, J. Powelson, M.B. Vaughn, A. Donovan, and D.M. Ward Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization Science 306 2004 2090 2093 (Pubitemid 40007660)
14. C. Pigeon, G. Ilyin, B. Courselaud, P. Leroyer, B. Turlin, and P. Brissot A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload J Biol Chem 276 2001 7811 7819
15. G. Nicolas, C. Chauvet, L. Viatte, J.L. Danan, X. Bigard, and I. Devaux The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation J Clin Invest 110 2002 1037 1044
16. G.J. Anderson, D.M. Frazer, S.J. Wilkins, E.M. Becker, K.N. Millard, and T.L. Murphy Relationship between intestinal iron-transporter expression, hepatic hepcidin levels and the control of iron absorption Biochem Soc Trans 30 2002 724 726 (Pubitemid 35001639)
17. E. Nemeth, S. Rivera, V. Gabayan, C. Keller, S. Taudorf, and B.K. Pedersen IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin J Clin Invest 113 2004 1271 1276 (Pubitemid 39069926)
18. J.S. Ferguson, D.R. Voelker, J.A. Ufnar, A.J. Dawson, and L.S. Schlesinger Surfactant protein D inhibition of human macrophage uptake of Mycobacterium tuberculosis is independent of bacterial agglutination J Immunol 168 2002 1309 1314 (Pubitemid 34094500)
19. K. Inaba, M. Inaba, N. Romani, H. Aya, M. Deguchi, and S. Ikehara Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor J Exp Med 176 1992 1693 1702
20. J.C. Chase, J. Celli, and C.M. Bosio Direct and indirect impairment of human dendritic cell function by virulent Francisella tularensis Schu S4 Infect Immun 77 2009 180 195
21. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408 (Pubitemid 34164012)
22. B.E. Garcia-Perez, R. Mondragon-Flores, and J. Luna-Herrera Internalization of Mycobacterium tuberculosis by macropinocytosis in non-phagocytic cells Microb Pathog 35 2003 49 55 (Pubitemid 36952282)
23. B. Rivas-Santiago, S.K. Schwander, C. Sarabia, G. Diamond, M.E. Klein-Patel, and R. Hernandez-Pando Human {beta}-defensin 2 is expressed and associated with Mycobacterium tuberculosis during infection of human alveolar epithelial cells Infect Immun 73 2005 4505 4511 (Pubitemid 41105604)
24. P. Mendez-Samperio, L. Alba, and A. Trejo Mycobacterium bovis-mediated induction of human beta-defensin-2 in epithelial cells is controlled by intracellular calcium and p38MAPK J Infect 54 2007 469 474 (Pubitemid 46577918)
25. P. Lee, H. Peng, T. Gelbart, L. Wang, and E. Beutler Regulation of hepcidin transcription by interleukin-1 and interleukin-6 Proc Natl Acad Sci U S A 102 2005 1906 1910 (Pubitemid 40261985)
26. P.J. Brennan Structure, function, and biogenesis of the cell wall of Mycobacterium Tuberculosis Tuberculosis (Edinb) 83 2003 91 97 (Pubitemid 36683556)
27. L.S. Schlesinger, S.R. Hull, and T.M. Kaufman Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages J Immunol 152 1994 4070 4079 (Pubitemid 24111079)
28. R.E. Geisel, K. Sakamoto, D.G. Russell, and E.R. Rhoades In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guerin is due principally to trehalose mycolates J Immunol 174 2005 5007 5015
29. G.S. Besra, and P.J. Brennan The mycobacterial cell wall: biosynthesis of arabinogalactan and lipoarabinomannan Biochem Soc Trans 25 1997 845 850 (Pubitemid 27416950)
30. J. Nigou, M. Gilleron, and G. Puzo Lipoarabinomannans: from structure to biosynthesis Biochimie 85 2003 153 166 (Pubitemid 36625990)
31. J.B. Torrelles, and L.S. Schlesinger Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host Tuberculosis (Edinb) 90 2010 84 93
32. V. Briken, S.A. Porcelli, G.S. Besra, and L. Kremer Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response Mol Microbiol 53 2004 391 403 (Pubitemid 38998163)
33. J.B. Torrelles, A.K. Azad, and L.S. Schlesinger Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors J Immunol 177 2006 1805 1816 (Pubitemid 44092518)
34. C. Villeneuve, M. Gilleron, I. Maridonneau-Parini, M. Daffe, C. Astarie-Dequeker, and G. Etienne Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process J Lipid Res 46 2005 475 483 (Pubitemid 43109784)
35. L.S. Schlesinger, A.K. Azad, J.B. Torrelles, E. Roberts, I. Vergne, and V. Deretic Determinants of phagocytosis, phagosome biogenesis and autophagy for Mycobacterium tuberculosis Weinheim S.H.E. Kaufmann, W.J. Britton, Handbook of tuberculosis immunology and cell biology 2008 Wiley-VCH Chichester 1 22 [John Wiley, distributor]
36. M. Rodriguez-Garcia, H. Oliva, N. Climent, F. Garcia, J.M. Gatell, and T. Gallart Human immature monocyte-derived dendritic cells produce and secrete alpha-defensins 1-3 J Leukoc Biol 82 2007 1143 1146 (Pubitemid 350133510)
37. X.M. Fang, Q. Shu, Q.X. Chen, M. Book, H.G. Sahl, and A. Hoeft Differential expression of alpha- and beta-defensins in human peripheral blood Eur J Clin Invest 33 2003 82 87 (Pubitemid 36051296)
38. P.K. Singh, H.P. Jia, K. Wiles, J. Hesselberth, L. Liu, and B.A. Conway Production of beta-defensins by human airway epithelia Proc Natl Acad Sci U S A 95 1998 14961 14966 (Pubitemid 29003739)
39. N. Reiling, C. Holscher, A. Fehrenbach, S. Kroger, C.J. Kirschning, and S. Goyert Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis J Immunol 169 2002 3480 3484
40. A. Bafica, C.A. Scanga, C.G. Feng, C. Leifer, A. Cheever, and A. Sher TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium Tuberculosis J Exp Med 202 2005 1715 1724 (Pubitemid 41815877)
41. F.B. Sow, G.R. Alvarez, R.P. Gross, A.R. Satoskar, L.S. Schlesinger, and B.S. Zwilling Role of STAT1, NF-kappaB, and C/EBPbeta in the macrophage transcriptional regulation of hepcidin by mycobacterial infection and IFN-gamma J Leukoc Biol 86 2009 1247 1258
42. J.B. Torrelles, A.K. Azad, L.N. Henning, T.K. Carlson, and L.S. Schlesinger Role of C-type lectins in mycobacterial infections Curr Drug Targets 9 2008 102 112 (Pubitemid 351461008)
43. C. Astarie-Dequeker, E.N. N'Diaye, V. Le Cabec, M.G. Rittig, J. Prandi, and I. Maridonneau-Parini The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages Infect Immun 67 1999 469 477 (Pubitemid 29059175)
44. P.B. Kang, A.K. Azad, J.B. Torrelles, T.M. Kaufman, A. Beharka, and E. Tibesar The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis J Exp Med 202 2005 987 999 (Pubitemid 41396898)
45. T.B. Geijtenbeek, S.J. Van Vliet, E.A. Koppel, M. Sanchez-Hernandez, C.M. Vandenbroucke-Grauls, and B. Appelmelk Mycobacteria target DC-SIGN to suppress dendritic cell function J Exp Med 197 2003 7 17 (Pubitemid 36110253)
46. L.P. Barker, K.M. George, S. Falkow, and P.L. Small Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages Infect Immun 65 1997 1497 1504 (Pubitemid 27146643)
47. D.M. Bowdish, K. Sakamoto, M.J. Kim, M. Kroos, S. Mukhopadhyay, and C.A. Leifer MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium Tuberculosis PLoS Pathog 5 2009 e1000474
48. K. Werninghaus, A. Babiak, O. Gross, C. Holscher, H. Dietrich, and E.M. Agger Adjuvanticity of a synthetic cord factor analogue for subunit Mycobacterium tuberculosis vaccination requires FcRgamma-Syk-Card9-dependent innate immune activation J Exp Med 206 2009 89 97
49. H. Schoenen, B. Bodendorfer, K. Hitchens, S. Manzanero, K. Werninghaus, and F. Nimmerjahn Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate J Immunol 184 2010 2756 2760
50. E. Ishikawa, T. Ishikawa, Y.S. Morita, K. Toyonaga, H. Yamada, and O. Takeuchi Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle J Exp Med 206 2009 2879 2888
51. K.A. Bodnar, N.V. Serbina, and J.L. Flynn Fate of Mycobacterium tuberculosis within murine dendritic cells Infect Immun 69 2001 800 809 (Pubitemid 32109542)
52. L. Tailleux, O. Neyrolles, S. Honore-Bouakline, E. Perret, F. Sanchez, and J.P. Abastado Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells J Immunol 170 2003 1939 1948 (Pubitemid 36197413)
53. M. Brinkmann, R. Teuffel, N. Laham, R. Ehrlich, P. Decker, and F.A. Lemonnier Expression of iron transport proteins divalent metal transporter-1, Ferroportin-1, HFE and transferrin receptor-1 in human monocyte-derived dendritic cells Cell Biochem Funct 25 2007 287 296 (Pubitemid 46827124)
54. J.L. Kramer, I. Baltathakis, O.S. Alcantara, and D.H. Boldt Differentiation of functional dendritic cells and macrophages from human peripheral blood monocyte precursors is dependent on expression of p21 (WAF1/CIP1) and requires iron Br J Haematol 117 2002 727 734 (Pubitemid 34539255)