Modulation of iron homeostasis in macrophages by bacterial intracellular pathogens

BMC Microbiology

Volumn 10, Issue , 2010, Pages

  Pan, Xin ^a   Tamilselvam, Batcha ^a   Hansen, Eric J ^a,b   Daefler, Simon ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIOXIDOREDUCTASE; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; OXIDOREDUCTASE; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; IRON; TFRC PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; FRANCISELLA TULARENSIS; GENE EXPRESSION; HOMEOSTASIS; HOST CELL; IRON METABOLISM; MACROPHAGE; MEMBRANE TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; REGULATORY MECHANISM; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TULAREMIA; ANIMAL; CELL GROWTH; CELL LINE; CYTOPLASM VESICLE; GENE EXPRESSION REGULATION; GENETICS; INTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY; UPREGULATION;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; SALMONELLA; SALMONELLA TYPHIMURIUM;

ANIMALS; CELL GROWTH PROCESSES; CELL LINE; CYTOPLASMIC VESICLES; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION; HOMEOSTASIS; INTRACELLULAR SPACE; IRON; MACROPHAGES; METABOLIC NETWORKS AND PATHWAYS; MICE; RECEPTORS, TRANSFERRIN; SALMONELLA TYPHIMURIUM; UP-REGULATION;

EID: 77949543589     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-10-64     Document Type: Article

References (56)

1. Intracellular innate resistance to bacterial pathogens. AL Radtke MX O'Riordan, Cell Microbiol 2006 8 1720 1729 10.1111/j.1462-5822.2006.00795.x 16939532
2. Iron-depletion limits intracellular bacterial growth in macrophages. P Paradkar I De Domenico N Durchfort I Zohn J Kaplan DM Ward, Blood 2008 112 866 874 10.1182/blood-2007-12-126854 18369153
3. The role of iron in infections with intracellular bacteria. HL Collins, Immunol Lett 2003 85 193 195 10.1016/S0165-2478(02)00229-8 12527227
4. The iron efflux protein ferroportin regulates the intracellular growth of Salmonella enterica. S Chlosta DS Fishman L Harrington EE Johnson MD Knutson M Wessling-Resnick BJ Cherayil, Infect Immun 2006 74 3065 3067 10.1128/IAI.74.5.3065-3067.2006 16622252
5. Natural resistance, iron and infection: a challenge for clinical medicine. JJ Bullen HJ Rogers PB Spalding CG Ward, J Med Microbiol 2006 55 251 258 10.1099/jmm.0.46386-0 16476787
6. Iron and microbial infection. UE Schaible SH Kaufmann, Nat Rev Microbiol 2004 2 946 953 10.1038/nrmicro1046 15550940
7. The Haber-Weiss reaction and mechanisms of toxicity. JP Kehrer, Toxicology 2000 149 43 50 10.1016/S0300-483X(00)00231-6 10963860
8. The macrophage: a cellular factory at the interphase between iron and immunity for the control of infections. I Theurl G Fritsche S Ludwiczek K Garimorth R Bellmann-Weiler G Weiss, Biometals 2005 18 359 367 10.1007/s10534-005-3710-1 16158228
9. Coxiella burnetii infection increases transferrin receptors on J774A. 1 cells. D Howe LP Mallavia, Infect Immun 1999 67 3236 3241 10377096
10. Ehrlichia chaffeensis and E. sennetsu, but not the human granulocytic ehrlichiosis agent, colocalize with transferrin receptor and up-regulate transferrin receptor mRNA by activating iron-responsive protein 1. RE Barnewall N Ohashi Y Rikihisa, Infect Immun 1999 67 2258 2265 10225882
11. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. DL Clemens MA Horwitz, J Exp Med 1996 184 1349 1355 10.1084/jem.184.4.1349 8879207
12. The Salmonella-containing vacuole-Moving with the times. O Steele-Mortimer, Curr Opin Microbiol 2008 11 38 45 10.1016/j.mib.2008.01.002 18304858
13. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. DL Clemens BY Lee MA Horwitz, Infect Immun 2004 72 3204 3217 10.1128/IAI.72.6.3204-3217.2004 15155622
14. Identification of Francisella tularensis genes affected by iron limitation. K Deng RJ Blick W Liu EJ Hansen, Infect Immun 2006 74 4224 4236 10.1128/IAI.01975-05 16790797
15. Characterization of the siderophore of Francisella tularensis and role of fslA in siderophore production. JT Sullivan EF Jeffery JD Shannon G Ramakrishnan, J Bacteriol 2006 188 3785 3795 10.1128/JB.00027-06 16707671
16. Genome-wide identification of Francisella tularensis virulence determinants. J Su J Yang D Zhao TH Kawula JA Banas JR Zhang, Infect Immun 2007 75 3089 3101 10.1128/IAI.01865-06 17420240
17. In vivo negative selection screen identifies genes required for Francisella virulence. DS Weiss A Brotcke T Henry JJ Margolis K Chan DM Monack, Proc Natl Acad Sci USA 2007 104 6037 6042 10.1073/pnas.0609675104 17389372
18. Proteomics analysis of the Francisella tularensis LVS response to iron restriction: induction of the F. tularensis pathogenicity island proteins IglABC. J Lenco M Hubalek P Larsson A Fucikova M Brychta A Macela J Stulik, FEMS Microbiol Lett 2007 269 11 21 10.1111/j.1574-6968.2006.00595.x 17227466
19. The effects of Francisella tularensis infection on iron metabolism in man. RS Pekarek KA Bostian PJ Bartelloni FM Calia WR Beisel, Am J Med Sci 1969 258 14 25 10.1097/00000441-196907000-00003 4894492
20. Iron uptake from lactoferrin and transferrin by Neisseria gonorrhoeae. WR McKenna PA Mickelsen PF Sparling DW Dyer, Infect Immun 1988 56 785 791 3126143
21. Iron metabolism in pathogenic bacteria. C Ratledge LG Dover, Annu Rev Microbiol 2000 54 881 941 10.1146/annurev.micro.54.1.881 11018148
22. Iron uptake mechanisms and their regulation in pathogenic bacteria. V Braun, Int J Med Microbiol 2001 291 67 79 10.1078/1438-4221-00103 11437341
23. The 58-kilodalton major virulence factor of Francisella tularensis is required for efficient utilization of iron. H Lindgren M Honn I Golovlev K Kadzhaev W Conlan A Sjostedt, Infect Immun 2009 77 4429 4436 10.1128/IAI.00702-09 19651867
24. Potential source of Francisella tularensis live vaccine strain attenuation determined by genome comparison. L Rohmer M Brittnacher K Svensson D Buckley E Haugen Y Zhou J Chang R Levy H Hayden M Forsman M Olson A Johansson R Kaul SI Miller, Infect Immun 2006 74 6895 6906 10.1128/IAI.01006-06 17000723
25. Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. S Hashim K Mukherjee M Raje SK Basu A Mukhopadhyay, J Biol Chem 2000 275 16281 16288 10.1074/jbc.275.21.16281 10821869
26. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. O Steele-Mortimer S Meresse JP Gorvel BH Toh BB Finlay, Cell Microbiol 1999 1 33 49 10.1046/j.1462-5822.1999.00003.x 11207539
27. Early endocytic Rabs: functional prediction to functional characterization. JC Simpson AT Jones, Biochem Soc Symp 2005 99 108 15649134
28. The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella typhimurium. M Nairz I Theurl S Ludwiczek M Theurl SM Mair G Fritsche G Weiss, Cell Microbiol 2007 9 2126 2140 10.1111/j.1462-5822.2007.00942.x 17466014
29. The labile iron pool: characterization, measurement, and participation in cellular processes(1). O Kakhlon ZI Cabantchik, Free Radic Biol Med 2002 33 1037 1046 10.1016/S0891-5849(02)01006-7 12374615
30. Cellular pool of transient ferric iron, chelatable by deferoxamine and distinct from ferritin, that is involved in oxidative cell injury. RJ Rothman A Serroni JL Farber, Mol Pharmacol 1992 42 703 710 1435746
31. Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). W Breuer S Epsztejn ZI Cabantchik, J Biol Chem 1995 270 24209 24215 10.1074/jbc.270.33.19330 7592626
32. A Salmonella virulence protein that inhibits cellular trafficking. K Uchiya MA Barbieri K Funato AH Shah PD Stahl EA Groisman, Embo J 1999 18 3924 3933 10.1093/emboj/18.14.3924 10406797
33. Identification of a pathogenicity island required for Salmonella survival in host cells. H Ochman FC Soncini F Solomon EA Groisman, Proc Natl Acad Sci USA 1996 93 7800 7804 10.1073/pnas.93.15.7800 8755556
34. The Steap proteins are metalloreductases. RS Ohgami DR Campagna A McDonald MD Fleming, Blood 2006 108 1388 1394 10.1182/blood-2006-02-003681 16609065
35. Iron homeostasis. NC Andrews PJ Schmidt, Annu Rev Physiol 2007 69 69 85 10.1146/annurev.physiol.69.031905.164337 17014365
36. Balancing acts: molecular control of mammalian iron metabolism. MW Hentze MU Muckenthaler NC Andrews, Cell 2004 117 285 297 10.1016/S0092-8674(04)00343-5 15109490
37. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. A Donovan A Brownlie Y Zhou J Shepard SJ Pratt J Moynihan BH Paw A Drejer B Barut A Zapata TC Law C Brugnara SE Lux GS Pinkus JL Pinkus PD Kingsley J Palis MD Fleming NC Andrews LI Zon, Nature 2000 403 776 781 10.1038/35001596 10693807
38. TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens. C Peyssonnaux AS Zinkernagel V Datta X Lauth RS Johnson V Nizet, Blood 2006 107 3727 3732 10.1182/blood-2005-06-2259 16391018
39. Cytokine-mediated regulation of iron transport in human monocytic cells. S Ludwiczek E Aigner I Theurl G Weiss, Blood 2003 101 4148 4154 10.1182/blood-2002-08-2459 12522003
40. Hepcidin expression and iron transport in alveolar macrophages. NB Nguyen KD Callaghan AJ Ghio DJ Haile F Yang, Am J Physiol Lung Cell Mol Physiol 2006 291 417 25 10.1152/ajplung.00484.2005 16648237
41. Constitutive hepcidin expression prevents iron overload in a mouse model of hemochromatosis. G Nicolas L Viatte DQ Lou M Bennoun C Beaumont A Kahn NC Andrews S Vaulont, Nat Genet 2003 34 97 101 10.1038/ng1150 12704388
42. Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity. LE Cole KL Elkins SM Michalek N Qureshi LJ Eaton P Rallabhandi N Cuesta SN Vogel, J Immunol 2006 176 6888 6899 16709849
43. A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. LR Devireddy C Gazin X Zhu MR Green, Cell 2005 123 1293 1305 10.1016/j.cell.2005.10.027 16377569
44. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. TH Flo KD Smith S Sato DJ Rodriguez MA Holmes RK Strong S Akira A Aderem, Nature 2004 432 917 921 10.1038/nature03104 15531878
45. Heme oxygenase-1: from bench to bedside. D Morse AM Choi, Am J Respir Crit Care Med 2005 172 660 670 10.1164/rccm.200404-465SO 15901614
46. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. LD Orozco MH Kapturczak B Barajas X Wang MM Weinstein J Wong J Deshane S Bolisetty Z Shaposhnik DM Shih A Agarwal AJ Lusis JA Araujo, Circ Res 2007 100 1703 1711 10.1161/CIRCRESAHA.107.151720 17495224
47. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. TF Byrd MA Horwitz, J Clin Invest 1989 83 1457 1465 10.1172/JCI114038 2496141
48. Aberrantly low transferrin receptor expression on human monocytes is associated with nonpermissiveness for Legionella pneumophila growth. TF Byrd MA Horwitz, J Infect Dis 2000 181 1394 1400 10.1086/315390 10762570
49. Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. RE Barnewall Y Rikihisa EH Lee, Infect Immun 1997 65 1455 1461 9119487
50. Gallium disrupts iron metabolism of mycobacteria residing within human macrophages. O Olakanmi BE Britigan LS Schlesinger, Infect Immun 2000 68 5619 5627 10.1128/IAI.68.10.5619-5627.2000 10992462
51. Intraphagosomal Mycobacterium tuberculosis acquires iron from both extracellular transferrin and intracellular iron pools. Impact of interferon-gamma and hemochromatosis. O Olakanmi LS Schlesinger A Ahmed BE Britigan, J Biol Chem 2002 277 49727 49734 10.1074/jbc.M209768200 12399453
52. Exochelins of Mycobacterium tuberculosis remove iron from human iron-binding proteins and donate iron to mycobactins in the M. tuberculosis cell wall. J Gobin MA Horwitz, J Exp Med 1996 183 1527 1532 10.1084/jem.183.4.1527 8666910
53. JH Miller, Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory 1972
54. Construction and characterization of a highly efficient Francisella shuttle plasmid. TM Maier A Havig M Casey FE Nano DW Frank TC Zahrt, Appl Environ Microbiol 2004 70 7511 7519 10.1128/AEM.70.12.7511-7519.2004 15574954
55. Identification of a NIPSNAP homologue as host cell target for Salmonella virulence protein SpiC. AH Lee M Papari S Daefler, Cell Microbiol 2002 4 739 750 10.1046/j.1462-5822.2002.00225.x 12427096
56. Fluorescence analysis of the labile iron pool of mammalian cells. S Epsztejn O Kakhlon H Glickstein W Breuer I Cabantchik, Anal Biochem 1997 248 31 40 10.1006/abio.1997.2126 9177722