Attenuated inflammatory responses in hemochromatosis reveal a role for iron in the regulation of macrophage cytokine translation

Journal of Immunology

Volumn 181, Issue 4, 2008, Pages 2723-2731

  Wang, Lijian ^a,c   Johnson, Erin E ^c   Hai, Ning Shi ^a,b   Walker, W Allan ^a,b,c   Wessling Resnick, Marianne ^c   Cherayil, Bobby J ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FERROPORTIN; INTERLEUKIN 6; IRON; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CATION TRANSPORT PROTEIN; HFE PROTEIN, MOUSE; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; METAL TRANSPORTING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL LEVEL; CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTEROCOLITIS; GENE OVEREXPRESSION; HEMOCHROMATOSIS; HOMEOSTASIS; IMMUNE FUNCTION TEST; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; IRON CHELATION; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; MUTANT; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; TRANSCRIPTION INITIATION; UPREGULATION; WILD TYPE; ANIMAL; ANIMAL SALMONELLOSIS; C57BL MOUSE; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; PERITONEUM MACROPHAGE; PHYSIOLOGY; PROTEIN SYNTHESIS; SALMONELLA TYPHIMURIUM;

ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE; CYTOKINES; ENTEROCOLITIS; HEMOCHROMATOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNITY, NATURAL; INFLAMMATION MEDIATORS; IRON; MACROPHAGES, PERITONEAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN BIOSYNTHESIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM;

EID: 53149123286     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.4.2723     Document Type: Article

References (56)

1. Schaible, U. E., and S. H. Kaufmann. 2004. Iron and microbial infection. Nat. Rev. Microbiol. 2: 946-953.
2. Gangaidzo, I. T., V. M. Moyo, E. Mvundura, G. Aggrey, N. L. Murphree, H. Khumalo, T. Saungwenre, I. I. Kasvosve, Z. A. Gomo, T. Rouault, et al. 2001. Association of pulmonary tuberculosis with increased dietary iron. J. Infect. Dis. 184: 936-939.
3. Gordeuk, V. R., C. E. McLaren, A. P. MacPhail, G. Deichsel, and T. H. Bothwell. 1996. Associations of iron overload in Africa with hepatocellular carcinoma and tuberculosis: Strachan's 1929 thesis revisited. Blood 87: 3470-3476.
4. Magnus, S. A., I. R. Hambleton, F. Moosdeen, and G. R. Serjeant. 1999. Recurrent infections in homozygous sickle cell disease. Arch. Dis. Child 80: 537-541.
5. Moyo, V. M., I. T. Gangaidzo, V. R. Gordeuk, C. F. Kiire, and A. P. Macphail. 1997. Tuberculosis and iron overload in Africa: a review. Centr. Afr. J. Med. 43: 334-339.
6. Wanachiwanawin, W. 2000. Infections in E-beta thalassemia. J. Pediatr. Hematol. Oncol. 22: 581-587.
7. Murray, M. J., A. B. Murray, M. B. Murray, and C. J. Murray. 1978. The adverse effect of iron repletion on the course of certain infections. Br. Med. J. 2: 1113-1115.
8. Nyakeriga, A. M., M. Troye-Blomberg, J. R. Dorfman, N. D. Alexander, R. Back, M. Kortoak, A. K. Chemtai, K. Marsh, and T. N. Williams. 2004. Iron deficiency and malaria among children living on the coast of Kenya. J. Infect Dis. 190: 439-447.
9. Sazawal, S., R. E. Black, M. Ramsan, H. M. Chwaya, R. J. Stoltzfus, A. Dutta, U. Dhingra, I. Kabole, S. Deb, M. K. Othman, and F. M. Kabole. 2006. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomized, placebo-controlled trial. Lancet 367: 133-143.
10. Alford, C. E., T. E. King, Jr., and P. A. Campbell. 1991. Role of transferrin, transferrin receptors, and iron in macrophage listericidal activity. J. Exp. Med. 174: 459-466.
11. Collins, H. L., S. H. E. Kaufmann, and U. E. Schaible. 2002. Iron chelation via deferoxamine exacerbates experimental salmonellosis via inhibition of the nicotinamide adenine dinucleotide phosphate oxidase-dependent respiratory burst. J. Immunol. 168: 3458-3463.
12. Puschmann, M., and A. M. Ganzoni. 1977. Increased resistance of iron-deficient mice to Salmonella infection. Infect. Immun. 17: 663-664.
13. Roy, M. F., N. Riendeau, C. Bedard, P. Helie, G. Min-Oo, K. Turcotte, P. Gros, F. Canonne-Hergaux, and D. Malo. 2007. Pyruvate kinase deficiency confers susceptibility to Salmonella typhimurium infection in mice. J. Exp. Med. 204: 2949-2961.
14. Pietrangelo, A. 2006. Hereditary hemochromatosis. Annu. Rev. Nutr. 26: 251-270.
15. Feder, J. N., A. Gnirke, W. Thomas, Z. Tsuchihashi, D. A. Ruddy, A. Basava, F. Dormishian, R. Domingo, Jr., M. C. Ellis, A. Fullan, et al. 1996. A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat. Genet. 13: 399-408.
16. Andrews, N. C. 2007. Iron homeostasis. Annu. Rev. Physiol. 69: 69-85.
17. Nemeth, E., and T. Ganz. 2006. Regulation of iron metabolism by hepcidin. Annu. Rev. Nutr. 26: 323-342.
18. Goswami, T., and N. C. Andrews. 2006. Hereditary hemochromatosis protein, HFE, interaction with transferrin receptor 2 suggests a molecular mechanism for mammalian iron sensing. J. Biol. Chem. 281: 28494-28498.
19. Nemeth, E., M. S. Tuttle, J. Powelson, M. B. Vaughn, A. Donovan, D. M. Ward, T. Ganz, and J. Kaplan. 2004. Hepcidin regulates cellular iron efflux by binding ferroportin and inducing its degradation. Science 306: 2090-2093.
20. Ahmad, K. A., J. R Ahmann, M. C. Migas, A. Waheed, R. S. Britton, B. R. Bacon, W. S. Sly, and R. E. Fleming. 2002. Decreased liver hepcidin expression in the Hfe knock-out mouse. Blood Cells Mol. Dis. 29: 361-366.
21. Bahram, S., S. Gilfillan, L. C. Kuhn, R. Moret, J. B. Schulze, A. Lebeau, and K. Schumann. 1999. Experimental hemochromatosis due to MHC class I HFE deficiency: immune status and iron metabolism. Proc. Natl. Acad. Sci. USA 96: 13312-13317.
22. Levy, J. E., L. K. Montross, D. E. Cohen, M. D. Fleming, and N. C. Andrews. 1999. The C282Y mutation causing hereditary hemochromatosis does not produce a null allele. Blood 94: 9-11.
23. Zhou, X. Y., S. Tomatsu, R. E. Fleming, S. Parkkila, A. Waheed, J. Jiang, Y. Fei, E. M. Brundt, D. A. Ruddy, C. E. Prass, et al. 1998. HFE gene knock-out produces a mouse model of hereditary hemochromatosis. Proc. Natl. Acad. Sci. USA 95: 2492-2497.
24. Bullen, J. J., P. B. Spalding, C. G. Ward, and J. M. Gutteridge. 1991. Hemochromatosis, iron and septicemia caused by Vibrio vulnificus. Arch. Intern. Med. 151: 1606-1609.
25. Doherty, C. P. 2007. Host-pathogen interactions: the role of iron. J. Nutr. 137: 1341-1344.
26. Gerhard, G. S., K. A. Levin, G. J. Price, M. M. Wojnar, M. J. Chorney, and D. A. Belchis. 2001. Vibrio vulnificus septicemia in a patient with the hemochromatosis HFE C282Y mutation. Arch. Pathol. Lab. Med. 125: 1107-1109.
27. Moalem, S., E. D. Weinberg, and M. E. Percy. 2004. Hemochromatosis and the enigma of misplaced iron: implications for infectious disease and survival. Biometals 17: 135-139.
28. Chlosta, S., D. S. Fishman, L. Harrington, E. E. Johnson, M. D. Knutson, M. Wessling-Resnick, and B. J. Cherayil. 2006. The iron efflux protein ferroportin regulates the intracellular growth of Salmonella enterica. Infect. Immun. 74: 3065-3067.
29. Nairz, M., I. Theuri, S. Ludwiczek, M. Theuri, S. M. Mair, G. Fritsche, and G. Weiss. 2007. The coordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella typhimurium. Cell Microbiol. 9: 2126-2140.
30. Olakanmi, O., L. S. Schlesinger, and B. E. Britigan. 2007. Hereditary hemochromatosis results in decreased iron acquisition and growth by Mycobacterium tuberculosis within human macrophages. J. Leukocyte Biol. 81: 195-204.
31. Paradkar, P., I. De Domenico, N. Durchfort, I. Zohn, J. Kaplan, and D. M. Ward. 2008. Iron-depletion limits intracellular bacterial growth in macrophages. Blood. In press.
32. Barthel, M., S. Hapfelmeier, L. Quintanilla-Martínez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Rüssmann, and W.-D. Hardt. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71: 2839-2858.
33. Rhee, S. J., W. A. Walker, and B. J. Cherayil. 2005. Developmentally regulated intestinal expression of IFN and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 175: 1127-1136.
34. Li, Q., and B. J. Cherayil. 2003. Role of Toll-like receptor 4 in macrophage activation and tolerance during Salmonella enterica serovar Typhimurium infection. Infect. Immun. 71: 4873-4882.
35. Yu, C., B. York, S. Wang, Q. Feng, J. Xu, and B. W. O'Malley. 2007. An essential function of the SRC-3 co-activator in suppression of cytokine mRNA translation and inflammatory response. Mol. Cell. 25: 765-778.
36. Harrington, L., C. V. Srikanth, R. Antony, H. N. Shi, and B. J. Cherayil. 2007. A role for natural killer cells in intestinal inflammation caused by infection with Salmonella enterica serovar Typhimurium. FEMS Immunol. Med. Microbiol. 51: 372-380.
37. Rydström, A., and M. J. Wick. 2007. Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection. J. Immunol. 178: 5789-5801.
38. Wick, M. J. 2004. Living in the danger zone: innate immunity to Salmonella. Curr. Opin. Microbiol. 7: 51-57.
39. Royle, M. C., S. Tötemeyer, L. C. Alldridge, D. J. Maskell, and C. E. Bryant. 2003. Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella typhimurium is a critical but not exclusive event leading to macrophage responses. J. Immunol. 170: 5445-5454.
40. Weiss, D. S., B. Raupach, K. Takeda, S. Akira, and S. Zychlinsky. 2004. Toll-like receptors are temporally involved in host defense. J. Immunol. 172: 4463-4469.
41. Knutson, M. D., M. Oukka, L. M. Koss, F. Aydemir, and M. Wessling-Resnick. 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.
42. Brown, J. X., P. D. Buckett, and M. Wessling-Resnick. 2004. Identification of small molecule inhibitors that distinguish between transferrin bound iron uptake and transferrin mediated iron transport. Chem. Biol. 11: 407-416.
43. Kakhlon, O., and Z. L. Cabantchik. 2002. The labile iron pool: characterization, measurement and participation in cellular processes. Free Radic. Biol. Med. 33: 1037-1046.
44. Simunek, T., C. Boer, R. A. Bouwman, R. Vlasblom, A. M. Versteilen, M. Sterba, V. Gersl, R. Hrdina, P. Ponka, J. J. de Lange, et al. 2005. SIH, a novel lipophilic iron chelator, protects H9c2 cardiomyoblasts from oxidative stress-induced mitochondrial injury and cell death. J. Mol. Cell. Cardiol. 39: 345-354.
45. Templeton, D. M., and Y. Liu. 2003. Genetic regulation of cell function in response to iron overload or chelation. Biochim. Biophys. Acta 1619: 113-124.
46. Rouault, T. A. 2006. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2: 406-414.
47. Sanchez, M., B. Galy, M. U. Muckenthaler, and M. W. Hentze. 2007. Iron-regulatory proteins limit hypoxia-inducible factor-2α expression in iron deficiency. Nat. Struct. Mol. Biol. 14: 420-426.
48. Anderson, P. 2008. Post-transcriptional control of cytokine production. Nat. Immunol. 9: 353-359.
49. Arnold, J. W., D. W. Niesel, C. R. Annable, C. B. Hess, M. Asuncion, Y. J. Cho, J. W. Peterson, and G. R. Klimpel. 1993. TNFα mediates the early pathology in Salmonella infection of the gastrointestinal tract. Microb. Pathog. 14: 217-227.
50. Jones, S. A. 2005. Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol. 175: 3463-3468.
51. Nadeau, W. J., T. G. Pistole, and B. A. McCormick. 2002. Polymorphonuclear leukocyte migration across model intestinal epithelia enhances Salmonella typhimurium killing via the epithelial derived cytokine, IL-6. Microbes Infect. 4: 1379-1387.
52. Vazquez-Torres, A., G. Fantuzzi, C. K. Edwards, III, C. A. Dinarello, and F. C. Fang. 2001. Defective localization of the NADPH phagocyte oxidase to Salmonella-containing phagosomes in TNF p55 receptor-deficient mice. Proc. Natl. Acad. Sci. USA 98: 2561-2565.
53. Gordeuk, V. R., S. Ballou, G. Lozanski, and G. M. Rittenham. 1992. Decreased concentrations of TNFα in supernatants of monocytes from homozygotes for hereditary hemochromatosis. Blood 79: 1855-1860.
54. Lathem, W. A., P. A. Price, V. L. Miller, and W. E. Goldman. 2007. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315: 509-513.
55. Drakesmith, H., L. M. Schimanski, E. Ormerod, A. T. Merryweather-Clarke, V. Viprakasit, J. P. Edwards, E. Sweetland, J. M. Bastin, D. Cowley, Y. Chinthammitr, et al. 2005. Resistance to hepcidin is conferred by hemochromatosis-associated mutations of ferroportin. Blood 106: 1092-1097.
56. Tanno, T., N. V. Bhanu, P. A. Oneal, S. H. Goh, P. Staker, Y. T. Lee, J. W. Moroney, C. H. Reed, N. L. Luban, R. H. Wang, et al. 2007. High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nat. Med. 13: 1096-1101.