Iron Overload Favors the Elimination of Leishmania infantum from Mouse Tissues through Interaction with Reactive Oxygen and Nitrogen Species

PLoS Neglected Tropical Diseases

Volumn 7, Issue 2, 2013, Pages

  Vale Costa, Sílvia ^a,b   Gomes Pereira, Sandra ^a,c   Teixeira, Carlos Miguel ^a   Rosa, Gustavo ^a   Rodrigues, Pedro Nuno ^a,b   Tomás, Ana ^a,b   Appelberg, Rui ^a,b   Gomes, Maria Salomé ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD19 ANTIGEN; GLYCOPROTEIN P 15095; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; IRON; MESSENGER RNA; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRYS; HISTOLOGY; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IRON OVERLOAD; LEISHMANIA INFANTUM; MOUSE; NATURAL KILLER T CELL; NICK END LABELING; PARASITE LOAD; PROTEIN CARBONYLATION;

EID: 84874764417     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002061     Document Type: Article

References (67)

1. WHO (2010) Control of the Leishmaniasis. WHO Technical Report Series 949: 1-186.
2. Ready PD, (2010) Leishmaniasis emergence in Europe. Euro Surveillance 15: 19505.
3. Nagill R, Kaur S, (2011) Vaccine candidates for leishmaniasis: a review. Int Immunopharmacol 11: 1464-1488.
4. Mondal S, Bhattacharya P, Ali N, (2010) Current diagnosis and treatment of visceral leishmaniasis. Expert Rev Anti Infect Ther 8: 919-944.
5. Maltezou HC, (2010) Drug resistance in visceral leishmaniasis. J Biomed Biotechnol 2010: 617521.
6. Ganz T, (2009) Iron in innate immunity: starve the invaders. Curr Opin Immunol 21: 63-67.
7. Nairz M, Schroll A, Sonnweber T, Weiss G, (2010) The struggle for iron- a metal at the host-pathogen interface. Cell Microbiol 12: 1691-1702.
8. Weinberg ED, (2009) Iron availability and infection. Biochim Biophys Acta 1790: 600-605.
9. Alford CE, King TE Jr, Campbell PA, (1991) Role of transferrin, transferrin receptors, and iron in macrophage listericidal activity. Journal Exp Med 174: 459-466.
10. Collins HL, Kaufmann SH, Schaible UE, (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.
11. Jiang X, Baldwin CL, (1993) Iron augments macrophage-mediated killing of Brucella abortus alone and in conjunction with interferon-gamma. Cell Immunol 148: 397-407.
12. Bisti S, Konidou G, Papageorgiou F, Milon G, Boelaert JR, et al. (2000) The outcome of Leishmania major experimental infection in BALB/c mice can be modulated by exogenously delivered iron. Eur J Immunol 30: 3732-3740.
13. Bisti S, Konidou G, Boelaert J, Lebastard M, Soteriadou K, (2006) The prevention of the growth of Leishmania major progeny in BALB/c iron-loaded mice: a process coupled to increased oxidative burst, the amplitude and duration of which depend on initial parasite developmental stage and dose. Microbes Infect 8: 1464-1472.
14. Gomes-Pereira S, Rodrigues PN, Appelberg R, Gomes MS, (2008) Increased susceptibility to Mycobacterium avium in hemochromatosis protein HFE-deficient mice. Infect Immun 76: 4713-4719.
15. Gomes MS, Boelaert JR, Appelberg R, (2001) Role of iron in experimental Mycobacterium avium infection. J Clin Virol 20: 117-122.
16. Gomes MS, Appelberg R, (1998) Evidence for a link between iron metabolism and Nramp1 gene function in innate resistance against Mycobacterium avium. Immunology 95: 165-168.
17. Fernandes SS, Nunes A, Gomes AR, de Castro B, Hider RC, et al. (2010) Identification of a new hexadentate iron chelator capable of restricting the intramacrophagic growth of Mycobacterium avium. Microbes Infect 12: 287-294.
18. Sereno D, Lemesre JL, (1997) Axenically cultured amastigote forms as an in vitro model for investigation of antileishmanial agents. Antimicrob Agents Chemother 41: 972-976.
19. Torrance JD, Bothwell TH (1980) Tissue iron stores. In: Cook JD, editor. Methods in Hematology. New York, NY: Churchill Livingstone Press. pp. 104-109.
20. Weinberg ED, (1999) The role of iron in protozoan and fungal infectious diseases. J Eukaryot Microbiol 46: 231-238.
21. Ahmed S, Colmenares M, Soong L, Goldsmith-Pestana K, Munstermann L, et al. (2003) Intradermal infection model for pathogenesis and vaccine studies of murine visceral leishmaniasis. Infect Immun 71: 401-410.
22. Carrion J, Nieto A, Iborra S, Iniesta V, Soto M, et al. (2006) Immunohistological features of visceral leishmaniasis in BALB/c mice. Parasite Immunol 28: 173-183.
23. Halliday JW, Searle J, (1996) Hepatic iron deposition in human disease and animal models. Biometals 9: 205-209.
24. Papanikolaou G, Pantopoulos K, (2005) Iron metabolism and toxicity. Toxicol Appl Pharmacol 202: 199-211.
25. Stanley AC, Engwerda CR, (2007) Balancing immunity and pathology in visceral leishmaniasis. Immunol Cell Biol 85: 138-147.
26. Murray HW, (2001) Tissue granuloma structure-function in experimental visceral leishmaniasis. Int J Exp Pathol 82: 249-267.
27. Mehta A, Shaha C, (2006) Mechanism of metalloid-induced death in Leishmania spp.: role of iron, reactive oxygen species, Ca2+, and glutathione. Free Radic Biol Med 40: 1857-1868.
28. Bahram S, Gilfillan S, Kuhn LC, Moret R, Schulze JB, et al. (1999) Experimental hemochromatosis due to MHC class I HFE deficiency: immune status and iron metabolism. PNAS 96: 13312-13317.
29. Zhou XY, Tomatsu S, Fleming RE, Parkkila S, Waheed A, et al. (1998) HFE gene knockout produces mouse model of hereditary hemochromatosis. PNAS 95: 2492-2497.
30. Bisti S, Soteriadou K, (2006) Is the reactive oxygen species-dependent-NF-kappaB activation observed in iron-loaded BALB/c mice a key process preventing growth of Leishmania major progeny and tissue-damage? Microbes Infect 8: 1473-1482.
31. Murray HW, Nathan CF, (1999) Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J Exp Med 189: 741-746.
32. Linares E, Giorgio S, Mortara RA, Santos CX, Yamada AT, et al. (2001) Role of peroxynitrite in macrophage microbicidal mechanisms in vivo revealed by protein nitration and hydroxylation. Free Radic Biol Med 30: 1234-1242.
33. Blos M, Schleicher U, Soares Rocha FJ, Meissner U, Rollinghoff M, et al. (2003) Organ-specific and stage-dependent control of Leishmania major infection by inducible nitric oxide synthase and phagocyte NADPH oxidase. Eur J Immunol 33: 1224-1234.
34. Stenger S, Thuring H, Rollinghoff M, Bogdan C, (1994) Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J Exp Med 180: 783-793.
35. Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, et al. (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375: 408-411.
36. Melby PC, Chandrasekar B, Zhao W, Coe JE, (2001) The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J Immunol 166: 1912-1920.
37. Fang FC, (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2: 820-832.
38. Hoepelman IM, Bezemer WA, Vandenbroucke-Grauls CM, Marx JJ, Verhoef J, (1990) Bacterial iron enhances oxygen radical-mediated killing of Staphylococcus aureus by phagocytes. Infect Immun 58: 26-31.
39. Melby PC, Yang YZ, Cheng J, Zhao W, (1998) Regional differences in the cellular immune response to experimental cutaneous or visceral infection with Leishmania donovani. Infect Immun 66: 18-27.
40. Halliwell B, Gutteridge JCM (2007) Free Radicals in Biology and Medicine. New York: Oxford University Press. 851 p.
41. Porto G, De Sousa M, (2007) Iron overload and immunity. World J Gastroenterol 13: 4707-4715.
42. Xiong S, She H, Takeuchi H, Han B, Engelhardt JF, et al. (2003) Signaling role of intracellular iron in NF-kappaB activation. J Biol Chem 278: 17646-17654.
43. Bonizzi G, Karin M, (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
44. Sacks D, Noben-Trauth N, (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2: 845-858.
45. Galleano M, Simontacchi M, Puntarulo S, (2004) Nitric oxide and iron: effect of iron overload on nitric oxide production in endotoxemia. Mol Aspects Med 25: 141-154.
46. Hida AI, Kawabata T, Minamiyama Y, Mizote A, Okada S, (2003) Saccharated colloidal iron enhances lipopolysaccharide-induced nitric oxide production in vivo. Free Radic Biol Med 34: 1426-1434.
47. Komarov AM, Mattson DL, Mak IT, Weglicki WB, (1998) Iron attenuates nitric oxide level and iNOS expression in endotoxin-treated mice. FEBS Lett 424: 253-256.
48. Weiss G, Werner-Felmayer G, Werner ER, Grunewald K, Wachter H, et al. (1994) Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J Exp Med 180: 969-976.
49. Barluzzi R, Saleppico S, Nocentini A, Boelaert JR, Neglia R, et al. (2002) Iron overload exacerbates experimental meningoencephalitis by Cryptococcus neoformans. J Neuroimmunol 132: 140-146.
50. Mencacci A, Cenci E, Boelaert JR, Bucci P, Mosci P, et al. (1997) Iron overload alters innate and T helper cell responses to Candida albicans in mice. J Infect Dis 175: 1467-1476.
51. McMahon-Pratt D, Alexander J, (2004) Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol Rev 201: 206-224.
52. Rolao N, Cortes S, Gomes-Pereira S, Campino L, (2007) Leishmania infantum: mixed T-helper-1/T-helper-2 immune response in experimentally infected BALB/c mice. Exp Parasitol 115: 270-276.
53. Cerf BJ, Jones TC, Badaro R, Sampaio D, Teixeira R, et al. (1987) Malnutrition as a risk factor for severe visceral leishmaniasis. J Infect Dis 156: 1030-1033.
54. Harrison LH, Naidu TG, Drew JS, de Alencar JE, Pearson RD, (1986) Reciprocal relationships between undernutrition and the parasitic disease visceral leishmaniasis. Rev Infect Dis 8: 447-453.
55. Anstead GM, Chandrasekar B, Zhao W, Yang J, Perez LE, et al. (2001) Malnutrition alters the innate immune response and increases early visceralization following Leishmania donovani infection. Infect Immun 69: 4709-4718.
56. Oppenheimer SJ, (2001) Iron and its relation to immunity and infectious disease. J Nutr 131: 616S-633S discussion 633S-635S.
57. Malafaia G, Marcon Lde N, Pereira Lde F, Pedrosa ML, Rezende SA, (2011) Leishmania chagasi: effect of the iron deficiency on the infection in BALB/c mice. Exp Parasitol 127: 719-723.
58. Murray HW, Granger AM, Teitelbaum RF, (1991) Gamma interferon-activated human macrophages and Toxoplasma gondii, Chlamydia psittaci, and Leishmania donovani: antimicrobial role of limiting intracellular iron. Infect Immun 59: 4684-4686.
59. Borges VM, Vannier-Santos MA, de Souza W, (1998) Subverted transferrin trafficking in Leishmania-infected macrophages. Parasitol Res 84: 811-822.
60. Das NK, Biswas S, Solanki S, Mukhopadhyay CK, (2009) Leishmania donovani depletes labile iron pool to exploit iron uptake capacity of macrophage for its intracellular growth. Cell Microbiol 11: 83-94.
61. Segovia M, Navarro A, Artero JM, (1989) The effect of liposome-entrapped desferrioxamine on Leishmania donovani in vitro. Ann Trop Med Parasitol 83: 357-360.
62. Soteriadou K, Papavassiliou P, Voyiatzaki C, Boelaert J, (1995) Effect of iron chelation on the in-vitro growth of Leishmania promastigotes. J Antimicrob Chemother 35: 23-29.
63. Wilson ME, Vorhies RW, Andersen KA, Britigan BE, (1994) Acquisition of iron from transferrin and lactoferrin by the protozoan Leishmania chagasi. Infect Immun 62: 3262-3269.
64. Zarley JH, Britigan BE, Wilson ME, (1991) Hydrogen peroxide-mediated toxicity for Leishmania donovani chagasi promastigotes. Role of hydroxyl radical and protection by heat shock. J Clin Invest 88: 1511-1521.
65. Wyllie S, Cunningham ML, Fairlamb AH, (2004) Dual action of antimonial drugs on thiol redox metabolism in the human pathogen Leishmania donovani. J Biol Chem 279: 39925-39932.
66. Sen R, Saha P, Sarkar A, Ganguly S, Chatterjee M, (2010) Iron enhances generation of free radicals by Artemisinin causing a caspase-independent, apoptotic death in Leishmania donovani promastigotes. Free Radic Res 44: 1289-1295.
67. Wong IL, Chow LM, (2006) The role of Leishmania enriettii multidrug resistance protein 1 (LeMDR1) in mediating drug resistance is iron-dependent. Mol Biochem Parasitol 150: 278-287.