Human classical monocytes control the intracellular stage of leishmania braziliensis by reactive oxygen species

Journal of Infectious Diseases

Volumn 209, Issue 8, 2014, Pages 1288-1296

  Novais, Fernanda O ^a   Nguyen, Ba T ^a   Beiting, Daniel P ^a   Carvalho, Lucas P ^b   Glennie, Nelson D ^a   Passos, Sara ^b   Carvalho, Edgar M ^b   Scott, Phillip ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b FEDERAL UNIVERSITY OF BAHIA   (Brazil)

Author keywords

amastigotes; human monocytes; Leishmania braziliensis; nitric oxide; reactive oxygen species

Indexed keywords

GAMMA INTERFERON; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

AMASTIGOTE; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; LEISHMANIA BRAZILIENSIS; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; SKIN LEISHMANIASIS;

AMASTIGOTES; HUMAN MONOCYTES; LEISHMANIA BRAZILIENSIS; NITRIC OXIDE; REACTIVE OXYGEN SPECIES;

ANIMALS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, CUTANEOUS; MONOCYTES; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENNSYLVANIA; REACTIVE OXYGEN SPECIES;

EID: 84897420698     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jiu013     Document Type: Article

References (42)

1. Goncalves R, Zhang X, Cohen H, Debrabant A, Mosser D. Platelet activation attracts a subpopulation of effector monocytes to sites of Leishmania major infection. J Exp Med 2011; 208:1253-65.
2. Kaye P, Scott P. Leishmaniasis: Complexity at the host-pathogen interface. Nat Rev Microbiol 2011; 9:604-15.
3. Sacks D, Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2002; 2:845-58.
4. Stenger S, Thüring H, Röllinghoff M, Bogdan C. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J Exp Med 1994; 180:783-93.
5. Fang F, Nathan C. Man is not a mouse: Reply. J Leukoc Biol 2007; 81:580.
6. Schneemann M, Schoeden G. Macrophage biology and immunology: Man is not a mouse. J Leukoc Biol 2007; 81.
7. Schneemann M, Schoedon G, Hofer S, Blau N, Guerrero L, Schaffner A. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis 1993; 167:1358-63.
8. Gantt K, Goldman T, McCormick M, et al. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J Immunol 2001; 167:893-901.
9. Muñoz-Fernández M, Fernández M, Fresno M. Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-Alpha and IFN-gamma through a nitric oxide-dependent mechanism. Immunol Lett 1992; 33:35-40.
10. Denis M. Interferon-gamma-Treated murine macrophages inhibit growth of tubercle bacilli via the generation of reactive nitrogen intermediates. Cell Immunol 1991; 132:150-7.
11. Brüne B, Dehne N, Grossmann N, et al. Redox control of inflammation in macrophages. Antioxid Redox Signal 2013; 19:595-637.
12. Chang H, Thalhofer C, Duerkop B, et al. Oxidant generation by single infected monocytes after short-Term fluorescence labeling of a protozoan parasite. Infect Immun 2007; 75:1017-24.
13. Channon J, Roberts M, Blackwell J. A study of the differential respiratory burst activity elicited by promastigotes and amastigotes of Leishmania donovani in murine resident peritoneal macrophages. Immunology 1984; 53:345-55.
14. Novais F, Santiago R, Báfica A, et al. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol 2009; 183:8088-98.
15. Zarley J, Britigan B, Wilson M. Hydrogen peroxide-mediated toxicity for Leishmania donovani chagasi promastigotes. Role of hydroxyl radical and protection by heat shock. J Clin Invest 1991; 88:1511-21.
16. Rocha F, Schleicher U,Mattner J, Alber G, Bogdan C. Cytokines, signaling pathways, and effector molecules required for the control of Leishmania (Viannia) braziliensis in mice. Infect Immun 2007; 75:3823-32.
17. Khouri R, Bafica A, Silva M, et al. IFN-beta impairs superoxidedependent parasite killing in human macrophages: Evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J Immunol 2009; 182: 2525-31.
18. Murray H, Cartelli D. Killing of intracellular Leishmania donovani by human mononuclear phagocytes. Evidence for oxygen-dependent and-independent leishmanicidal activity. J Clin Invest 1983; 72:32-44.
19. Mallinson D, Coombs G. Interaction of leishmania metacyclics with macrophages. Int J Parasitol 1989; 19:647-56.
20. Pham N-K, Mouriz J, Kima P. Leishmania pifanoi amastigotes avoid macrophage production of superoxide by inducing heme degradation. Infect Immun 2005; 73:8322-33.
21. Novais FO, Carvalho LP, Graff JW, et al. Cytotoxic T cells mediate pathology and metastasis in cutaneous leishmaniasis. PLoS Pathog 2013; 9:e1003504.
22. Späth G, Beverley S. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp Parasitol 2001; 99:97-103.
23. Uzonna JE, Joyce KL, Scott P. Low dose Leishmania major promotes a transient T helper cell type 2 response that is down-regulated by interferon gamma-producing CD8+ T cells. J Exp Med 2004; 199:1559-66.
24. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov J. GenePattern 2.0. Nat Genet 2006; 38:500-1.
25. Richardson M, Ayliffe M, Helbert M, Davies E. A simple flow cytometry assay using dihydrorhodamine for the measurement of the neutrophil respiratory burst in whole blood: Comparison with the quantitative nitrobluetetrazolium test. J Immunol Methods 1998; 219:187-93.
26. Passlick B, Flieger D, Ziegler-Heitbrock H. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 1989; 74:2527-34.
27. Wong K, Tai J, Wong W-C, et al. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 2011; 118:31.
28. Zawada A, Rogacev K, Rotter B, et al. SuperSAGE evidence for CD14++ CD16+ monocytes as a third monocyte subset. Blood 2011; 118:61.
29. Ziegler-Heitbrock L, Ancuta P, Crowe S, et al. Nomenclature of monocytes and dendritic cells in blood. Blood 2010; 116:80.
30. Bokoch G, Zhao T. Regulation of the phagocyte NADPH oxidase by Rac GTPase. Antioxid Redox Signal 2006; 8:1533-48.
31. Da Silva R, Hall B, Joiner K, Sacks D. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J Immunol 1989; 143:617-22.
32. Giudice A, Vendrame C, Bezerra C, et al. Macrophages participate in host protection and the disease pathology associated with Leishmania braziliensis infection. BMC Infect Dis 2012; 12:75.
33. Haidaris C, Bonventre P. A role for oxygen-dependent mechanisms in killing of Leishmania donovani tissue forms by activated macrophages. J Immunol 1982; 129:850-5.
34. Van Assche T, Deschacht M, da Luz R, Maes L, Cos P. Leishmania-macrophage interactions: Insights into the redox biology. Free Radic Biol Med 2011; 51:337-51.
35. Kröncke K, Fehsel K, Kolb-Bachofen V. Inducible nitric oxide synthase in human diseases. Clin Exp Immunol 1998; 113:147-56.
36. Annane D, Sanquer S, Sébille V, et al. Compartmentalised inducible nitric-oxide synthase activity in septic shock. Lancet 2000; 355: 1143-8.
37. Blos M, Schleicher U, Soares Rocha F, Meissner U, Röllinghoff M, Bogdan C. Organ-specific and stage-dependent control of Leishmania major infection by inducible nitric oxide synthase and phagocyte NADPH oxidase. Eur J Immunol 2003; 33:1224-34.
38. Gonzalez-Lombana C, Gimblet C, Bacellar O, et al. IL-17 mediates immunopathology in the absence of IL-10 following Leishmania major infection. PLoS Pathog 2013; 9:e1003243.
39. Ellery P, Tippett E, Chiu Y-L, et al. The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 2007; 178:6581-9.
40. Fingerle G, Pforte A, Passlick B, Blumenstein M, Ströbel M, Ziegler-Heitbrock H. The novel subset of CD14+/CD16+ blood monocytes is expanded in sepsis patients. Blood 1993; 82:3170-6.
41. Jaworowski A, Kamwendo D, Ellery P, et al. CD16+ monocyte subset preferentially harbors HIV-1 and is expanded in pregnant Malawian women with Plasmodium falciparum malaria and HIV-1 infection. J Infect Dis 2007; 196:38-42.
42. Soares G, Barral A, Costa J, Barral-Netto M, VanWeyenbergh J. CD16+ monocytes in human cutaneous leishmaniasis: Increased ex vivo levels and correlation with clinical data. J Leukoc Biol 2006; 79:36-9.