Characterization of Neutrophil Function in Human Cutaneous Leishmaniasis Caused by Leishmania braziliensis

PLoS Neglected Tropical Diseases

Volumn 10, Issue 5, 2016, Pages

  Conceição, Jacilara ^a   Davis, Richard ^b   Carneiro, Pedro Paulo ^a   Giudice, Angela ^a   Muniz, Aline C ^a   Wilson, Mary E ^b,c,d   Carvalho, Edgar M ^a,e,f   Bacellar, Olívia ^a,e  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e Instituto Nacional de Ciência e Tecnologia de Doenças Tropicais INCT DT CNPq MCT   (Brazil)

^f INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; CD66B ANTIGEN; CELL ANTIGEN; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 8; L SELECTIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CD66 ANTIGENS; CELL ADHESION MOLECULE; CHEMOKINE; LEUKOCYTE ANTIGEN; TUMOR NECROSIS FACTOR;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LEISHMANIA BRAZILIENSIS; LEUKOCYTE ACTIVATION; NEUTROPHIL; PARASITE LOAD; PARASITE VIABILITY; PHAGOCYTOSIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SKIN LEISHMANIASIS; BIOSYNTHESIS; IMMUNOLOGY; LEISHMANIASIS, CUTANEOUS; METABOLISM; PHYSIOLOGY;

ANTIGENS, CD; CELL ADHESION MOLECULES; CHEMOKINES; HUMANS; L-SELECTIN; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, CUTANEOUS; NEUTROPHILS; PHAGOCYTOSIS; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84971592100     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004715     Document Type: Article

References (63)

1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One7: e35671. doi: 10.1371/journal.pone.003567122693548
2. Bacellar O, Lessa H, Schriefer A, Machado P, Ribeiro de Jesus A, et al. (2002) Up-regulation of Th1-type responses in mucosal leishmaniasis patients. Infect Immun70: 6734–6740. 12438348
3. Bottrel RL, Dutra WO, Martins FA, Gontijo B, Carvalho E, et al. (2001) Flow cytometric determination of cellular sources and frequencies of key cytokine-producing lymphocytes directed against recombinant LACK and soluble Leishmania antigen in human cutaneous leishmaniasis. Infect Immun69: 3232–3239. 11292745
4. Ribeiro-de-Jesus A, Almeida RP, Lessa H, Bacellar O, Carvalho EM, (1998) Cytokine profile and pathology in human leishmaniasis. Braz J Med Biol Res31: 143–148. 9686192
5. Antonelli LR, Dutra WO, Almeida RP, Bacellar O, Carvalho EM, et al. (2005) Activated inflammatory T cells correlate with lesion size in human cutaneous leishmaniasis. Immunol Lett101: 226–230. 16083969
6. Follador I, Araujo C, Bacellar O, Araujo CB, Carvalho LP, et al. (2002) Epidemiologic and immunologic findings for the subclinical form of Leishmania braziliensis infection. Clin Infect Dis34: E54–58. 12015707
7. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science321: 970–974. doi: 10.1126/science.115919418703742
8. Beil WJ, Meinardus-Hager G, Neugebauer DC, Sorg C, (1992) Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J Leukoc Biol52: 135–142. 1506767
9. Muller K, van Zandbergen G, Hansen B, Laufs H, Jahnke N, et al. (2001) Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Med Microbiol Immunol190: 73–76. 11770115
10. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A, (2012) Neutrophil function: from mechanisms to disease. Annu Rev Immunol30: 459–489. doi: 10.1146/annurev-immunol-020711-07494222224774
11. Charmoy M, Brunner-Agten S, Aebischer D, Auderset F, Launois P, et al. (2010) Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS Pathog6: e1000755. doi: 10.1371/journal.ppat.100075520140197
12. Hilda JN, Narasimhan M, Das SD, (2014) Neutrophils from pulmonary tuberculosis patients show augmented levels of chemokines MIP-1alpha, IL-8 and MCP-1 which further increase upon in vitro infection with mycobacterial strains. Hum Immunol75: 914–922. doi: 10.1016/j.humimm.2014.06.02024994463
13. Pham CT, (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol6: 541–550. 16799473
14. Mollinedo F, Janssen H, de la Iglesia-Vicente J, Villa-Pulgarin JA, Calafat J, (2010) Selective fusion of azurophilic granules with Leishmania-containing phagosomes in human neutrophils. J Biol Chem285: 34528–34536. doi: 10.1074/jbc.M110.12530220801889
15. Tacchini-Cottier F, Zweifel C, Belkaid Y, Mukankundiye C, Vasei M, et al. (2000) An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J Immunol165: 2628–2636. 10946291
16. Sousa LM, Carneiro MB, Resende ME, Martins LS, Dos Santos LM, et al. (2014) Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite Immunol36: 13–31. doi: 10.1111/pim.1207824102495
17. Charmoy M, Megnekou R, Allenbach C, Zweifel C, Perez C, et al. (2007) Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol82: 288–299. 17449725
18. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol83: 64–70. 17884993
19. Charmoy M, Milon G, Tacchini-Cottier F, Tacchini-Cottier F, Van Zandbergen G, (2011) Role of the neutrophils in the early shaping of the Leishmania major specific immune response in experimental murine cutaneous Leishmaniasis. In: Neutrophils in infectious diseases: Betham e Books. pp. 49–58.
20. Gueirard P, Laplante A, Rondeau C, Milon G, Desjardins M, (2008) Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell Microbiol10: 100–111. 17651446
21. Falcao SA, Weinkopff T, Hurrell BP, Celes FS, Curvelo RP, et al. (2015) Exposure to Leishmania braziliensis triggers neutrophil activation and apoptosis. PLoS Negl Trop Dis9: e0003601. doi: 10.1371/journal.pntd.000360125756874
22. Carlsen ED, Jie Z, Liang Y, Henard CA, Hay C, et al. (2015) Interactions between Neutrophils and Leishmania braziliensis Amastigotes Facilitate Cell Activation and Parasite Clearance. J Innate Immun7: 354–363. doi: 10.1159/00037392325766649
23. Laufs H, Muller K, Fleischer J, Reiling N, Jahnke N, et al. (2002) Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors. Infect Immun70: 826–835. 11796617
24. Tavares NM, Araujo-Santos T, Afonso L, Nogueira PM, Lopes UG, et al. (2014) Understanding the mechanisms controlling Leishmania amazonensis infection in vitro: the role of LTB4 derived from human neutrophils. J Infect Dis210: 656–666. doi: 10.1093/infdis/jiu15824634497
25. Afonso L, Borges VM, Cruz H, Ribeiro-Gomes FL, DosReis GA, et al. (2008) Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J Leukoc Biol84: 389–396. doi: 10.1189/jlb.010801818483206
26. Novais FO, Santiago RC, Bafica A, Khouri R, Afonso L, et al. (2009) Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol183: 8088–8098. doi: 10.4049/jimmunol.080372019923470
27. Kobayashi SD, Voyich JM, Burlak C, DeLeo FR, (2005) Neutrophils in the innate immune response. Arch Immunol Ther Exp (Warsz)53: 505–517.
28. El-Benna J, Dang PM, Gougerot-Pocidalo MA, (2008) Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol30: 279–289. doi: 10.1007/s00281-008-0118-318536919
29. Jirmanus L, Glesby MJ, Guimaraes LH, Lago E, Rosa ME, et al. (2012) Epidemiological and clinical changes in American tegumentary leishmaniasis in an area of Leishmania (Viannia) braziliensis transmission over a 20-year period. Am J Trop Med Hyg86: 426–433. doi: 10.4269/ajtmh.2012.11-037822403312
30. Weirather JL, Jeronimo SM, Gautam S, Sundar S, Kang M, et al. (2011) Serial quantitative PCR assay for detection, species discrimination, and quantification of Leishmania spp. in human samples. J Clin Microbiol49: 3892–3904. doi: 10.1128/JCM.r00764-1122042830
31. Brito G, Dourado M, Polari L, Celestino D, Carvalho LP, et al. (2014) Clinical and immunological outcome in cutaneous leishmaniasis patients treated with pentoxifylline. Am J Trop Med Hyg90: 617–620. doi: 10.4269/ajtmh.12-072924567316
32. Cupolillo E, Grimaldi G, Jr.Momen H, (1994) A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg50: 296–311. 8147488
33. Grekov I, Svobodova M, Nohynkova E, Lipoldova M, (2011) Preparation of highly infective Leishmania promastigotes by cultivation on SNB-9 biphasic medium. J Microbiol Methods87: 273–277. doi: 10.1016/j.mimet.2011.08.01221889549
34. Kamau SW, Nunez R, Grimm F, (2001) Flow cytometry analysis of the effect of allopurinol and the dinitroaniline compound (Chloralin) on the viability and proliferation of Leishmania infantum promastigotes. BMC Pharmacol1: 1. 11299045
35. Nauseef WM, (2007) Isolation of human neutrophils from venous blood. Methods Mol Biol412: 15–20. doi: 10.1007/978-1-59745-467-4_218453102
36. Machado PR, Lessa H, Lessa M, Guimaraes LH, Bang H, et al. (2007) Oral pentoxifylline combined with pentavalent antimony: a randomized trial for mucosal leishmaniasis. Clin Infect Dis44: 788–793. 17304449
37. Almeida RP, Brito J, Machado PL, DEJ AR, Schriefer A, et al. (2005) Successful treatment of refractory cutaneous leishmaniasis with GM-CSF and antimonials. Am J Trop Med Hyg73: 79–81. 16014838
38. Dantas ML, de Oliveira JM, Carvalho L, Passos ST, Queiroz A, et al. (2014) Comparative analysis of the tissue inflammatory response in human cutaneous and disseminated leishmaniasis. Mem Inst Oswaldo Cruz109: 202–209. 24676653
39. de Moura TR, Novais FO, Oliveira F, Clarencio J, Noronha A, et al. (2005) Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect Immun73: 5827–5834. 16113301
40. Dantas ML, Oliveira JC, Carvalho L, Passos ST, Queiroz A, et al. (2013) CD8+ T cells in situ in different clinical forms of human cutaneous leishmaniasis. Rev Soc Bras Med Trop46: 728–734. doi: 10.1590/0037-8682-0174-201324474014
41. Bittencourt AL, Barral A, (1991) Evaluation of the histopathological classifications of American cutaneous and mucocutaneous leishmaniasis. Mem Inst Oswaldo Cruz86: 51–56.
42. Machado P, Araujo C, Da Silva AT, Almeida RP, D'Oliveira A, Jret al. (2002) Failure of early treatment of cutaneous leishmaniasis in preventing the development of an ulcer. Clin Infect Dis34: E69–73. 12032913
43. Uriarte SM, Rane MJ, Luerman GC, Barati MT, Ward RA, et al. (2011) Granule exocytosis contributes to priming and activation of the human neutrophil respiratory burst. J Immunol187: 391–400. doi: 10.4049/jimmunol.100311221642540
44. Hafezi-Moghadam A, Thomas KL, Prorock AJ, Huo Y, Ley K, (2001) L-selectin shedding regulates leukocyte recruitment. J Exp Med193: 863–872. 11283159
45. Bezerra CA, Cardoso TM, Giudice A, Porto AF, Santos SB, et al. (2011) Evaluation of the microbicidal activity and cytokines/chemokines profile released by neutrophils from HTLV-1-infected individuals. Scand J Immunol74: 310–317. doi: 10.1111/j.1365-3083.2011.02579.x21595736
46. Hassani K, Shio MT, Martel C, Faubert D, Olivier M, (2014) Absence of metalloprotease GP63 alters the protein content of Leishmania exosomes. PLoS One9: e95007. doi: 10.1371/journal.pone.009500724736445
47. Majumdar R, Tavakoli Tameh A, Parent CA, (2016) Exosomes Mediate LTB4 Release during Neutrophil Chemotaxis. PLoS Biol14: e1002336. doi: 10.1371/journal.pbio.100233626741884
48. Carvalho LP, Pearce EJ, Scott P, (2008) Functional dichotomy of dendritic cells following interaction with Leishmania braziliensis: infected cells produce high levels of TNF-alpha, whereas bystander dendritic cells are activated to promote T cell responses. J Immunol181: 6473–6480. 18941238
49. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science303: 1532–1535. 15001782
50. Guimaraes-Costa AB, Nascimento MT, Froment GS, Soares RP, Morgado FN, et al. (2009) Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A106: 6748–6753. doi: 10.1073/pnas.090022610619346483
51. Novais FO, Nguyen BT, Beiting DP, Carvalho LP, Glennie ND, et al. (2014) Human classical monocytes control the intracellular stage of Leishmania braziliensis by reactive oxygen species. J Infect Dis209: 1288–1296. doi: 10.1093/infdis/jiu01324403561
52. Carneiro PP, Conceicao J, Macedo M, Magalhaes V, Carvalho EM, et al. (2016) The Role of Nitric Oxide and Reactive Oxygen Species in the Killing of Leishmania braziliensis by Monocytes from Patients with Cutaneous Leishmaniasis. PLoS One11: e0148084. doi: 10.1371/journal.pone.014808426840253
53. van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, et al. (2004) Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol173: 6521–6525. 15557140
54. Lopes MF, Costa-da-Silva AC, DosReis GA, (2014) Innate immunity to Leishmania infection: within phagocytes. Mediators Inflamm2014: 754965. doi: 10.1155/2014/75496525110400
55. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, et al. (2000) The neutrophil as a cellular source of chemokines. Immunol Rev177: 195–203. 11138776
56. Mantovani A, Cassatella MA, Costantini C, Jaillon S, (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol11: 519–531. doi: 10.1038/nri302421785456
57. Guan E, Wang J, Norcross MA, (2001) Identification of human macrophage inflammatory proteins 1alpha and 1beta as a native secreted heterodimer. J Biol Chem276: 12404–12409. 11278300
58. van Zandbergen G, Hermann N, Laufs H, Solbach W, Laskay T, (2002) Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes. Infect Immun70: 4177–4184. 12117926
59. Giudice A, Vendrame C, Bezerra C, Carvalho LP, Delavechia T, et al. (2012) Macrophages participate in host protection and the disease pathology associated with Leishmania braziliensis infection. BMC Infect Dis12: 75. doi: 10.1186/1471-2334-12-7522458474
60. Da-Cruz AM, de Oliveira MP, De Luca PM, Mendonca SC, Coutinho SG, (1996) Tumor necrosis factor-alpha in human american tegumentary leishmaniasis. Mem Inst Oswaldo Cruz91: 225–229. 8736095
61. Carvalho EM, Johnson WD, Barreto E, Marsden PD, Costa JL, et al. (1985) Cell mediated immunity in American cutaneous and mucosal leishmaniasis. J Immunol135: 4144–4148. 4067312
62. Yao Y, Matsushima H, Ohtola JA, Geng S, Lu R, et al. (2015) Neutrophil priming occurs in a sequential manner and can be visualized in living animals by monitoring IL-1beta promoter activation. J Immunol194: 1211–1224. doi: 10.4049/jimmunol.140201825527787
63. Wright HL, Moots RJ, Bucknall RC, Edwards SW, (2010) Neutrophil function in inflammation and inflammatory diseases. Rheumatology (Oxford)49: 1618–1631.