Permissive and protective roles for neutrophils in leishmaniasis

Clinical and Experimental Immunology

Volumn 182, Issue 2, 2015, Pages 109-118

  Carlsen, E D ^a   Liang, Y ^a   Shelite, T R ^a   Walker, D H ^a   Melby, P C ^a   Soong, L ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Leishmania, monoclonal antibody; Mouse model; Neutrophil

Indexed keywords

GRANULOCYTE ANTIBODY;

AMASTIGOTE; ARTICLE; DENDRITIC CELL; DEVELOPING COUNTRY; HUMAN; IMMUNITY; LEISHMANIA; LEISHMANIASIS; MACROPHAGE; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; SKIN LEISHMANIASIS; TROPICAL DISEASE; VISCERAL LEISHMANIASIS; ANIMAL; HOST PARASITE INTERACTION; IMMUNOLOGY; MOUSE; NEUTROPHIL CHEMOTAXIS; PARASITOLOGY; PHYSIOLOGY;

ANIMALS; HOST-PARASITE INTERACTIONS; HUMANS; LEISHMANIA; LEISHMANIASIS, CUTANEOUS; LEISHMANIASIS, VISCERAL; MACROPHAGES; MICE; NEUTROPHIL INFILTRATION; NEUTROPHILS;

EID: 84944161107     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12674     Document Type: Article

References (98)

1. Paniz Mondolfi AE, Duffey GB, Horton LE et al. Intermediate/borderline disseminated cutaneous leishmaniasis. Int J Dermatol 2013; 52:446-55.
2. Soong L. Subversion and utilization of host innate defense by Leishmania amazonensis. Front Immunol 2012; 3:58.
3. Mendonca MG, de Brito ME, Rodrigues EH, Bandeira V, Jardim ML, Abath FG. Persistence of Leishmania parasites in scars after clinical cure of American cutaneous leishmaniasis: is there a sterile cure? J Infect Dis 2004; 189:1018-23.
4. Tuon FF, Sabbaga Amato V, Floeter-Winter LM et al. Cutaneous leishmaniasis reactivation 2 years after treatment caused by systemic corticosteroids - first report. Int J Dermatol 2007; 46:628-30.
5. Okwor I, Uzonna JE. The immunology of Leishmania/HIV co-infection. Immunol Res 2013; 56:163-71.
6. McGwire BS, Satoskar AR. Leishmaniasis: clinical syndromes and treatment. Q J Med 2014; 107:7-14.
7. Belo VS, Werneck GL, Barbosa DS et al. Factors associated with visceral leishmaniasis in the Americas: a systematic review and meta-analysis. PLOS Negl Trop Dis 2013; 7:e2182.
8. Werneck GL, Batista MS, Gomes JR, Costa DL, Costa CH. Prognostic factors for death from visceral leishmaniasis in Teresina, Brazil. Infection 2003; 31:174-7.
9. Peters NC, Egen JG, Secundino N et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008; 321:970-4.
10. Laskay T, van Zandbergen G, Solbach W. Neutrophil granulocytes - Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol 2003; 11:210-4.
11. Charmoy M, Megnekou R, Allenbach C et al. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 2007; 82:288-99.
12. Chen L, Zhang ZH, Watanabe T et al. The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. Parasitol Int 2005; 54:109-18.
13. Gabriel C, McMaster WR, Girard D, Descoteaux A. Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. J Immunol 2010; 185:4319-27.
14. Gueirard P, Laplante A, Rondeau C, Milon G, Desjardins M. Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell Microbiol 2008; 10:100-11.
15. Laufs H, Muller K, Fleischer J et al. Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors. Infect Immun 2002; 70:826-35.
16. McFarlane E, Perez C, Charmoy M et al. Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infect Immun 2008; 76:532-41.
17. Mollinedo F, Janssen H, de la Iglesia-Vicente J, Villa-Pulgarin JA, Calafat J. Selective fusion of azurophilic granules with Leishmania-containing phagosomes in human neutrophils. J Biol Chem 2010; 285:34528-36.
18. Ribeiro-Gomes FL, Peters NC, Debrabant A, Sacks DL. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-Leishmania response. PLOS Pathog 2012; 8:e1002536.
19. Ribeiro-Gomes FL, Sacks D. The influence of early neutrophil-Leishmania interactions on the host immune response to infection. Front Cell Infect Microbiol 2012; 2:59.
20. + Th2 response in BALB/c mice infected with Leishmania major. J Immunol 2000; 165:2628-36.
21. Xin L, Vargas-Inchaustegui DA, Raimer SS et al. Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites. J Immunol 2010; 184:7047-56.
22. Wang Y, Chen Y, Xin L et al. Differential microbicidal effects of human histone proteins H2A and H2B on Leishmania promastigotes and amastigotes. Infect Immun 2011; 79:1124-33.
23. Massberg S, Grahl L, von Bruehl ML et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16:887-96.
24. Hahn I, Klaus A, Janze AK et al. Cathepsin G and neutrophil elastase play critical and nonredundant roles in lung-protective immunity against Streptococcus pneumoniae in mice. Infect Immun 2011; 79:4893-901.
25. Bonfim-Mendonca Pde S, Ratti BA, Godoy Jda S et al. β-glucan induces reactive oxygen species production in human neutrophils to improve the killing of Candida albicans and Candida glabrata isolates from vulvovaginal candidiasis. PLOS ONE 2014; 9:e107805.
26. Lu T, Kobayashi SD, Quinn MT, Deleo FR. A NET Outcome. Front Immunol 2012; 3:365.
27. Tecchio C, Micheletti A, Cassatella MA. Neutrophil-derived cytokines: facts beyond expression. Front Immunol 2014; 5:508.
28. Heijink IH, Pouwels SD, Leijendekker C et al. Cigarette Smoke Induced DAMP Release from Necrotic Neutrophils Triggers Pro-inflammatory Mediator Release. Am J Respir Cell Mol Biol 2015; 52:554-62.
29. El Kebir D, Gjorstrup P, Filep JG. Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc Natl Acad Sci USA 2012; 109:14983-8.
30. Kambayashi T, Laufer TM. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol 2014; 14:719-30.
31. Hock BD, Taylor KG, Cross NB, Kettle AJ, Hampton MB, McKenzie JL. Effect of activated human polymorphonuclear leucocytes on T lymphocyte proliferation and viability. Immunology 2012; 137:249-58.
32. Puga I, Cols M, Barra CM et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 2012; 13:170-80.
33. Verri WA Jr, Souto FO, Vieira SM et al. IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy. Ann Rheum Dis 2010; 69:1697-703.
34. Leffler J, Martin M, Gullstrand B et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 2012; 188:3522-31.
35. Lee DJ, Li H, Ochoa MT et al. Integrated pathways for neutrophil recruitment and inflammation in leprosy. J Infect Dis 2010; 201:558-69.
36. Lowe DM, Redford PS, Wilkinson RJ, O'Garra A, Martineau AR. Neutrophils in tuberculosis: friend or foe? Trends Immunol 2012; 33:14-25.
37. Lopez Kostka S, Dinges S, Griewank K, Iwakura Y, Udey MC, von Stebut E. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J Immunol 2009; 182:3039-46.
38. Souza-Lemos C, de-Campos SN, Teva A et al. Dynamics of immune granuloma formation in a Leishmania braziliensis-induced self-limiting cutaneous infection in the primate Macaca mulatta. J Pathol 2008; 216:375-86.
39. Vercosa BL, Melo MN, Puerto HL, Mendonca IL, Vasconcelos AC. Apoptosis, inflammatory response and parasite load in skin of Leishmania (Leishmania) chagasi naturally infected dogs: a histomorphometric analysis. Vet Parasitol 2012; 189:162-70.
40. Morgado FN, Schubach A, Rosalino CM et al. Is the in situ inflammatory reaction an important tool to understand the cellular immune response in American tegumentary leishmaniasis? Br J Dermatol 2008; 158:50-8.
41. Dabiri S, Hayes MM, Meymandi SS, Basiri M, Soleimani F, Mousavi MR. Cytologic features of 'dry-type' cutaneous leishmaniasis. Diagn Cytopathol 1998; 19:182-5.
42. Daboul MW. Role of neutrophils in cutaneous leishmaniasis. East Mediterr Health J 2010; 16:1055-8.
43. Dantas ML, Oliveira JM, Carvalho L et al. Comparative analysis of the tissue inflammatory response in human cutaneous and disseminated leishmaniasis. Mem Inst Oswaldo Cruz 2014; 109:202-9.
44. Boaventura VS, Santos CS, Cardoso CR et al. Human mucosal leishmaniasis: neutrophils infiltrate areas of tissue damage that express high levels of Th17-related cytokines. Eur J Immunol 2010; 40:2830-6.
45. Beil WJ, Meinardus-Hager G, Neugebauer DC, Sorg C. Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J Leukoc Biol 1992; 52:135-42.
46. Muller K, van Zandbergen G, Hansen B et al. Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Med Microbiol Immunol 2001; 190:73-6.
47. Thalhofer CJ, Chen Y, Sudan B, Love-Homan L, Wilson ME. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi. Infect Immun 2011; 79:108-17.
48. Carlsen ED, Hay C, Henard CA, Popov V, Garg NJ, Soong L. Leishmania amazonensis amastigotes trigger neutrophil activation but resist neutrophil microbicidal mechanisms. Infect Immun 2013; 81:3966-74.
49. Guimaraes-Costa AB, Nascimento MT, Froment GS et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 2009; 106:6748-53.
50. Ritter U, Frischknecht F, van Zandbergen G. Are neutrophils important host cells for Leishmania parasites? Trends Parasitol 2009; 25:505-10.
51. van Zandbergen G, Klinger M, Mueller A et al. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 2004; 173:6521-5.
52. Ribeiro-Gomes FL, Roma EH, Carneiro MB, Doria NA, Sacks DL, Peters NC. Site-dependent recruitment of inflammatory cells determines the effective dose of Leishmania major. Infect Immun 2014; 82:2713-27.
53. Peters NC, Kimblin N, Secundino N, Kamhawi S, Lawyer P, Sacks DL. Vector transmission of Leishmania abrogates vaccine-induced protective immunity. PLOS Pathog 2009; 5:e1000484.
54. Schuster S, Hurrell B, Tacchini-Cottier F. Crosstalk between neutrophils and dendritic cells: a context-dependent process. J Leukoc Biol 2013; 94:671-5.
55. Silva MT. When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol 2010; 87:93-106.
56. Costantini C, Cassatella MA. The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol 2011; 89:221-33.
57. Jaeger BN, Donadieu J, Cognet C et al. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 2012; 209:565-80.
58. Kalyan S, Kabelitz D. When neutrophils meet T cells: beginnings of a tumultuous relationship with underappreciated potential. Eur J Immunol 2014; 44:627-33.
59. Sabbione F, Gabelloni ML, Ernst G et al. Neutrophils suppress gammadelta T-cell function. Eur J Immunol 2014; 44:819-30.
60. Afonso L, Borges VM, Cruz H et al. Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J Leukoc Biol 2008; 84:389-96.
61. Ribeiro-Gomes FL, Otero AC, Gomes NA et al. Macrophage interactions with neutrophils regulate Leishmania major infection. J Immunol 2004; 172:4454-62.
62. de Souza Carmo EV, Katz S, Barbieri CL. Neutrophils reduce the parasite burden in Leishmania (Leishmania) amazonensis-infected macrophages. PLoS One 2010; 5:e13815.
63. Novais FO, Santiago RC, Bafica A et al. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol 2009; 183:8088-98.
64. Carlsen ED, Jie Z, Liang Y et al. Interactions between neutrophils and Leishmania braziliensis amastigotes facilitate cell activation and parasite clearance. J Innate Immun 2015; 7:354-63.
65. Mougneau E, Bihl F, Glaichenhaus N. Cell biology and immunology of Leishmania. Immunol Rev 2011; 240:286-96.
66. Bertrand A, Jourdan J, Prefaut C. Granulopenia of infectious origin. Sem Hop 1975; 51:667-76.
67. Costa CH, Werneck GL, Costa DL et al. Is severe visceral leishmaniasis a systemic inflammatory response syndrome? A case control study. Rev Soc Bras Med Trop 2010; 43:386-92.
68. Musumeci S, D'Agata A, Schiliro G, Fischer A. Studies of the neutropenia in kala-azar: results in two patients. Trans R Soc Trop Med Hyg 1976; 70:500-3.
69. Pollack S, Nagler A, Liberman D et al. Immunological studies of pancytopenia in visceral leishmaniasis. Isr J Med Sci 1988; 24:70-4.
70. Badaro R, Nascimento C, Carvalho JS et al. Recombinant human granulocyte-macrophage colony-stimulating factor reverses neutropenia and reduces secondary infections in visceral leishmaniasis. J Infect Dis 1994; 170:413-8.
71. Almeida BF, Narciso LG, Bosco AM et al. Neutrophil dysfunction varies with the stage of canine visceral leishmaniosis. Vet Parasitol 2013; 196:6-12.
72. + neutrophils are dispensable for defense against systemic Listeria monocytogenes infection. J Immunol 2011; 187:5293-8.
73. Archer NK, Harro JM, Shirtliff ME. Clearance of Staphylococcus aureus nasal carriage is T cell dependent and mediated through interleukin-17A expression and neutrophil influx. Infect Immun 2013; 81:2070-5.
74. Ribes S, Regen T, Meister T et al. Resistance of the brain to Escherichia coli K1 infection depends on MyD88 signaling and the contribution of neutrophils and monocytes. Infect Immun 2013; 81:1810-9.
75. Wang JX, Bair AM, King SL et al. Ly6G ligation blocks recruitment of neutrophils via a beta2-integrin-dependent mechanism. Blood 2012; 120:1489-98.
76. Lima GM, Vallochi AL, Silva UR, Bevilacqua EM, Kiffer MM, Abrahamsohn IA. The role of polymorphonuclear leukocytes in the resistance to cutaneous Leishmaniasis. Immunol Lett 1998; 64:145-51.
77. Smelt SC, Cotterell SE, Engwerda CR, Kaye PM. B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol 2000; 164:3681-8.
78. Rousseau D, Demartino S, Ferrua B et al. In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection. BMC Microbiol 2001; 1:17.
79. Sousa LM, Carneiro MB, Resende ME et al. Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite Immunol 2014; 36:13-31.
80. Hurrell BP, Schuster S, Grun E et al. Rapid sequestration of Leishmania mexicana by neutrophils contributes to the development of chronic lesion. PLOS Pathog 2015; 11:e1004929.
81. + cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001; 194:1171-8.
82. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19:71-82.
83. Tepper RI, Coffman RL, Leder P. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 1992; 257:548-51.
84. + T cell subsets by the administration of anti-Gr-1 monoclonal antibody in vivo. Cell Immunol 2003; 224:98-105.
85. Tasew G, Nylen S, Lieke T et al. Systemic FasL and TRAIL neutralisation reduce leishmaniasis induced skin ulceration. PLOS Negl Trop Dis 2010; 4:e844.
86. Souza VL, Veras PS, Welby-Borges M et al. Immune and inflammatory responses to Leishmania amazonensis isolated from different clinical forms of human leishmaniasis in CBA mice. Mem Inst Oswaldo Cruz 2011; 106:23-31.
87. Guerra JA, Prestes SR, Silveira H et al. Mucosal Leishmaniasis caused by Leishmania (Viannia) braziliensis and Leishmania (Viannia) guyanensis in the Brazilian Amazon. PLOS Negl Trop Dis 2011; 5:e980.
88. Vargas-Inchaustegui DA, Tai W, Xin L, Hogg AE, Corry DB, Soong L. Distinct roles for MyD88 and Toll-like receptor 2 during Leishmania braziliensis infection in mice. Infect Immun 2009; 77:2948-56.
89. Soong L, Henard CA, Melby PC. Immunopathogenesis of non-healing American cutaneous leishmaniasis and progressive visceral leishmaniasis. Semin Immunopathol 2012; 34:735-51.
90. Vargas-Inchaustegui DA, Xin L, Soong L. Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. J Immunol 2008; 180:7537-45.
91. Tenorio Mda S, Oliveira e Sousa L, Paixao Mdos S et al. Visceral leishmaniasis in a captive crab-eating fox Cerdocyon thous. J Zoo Wildl Med 2011; 42:608-16.
92. Liu C, Desikan R, Ying Z et al. Effects of a novel pharmacologic inhibitor of myeloperoxidase in a mouse atherosclerosis model. PLOS ONE 2012; 7: e50767.
93. Hazen SL, Zhang R, Shen Z et al. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo. Circ Res 1999; 85:950-8.
94. Rosas M, Thomas B, Stacey M, Gordon S, Taylor PR. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. J Leukoc Biol 2010; 88:169-80.
95. Sadick MD, Locksley RM, Tubbs C, Raff HV. Murine cutaneous leishmaniasis: resistance correlates with the capacity to generate interferon-gamma in response to Leishmania antigens in vitro. J Immunol 1986; 136:655-61.
96. Locksley RM, Heinzel FP, Sadick MD, Holaday BJ, Gardner KD Jr. Murine cutaneous leishmaniasis: susceptibility correlates with differential expansion of helper T-cell subsets. Ann Inst Pasteur Immunol 1987; 138:744-9.
97. + T cells in pathogenesis associated with Leishmania amazonensis infection. J Immunol 1997; 158:5374-83.
98. Qi H, Ji J, Wanasen N, Soong L. Enhanced replication of Leishmania amazonensis amastigotes in gamma interferon-stimulated murine macrophages: implications for the pathogenesis of cutaneous leishmaniasis. Infect Immun 2004; 72:988-95.