Visceral leishmaniasis patients display altered composition and maturity of neutrophils as well as impaired neutrophil effector functions

Frontiers in Immunology

Volumn 7, Issue NOV, 2016, Pages

  Yizengaw, Endalew ^a   Getahun, Mulusew ^a   Tajebe, Fitsumbrhan ^a   Cervera, Edward Cruz ^b   Adem, Emebet ^a   Mesfin, Getnet ^a   Hailu, Asrat ^c   Van der Auwera, Gert ^d   Yardley, Vanessa ^e   Lemma, Mulualem ^a   Skhedy, Ziv ^f   Diro, Ermias ^a   Yeshanew, Arega ^a   Melkamu, Roma ^a   Mengesha, Bewketu ^a   Modolell, Manuel ^g   Munder, Markus ^h   Müller, Ingrid ^b   Takele, Yegnasew ^a,b   Kropf, Pascale ^b  

^a UNIVERSITY OF GONDAR   (Ethiopia)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c ADDIS ABABA UNIVERSITY   (Ethiopia)

^d INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^e LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^f HASSELT UNIVERSITY   (Belgium)

^g MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^h UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Neutrophil extracellular traps; Neutrophils; Phagocytosis; Reactive oxygen species; Visceral leishmaniasis

Indexed keywords

AMPHOTERICIN B LIPID COMPLEX; ARGINASE; ELASTASE; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 27; MYELOPEROXIDASE; PAROMOMYCIN; REACTIVE OXYGEN METABOLITE; STIBOGLUCONATE SODIUM;

ADULT; ARTICLE; CELL COMPOSITION; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR TRAP; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; INFLAMMATION; LEISHMANIA DONOVANI; LEUKOCYTE ACTIVATION; MALE; NEUTROPHIL; NONHUMAN; PATHOGEN CLEARANCE; PHAGOCYTOSIS; VISCERAL LEISHMANIASIS;

EID: 85006176232     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00517     Document Type: Article

References (68)

1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One (2012) 7:e35671. doi: 10.1371/journal.pone.0035671
2. Bern C, Maguire JH, Alvar J. Complexities of assessing the disease burden attributable to leishmaniasis. PLoS Negl Trop Dis (2008) 2:e313. doi:10.1371/journal.pntd.0000313
3. Nylen S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol (2007) 28:378-84. doi:10.1016/j.it.2007.07.004
4. Goto H, Prianti MG. Immunoactivation and immunopathogeny during active visceral leishmaniasis. Rev Inst Med Trop Sao Paulo (2009) 51:241-6. doi:10.1590/S0036-46652009000500002
5. Gidwani K, Jones S, Kumar R, Boelaert M, Sundar S. Interferon-gamma release assay (modified QuantiFERON) as a potential marker of infection for Leishmania donovani, a proof of concept study. PLoS Negl Trop Dis (2011) 5:e1042. doi:10.1371/journal.pntd.0001042
6. Singh OP, Gidwani K, Kumar R, Nylen S, Jones SL, Boelaert M, et al. Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clin Vaccine Immunol (2012) 19:961-6. doi:10.1128/CVI.00143-12
7. Adem E, Tajebe F, Getahun M, Kiflie A, Diro E, Hailu A, et al. Successful treatment of human visceral leishmaniasis restores antigen-specific IFN-gamma, but not IL-10 production. PLoS Negl Trop Dis (2016) 10:e0004468. doi:10.1371/journal.pntd.0004468
8. Perez-Mazliah D, Langhorne J. CD4 T-cell subsets in malaria: TH1/TH2 revisited. Front Immunol (2014) 5:671. doi:10.3389/fimmu.2014.00671
9. Cohen J, Vincent JL, Adhikari NK, Machado FR, Angus DC, Calandra T, et al. Sepsis: a roadmap for future research. Lancet Infect Dis (2015) 15:581-614. doi:10.1016/S1473-3099(15)70112-X
10. Jaillon S, Galdiero MR, Del Prete D, Cassatella MA, Garlanda C, Mantovani A. Neutrophils in innate and adaptive immunity. Semin Immunopathol (2013) 35:377-94. doi:10.1007/s00281-013-0374-8
11. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol (2011) 11:519-31. doi:10.1038/nri3024
12. Kruger P, Saffarzadeh M, Weber AN, Rieber N, Radsak M, von Bernuth H, et al. Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog (2015) 11:e1004651. doi:10.1371/journal.ppat.1004651
13. Conceicao J, Davis R, Carneiro PP, Giudice A, Muniz AC, Wilson ME, et al. Characterization of neutrophil function in human cutaneous leishmaniasis caused by Leishmania braziliensis. PLoS Negl Trop Dis (2016) 10:e0004715. doi:10.1371/journal.pntd.0004715
14. Morgado FN, Nascimento MT, Saraiva EM, de Oliveira-Ribeiro C, Madeira Mde F, da Costa-Santos M, et al. Are neutrophil extracellular traps playing a role in the parasite control in active American tegumentary leishmaniasis lesions? PLoS One (2015) 10:e0133063. doi:10.1371/journal.pone.0133063
15. Safaiyan S, Bolhassani A, Nylen S, Akuffo H, Rafati S. Contribution of human neutrophils in the development of protective immune response during in vitro Leishmania major infection. Parasite Immunol (2011) 33:609-20. doi:10.1111/j.1365-3024.2011.01321.x
16. Carlsen ED, Liang Y, Shelite TR, Walker DH, Melby PC, Soong L. Permissive and protective roles for neutrophils in leishmaniasis. Clin Exp Immunol (2015) 182(2):109-18. doi:10.1111/cei.12674
17. Hurrell BP, Regli IB, Tacchini-Cottier F. Different Leishmania species drive distinct neutrophil functions. Trends Parasitol (2016) 32:392-401. doi:10.1016/j.pt.2016.02.003
18. Costa DL, Rocha RL, Carvalho RM, Lima-Neto AS, Harhay MO, Costa CH, et al. Serum cytokines associated with severity and complications of kala-azar. Pathog Glob Health (2013) 107:78-87. doi:10.1179/2047773213Y.0000000078
19. Santos-Oliveira JR, Regis EG, Giacoia-Gripp CB, Valverde JG, Alexandrino-de-Oliveira P, Lindoso JA, et al. Microbial translocation induces an intense proinflammatory response in patients with visceral leishmaniasis and HIV type 1 coinfection. J Infect Dis (2013) 208:57-66. doi:10.1093/infdis/jit135
20. Pearson RD, Steigbigel RT. Phagocytosis and killing of the protozoan Leishmania donovani by human polymorphonuclear leukocytes. J Immunol (1981) 127:1438-43.
21. Remaley AT, Kuhns DB, Basford RE, Glew RH, Kaplan SS. Leishmanial phosphatase blocks neutrophil O-2 production. J Biol Chem (1984) 259:11173-5.
22. 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. doi:10.1074/jbc.M110.125302
23. 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. doi:10.4049/jimmunol.1000893
24. Guimaraes-Costa AB, DeSouza-Vieira TS, Paletta-Silva R, Freitas-Mesquita AL, Meyer-Fernandes JR, Saraiva EM. 3'-nucleotidase/nuclease activity allows Leishmania parasites to escape killing by neutrophil extracellular traps. Infect Immun (2014) 82:1732-40. doi:10.1128/IAI.01232-13
25. Endris M, Takele Y, Woldeyohannes D, Tiruneh M, Mohammed R, Moges F, et al. Bacterial sepsis in patients with visceral leishmaniasis in Northwest Ethiopia. Biomed Res Int (2014) 2014:361058. doi:10.1155/2014/361058
26. Badaro R, Nascimento C, Carvalho JS, Badaro F, Russo D, Ho JL, 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. doi:10.1093/infdis/170.2.413
27. Chulay JD, Bryceson AD. Quantitation of amastigotes of Leishmania donovani in smears of splenic aspirates from patients with visceral leishmaniasis. Am J Trop Med Hyg (1983) 32:475-9.
28. Cloke T, Munder M, Taylor GP, Müller I, Kropf P. Characterization of a novel population of low-density granulocytes associated with disease severity in HIV seropositive patients. PLoS One (2012) 7:e48939. doi:10.1371/journal.pone.0048939
29. Van der Auwera G, Maes I, De Doncker S, Ravel C, Cnops L, Van Esbroeck M, et al. Heat-shock protein 70 gene sequencing for Leishmania species typing in European tropical infectious disease clinics. Euro Surveill (2013) 18:20543. doi:10.2807/1560-7917.ES2013.18.30.20543
30. Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM, et al. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol (2007) 37:935-45. doi:10.1002/eji.200636542
31. Choi BS, Martinez-Falero IC, Corset C, Munder M, Modolell M, Muller I, et al. Differential impact of l-arginine deprivation on the activation and effector functions of T cells and macrophages. J Leukoc Biol (2009) 85:268-77. doi:10.1189/jlb.0508310
32. Kropf P, Fuentes JM, Fahnrich E, Arpa L, Herath S, Weber V, et al. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J (2005) 19:1000-2. doi:10.1096/fj.04-3416fje
33. Cloke T, Munder M, Bergin P, Herath S, Modolell M, Taylor G, et al. Phenotypic alteration of neutrophils in the blood of HIV seropositive patients. PLoS One (2013) 8:e72034. doi:10.1371/journal.pone.0072034
34. Elghetany MT. Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol Dis (2002) 28:260-74. doi:10.1006/bcmd.2002.0513
35. Takele Y, Abebe T, Weldegebreal T, Hailu A, Hailu W, Hurissa Z, et al. Arginase activity in the blood of patients with visceral leishmaniasis and HIV infection. PLoS Negl Trop Dis (2013) 7:e1977. doi:10.1371/journal.pntd.0001977
36. Abebe T, Takele T, Weldegebreal T, Cloke T, Closs E, Corset C, et al. Arginase: a marker of disease status in patients with visceral leishmaniasis. PLoS Negl Trop Dis (2013) 7:e2134. doi:10.1371/journal.pntd.0002134
37. Ssemaganda A, Kindinger L, Bergin P, Nielsen L, Mpendo J, Ssetaala A, et al. Characterization of neutrophil subsets in healthy human pregnancies. PLoS One (2014) 9:e85696. doi:10.1371/journal.pone.0085696
38. Kuijpers TW, Tool AT, van der Schoot CE, Ginsel LA, Onderwater JJ, Roos D, et al. Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood (1991) 78:1105-11.
39. Martin-Martin B, Nabokina SM, Blasi J, Lazo PA, Mollinedo F. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood (2000) 96:2574-83.
40. Modolell M, Choi B-S, Ryan RO, Hancock M, Titus RG, Abebe T, et al. Local suppression of T cell responses by arginase-induced l-arginine depletion in nonhealing leishmaniasis. PLoS Negl Trop Dis (2009) 14:e480. doi:10.1371/journal.pntd.0000480
41. Munder M. Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol (2009) 158:638-51. doi:10.1111/j.1476-5381.2009.00291.x
42. Klebanoff SJ, Kettle AJ, Rosen H, Winterbourn CC, Nauseef WM. Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J Leukoc Biol (2013) 93:185-98. doi:10.1189/jlb.0712349
43. Locksley RM, Nelson CS, Fankhauser JE, Klebanoff SJ. Loss of granule myeloperoxidase during in vitro culture of human monocytes correlates with decay in antiprotozoa activity. Am J Trop Med Hyg (1987) 36:541-8.
44. Faria MS, Calegari-Silva TC, de Carvalho Vivarini A, Mottram JC, Lopes UG, Lima AP. Role of protein kinase R in the killing of Leishmania major by macrophages in response to neutrophil elastase and TLR4 via TNFalpha and IFNbeta. FASEB J (2014) 28:3050-63. doi:10.1096/fj.13-245126
45. Henriksen PA. The potential of neutrophil elastase inhibitors as anti-inflammatory therapies. Curr Opin Hematol (2014) 21:23-8. doi:10.1097/MOH.0000000000000001
46. Dos Santos PL, de Oliveira FA, Santos ML, Cunha LC, Lino MT, de Oliveira MF, et al. The severity of visceral leishmaniasis correlates with elevated levels of serum IL-6, IL-27 and sCD14. PLoS Negl Trop Dis (2016) 10:e0004375. doi:10.1371/journal.pntd.0004375
47. Ansari NA, Kumar R, Gautam S, Nylen S, Singh OP, Sundar S, et al. IL-27 and IL-21 are associated with T cell IL-10 responses in human visceral leishmaniasis. J Immunol (2011) 186:3977-85. doi:10.4049/jimmunol.1003588
48. van den Bogaart E, Talha AB, Straetemans M, Mens PF, Adams ER, Grobusch MP, et al. Cytokine profiles amongst Sudanese patients with visceral leishmaniasis and malaria co-infections. BMC Immunol (2014) 15:16. doi:10.1186/1471-2172-15-16
49. Banerjee A, Bhattacharya P, Joshi AB, Ismail N, Dey R, Nakhasi HL. Role of pro-inflammatory cytokine IL-17 in Leishmania pathogenesis and in protective immunity by Leishmania vaccines. Cell Immunol (2016). doi:10.1016/j.cellimm.2016.07.004
50. 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. doi:10.4049/jimmunol.0713598
51. Anderson CF, Stumhofer JS, Hunter CA, Sacks D. IL-27 regulates IL-10 and IL-17 from CD4+ cells in nonhealing Leishmania major infection. J Immunol (2009) 183:4619-27. doi:10.4049/jimmunol.0804024
52. Barreto-de-Souza V, Ferreira PL, Vivarini Ade C, Calegari-Silva T, Soares DC, Regis EG, et al. IL-27 enhances Leishmania amazonensis infection via ds-RNA dependent kinase (PKR) and IL-10 signaling. Immunobiology (2015) 220:437-44. doi:10.1016/j.imbio.2014.11.006
53. Quirino GF, Nascimento MS, Davoli-Ferreira M, Sacramento LA, Lima MH, Almeida RP, et al. Interleukin-27 (IL-27) mediates susceptibility to visceral leishmaniasis by suppressing the IL-17-neutrophil response. Infect Immun (2016) 84:2289-98. doi:10.1128/IAI.00283-16
54. Sharma S, Davis RE, Srivastva S, Nylen S, Sundar S, Wilson ME. A subset of neutrophils expressing markers of antigen-presenting cells in human visceral leishmaniasis. J Infect Dis (2016) 214(10):1531-8. doi:10.1093/infdis/jiw394
55. Musumeci S, D'Agata A, Schiliro G, Fischer A. Leukokinetic studies in Mediterranean kala azar. Acta Trop (1978) 35:183-93.
56. Zarco MA, Ribera JM, Urbano-Ispizua A, Filella X, Arriols R, Martinez C, et al. Phenotypic changes in neutrophil granulocytes of healthy donors after G-CSF administration. Haematologica (1999) 84:874-8.
57. Denny MF, Yalavarthi S, Zhao W, Thacker SG, Anderson M, Sandy AR, et al. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol (2010) 184:3284-97. doi:10.4049/jimmunol.0902199
58. Kaneko T, Stearns-Kurosawa DJ, Taylor F Jr, Twigg M, Osaki K, Kinasewitz GT, et al. Reduced neutrophil CD10 expression in nonhuman primates and humans after in vivo challenge with E. coli or lipopolysaccharide. Shock (2003) 20:130-7. doi:10.1097/01.shk.0000068326.68761.34
59. Laskay T, van Zandbergen G, Solbach W. Neutrophil granulocytes-Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol (2003) 11:210-4. doi:10.1016/S0966-842X(03)00075-1
60. van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, Solbach W, et al. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol (2004) 173:6521-5. doi:10.4049/jimmunol.173.11.6521
61. Laufs H, Müller K, Fleischer J, Reiling N, Jahnke N, Jensenius JC, 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. doi:10.1128/IAI.70.2.826-835.2002
62. Tavares NM, Araujo-Santos T, Afonso L, Nogueira PM, Lopes UG, Soares RP, et al. Understanding the mechanisms controlling Leishmania amazonensis infection in vitro: the role of LTB4 derived from human neutrophils. J Infect Dis (2014) 210:656-66. doi:10.1093/infdis/jiu158
63. Atayde VD, Hassani K, da Silva Lira Filho A, Borges AR, Adhikari A, Martel C, et al. Leishmania exosomes and other virulence factors: impact on innate immune response and macrophage functions. Cell Immunol (2016). doi:10.1016/j.cellimm.2016.07.013
64. Gorski S, Collin SM, Ritmeijer K, Keus K, Gatluak F, Mueller M, et al. Visceral leishmaniasis relapse in Southern Sudan (1999-2007): a retrospective study of risk factors and trends. PLoS Negl Trop Dis (2010) 4:e705. doi:10.1371/journal.pntd.0000705
65. Diro E, Lynen L, Mohammed R, Boelaert M, Hailu A, van Griensven J. High parasitological failure rate of visceral leishmaniasis to sodium stibogluconate among HIV co-infected adults in Ethiopia. PLoS Negl Trop Dis (2014) 8:e2875. doi:10.1371/journal.pntd.0002875
66. Hurrell BP, Schuster S, Grun E, Coutaz M, Williams RA, Held W, et al. Rapid sequestration of Leishmania mexicana by neutrophils contributes to the development of chronic lesion. PLoS Pathog (2015) 11:e1004929. doi:10.1371/journal.ppat.1004929
67. Guimaraes-Costa AB, Nascimento MT, Froment GS, Soares RP, Morgado FN, Conceicao-Silva F, et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A (2009) 106:6748-53. doi:10.1073/pnas.0900226106
68. Carlsen ED, Jie Z, Liang Y, Henard CA, Hay C, Sun J, et al. Interactions between neutrophils and Leishmania braziliensis amastigotes facilitate cell activation and parasite clearance. J Innate Immun (2015) 7:354-63. doi:10.1159/000373923