Interleukin 17A acts synergistically with interferon γ to promote protection against leishmania infantum infection

Journal of Infectious Diseases

Volumn 211, Issue 6, 2015, Pages 1015-1026

  Nascimento, Manuela Sales Lima ^a   Carregaro, Vanessa ^a   Lima Júnior, Djalma Souza ^a   Costa, Diego Luís ^a   Ryffel, Bernhard ^c   Duthie, Malcolm S ^d   De Jesus, Amélia ^b   De Almeida, Roque Pacheco ^b   Da Silva, João Santana ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^c UNIVERSITÉ D'ORLÉANS   (France)

^d INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

Author keywords

IL 17; Leishmania infantum; nitric oxide; visceral leishmaniasis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; MEGLUMINE ANTIMONATE; NITRIC OXIDE; TRANSCRIPTION FACTOR FOXP3; IL17A PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; FEMALE; HUMAN; INFLAMMATORY INFILTRATE; LEISHMANIA INFANTUM; MALE; MOUSE; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH1 CELL; VISCERAL LEISHMANIASIS; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CELLULAR IMMUNITY; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; INTERLEUKIN-17; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; YOUNG ADULT;

EID: 84924365575     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu531     Document Type: Article

References (45)

1. Gardener PJ. Taxonomy of the genus Leishmania: a review of nomenclature and classification. Trop Dis Bull 1977; 74:1069-88
2. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 2004; 27:305-18
3. Ghalib HW, Whittle JA, Kubin M, et al. IL-12 enhances Th1-type responses in human Leishmania donovani infections. J Immunol 1995; 154:4623-9
4. Sacks D, Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2002; 2:845-58
5. Biron CA, Gazzinelli RT. Effects of IL-12 on immune responses to microbial infections: a key mediator in regulating disease outcome. Curr Opin Immunol 1995; 7:485-96
6. Gantt KR, Goldman TL, McCormick ML, et al. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J Immunol 2001; 167:893-901
7. Kopf M, Brombacher F, Kohler G, et al. IL-4-deficient Balb/c mice resist infection with Leishmania major. J Exp Med 1996; 184:1127-36
8. Kedzierski L, Curtis JM, Doherty PC, Handman E, Kedzierska K. Decreased IL-10 and IL-13 production and increased CD44hi T cell recruitment contribute to Leishmania major immunity induced by non-persistent parasites. Eur J Immunol 2008; 38:3090-100
9. Ghalib HW, Piuvezam MR, Skeiky YA, et al. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 1993; 92:324-9
10. Gautam S, Kumar R, Maurya R, et al. IL-10 neutralization promotes parasite clearance in splenic aspirate cells from patients with visceral leishmaniasis. J Infect Dis 2011; 204:1134-7
11. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003; 171:6173-7
12. Kurasawa K, Hirose K, Sano H, et al. Increased interleukin-17 production in patients with systemic sclerosis. Arthritis Rheum 2000; 43:2455-63
13. Kryczek I, Banerjee M, Cheng P, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 2009; 114:1141-9
14. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin- 17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 2004; 190:624-31
15. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004; 21:467-76
16. da Matta Guedes PM, Gutierrez FR, Maia FL, et al. IL-17 produced during Trypanosoma cruzi infection plays a central role in regulating parasite- induced myocarditis. PLoS Negl Trop Dis 2010; 4:e604
17. Lopez KS, Dinges S, Griewank K, Iwakura Y, Udey MC, von SE. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J Immunol 2009; 182:3039-46
18. Novoa R, Bacellar O, Nascimento M, et al. IL-17 and regulatory cytokines (IL-10 and IL-27) in L. braziliensis infection. Parasite Immunol 2011; 33:132-6
19. Pitta MG, Romano A, Cabantous S, et al. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J Clin Invest 2009; 119:2379-87
20. Titus RG, Marchand M, Boon T, Louis JA. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol 1985; 7:545-55
21. Buffet PA, Sulahian A, Garin YJ, Nassar N, Derouin F. Culture microtitration: a sensitive method for quantifying Leishmania infantum in tissues of infected mice. Antimicrob Agents Chemother 1995; 39: 2167-8
22. Englen MD, Valdez YE, Lehnert NM, Lehnert BE. Granulocyte/macrophage colony-stimulating factor is expressed and secreted in cultures of murine L929 cells. J Immunol Methods 1995; 184:281-3
23. Sebastiani S, Allavena P, Albanesi C, et al. Chemokine receptor expression and function in CD4+ T lymphocytes with regulatory activity. J Immunol 2001; 166:996-1002
24. Vargas-IncXin 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
25. Ghosh K, Sharma G, Saha A, Kar S, Das PK, Ukil A. Successful therapy of visceral leishmaniasis with curdlan involves T-helper 17 cytokines. J Infect Dis 2013; 207:1016-25
26. Guedes PM, Gutierrez FR, Silva GK, et al. Deficient regulatory T cell activity and low frequency of IL-17-producing T cells correlate with the extent of cardiomyopathy in human Chagas' disease. PLoS Negl Trop Dis 2012; 6:e1630
27. Bermejo DA, Jackson SW, Gorosito-Serran M, et al. Trypanosoma cruzi trans-sialidase initiates a program independent of the transcription factors RORgammat and Ahr that leads to IL-17 production by activated B cells. Nat Immunol 2013; 14:514-22
28. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide- induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003; 170:2106-12
29. Qiu Z, Dillen C, Hu J, et al. Interleukin-17 regulates chemokine and gelatinase B expression in fibroblasts to recruit both neutrophils and monocytes. Immunobiology 2009; 214:835-42
30. Onishi RM, Gaffen SL. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 2010; 129: 311-21
31. Sallusto F, Lanzavecchia A, Mackay CR. Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol Today 1998; 19:568-74
32. Sallusto F, Lenig D, Mackay CR, Lanzavecchia A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med 1998; 187:875-83
33. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol 2008; 9:970-80
34. Nylen S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol 2007; 28:378-84
35. Nylen S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, Sacks D. Splenic accumulation of IL-10 mRNA in T cells distinct from CD4- +CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 2007; 204:805-17
36. 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
37. Rodrigues OR, Marques C, Soares-Clemente M, Ferronha MH, Santos-Gomes GM. Identification of regulatory T cells during experimental Leishmania infantum infection. Immunobiology 2009; 214: 101-11
38. Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson WD Jr. Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. J Clin Invest 1985; 76:2066-9
39. Carvalho EM, Bacellar O, Brownell C, Regis T, Coffman RL, Reed SG. Restoration of IFN-gamma production and lymphocyte proliferation in visceral leishmaniasis. J Immunol 1994; 152:5949-56
40. Lin Y, Ritchea S, Logar A, et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009; 31:799-810
41. Ishigame H, Kakuta S, Nagai T, et al. Differential roles of interleukin- 17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009; 30:108-19
42. Yang ZS, Peng ZH, Li XL, Song JW, Ren JW. Effect of curcumin on IL-17-induced nitric oxide production and expression of iNOS in human keratinocytes. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2011; 27:959-61
43. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH. TLR4 mediates vaccineinduced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 2006; 177:7980-9
44. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009; 9:556-67
45. Ayres JS, Schneider DS. Tolerance of infections. Annu Rev Immunol 2012; 30:271-94