Toll-like receptor 9 signaling in dendritic cells regulates neutrophil recruitment to inflammatory foci following Leishmania infantum infection

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4604-4616

  Sacramento, Laís ^a   Trevelin, Silvia C ^a   Nascimento, Manuela S ^a   Lima Jùnior, Djalma S ^a   Costa, Diego L ^a   Almeida, Roque P ^b   Cunha, Fernando Q ^a   Silva, João S ^a   Carregaro, Vanessa ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 17; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; MYD88 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; INFECTION SENSITIVITY; INFLAMMATION; INFLAMMATORY CELL; LEISHMANIA INFANTUM; LEUKOCYTE ACTIVATION; LIVER; MOUSE; MYELOID DENDRITIC CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PARASITE LOAD; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPLEEN; TH1 CELL; TH17 CELL; ANIMAL; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; NEUTROPHIL; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; VISCERAL LEISHMANIASIS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHIL INFILTRATION; NEUTROPHILS; SIGNAL TRANSDUCTION; SPLEEN; TH1 CELLS; TH17 CELLS; TOLL-LIKE RECEPTOR 9;

EID: 84949660666     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00975-15     Document Type: Article

References (56)

1. Liese J, Schleicher U, Bogdan C. 2008. The innate immune response against Leishmania parasites. Immunobiology 213:377-387. http://dx.doi.org/10.1016/j.imbio.2007.12.005.
2. Engwerda CR, Kaye PM. 2000. Organ-specific immune responses associated with infectious disease. Immunol Today 21:73-78. http://dx.doi.org/10.1016/S0167-5699(99)01549-2.
3. Ghosh K, Sharma G, Saha A, Kar S, Das PK, Ukil A. 2013. Successful therapy of visceral leishmaniasis with curdlan involves T-helper 17 cytokines. J Infect Dis 207:1016-1025. http://dx.doi.org/10.1093/infdis/jis771.
4. Bafica A, Santiago HC, Goldszmid R, Ropert C, Gazzinelli RT, Sher A. 2006. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol 177:3515-3519. http://dx.doi.org/10.4049/jimmunol.177.6.3515.
5. Debierre-Grockiego F, Azzouz N, Schmidt J, Dubremetz J-F, Geyer H, Geyer R, Weingart R, Schmidt RR, Schwarz RT. 2003. Roles of glycosylphosphatidylinositols of Toxoplasma gondii induction of tumor necrosis factor-α production in macrophages. J Biol Chem 278:32987-32993. http://dx.doi.org/10.1074/jbc.M304791200.
6. Shoda LKM, Kegerreis KA, Suarez CE, Roditi I, Corral RS, Bertot GM, Norimine J, Brown WC. 2001. DNA from protozoan parasites Babesia bovis, Trypanosoma cruzi, and T. brucei is mitogenic for B lymphocytes and stimulates macrophage expression of interleukin-12, tumor necrosis factor alpha, and nitric oxide. Infect Immun 69:2162-2171. http://dx.doi.org/10.1128/IAI.69.4.2162-2171.2001.
7. Campos MAS, Almeida IC, Takeuchi O, Akira S, Valente EP, Procópio DO, Travassos LR, Smith JA, Golenbock DT, Gazzinelli RT. 2001. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J Immunol 167:416-423. http://dx.doi.org/10.4049/jimmunol.167.1.416.
8. de Veer MJ, Curtis JM, Baldwin TM, DiDonato JA, Sexton A, McConville MJ, Handman E, Schofield L. 2003. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur J Immunol 33:2822-2831. http://dx.doi.org/10.1002/eji.200324128.
9. McConville MJ, Schnur LF, Jaffe C, Schneider P. 1995. Structure of Leishmania lipophosphoglycan: inter-and intra-specific polymorphism in Old World species. Biochem J 310:807-818. http://dx.doi.org/10.1042/bj3100807.
10. Muraille E, De Trez C, Brait M, De Baetselier P, Leo O, Carlier Y. 2003. Genetically resistant mice lacking MyD88-adapter protein display a high susceptibility to Leishmania major infection associated with a polarized Th2 response. J Immunol 170:4237-4241. http://dx.doi.org/10.4049/jimmunol.170.8.4237.
11. De Trez C, Brait M, Leo O, Aebischer T, Torrentera FA, Carlier Y, Muraille E. 2004. Myd88-dependent in vivo maturation of splenic dendritic cells induced by Leishmania donovani and other Leishmania species. Infect Immun 72:824-832. http://dx.doi.org/10.1128/IAI.72.2.824-832.2004.
12. Osanya A, Song EH, Metz K, Shimak RM, Boggiatto PM, Huffman E, Johnson C, Hostetter JM, Pohl NLB, Petersen CA. 2011. Pathogenderived oligosaccharides improve innate immune response to intracellular parasite infection. Am J Pathol 179:1329-1337. http://dx.doi.org/10.1016/j.ajpath.2011.05.053.
13. Bhattacharya P, Bhattacharjee S, Gupta G, Majumder S, Adhikari A, Mukherjee A, Majumdar SB, Saha B, Majumdar S. 2010. Arabinosylated lipoarabinomannan-mediated protection in visceral leishmaniasis through up-regulation of Toll-like receptor 2 signaling: an immunoprophylactic approach. J Infect Dis 202:145-155. http://dx.doi.org/10.1086/653210.
14. Flandin JF, Chano F, Descoteaux A. 2006. RNA interference reveals a role for TLR2 and TLR3 in the recognition of Leishmania donovani promastigotes by interferon-α-primed macrophages. Eur J Immunol 36:411-420. http://dx.doi.org/10.1002/eji.200535079.
15. Kropf P, Freudenberg MA, Modolell M, Price HP, Herath S, Antoniazi S, Galanos C, Smith DF, Müller I. 2004. Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infect Immun 72:1920-1928. http://dx.doi.org/10.1128/IAI.72.4.1920-1928.2004.
16. Abou Fakher FH, Rachinel N, Klimczak M, Louis J, Doyen N. 2009. TLR9-dependent activation of dendritic cells by DNA from Leishmania major favors Th1 cell development and the resolution of lesions. J Immunol 182:1386-1396. http://dx.doi.org/10.4049/jimmunol.182.3.1386.
17. Carvalho LP, Petritus PM, Trochtenberg AL, Zaph C, Hill DA, Artis D, Scott P. 2012. Lymph node hypertrophy following Leishmania major infection is dependent on TLR9. J Immunol 188:1394-1401. http://dx.doi.org/10.4049/jimmunol.1101018.
18. Weinkopff T, Mariotto A, Simon G, Hauyon-La Torre Y, Auderset F, Schuster S, Zangger H, Fasel N, Barral A, Tacchini-Cottier F. 2013. Role of Toll-like receptor 9 signaling in experimental Leishmania braziliensis infection. Infect Immun 81:1575-1584. http://dx.doi.org/10.1128/IAI.01401-12.
19. Schleicher U, Liese J, Knippertz I, Kurzmann C, Hesse A, Heit A, Fischer JAA, Weiss S, Kalinke U, Kunz S. 2007. NK cell activation in visceral leishmaniasis requires TLR9, myeloid DCs, and IL-12, but is independent of plasmacytoid DCs. J Exp Med 204:893-906. http://dx.doi.org/10.1084/jem.20061293.
20. Carregaro V, Valenzuela JG, Cunha TM, Verri WA, Grespan R, Matsumura G, Ribeiro JMC, Elnaiem DE, Silva JS, Cunha FQ. 2008. Phlebotomine salivas inhibit immune inflammation-induced neutrophil migration via an autocrine DC-derived PGE2/IL-10 sequential pathway. J Leukoc Biol 84:104-114. http://dx.doi.org/10.1189/jlb.1107797.
21. Colonna M, Trinchieri G, Liu Y-J. 2004. Plasmacytoid dendritic cells in immunity. Nat Immunol 5:1219-1226. http://dx.doi.org/10.1038/ni1141.
22. Coura-Vital W, Marques M, Giunchetti R, Teixeira-Carvalho A, Moreira N, Vitoriano-Souza J, Vieira P, Carneiro C, Corrêa-Oliveira R, Martins-Filho O. 2011. Humoral and cellular immune responses in dogs with inapparent natural Leishmania infantum infection. Vet J 190:e43-e47. http://dx.doi.org/10.1016/j.tvjl.2011.04.005.
23. Rodrigues V, Laforge M, Campillo-Gimenez L, Soundaramourty C, Correia-de-Oliveira A, Dinis-Oliveira RJ, Ouaissi A, Cordeiro-da-Silva A, Silvestre R, Estaquier J. 2014. Abortive T follicular helper development is associated with a defective humoral response in Leishmania infantum-infected macaques. PLoS Pathog 10:e1004096. http://dx.doi.org/10.1371/journal.ppat.1004096.
24. Fan J, Malik AB. 2003. Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat Med 9:315-321. http://dx.doi.org/10.1038/nm832.
25. Sabroe I, Prince LR, Jones EC, Horsburgh MJ, Foster SJ, Vogel SN, Dower SK, Whyte MKB. 2003. Selective roles for Toll-like receptor (TLR) 2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol 170:5268-5275. http://dx.doi.org/10.4049/jimmunol.170.10.5268.
26. Gorak P, Engwerda CR, Kaye PM. 1998. Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur J Immunol 28:687-695.
27. Von Stebut E, Belkaid Y, Jakob T, Sacks DL, Udey MC. 1998. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J Exp Med 188:1547-1552. http://dx.doi.org/10.1084/jem.188.8.1547.
28. León B, López-Bravo M, Ardavín C. 2007. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26:519-531. http://dx.doi.org/10.1016/j.immuni.2007.01.017.
29. Broz P, Monack DM. 2013. Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13:551-565. http://dx.doi.org/10.1038/nri3479.
30. Nandi B, Behar SM. 2011. Regulation of neutrophils by interferon-α limits lung inflammation during tuberculosis infection. J Exp Med 208: 2251-2262. http://dx.doi.org/10.1084/jem.20110919.
31. Sacramento LA, Cunha FQ, de Almeida RP, da Silva JS, Carregaro V. 2014. Protective role of 5-lipoxigenase during Leishmania infantum infec-tion is associated with Th17 subset. Biomed Res Int 2014:264270. http://dx.doi.org/10.1155/2014/264270.
32. Volpi C, Fallarino F, Pallotta MT, Bianchi R, Vacca C, Belladonna ML, Orabona C, De Luca A, Boon L, Romani L. 2013. High doses of CpG oligodeoxynucleotides stimulate a tolerogenic TLR9-TRIF pathway. Nat Commun 4:1852. http://dx.doi.org/10.1038/ncomms2874.
33. Cezário GAG, Oliveira LRC, Peresi E, Nicolete VC, Polettini J, Lima CRG, Gatto M, Calvi SA. 2011. Analysis of the expression of Toll-like receptors 2 and 4 and cytokine production during experimental Leishmania chagasi infection. Mem Inst Oswaldo Cruz 106:573-583. http://dx.doi.org/10.1590/S0074-02762011000500010.
34. Liese J, Schleicher U, Bogdan C. 2007. TLR9 signaling is essential for the innate NK cell response in murine cutaneous leishmaniasis. Eur J Immunol 37:3424-3434. http://dx.doi.org/10.1002/eji.200737182.
35. Johnson AC, Heinzel FP, Diaconu E, Sun Y, Hise AG, Golenbock D, Lass JH, Pearlman E. 2005. Activation of Toll-like receptor (TLR) 2, TLR4, and TLR9 in the mammalian cornea induces MyD88-dependent corneal inflammation. Invest Ophthalmol Vis Sci 46:589-595. http://dx.doi.org/10.1167/iovs.04-1077.
36. Huang X, Barrett RP, McClellan SA, Hazlett LD. 2005. Silencing Tolllike receptor-9 in Pseudomonas aeruginosa keratitis. Invest Ophthalmol Vis Sci 46:4209-4216. http://dx.doi.org/10.1167/iovs.05-0185.
37. Trevelin SC, Alves-Filho JC, Sônego F, Turato W, Nascimento DC, Souto FO, Cunha TM, Gazzinelli RT, Cunha FQ. 2012. Toll-like receptor 9 activation in neutrophils impairs chemotaxis and reduces sepsis outcome. Crit Care Med 40:2631-2637. http://dx.doi.org/10.1097/CCM.0b013e318258fb70.
38. Müller K, Zandbergen G, Hansen B, Laufs H, Jahnke N, Solbach W, Laskay T. 2001. Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Med Microbiol Immunol 190:73-76. http://dx.doi.org/10.1007/s004300100084.
39. Thalhofer CJ, Chen Y, Sudan B, Love-Homan L, Wilson ME. 2011. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi. Infect Immun 79:108-117. http://dx.doi.org/10.1128/IAI.00338-10.
40. Charmoy M, Megnekou R, Allenbach C, Zweifel C, Perez C, Monnat K, Breton M, Ronet C, Launois P, Tacchini-Cottier F. 2007. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 82:288-299. http://dx.doi.org/10.1189/jlb.0706440.
41. McFarlane E, Perez C, Charmoy M, Allenbach C, Carter KC, Alexander J, Tacchini-Cottier F. 2008. Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infect Immun 76:532-541. http://dx.doi.org/10.1128/IAI.01388-07.
42. Rousseau D, Demartino S, Ferrua B, Michiels JF, Anjuère F, Fragaki K, Le Fichoux Y, Kubar J. 2001. In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection.BMCMicrobiol 1:17. http://dx.doi.org/10.1186/1471-2180-1-17.
43. Smelt SC, Cotterell SEJ, Engwerda CR, Kaye PM. 2000. B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J Immunol 164:3681-3688. http://dx.doi.org/10.4049/jimmunol.164.7.3681.
44. Lima GMAC, Vallochi AL, Silva UR, Bevilacqua EMAF, Kiffer MMF, Abrahamsohn IA. 1998. The role of polymorphonuclear leukocytes in the resistance to cutaneous Leishmaniasis. Immunol Lett 64:145-151. http://dx.doi.org/10.1016/S0165-2478(98)00099-6.
45. Tacchini-Cottier F, Zweifel C, Belkaid Y, Mukankundiye C, Vasei M, Launois P, Milon G, Louis J. 2000. An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J Immunol 165:2628-2636. http://dx.doi.org/10.4049/jimmunol.165.5.2628.
46. Ribeiro-Gomes FL, Otero AC, Gomes NA, Moniz-de-Souza MCA, Cysne-Finkelstein L, Arnholdt AC, Calich VL, Coutinho SG, Lopes MF, DosReis GA. 2004. Macrophage interactions with neutrophils regulate Leishmania major infection. J Immunol 172:4454-4462. http://dx.doi.org/10.4049/jimmunol.172.7.4454.
47. Sabroe I, Dower SK, Whyte MKB. 2005. The role of Toll-like receptors in the regulation of neutrophil migration, activation, and apoptosis. Clin Infect Dis 41:S421-S426. http://dx.doi.org/10.1086/431992.
48. Badolato R, Sacks DL, Savoia D, Musso T. 1996. Leishmania major: infection of human monocytes induces expression of IL-8 and MCAF. Exp Parasitol 82:21-26. http://dx.doi.org/10.1006/expr.1996.0003.
49. van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, Solbach W, Laskay T. 2004. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173:6521-6525. http://dx.doi.org/10.4049/jimmunol.173.11.6521.
50. Liu D, Uzonna JE. 2012. The early interaction of Leishmania with macrophages and dendritic cells and its influence on the host immune response. Front Cell Infect Microbiol 2:83. http://dx.doi.org/10.3389/fcimb.2012.00083.
51. Basu A, Chakrabarti G, Saha A, Bandyopadhyay S. 2001. Modulation of CD11C+ splenic dendritic cell functions in murine visceral leishmaniasis: correlation with parasite replication in the spleen. Immunology 99:305-313.
52. Moll H. 2000. The role of dendritic cells at the early stages of Leishmania infection. Adv Exp Med Biol 497:163-173.
53. Proietto AI, O'Keeffe M, Gartlan K, Wright MD, Shortman K, Wu L, Lahoud MH. 2004. Differential production of inflammatory chemokines by murine dendritic cell subsets. Immunobiology 209:163-172. http://dx.doi.org/10.1016/j.imbio.2004.03.002.
54. Guillerey C, Mouriès J, Polo G, Doyen N, Law HK, Chan S, Kastner P, Leclerc C, Dadaglio G. 2012. Pivotal role of plasmacytoid dendritic cells in inflammation and NK-cell responses after TLR9 triggering in mice. Blood 120:90-99. http://dx.doi.org/10.1182/blood-2012-02-410936.
55. Ashok D, Acha-Orbea H. 2014. Timing is everything: dendritic cell subsets in murine Leishmania infection. Trends Parasitol 30:499-507. http://dx.doi.org/10.1016/j.pt.2014.08.001.
56. De Filippo K, Dudeck A, Hasenberg M, Nye E, van Rooijen N, Hartmann K, Gunzer M, Roers A, Hogg N. 2013. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood 121:4930-4937. http://dx.doi.org/10.1182/blood-2013-02-486217.