TLR9 and MyD88 are crucial for the maturation and activation of dendritic cells by paromomycin-miltefosine combination therapy in visceral leishmaniasis

British Journal of Pharmacology

Volumn 171, Issue 5, 2014, Pages 1260-1274

  Das, Sushmita ^a,b   Rani, Mukta ^a   Rabidas, Vidyanand ^a   Pandey, Krishna ^a   Sahoo, Ganesh Chandra ^a   Das, Pradeep ^a  

^a INDIAN COUNCIL OF MEDICAL RESEARCH   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

combination therapy; DC maturation; miltefosine; paromomycin; TLR9; visceral leishmaniasis

Indexed keywords

GAMMA INTERFERON; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MILTEFOSINE; MYELOID DIFFERENTIATION FACTOR 88; PAROMOMYCIN; TOLL LIKE RECEPTOR 9;

ADULT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CELL ACTIVATION; CELL MATURATION; CELL STIMULATION; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; COMBINATION CHEMOTHERAPY; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; DRUG DETERMINATION; DRUG EFFECT; DRUG PROTEIN BINDING; FEMALE; HUMAN; HUMAN CELL; IMMUNOREGULATION; LYMPHOCYTE ACTIVATION; MALE; MONOTHERAPY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; RNA INTERFERENCE; T LYMPHOCYTE; UPREGULATION; VISCERAL LEISHMANIASIS;

COMBINATION THERAPY; DC MATURATION; MILTEFOSINE; PAROMOMYCIN; TLR9; VISCERAL LEISHMANIASIS;

ADULT; ANTIPROTOZOAL AGENTS; CELLS, CULTURED; DENDRITIC CELLS; DRUG COMBINATIONS; FEMALE; HEK293 CELLS; HUMANS; INTERLEUKIN-10; INTERLEUKIN-12; LEISHMANIASIS, VISCERAL; MALE; MYELOID DIFFERENTIATION FACTOR 88; PAROMOMYCIN; PHOSPHORYLCHOLINE; TOLL-LIKE RECEPTOR 9;

EID: 84895092383     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12530     Document Type: Article

References (43)

1. 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.
2. Banchereau J, Steinman RM, (1998). Dendritic cells and the control of immunity. Nature 392: 245-252.
3. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. (2000). Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
4. Bellocchio S, Gaziano R, Bozza S, Rossi G, Montagnoli C, Perruccio K, et al. (2005). Liposomal amphotericin B activates antifungal resistance with reduced toxicity by diverting Toll-like receptor signaling from TLR-2 to TLR-4. J Antimicrob Chemother 55: 214-222.
5. Bern C, Adler-Moore J, Berenguer J, Boelaert M, den Boer M, Davidson RN, et al. (2006). Liposomal amphotericin B for the treatment of visceral leishmaniasis. Clin Infect Dis 43: 917-924.
6. Bhattacharya P, Gupta G, Majumder S, Adhikari A, Banerjee S, Halder K, et al. (2011). Arabinosylated lipoarabinomannan skews Th2 phenotype towards Th1 during Leishmania infection by chromatin modification: involvement of MAPK signaling. PLoS ONE 6: e24141.
7. Bowie JU, Lüthy R, Eisenberg D, (1991). A method to identify protein sequences that fold into a known three-dimensional structure. Science 253: 164-170.
8. Bryceson A, (2001). A policy for leishmaniasis with respect to the prevention and control of drug resistance. Trop Med Int Health 6: 928-934.
9. Chakraborty D, Banerjee S, Sen A, Banerjee KK, Das P, Roy S, (2005). Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J Immunol 175: 3214-3224.
10. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, et al. (2007). Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol 5: 873-882.
11. 1 re-programs TLR4 signaling in L. donovani infection: enhancement of SHP-1 and ubiquitin-editing enzyme A20. Immunol Cell Biol 90: 640-654.
12. Das S, Rani M, Pandey K, Sahoo GC, Rabidas VN, Singh D, et al. (2012). Combination of paromomycin and miltefosine promotes TLR4-dependent induction of anti-leishmanial immune response in vitro. J Antimicrob Chemother 67: 2373-2378.
13. Das VNR, Ranjan A, Bimal S, Siddique NA, Pandey K, Kumar N, et al. (2005). Magnitude of unresponsiveness to sodium stibogluconate in the treatment of visceral leishmaniasis in Bihar. Natl Med J India 18: 131-133.
14. Desjeux P, (2004). Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27: 305-318.
15. Gallego C, Golenbock D, Gomez MA, Saravia NG, (2011). Toll-like receptors participate in macrophage activation and intracellular control of Leishmania (Viannia) panamensis. Infect Immun 79: 2871-2879.
16. Garci'a-Herna'ndez R, Manzano JI, Castanys S, Gamarro F, (2012). Leishmania donovani develops resistance to drug combinations. PLoS Negl Trop Dis 6: e1974.
17. Gradoni L, Gramiccia M, Scalone A, (2003). Visceral leishmaniasis treatment. Emerg Infect Dis 9: 1617-1620.
18. Janeway CA Jr, Medzhitov R, (2002). Innate immune recognition. Annu Rev Immunol 20: 197-216.
19. Kaisho T, Akira S, (2001). Dendritic-cell function in Toll-like receptor and MyD88-knockout mice. Trends Immunol 2: 78-83.
20. Kaisho T, Takeuchi O, Kawai T, Hoshino K, Akira S, (2001). Endotoxin-induced maturation of MyD88-deficient dendritic cells. J Immunol 166: 5688-5694.
21. Kropf P, Freudenberg MA, Modolell M, Price HP, Herath S, Antoniazi S, et al. (2004). Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infect Immun 72: 1920-1928.
22. 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.
23. Medzhitov R, Janeway CA, (1997). Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 9: 4-9.
24. Moser M, Murphy KM, (2000). Dendritic cell regulation of TH1-TH2 development. Nat Immunol 1: 199-205.
25. Mukherjee AK, Gupta G, Adhikari A, Majumder S, Kar Mahapatra S, Bhattacharyya Majumdar S, et al. (2012). Miltefosine triggers a strong proinflammatory cytokine response during visceral leishmaniasis: role of TLR4 and TLR9. Int Immunopharmacol 12: 565-572.
26. Prez-Victoria FJ, Castanys S, Gamarro F, (2003). Leishmania donovani resistance to miltefosine involves a defective inward translocation of the drug. Antimicrob Agents Chemother 47: 2397-2403.
27. Raman VS, Bhatia A, Picone A, Whittle J, Bailor HR, O'Donnell J, et al. (2010). Applying TLR synergy in immunotherapy: implications in cutaneous leishmaniasis. J Immunol 185: 1701-1710.
28. Razonable RR, Henault M, Watson HL, Paya CV, (2005). Nystatin induces secretion of interleukin (IL)-1β, IL-8, and tumor necrosis factor alpha by a toll-like receptor-dependent mechanism. Antimicrob Agents Chemother 49: 3546-3549.
29. Saccani S, Pantano S, Natoli G, (2002). p38-Dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat Immunol 1: 69-75.
30. Sau K, Mambula SS, Latz E, Henneke P, Golenbock DT, Levitz SM, (2003). The antifungal drug amphotericin B promotes inflammatory cytokine release by a Toll-like receptor- and CD14-dependent mechanism. J Biol Chem 278: 37561-37568.
31. Schleicher U, Liese J, Knippertz I, Kurzmann C, Hesse A, Heit A, et al. (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.
32. Seifert K, Croft SL, (2006). In vitro and in vivo interactions between miltefosine and other antileishmanial drugs. Antimicrob Agents Chemother 50: 73-79.
33. Seifert K, Escobar P, Croft SL, (2010). In vitro activity of antileishmanial drugs against Leishmania donovani is host cell dependent. J Antimicrob Chemother 65: 508-511.
34. Sundar S, (2001). Drug resistance in Indian visceral leishmaniasis. Trop Med Int Health 6: 849-854.
35. Sundar S, Makharia A, More DK, Agrawal G, Voss A, Fischer C, et al. (2000). Short-course of oral miltefosine for treatment of visceral leishmaniasis. Clin Infect Dis 31: 1110-1113.
36. Sundar S, Jha TK, Thakur CP, Engel J, Sinderman H, Fischer C, et al. (2002). Oral miltefosine for Indian visceral leishmaniasis. N Engl J Med 347: 1739-1746.
37. Sundar S, Jha TK, Thakur CP, Sinha PK, Bhattacharya SK, (2007). Injectable paromomycin for visceral leishmaniasis in India. N Engl J Med 356: 2571-2581.
38. Sundar S, Sinha PK, Rai M, Verma DK, Nawin K, Alam S, et al. (2011). Comparison of short-course multidrug treatment with standard therapy for visceral leishmaniasis in India: an open-label, non-inferiority, randomised controlled trial. Lancet 377: 477-486.
39. Theiner G, Rössner S, Dalpke A, Bode K, Berger T, Gessner A, et al. (2008). TLR9 cooperates with TLR4 to increase IL-12 release by murine dendritic cells. Mol Immunol 45: 244-252.
40. Tuon FF, Fernandes ER, Pagliari C, Duarte MI, Amato VS, (2010). The expression of TLR9 in human cutaneous leishmaniasis is associated with granuloma. Parasite Immunol 2: 769-772.
41. Wadhone P, Maiti M, Agarwal R, Kamat V, Martin S, Saha B, (2009). Miltefosine promotes IFN-gamma-dominated anti-leishmanial immune response. J Immunol 182: 7146-7154.
42. Wang X, Loram LC, Ramos K, de Jesus AJ, Thomas J, Cheng K, et al. (2012). Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci USA 109: 6325-6330.
43. Zhu Q, Egelston C, Vivekanandhan A, Uematsu S, Akira S, Klinman DM, et al. (2008). Toll-like receptor ligands synergize through distinct dendritic cell pathways to induce T cell responses: implications for vaccines. Proc Natl Acad Sci USA 105: 16260-16265.