TLR4 and NKT cell synergy in immunotherapy against visceral leishmaniasis

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Karmakar, Subir ^a   Bhaumik, Siddhartha Kumar ^a,b   Paul, Joydeep ^a   De, Tripti ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; GALACTOSE; GAMMA INTERFERON; GLYCOSPHINGOPHOSPHOLIPID ANTIGEN; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; LIGAND; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; CD1D ANTIGEN; CD1D1 PROTEIN, MOUSE; GLYCOSPHINGOLIPID; PARASITE ANTIGEN; POLYSACCHARIDE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; FEMALE; IMMUNOTHERAPY; INTRACELLULAR SIGNALING; LEISHMANIA DONOVANI; MALE; MOLECULAR SENSOR; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PARASITE LOAD; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TH2 CELL; VISCERAL LEISHMANIASIS; ANIMAL; ANTIGEN PRESENTATION; BAGG ALBINO MOUSE; DRUG EFFECT; GENETICS; HAMSTER; IMMUNOLOGY; METABOLISM; METHODOLOGY;

ANIMALIA; LEISHMANIA DONOVANI;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD1D; ANTIGENS, PROTOZOAN; CRICETINAE; GLYCOSPHINGOLIPIDS; IMMUNOTHERAPY; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MICE; MICE, INBRED BALB C; NATURAL KILLER T-CELLS; POLYSACCHARIDES; TH1 CELLS; TOLL-LIKE RECEPTOR 4;

EID: 84861212277     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002646     Document Type: Article

References (62)

1. Murray HW, (2001) Clinical and experimental advances in treatment of visceral leishmaniasis. Antimicrob Agents Chemother 45: 2185-2197.
2. Sundar S, More DK, Singh MK, Singh VP, Sharma S, et al. (2000) Failure of pentavalent antimony in visceral leishmaniasis in India: report from the center of the Indian epidemic. Clin Infect Dis 31: 1104-1107.
3. Okwor I, Uzonna JE, (2009) Immunotherapy as a strategy for treatment of leishmaniasis: a review of the literature. Immunotherapy 1: 765-776.
4. Vincent MS, Gumperz JE, Brenner MB, (2003) Understanding the function of CD1-restricted T cells. Nat Immunol 4: 517-523.
5. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H, (2003) The regulatory role of Valpha14 NKT cells in innate and acquired immune response. Annu Rev Immunol 21: 483-513.
6. Bendelac A, Savage PB, Teyton L, (2007) The biology of NKT cells. Annu Rev Immunol 25: 297-336.
7. Mattner J, Debord KL, Ismail N, Goff RD, Cantu C 3rd, et al. (2005) Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434: 525-529.
8. Dissanayake S, Shahin A, (2007) Induction of interferon-gamma by Taenia crassiceps glycans and Lewis sugars in naive BALB/c spleen and peritoneal exudate cells. Mol Immunol 44: 1623-1630.
9. De-Majumdar T, (1992) Leishmania donovani:purification and partial characterization of a glycophosphosphingolipid antigen expressed on promastigote surface. Exp Parasitol 74: 251-260.
10. Baenziger JU, Fiete D, (1979) Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. J Biol Chem 254: 9795-9799.
11. Karmakar S, Paul J, De T, (2011) Leishmania donovani glycosphingolipid facilitates antigen presentation by inducing relocation of CD1d into lipid rafts in infected macrophages. Eur J Immunol 41: 1376-1387.
12. Bhaumik SK, Singh MK, Karmakar S, De T, (2008) Immuno stimulating glycophosphosphingolipid antigen from Leishmania donovani is recognized by visceral leishmaniasis patient sera. Mol Biochem Parasitol 159: 121-129.
13. Rosas LE, Keiser T, Barbi J, Satoskar AA, Septer A, et al. (2005) Genetic background influences immune responses and disease outcome of cutaneous L. mexicana infection in mice. Int Immunol 17: 1347-1357.
14. Tripathi P, Singh V, Naik S, (2007) Immune response to leishmania: paradox rather than paradigm. FEMS Immunol Med Microbiol 51: 229-242.
15. Alexander J, Satoskar AR, Russel DG, (1999) Leishmania species: models of intracellular parasitism. J Cell Sci 112: 2993-3002.
16. Bhaumik SK, Naskar K, De T, (2009) Complete protection against experimental visceral leishmaniasis with complete soluble antigen from attenuated Leishmania donovani promastigotes involves Th1-immunity and down-regulation of IL-10. Eur J Immunol 39: 2146-2160.
17. Tuon FF, Amato VS, Bacha HA, Almusai T, Durate MI, et al. (2008) Toll-like receptors and leishmaniasis. Infec Immun 76: 866-872.
18. Neeyea MG, Van der Meer JW, Sutmuller RP, Adema GJ, Kulberg BJ, (2005) From the Th1/Th2 paradigm towards a Toll-like receptor/T-helper bias. Antimicrob Agents Chemother 49: 3991-3996.
19. Maruo S, Oh-hora M, Ahn HJ, Ono S, Wysocka M, et al. (1997) B cells regulate CD40 ligand-induced IL-12 production in antigen-presenting cells (APC) during T cell/APC interactions. J Immunol 158: 120-126.
20. Krummen M, Balkow S, Shen L, Heinz S, Loquai C, et al. (2010) Release of IL-12 by dendritic cells activated by TLR ligation is dependent on MyD88 signaling, whereas TRIF signaling is indispensable for TLR synergy. J Leukoc Biol 88: 189-199.
21. Lauwerys BR, Garot N, Renauld JC, Houssiau FA, (2000) Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18. J Immunol 165: 1847-1853.
22. Baxeyanis CN, Gritzapis AD, Papamichail M, (2003) In vivo antitumor activity of NKT cells activated by the combination of IL-12 and IL-18. J Immunol 171: 2953-2959.
23. van der Wetering D, de Paus RA, van Dissel JT, van de Vosse E, (2009) IL-23 modulates CD56+/CD3- NK cell and CD56+/CD3+ NK-like T cell function differentially from IL-12. Int Immunol 21: 145-153.
24. Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, et al. (2008) NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol 180: 5167-5171.
25. Doisne JM, Soulard V, Becourt C, Amnial L, Henrot P, et al. (2011) Cutting edge: crucial role of IL-1 and IL-23 in the innate IL-17 response of peripheral lymph node NK1.1- invariant NKT cells to bacteria. J Immunol 186: 662-666.
26. Caielli S, Conforti-Andreoni C, Di Pierto C, Usuelli V, Badami E, et al. (2010) On/off TLR signaling decides proinflammatory or tolerogenic dendritic cell maturation upon CD1d-mediated interaction with invariant NKT cells. J immunol 185: 7317-7329.
27. Campos-Martin Y, Colmenares M, Gozalbo-Lopez B, Lopez-Nunez M, Savage PB, et al. (2006) Immature human dendritic cells infected with Leishmania infantum are resistant to NK-mediated cytolysis but are efficiently recognized by NKT cells. J Immunol 176: 6172-6179.
28. Stanley AC, Zhou Y, Amante FH, Randall LM, Haque A, (2008) Activation of invariant NKT cells exacerbates experimental visceral leishmaniasis. Plos Pathog 4: e1000028.
29. Mukherjee P, Ghosh AK, Ghosh AC, (2003) Infection pattern and immune response in the spleen and liver of BALB/c mice intracardially infected with Leishmania donovani amastigotes. Immunol Letters 86: 131-138.
30. Nieto A, Dominguez-Bernal G, Orden JA, De La Fuente R, Madrid-Elena N, et al. (2011) Mechanisms of resistance and susceptibility to experimental visceral leishmaniasis: BALB/c mouse versus Syrian hamster model. Vet Res 42: 39.
31. Wilson ME, Jeronimo SM, Pearson RD, (2005) Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog 38: 147-160.
32. Schulz O, Edwards AD, Schito M, Aliberti J, Manickasingham S, et al. (2000) CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 13: 453-462.
33. Hermans IF, Silk JD, Gileadi U, Masri SH, Shepherd D, et al. (2007) Dendritic Cell Function Can Be Modulated through Cooperative Actions of TLR Ligands and Invariant NKT Cells. J Immunol 178: 2721-2729.
34. Howard MD, Willis L, Wakarchuk W, St.Michael F, Cox A, (2011) Genetics and molecular specificity of sialylation of Histophilussomni lipooligosaccharide (LOS) and the effect of LOS sialylation on Toll-like receptor-4 signaling. Vet Microbiol 153: 163-172.
35. O'Mahony DS, Pham U, Iyer R, Hawn TR, Liles WC, (2008) Differential constitutive and cytokine-modulated expression of human toll-like receptors in primary neutrophils, monocytes, and macrophages. Int J Med Sci 5: 1-8.
36. Lee C-W, Chien C-S, Yang C-M, (2004) Lipoteichoic acid-stimulated p42/p44 MAPK activation via Toll-like receptor 2 in tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 286: L921-L930.
37. Kropf P, Freudenberg MA, Modolell M, Price HP, Herath 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.
38. Muraille E, De Trez C, Brait M, De Baetselier P, Leo O, et al. (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.
39. De Veer MJ, Curtis JM, Baldwin TM, DiDonato JA, Sexton A, et al. (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.
40. 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-gamma-primed macrophages. Eur J Immunol 36: 411-420.
41. Schleicher U, Liese J, Knippertz I, Kurzmann C, Hesse 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.
42. 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.
43. Kar S, Ukil A, Das PK, (2011) Cystatin cures visceral leishmaniasis by NF-κB mediated proinflammatory response through co-ordination of TLR/MyD88 signaling with p105-Tpl2-ERK pathway. Eur J Immunol 41: 116-127.
44. Kanzler H, Barrat FJ, Hessel EM, Coffman RL, (2007) Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nature Medicine 13: 552-559.
45. Alexander J, Bryson K, (2005) T helper (h)1/Th2 and Leishmania: paradox rather than paradigm. Immunol Letters 99: 17-23.
46. Netea MG, Van der Meer JW, Sutmuller RP, Adema GJ, Kulberg BJ, (2005) From the Th1/Th2 paradigm towards a Toll-like receptor/T-helper bias. Antimicrob Agents Chemother 49: 3991-3996.
47. Duthie MS, Windish HP, Fox CB, Reed SG, (2011) Use of defined TLR ligands as adjuvants within human vaccines. Immunol Rev 239: 178-196.
48. Medzhitov R, Janeway C Jr, (2000) Innate immune recognition: mechanism and pathways. Immunol Rev 173: 89-97.
49. Akira S, Takeda K, Kaisho T, (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2: 675-680.
50. Roberts MTM, (2005) Current understandings on the immunology of leishmaniasis and recent developments in prevention and treatment. Br Med Bull 75-76: 115-130.
51. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM, (2008) Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages. Produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog 4: e1000239.
52. Launois P, Maillard I, Pingel S, Swihart KG, Xenarios I, et al. (1997) IL-4 rapidly produced by V beta 4 V alpha 8 CD4+ T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity 6: 541-549.
53. Matthews DJ, Emson CL, McKenzie GJ, Jolin HE, Blackwell JM, et al. (2000) IL-13 is a susceptibility factor for Leishmania major infection. J Immunol 164: 1458-1462.
54. Satoskar A, Bluethmann H, Alexander J, (1995) Disruption of the murine interleukin-4 gene inhibits disease progression during Leishmania mexicana infection but does not increase control of Leishmania donovani infection. Infect Immun 63: 4894-4899.
55. Alexander J, Carter KC, Al-Fasi N, Satoskar A, Brombacher F, (2000) Endogenous IL-4 is necessary for effective drug therapy against visceral leishmaniasis. Eur J Immunol 30: 2935-2943.
56. Murray HW, Tsai CW, Liu J, Ma X, (2006) Visceral Leishmania donovani infection in interleukin-13-/- mice. Infect Immun 74: 2487-2490.
57. Mitchel ML, Keller AC, Paget C, Fujio M, Trottein F, et al. (2007) Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 204: 995-1001.
58. Leeden RW, Yu RK, (1982) Ganglioside: structure, isolation and analysis. In: Ginsburg V, editors. Methods Enzymology 83: 139-191.
59. Ryu EK, MacCoss M, (1979) Modifications of the Dittmer-Lester reagent for the detection of phospholipids derivatives on thin-layer chromatograms. J Lipid Res 20: 561-563.
60. Anderson K, Li SC, Li YT, (2000) Diphenylamine-aniline-phosphoric acid reagent, a versatile spray reagent for revealing glycoconjugates on thin-layer chromatography plates. Anal Biochem 287: 337-339.
61. Towbin H, Schoenenberger C, Ball R, Braun DG, Rosenfelder G, (1984) Glycosphingolipid-blotting: an immunological detection procedure after separation by thin layer chromatography. J Immunol Methods 72: 471-479.
62. Benlagha K, Wei DG, Veiga J, Teyton L, Bendelac A, (2005) Characterization of the early stages of thymic NKT cell development. J Exp Med 202: 485-492.