Antimony Resistant Leishmania donovani but Not Sensitive Ones Drives Greater Frequency of Potent T-Regulatory Cells upon Interaction with Human PBMCs: Role of IL-10 and TGF-β in Early Immune Response

PLoS Neglected Tropical Diseases

Volumn 8, Issue 7, 2014, Pages

  Guha, Rajan ^a   Das, Shantanabha ^a   Ghosh, June ^a   Sundar, Shyam ^b   Dujardin, Jean Claude ^c   Roy, Syamal ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b BANARAS HINDU UNIVERSITY   (India)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; CD14 ANTIGEN; GAMMA INTERFERON; GLYCOPHORIN A; INTERLEUKIN 10; INTERLEUKIN 27; LATENCY ASSOCIATED PEPTIDE; RNA 18S; TRANSFORMING GROWTH FACTOR BETA; ANTIPROTOZOAL AGENT; IL10 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETER; FLUORESCENCE ACTIVATED CELL SORTING; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; LEISHMANIA DONOVANI; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROMASTIGOTE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; CELL CULTURE; IMMUNOLOGY; MONONUCLEAR CELL;

ANTIMONY; ANTIPROTOZOAL AGENTS; CELLS, CULTURED; HUMANS; INTERLEUKIN-10; LEISHMANIA DONOVANI; LEUKOCYTES, MONONUCLEAR; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84905457298     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002995     Document Type: Article

References (62)

1. Croft SL, Sundar S, Fairlamb AH, (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19: 111-126.
2. Sundar S, Chatterjee M, (2006) Visceral leishmaniasis- current therapeutic modalities. Indian J Med Res 123: 345-352.
3. Vanaerschot M, Decuypere S, Downing T, Imamura H, Stark O, et al. (2012) Genetic markers for SSG resistance in Leishmania donovani and SSG treatment failure in visceral leishmaniasis patients of the Indian subcontinent. J Infect Dis 206: 752-755.
4. Awasthi A, Mathur RK, Saha B, (2004) Immune response to Leishmania infection. Indian J Med Res 119: 238-258.
5. Biedermann T, Zimmermann S, Himmelrich H, Gumy A, Egeter O, et al. (2001) IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat Immunol 2: 1054-1060.
6. Thakur CP, Mitra DK, Narayan S, (2003) Skewing of cytokine profiles towards T helper cell type 2 response in visceral leishmaniasis patients unresponsive to sodium antimony gluconate. Trans R Soc Trop Med Hyg 97: 409-412.
7. Chakraborty D, Banerjee S, Sen A, Banerjee KK, Das P, et al. (2005) Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J Immunol 175: 3214-3224.
8. Meier CL, Svensson M, Kaye PM, (2003) Leishmania-induced inhibition of macrophage antigen presentation analyzed at the single-cell level. J Immunol 171: 6706-6713.
9. Mendez S, Reckling SK, Piccirillo CA, Sacks D, Belkaid Y, (2004) Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med 200: 201-210.
10. Alexander J, Brombacher F, (2012) T helper1/t helper2 cells and resistance/susceptibility to leishmania infection: is this paradigm still relevant? Front Immunol 3: 80.
11. Liew FY, (1989) Functional heterogeneity of CD4+ T cells in leishmaniasis. Immunol Today 10: 40-45.
12. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL, (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
13. Rai AK, Thakur CP, Singh A, Seth T, Srivastava SK, et al. (2012) Regulatory T cells suppress T cell activation at the pathologic site of human visceral leishmaniasis. PLoS One 7: e31551.
14. Curotto de Lafaille MA, Lafaille JJ, (2009) Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30: 626-635.
15. Facciabene A, Motz GT, Coukos G, (2012) T-regulatory cells: key players in tumor immune escape and angiogenesis. Cancer Res 72: 2162-2171.
16. Mukhopadhyay R, Mukherjee S, Mukherjee B, Naskar K, Mondal D, et al. (2011) Characterisation of antimony-resistant Leishmania donovani isolates: biochemical and biophysical studies and interaction with host cells. Int J Parasitol 41: 1311-1321.
17. Haldar AK, Yadav V, Singhal E, Bisht KK, Singh A, et al. (2010) Leishmania donovani isolates with antimony-resistant but not-sensitive phenotype inhibit sodium antimony gluconate-induced dendritic cell activation. PLoS Pathog 6: e1000907.
18. Nylen S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, et al. (2007) Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 204: 805-817.
19. Nylen S, Sacks D, (2007) Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol 28: 378-384.
20. Aslan H, Dey R, Meneses C, Castrovinci P, Jeronimo SM, et al. (2013) A new model of progressive visceral leishmaniasis in hamsters by natural transmission via bites of vector sand flies. J Infect Dis 207: 1328-1338.
21. Mukherjee B, Mukhopadhyay R, Bannerjee B, Chowdhury S, Mukherjee S, et al. (2013) Antimony-resistant but not antimony-sensitive Leishmania donovani up-regulates host IL-10 to overexpress multidrug-resistant protein 1. Proc Natl Acad Sci U S A 110: E575-582.
22. Bosque F, Saravia NG, Valderrama L, Milon G, (2000) Distinct innate and acquired immune responses to Leishmania in putative susceptible and resistant human populations endemically exposed to L. (Viannia) panamensis infection. Scand J Immunol 51: 533-541.
23. Samant M, Gupta R, Kumari S, Misra P, Khare P, et al. (2009) Immunization with the DNA-encoding N-terminal domain of proteophosphoglycan of Leishmania donovani generates Th1-type immunoprotective response against experimental visceral leishmaniasis. J Immunol 183: 470-479.
24. Rama Iniguez S, Dea-Ayuela MA, Sanchez-Brunete JA, Torrado JJ, Alunda JM, et al. (2006) Real-time reverse transcription-PCR quantification of cytokine mRNA expression in golden Syrian hamster infected with Leishmania infantum and treated with a new amphotericin B formulation. Antimicrob Agents Chemother 50: 1195-1201.
25. Perez-Victoria JM, Perez-Victoria FJ, Parodi-Talice A, Jimenez IA, Ravelo AG, et al. (2001) Alkyl-lysophospholipid resistance in multidrug-resistant Leishmania tropica and chemosensitization by a novel P-glycoprotein-like transporter modulator. Antimicrob Agents Chemother 45: 2468-2474.
26. Saha S, Mondal S, Ravindran R, Bhowmick S, Modak D, et al. (2007) IL-10- and TGF-beta-mediated susceptibility in kala-azar and post-kala-azar dermal leishmaniasis: the significance of amphotericin B in the control of Leishmania donovani infection in India. J Immunol 179: 5592-5603.
27. Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, et al. (2006) CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 203: 1701-1711.
28. Wang R, Kozhaya L, Mercer F, Khaitan A, Fujii H, et al. (2009) Expression of GARP selectively identifies activated human FOXP3+ regulatory T cells. Proc Natl Acad Sci U S A 106: 13439-13444.
29. Rogers KA, Titus RG, (2004) Characterization of the early cellular immune response to Leishmania major using peripheral blood mononuclear cells from Leishmania-naive humans. Am J Trop Med Hyg 71: 568-576.
30. Rogers KA, Titus RG, (2004) The human cytokine response to Leishmania major early after exposure to the parasite in vitro. J Parasitol 90: 557-563.
31. Kimblin N, Peters N, Debrabant A, Secundino N, Egen J, et al. (2008) Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci U S A 105: 10125-10130.
32. Maia C, Seblova V, Sadlova J, Votypka J, Volf P, (2011) Experimental transmission of Leishmania infantum by two major vectors: a comparison between a viscerotropic and a dermotropic strain. PLoS Negl Trop Dis 5: e1181.
33. Rogers ME, Corware K, Muller I, Bates PA, (2010) Leishmania infantum proteophosphoglycans regurgitated by the bite of its natural sand fly vector, Lutzomyia longipalpis, promote parasite establishment in mouse skin and skin-distant tissues. Microbes Infect 12: 875-879.
34. Diaz YR, Rojas R, Valderrama L, Saravia NG, (2010) T-bet, GATA-3, and Foxp3 expression and Th1/Th2 cytokine production in the clinical outcome of human infection with Leishmania (Viannia) species. J Infect Dis 202: 406-415.
35. Nylen S, Mortberg U, Kovalenko D, Satti I, Engstrom K, et al. (2001) Differential induction of cellular responses by live and dead Leishmania promastigotes in healthy donors. Clin Exp Immunol 124: 43-53.
36. Hviid L, Sorensen AL, Kharazmi A, Theander TG, (1990) Functional and phenotypic changes in human lymphocytes after coincubation with Leishmania donovani in vitro. Infect Immun 58: 3163-3167.
37. Costa SR, D'Oliveira A Jr, Bacellar O, Carvalho EM, (1999) T cell response of asymptomatic Leishmania chagasi infected subjects to recombinant leishmania antigens. Mem Inst Oswaldo Cruz 94: 367-370.
38. White AC Jr, Castes M, Garcia L, Trujillo D, Zambrano L, (1992) Leishmania chagasi antigens recognized in cured visceral leishmaniasis and asymptomatic infection. Am J Trop Med Hyg 46: 123-131.
39. Singh OP, Gidwani K, Kumar R, Nylen S, Jones SL, et al. (2012) Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clin Vaccine Immunol 19: 961-966.
40. Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, et al. (2004) Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci U S A 101: 4560-4565.
41. Savage ND, de Boer T, Walburg KV, Joosten SA, van Meijgaarden K, et al. (2008) Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1. J Immunol 181: 2220-2226.
42. Walther M, Tongren JE, Andrews L, Korbel D, King E, et al. (2005) Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23: 287-296.
43. Li S, Gowans EJ, Chougnet C, Plebanski M, Dittmer U, (2008) Natural regulatory T cells and persistent viral infection. J Virol 82: 21-30.
44. Peng G, Li S, Wu W, Sun Z, Chen Y, et al. (2008) Circulating CD4+ CD25+ regulatory T cells correlate with chronic hepatitis B infection. Immunology 123: 57-65.
45. Nasser R, Pelegrin M, Plays M, Gros L, Piechaczyk M, (2013) Control of regulatory T cells is necessary for vaccine-like effects of antiviral immunotherapy by monoclonal antibodies. Blood 121: 1102-1111.
46. Guha R, Das S, Ghosh J, Naskar K, Mandala A, et al. (2013) Heterologous priming-boosting with DNA and vaccinia virus expressing kinetoplastid membrane protein-11 induces potent cellular immune response and confers protection against infection with antimony resistant and sensitive strains of Leishmania (Leishmania) donovani. Vaccine 31: 1905-1915.
47. Guha R, Gupta D, Rastogi R, Vikram R, Krishnamurthy G, et al. (2013) Vaccination with leishmania hemoglobin receptor-encoding DNA protects against visceral leishmaniasis. Sci Transl Med 5: 202ra121.
48. Alvar J, Croft SL, Kaye P, Khamesipour A, Sundar S, et al. (2013) Case study for a vaccine against leishmaniasis. Vaccine 31 (Suppl 2):: B244-249.
49. Stober CB, Lange UG, Roberts MT, Alcami A, Blackwell JM, (2005) IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J Immunol 175: 2517-2524.
50. Katara GK, Ansari NA, Verma S, Ramesh V, Salotra P, (2011) Foxp3 and IL-10 expression correlates with parasite burden in lesional tissues of post kala azar dermal leishmaniasis (PKDL) patients. PLoS Negl Trop Dis 5: e1171.
51. Battaglia M, Roncarolo MG, (2009) The Tregs' world according to GARP. Eur J Immunol 39: 3296-3300.
52. Maloy KJ, Powrie F, (2001) Regulatory T cells in the control of immune pathology. Nat Immunol 2: 816-822.
53. Stockis J, Colau D, Coulie PG, Lucas S, (2009) Membrane protein GARP is a receptor for latent TGF-beta on the surface of activated human Treg. Eur J Immunol 39: 3315-3322.
54. Nakamura K, Kitani A, Strober W, (2001) Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 194: 629-644.
55. van Vliet SJ, Garcia-Vallejo JJ, van Kooyk Y, (2008) Dendritic cells and C-type lectin receptors: coupling innate to adaptive immune responses. Immunol Cell Biol 86: 580-587.
56. Kapsenberg ML, (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 3: 984-993.
57. Vanaerschot M, De Doncker S, Rijal S, Maes L, Dujardin JC, et al. (2011) Antimonial resistance in Leishmania donovani is associated with increased in vivo parasite burden. PLoS One 6: e23120.
58. Resende M, Moreira D, Augusto J, Cunha J, Neves B, et al. (2013) Leishmania-infected MHC class IIhigh dendritic cells polarize CD4+ T cells toward a nonprotective T-bet+ IFN-gamma+ IL-10+ phenotype. J Immunol 191: 262-273.
59. Owens BM, Beattie L, Moore JW, Brown N, Mann JL, et al. (2012) IL-10-producing Th1 cells and disease progression are regulated by distinct CD11c(+) cell populations during visceral leishmaniasis. PLoS Pathog 8: e1002827.
60. Rogers M, Kropf P, Choi BS, Dillon R, Podinovskaia M, et al. (2009) Proteophosophoglycans regurgitated by Leishmania-infected sand flies target the L-arginine metabolism of host macrophages to promote parasite survival. PLoS Pathog 5: e1000555.
61. Ready PD, (2013) Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58: 227-250.
62. Gomes R, Oliveira F, (2012) The immune response to sand fly salivary proteins and its influence on leishmania immunity. Front Immunol 3: 110.