Immune responses during cutaneous and visceral leishmaniasis

Parasitology

Volumn 141, Issue 12, 2014, Pages 1544-1562

  Kedzierski, Lukasz ^a,b   Evans, Krystal J ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ADAPTIVE IMMUNITY; ANTIBODY SPECIFICITY; B LYMPHOCYTE; CYTOKINE RESPONSE; GRANULOMA; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LEISHMANIA; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKIN LEISHMANIASIS; T LYMPHOCYTE; VISCERAL LEISHMANIASIS;

ANIMALIA; HEXAPODA; PROTOZOA;

EID: 84906936557     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S003118201400095X     Document Type: Review

References (227)

1. Ahmed, S., Colmenares, M., Soong, L., Goldsmith-Pestana, K., Munstermann, L., Molina, R. and McMahon-Pratt, D. (2003). Intradermal infection model for pathogenesis and vaccine studies of murine visceral leishmaniasis. Infection and Immunity 71, 401-410.
2. Ajdary, S., Alimohammadian, M. H., Eslami, M. B., Kemp, K. and Kharazmi, A. (2000). Comparison of the immune profile of nonhealing cutaneous leishmaniasis patients with those with active lesions and those who have recovered from infection. Infection and Immunity 68, 1760-1764.
3. Alexander, C. E., Kaye, P. M. and Engwerda, C. R. (2001). CD95 is required for the early control of parasite burden in the liver of Leishmania donovani-infected mice. European Journal of Immunology 31, 1199-1210.
4. Alexander, J., Brombacher, F., McGachy, H. A., McKenzie, A. N., Walker, W. and Carter, K. C. (2002). An essential role for IL-13 in maintaining a non-healing response following Leishmania mexicana infection. European Journal of Immunology 32, 2923-2933.
5. Ali, A. (2002). Leishmaniases and HIV/AIDS co-infections: review of common features and management experiences. Ethiopian Medical Journal 40 (Suppl. 1), 37-49.
6. Amprey, J. L., Im, J. S., Turco, S. J., Murray, H.W., Illarionov, P. A., Besra, G. S., Porcelli, S. A. and Spath, G. F. (2004). A subset of liver NK T cells is activated during Leishmania donovani infection by CD1d-bound lipophosphoglycan. Journal of Experimental Medicine 200, 895-904. doi: 10.1084/jem.20040704.
7. Anam, K., Afrin, F., Banerjee, D., Pramanik, N., Guha, S. K., Goswami, R. P., Saha, S. K. and Ali, N. (1999). Differential decline in Leishmania membrane antigen-specific immunoglobulin G (IgG), IgM, IgE, and IgG subclass antibodies in Indian kala-azar patients after chemotherapy. Infection and Immunity 67, 6663-6669.
8. Anderson, C. F., Mendez, S. and Sacks, D. L. (2005). Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. Journal of Immunology 174, 2934-2941.
9. Anderson, C. F., Oukka, M., Kuchroo, V. J. and Sacks, D. (2007). CD4+CD25-Foxp3-Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. Journal of Experimental Medicine 204, 285-297. doi: 10.1084/jem.20061886.
10. Antinori, S., Cascio, A., Parravicini, C., Bianchi, R. and Corbellino, M. (2008). Leishmaniasis among organ transplant recipients. Lancet Infectious Diseases 8, 191-199. doi: 10.1016/S1473-3099(08)70043-4.
11. Arendse, B., Van Snick, J. and Brombacher, F. (2005). IL-9 is a susceptibility factor in Leishmania major infection by promoting detrimental Th2/type 2 responses. Journal of Immunology 174, 2205-2211.
12. Artis, D., Johnson, L. M., Joyce, K., Saris, C., Villarino, A., Hunter, C. A. and Scott, P. (2004). Cutting edge: early IL-4 production governs the requirement for IL-27-WSX-1 signaling in the development of protective Th1 cytokine responses following Leishmania major infection. Journal of Immunology 172, 4672-4675.
13. Ato, M., Stager, S., Engwerda, C. R. and Kaye, P. M. (2002). Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nature Immunology 3, 1185-1191. doi: 10.1038/ni861.
14. Ato, M., Maroof, A., Zubairi, S., Nakano, H., Kakiuchi, T. and Kaye, P. M. (2006). Loss of dendritic cell migration and impaired resistance to Leishmania donovani infection in mice deficient in CCL19 and CCL21. Journal of Immunology 176, 5486-5493.
15. Bacellar, O., Faria, D., Nascimento, M., Cardoso, T. M., Gollob, K. J., Dutra, W. O., Scott, P. and Carvalho, E.M. (2009). Interleukin 17 production among patients with American cutaneous leishmaniasis. Journal of Infectious Diseases 200, 75-78. doi: 10.1086/599380.
16. Badaro, R. and Johnson, W. D. Jr. (1993). The role of interferon-gamma in the treatment of visceral and diffuse cutaneous leishmaniasis. Journal of Infectious Diseases 167 (Suppl. 1), S13-S17.
17. Bajenoff, M., Breart, B., Huang, A. Y., Qi, H., Cazareth, J., Braud, V. M., Germain, R. N. and Glaichenhaus, N. (2006). Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. Journal of Experimental Medicine 203, 619-631.
18. Banchereau, J. and Steinman, R.M. (1998). Dendritic cells and the control of immunity. Nature 392, 245-252. doi: 10.1038/32588.
19. Bankoti, R., Gupta, K., Levchenko, A. and Stager, S. (2012). Marginal zone B cells regulate antigen-specific T cell responses during infection. Journal of Immunology 188, 3961-3971. doi: 10.4049/jimmunol.1102880.
20. Barral-Netto, M., Barral, A., Brownell, C. E., Skeiky, Y. A., Ellingsworth, L. R., Twardzik, D. R. and Reed, S. G. (1992). Transforming growth factor-beta in leishmanial infection: a parasite escape mechanism. Science 257, 545-548.
21. Basu, M. K. and Ray, M. (2005). Macrophage and Leishmania: an unacceptable coexistence. Critical Reviews in Microbiology 31, 145-154. doi: 10.1080/10408410591005101.
22. Beattie, L., Peltan, A., Maroof, A., Kirby, A., Brown, N., Coles, M., Smith, D. F. and Kaye, P. M. (2010a). Dynamic imaging of experimental Leishmania donovani-induced hepatic granulomas detects Kupffer cellrestricted antigen presentation to antigen-specific CD8T cells. PLOS Pathogens 6, e1000805. doi: 10.1371/journal.ppat.1000805.
23. Beattie, L., Svensson, M., Bune, A., Brown, N., Maroof, A., Zubairi, S., Smith, K. R. and Kaye, P. M. (2010b). Leishmania donovani-induced expression of signal regulatory protein alpha on Kupffer cells enhances hepatic invariant NKT-cell activation. European Journal of Immunology 40, 117-123. doi: 10.1002/eji.200939863.
24. Belkaid, Y. and Rouse, B. T. (2005). Natural regulatory T cells in infectious disease. Nature Immunology 6, 353-360. doi: 10.1038/ni1181.
25. Belkaid, Y., Butcher, B. and Sacks, D. L. (1998). Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. European Journal of Immunology 28, 1389-1400.
26. Belkaid, Y., Mendez, S., Lira, R., Kadambi, N., Milon, G. and Sacks, D. (2000). A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. Journal of Immunology 165, 969-977.
27. Belkaid, Y., Hoffmann, K. F., Mendez, S., Kamhawi, S., Udey, M. C., Wynn, T. A. and Sacks, D. L. (2001). The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. Journal of Experimental Medicine 194, 1497-1506.
28. Belkaid, Y., Piccirillo, C. A., Mendez, S., Shevach, E. M. and Sacks, D. L. (2002a). CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507.
29. Belkaid, Y., Von Stebut, E., Mendez, S., Lira, R., Caler, E., Bertholet, S., Udey, M. C. and Sacks, D. (2002b). CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. Journal of Immunology 168, 3992-4000.
30. Bennett, C. L., Misslitz, A., Colledge, L., Aebischer, T. and Blackburn, C. C. (2001). Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. European Journal of Immunology 31, 876-883.
31. Bern, C., Maguire, J. H. and Alvar, J. (2008). Complexities of assessing the disease burden attributable to leishmaniasis. PLOS Neglected Tropical Diseases 2, e313.
32. Bertholet, S., Goldszmid, R., Morrot, A., Debrabant, A., Afrin, F., Collazo-Custodio, C., Houde, M., Desjardins, M., Sher, A. and Sacks, D. (2006). Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. Journal of Immunology 177, 3525-3533.
33. Bhattacharyya, S., Ghosh, S., Jhonson, P. L., Bhattacharya, S. K. and Majumdar, S. (2001). Immunomodulatory role of interleukin-10 in visceral leishmaniasis: defective activation of protein kinase C-mediated signal transduction events. Infection and Immunity 69, 1499-1507. doi: 10.1128/IAI.69.3.1499-1507.2001.
34. Biedermann, T., Zimmermann, S., Himmelrich, H., Gumy, A., Egeter, O., Sakrauski, A. K., Seegmuller, I., Voigt, H., Launois, P., Levine, A. D., Wagner, H., Heeg, K., Louis, J. A. and Rocken, M. (2001). IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nature Immunology 2, 1054-1060.
35. Blackwell, J. M., Barton, C. H., White, J. K., Searle, S., Baker, A. M., Williams, H. and Shaw, M. A. (1995). Genomic organization and sequence of the human NRAMP gene: identification and mapping of a promoter region polymorphism. Molecular Medicine 1, 194-205.
36. Blackwell, J. M., Goswami, T., Evans, C. A., Sibthorpe, D., Papo, N., White, J. K., Searle, S., Miller, E. N., Peacock, C. S., Mohammed, H. and Ibrahim, M. (2001). SLC11A1 (formerly NRAMP1) and disease resistance. Cellular Microbiology 3, 773-784.
37. Bogdan, C., Moll, H., Solbach, W. and Rollinghoff, M. (1990). Tumor necrosis factor-alpha in combination with interferon-gamma, but not with interleukin 4 activates murine macrophages for elimination of Leishmania major amastigotes. European Journal of Immunology 20, 1131-1135. doi: 10.1002/eji.1830200528.
38. Bogdan, C., Vodovotz, Y. and Nathan, C. (1991). Macrophage deactivation by interleukin 10. Journal of Experimental Medicine 174, 1549-1555.
39. Bogdan, C., Rollinghoff, M. and Diefenbach, A. (2000). The role of nitric oxide in innate immunity. Immunological Reviews 173, 17-26.
40. Bohme, M.W., Evans, D. A., Miles, M. A. and Holborow, E. J. (1986). Occurrence of autoantibodies to intermediate filament proteins in human visceral leishmaniasis and their induction by experimental polyclonal B-cell activation. Immunology 59, 583-588.
41. Boulay, J. L., O'Shea, J. J. and Paul, W. E. (2003). Molecular phylogeny within type I cytokines and their cognate receptors. Immunity 19, 159-163.
42. Bourreau, E., Ronet, C., Darcissac, E., Lise, M. C., Sainte Marie, D., Clity, E., Tacchini-Cottier, F., Couppie, P. and Launois, P. (2009). Intralesional regulatory T-cell suppressive function during human acute and chronic cutaneous leishmaniasis due to Leishmania guyanensis. Infection and Immunity 77, 1465-1474. doi: 10.1128/IAI.01398-08.
43. Brombacher, F. (2000). The role of interleukin-13 in infectious diseases and allergy. Bioessays 22, 646-656.
44. Brown, D. R. and Reiner, S. L. (1999). Polarized helper-T-cell responses against Leishmania major in the absence of B cells. Infection and Immunity 67, 266-270.
45. Campanelli, A. P., Roselino, A. M., Cavassani, K. A., Pereira, M. S., Mortara, R. A., Brodskyn, C. I., Goncalves, H. S., Belkaid, Y., Barral-Netto, M., Barral, A. and Silva, J. S. (2006). CD4+CD25+ Tcells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. Journal of Infectious Diseases 193, 1313-1322. doi: 10.1086/502980.
46. Carrera, L., Gazzinelli, R. T., Badolato, R., Hieny, S., Muller, W., Kuhn, R. and Sacks, D. L. (1996). Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. Journal of Experimental Medicine 183, 515-526.
47. Cervia, J. S., Rosen, H. and Murray, H.W. (1993). Effector role of blood monocytes in experimental visceral leishmaniasis. Infection and Immunity 61, 1330-1333.
48. Chen, Q., Ghilardi, N., Wang, H., Baker, T., Xie, M. H., Gurney, A., Grewal, I. S. and de Sauvage, F. J. (2000). Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 407, 916-920. doi: 10.1038/35038103.
49. Cotterell, S. E., Engwerda, C. R. and Kaye, P. M. (1999). Leishmania donovani infection initiates T cell-independent chemokine responses, which are subsequently amplified in a T cell-dependent manner. European Journal of Immunology 29, 203-214.
50. Dalton, J. E., Maroof, A., Owens, B. M., Narang, P., Johnson, K., Brown, N., Rosenquist, L., Beattie, L., Coles, M. and Kaye, P. M. (2010). Inhibition of receptor tyrosine kinases restores immunocompetence and improves immune-dependent chemotherapy against experimental leishmaniasis in mice. Journal of Clinical Investigation 120, 1204-1216. doi: 10.1172/JCI41281.
51. Darrah, P. A., Patel, D. T., De Luca, P. M., Lindsay, R.W., Davey, D. F., Flynn, B. J., Hoff, S. T., Andersen, P., Reed, S. G., Morris, S. L., Roederer, M. and Seder, R. A. (2007). Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nature Medicine 13, 843-850. doi: 10.1038/nm1592.
52. Darrah, P. A., Hegde, S. T., Patel, D. T., Lindsay, R.W., Chen, L., Roederer, M. and Seder, R. A. (2010). IL-10 production differentially influences the magnitude, quality, and protective capacity of Th1 responses depending on the vaccine platform. Journal of Experimental Medicine 207, 1421-1433. doi: 10.1084/jem.20092532.
53. da Silva Santos, S., Boaventura, V., Ribeiro Cardoso, C., Tavares, N., Lordelo, M. J., Noronha, A., Costa, J., Borges, V. M., de Oliveira, C. I., Van Weyenbergh, J., Barral, A., Barral-Netto, M. and Brodskyn, C. I. (2013). CD8(+) granzyme B(+)-mediated tissue injury vs. CD4(+) IFNgamma(+)-mediated parasite killing in human cutaneous leishmaniasis. Journal of Investigative Dermatology 133, 1533-1540. doi: 10.1038/jid.2013.4.
54. Deak, E., Jayakumar, A., Cho, K.W., Goldsmith-Pestana, K., Dondji, B., Lambris, J. D. and McMahon-Pratt, D. (2010). Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. European Journal of Immunology 40, 1355-1368. doi: 10.1002/eji.200939455.
55. Demoulin, J. B. and Renauld, J. C. (1998). Interleukin 9 and its receptor: an overview of structure and function. International Reviews of Immunology 16, 345-364.
56. Dey, R., Majumder, N., Bhattacharyya Majumdar, S., Bhattacharjee, S., Banerjee, S., Roy, S. and Majumdar, S. (2007). Induction of host protective Th1 immune response by chemokines in Leishmania donovani-infected BALB/c mice. Scandinavian Journal of Immunology 66, 671-683. doi: 10.1111/j.1365-3083.2007. 02025.x.
57. Diefenbach, A., Schindler, H., Donhauser, N., Lorenz, E., Laskay, T., MacMicking, J., Rollinghoff, M., Gresser, I. and Bogdan, C. (1998). Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 8, 77-87.
58. Ehrchen, J. M., Roebrock, K., Foell, D., Nippe, N., von Stebut, E., Weiss, J. M., Munck, N. A., Viemann, D., Varga, G., Muller-Tidow, C., Schuberth, H. J., Roth, J. and Sunderkotter, C. (2010). Keratinocytes determine Th1 immunity during early experimental leishmaniasis. PLOS Pathogens 6, e1000871. doi: 10.1371/journal.ppat. 1000871.
59. Engwerda, C. R. and Kaye, P. M. (2000). Organ-specific immune responses associated with infectious disease. Immunology Today 21, 73-78. doi: 10.1016/S0167-5699(99)01549-2.
60. Engwerda, C. R., Smelt, S. C. and Kaye, P. M. (1996). An in vivo analysis of cytokine production during Leishmania donovani infection in scid mice. Experimental Parasitology 84, 195-202. doi: 10.1006/expr.1996.0105.
61. Engwerda, C. R., Murphy, M. L., Cotterell, S. E., Smelt, S. C. and Kaye, P. M. (1998). Neutralization of IL-12 demonstrates the existence of discrete organ-specific phases in the control of Leishmania donovani. European Journal of Immunology 28, 669-680.
62. Engwerda, C. R., Ato, M., Cotterell, S. E., Mynott, T. L., Tschannerl, A., Gorak-Stolinska, P. M. and Kaye, P. M. (2002). A role for tumor necrosis factor-alpha in remodeling the splenic marginal zone during Leishmania donovani infection. American Journal of Pathology 161, 429-437.
63. Engwerda, C. R., Ato, M., Stager, S., Alexander, C. E., Stanley, A. C. and Kaye, P. M. (2004). Distinct roles for lymphotoxin-alpha and tumor necrosis factor in the control of Leishmania donovani infection. American Journal of Pathology 165, 2123-2133.
64. Faria, D. R., Souza, P. E., Duraes, F. V., Carvalho, E. M., Gollob, K. J., Machado, P. R. and Dutra, W. O. (2009). Recruitment of CD8(+) T cells expressing granzyme A is associated with lesion progression in human cutaneous leishmaniasis. Parasite Immunology 31, 432-439. doi: 10.1111/j.1365-3024.2009. 01125.x.
65. Flohe, S., Lang, T. and Moll, H. (1997). Synthesis, stability, and subcellular distribution of major histocompatibility complex class II molecules in Langerhans cells infected with Leishmania major. Infection and Immunity 65, 3444-3450.
66. Galvao-Castro, B., Sa Ferreira, J. A., Marzochi, K. F., Marzochi, M. C., Coutinho, S. G. and Lambert, P. H. (1984). Polyclonal B cell activation, circulating immune complexes and autoimmunity in human American visceral leishmaniasis. Clinical and Experimental Immunology 56, 58-66.
67. Gautam, S., Kumar, R., Singh, N., Singh, A. K., Rai, M., Sacks, D., Sundar, S. and Nylen, S. (2014). CD8T cell exhaustion in human visceral leishmaniasis. Journal of Infectious Diseases 209, 290-299. doi: 10.1093/infdis/jit401.
68. Gessner, A., Blum, H. and Rollinghoff, M. (1993a). Differential regulation of IL-9-expression after infection with Leishmania major in susceptible and resistant mice. Immunobiology 189, 419-435.
69. Gessner, A., Vieth, M., Will, A., Schroppel, K. and Rollinghoff, M. (1993b). Interleukin-7 enhances antimicrobial activity against Leishmania major in murine macrophages. Infection and Immunity 61, 4008-4012.
70. Ghalib, H.W., Piuvezam, M. R., Skeiky, Y. A., Siddig, M., Hashim, F. A., el-Hassan, A. M., Russo, D. M. and Reed, S. G. (1993). Interleukin 10 production correlates with pathology in human Leishmania donovani infections. Journal of Clinical Investigation 92, 324-329. doi: 10.1172/JCI116570.
71. Ghalib, H.W., Whittle, J. A., Kubin, M., Hashim, F. A., el-Hassan, A. M., Grabstein, K. H., Trinchieri, G. and Reed, S. G. (1995). IL-12 enhances Th1-type responses in human Leishmania donovani infections. Journal of Immunology 154, 4623-4629.
72. Ghose, A. C., Haldar, J. P., Pal, S. C., Mishra, B. P. and Mishra, K. K. (1980). Serological investigations on Indian kala-azar. Clinical and Experimental Immunology 40, 318-326.
73. Gollob, K. J., Antonelli, L. R., Faria, D. R., Keesen, T. S. and Dutra, W. O. (2008). Immunoregulatory mechanisms and CD4-CD8-(double negative) T cell subpopulations in human cutaneous leishmaniasis: a balancing act between protection and pathology. International Immunopharmacology 8, 1338-1343. doi: 10.1016/j.intimp.2008.03.016.
74. Gonzalez-Lombana, C., Gimblet, C., Bacellar, O., Oliveira, W.W., Passos, S., Carvalho, L. P., Goldschmidt, M., Carvalho, E.M. and Scott, P. (2013). IL-17 mediates immunopathology in the absence of IL-10 following Leishmania major infection. PLOS Pathogens 9, e1003243. doi: 10.1371/journal.ppat.1003243.
75. Gorak, P. M., Engwerda, C. R. and Kaye, P. M. (1998). Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. European Journal of Immunology 28, 687-695.
76. Goswami, T., Bhattacharjee, A., Babal, P., Searle, S., Moore, E., Li, M. and Blackwell, J. M. (2001). Natural-resistance-associated macrophage protein 1 is an H+/bivalent cation antiporter. Biochemical Journal 354, 511-519.
77. Groux, H., Cottrez, F., Rouleau, M., Mauze, S., Antonenko, S., Hurst, S., McNeil, T., Bigler, M., Roncarolo, M. G. and Coffman, R. L. (1999). A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells. Journal of Immunology 162, 1723-1729.
78. Guimaraes-Costa, A. B., Nascimento, M. T., Froment, G. S., Soares, R. P., Morgado, F. N., Conceicao-Silva, F. and Saraiva, E. M. (2009). Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proceedings of the National Academy of Sciences USA 106, 6748-6753. doi: 10.1073/pnas.0900226106.
79. Gupta, G., Bhattacharjee, S., Bhattacharyya, S., Bhattacharya, P., Adhikari, A., Mukherjee, A., Bhattacharyya Majumdar, S. and Majumdar, S. (2009). CXC chemokine-mediated protection against visceral leishmaniasis: involvement of the proinflammatory response. Journal of Infectious Diseases 200, 1300-1310. doi: 10.1086/605895.
80. Handman, E. (1999). Cell biology of Leishmania. Advances in Parasitology 44, 1-39.
81. Havell, E. A. (1989). Evidence that tumor necrosis factor has an important role in antibacterial resistance. Journal of Immunology 143, 2894-2899.
82. Heinzel, F. P., Rerko, R. M., Hatam, F. and Locksley, R.M. (1993). IL-2 is necessary for the progression of leishmaniasis in susceptible murine hosts. Journal of Immunology 150, 3924-3931.
83. Himmelrich, H., Launois, P., Maillard, I., Biedermann, T., Tacchini-Cottier, F., Locksley, R. M., Rocken, M. and Louis, J. A. (2000). In BALB/c mice, IL-4 production during the initial phase of infection with Leishmania major is necessary and sufficient to instruct Th2 cell development resulting in progressive disease. Journal of Immunology 164, 4819-4825.
84. Hoerauf, A., Solbach, W., Rollinghoff, M. and Gessner, A. (1995). Effect of IL-7 treatment on Leishmania major-infected BALB. Xid mice: enhanced lymphopoiesis with sustained lack of B1 cells and clinical aggravation of disease. International Immunology 7, 1879-1884.
85. Houde, M., Bertholet, S., Gagnon, E., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F., Thibault, P., Sacks, D. and Desjardins, M. (2003). Phagosomes are competent organelles for antigen cross-presentation. Nature 425, 402-406.
86. Huber, M., Timms, E., Mak, T.W., Rollinghoff, M. and Lohoff, M. (1998). Effective and long-lasting immunity against the parasite Leishmania major in CD8-deficient mice. Infection and Immunity 66, 3968-3970.
87. Iezzi, G., Karjalainen, K. and Lanzavecchia, A. (1998). The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8, 89-95. doi: 10.1016/S1074-7613(00)80461-6.
88. Iniesta, V., Gomez-Nieto, L. C. and Corraliza, I. (2001). The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. Journal of Experimental Medicine 193, 777-784.
89. Joshi, T., Rodriguez, S., Perovic, V., Cockburn, I. A. and Stager, S. (2009). B7-H1 blockade increases survival of dysfunctional CD8(+) T cells and confers protection against Leishmania donovani infections. PLOS Pathogens 5, e1000431. doi: 10.1371/journal.ppat.1000431.
90. Kane, M. M. and Mosser, D. M. (2001). The role of IL-10 in promoting disease progression in leishmaniasis. Journal of Immunology 166, 1141-1147.
91. Karplus, T. M., Jeronimo, S. M., Chang, H., Helms, B. K., Burns, T. L., Murray, J. C., Mitchell, A. A., Pugh, E.W., Braz, R. F., Bezerra, F. L. and Wilson, M. E. (2002). Association between the tumor necrosis factor locus and the clinical outcome of Leishmania chagasi infection. Infection and Immunity 70, 6919-6925.
92. Kaye, P. M. and Bancroft, G. J. (1992). Leishmania donovani infection in scid mice: lack of tissue response and in vivo macrophage activation correlates with failure to trigger natural killer cell-derived gamma interferon production in vitro. Infection and Immunity 60, 4335-4342.
93. Kedzierski, L., Curtis, J. M., Doherty, P. C., Handman, E. and Kedzierska, K. (2008). Decreased IL-10 and IL-13 production and increased CD44hi T cell recruitment contribute to Leishmania major immunity induced by non-persistent parasites. European Journal of Immunology 38, 3090-3100. doi: 10.1002/eji.200838423.
94. Kedzierski, L., Zhu, Y. and Handman, E. (2006). Leishmania vaccines: progress and problems. Parasitology 133 (Suppl.), S87-S112.
95. Kedzierski, L., Sakthianandeswaren, A., Curtis, J. M., Andrews, P. C., Junk, P. C. and Kedzierska, K. (2009). Leishmaniasis: current treatment and prospects for new drugs and vaccines. Current Medicinal Chemistry 16, 599-614.
96. Khalil, E. A., Ayed, N. B., Musa, A. M., Ibrahim, M. E., Mukhtar, M. M., Zijlstra, E. E., Elhassan, I. M., Smith, P. G., Kieny, P. M., Ghalib, H.W., Zicker, F., Modabber, F. and Elhassan, A. M. (2005). Dichotomy of protective cellular immune responses to human visceral leishmaniasis. Clinical and Experimental Immunology 140, 349-353.
97. Kirkpatrick, C. E., Farrell, J. P., Warner, J. F. and Denner, G. (1985). Participation of natural killer cells in the recovery of mice from visceral leishmaniasis. Cellular Immunology 92, 163-171.
98. Kopf, M., Le Gros, G., Bachmann, M., Lamers, M. C., Bluethmann, H. and Kohler, G. (1993). Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362, 245-248.
99. Kopf, M., Brombacher, F., Kohler, G., Kienzle, G., Widmann, K. H., Lefrang, K., Humborg, C., Ledermann, B. and Solbach, W. (1996). IL-4-deficient Balb/c mice resist infection with Leishmania major. Journal of Experimental Medicine 184, 1127-1136.
100. Kurkjian, K. M., Mahmutovic, A. J., Kellar, K. L., Haque, R., Bern, C. and Secor, W. E. (2006). Multiplex analysis of circulating cytokines in the sera of patients with different clinical forms of visceral leishmaniasis. Cytometry A 69, 353-358. doi: 10.1002/cyto.a.20256.
101. Lachaud, L., Bourgeois, N., Plourde, M., Leprohon, P., Bastien, P. and Ouellette, M. (2009). Parasite susceptibility to amphotericin B in failures of treatment for visceral leishmaniasis in patients coinfected with HIV type 1 and Leishmania infantum. Clinical Infectious Diseases 48, e16-e22. doi: 10.1086/595710.
102. Langrish, C. L., McKenzie, B. S., Wilson, N. J., de Waal Malefyt, R., Kastelein, R. A. and Cua, D. J. (2004). IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunological Reviews 202, 96-105. doi: 10.1111/j.0105-2896.2004.00214.x.
103. Lazarski, C. A., Ford, J., Katzman, S. D., Rosenberg, A. F. and Fowell, D. J. (2013). IL-4 attenuates Th1-associated chemokine expression and Th1 trafficking to inflamed tissues and limits pathogen clearance. PLOS ONE 8, e71949. doi: 10.1371/journal.pone.0071949.
104. Leclercq, V., Lebastard, M., Belkaid, Y., Louis, J. and Milon, G. (1996). The outcome of the parasitic process initiated by Leishmania infantum in laboratory mice: a tissue-dependent pattern controlled by the Lsh and MHC loci. Journal of Immunology 157, 4537-4545.
105. Li, J., Hunter, C. A. and Farrell, J. P. (1999). Anti-TGF-beta treatment promotes rapid healing of Leishmania major infection in mice by enhancing in vivo nitric oxide production. Journal of Immunology 162, 974-979.
106. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K. and Flavell, R. A. (2006). Transforming growth factor-beta regulation of immune responses. Annual Review of Immunology 24, 99-146. doi: 10.1146/annurev.immunol. 24.021605.090737.
107. Liese, J., Schleicher, U. and Bogdan, C. (2008). The innate immune response against Leishmania parasites. Immunobiology 213, 377-387. doi: 10.1016/j.imbio.2007.12.005.
108. Liew, F. Y., Li, Y. and Millott, S. (1990). Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. Journal of Immunology 145, 4306-4310.
109. Maroof, A., Beattie, L., Zubairi, S., Svensson, M., Stager, S. and Kaye, P. M. (2008). Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29, 295-305. doi: 10.1016/j.immuni.2008.06.012.
110. Maroof, A., Brown, N., Smith, B., Hodgkinson, M. R., Maxwell, A., Losch, F. O., Fritz, U., Walden, P., Lacey, C. N., Smith, D. F., Aebischer, T. and Kaye, P. M. (2012). Therapeutic vaccination with recombinant adenovirus reduces splenic parasite burden in experimental visceral leishmaniasis. Journal of Infectious Diseases 205, 853-863. doi: 10.1093/infdis/jir842.
111. Mary, C., Auriault, V., Faugere, B. and Dessein, A. J. (1999). Control of Leishmania infantum infection is associated with CD8(+) and gamma interferon- and interleukin-5-producing CD4(+) antigen-specific T cells. Infection and Immunity 67, 5559-5566.
112. Matheoud, D., Moradin, N., Bellemare-Pelletier, A., Shio, M. T., Hong, W. J., Olivier, M., Gagnon, E., Desjardins, M. and Descoteaux, A. (2013). Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe 14, 15-25. doi: 10.1016/j.chom.2013.06.003.
113. Matthews, D. J., Emson, C. L., McKenzie, G. J., Jolin, H. E., Blackwell, J. M. and McKenzie, A. N. (2000). IL-13 is a susceptibility factor for Leishmania major infection. Journal of Immunology 164, 1458-1462.
114. Mattner, F., Magram, J., Ferrante, J., Launois, P., Di Padova, K., Behin, R., Gately, M. K., Louis, J. A. and Alber, G. (1996). Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. European Journal of Immunology 26, 1553-1559.
115. Maurer, M., Lopez Kostka, S., Siebenhaar, F., Moelle, K., Metz, M., Knop, J. and von Stebut, E. (2006). Skin mast cells control T celldependent host defense in Leishmania major infections. FASEB Journal 20, 2460-2467.
116. McElrath, M. J., Murray, H.W. and Cohn, Z. A. (1988). The dynamics of granuloma formation in experimental visceral leishmaniasis. Journal of Experimental Medicine 167, 1927-1937.
117. McFarlane, E., Perez, C., Charmoy, M., Allenbach, C., Carter, K. C., Alexander, J. and Tacchini-Cottier, F. (2008). Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infection and Immunity 76, 532-541.
118. Miralles, G. D., Stoeckle, M. Y., McDermott, D. F., Finkelman, F. D. and Murray, H.W. (1994). Th1 and Th2 cell-associated cytokines in experimental visceral leishmaniasis. Infection and Immunity 62, 1058-1063.
119. Modabber, F. (2010). Leishmaniasis vaccines: past, present and future. International Journal of Antimicrobial Agents 36 (Suppl. 1), S58-S61. doi: 10.1016/j.ijantimicag.2010.06.024.
120. Monteyne, P., Renauld, J. C., Van Broeck, J., Dunne, D.W., Brombacher, F. and Coutelier, J. P. (1997). IL-4-independent regulation of in vivo IL-9 expression. Journal of Immunology 159, 2616-2623.
121. Moore, J.W., Beattie, L., Dalton, J. E., Owens, B. M., Maroof, A., Coles, M. C. and Kaye, P. M. (2012). B cell: T cell interactions occur within hepatic granulomas during experimental visceral leishmaniasis. PLOS ONE 7, e34143. doi: 10.1371/journal.pone.0034143.
122. Moore, K.W., de Waal Malefyt, R., Coffman, R. L. and O'Garra, A. (2001). Interleukin-10 and the interleukin-10 receptor. Annual Review of Immunology 19, 683-765. doi: 10.1146/annurev.immunol.19.1.683.
123. Mougneau, E., Bihl, F. and Glaichenhaus, N. (2011). Cell biology and immunology of Leishmania. Immunological Reviews 240, 286-296. doi: 10.1111/j.1600-065X.2010.00983.x.
124. Mukbel, R. M., Patten, C., Jr., Gibson, K., Ghosh, M., Petersen, C. and Jones, D. E. (2007). Macrophage killing of Leishmania amazonensis amastigotes requires both nitric oxide and superoxide. American Journal of Tropical Medicine and Hygiene 76, 669-675.
125. Muller, I., Kropf, P., Etges, R. J. and Louis, J. A. (1993). Gamma interferon response in secondary Leishmania major infection: role of CD8+ T cells. Infection and Immunity 61, 3730-3738.
126. Murphy, M. L., Wille, U., Villegas, E. N., Hunter, C. A. and Farrell, J. P. (2001). IL-10 mediates susceptibility to Leishmania donovani infection. European Journal of Immunology 31, 2848-2856.
127. Murray, H.W. (1990). Effect of continuous administration of interferongamma in experimental visceral leishmaniasis. Journal of Infectious Diseases 161, 992-994.
128. Murray, H.W. (1997). Endogenous interleukin-12 regulates acquired resistance in experimental visceral leishmaniasis. Journal of Infectious Diseases 175, 1477-1479.
129. Murray, H.W. (2001). Tissue granuloma structure-function in experimental visceral leishmaniasis. International Journal of Experimental Pathology 82, 249-267.
130. Murray, H.W. (2008). Accelerated control of visceral Leishmania donovani infection in interleukin-6-deficient mice. Infection and Immunity 76, 4088-4091. doi: 10.1128/IAI.00490-08.
131. Murray, H.W. and Cartelli, D. M. (1983). Killing of intracellular Leishmania donovani by human mononuclear phagocytes. Evidence for oxygen-dependent and -independent leishmanicidal activity. Journal of Clinical Investigation 72, 32-44.
132. Murray, H.W. and Nathan, C. F. (1999). Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. Journal of Experimental Medicine 189, 741-746.
133. Murray, H.W., Stern, J. J., Welte, K., Rubin, B. Y., Carriero, S. M. and Nathan, C. F. (1987). Experimental visceral leishmaniasis: production of interleukin 2 and interferon-gamma, tissue immune reaction, and response to treatment with interleukin 2 and interferon-gamma. Journal of Immunology 138, 2290-2297.
134. Murray, H.W., Squires, K. E., Miralles, C. D., Stoeckle, M. Y., Granger, A. M., Granelli-Piperno, A. and Bogdan, C. (1992). Acquired resistance and granuloma formation in experimental visceral leishmaniasis. Differential T cell and lymphokine roles in initial versus established immunity. Journal of Immunology 148, 1858-1863.
135. Murray, H.W., Miralles, G. D., Stoeckle, M. Y. and McDermott, D. F. (1993). Role and effect of IL-2 in experimental visceral leishmaniasis. Journal of Immunology 151, 929-938.
136. Murray, H.W., Cervia, J. S., Hariprashad, J., Taylor, A. P., Stoeckle, M. Y. and Hockman, H. (1995a). Effect of granulocyte-macrophage colony-stimulating factor in experimental visceral leishmaniasis. Journal of Clinical Investigation 95, 1183-1192. doi: 10.1172/JCI117767.
137. Murray, H.W., Hariprashad, J., Aguero, B., Arakawa, T. and Yeganegi, H. (1995b). Antimicrobial response of a T cell-deficient host to cytokine therapy: effect of interferon-gamma in experimental visceral leishmaniasis in nude mice. Journal of Infectious Diseases 171, 1309-1316.
138. Murray, H.W., Jungbluth, A., Ritter, E., Montelibano, C. and Marino, M.W. (2000). Visceral leishmaniasis in mice devoid of tumor necrosis factor and response to treatment. Infection and Immunity 68, 6289-6293.
139. Murray, H.W., Moreira, A. L., Lu, C. M., DeVecchio, J. L., Matsuhashi, M., Ma, X. and Heinzel, F. P. (2003). Determinants of response to interleukin-10 receptor blockade immunotherapy in experimental visceral leishmaniasis. Journal of Infectious Diseases 188, 458-464. doi: 10.1086/376510.
140. Nacy, C. A., Meierovics, A. I., Belosevic, M. and Green, S. J. (1991). Tumor necrosis factor-alpha: central regulatory cytokine in the induction of macrophage antimicrobial activities. Pathobiology 59, 182-184.
141. Nashed, B. F., Maekawa, Y., Takashima, M., Zhang, T., Ishii, K., Dainichi, T., Ishikawa, H., Sakai, T., Hisaeda, H. and Himeno, K. (2000). Different cytokines are required for induction and maintenance of the Th2 type response in DBA/2 mice resistant to infection with Leishmania major. Microbes and Infection 2, 1435-1443. doi: 10.1016/S1286-4579(00) 01298-3.
142. Ng, L. G., Hsu, A., Mandell, M. A., Roediger, B., Hoeller, C., Mrass, P., Iparraguirre, A., Cavanagh, L. L., Triccas, J. A., Beverley, S. M., Scott, P. and Weninger, W. (2008). Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLOS Pathogens 4, e1000222. doi: 10.1371/journal.ppat. 1000222.
143. Noben-Trauth, N., Kropf, P. and Muller, I. (1996). Susceptibility to Leishmania major infection in interleukin-4-deficient mice. Science 271, 987-990.
144. Nylen, S., Maurya, R., Eidsmo, L., Manandhar, K. D., Sundar, S. and Sacks, D. (2007). Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. Journal of Experimental Medicine 204, 805-817. doi: 10.1084/jem.20061141.
145. O'Garra, A. (1998). Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275-283. doi: 10.1016/S1074-7613(00)80533-6.
146. O'Garra, A. and Vieira, P. (2007). T(H)1 cells control themselves by producing interleukin-10. Nature Reviews Immunology 7, 425-428. doi: 10.1038/nri2097.
147. Oghumu, S., Lezama-Davila, C. M., Isaac-Marquez, A. P. and Satoskar, A. R. (2010). Role of chemokines in regulation of immunity against leishmaniasis. Experimental Parasitology 126, 389-396. doi: 10.1016/j.exppara.2010.02.010.
148. Okwor, I., Liu, D., Beverley, S.M. and Uzonna, J. E. (2009). Inoculation of killed Leishmania major into immune mice rapidly disrupts immunity to a secondary challenge via IL-10-mediated process. Proceedings of the National Academy of Sciences USA 106, 13951-13956.
149. Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F., Yu, N., Wang, J., Singh, K., Zonin, F., Vaisberg, E., Churakova, T., Liu, M., Gorman, D., Wagner, J., Zurawski, S., Liu, Y., Abrams, J. S., Moore, K.W., Rennick, D., de Waal-Malefyt, R., Hannum, C., Bazan, J. F. and Kastelein, R. A. (2000). Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725.
150. Owens, B. M., Beattie, L., Moore, J.W., Brown, N., Mann, J. L., Dalton, J. E., Maroof, A. and Kaye, P. M. (2012). IL-10-producing Th1 cells and disease progression are regulated by distinct CD11c(+) cell populations during visceral leishmaniasis. PLOS Pathogens 8, e1002827. doi: 10.1371/journal.ppat.1002827.
151. Padigel, U. M., Alexander, J. and Farrell, J. P. (2003). The role of interleukin-10 in susceptibility of BALB/c mice to infection with Leishmania mexicana and Leishmania amazonensis. Journal of Immunology 171, 3705-3710.
152. Pakpour, N., Zaph, C. and Scott, P. (2008). The central memory CD4+ T cell population generated during Leishmania major infection requires IL-12 to produce IFN-gamma. Journal of Immunology 180, 8299-8305.
153. Pavli, A. and Maltezou, H. C. (2010). Leishmaniasis, an emerging infection in travelers. International Journal of Infectious Diseases 14, e1032-e1039. doi: 10.1016/j.ijid.2010.06.019.
154. Peters, N. C. and Sacks, D. L. (2009). The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Cellular Microbiology 11, 1290-1296.
155. Peters, N. C., Egen, J. G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P., Fay, M. P., Germain, R. N. and Sacks, D. (2008). In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974.
156. Phillips, R., Svensson, M., Aziz, N., Maroof, A., Brown, N., Beattie, L., Signoret, N. and Kaye, P. M. (2010). Innate killing of Leishmania donovani by macrophages of the splenic marginal zone requires IRF-7. PLOS Pathogens 6, e1000813. doi: 10.1371/journal.ppat.1000813.
157. Polley, R., Zubairi, S. and Kaye, P. M. (2005). The fate of heterologous CD4+ T cells during Leishmania donovani infection. European Journal of Immunology 35, 498-504. doi: 10.1002/eji.200425436.
158. Polley, R., Stager, S., Prickett, S., Maroof, A., Zubairi, S., Smith, D. F. and Kaye, P. M. (2006). Adoptive immunotherapy against experimental visceral leishmaniasis with CD8+ T cells requires the presence of cognate antigen. Infection and Immunity 74, 773-776. doi: 10.1128/IAI.74.1.773-776.2006.
159. Pontes De Carvalho, L. C., Badaro, R., Carvalho, E. M., Lannes-Vieira, J., Vinhaes, L., Orge, G., Marsochi, M. C. and Galvao-Castro, B. (1986). Nature and incidence of erythrocytebound IgG and some aspects of the physiopathogenesis of anaemia in American visceral leishmaniasis. Clinical and Experimental Immunology 64, 495-502.
160. Radwanska, M., Cutler, A. J., Hoving, J. C., Magez, S., Holscher, C., Bohms, A., Arendse, B., Kirsch, R., Hunig, T., Alexander, J., Kaye, P. and Brombacher, F. (2007). Deletion of IL-4Ralpha on CD4T cells renders BALB/c mice resistant to Leishmania major infection. PLOS Pathogens 3, e68.
161. Randolph, G. J. (2001). Dendritic cell migration to lymph nodes: cytokines, chemokines, and lipid mediators. Seminars in Immunology 13, 267-274. doi: 10.1006/smim.2001.0322S1044-5323(01)90322-7.
162. Reiner, S. L. and Locksley, R.M. (1995). The regulation of immunity to Leishmania major. Annual Review of Immunology 13, 151-177.
163. Ricardo-Carter, C., Favila, M., Polando, R. E., Cotton, R. N., Bogard Horner, K., Condon, D., Ballhorn, W., Whitcomb, J. P., Yadav, M., Geister, R. L., Schorey, J. S. and McDowell, M. A. (2013). Leishmania major inhibits IL-12 in macrophages by signalling through CR3 (CD11b/CD18) and down-regulation of ETS-mediated transcription. Parasite Immunology 35, 409-420. doi: 10.1111/pim.12049.
164. Ritter, U., Meissner, A., Scheidig, C. and Korner, H. (2004). CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. European Journal of Immunology 34, 1542-1550. doi: 10.1002/eji.200324586.
165. Rodriguez, A., Regnault, A., Kleijmeer, M., Ricciardi-Castagnoli, P. and Amigorena, S. (1999). Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nature Cell Biology 1, 362-368.
166. Ronet, C., Voigt, H., Himmelrich, H., Doucey, M. A., Hauyon-La Torre, Y., Revaz-Breton, M., Tacchini-Cottier, F., Bron, C., Louis, J. and Launois, P. (2008). Leishmania major-specific B cells are necessary for Th2 cell development and susceptibility to L. major LV39 in BALB/c mice. Journal of Immunology 180, 4825-4835.
167. Ronet, C., Hauyon-La Torre, Y., Revaz-Breton, M., Mastelic, B., Tacchini-Cottier, F., Louis, J. and Launois, P. (2010). Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. Journal of Immunology 184, 886-894. doi: 10.4049/jimmunol.0901114.
168. Rosas, L. E., Satoskar, A. A., Roth, K. M., Keiser, T. L., Barbi, J., Hunter, C., de Sauvage, F. J. and Satoskar, A. R. (2006). Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to Leishmania donovani infection but develop severe liver immunopathology. American Journal of Pathology 168, 158-169.
169. Rostan, O., Gangneux, J. P., Piquet-Pellorce, C., Manuel, C., McKenzie, A. N., Guiguen, C., Samson, M. and Robert-Gangneux, F. (2013). The IL-33/ST2 axis is associated with human visceral leishmaniasis and suppresses Th1 responses in the livers of BALB/c mice infected with Leishmania donovani. mBio 4, e00383-e00313. doi: 10.1128/mBio.00383-13.
170. Rousseau, D., Demartino, S., Ferrua, B., Michiels, J. F., Anjuere, F., Fragaki, K., Le Fichoux, Y. and Kubar, J. (2001). In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection. BMC Microbiology 1, 17.
171. Ruiz, J.H. and Becker, I. (2007). CD8 cytotoxic T cells in cutaneous leishmaniasis. Parasite Immunology 29, 671-678.
172. Sacks, D. and Noben-Trauth, N. (2002). The immunology of susceptibility and resistance to Leishmania major in mice. Nature Reviews Immunology 2, 845-858.
173. Sacks, D. L., Scott, P. A., Asofsky, R. and Sher, F. A. (1984). Cutaneous leishmaniasis in anti-IgM-treated mice: enhanced resistance due to functional depletion of a B cell-dependent T cell involved in the suppressor pathway. Journal of Immunology 132, 2072-2077.
174. Sacks, D. L., Lal, S. L., Shrivastava, S. N., Blackwell, J. and Neva, F. A. (1987). An analysis of T cell responsiveness in Indian kalaazar. Journal of Immunology 138, 908-913.
175. Sadick, M. D., Heinzel, F. P., Holaday, B. J., Pu, R. T., Dawkins, R. S. and Locksley, R.M. (1990). Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon gamma-independent mechanism. Journal of Experimental Medicine 171, 115-127.
176. Sato, N., Kuziel, W. A., Melby, P. C., Reddick, R. L., Kostecki, V., Zhao, W., Maeda, N., Ahuja, S. K. and Ahuja, S. S. (1999). Defects in the generation of IFN-gamma are overcome to control infection with Leishmania donovani in CC chemokine receptor (CCR) 5-, macrophage inflammatory protein-1 alpha-, or CCR2-deficient mice. Journal of Immunology 163, 5519-5525.
177. Satoskar, A. R., Stamm, L. M., Zhang, X., Satoskar, A. A., Okano, M., Terhorst, C., David, J. R. and Wang, B. (1999). Mice lacking NK cells develop an efficient Th1 response and control cutaneous Leishmania major infection. Journal of Immunology 162, 6747-6754.
178. Scharton, T. M. and Scott, P. (1993). Natural killer cells are a source of interferon gamma that drives differentiation of CD4+ T cell subsets and induces early resistance to Leishmania major in mice. Journal of Experimental Medicine 178, 567-577.
179. Schwarz, T., Remer, K. A., Nahrendorf, W., Masic, A., Siewe, L., Muller, W., Roers, A. and Moll, H. (2013). T cell-derived IL-10 determines leishmaniasis disease outcome and is suppressed by a dendritic cell based vaccine. PLOS Pathogens 9, e1003476. doi: 10.1371/journal. ppat.1003476.
180. Scott, P. (1989). The role of TH1 and TH2 cells in experimental cutaneous leishmaniasis. Experimental Parasitology 68, 369-372.
181. Scott, P., Eaton, A., Gause, W. C., di Zhou, X. and Hondowicz, B. (1996). Early IL-4 production does not predict susceptibility to Leishmania major. Experimental Parasitology 84, 178-187. doi: 10.1006/expr.1996.0103.
182. Scott, P., Artis, D., Uzonna, J. and Zaph, C. (2004). The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Immunological Reviews 201, 318-338.
183. Searle, S., Bright, N. A., Roach, T. I., Atkinson, P. G., Barton, C. H., Meloen, R.H. and Blackwell, J. M. (1998). Localisation of Nramp1 in macrophages: modulation with activation and infection. Journal of Cell Science 111, 2855-2866.
184. Segal, A.W. (2005). How neutrophils kill microbes. Annual Review of Immunology 23, 197-223. doi: 10.1146/annurev.immunol.23.021704. 115653.
185. Silveira, F. T., Lainson, R., Gomes, C. M., Laurenti, M. D. and Corbett, C. E. (2008). Reviewing the role of the dendritic Langerhans cells in the immunopathogenesis of American cutaneous leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 1075-1080. doi: 10.1016/j.trstmh.2008.05.020.
186. Silvestre, R., Cordeiro-Da-Silva, A., Santarem, N., Vergnes, B., Sereno, D. and Ouaissi, A. (2007). SIR2-deficient Leishmania infantum induces a defined IFN-gamma/IL-10 pattern that correlates with protection. Journal of Immunology 179, 3161-3170.
187. Singh, O. P., Gidwani, K., Kumar, R., Nylen, S., Jones, S. L., Boelaert, M., Sacks, D. and Sundar, S. (2012). Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clinical and Vaccine Immunology 19, 961-966. doi: 10.1128/CVI.00143-12.
188. Smelt, S. C., Engwerda, C. R., McCrossen, M. and Kaye, P. M. (1997). Destruction of follicular dendritic cells during chronic visceral leishmaniasis. Journal of Immunology 158, 3813-3821.
189. Smelt, S. C., Cotterell, S. E., Engwerda, C. R. and Kaye, P. M. (2000). B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. Journal of Immunology 164, 3681-3688.
190. Soong, L. (2008). Modulation of dendritic cell function by Leishmania parasites. Journal of Immunology 180, 4355-4360.
191. Squires, K. E., Schreiber, R. D., McElrath, M. J., Rubin, B. Y., Anderson, S. L. and Murray, H.W. (1989). Experimental visceral leishmaniasis: role of endogenous IFN-gamma in host defense and tissue granulomatous response. Journal of Immunology 143, 4244-4249.
192. Stager, S., Smith, D. F. and Kaye, P. M. (2000). Immunization with a recombinant stage-regulated surface protein from Leishmania donovani induces protection against visceral leishmaniasis. Journal of Immunology 165, 7064-7071.
193. Stager, S., Alexander, J., Carter, K. C., Brombacher, F. and Kaye, P. M. (2003). Both interleukin-4 (IL-4) and IL-4 receptor alpha signaling contribute to the development of hepatic granulomas with optimal antileishmanial activity. Infection and Immunity 71, 4804-4807.
194. Stager, S., Maroof, A., Zubairi, S., Sanos, S. L., Kopf, M. and Kaye, P. M. (2006). Distinct roles for IL-6 and IL-12p40 in mediating protection against Leishmania donovani and the expansion of IL-10+ CD4+ T cells. European Journal of Immunology 36, 1764-1771. doi: 10.1002/eji.200635937.
195. Stanley, A. C. and Engwerda, C. R. (2007). Balancing immunity and pathology in visceral leishmaniasis. Immunology and Cell Biology 85, 138-147. doi: 10.1038/sj.icb7100011.
196. Stanley, A. C., Dalton, J. E., Rossotti, S. H., MacDonald, K. P., Zhou, Y., Rivera, F., Schroder, W. A., Maroof, A., Hill, G. R., Kaye, P. M. and Engwerda, C. R. (2008a). VCAM-1 and VLA-4 modulate dendritic cell IL-12p40 production in experimental visceral leishmaniasis. PLOS Pathogens 4, e1000158. doi: 10.1371/journal. ppat.1000158.
197. Stanley, A. C., Zhou, Y., Amante, F. H., Randall, L. M., Haque, A., Pellicci, D. G., Hill, G. R., Smyth, M. J., Godfrey, D. I. and Engwerda, C. R. (2008b). Activation of invariant NKT cells exacerbates experimental visceral leishmaniasis. PLOS Pathogens 4, e1000028. doi: 10.1371/journal.ppat.1000028.
198. Steinman, R. M. and Hemmi, H. (2006). Dendritic cells: translating innate to adaptive immunity. Current Topics in Microbiology and Immunology 311, 17-58.
199. Stern, J. J., Oca, M. J., Rubin, B. Y., Anderson, S. L. and Murray, H.W. (1988). Role of L3T4+ and LyT-2+ cells in experimental visceral leishmaniasis. Journal of Immunology 140, 3971-3977.
200. Stober, C. B., Lange, U. G., Roberts, M. T., Alcami, A. and Blackwell, J. M. (2005). IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. Journal of Immunology 175, 2517-2524.
201. Stober, C. B., Brode, S., White, J. K., Popoff, J. F. and Blackwell, J. M. (2007). Slc11a1, formerly Nramp1, is expressed in dendritic cells and influences major histocompatibility complex class II expression and antigen-presenting cell function. Infection and Immunity 75, 5059-5067. doi: 10.1128/IAI.00153-07.
202. Sundar, S., Reed, S. G., Sharma, S., Mehrotra, A. and Murray, H.W. (1997). Circulating T helper 1 (Th1) cell- and Th2 cell-associated cytokines in Indian patients with visceral leishmaniasis. American Journal of Tropical Medicine and Hygiene 56, 522-525.
203. Sunderkotter, C., Kunz, M., Steinbrink, K., Meinardus-Hager, G., Goebeler, M., Bildau, H. and Sorg, C. (1993). Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. Journal of Immunology 151, 4891-4901.
204. Svensson, M., Zubairi, S., Maroof, A., Kazi, F., Taniguchi, M. and Kaye, P. M. (2005). Invariant NKT cells are essential for the regulation of hepatic CXCL10 gene expression during Leishmania donovani infection. Infection and Immunity 73, 7541-7547. doi: 10.1128/IAI.73.11.7541-7547.2005.
205. Swihart, K., Fruth, U., Messmer, N., Hug, K., Behin, R., Huang, S., Del Giudice, G., Aguet, M. and Louis, J. A. (1995). Mice from a genetically resistant background lacking the interferon gamma receptor are susceptible to infection with Leishmania major but mount a polarized T helper cell 1-type CD4+ T cell response. Journal of Experimental Medicine 181, 961-971.
206. Tan, Z. Y., Bealgey, K.W., Fang, Y., Gong, Y. M. and Bao, S. (2009). Interleukin-23: immunological roles and clinical implications. International Journal of Biochemistry and Cell Biology 41, 733-735. doi: 10.1016/j. biocel.2008.04.027.
207. Taylor, A. P. and Murray, H.W. (1997). Intracellular antimicrobial activity in the absence of interferon-gamma: effect of interleukin-12 in experimental visceral leishmaniasis in interferon-gamma gene-disrupted mice. Journal of Experimental Medicine 185, 1231-1239.
208. Titus, R. G., Sherry, B. and Cerami, A. (1989). Tumor necrosis factor plays a protective role in experimental murine cutaneous leishmaniasis. Journal of Experimental Medicine 170, 2097-2104.
209. Tolouei, S., Ghaedi, K., Khamesipour, A., Akbari, M., Baghaei, M., Hasheminia, S., Narimani, M. and Hejazi, S. (2012). IL-23 and IL-27 levels in macrophages collected from peripheral blood of patients with healing vs non-healing form of cutaneous leishmaniasis. Iran Journal of Parasitology 7, 18-25.
210. Trinchieri, G. (1998). Interleukin-12: a cytokine at the interface of inflammation and immunity. Advances in Immunology 70, 83-243.
211. Tsagozis, P., Karagouni, E. and Dotsika, E. (2003). CD8(+) T cells with parasite-specific cytotoxic activity and a Tc1 profile of cytokine and chemokine secretion develop in experimental visceral leishmaniasis. Parasite Immunology 25, 569-579. doi: 10.1111/j.0141-9838.2004.00672. xPIM672.
212. Tumang, M. C., Keogh, C., Moldawer, L. L., Helfgott, D. C., Teitelbaum, R., Hariprashad, J. and Murray, H.W. (1994). Role and effect of TNF-alpha in experimental visceral leishmaniasis. Journal of Immunology 153, 768-775.
213. Uzonna, J. E., Joyce, K. L. and Scott, P. (2004a). Low dose Leishmania major promotes a transient T helper cell type 2 response that is downregulated by interferon gamma-producing CD8+ T cells. Journal of Experimental Medicine 199, 1559-1566.
214. Uzonna, J. E., Spath, G. F., Beverley, S.M. and Scott, P. (2004b). Vaccination with phosphoglycan-deficient Leishmania major protects highly susceptible mice from virulent challenge without inducing a strong Th1 response. Journal of Immunology 172, 3793-3797.
215. Vidal, S., Tremblay, M. L., Govoni, G., Gauthier, S., Sebastiani, G., Malo, D., Skamene, E., Olivier, M., Jothy, S. and Gros, P. (1995). The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. Journal of Experimental Medicine 182, 655-666.
216. Von Stebut, E. (2007). Immunology of cutaneous leishmaniasis: the role of mast cells, phagocytes and dendritic cells for protective immunity. European Journal of Dermatology 17, 115-122.
217. von Stebut, E. and Udey, M. C. (2004). Requirements for Th1-dependent immunity against infection with Leishmania major. Microbes and Infection 6, 1102-1109.
218. von Stebut, E., Belkaid, Y., Jakob, T., Sacks, D. L. and Udey, M. C. (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. Journal of Experimental Medicine 188, 1547-1552.
219. Von Stebut, E., Ehrchen, J. M., Belkaid, Y., Kostka, S. L., Molle, K., Knop, J., Sunderkotter, C. and Udey, M. C. (2003). Interleukin 1alpha promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. Journal of Experimental Medicine 198, 191-199. doi: 10.1084/jem.20030159.
220. Wang, Z. E., Reiner, S. L., Zheng, S., Dalton, D. K. and Locksley, R.M. (1994). CD4+ effector cells default to the Th2 pathway in interferon gamma-deficient mice infected with Leishmania major. Journal of Experimental Medicine 179, 1367-1371.
221. Wei, X. Q., Charles, I. G., Smith, A., Ure, J., Feng, G. J., Huang, F. P., Xu, D., Muller, W., Moncada, S. and Liew, F. Y. (1995). Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408-411.
222. Wilson, M. E., Young, B. M., Davidson, B. L., Mente, K. A. and McGowan, S. E. (1998). The importance of TGF-beta in murine visceral leishmaniasis. Journal of Immunology 161, 6148-6155.
223. Wilson, M. E., Recker, T. J., Rodriguez, N. E., Young, B. M., Burnell, K. K., Streit, J. A. and Kline, J. N. (2002). The TGF-beta response to Leishmania chagasi in the absence of IL-12. European Journal of Immunology 32, 3556-3565. doi: 10.1002/1521-4141(200212)32:12<3556::AID-IMMU3556>3.0.CO;2-Q.
224. Woelbing, F., Kostka, S. L., Moelle, K., Belkaid, Y., Sunderkoetter, C., Verbeek, S., Waisman, A., Nigg, A. P., Knop, J., Udey, M. C. and von Stebut, E. (2006). Uptake of Leishmania major by dendritic cells is mediated by Fcgamma receptors and facilitates acquisition of protective immunity. Journal of Experimental Medicine 203, 177-188.
225. Xin, L., Li, K. and Soong, L. (2008). Down-regulation of dendritic cell signaling pathways by Leishmania amazonensis amastigotes. Molecular Immunology 45, 3371-3382. doi: 10.1016/j.molimm.2008.04.018.
226. Yoshida, H., Hamano, S., Senaldi, G., Covey, T., Faggioni, R., Mu, S., Xia, M., Wakeham, A. C., Nishina, H., Potter, J., Saris, C. J. and Mak, T.W. (2001). WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 15, 569-578.
227. Zijlstra, E. E. and el-Hassan, A. M. (2001). Leishmaniasis in Sudan. Visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 95 (Suppl. 1), S27-S58.