Volume 26, Issue 2 (3-2022)                   IBJ 2022, 26(2): 99-109 | Back to browse issues page

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Alimohmmadian M H, Ajdary S, Bahrami F. A Historic Review of the Role of CD4+ T-Cell Subsets in Development of the Immune Responses against Cutaneous and Visceral Leishmaniases. IBJ 2022; 26 (2) :99-109
URL: http://ibj.pasteur.ac.ir/article-1-3591-en.html
The heterogeneity of CD4+ T cells has been investigated since the late 1970s, when their Th1 and Th2 subsets were coined. Later studies on the cutaneous form of the Leishmaniasis were focused on the experimental models of Leishmania major infection using the susceptible BALB/c and the resistant C57BL/6 mice. At the early 21st century, the regulatory T-cells subpopulation was introduced and its role in concomitant immunity, responsible for lifelong resistance of the host to the reinfection was proposed. Subsequent studies, mainly focused on the visceral form of the infection pointed to the role of IL-17, produced by Th17 subset of CD4+ T cells that along the neutrophils were shown to have important yet equivocal functions in protection against or exacerbation of the infection. Altogether, the current knowledge indicates that the above four subsets could orchestrate the immune, the regulatory and the inflammatory responses of the host against different forms of leishmaniases.
Type of Study: Review Article | Subject: Related Fields

1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M, Team WHOLC. Leishmaniasis worldwide and global estimates of its incidence. Plos one 2012; 7(5): e35671. [DOI:10.1371/journal.pone.0035671]
2. Fraga J, Montalvo AM, De Doncker S, Dujardin JC, Van der Auwera G. Phylogeny of Leishmania species based on the heat-shock protein 70 gene. Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases 2010; 10(2): 238-245. [DOI:10.1016/j.meegid.2009.11.007]
3. Seimenis A, Morelli D, Mantovani A. Zoonoses in the Mediterranean region. Annali dell'Istituto superiore di sanita 2006; 42(4): 437-445.
4. Zijlstra EE. Visceral leishmaniasis: a forgotten epidemic. Archives of disease in childhood 2016; 101(6): 561-567 . [DOI:10.1136/archdischild-2015-309302]
5. Bates PA, Depaquit J, Galati EA, Kamhawi S, Maroli M, McDowell MA, Picado A, Ready PD, Salomon OD, Shaw JJ, Traub-Cseko YM, Warburg A. Recent advances in phlebotomine sand fly research related to leishmaniasis control. Parasites and vectors 2015; 8: 131. [DOI:10.1186/s13071-015-0712-x]
6. Sacks D, Sher A. Evasion of innate immunity by parasitic protozoa. Nature immunology 2002; 3(11): 1041-1047. [DOI:10.1038/ni1102-1041]
7. Reiner SL, Locksley RM. The regulation of immunity to Leishmania major. Annual review of immunology 1995; 13: 151-177. [DOI:10.1146/annurev.iy.13.040195.001055]
8. Sacks D, Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nature reviews immunology 2002; 2(11): 845-858. [DOI:10.1038/nri933]
9. Xu D, Liu H, Komai-Koma M, Campbell C, McSharry C, Alexander J, Liew FY. CD4+CD25+ regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. Journal of immunology 2003; 170(1): 394-399. [DOI:10.4049/jimmunol.170.1.394]
10. Bhattacharya P, Ali N. Involvement and interactions of different immune cells and their cytokines in human visceral leishmaniasis. Revista da sociedade brasileira de medicina tropical 2013; 46(2): 128-134 . [DOI:10.1590/0037-8682-0022-2012]
11. Dennert G. Evidence for non-identity of T killer and T helper cells sensitised to allogeneic cell antigens. Nature 1974; 249(455): 358-360 . [DOI:10.1038/249358a0]
12. Cantor H, Boyse EA. Functional subclasses of T-lymphocytes bearing different Ly antigens. I. The generation of functionally distinct T-cell subclasses is a differentiative process independent of antigen. The Journal of experimental medicine 1975; 141(6): 1376-1389 . [DOI:10.1084/jem.141.6.1376]
13. Kisielow P, Hirst JA, Shiku H, Beverley PC, Hoffman MK, Boyse EA, Oettgen HF. Ly antigens as markers for functionally distinct subpopulations of thymus-derived lymphocytes of the mouse. Nature 1975; 253(5488): 219-220 . [DOI:10.1038/253219a0]
14. Nasseri M, Modabber FZ. Generalized infection and lack of delayed hypersensitivity in BALB/c mice infected with Leishmania tropica major. Infection and immunity 1979; 26(2): 611-614. [DOI:10.1128/iai.26.2.611-614.1979]
15. Howard JG, Hale C, Liew FY. Immunological regulation of experimental cutaneous leishmaniasis. III. Nature and significance of specific suppression of cell-mediated immunity in mice highly susceptible to Leishmania tropica. The journal of experimental medicine 1980; 152(3): 594-607 . [DOI:10.1084/jem.152.3.594]
16. Howard JG, Hale C, Liew FY. Immunological regulation of experimental cutaneous leishmaniasis. IV. Prophylactic effect of sublethal irradiation as a result of abrogation of suppressor T cell generation in mice genetically susceptible to Leishmania tropica. The jurnal of experimental medicine 1981; 153(3): 557-568. [DOI:10.1084/jem.153.3.557]
17. Louis JA, Zubler RH, Coutinho SG, Lima G, Behin R, Mauel J, Engers HD. The in vitro generation and functional analysis of murine T cell populations and clones specific for a protozoan parasite, Leishmania tropica. Immunological reviews 1982; 61: 215-243. [DOI:10.1111/j.1600-065X.1982.tb00378.x]
18. Dialynas DP, Quan ZS, Wall KA, Pierres A, Quintans J, Loken MR, Pierres M, Fitch FW. Characterization of the murine T cell surface molecule, designated L3T4, identified by monoclonal antibody GK1.5: similarity of L3T4 to the human Leu-3/T4 molecule. Journal of immunology 1983; 131(5): 2445-2451.
19. Haregewoin A, Louis J. Characterization and functional studies of the murine T-lymphocyte response to Mycobacterium leprae antigen. Scandinavian journal of immunology 1983; 18(3): 225-233. [DOI:10.1111/j.1365-3083.1983.tb00861.x]
20. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of immunology 1986; 136(7): 2348-2357.
21. Muller I, Garcia-Sanz JA, Titus R, Behin R, Louis J. Analysis of the cellular parameters of the immune responses contributing to resistance and susceptibility of mice to infection with the intracellular parasite, Leishmania major. Immunological reviews 1989; 112: 95-113. [DOI:10.1111/j.1600-065X.1989.tb00554.x]
22. Chatila TA, Blaeser F, Ho N, Lederman HM, Voulgaropoulos C, Helms C, Bowcock AM. JM2, encoding a fork head-related protein, is mutated in X-linked autoimmunity-allergic disregulation syndrome. The journal of clinical investigation 2000; 106(12): R75-81. [DOI:10.1172/JCI11679]
23. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nature genetics 2001; 27(1): 68-73. [DOI:10.1038/83784]
24. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nature immunology 2003; 4(4): 330-336. [DOI:10.1038/ni904]
25. Benoist C, Mathis D. Treg cells, life history, and diversity. Cold spring harbor perspectives in biology 2012; 4(9): a007021. [DOI:10.1101/cshperspect.a007021]
26. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420(6915): 502-507. [DOI:10.1038/nature01152]
27. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nature immunology 2005; 6(11): 1123-1132. [DOI:10.1038/ni1254]
28. Tacchini-Cottier F, Weinkopff T, Launois P. Does T Helper Differentiation Correlate with Resistance or Susceptibility to Infection with L. major? Some Insights From the Murine Model. Frontiers in immunology 2012; 3: 32. [DOI:10.3389/fimmu.2012.00032]
29. Park AY, Hondowicz BD, Scott P. IL-12 is required to maintain a Th1 response during Leishmania major infection. Journal of immunology 2000; 165(2): 896-902. [DOI:10.4049/jimmunol.165.2.896]
30. Reiner SL, Zheng S, Wang ZE, Stowring L, Locksley RM. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. The journal of experimental medicine 1994; 179(2): 447-456. [DOI:10.1084/jem.179.2.447]
31. Trinchieri G. Interleukin-12 and its role in the generation of TH1 cells. Immunology today 1993; 14(7): 335-338. [DOI:10.1016/0167-5699(93)90230-I]
32. Darabi S, Khaze V, Riazi-Rad F, Darabi H, Bahrami F, Ajdary S, Alimohammadian MH. Leishmania major strains isolated from distinct endemic areas show diverse cytokine mRNA expression levels in C57BL/6 mice: Toward selecting an ideal strain for the vaccine studies. Cytokine 2015; 76(2): 303-308. [DOI:10.1016/j.cyto.2015.05.022]
33. Fitch FW, McKisic MD, Lancki DW, Gajewski TF. Differential regulation of murine T lymphocyte subsets. Annual review of immunology 1993; 11: 29-48. [DOI:10.1146/annurev.iy.11.040193.000333]
34. Heinzel FP, Sadick MD, Holaday BJ, Coffman RL, Locksley RM. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. The journal of experimental medicine 1989; 169(1): 59-72. [DOI:10.1084/jem.169.1.59]
35. Locksley RM, Scott P. Helper T-cell subsets in mouse leishmaniasis: induction, expansion and effector function. Immunology today 1991; 12(3): A58-61. [DOI:10.1016/S0167-5699(05)80017-9]
36. Launois P, Maillard I, Pingel S, Swihart KG, Xenarios I, Acha-Orbea H, Diggelmann H, Locksley RM, MacDonald HR, Louis JA. 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 1997; 6(5): 541-549. [DOI:10.1016/S1074-7613(00)80342-8]
37. Alimohammadian MH, Darabi H, Ajdary S, Khaze V, Torkabadi E. Genotypically distinct strains of Leishmania major display diverse clinical and immunological patterns in BALB/c mice. Infection, genetics and evolution 2010; 10(7): 969-975. [DOI:10.1016/j.meegid.2010.06.006]
38. Asadpour A, Riazi-Rad F, Khaze V, Ajdary S, Alimohammadian MH. Distinct strains of Leishmania major induce different cytokine mRNA expression in draining lymph node of BALB/c mice. Parasite immunology 2013; 35(1): 42-50. [DOI:10.1111/pim.12018]
39. Indiani de Oliveira C, Teixeira MJ, Teixeira CR, Ramos de Jesus J, Bomura Rosato A, Santa da Silva J, Brodskyn C, Barral-Netto M, Barral A. Leishmania braziliensis isolates differing at the genome level display distinctive features in BALB/c mice. Microbes and infection 2004; 6(11): 977-984. [DOI:10.1016/j.micinf.2004.05.009]
40. Dowlati Y. Cutaneous leishmaniasis: clinical aspect. Clinics in dermatology 1996; 14(5): 425-431. [DOI:10.1016/0738-081X(96)00058-2]
41. Nadim A, Faghih M. The epidemiology of cutaneous leishmaniasis in the Isfahan province of Iran. I. The reservoir. II. The human disease. Transactions of the royal society of tropical medicine and hygiene 1968; 62(4): 534-542. [DOI:10.1016/0035-9203(68)90140-5]
42. Mendonca SC, De Luca PM, Mayrink W, Restom TG, Conceicao-Silva F, Da-Cruz AM, Bertho AL, Da Costa CA, Genaro O, Toledo VP. Characterization of human T lymphocyte-mediated immune responses induced by a vaccine against American tegumentary leishmaniasis. The American journal of tropical medicine and hygiene 1995; 53(2): 195-201. [DOI:10.4269/ajtmh.1995.53.195]
43. Da-Cruz AM, Conceicao-Silva F, Bertho AL, Coutinho SG. Leishmania-reactive CD4+ and CD8+ T cells associated with cure of human cutaneous leishmaniasis. Infection and immunity 1994; 62(6): 2614-2618. [DOI:10.1128/iai.62.6.2614-2618.1994]
44. Da-Cruz AM, Bittar R, Mattos M, Oliveira-Neto MP, Nogueira R, Pinho-Ribeiro V, Azeredo-Coutinho RB, Coutinho SG. T-cell-mediated immune responses in patients with cutaneous or mucosal leishmaniasis: long-term evaluation after therapy. Clinical and diagnostic laboratory immunology 2002; 9(2): 251-256. [DOI:10.1128/CDLI.9.2.251-256.2002]
45. Gaafar A, Kharazmi A, Ismail A, Kemp M, Hey A, Christensen CB, Dafalla M, el Kadaro AY, el Hassan AM, Theander TG. Dichotomy of the T cell response to Leishmania antigens in patients suffering from cutaneous leishmaniasis; absence or scarcity of Th1 activity is associated with severe infections. Clinical and experimental immunology 1995; 100(2): 239-245. [DOI:10.1111/j.1365-2249.1995.tb03660.x]
46. Ajdary S, Eslami MB, Pakzad S, Alimohammadia nMH. Cytokine production pattern by different subtypes of T cells in cutaneous leishmaniasis. Iranian journal of medical sciences 1999; 24: 1-75.
47. Rafati S, Couty-Jouve S, Alimohammadian MH, Louis JA. Biochemical analysis and immunogenicity of Leishmania major amastigote fractions in cutaneous leishmaniasis. Clinical and experimental immunology 1997; 110(2): 203-211. [DOI:10.1111/j.1365-2249.1997.tb08318.x]
48. Ajdary S, Alimohammadian MH, Eslami MB, Kemp K, Kharazmi A. 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 2000; 68(4): 1760-1764. [DOI:10.1128/IAI.68.4.1760-1764.2000]
49. Alimohammadian MH, Khamesipour A, Darabi H, Firooz A, Malekzadeh S, Bahonar A, Dowlati Y, Modabber F. The role of BCG in human immune responses induced by multiple injections of autoclaved Leishmania major as a candidate vaccine against leishmaniasis. Vaccine 2002; 21(3-4): 174-180. [DOI:10.1016/S0264-410X(02)00458-9]
50. Alimohammadian MH, Jones SL, Darabi H, Riazirad F, Ajdary S, Shabani A, Rezaee MA, Mohebali M, Hosseini Z, Modabber F. Assessment of interferon-gamma levels and leishmanin skin test results in persons recovered for leishmaniasis. The American journal of tropical medicine and hygiene 2012; 87(1): 70-75. [DOI:10.4269/ajtmh.2012.11-0479]
51. Farajnia S, Mahboudi F, Ajdari S, Reiner NE, Kariminia A, Alimohammadian MH. Mononuclear cells from patients recovered from cutaneous leishmaniasis respond to Leishmania major amastigote class I nuclease with a predominant Th1-like response. Clinical and experimental immunology 2005; 139(3): 498-505. [DOI:10.1111/j.1365-2249.2004.02702.x]
52. Ajdary S, Riazi-Rad F, Alimohammadian MH, Pakzad SR. Immune response to Leishmania antigen in anthroponotic cutaneous leishmaniasis. The journal of infection 2009; 59(2): 139-143. [DOI:10.1016/j.jinf.2009.05.010]
53. Alimohammadian MH, Darabi H, Malekzadeh S, Mahmoodzadeh-Niknam H, Ajdary S, Khamesipour A, Bahonar A, Mofarrah A. Exposure to Leishmania major modulates the proportion of CD4+ T cells without affecting cellular immune responses. Microbiology and immunology 2007; 51(10): 1003-1011. [DOI:10.1111/j.1348-0421.2007.tb03984.x]
54. Jafarzadeh A, Nemati M, Chauhan P, Patidar A, Sarkar A, Sharifi I, Saha B. Interleukin-27 Functional Duality Balances Leishmania Infectivity and Pathogenesis. Frontiers in immunology 2020; 11: 1573. [DOI:10.3389/fimmu.2020.01573]
55. Novoa R, Bacellar O, Nascimento M, Cardoso TM, Ramasawmy R, Oliveira WN, Schriefer A, Carvalho EM. IL-17 and Regulatory Cytokines (IL-10 and IL-27) in L. braziliensis Infection. Parasite immunology 2011; 33(2): 132-136 . [DOI:10.1111/j.1365-3024.2010.01256.x]
56. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nature immunology 2005; 6(11): 1133-1141. [DOI:10.1038/ni1261]
57. Nylen S, Gautam S. Immunological perspectives of leishmaniasis. Journal of global infectious diseases 2010; 2(2): 135-146. [DOI:10.4103/0974-777X.62876]
58. Belkaid Y. The role of CD4+CD25+ regulatory T cells in Leishmania infection. Expert opinion on biological therapy 2003; 3(6): 875-885. [DOI:10.1517/14712598.3.6.875]
59. Dietze-Schwonberg K, Lorenz B, Lopez Kostka S, Waisman A, von Stebut E. Parasite Clearance in Leishmaniasis in Resistant Animals Is Independent of the IL-23/IL-17A Axis. The journal of investigative dermatology 2016; 136(9): 1906-1908. [DOI:10.1016/j.jid.2016.05.111]
60. Peters N, Sacks D. Immune privilege in sites of chronic infection: Leishmania and regulatory T cells. Immunological reviews 2006; 213: 159-179. [DOI:10.1111/j.1600-065X.2006.00432.x]
61. Bourreau E, Ronet C, Darsissac E, Lise MC, Marie DS, Clity E, Tacchini-Cottier F, Couppie P, Launois P. In leishmaniasis due to Leishmania guyanensis infection, distinct intralesional interleukin-10 and Foxp3 mRNA expression are associated with unresponsiveness to treatment. The journal of infectious diseases 2009; 199(4): 576-579. [DOI:10.1086/596508]
62. Campanelli AP, Roselino AM, Cavassani KA, Pereira MS, Mortara RA, Brodskyn CI, Goncalves HS, Belkaid Y, Barral-Netto M, Barral A, Silva JS. CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. The journal of infectious diseases 2006; 193(9): 1313-1322. [DOI:10.1086/502980]
63. Suffia IJ, Reckling SK, Piccirillo CA, Goldszmid RS, Belkaid Y. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. The journal of experimental medicine 2006; 203(3): 777-788. [DOI:10.1084/jem.20052056]
64. Hoseini SG, Javanmard SH, Zarkesh SH, Khamesipour A, Rafiei L, Karbalaie K, Nilforoushzade M, Baghaei M, Hejazi SH. Regulatory T-cell profile in early and late lesions of cutaneous leishmaniasis due to Leishmania major. Journal of research in medical sciences 2012; 17(6): 513-518.
65. Bahrami F, Darabi H, Riazi-Rad F, Khaze V, Ajdary S, Alimohammadian MH. FOXP3 expression and frequency of regulatory T cells in healed individuals from Leishmania major infection and the asymptomatic cases. Human immunology 2014; 75(10): 1026-1033. [DOI:10.1016/j.humimm.2014.08.204]
66. Bacellar O, Faria D, Nascimento M, Cardoso TM, Gollob KJ, Dutra WO, Scott P, Carvalho EM. Interleukin 17 production among patients with American cutaneous leishmaniasis. The journal of infectious diseases 2009; 200(1): 75-78 . [DOI:10.1086/599380]
67. Katara GK, Raj A, Kumar R, Avishek K, Kaushal H, Ansari NA, Bumb RA, Salotra P. Analysis of localized immune responses reveals presence of Th17 and Treg cells in cutaneous leishmaniasis due to Leishmania tropica. BMC immunology 2013; 14: 52. [DOI:10.1186/1471-2172-14-52]
68. Boaventura VS, Santos CS, Cardoso CR, de Andrade J, Dos Santos WL, Clarencio J, Silva JS, Borges VM, Barral-Netto M, Brodskyn CI, Barral A. Human mucosal leishmaniasis: neutrophils infiltrate areas of tissue damage that express high levels of Th17-related cytokines. European journal of immunology 2010; 40(10): 2830-2836. [DOI:10.1002/eji.200940115]
69. Lopez Kostka S, Dinges S, Griewank K, Iwakura Y, Udey MC, von Stebut E. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. Journal of immunology 2009; 182(5): 3039-3046. [DOI:10.4049/jimmunol.0713598]
70. Anderson CF, Stumhofer JS, Hunter CA, Sacks D. IL-27 regulates IL-10 and IL-17 from CD4+ cells in nonhealing Leishmania major infection. Journal of immunology 2009; 183(7): 4619-4627. [DOI:10.4049/jimmunol.0804024]
71. Souza MA, Castro MC, Oliveira AP, Almeida AF, Reis LC, Silva CJ, Brito ME, Pereira VR. American tegumentary leishmaniasis: cytokines and nitric oxide in active disease and after clinical cure, with or without chemotherapy. Scandinavian journal of immunology 2012; 76(2): 175-180. [DOI:10.1111/j.1365-3083.2012.02717.x]
72. Goncalves-de-Albuquerque SDC, Pessoa ESR, Trajano-Silva LAM, de Goes TC, de Morais RCS, da COCN, de Lorena VMB, de Paiva-Cavalcanti M. The Equivocal Role of Th17 Cells and Neutrophils on Immunopathogenesis of Leishmaniasis. Frontiers in immunology 2017; 8: 1437. [DOI:10.3389/fimmu.2017.01437]
73. Tiwananthagorn S, Iwabuchi K, Ato M, Sakurai T, Kato H, Katakura K. Involvement of CD4+ Foxp3+ regulatory T cells in persistence of Leishmania donovani in the liver of alymphoplastic aly/aly mice. PLoS neglected tropical diseases 2012; 6(8): e1798. [DOI:10.1371/journal.pntd.0001798]
74. Pitta MG, Romano A, Cabantous S, Henri S, Hammad A, Kouriba B, Argiro L, el Kheir M, Bucheton B, Mary C, El-Safi SH, Dessein A. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. The journal of clinical investigation 2009; 119(8): 2379-2387. [DOI:10.1172/JCI38813]
75. Katara GK, Ansari NA, Singh A, Ramesh V, Salotra P. Evidence for involvement of Th17 type responses in post kala azar dermal leishmaniasis (PKDL). PLoS neglected tropical diseases 2012; 6(6): e1703. [DOI:10.1371/journal.pntd.0001703]
76. Mahmoudzadeh-Niknam H, Abrishami F, Doroudian M, Moradi M, Alimohammadian MH, Parvizi P. Complete conservation of an immunogenic gene (lcr1) in Leishmania infantum and Leishmania chagasi isolated from Iran, Spain and Brazil. Journal of vector borne diseases 2010; 47(4): 204-210.
77. Desjeux P. Leishmaniasis: current situation and new perspectives. Comparative immunology, microbiology and infectious diseases 2004; 27(5): 305-318. [DOI:10.1016/j.cimid.2004.03.004]
78. Blackwell JM, Fakiola M, Ibrahim ME, Jamieson SE, Jeronimo SB, Miller EN, Mishra A, Mohamed HS, Peacock CS, Raju M, Sundar S, Wilson ME. Genetics and visceral leishmaniasis: of mice and man. Parasite immunology 2009; 31(5): 254-266. [DOI:10.1111/j.1365-3024.2009.01102.x]
79. Sacks DL, Lal SL, Shrivastava SN, Blackwell J, Neva FA. An analysis of T cell responsiveness in Indian kala-azar. Journal of immunology 1987; 138(3): 908-913.
80. Saha S, Mondal S, Banerjee A, Ghose J, Bhowmick S, Ali N. Immune responses in kala-azar. The indian journal of medical research 2006; 123(3): 245-266.
81. Manson-Bahr PE. Immunity in kala-azar. Transactions of the royal society of tropical medicine and hygiene 1961; 55: 550-555. [DOI:10.1016/0035-9203(61)90078-5]
82. Reed SG, Badaro R, Masur H, Carvalho EM, Lorenco R, Lisboa A, Teixeira R, Johnson WD, Jr., Jones TC. Selection of a skin test antigen for American visceral leishmaniasis. The American journal of tropical medicine and hygiene 1986; 35(1): 79-85. [DOI:10.4269/ajtmh.1986.35.79]
83. Ghalib HW, Whittle JA, Kubin M, Hashim FA, el-Hassan AM, Grabstein KH, Trinchieri G, Reed SG. IL-12 enhances Th1-type responses in human Leishmania donovani infections. Journal of immunology 1995; 154(9): 4623-4629.
84. Holaday BJ, Pompeu MM, Jeronimo S, Texeira MJ, Sousa Ade A, Vasconcelos AW, Pearson RD, Abrams JS, Locksley RM. Potential role for interleukin-10 in the immunosuppression associated with kala azar. The journal of clinical investigation 1993; 92(6): 2626-2632. [DOI:10.1172/JCI116878]
85. Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson WD, Jr. Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. The journal of clinical investigation 1985; 76(6): 2066-2069. [DOI:10.1172/JCI112209]
86. Singh OP, Gidwani K, Kumar R, Nylen S, Jones SL, Boelaert M, Sacks D, Sundar S. Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clinical and vaccine immunology 2012; 19(6): 961-966. [DOI:10.1128/CVI.00143-12]
87. Gidwani K, Jones S, Kumar R, Boelaert M, Sundar S. Interferon-gamma release assay (modified QuantiFERON) as a potential marker of infection for Leishmania donovani, a proof of concept study. PLoS neglected tropical diseases 2011; 5(4): e1042. [DOI:10.1371/journal.pntd.0001042]
88. Nylen S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends in immunology 2007; 28(9): 378-384. [DOI:10.1016/j.it.2007.07.004]
89. Hailu A, van der Poll T, Berhe N, Kager PA. Elevated plasma levels of interferon (IFN)-gamma, IFN-gamma inducing cytokines, and IFN-gamma inducible CXC chemokines in visceral leishmaniasis. The American journal of tropical medicine and hygiene 2004; 71(5): 561-567. [DOI:10.4269/ajtmh.2004.71.561]
90. Peruhype-Magalhaes V, Martins-Filho OA, Prata A, Silva Lde A, Rabello A, Teixeira-Carvalho A, Figueiredo RM, Guimaraes-Carvalho SF, Ferrari TC, Van Weyenbergh J, Correa-Oliveira R. Mixed inflammatory/regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral Leishmaniasis due to Leishmania chagasi infection. Clinical and experimental immunology 2006; 146(1): 124-132. [DOI:10.1111/j.1365-2249.2006.03171.x]
91. Costa AS, Costa GC, Aquino DM, Mendonca VR, Barral A, Barral-Netto M, Caldas Ade J. Cytokines and visceral leishmaniasis: a comparison of plasma cytokine profiles between the clinical forms of visceral leishmaniasis. Memorias do instituto oswaldo cruz 2012; 107(6): 735-739. [DOI:10.1590/S0074-02762012000600005]
92. Kumar R, Singh N, Gautam S, Singh OP, Gidwani K, Rai M, Sacks D, Sundar S, Nylen S. Leishmania specific CD4 T cells release IFNgamma that limits parasite replication in patients with visceral leishmaniasis. PLoS neglected tropical diseases 2014; 8(10): e3198. [DOI:10.1371/journal.pntd.0003198]
93. Adem E, Tajebe F, Getahun M, Kiflie A, Diro E, Hailu A, Shkedy Z, Mengesha B, Mulaw T, Atnafu S, Deressa T, Mathewos B, Abate E, Modolell M, Munder M, Muller I, Takele Y, Kropf P. Successful treatment of human visceral leishmaniasis restores antigen-specific IFN-gamma, but not IL-10 production. PLoS neglected tropical diseases 2016; 10(3): e0004468. [DOI:10.1371/journal.pntd.0004468]

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