ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Peruhype-Magalhaes V et al.., 2006. 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. Clin Exp Immunol 146: 124–132.
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CD45RO+ T Cells and T Cell Activation in the Long-Lasting Immunity after Leishmania infantum Infection
João F. Rodrigues-Neto
João F. Rodrigues-Neto
Department of Biochemistry, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Gloria R. Monteiro
Gloria R. Monteiro
Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Tatjana S. L. Keesen
Tatjana S. L. Keesen
Department of Biochemistry, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Henio G. Lacerda
Henio G. Lacerda
Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
Department of Infectious Diseases, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Department of Infectious Diseases, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
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Edgar M. Carvalho
Edgar M. Carvalho
National Institute of Science and Technology of Tropical Diseases (INCT-DT/CNPq), Federal University of Bahia, Salvador, Bahia, Brazil;
Immunology Service, Federal University of Bahia, Salvador, Bahia, Brazil
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Immunology Service, Federal University of Bahia, Salvador, Bahia, Brazil
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Selma M. B. Jeronimo
Selma M. B. Jeronimo
Department of Biochemistry, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
National Institute of Science and Technology of Tropical Diseases (INCT-DT/CNPq), Federal University of Bahia, Salvador, Bahia, Brazil;
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Institute of Tropical Medicine of Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil;
National Institute of Science and Technology of Tropical Diseases (INCT-DT/CNPq), Federal University of Bahia, Salvador, Bahia, Brazil;
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Manifestations of Leishmania infantum infection range from asymptomatic to symptomatic visceral leishmaniasis (VL). People with symptomatic VL (sVL) have suppressed immune responses against Leishmania antigens that are reversed after clinical cure. The intradermal leishmanin skin test (LST) is negative during sVL, but it becomes positive after treatment. The aim of this study was to compare T cell responses in individuals with sVL, recovered VL (RecVL), and endemic controls. Endemic controls were household contacts of a VL case and they were grouped by their LST results, either positive (LST+) or negative (LST−). Mononuclear cells were studied ex vivo or after stimulation with soluble Leishmania antigens (SLA); cell surface markers and cytokines were determined. T cells, ex vivo, from individuals with sVL and from LST+ individuals presented a higher activation for CD4+ and CD8+ cells expressing CD69. However, lymphocytes from sVL stimulated with SLA had lower percentages of CD4+ and CD8+ cells expressing CD69 and CD8+ cells expressing CD25, with no release of interferon-γ or tumor necrosis factor. sVL subjects had lower percentage of memory cells (CD4+ CD45RO+), ex vivo, without SLA stimulation than RecVL, LST+, or LST− (P = 0.0022). However, individuals with sVL had fewer regulatory cells after SLA stimulation (CD4+ CD25HIGH, P = 0.04 and CD4+ FOXP3+, P = 0.02) than RecVL. The decrease in specific memory and activated CD4+ and CD8+ cells, as in response to Leishmania antigens, could explain, in part, the immune impairment during sVL. Finally, protective T cell responses are long lasting because both RecVL or LST+ individuals maintain a specific protective response to Leishmania years after the primary infection.
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Author Notes
Financial support: This work was supported by the National Institutes of Health (AI-30639). J. F. R-N. received a fellowship from CAPES.
Authors’ addresses: João F. Rodrigues-Neto and Tatjana S. L. Keesen, Department of Biochemistry, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil, E-mails: joao_rneto@yahoo.com.br and tat.keesen@gmail.com. Gloria R. Monteiro, Instituto de Medicina Tropical do Rio Grande do Norte, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil, E-mail: gloriag74@hotmail.com. Henio G. Lacerda, Department of Infectious Diseases, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil, E-mail: heniolacerda@ufrnet.br. Edgar M. Carvalho, Serviço de Imunologia, Universidade Federal da Bahia, Salvador, Bahia, Brazil, E-mail: edgar@ufba.br. Selma M. B. Jeronimo, Department of Biochemistry, Universidad Federal do Rio do Norte, Natal, Rio Grande do Norte, Brazil and Universidade Federal do Rio Grand do Norte, Natal, Rio Grande do Norte, Brazil, E-mail: smbj@cb.ufrn.br.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Lainson R, Shaw JJ, Silveira FT, Braga RR, 1987. American visceral leishmaniasis: on the origin of Leishmania (Leishmania) chagasi. Trans R Soc Trop Med Hyg 81: 517.
-
2.
Mauricio IL, Stothard JR, Miles MA, 2000. The strange case of Leishmania chagasi. Parasitol Today 16: 188–189.
-
3.
Evans TG, Teixeira MJ, McAuliffe IT, Vasconcelos I, Vasconcelos AW, Sousa AA, Lima JW, Pearson RD, 1992. Epidemiology of visceral leishmaniasis in northeast Brazil. J Infect Dis 166: 1124–1132.
-
4.
Wilson ME, Jeronimo SM, Pearson RD, 2005. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog 38: 147–160.
-
5.
Caldas AJ, Costa JM, Silva AA, Vinhas V, Barral A, 2002. Risk factors associated with asymptomatic infection by Leishmania chagasi in north-east Brazil. Trans R Soc Trop Med Hyg 96: 21–28.
-
6.
Badaro R, Jones TC, Lorenco R, Cerf BJ, Sampaio D, Carvalho EM, Rocha H, Teixeira R, Johnson WD Jr, 1986. A prospective study of visceral leishmaniasis in an endemic area of Brazil. J Infect Dis 154: 639–649.
-
7.
Costa CH et al.., 2002. Asymptomatic human carriers of Leishmania chagasi. Am J Trop Med Hyg 66: 334–337.
-
8.
Lima ID et al.., 2012. Leishmania infantum chagasi in northeastern Brazil: asymptomatic infection at the urban perimeter. Am J Trop Med Hyg 86: 99–107.
-
9.
Carvalho EM, Barral A, Pedral-Sampaio D, Barral-Netto M, Badaro R, Rocha H, Johnson WD Jr, 1992. Immunologic markers of clinical evolution in children recently infected with Leishmania donovani chagasi. J Infect Dis 165: 535–540.
-
10.
Badaro R, Carvalho EM, Rocha H, Queiroz AC, Jones TC, 1986. Leishmania donovani: an opportunistic microbe associated with progressive disease in three immunocompromised patients. Lancet 1: 647–649.
-
11.
Jeronimo SM, Teixeira MJ, Sousa A, Thielking P, Pearson RD, Evans TG, 2000. Natural history of Leishmania (Leishmania) chagasi infection in northeastern Brazil: long-term follow-up. Clin Infect Dis 30: 608–609.
-
12.
Kaye P, Scott P, 2011. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 9: 604–615.
-
13.
Stassen M et al.., 2004. Human CD25+ regulatory T cells: two subsets defined by the integrins alpha 4 beta 7 or alpha 4 beta 1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 34: 1303–1311.
-
14.
Fakiola M et al.., 2011. Genetic and functional evidence implicating DLL1 as the gene that influences susceptibility to visceral leishmaniasis at chromosome 6q27. J Infect Dis 204: 467–477.
-
15.
Mehrotra S et al.., 2011. No evidence for association between SLC11A1 and visceral leishmaniasis in India. BMC Med Genet 12: 71.
-
16.
Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JM, 2001. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 194: 331–342.
-
17.
Carvalho EM, Bacellar O, Barral A, Badaro R, Johnson WD Jr, 1989. Antigen-specific immunosuppression in visceral leishmaniasis is cell mediated. J Clin Invest 83: 860–864.
-
18.
Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson WD Jr, 1985. Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. J Clin Invest 76: 2066–2069.
-
19.
Saha S 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.
-
20.
Ansari NA, Kumar R, Gautam S, Nylen S, Singh OP, Sundar S, Sacks D, 2011. IL-27 and IL-21 are associated with T cell IL-10 responses in human visceral leishmaniasis. J Immunol 186: 3977–3985.
-
21.
Ansari NA, Saluja S, Salotra P, 2006. Elevated levels of interferon-gamma, interleukin-10, and interleukin-6 during active disease in Indian kala azar. Clin Immunol 119: 339–345.
-
22.
Peruhype-Magalhaes V et al.., 2006. 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. Clin Exp Immunol 146: 124–132.
-
23.
Singh OP, Gidwani K, Kumar R, Nylen S, Jones SL, Boelaert M, Sacks D, Sundar S, 2012. Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clin Vaccine Immunol 19: 961–966.
-
24.
Jordan KA, Hunter CA, 2010. Regulation of CD8+ T cell responses to infection with parasitic protozoa. Exp Parasitol 126: 318–325.
-
25.
Gollob KJ, Antonelli LR, Dutra WO, 2005. Insights into CD4+ memory T cells following Leishmania infection. Trends Parasitol 21: 347–350.
-
26.
Maurya R, Kumar R, Prajapati VK, Manandhar KD, Sacks D, Sundar S, Nylen S, 2010. Human visceral leishmaniasis is not associated with expansion or accumulation of Foxp3+ CD4 cells in blood or spleen. Parasite Immunol 32: 479–483.
-
27.
Pakpour N, Zaph C, Scott P, 2008. The central memory CD4+ T cell population generated during Leishmania major infection requires IL-12 to produce IFN-gamma. J Immunol 180: 8299–8305.
-
28.
Polley R, Zubairi S, Kaye PM, 2005. The fate of heterologous CD4+ T cells during Leishmania donovani infection. Eur J Immunol 35: 498–504.
-
29.
Nylen S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, Sacks D, 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.
-
30.
Rai AK, Thakur CP, Singh A, Seth T, Srivastava SK, Singh P, Mitra DK, 2012. Regulatory T cells suppress T cell activation at the pathologic site of human visceral leishmaniasis. PLoS One 7: e31551.
-
31.
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.
-
32.
Baeten DL, Kuchroo VK, 2013. How cytokine networks fuel inflammation: interleukin-17 and a tale of two autoimmune diseases. Nat Med 19: 824–825.
-
33.
Banerjee A, Bhattacharya P, Joshi AB, Ismail N, Dey R, Nakhasi HL, 2016. Role of pro-inflammatory cytokine IL-17 in Leishmania pathogenesis and in protective immunity by Leishmania vaccines. Cell Immunol 309: 37–41.
-
34.
Jeronimo SM et al.., 2007. Genetic predisposition to self-curing infection with the protozoan Leishmania chagasi: a genomewide scan. J Infect Dis 196: 1261–1269.
-
35.
Jeronimo SM et al.., 2004. An emerging peri-urban pattern of infection with Leishmania chagasi, the protozoan causing visceral leishmaniasis in northeast Brazil. Scand J Infect Dis 36: 443–449.
-
36.
Braz RF, Nascimento ET, Martins DR, Wilson ME, Pearson RD, Reed SG, Jeronimo SM, 2002. The sensitivity and specificity of Leishmania chagasi recombinant K39 antigen in the diagnosis of American visceral leishmaniasis and in differentiating active from subclinical infection. Am J Trop Med Hyg 67: 344–348.
-
37.
Jose FF, da Silva IM, Araujo MI, Almeida RP, Bacellar O, Carvalho EM, 2001. Evaluation of the sensitization power of Montenegro skin test. Rev Soc Bras Med Trop 34: 537–542.
-
38.
Sokal JE, 1975. Editorial: measurement of delayed skin-test responses. N Engl J Med 293: 501–502.
-
39.
Alvar J, Yactayo S, Bern C, 2006. Leishmaniasis and poverty. Trends Parasitol 22: 552–557.
-
40.
Belo VS, Struchiner CJ, Barbosa DS, Nascimento BW, Horta MA, da Silva ES, Werneck GL, 2014. Risk factors for adverse prognosis and death in American visceral leishmaniasis: a meta-analysis. PLoS Negl Trop Dis 8: e2982.
-
41.
Kaushal H, Bras-Goncalves R, Negi NS, Lemesre JL, Papierok G, Salotra P, 2014. Role of CD8(+) T cells in protection against Leishmania donovani infection in healed visceral leishmaniasis individuals. BMC Infect Dis 14: 653.
-
42.
Darrah PA et al.., 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843–850.
-
43.
Selvapandiyan A, Dey R, Nylen S, Duncan R, Sacks D, Nakhasi HL, 2009. Intracellular replication-deficient Leishmania donovani induces long lasting protective immunity against visceral leishmaniasis. J Immunol 183: 1813–1820.
-
44.
Ferrari C, 2015. HBV and the immune response. Liver Int 35 (Suppl 1): 121–128.
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