CD4+FOXP3+ cells produce IL-10 in the spleens of dogs with visceral leishmaniasis

Veterinary Parasitology

Volumn 202, Issue 3-4, 2014, Pages 313-318

  Silva, Kathlenn Liezbeth Oliveira ^a   De Andrade, Mariana M C ^a   Melo, Larissa M ^a   Perosso, Juliana ^a   Vasconcelos, Rosemeri O ^a   Munari, Danisio P ^a   Lima, Valéria M F ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Dog cytokines; IL 10; Leishmania; Regulatory T cells; TGF

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CD4+ FOXP3+ REGULATORY T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOG DISEASE; FEMALE; FLOW CYTOMETRY; IMMUNOMODULATION; LEISHMANIA; LYMPHOCYTE COUNT; MALE; NONHUMAN; PARASITE LOAD; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; VISCERAL LEISHMANIASIS;

ANIMALIA; CANIS FAMILIARIS; PHLEBOTOMINAE;

DOG CYTOKINES; IL-10; LEISHMANIA; REGULATORY T CELLS; TGF-Β;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; DOG DISEASES; DOGS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-10; LEISHMANIASIS, VISCERAL; MALE; PARASITE LOAD; SPLEEN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84900414867     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2014.03.010     Document Type: Article

References (44)

1. Ashford R.W., Desjeux P., de Raadt P. Estimation of population at risk of infection and number of cases of Leishmaniasis. Parasitol. Today 1992, 8:104-105.
2. Biller B.J., Elmslie R.E., Burnett R.C., Avery A.C., Dow S.W. Use of FoxP3 expression to identify regulatory T cells in healthy dogs and dogs with cancer. Vet. Immunol. Immunopathol. 2007, 116:69-78.
3. Boggiatto P.M., Ramer-Tait A.E., Metz K., Kramer E.E., Gibson-Corley K., Mullin K., Hostetter J.M., Gallup J.M., Jones D.E., Petersen C.A. Immunologic indicators of clinical progression during canine Leishmania infantum infection. Clin. Vaccine Immunol. 2010, 17:267-273.
4. Chen Y., Kuchroo V.K., Inobe J., Hafler D.A., Weiner H.L. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994, 265:1237-1240.
5. Corrêa A.P., Dossi A.C., de Oliveira Vasconcelos R., Munari D.P., de Lima V.M. Evaluation of transformation growth factor beta1, interleukin-10, and interferon-gamma in male symptomatic and asymptomatic dogs naturally infected by Leishmania (Leishmania) chagasi. Vet. Parasitol. 2007, 143:267-274.
6. Cortese L., Annunziatella M., Palatucci A.T., Rubino V., Piantedosi D., Di Loria A., Ruggiero G., Ciaramella P., Terrazzano G. Regulatory T cells, cytotoxic T lymphocytes and a TH1 cytokine profile in dogs naturally infected by Leishmania infantum. Res. Vet. Sci 2013, 10.1016/j.rvsc.2013.08.005.
7. Das G., Vohra H., Rao K., Saha B., Mishra G.C. Leishmania donovani infection of a susceptible host results in CD4+ T-cell apoptosis and decreased Th1 cytokine production. Scand. J. Immunol. 1999, 49:307-310.
8. Deane L.M., Deane M.P. Observações preliminares sobre a importância comparativa do homem, do cão e da raposa (Lycalopex vetulus) como reservatórios de Leishmania donovani em área endêmica de calazar no Ceará. Hospital (Rio. J). 1955, 48:61-76.
9. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 2004, 27:305-318.
10. Fehervari Z., Sakaguchi S. CD4+ Tregs and immune control. J. Clin. Invest. 2004, 114:1209-1217.
11. Foglia Manzillo V., Pagano A., Paciello O., Di Muccio T., Gradoni L., Oliva G. Papular-like glossitis in a dog with leishmaniosis. Vet. Rec. 2005, 156:213-215.
12. Furtado G.C., Curotto de Lafaille M.A., Kutchukhidze N., Lafaille J.J. Interleukin 2 signaling is required for CD4(+) regulatory T cell function. J. Exp. Med. 2002, 196:851-857.
13. Gesser B., Leffers H., Jinquan T., Vestergaard C., Kirstein N., Sindet-Pedersen S., Jensen S.L., Thestrup-Pedersen K., Larsen C.G. Identification of functional domains on human interleukin 10. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14620-14625.
14. Ghalib H.W., Piuvezam M.R., Skeiky Y.A., Siddig M., Hashim F.A., el-Hassan A.M., Russo D.M., Reed S.G. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 1993, 92:324-329.
15. Ginel P.J., Camacho S., Lucena R. Anti-histone antibodies in dogs with leishmaniasis and glomerulonephritis. Res. Vet. Sci. 2008, 85:510-514.
16. Gontijo C.M.F., Melo M.N. Leishmaniose Visceral no Brasil: quadro atual, desafios e perspectivas. Rev. Bras. Epidemiol. 2004, 7:338-349.
17. Katara G.K., Ansari N.A., Verma S., Ramesh V., Salotra P. Foxp3 and IL-10 expression correlates with parasite burden in lesional tissues of post kala azar dermal leishmaniasis (PKDL) patients. PLoS Negl. Trop. 2011, 5:e1171.
18. Kenney R.T., Sacks D.L., Gam A.A., Murray H.W., Sundar S. Splenic cytokine responses in Indian kala-azar before and after treatment. J. Infect. Dis. 1998, 177:815-818.
19. Keppel K.E., Campbell K.L., Zuckermann F.A., Greeley E.A., Schaeffer D.J., Husmann R.J. Quantitation of canine regulatory T cell populations, serum interleukin-10 and allergen-specific IgE concentrations in healthy control dogs and canine atopic dermatitis patients receiving allergen-specific immunotherapy. Vet. Immunol. Immunopathol. 2008, 123:337-344.
20. Kim J.H., Hur J.H., Lee S.M., Im K.S., Kim N.H., Sur J.H. Correlation of Foxp3 positive regulatory T cells with prognostic factors in canine mammary carcinomas. Vet. J. 2012, 193:222-227.
21. Kim J.H., Chon S.K., Im K.S., Kim N.H., Cho K.W., Sur J.H. Infiltrating Foxp3+ regulatory T cells and histopathological features in canine classical and spermatocytic seminomas. Reprod. Domest. Anim. 2013, 48:218-222.
22. Lage R.S., Oliveira G.C., Busek S.U., Guerra L.L., Giunchetti R.C., Corrêa-Oliveira R., Reis A.B. Analysis of the cytokine profile in spleen cells from dogs naturally infected by Leishmania chagasi. Vet. Immunol. Immunopathol. 2007, 115:135-145.
23. Lima V.M., Gonçalves M.E., Ikeda F.A., Luvizotto M.C., Feitosa M.M. Anti-leishmania antibodies in cerebrospinal fluid from dogs with visceral leishmaniasis. Braz. J. Med. Biol. 2003, 36:485-489.
24. Lima V.M., Fattori K.R., de Souza F., Eugênio F.R., dos Santos P.S., Rozza D.B., Machado G.F. Apoptosis in T lymphocytes from spleen tissue and peripheral blood of L. (L.) chagasi naturally infected dogs. Vet. Parasitol. 2012, 184:147-153.
25. Lu P., Zucker K., Fuller L., Tzakis A., Esquenazi V., Miller J. Cloning and expression of canine interleukin-10. J. Interferon Cytokine Res. 1995, 15:1103-1109.
26. Maia C., Campino L. Cytokine and phenotypic cell profiles of Leishmania infantum infection in the dog. J. Trop. Med. 2012, 2012:541571.
27. Maurya R., Kumar R., Prajapati V.K., Manandhar K.D., Sacks D., Sundar S., Nylén S. Brief definitive report: human visceral leishmaniasis is not associated with expansion or accumulation of Foxp3+ CD4 cells in blood or spleen. Parasite Immunol. 2010, 32:479-483.
28. Menezes-Souza D., Corrêa-Oliveira R., Guerra-Sá R., Giunchetti R.C., Teixeira-Carvalho A., Martins-Filho O.A., Oliveira G.C., Reis A.B. Cytokine and transcription factor profiles in the skin of dogs naturally infected by Leishmania (Leishmania) chagasi presenting distinct cutaneous parasite density and clinical status. Vet. Parasitol. 2011, 177:39-49.
29. Nylén S., Maurya R., Eidsmo L., Manandhar K.D., Sundar S., Sacks D. Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (FOXP3) regulatory T cells in human visceral leishmaniasis. J. Exp. Med. 2007, 204:805-817.
30. O'Neill K., Guth A., Biller B., Elmslie R., Dow S. Changes in regulatory T cells in dogs with cancer and associations with tumor type. J. Vet. Intern. Med. 2009, 23:875-881.
31. Pinelli E., Killick-Kendrick R., Wagennar J., Bernadina W., Del Real G., Ruitenberg E.J. Cellular and humoral responses in dogs experimentally and naturally infected with Leishmania infantum. Infect. Immun. 1994, 62:229-235.
32. Pinelli E., Gonzalo R.M., Boog C.J., Rutten V.P., Gebhard D., Del Real G., Ruitenberg E.J. Leishmania infantum-specific T cell lines derived from asymptomatic dogs that lyse infected macrophages in a major histocompatibility complex-restricted manner. Eur. J. Immunol. 1995, 25:1594-1600.
33. Pinelli E., Rutten V.P., Bruysters M., Moore P.F., Ruitenberg E.J. Compensation for decreased expression of B7 molecules on Leishmania infantum-infected canine macrophages results in restoration of parasite-specific T-cell proliferation and gamma interferon production. Infect. Immun. 1999, 67:237-243.
34. Pinheiro D., Singh Y., Grant C.R., Appleton R.C., Sacchini F., Walker K.R., Chadbourne A.H., Palmer C.A., Armitage-Chan E., Thompson I., Williamson L., Cunningham F., Garden O.A. Phenotypic and functional characterization of a CD4(+) CD25(high) FOXP3(high) regulatory T-cell population in the dog. Immunology 2011, 132:111-122.
35. Rai A.K., Thakur C.P., Singh A., Seth T., Srivastava S.K., Singh P., Mitra D.K. Regulatory T cells suppress T cell activation at the pathologic site of human visceral leishmaniasis. PLoS One 2012, 7:e31551.
36. Ramsdell F. Foxp3 and natural regulatory T cells: key to a cell lineage?. Immunity 2003, 19:165-168.
37. Roatt B.M., Aguiar-Soares R.D., Vitoriano-Souza J., Coura-Vital W., Braga S.L., Corrêa-Oliveira R., Martins-Filho O.A., Teixeira-Carvalho A., de Lana M., Figueiredo Gontijo N., Marques M.J., Giunchetti R.C., Reis A.B. Performance of LBSap vaccine after intradermal challenge with L. infantum and saliva of Lu. longipalpis: immunogenicity and parasitological evaluation. PLoS One 2012, 7:e49780.
38. Rodgers M.R., Popper S.J., Wirth D.F. Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Exp. Parasitol. 1990, 71:267-275.
39. Rodrigues O.R., Marques C., Soares-Clemente M., Ferronha M.H., Santos-Gomes G.M. Identification of regulatory T cells during experimental Leishmania infantum infection. Immunobiology 2009, 214:101-111.
40. Saha S., Mondal S., Ravindran R., Bhowmick S., Modak D., Mallick S., Rahman M., Kar S., Goswami R., Guha S.K., Pramanik N., Saha B., Ali N. 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. (Baltimore Md. 1950) 2007, 179:5592-5603.
41. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated t cells expressing IL-2 Receptor-alfa-chains (CD25). J. Immunol. 1995, 155:1151-1164.
42. Too H.P. Real time PCR quantification of GFR-2 alternatively spliced isoforms in murine brain and peripheral tissues. Brain Res. Mol. Brain Res. 2003, 114:146-154.
43. Verma S., Kumar R., Katara G.K., Singh C.L., Negi N.S., Ramesh V., Salotra P. Foxp3 quantification of parasite load in clinical samples of leishmaniasis patients: IL-10 level correlates with parasite load in visceral leishmaniasis. PLoS. Negl. Trop. Dis. 2011, 5(4):e1171.
44. Wilson M.E., Young B.M., Davidson B.L., Mente K.A., Mcgowan S.E. The importance of TGF-b in murine visceral leishmaniasis. J. Immunol. 1998, 161:6148-6155.