Cytokine and transcription factor profiles in the skin of dogs naturally infected by Leishmania (Leishmania) chagasi presenting distinct cutaneous parasite density and clinical status

Veterinary Parasitology

Volumn 177, Issue 1-2, 2011, Pages 39-49

  Menezes Souza, Daniel ^a,b   Corrêa Oliveira, Rodrigo ^b   Guerra Sá, Renata ^a   Giunchetti, Rodolfo Cordeiro ^a,b   Teixeira Carvalho, Andréa ^b   Martins Filho, Olindo Assis ^b   Oliveira, Guilherme Corrêa ^b   Reis, Alexandre Barbosa ^a,b  

^a FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Canine visceral leishmaniasis; Cytokines; Leishmania chagasi; Parasitism; Real time PCR; Transcription factors

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL TISSUE; ARTICLE; ASYMPTOMATIC INFECTION; CONTROLLED STUDY; DOG; FEMALE; IMMUNOREGULATION; INFLAMMATION; LEISHMANIA CHAGASI; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IMMUNITY; PROTEIN EXPRESSION; SKIN LEISHMANIASIS; VISCERAL LEISHMANIASIS;

ANIMALS; CYTOKINES; DOG DISEASES; DOGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; SKIN; TRANSCRIPTION FACTORS;

CANIS FAMILIARIS; LEISHMANIA DONOVANI CHAGASI;

EID: 79953161829     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2010.11.025     Document Type: Article

References (44)

1. Abranches P., Silva-Pereira M.C., Conceição-Silva F.M., Santos-Gomes G.M., Janz J.G. Canine leishmaniasis: pathological and ecological factors influencing transmission of infection. J. Parasitol. 1991, 77:557-561.
2. Alves C.F., de Amorim I.F., Moura E.P., Ribeiro R.R., Michalick M.S., Kalapothakis E., Bruna-Romero O., Tafuri W.L., Teixeira M.M., Melo M.N. Expression of IFN-gamma, TNF-alpha, IL-10 and TGF-beta in lymph nodes associates with parasite load and clinical form of disease in dogs naturally infected with Leishmania (Leishmania) chagasi. Vet. Immunol. Immunopathol. 2009, 128(4):349-358.
3. 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.
4. Carrillo E., Moreno J. Cytokine profiles in canine visceral leishmaniasis. Vet. Immunol. Immunopathol. 2009, 128:67-70.
5. Chamizo C., Moreno J., Alvar J. Semi-quantitative analysis of cytokine expression in asymptomatic canine leishmaniasis. Vet. Immunol. Immunopathol. 2005, 103:67-75.
6. D'Andrea A., Ma X., Aste-Amezaga M., Paganin C., Trinchieri G. Stimulatory and inhibitory effects of interleukin (IL)-4 and IL-13 on the production of cytokines by human peripheral blood mononuclear cells: priming for IL-12 and tumor necrosis factor-α production. J. Exp. Med. 1995, 181:537-546.
7. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 2004, 27:305-318.
8. Dos-Santos L.R., Barrouin-Melo S.M., Chang Y.F., Olsen J., McDonough S.P., Quimby F., dos Santos W.L., Pontes-de-Carvalho L.C., Oliveira G.G. Recombinant single-chain canine interleukin 12 induces interferon gamma mRNA expression in peripheral blood mononuclear cells of dogs with visceral leishmaniasis. Vet. Immunol. Immunopathol. 2004, 98:43-48.
9. Gantt K.R., Schultz-Cherry S., Rodriguez N., Jeronimo S.M., Nascimento E.T., Goldman T.L., Recker T.J., Miller M.A., Wilson M.E. Activation of TGF-beta by Leishmania chagasi: importance for parasite survival in macrophages. J. Immunol. 2003, 170:2613-2620.
10. Giunchetti R.C., Mayrink W., Genaro O., Carneiro C.M., Corrêa-Oliveira R., Martins-Filho O.A., Marques M.J., Tafuri W.L., Reis A.B. Relationship between canine visceral leishmaniasis and the Leishmania (Leishmania) chagasi burden in dermal inflammatory foci. J. Comp. Pathol. 2006, 135:100-107.
11. Giunchetti R.C., Martins-Filho O.A., Carneiro C.M., Mayrink W., Marques M.J., Tafuri W.L., Corrêa-Oliveira R., Reis A.B. Histopathology, parasite density and cell phenotypes of the popliteal lymph node in canine visceral leishmaniasis. Vet. Immunol. Immunopathol. 2008, 121:23-33.
12. Giunchetti R.C., Mayrink W., Carneiro C.M., Corrêa-Oliveira R., Martins-Filho O.A., Marques M.J., Tafuri W.L., Reis A.B. Histopathological and immunohistochemical investigations of the hepatic compartment associated with parasitism and serum biochemical changes in canine visceral leishmaniasis. Res. Vet. Sci. 2008, 84:269-277.
13. Guerra L.L., Teixeira-Carvalho A., Giunchetti R.C., Martins-Filho O.A., Reis A.B., Corrêa-Oliveira R. Evaluation of the influence of tissue parasite density on hematological and phenotypic cellular parameters of circulating leukocytes and splenocytes during ongoing canine visceral leishmaniasis. Parasitol Res. 2009, 104:611-622.
14. Kemp M., Theander T.G., Kharazmi A. The contrasting roles of CD4+ T cells in intracellular infections in humans: leishmaniasis as an example. Immunol. Today 1996, 17:13-16.
15. Kitamura N., Kaminuma O., Mori A., Hashimoto T., Kitamura F., Miyagishi M., Taira K., Miyatake S. Correlation between mRNA expression of Th1/Th2 cytokines and their specific transcription factors in human helper T-cells clones. Immunol. Cell Biol. 2005, 83:536-541.
16. 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.
17. Manna L., Reale S., Vitale F., Gravino A.E. Evidence for a relationship between Leishmania load and clinical manifestations. Res. Vet. Sci. 2009, 87:76-78.
18. Mancianti F., Gramiccia M., Gradoni L., Pieri S. Studies on canine leishmaniasis control. I. Evolution of infection of different clinical forms of canine leishmaniasis following antimonial treatment. Trans. R. Soc. Trop. Med. Hyg. 1988, 82:566-567.
19. Marson A., Kretschmer K., Frampton G.M., Jacobsen E.S., Polansky J.K., MacIsaac K.D., Levine S.S., Fraenkel E., von Boehmer H., Young R.A. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007, 445:931-935.
20. Mary C., Auriault V., Faugere B., Dessein A. Control of Leishmania infantun infection is associated with CD8+ and gamma interferon and interleukin-5-production CD4+ antigen-specific T-cells. Infect. Immun. 1999, 67:5559-5566.
21. Moreno J., Alvar J. Canine leishmaniasis: epidemiological risk and the experimental model. Trends Parasitol. 2002, 18:399-405.
22. Murray H.W., Tsai C.W., Liu J., Ma X. Visceral Leishmania donovani infection in interleukin-13-/- mice. Infect. Immun. 2006, 74:2487-2490.
23. Nagasawa M., Ohshiba A., Yata J. Effect of recombinant interleukin 5 on the generation of cytotoxic T cells (CTL). Cell Immunol. 1991, 133:317-326.
24. Peruhype-Magalhães V., Martins-Filho O.A., Prata A., Silva L.De-A., Rabello A., Teixeira-Carvalho A., Figueiredo R.M., Guimarães-Carvalho S.F., Ferrari T.C., Corrêa-Oliveira R. Immune response in human visceral leishmaniasis: analysis of the correlation between innate immunity cytokine profile and disease outcome. Scand. J. Immunol. 2005, 62:487-495.
25. Peruhype-Magalhães V., Martins-Filho O.A., Prata A., Silva L.De-A., Rabello A., Teixeira-Carvalho A., Figueiredo R.M., Guimarães-Carvalho S.F., Ferrari T.C., 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. Clin. Exp. Immunol. 2006, 146:124-132.
26. Pinelli E., Killick-Kendrick R., Wagenaar J., Bernadina W., del Real G., Ruitenberg J. Cellular and humoral immune responses in dogs experimentally and naturally infected with Leishmania infantum. Infect. Immun. 1994, 62:229-235.
27. Quinnell R.J., Courtenay O., Shaw M.A., Day M.J., Garcez L.M., Dye C., Kaye P.M. Tissue cytokine responses in canine visceral leishmaniasis. J. Infect. Dis. 2001, 183:1421-1424.
28. Raziuddin S., Abdalla R.E., el-Awad E.H., al-Janadi M. Immunoregulatory and proinflammatory cytokine production in visceral and cutaneous leishmaniasis. J. Infect. Dis. 1994, 170:1037-1040.
29. Reis A.B., Martins-Filho O.A., Teixeira-Carvalho A., Carvalho M.G., Mayrink W., Franca-Silva J.C., Giunchetti R.C., Genaro O., Corrêa-Oliveira R. Parasite density and impaired biochemical/hematological status are associated with severe clinical aspects of canine visceral leishmaniasis. Res. Vet. Sci. 2006, 81:68-75.
30. Reis A.B., Teixeira-Carvalho A., Vale A.M., Marques M.J., Giunchetti R.C., Mayrink W., Guerra L.L., Andrade R.A., Correa-Oliveira R., Martins-Filho O.A. Isotype patterns of immunoglobulins: hallmarks for clinical status and tissue parasite density in Brazilian dogs naturally infected by Leishmania (Leishmania) chagasi. Vet. Immunol. Immunopathol. 2006, 112:102-116.
31. Reis A.B., Teixeira-Carvalho A., Giunchetti R.C., Guerra L.L., Carvalho M.G., Mayrink W., Genaro O., Corrêa-Oliveira R., Martins-Filho O.A. Phenotypic features of circulating leucocytes as immunological markers for clinical status and bone marrow parasite density in dogs naturally infected by Leishmania chagasi. Clin. Exp. Immunol. 2006, 146:303-311.
32. Reis A.B., Martins-Filho O.A., Teixeira-Carvalho A., Giunchetti R.C., Carneiro C.M., Mayrink W., Tafuri W.L., Corrêa-Oliveira R. Systemic and compartmentalized immune response in canine visceral leishmaniasis. Vet. Immunol. Immunopathol. 2009, 128:87-95.
33. Rosas L.E., Snider H.M., Barbi J., Satoskar A.A., Lugo-Villarino G., Keiser T., Papenfuss T., Durbin J.E., Radzioch D., Glimcher L.H., Satoskar A.R. Cutting Edge: STAT1 and T-bet play distinct roles in determining outcome of visceral leishmaniasis caused by Leishmania donovani. J. Immunol. 2006, 177:22-25.
34. Sanchez M.A., Diaz N.L., Zerpa O., Negron E., Convit J., Tapia F.J. Organ-specific immunity in canine visceral leishmaniasis: analysis of symptomatic and asymptomatic dogs naturally infected with Leishmania chagasi. Am. J. Trop. Med. Hyg. 2004, 70:618-624.
35. Sanchez-Robert E., Altet L., Alberola J., Rodriguez-Cortés A., Ojeda A., López-Fuertes L., Timon M., Sanchez A., Francino O. Longitudinal analysis of cytokine gene expression and parasite load in PBMC in Leishmania infantum experimentally infected dogs. Vet. Immunol. Immunopathol. 2008, 15:168-175.
36. Satoskar A., Bluethmann H., Alexander J. Disruption of the murine interleukin-4 gene inhibits disease progression during Leishmania mexicana infection but does not increase control of Leishmania donovani infection. Infect. Immun. 1995, 63:4894-4899.
37. Silvestre R., Cordeiro-Da-Silva A., Santarém N., Vergnes B., Sereno D., Ouaissi A. SIR2-deficient Leishmania infantum induces a defined IFN-gamma/IL-10 pattern that correlates with protection. J. Immunol. 2007, 179:3161-3170.
38. Stauber L.A. Leishmaniasis in the hamster. Some Physiological Aspects and Consequences of Parasitism 1955, 77-90. Rugers University Press, New Brunswick. W.H. Cole (Ed.).
39. Strauss-Ayali D., Baneth G., Shor S., Okano F., Jaffe C.L. Interleukin-12 augments a Th1-type immune response manifested as lymphocyte proliferation and interferon gamma production in Leishmania infantum-infected dogs. Int. J. Parasitol. 2005, 35:63-73.
40. Strauss-Ayali D., Baneth G., Jaffe C. Splenic immune responses during canine visceral leishmaniasis. Vet. Res. 2007, 38:547-564.
41. Szabo S.J., Sullivan B.M., Stemmann C., Satoskar A.R., Sleckman B.P., Glimcher L.H. Distinct effects of T-bet in TH1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 2002, 295:338-342.
42. Trinchieri G., Pflanz S., Kastelein R.A. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003, 19:641-644.
43. Vouldoukis I., Bécherel P.A., Riveros-Moreno V., Arock M., da Silva O., Debré P., Mazier D., Mossalayi M.D. Interleukin-10 and interleukin-4 inhibit intracellular killing of Leishmania infantum and Leishmania major by human macrophages by decreasing nitric oxide generation. Eur. J. Immunol. 1997, 27:860-865.
44. Zheng Y., Josefowicz S.Z., Kas A., Chu T.T., Gavin M.A., Rudensky A.Y. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 2007, 445:936-940.