Histopathology, humoral and cellular immune response in the murine model of Leishmania (Viannia) shawi

Parasitology International

Volumn 59, Issue 2, 2010, Pages 159-165

  Passero, Luiz Felipe Domingues ^a   Marques, Cláudia ^b   Vale Gato, Inês ^b   Corbett, Carlos Eduardo Pereira ^a   Laurenti, Márcia Dalastra ^a   Santos Gomes, Gabriela ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

Author keywords

Cytokines; Histopathology; IgG1; IL 10; Leishmania (Viannia) shawi; TGF

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

AMASTIGOTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNOPATHOLOGY; INFLAMMATORY INFILTRATE; LEISHMANIA; LEISHMANIA SHAWI; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN LEISHMANIASIS; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIBODIES, PROTOZOAN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DERMIS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOGLOBULIN G; LEISHMANIA; LEISHMANIASIS, CUTANEOUS; MACROPHAGES; MICE; MICE, INBRED BALB C;

LEISHMANIA SHAWI; MURINAE; MUS;

EID: 77951652826     PISSN: 13835769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.parint.2009.12.010     Document Type: Article

References (51)

1. Shaw J.J. Taxonomy of the genus Leishmania: present and future trends and their implications. Mem Inst Oswaldo Cruz 89 (1994) 471-478
2. Sinha S., Fernández G., Kapila R., Lambert W.C., and Schwartz R.A. Diffuse cutaneous leishmaniasis associated with the immune reconstitution inflammatory syndrome. Int J Dermatol 47 (2008) 1263-1270
3. Louis J.A., Gumy A., Voigt H., Launois P., and Rocken M. Experimental cutaneous Leishmaniasis: a powerful model to study in vivo the mechanisms underlying genetic differences in Th subset differentiation. Eur J Dermatol 12 (2002) 316-318
4. Bourreau E., Gardon J., Pradinaud R., Pascalis H., Prévot-Linguet G., Kariminia A., et al. Th2 responses predominate during the early phases of infection in patients with localized cutaneous leishmaniasis and precede the development of Th1 responses. Infect Immun 71 (2003) 2244-2256
5. Ajdary S., Alimohammadian M.H., Eslami M.B., Kemp K., and Kharazmi A. Comparison of the immune profile of nonhealing cutaneous Leishmaniasis patients with those with active lesions and those who have recovered from infection. Infect Immun 68 (2000) 1760-1764
6. Louzir H., Melby P.C., Ben Salah A., Marrakchi H., Aoun K., Ben Ismail R., et al. Immunologic determinants of disease evolution in localized cutaneous leishmaniasis due to Leishmania major. J Infect Dis 177 (1998) 1687-1695
7. Maioli T.U., Takane E., Arantes R.M., Fietto J.L., and Afonso L.C. Immune response induced by New World Leishmania species in C57BL/6 mice. Parasitol Res 94 (2004) 207-212
8. Rocha F.J., Schleicher U., Mattner J., Alber G., and Bogdan C. Cytokines, signaling pathways, and effector molecules required for the control of Leishmania (Viannia) braziliensis in mice. Infect Imun 75 (2008) 3823-3832
9. Abreu-Silva A.L., Calabrese K.S., Cupolilo S.M., Cardoso F.O., Souza C.S., and Gonçalves da Costa S.C. Histopathological studies of visceralized Leishmania (Leishmania) amazonensis in mice experimentally infected. Vet Parasitol 121 (2004) 179-187
10. Lainson R., Braga R.R., De Souza A.A., Pôvoa M.M., Ishikawa E.A., and Silveira F.T. Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths and procyonids in Amazonian Brazil. Ann Parasitol Hum Comp 64 (1989) 200-207
11. Shaw J.J., Ishikawa E.A., Lainson R., Braga R.R., and Silveira F.T. Cutaneous leishmaniasis of man due to Leishmania (Viannia) shawi Lainson, de Souza, Póvoa, Ishikawa & Silveira, in Pará State, Brazil. Ann Parasitol Hum Comp 66 (1991) 243-246
12. Brito M.E., Andrade M.S., Mendonça M.G., Silva C.J., Almeida E.L., Lima B.S., et al. Species diversity of Leishmania (Viannia) parasites circulating in an endemic area for cutaneous leishmaniasis located in the Atlantic rainforest region of northeastern Brazil. Trop Med Int Health 14 (2009) 1278-1286
13. Rodrigues O.R., Marques C., Soares-Clemente M., Ferronha M.H., and Santos-Gomes G.M. Identification of regulatory T cells during experimental Leishmania infantum infection. Immunobiol 214 (2009) 101-111
14. Giunchetti R.C., Martins-Filho O.A., Carneiro C.M., Mayrink W., Marques M.J., Tafuri W.L., et al. Histopathology, parasite density and cell phenotypes of the popliteal lymph node in canine visceral leishmaniasis. Vet Immunol Immunopathol 121 (2008) 23-33
15. Passero L.F.D., Laurenti M.D., Tomokane T.Y., Corbett C.E.P., and Toyama M.H. The effect of phospholipase A2 from Crotalus durissus collilineatus on Leishmania (Leishmania) amazonensis infection. Parasitol Res 102 (2008) 1025-1033
16. Rosa R., Rodrigues O.R., Marques C., and Santos-Gomes G.M. Leishmania infantum: soluble proteins released by the parasite exert differential effects on host immune response. Exp Parasitol 109 (2005) 106-114
17. Rodrigues O.R., Moura R.A., Gomes-Pereira S., and Santos-Gomes G.M. H-2 complex influences cytokine gene expression in Leishmania infantum-infected macrophages. Cell Immunol 243 (2006) 118-126
18. Morgado F.N., Schubach A., Rosalino C.M., Quintella L.P., Santos G., Salgueiro M., et al. Is the in situ inflammatory reaction an important tool to understand the cellular immune response in American tegumentary leishmaniasis?. Br J Dermatol 158 (2008) 50-58
19. Donnely K.B., Lima H.C., and Titus R.G. Histologic characterization of experimental cutaneous leishmaniasis in mice infected with Leishmania braziliensis in the presence or absence of sand fly vector salivary gland lysate. J Parasitol 84 (1998) 97-103
20. Wanasen N., Xin L., and Soong L. Pathogenic role of B cells and antibodies in murine Leishmania amazonensis infection. Int J Parasitol 38 (2008) 417-429
21. Tacchini-Cottier F., Zweifel C., Belkaid Y., Mukankundiye C., Vasei M., Launois P., et al. An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J Immunol 165 (2000) 2628-2636
22. Silveira F.T., Lainson R., and Corbett C.E. Further observations on clinical, histopathological, and immunological features of borderline disseminated cutaneous leishmaniasis caused by Leishmania (Leishmania) amazonensis. Mem Inst Oswaldo Cruz 100 (2005) 525-534
23. Moraes M.A., and Silveira F.T. Histopathology of the localized form of cutaneous leishmaniasis caused by Leishmania (Leishmania) amazonensis. Rev Inst Med Trop Sao Paulo 36 (1994) 459-463
24. McKinney L.A., and Hendricks L.D. Experimental infection of Mystromys albicaudatus with Leishmania braziliensis: pathology. Am J Trop Med Hyg 29 (1980) 753-760
25. Lujan R., Dennis V.A., Chapman Jr. W.L., and Hanson W.L. Blastogenic responses of peripheral blood leukocytes from owl monkeys experimentally infected with Leishmania braziliensis panamensis. Am J Trop Med Hyg 35 (1986) 1103-1109
26. de Moura T.R., Novais F.O., Oliveira F., Clarêncio J., Noronha A., Barral A., et al. Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect Immun 73 (2005) 5827-5834
27. Gutierrez Y., Salinas G.H., Palma G., Valderrama L.B., Santrich C.V., and Saravia N.G. Correlation between histopathology, immune response, clinical presentation, and evolution in Leishmania braziliensis infection. Am J Trop Med Hyg 45 (1991) 281-289
28. Pirmez C., Yamamura M., Uyemura K., Paes-Oliveira M., Conceição-Silva F., and Modlin R.L. Cytokine patterns in the pathogenesis of human leishmaniasis. J Clin Invest 91 (1993) 1390-1395
29. de Souza-Neto S.M., Carneiro C.M., Vieira L.Q., and Afonso L.C. Leishmania braziliensis: partial control of experimental infection by interleukin-12 p40 deficient mice. Mem Inst Oswaldo Cruz 99 (2004) 289-294
30. Laurenti M.D., da Matta V.L., Pernichelli T., Secundino N.F., Pinto L.C., Corbett C.E., et al. Effects of salivary gland homogenate from wild-caught and laboratory-reared Lutzomyia longipalpis on the evolution and immunomodulation of Leishmania (Leishmania) amazonensis infection. Scand J Immunol 70 (2009) 389-395
31. Guevara-Mendoza O., Une C., Franceschi Carreira P., and Orn A. Experimental infection of Balb/c mice with Leishmania panamensis and Leishmania mexicana: induction of early IFN-gamma but not IL-4 is associated with the development of cutaneous lesions. Scand J Immunol 46 (1997) 35-40
32. Jones D.E., Buxbaum L.U., and Scott P. IL-4-independent inhibition of IL-12 responsiveness during Leishmania amazonensis infection. J Immunol 165 (2000) 364-372
33. Kane M.M., and Mosser D.M. The role of IL10 in promoting disease progression in leishmaniasis. J Immunol 166 (2001) 1141-1147
34. Ghalib H.W., Piuvezam M.R., Skeiky Y.A., Siddig M., Hashim F.A., el-Hassan A.M., et al. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 92 (1993) 324-329
35. Stenger S., Thüring H., Röllinghoff M., and Bogdan C. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J Exp Med 180 (1994) 783-793
36. Liew F.Y., Li Y., and Millott S. Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J Immunol 145 (1990) 4306-4310
37. Alves C.F., de Amorim I.F., Moura E.P., Ribeiro R.R., Alves C.F., Michalick M.S., et al. 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 128 (2009) 349-358
38. Dobrzanski M.J., Reome J.B., Hollenbaugh J.A., and Dutton R.W. Tc1 and Tc2 effector cell therapy elicit long-term tumor immunity by contrasting mechanisms that result in complementary endogenous type 1 antitumor responses. J Immunol 172 (2004) 1380-1390
39. Norsworthy N.B., Sun J., Elnaiem D., Lanzaro G., and Soong L. Sand fly saliva enhances Leishmania amazonensis infection by modulating interleukin-10 production. Infect Immun 72 (2004) 1240-1247
40. Charmoy M., Megnekou R., Allenbach C., Zweifel C., Perez C., Monnat K., et al. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 82 (2007) 288-299
41. Taylor A.W. Review of the activation of TGF-beta in immunity. J Leukoc Biol 85 (2009) 29-33
42. Magerus-Chatinet A., Stolzenberg M.C., Loffredo M.S., Neven B., Schaffner C., Ducrot N., et al. FAS-L, IL-10, and double-negative CD4- CD8- TCR alpha/beta + T cells are reliable markers of autoimmune lymphoproliferative syndrome (ALPS) associated with FAS loss of function. Blood 113 (2009) 3027-3030
43. Antonelli L.R., Dutra W.O., Oliveira R.R., Torres K.C., Guimarães L.H., Bacellar O., et al. Disparate immunoregulatory potentials for double-negative (CD4- CD8-) alpha beta and gamma delta T cells from human patients with cutaneous leishmaniasis. Infect Immun 74 (2006) 6317-6323
44. Gollob K.J., Antonelli L.R., Faria D.R., Keesen T.S., and Dutra W.O. Immunoregulatory mechanisms and CD4-CD8- (double negative) T cell subpopulations in human cutaneous leishmaniasis: a balancing act between protection and pathology. Int Immunopharmacol 8 (2008) 1338-1343
45. Salhi A., VJr R., Santoro F., Dessein H., Romano A., Castellano L.R., et al. Immunological and genetic evidence for a crucial role of IL-10 in cutaneous lesions in humans infected with Leishmania braziliensis. J Immunol 180 (2008) 6139-6148
46. Padigel U.M., Alexander J., and Farrell J.P. The role of interleukin-10 in susceptibility of BALB/c mice to infection with Leishmania mexicana and Leishmania amazonensis. J Immunol 171 (2003) 3705-3710
47. Garcez L.M., Silveira F.T., el Harith A., Lainson R., and Shaw J.J. Experimental cutaneous leishmaniasis. IV. The humoral response of Cebus apella (Primates: Cebidae) to infections of Leishmania (Leishmania) amazonensis, L. (Viannia) lainsoni and L. (V.) braziliensis using the direct agglutination test. Acta Trop 68 (1997) 65-76
48. Coffman R.L., Lebman D.A., and Rothman P. Mechanism and regulation of immunoglobulin isotype switching. Adv Immunol 54 (1993) 229-270
49. Lebrun P., Lucas A.H., McKenzie D.T., and Spiegelberg H.L. Interleukin 4 acts on both high- and low-density murine B cell subpopulations to induce IgE and IgG1 synthesis in vitro. Int Arch Allergy Appl Immunol 88 (1989) 108-110
50. Fischer K., Collins H., Taniguchi M., Kaufmann S.H., and Schaible U.E. IL-4 and T cells are required for the generation of IgG1 isotype antibodies against cardiolipin. J Immunol 168 (2002) 2689-2694
51. Guo L., Hu-Li J., and Paul W.E. Probabilistic regulation of IL-4 production. J Clin Immunol 25 (2005) 573-581