Dynamics of immune granuloma formation in a Leishmania braziliensis-induced self-limiting cutaneous infection in the primate Macaca mulatta

Journal of Pathology

Volumn 216, Issue 3, 2008, Pages 375-386

  Souza Lemos, C ^a   De Campos, S N ^a   Teva, A ^a   Corte Real S ^a   Fonseca, E C ^b   Porrozzi, R ^a   Grimaldi Jr , G ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Cutaneous infection; Human like granulomatous response; Leishmania braziliensis; Primate model

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL TYPE; CONTROLLED STUDY; GRANULOMA; HELPER CELL; LEISHMANIA BRAZILIENSIS; MACACA; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SKIN DEFECT; SKIN LEISHMANIASIS; SKIN ULCER; T LYMPHOCYTE; ULCER HEALING;

EID: 55249088316     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2403     Document Type: Article

References (41)

1. Grimaldi G Jr, Tesh RB. Leishmaniasis of the New World: current concepts and implications for future research. Clin Microbiol Rev 1993;6:230-250.
2. Turetz ML, Machado PR, Ko AI, Alves F, Bittencourt A, Almeida RP, et al. Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis 2002;186:1829-1834.
3. McConville MJ, Handman E. The molecular basis of Leishmania pathogenesis. Int J Parasitol 2007;37:1047-1051.
4. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nature Genet 2007;39:839-847.
5. Vanloubbeeck Y, Jones DE. The immunology of Leishmania infection and the implications for vaccine development. Ann N Y Acad Sci 2004;1026:267-272.
6. Teixeira MJ, Teixeira CR, Andrade BB, Barral-Neto M, Barral A. Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol 2006;22:32-38.
7. Gaze ST, Dutra WO, Lessa H, Guimarães LH, de Jesus AR, Carvalho LP, et al. Mucosal leishmaniasis patients display an activated inflammatory T-cell phenotype associated with a nonbalanced monocyte population. Scand J Immunol 2006;63:70-78.
8. Carvalho LP, Passos S, Bacellar O, Lessa M, Almeida RP, Magalhães A, et al. Differential immune regulation of activated T cells between cutaneous and mucosal leishmaniasis as a model for pathogenesis. Parasite Immunol 2007;29:251-258.
9. + T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J Infect Dis 2006;193:1313-1322.
10. Antonelli LRV, Dutra WO, Oliveira RR, Torres KCL, Guimarães LH, 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 2006;74:6317- 6323.
11. Anderson CF, Oukka M, Kuchroo VJ, Sacks DL. CD4 + CD25 - Foxp3- Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med 2007;204:285-297.
12. Pirmez C, Cooper C, Paes-Oliveira M, Schubach A, Torigian VK, Modlin RL. Immunologic responsiveness in American cutaneous leishmaniasis lesions. J Immunol 1990;145:3100-3104.
13. Murray HW. Tissue granuloma structure-function in experimental visceral leishmaniasis. Int J Exp Pathol 2001;82:249-267.
14. Stanley AC, Engwerda CR. Balancing immunity and pathology in visceral leishmaniasis. Immunol Cell Biol 2007;85:138-147.
15. Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, et al. Rhesus macaque genome sequencing and analysis consortium. Evolutionary and biomedical insights from the rhesus macaque genome. Science 2007;316:222-234.
16. Amaral VF, Ransatto VAO, Conceição-Silva F, Molinaro E, Ferreira V, Coutinho SG, et al. The Asian rhesus macaques (Macaca mulatta) as an experimental model for study of cutaneous leishmaniasis. Exp Parasitol 1996;82:34-44.
17. Amaral VF, Teva A, Porrozzi R, Silva AJ, Pereira MS, Grimaldi G Jr. Leishmania (Leishmania) major-infected rhesus macaques (Macaca mulatta) develop varying levels of resistance against homologous reinfections. Mem Inst Oswaldo Cruz 2001;96:795-804.
18. Teva A, Porrozzi R, Cupolillo E, Pirmez C, Oliveira-Neto MP, Grimaldi G Jr. Leishmania (Viannia) braziliensis induced chronic granulomatous cutaneous lesions affecting the nasal mucosa in the rhesus monkey (Macaca mulatta) model. Parasitology 2003;127:437-447.
19. Porrozzi R, Pereira MS, Teva A, Volpini AC, Pinto MA, Marchevsky RS, et al. Leishmania infantum-induced primary and challenge infections in rhesus monkeys (Macaca mulatta): a primate model for visceral leishmaniasis. Trans R Soc Trop Med Hyg 2006;100:926-937.
20. Pahar B, Li J, Rourke T, Miller CJ, McChesney MB. Detection of antigen-specific T cell interferon-ã expression by ELISPOT and cytokine flow cytometry assays in rhesus macaques. J Immunol Methods 2003;282:103-115.
21. Giavedoni LD. Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J Immunol Methods 2005;301:89-101.
22. Andrade MCR, Penedo MCT, Ward T, Silva VF, Bertolini LR, Roberts JA, et al. Determination of genetic status in a closed colony of rhesus monkeys (Macaca mulatta). Primates 2004;45:183-186.
23. Grimaldi G Jr, Soares MJ, Moriearty PL. Tissue eosinophilia and Leishmania mexicana mexicana eosinophil interactions in murine cutaneous leishmaniasis. Parasite Immunol 1984;6:397-408.
24. Silva Francisco J, Moraes HP, Dias EP. Evaluation of the Image-Pro Plus 4.5 software for automatic counting of labeled nucleic by PCNA immunohistochemistry. Braz Oral Res 2004;18:100-104.
25. Wells WA, Rainer RO, Memoli VA. Equipment, standardization and application of image processing. Am J Clin Pathol 1993;99:48-56.
26. Bottrel RLA, Dutra WO, Martins FA, Gontijo B, Carvalho E, Barral-Neto M, et al. Flow cytometry determination of cellular sources and frequencies of key-cytokine-producing lymphocytes directed against recombinant LACK and soluble Leishmania antigen in human cutaneous leishmaniasis. Infect Immun 2001;69:3232-3239.
27. Lainson R, Shaw JJ. Leishmaniasis in Brazil: XII. Observations on cross-immunity in monkeys and man infected with Leishmania mexicana mexicana, L. m. amazonensis, L. braziliensis braziliensis, L. b. guyanensis and L. b. panamensis. J Trop Med Hyg 1977;80:29-35.
28. Cuba Cuba CA, Ferreira V, Bampi M, Magalhães A, Marsden PD, Vexenat A, et al. Experimental infection with Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the marmoset, Callithrix penicillata (primates: callithricidae). Mem Inst Oswaldo Cruz 1990;85:459-467.
29. Lima GMAC, Vallochi AL, Silva UR, Bevilacqua EMAF, Kiffer MMF, Abrahamsohn IA. The role of polymorphonuclear leukocytes in the resistance to cutaneous leishmaniasis. Immunol Lett 1998;64:145-151.
30. Laufs H, Müller K, Fleischer J, Reiling N, Jahnke N, Jensenius JC, et al. Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors. Infect Immun 2002;70:826-835.
31. van Zandbergen GM, Hermann N, Laufs H, Solbach W, Laskay T. Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes. Infect Immun 2002;70:4177- 4184.
32. van Zandbergen GM, Klinger M, Mueller A, Dannenberg S, Gebert A, Solbach W, et al. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 2004;173:6521- 6525.
33. Meagher LC, Savill JS, Baker A, Fuller RW, Haslett C. Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2. J Leukoc Biol 1992;52:269-273.
34. Von Stebut E. Immunology of cutaneous leishmaniasis: the role of mast cells, phagocytes and dendritic cells for protective immunity. Eur J Dermatol 2007;17:115-122.
35. Ritter U, Moll H, Laskay T, Bröcker E, Velazco O, Becker I, et al. Differential expression of chemokines in patients with localized and diffuse cutaneous American leishmaniasis. J Infect Dis 1996;173:699-709.
36. Barral A, Jesus AR, Almeida RP, Carvalho EM, Barral-Neto M, Costa JM, et al. Evaluation of T-cell subsets in the lesion infiltrates of human cutaneous and mucocutaneous leishmaniasis. Parasite Immunol 1987;9:487-497.
37. Lima HC, Vasconcelos AW, David JR, Lerner EA. American cutaneous leishmaniasis: in situ characterization of the cellular immune response with time. Am J Trop Med Hyg 1994;50:743-747.
38. Modlin RL, Tapia FJ, Bloom BR, Gallinoto ME, Castes M, Rondon AJ, et al. In situ characterization of the cellular immune response in American cutaneous leishmaniasis. Clin Exp Immunol 1985;60:241-248.
39. Pirmez C, Yamamura M, Uyemura K, Paes-Oliveira M, Conceição- Silva F, Modlin RL. Cytokine patterns in the pathogenesis of human leishmaniasis. J Clin Invest 1993;91:1390-1395.
40. Vieira MG, Oliveira F, Arruda S, Bittencourt AL, Barbosa AA Jr, Barral-Neto M, et al. B-cell infiltration and frequency of cytokine producing cells differ between localized and disseminated human cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 2002;97:979-983.
41. Da-Cruz AM, Bittar R, Mattos M, Oliveira-Neto M, Noguira R, Pinho-Ribeiro V, et al. T-cell-mediated immune responses in patients with cutaneous or mucosal leishmaniasis: long-term evaluation after therapy. Clin Diagn Lab Immunol 2005;9:251-256.