Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L) amazonensis in mammalian hosts

Journal of Immunology

Volumn 176, Issue 3, 2006, Pages 1834-1839

  Wanderley, João L M ^a,b   Moreira, Maria E C ^a   Benjamin, Aline ^a,b   Bonomo, Adrians C ^a,b   Barcinski, Marcello A ^a,c  

^a INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; PHOSPHATIDYLSERINE; PROPIDIUM IODIDE; THIOGLYCOLIC ACID; TRANSFORMING GROWTH FACTOR BETA1;

ADOLESCENT; AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LEISHMANIA; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PARASITE VIRULENCE; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 31144454859     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.3.1834     Document Type: Article

References (37)

1. Sacks, D., and A. Sher. 2002. Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 3: 1041-1047.
2. Spath, G. F., L. A. Garraway, S. J. Turco, and S. M. Beverley. 2003. The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc. Natl. Acad. Sci. USA 100: 9536-9541.
3. Proudfoot, L., A. V. Nikolaev, G. J. Feng, W. Q. Wei, M. A. Ferguson, J. S. Brimacombe, and F. Y. Liew. 1996. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA 93: 10984-10989.
4. Descoteaux, A., S. J. Turco, D. L. Sacks, and G. Matlashewski. 1991. Leishmania donovani lipophosphoglycan selectively inhibits signal transduction in macrophages. J. Immunol. 146: 2747-2753.
5. Sorensen, A. L., A. S. Hey, and A. Kharazmi. 1994. Leishmania major surface protease Gp63 interferes with the function of human monocytes and neutrophils in vitro. APMIS 102: 265-271.
6. Balanco, J. M. F., M. E. C. Moreira, A. Bonomo, P. T. Bozza, G. Amarante-Mendes, C. Pirmez, and M. A. Barcinski. 2001. Apoptotic mimicry by an obligate intracellular parasite downregulates macrophage microbicidal activity. Curr. Biol. 11: 1870-1873.
7. Hoffmann, P., A. M. deCathelineau, C. A. Ogden, Y. Leverrier, D. L. Bratton, D. L. Daleke, A. J. Ridley, V. A. Fadok, and P. M. Henson. 2001. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J. Cell Biol. 155: 649-659.
8. Saraiva, E. M. B., P. F. P. Pimenta, M. E. A. Pereira, and W. Souza. 1983. Isolation and purification of amastigotes of Leishmania mexicana amazonensis by a gradient of metrizamide. J. Parasitol. 89: 627-629.
9. Dominguez, M., and A. Torano. 1999. Immune adherence-mediated opsonophagocytosis: the mechanism of Leishmania infection. J. Exp. Med. 189: 25-35.
10. Swanson, J. A. 1989. Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J. Cell Sci. 94: 135-142.
11. Swanson, J. A., and C. Watts. 1995. Macropinocytosis. Trends Cell Biol. 5: 424-424.
12. Dowrick, P., P. Kenworthy, B. McCann, and R. Warn. 1993. Circular ruffle formation and closure lead to macropinocytosis in hepatocyte growth factor/scatter factor-treated cells. Eur. J. Cell Biol. 61: 44-53.
13. 2, and PAF. J. Clin. Invest. 101: 890-898.
14. Hoffmann, P. R., J. A. Kench, A. Vondracek, E. Kruk, D. L. Daleke, M. Jordan, P. Marrack, P. M. Henson, and V. A. Fadok. 2005. Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J. Immunol. 174: 1393-1404.
15. Barral-Netto, M., A. Barral, C. E. Brownell, Y. A. Skeiky, L. R. Ellingsworth, D. R. Twardzik, and S. G. Reed. 1992. Transforming growth factor-β in leishmanial infection: a parasite escape mechanism. Science 257: 545-548.
16. Murray, H. W., C. M. Lu, S. Mauze, S. Freeman, A. L. Moreira, G. Kaplan, and R. L. Coffman. 2002. Interleukin-10 (IL10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy Infect. Immun. 70: 6284-6293.
17. Chatelain, R., S. Mauze, and R. L. Coffman. 1999. Experimental Leishmania major infection in mice: role of IL-10. Parasite Immunol. 21: 211-218.
18. 1. J. Immunol. 146: 1849-1857.
19. 3). J. Immunol. 161: 6250-6257.
20. Fadok, V., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148: 2207-2216.
21. Tripathi, A., and C. M. Gupta. 2003. Transbilayer translocation of membrane phosphatidylserine and its role in macrophage invasion in Leishmania promastigotes. Mol. Biochem. Parasitol. 128: 1-9.
22. Noben-Trauth, N., W. E. Paul, and D. L. Sacks. IL-4- and IL-4 receptor-deficient BALB/c mice reveal differences in susceptibility to Leishmania major parasite substrains. 1999. J. Immunol. 162: 6132-6140.
23. Iniesta, V., L. C. Gomez-Nieto, I. Molano, A. Mohedano, J. Carcelen, C. Miron, C. Alonso, and I. Corraliza. 2002. Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol. 24: 113-118.
24. Munder, M., K. Eichmann, J. M. Moran, F. Centeno, G. Soler, and M. Modolell. 1999. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163: 3771-3377.
25. Bratton, D. L., V. A. Fadok, D. A. Richter, J. M. Kailey, S. C. Frasch, T. Nakamura, and P. M. Henson. 1999. Polyamine regulation of plasma membrane phospholipid flip-flop during apoptosis. J. Biol. Chem. 274: 28113-28120.
26. Mills, C. D., K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164: 6166-6173.
27. Ravetch, J. V., and J. P. Kinet. 1991. Fc receptors. Annu. Rev. Immunol. 9: 457-492.
28. Lefeber, D. J., B. Benaissa-Trouw, J. F. Vliegenthart, J. P. Kamerling, W. T. Jansen, K. Kraaijeveld, and H. Snippe, H. 2003. Th1-directing adjuvants increase the immunogenicity of oligosaccharide-protein conjugate vaccines related to Streptococcus pneumoniae type 3. Infect. Immun. 71: 6915-6920.
29. Ji, J., J. Sun, H. Qi, and L. Soong. 2002. Analysis of T helper cell responses during infection with Leishmania amazonensis. Am. J. Trop. Med. Hyg. 66: 338-345.
30. Doherty, T. M., R. A. Seder, and A. Sher. 1996. Induction and regulation of IL-15 expression in murine macrophages. J. Immunol. 156: 735-741.
31. Padigel, U. M., and J. P. Farrell. 2005. Control of infection with Leishmania major in susceptible BALB/c mice lacking the common γ-chain for FcR is associated with reduced production of IL-10 and TGF-β by parasitized cells. J. Immunol. 174: 6340-6345.
32. Kim, S., K. B. Elkon, and X. Ma. 2004. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 21: 643-653.
33. Heinzel, F. P., D. S. Schoenhaut, R. M. Rerko, L. E. Rosser, and M. K. Gately. 1993. Recombinant IL-12 cures mice infected with Leishmania major. J. Exp. Med. 77: 1505-1509
34. Von Stebut, E., Y. Belkaid, T. Jakob, D. Sacks, and M. Udey. 1998. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-leishmania immunity. J. Exp. Med. 188: 1547-1552.
35. Chen, X., K. Doffek, S. L. Sugg, and J. Shilyansky. 2004. Phosphatidylserine regulates the maturation of human dendritic cells. J. Immunol. 173: 2985-2994.
36. van der Kleij, D., E. Latz, J. F. Brouwers, Y. C. Kruize, M. Schmitz, E. A. Kurt-Jones, T. Espevik, E. C. de Jong, M. L. Kapsenberg, D. T. Golenbock, et al. 2002. A novel host-parasite lipid cross-talk: schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277: 48122-48129.
37. Seabra, S. H., W. de Souza, and R. A. Damatta. 2004. Toxoplasma gondii exposes phosphatidylserine inducing a TGF-β1 autocrine effect orchestrating macrophage evasion. Biochem. Biophys. Res. Commun. 324: 744-752.