Efficient phagosomal maturation and degradation of Plasmodium-infected erythrocytes by dendritic cells and macrophages

Parasite Immunology

Volumn 32, Issue 6, 2010, Pages 389-398

  Bettiol, E ^a   Van De Hoef, D L ^a   Carapau, D ^a   Rodriguez, A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acidification; Dendritic cell; Lamp 1; Macrophage; MHC II; Phagosomal degradation; Plasmodium

Indexed keywords

GREEN FLUORESCENT PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; ERYTHROCYTE; FLUORESCENCE ANALYSIS; INTERNALIZATION; MACROPHAGE; MALARIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PLASMODIUM YOELII; PRIORITY JOURNAL;

ANIMALS; DENDRITIC CELLS; ERYTHROCYTES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYDROGEN-ION CONCENTRATION; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MACROPHAGES; MICE; MICROBIAL VIABILITY; PHAGOSOMES; PLASMODIUM YOELII;

PLASMODIUM PARASITES; PLASMODIUM YOELII;

EID: 77952249404     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2010.01198.x     Document Type: Article

References (36)

1. Hviid L. Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop 2005 95 : 270 275.
2. Plebanski M Hill AV. The immunology of malaria infection. Curr Opin Immunol 2000 12 : 437 441.
3. Freitas do Rosario AP, Muxel SM, Rodriguez-Malaga SM, et al. Gradual decline in malaria-specific memory T cell responses leads to failure to maintain long-term protective immunity to Plasmodium chabaudi AS despite persistence of B cell memory and circulating antibody. J Immunol 2008 181 : 8344 8355.
4. Walther M, Tongren JE, Andrews L, et al. Upregulation of TGF-beta, FOXP3, and CD4 + CD25 + regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 2005 23 : 287 296.
5. Wong KA Rodriguez A. Plasmodium infection and endotoxic shock induce the expansion of regulatory dendritic cells. J Immunol 2008 180 : 716 726.
6. Wykes MN Good MF. What really happens to dendritic cells during malaria? Nat Rev Microbiol 2008 6 : 864 870.
7. Leitner WW Krzych U. Plasmodium falciparum malaria blood stage parasites preferentially inhibit macrophages with high phagocytic activity. Parasite Immunol 1997 19 : 103 110.
8. Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 1992 176 : 1033 1041.
9. Blander JM Medzhitov R. On regulation of phagosome maturation and antigen presentation. Nat Immunol 2006 7 : 1029 1035.
10. McGilvray ID, Serghides L, Kapus A, Rotstein OD Kain KC. Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 2000 96 : 3231 3240.
11. Ing R, Segura M, Thawani N, Tam M Stevenson MM. Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation. J Immunol 2006 176 : 441 450.
12. Olliaro P, Lombardi L, Frigerio S, Basilico N, Taramelli D Monti D. Phagocytosis of hemozoin (native and synthetic malaria pigment), and Plasmodium falciparum intraerythrocyte-stage parasites by human and mouse phagocytes. Ultrastruct Pathol 2000 24 : 9 13.
13. Ono T, Tadakuma T Rodriguez A. Plasmodium yoelii yoelii 17XNL constitutively expressing GFP throughout the life cycle. Exp Parasitol 2007 115 : 310 313.
14. Winzler C, Rovere P, Rescigno M, et al. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med 1997 185 : 317 328.
15. Stockinger B, Zal T, Zal A Gray D. B cells solicit their own help from T cells. J Exp Med 1996 183 : 891 899.
16. Steinberg BE, Huynh KK Grinstein S. Phagosomal acidification: measurement, manipulation and functional consequences. Biochem Soc Trans 2007 35 (Pt 5 1083 1087.
17. Guermonprez P, Valladeau J, Zitvogel L, Thery C Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol 2002 20 : 621 667.
18. Savina A, Jancic C, Hugues S, et al. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006 126 : 205 218.
19. Millington OR, Di Lorenzo C, Phillips RS, Garside P Brewer JM. Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J Biol 2006 5 : 5.
20. Ocana-Morgner C, Mota MM Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 2003 197 : 143 151.
21. Urban BC, Ferguson DJ, Pain A, et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999 400 : 73 77.
22. Stevenson MM Riley EM. Innate immunity to malaria. Nat Rev Immunol 2004 4 : 169 180.
23. Artavanis-Tsakonas K, Love JC, Ploegh HL Vyas JM. Recruitment of CD63 to Cryptococcus neoformans phagosomes requires acidification. Proc Natl Acad Sci USA 2006 103 : 15945 15950.
24. Ramachandra L, Noss E, Boom WH Harding CV. Phagocytic processing of antigens for presentation by class II major histocompatibility complex molecules. Cell Microbiol 1999 1 : 205 214.
25. Lang F, Lang PA, Lang KS, et al. Channel-induced apoptosis of infected host cells-the case of malaria. Pflugers Arch 2004 448 : 319 324.
26. Arese P, Turrini F Ginsburg H. Erythrophagocytosis in malaria: host defence or menace to the macrophage? Parasitol Today 1991 7 : 25 28.
27. Arese P, Turrini F, Bussolino F, et al. Recognition signals for phagocytic removal of favic, malaria-infected and sickled erythrocytes. Adv Exp Med Biol 1991 307 : 317 327.
28. Schwarzer E, Bellomo G, Giribaldi G, Ulliers D Arese P. Phagocytosis of malarial pigment haemozoin by human monocytes: a confocal microscopy study. Parasitology 2001 123 (Pt 2 125 131.
29. Schwarzer E, De Matteis F, Giribaldi G, Ulliers D, Valente E Arese P. Hemozoin stability and dormant induction of heme oxygenase in hemozoin-fed human monocytes. Mol Biochem Parasitol 1999 100 : 61 72.
30. Schwarzer E, Alessio M, Ulliers D Arese P. Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 1998 66 : 1601 1606.
31. Scorza T, Magez S, Brys L De Baetselier P. Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol 1999 21 : 545 554.
32. Diou J, Gauthier S, Tardif MR, Fromentin R, Lodge R Sullivan DJ Jr., et al. Ingestion of the malaria pigment hemozoin renders human macrophages less permissive to HIV-1 infection. Virology 2009 395 : 56 66.
33. Noland GS, Briones N Sullivan DJ Jr. The shape and size of hemozoin crystals distinguishes diverse Plasmodium species. Mol Biochem Parasitol 2003 130 : 91 99.
34. Sponaas AM, Cadman ET, Voisine C, et al. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J Exp Med 2006 203 : 1427 1433.
35. Ocana-Morgner C, Wong KA Rodriguez A. Interactions between dendritic cells and CD4 + T cells during Plasmodium infection. Malar J 2008 7 : 88.
36. Millington OR, Gibson VB, Rush CM, et al. Malaria impairs T cell clustering and immune priming despite normal signal 1 from dendritic cells. PLoS Pathog 2007 3 : 1380 1387.