Dendritic cells and their multiple roles during malaria infection

Journal of Immunology Research

Volumn 2016, Issue , 2016, Pages

  Amorim, Kelly N S ^a   Chagas, Daniele C G ^a   Sulczewski, Fernando B ^a   Boscardin, Silvia B ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b National Institute of Science and Technology in Tropical Diseases   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD45 ANTIGEN; CD8ALPHA ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 6; LECTIN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; PATTERN RECOGNITION RECEPTOR; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; APOPTOSIS; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL ADHESION; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; GAMETOCYTE; IMMUNOLOGICAL MEMORY; IMMUNOREGULATION; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALARIA; MALARIA FALCIPARUM; MORBIDITY; MORTALITY; MYELOID DENDRITIC CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGICAL PROCEDURES; IMMUNOLOGY; LIFE CYCLE STAGE; PARASITOLOGY; PLASMODIUM;

ANTIGEN PRESENTATION; DENDRITIC CELLS; HUMANS; IMMUNOLOGIC TESTS; LIFE CYCLE STAGES; MALARIA; PLASMODIUM; T-LYMPHOCYTES;

EID: 84964798647     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2016/2926436     Document Type: Review

References (126)

1. M. C. Nussenzweig and R. M. Steinman, "Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction, " Journal of Experimental Medicine, vol. 151, no. 5, pp. 1196-1212, 1980.
2. D. T. Avery, S. L. Kalled, J. I. Ellyard et al., "BAFF selectively enhances the survival of plasmablasts generated from human memory B cells, " Journal of Clinical Investigation, vol. 112, no. 2, pp. 286-297, 2003.
3. G. Ferlazzo, M. L. Tsang, L. Moretta, G. Melioli, R. M. Steinman, and C. Munz, "Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells, " Journal of Experimental Medicine, vol. 195, no. 3, pp. 343-351, 2002.
4. F. Gerosa, A. Gobbi, P. Zorzi et al., "The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions, " The Journal of Immunology, vol. 174, no. 2, pp. 727-734, 2005.
5. C. Reis e Sousa, "Dendritic cells in amature age, " Nature Reviews Immunology, vol. 6, no. 6, pp. 476-483, 2006.
6. T. Brocker, M. Riedinger, and K. Karjalainen, "Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo, " Journal of Experimental Medicine, vol. 185, no. 3, pp. 541-550, 1997.
7. R. M. Steinman and M. C. Nussenzweig, "Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance, " Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 1, pp. 351-358, 2002.
8. A. Iwasaki and R. Medzhitov, "Control of adaptive immunity by the innate immune system, " Nature Immunology, vol. 16, no. 4, pp. 343-353, 2015.
9. T. Kawai and S. Akira, "The role of pattern-recognition receptors in innate immunity: update on toll-like receptors, " Nature Immunology, vol. 11, no. 5, pp. 373-384, 2010.
10. J. C. Hoving, G. J. Wilson, and G. D. Brown, "SignallingC-type lectin receptors, microbial recognition and immunity, " Cellular Microbiology, vol. 16, no. 2, pp. 185-194, 2014.
11. V. A. K. Rathinam, S. K. Vanaja, and K. A. Fitzgerald, "Regulation of inflammasome signaling, " Nature Immunology, vol. 13, no. 4, pp. 333-342, 2012.
12. J. Wu and Z. J. Chen, "Innate immune sensing and signaling of cytosolic nucleic acids, " Annual Review of Immunology, vol. 32, pp. 461-488, 2014.
13. B. Lemaitre, E. Nicolas, L. Michaut, J.-M. Reichhart, and J. A. Hoffmann, "The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults, " Cell, vol. 86, no. 6, pp. 973-983, 1996.
14. R. Luger, S. Valookaran, N. Knapp, C. Vizzardelli, A. M. Dohnal, and T. Felzmann, "Toll-like receptor 4 engagement drives differentiation of human and murine dendritic cells from a pro- into an anti-inflammatory mode, " PLoS ONE, vol. 8, no. 2, Article ID e54879, pp. 1-13, 2013.
15. M. Merad, P. Sathe, J. Helft, J. Miller, and A. Mortha, "The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting, " Annual Review of Immunology, vol. 31, pp. 563-604, 2013.
16. F. Ginhoux and M. Merad, "Ontogeny and homeostasis of Langerhans cells, " Immunology and Cell Biology, vol. 88, no. 4, pp. 387-392, 2010.
17. G. T. Belz, K. Shortman, M. J. Bevan, and W. R. Heath, "CD8α+ dendritic cells selectively presentMHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo, " Journal of Immunology, vol. 175, no. 1, pp. 196-200, 2005.
18. J. M. M. den Haan, S. M. Lehar, and M. J. Bevan, "CD8+ but not CD8- dendritic cells cross-prime cytotoxic T cells in vivo, " Journal of ExperimentalMedicine, vol. 192, no. 12, pp. 1685-1695, 2000.
19. T.-P. VuManh, N. Bertho, A. Hosmalin, I. Schwartz-Cornil, and M. Dalod, "Investigating evolutionary conservation of dendritic cell subset identity and functions, " Frontiers in Immunology, vol. 6, article 260, 2015.
20. K. Liu and M. C. Nussenzweig, "Origin and development of dendritic cells, " Immunological Reviews, vol. 234, no. 1, pp. 45-54, 2010.
21. B. T. Edelson, K. C. Wumesh, R. Juang et al., "Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8α + conventional dendritic cells, " The Journal of Experimental Medicine, vol. 207, no. 4, pp. 823-836, 2010.
22. H. Nakano, M. Yanagita, and M. D. Gunn, "CD11c+B220+Gr-1+ cells inmouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells, " Journal of ExperimentalMedicine, vol. 194, no. 8, pp. 1171-1178, 2001.
23. C. Asselin-Paturel, A. Boonstra, M. Dalod et al., "Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology, " Nature Immunology, vol. 2, no. 12, pp. 1144-1150, 2001.
24. M. O'Keeffe, H. Hochrein, D. Vremec et al., "Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8- dendritic cells only after microbial stimulus, " Journal of ExperimentalMedicine, vol. 196, no. 10, pp. 1307-1319, 2002.
25. G. Schlecht, S. Garcia, N. Escriou, A. A. Freitas, C. Leclerc, and G. Dadaglio, "Murine plasmacytoid dendritic cells induce effector/memory CD8+ T-cell responses in vivo after viral stimulation, " Blood, vol. 104, no. 6, pp. 1808-1815, 2004.
26. J. A. Villadangos and L. Young, "Antigen-presentation properties of plasmacytoid dendritic cells, " Immunity, vol. 29, no. 3, pp. 352-361, 2008.
27. U. O'Doherty, M. Peng, S. Gezelter et al., "Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature, " Immunology, vol. 82, no. 3, pp. 487-493, 1994.
28. A. Dzionek, A. Fuchs, P. Schmidt et al., "BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood, " The Journal of Immunology, vol. 165, no. 11, pp. 6037-6046, 2000.
29. B. Reizis, A. Bunin, H. S. Ghosh, K. L. Lewis, and V. Sisirak, "Plasmacytoid dendritic cells: recent progress and open questions, " Annual Review of Immunology, vol. 29, pp. 163-183, 2011.
30. F. O. Nestle, X.-G. Zheng, C. B. Thompson, L. A. Turka, and B. J. Nickoloff, "Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets, " The Journal of Immunology, vol. 151, no. 11, pp. 6535-6545, 1993.
31. A. Boltjes and F. van Wijk, "Human dendritic cell functional specialization in steady-state and inflammation, " Frontiers in Immunology, vol. 5, article 131, 2014.
32. WHO, "World malaria report 2014, " WHO Report, World Health Organization, 2014.
33. R. Amino, S. Thiberge, B. Martin et al., "Quantitative imaging of Plasmodium transmission from mosquito to mammal, " Nature Medicine, vol. 12, no. 2, pp. 220-224, 2006.
34. L. M. Yamauchi Lucy, A. Coppi, G. Snounou, and P. Sinnis, "Plasmodium sporozoites trickle out of the injection site, " Cellular Microbiology, vol. 9, no. 5, pp. 1215-1222, 2007.
35. M. M. Mota, G. Pradel, J. P. Vanderberg et al., "Migration of Plasmodium sporozoites through cells before infection, " Science, vol. 291, no. 5501, pp. 141-144, 2001.
36. A. Sturm, R. Amino, C. van de Sand et al., "Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids, " Science, vol. 313, no. 5791, pp. 1287-1290, 2006.
37. A. Bartoloni and L. Zammarchi, "Clinical aspects of uncomplicated and severemalaria, "Mediterranean Journal ofHematology and Infectious Diseases, vol. 4, no. 1, Article ID e2012026, 2012.
38. W. R. J. Taylor, J. Hanson, G. D. H. Turner, N. J. White, and A. M. Dondorp, "Respiratory manifestations of malaria, " Chest, vol. 142, no. 2, pp. 492-505, 2012.
39. L. H. Miller, D. I. Baruch, K. Marsh, and O. K. Doumbo, "The pathogenic basis ofmalaria, " Nature, vol. 415, no. 6872, pp. 673-679, 2002.
40. J. W. Barnwell, A. S. Asch, R. L. Nachman, M. Yamaya, M. Aikawa, and P. Ingravallo, "A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes, " The Journal of Clinical Investigation, vol. 84, no. 3, pp. 765-772, 1989.
41. A. R. Berendt, D. L. Simmons, J. Tansey, C. I. Newbold, and K. Marsh, "Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum, " Nature, vol. 341, no. 6237, pp. 57-59, 1989.
42. J. A. Rowe, A. Claessens, R. A. Corrigan, and M. Arman, "Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications, " Expert Reviews inMolecularMedicine, vol. 11, article e16, 2009.
43. P. C. Bull, B. S. Lowe, M. Kortok, C. S. Molyneux, C. I. Newbold, and K. Marsh, "Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria, " Nature Medicine, vol. 4, no. 3, pp. 358-360, 1998.
44. M. M. Stevenson and E. M. Riley, "Innate immunity to malaria, " Nature Reviews Immunology, vol. 4, no. 3, pp. 169-180, 2004.
45. J. K. Baird, T. R. Jones, E. W. Danudirgo et al., "Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria, " The American Journal of Tropical Medicine andHygiene, vol. 45, no. 1, pp. 65-76, 1991.
46. A. F. Egan, J. Morris, G. Barnish et al., "Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19-kDa C-terminal fragment of the merozoite surface antigen, PfMSP-1, " Journal of InfectiousDiseases, vol. 173, no. 3, pp. 765-769, 1996.
47. D. Webster and A. V. S. Hill, "Progress with new malaria vaccines, " Bulletin of theWorld Health Organization, vol. 81, no. 12, pp. 902-909, 2003.
48. M. N. Wykes and M. F. Good, "What really happens to dendritic cells during malaria?" Nature Reviews Microbiology, vol. 6, no. 11, pp. 864-870, 2008.
49. S.-I. Inoue, M. Niikura, S. Mineo, and F. Kobayashi, "Roles of IFN-γ and γδ T cells in protectiveimmunity against blood-stage malaria, " Frontiers in Immunology, vol. 4, article 258, 2013.
50. W. R. Weiss and C. G. Jiang, "Protective CD8+ T lymphocytes in primates immunized with malaria sporozoites, " PLoS ONE, vol. 7, no. 2, Article ID e31247, 2012.
51. W. R. Weiss, M. Sedegah, R. L. Beaudoin, L. H. Miller, and M. F. Good, "CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites, " Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 2, pp. 573-576, 1988.
52. M. Tsuji, "A retrospective evaluation of the role of T cells in the development of malaria vaccine, " Experimental Parasitology, vol. 126, no. 3, pp. 421-425, 2010.
53. B. Wizel, R. A. Houghten, K. C. Parker et al., "Irradiated sporozoite vaccine induces HLA-B8-restricted cytotoxic T lymphocyte responses against two overlapping epitopes of the Plasmodium falciparum sporozoite surface protein 2, " Journal of Experimental Medicine, vol. 182, no. 5, pp. 1435-1445, 1995.
54. N. S. Butler, N. W. Schmidt, and J. T. Harty, "Differential effector pathways regulate memory CD8 T cell immunity against Plasmodium berghei versus P. yoelii sporozoites, " The Journal of Immunology, vol. 184, no. 5, pp. 2528-2538, 2010.
55. D. Perez-Mazliah and J. Langhorne, "CD4 T-cell subsets in malaria: Th1/Th2 revisited, " Frontiers in Immunology, vol. 5, article 671, 2014.
56. J. Banchereau and R. M. Steinman, "Dendritic cells and the control of immunity, " Nature, vol. 392, no. 6673, pp. 245-252, 1998.
57. B. C. Urban, D. J. P. Ferguson, A. Pain et al., "Plasmodium falciparuminfected erythrocytes modulate the maturation of dendritic cells, " Nature, vol. 400, no. 6739, pp. 73-77, 1999.
58. S. R. Elliott, T. P. Spurck, J. M. Dodin et al., "Inhibition of dendritic cellmaturation bymalaria is dose dependent and does not require Plasmodium falciparum erythrocyte membrane protein 1, " Infection and Immunity, vol. 75, no. 7, pp. 3621-3632, 2007.
59. B. C. Urban, D. Cordery, M. J. Shafi et al., "The frequency of BDCA3-positive dendritic cells is increased in the peripheral circulation of Kenyan children with severe malaria, " Infection and Immunity, vol. 74, no. 12, pp. 6700-6706, 2006.
60. P. Guermonprez, J. Helft, C. Claser et al., "Inflammatory Flt3l is essential to mobilize dendritic cells and for T cell responses during Plasmodium infection, " Nature Medicine, vol. 19, no. 6, pp. 730-738, 2013.
61. B. C. Urban, M. J. Shafi, D. V. Cordery et al., "Frequencies of peripheral blood myeloid cells in healthy Kenyan children with alpha+ thalassemia and the sickle cell trait, " The American Journal of TropicalMedicine and Hygiene, vol. 74, no. 4, pp. 578-584, 2006.
62. R. M. Goncalves, K. C. Salmazi, B. A. N. Santos et al., "CD4+ CD25+ Foxp3+ regulatory T cells, dendritic cells, and circulating cytokines in uncomplicated malaria: do different parasite species elicit similar host responses?" Infection and Immunity, vol. 78, no. 11, pp. 4763-4772, 2010.
63. K. Jangpatarapongsa, P. Chootong, J. Sattabongkot et al., "Plasmodium vivax parasites alter the balance of myeloid and plasmacytoid dendritic cells and the induction of regulatory T cells, " European Journal of Immunology, vol. 38, no. 10, pp. 2697-2705, 2008.
64. A. Pinzon-Charry, T. Woodberry, V. Kienzle et al., "Apoptosis and dysfunction of blood dendritic cells in patients with falciparum and vivax malaria, " The Journal of Experimental Medicine, vol. 210, no. 8, pp. 1635-1646, 2013.
65. S. Kho, J. Marfurt, R. Noviyanti et al., "Preserved dendritic cell HLA-DR expression and reduced regulatory T cell activation in Asymptomatic Plasmodium falciparum and P. vivax infection, " Infection and Immunity, vol. 83, no. 8, pp. 3224-3232, 2015.
66. P. Vichchathorn, R. Jenwithisuk, S. Leelaudomlipi et al., "Induction of specificimmune responses against the Plasmodiumvivax liver-stage via in vitro activation by dendritic cells, " Parasitology International, vol. 55, no. 3, pp. 187-193, 2006.
67. O. Bruna-Romero and A. Rodriguez, "Dendritic cells can initiate protective immune responses againstmalaria, " Infection and Immunity, vol. 69, no. 8, pp. 5173-5176, 2001.
68. S. Jung, D. Unutmaz, P. Wong et al., "In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens, " Immunity, vol. 17, no. 2, pp. 211-220, 2002.
69. S. Chakravarty, I. A. Cockburn, S. Kuk, M. G. Overstreet, J. B. Sacci, and F. Zavala, "CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes, " Nature Medicine, vol. 13, no. 9, pp. 1035-1041, 2007.
70. A. J. Radtke, W. Kastenmuller, D. A. Espinosa et al., "Lymphnode resident CD8α + dendritic cells capture antigens from migratory malaria sporozoites and induce CD8+ T cell responses, " PLoS Pathogens, vol. 11, no. 2, Article ID e1004637, 2015.
71. M. Plebanski, C. M. Hannan, S. Behboudi et al., "Direct processing and presentation of antigen frommalaria sporozoites by professional antigen-presenting cells in the induction of CD8+ T-cell responses, " Immunology and Cell Biology, vol. 83, no. 3, pp. 307-312, 2005.
72. S. Behboudi, A. Moore, and A. V. S. Hill, "Splenic dendritic cell subsets prime and boost CD8 T cells and are involved in the generation of effector CD8 T cells, " Cellular Immunology, vol. 228, no. 1, pp. 15-19, 2004.
73. S. A. Murray, I. Mohar, J. L. Miller et al., "CD40 is required for protective immunity against liver stage Plasmodium infection, " Journal of Immunology, vol. 194, no. 5, pp. 2268-2279, 2015.
74. C. Ocana-Morgner, M. M. Mota, and A. Rodriguez, "Malaria blood stage suppression of liver stage immunity by dendritic cells, " The Journal of Experimental Medicine, vol. 197, no. 2, pp. 143-151, 2003.
75. J. M. Orengo, K. A. Wong, C. Ocaa-Morgner, and A. Rodriguez, "A Plasmodium yoelii soluble factor inhibits the phenotypic maturation of dendritic cells, "Malaria Journal, vol. 7, article 254, 2008.
76. N. S. Wilson, G. M. N. Behrens, R. J. Lundie et al., "Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity, " Nature Immunology, vol. 7, no. 2, pp. 165-172, 2006.
77. R. J. Lundie, T. F. de Koning-Ward, G. M. Davey et al., "Bloodstage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8α + dendritic cells, " Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 38, pp. 14509-14514, 2008.
78. J. A. Perry, A. Rush, R. J. Wilson, C. S. Olver, and A. C. Avery, "Dendritic cells frommalaria-infected mice are fully functional APC, " The Journal of Immunology, vol. 172, no. 1, pp. 475-482, 2004.
79. J. Luyendyk, O. R. Olivas, L. A. Ginger, and A. C. Avery, "Antigen-presenting cell function during Plasmodium yoelii infection, " Infection and Immunity, vol. 70, no. 6, pp. 2941-2949, 2002.
80. E. Seixas, C. Cross, S. Quin, and J. Langhorne, "Direct activation of dendritic cells by the malaria parasite, Plasmodium chabaudi chabaudi, " European Journal of Immunology, vol. 31, no. 10, pp. 2970-2978, 2001.
81. A. L. Leisewitz, K. A. Rockett, B. Gumede, M. Jones, B. Urban, and D. P. Kwiatkowski, "Response of the splenic dendritic cell population to malaria infection, " Infection and Immunity, vol. 72, no. 7, pp. 4233-4239, 2004.
82. A.-M. Sponaas, E. T. Cadman, C. Voisine et al., "Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells, " Journal of Experimental Medicine, vol. 203, no. 6, pp. 1427-1433, 2006.
83. A.-M. Sponaas, N. Belyaev, M. Falck-Hansen, A. Potocnik, and J. Langhorne, "Transient deficiency of dendritic cells results in lack of a merozoite surface protein 1-specific CD4 T cell response during peak Plasmodium chabaudi blood-stage infection, " Infection and Immunity, vol. 80, no. 12, pp. 4248-4256, 2012.
84. J. Langhorne, F. M. Ndungu, A.-M. Sponaas, and K. Marsh, "Immunity to malaria: more questions than answers, " Nature Immunology, vol. 9, no. 7, pp. 725-732, 2008.
85. C. Voisine, B. Mastelic, A.-M. Sponaas, and J. Langhorne, "Classical CD11c+ dendritic cells, not plasmacytoid dendritic cells, induce T cell responses to Plasmodium chabaudi malaria, " International Journal for Parasitology, vol. 40, no. 6, pp. 711-719, 2010.
86. K. A. Wong and A. Rodriguez, "Plasmodium infection and endotoxic shock induce the expansion of regulatory dendritic cells, " Journal of Immunology, vol. 180, no. 2, pp. 716-726, 2008.
87. R. Ing, M. Segura, N. Thawani, M. Tam, and M. M. Stevenson, "Interaction of mouse dendritic cells and malaria-infected erythrocytes: Uptake, maturation, and antigen presentation, " Journal of Immunology, vol. 176, no. 1, pp. 441-450, 2006.
88. H. Borges da Silva, R. Fonseca, A. D. A. Cassado et al., "In vivo approaches reveal a key role for DCs in CD4+ T cell activation and parasite clearance during the acute phase of experimental blood-stage malaria, " PLoS Pathogens, vol. 11, no. 2, Article ID e1004598, 2015.
89. S. deWalick, F. H. Amante, K. A. McSweeney et al., "Cutting edge: conventional dendritic cells are the critical APC required for the induction of experimental cerebralmalaria, " The Journal of Immunology, vol. 178, no. 10, pp. 6033-6037, 2007.
90. T. Tamura, K. Kimura, K. Yui, and S. Yoshida, "Reduction of conventional dendritic cells during Plasmodium infection is dependent on activation induced cell death by type I and II interferons, " Experimental Parasitology, vol. 159, pp. 127-135, 2015.
91. X. Q. Liu, K. J. Stacey, J. M. Horne-Debets et al., "Malaria infection alters the expression of B-cell activating factor resulting in diminished memory antibody responses and survival, " European Journal of Immunology, vol. 42, no. 12, pp. 3291-3301, 2012.
92. V. Ryg-Cornejo, C. Q. Nie, N. J. Bernard et al., "NK cells and conventional dendritic cells engage in reciprocal activation for the induction of inflammatory responses during Plasmodium berghei ANKA infection, " Immunobiology, vol. 218, no. 2, pp. 263-271, 2013.
93. S. Loharungsikul, M. Troye-Blomberg, P. Amoudruz et al., "Expression of Toll-like receptors on antigen-presenting cells in patients with falciparum malaria, " Acta Tropica, vol. 105, no. 1, pp. 10-15, 2008.
94. S. Pichyangkul, K. Yongvanitchit, U. Kum-Arb et al., "Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a toll-like receptor 9- dependent pathway, " Journal of Immunology, vol. 172, no. 8, pp. 4926-4933, 2004.
95. B. S. Franklin, S. O. Rodrigues, L. R. Antonelli et al., "MyD88- dependent activation of dendritic cells and CD4+ T lymphocytes mediates symptoms, but is not required for the immunological control of parasites during rodent malaria, " Microbes and Infection, vol. 9, no. 7, pp. 881-890, 2007.
96. R. T. Gazzinelli, P. Kalantari, K. A. Fitzgerald, and D. T. Golenbock, "Innate sensing of malaria parasites, " Nature Reviews Immunology, vol. 14, no. 11, pp. 744-757, 2014.
97. D. Jani, R. Nagarkatti, W. Beatty et al., "HDP-a novel heme detoxification protein from the malaria parasite, " PLoS Pathogens, vol. 4, no. 4, Article ID e1000053, 2008.
98. E. Schwarzer, M. Alessio, D. Ulliers, and P. Arese, "Phagocytosis of themalarial pigment, hemozoin, impairs expression ofmajor histocompatibility complex class II antigen, CD54, and CD11c in human monocytes, " Infection and Immunity, vol. 66, no. 4, pp. 1601-1606, 1998.
99. O. A. Skorokhod, M. Alessio, B. Mordmuller, P. Arese, and E. Schwarzer, "Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-γ-mediated effect, " Journal of Immunology, vol. 173, no. 6, pp. 4066-4074, 2004.
100. O. Skorokhod, E. Schwarzer, T. Grune, and P. Arese, "Role of 4-hydroxynonenal in the hemozoin-mediated inhibition of differentiation of human monocytes to dendritic cells induced by GM-CSF/IL-4, " BioFactors, vol. 24, no. 1-4, pp. 283-289, 2005.
101. P. Giusti, B. C. Urban, G. Frascaroli et al., "Plasmodium falciparum-infected erythrocytes and β-hematin induce partial maturation of human dendritic cells and increase their migratory ability in response to lymphoid chemokines, " Infection and Immunity, vol. 79, no. 7, pp. 2727-2736, 2011.
102. I. Bujila, E. Schwarzer, O. Skorokhod, J. M. Weidner, M. Troye-Blomberg, and A. Ostlund Farrants, "Malaria-derived hemozoin exerts earlymodulatory effects on the phenotype and maturation of human dendritic cells, " CellularMicrobiology, vol. 18, no. 3, pp. 413-423, 2016.
103. O. R. Millington, C. Di Lorenzo, R. S. Phillips, P. Garside, and J. M. Brewer, "Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoininduced failure of dendritic cell function, " Journal of Biology, vol. 5, no. 2, p. 5, 2006.
104. O. R. Millington, V. B. Gibson, C. M. Rush et al., "Malaria impairs T cell clustering and immune priming despite normal signal 1 from dendritic cells, " PLoS Pathogens, vol. 3, no. 10, pp. 1380-1387, 2007.
105. C. Coban, K. J. Ishii, D. J. Sullivan, and N. Kumar, "Purified malaria pigment (hemozoin) enhances dendritic cell maturation andmodulates the isotype of antibodies induced by a DNA vaccine, " Infection and Immunity, vol. 70, no. 7, pp. 3939-3943, 2002.
106. C. Coban, K. J. Ishii, T. Kawai et al., "Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin, " The Journal of Experimental Medicine, vol. 201, no. 1, pp. 19-25, 2005.
107. P. Parroche, F. N. Lauw, N. Goutagny et al., "Malariahemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9, " Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 6, pp. 1919-1924, 2007.
108. X. Wu, N. M. Gowda, S. Kumar, and D. C. Gowda, "Protein- DNA complex is the exclusivemalaria parasite component that activates dendritic cells and triggers innate immune responses, " Journal of Immunology, vol. 184, no. 8, pp. 4338-4348, 2010.
109. M. T. Shio, S. C. Eisenbarth, M. Savaria et al., "Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases, " PLoS Pathogens, vol. 5, no. 8, Article ID e1000559, 2009.
110. C. Dostert, G. Guarda, J. F. Romero et al., "Malarial hemozoin is a Nalp3 inflammasome activating danger signal, " PLoS ONE, vol. 4, no. 8, Article ID e6510, 2009.
111. S. Sharma, R. B. DeOliveira, P. Kalantari et al., "Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome, " Immunity, vol. 35, no. 2, pp. 194-207, 2011.
112. S. D. Tachado, P. Gerold, M. J. McConville et al., "Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase Cdependent signaling pathway, " Journal of Immunology, vol. 156, no. 5, pp. 1897-1907, 1996.
113. J. Zhu, G. Krishnegowda, and D. C. Gowda, "Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: the requirement of extracellular signal-regulated kinase, p38, c-Jun N-terminal kinase and NF-κB pathways for the expression of proinflammatory cytokines and nitric oxide, " The Journal of Biological Chemistry, vol. 280, no. 9, pp. 8617-8627, 2005.
114. G. Krishnegowda, A. M. Hajjar, J. Zhu et al., "Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity, " The Journal of Biological Chemistry, vol. 280, no. 9, pp. 8606-8616, 2005.
115. L. K. Erdman, G. Cosio, A. J. Helmers, D. C. Gowda, S. Grinstein, and K. C. Kain, "CD36 and TLR interactions in inflammation and phagocytosis: implications for malaria, " The Journal of Immunology, vol. 183, no. 10, pp. 6452-6459, 2009.
116. S. Kumar, N. M. Gowda, X. Wu, R. N. Gowda, and D. C. Gowda, "CD36modulates proinflammatory cytokine responses to Plasmodium falciparum glycosylphosphatidylinositols and merozoites by dendritic cells, " Parasite Immunology, vol. 34, no. 7, pp. 372-382, 2012.
117. D. Togbe, L. Schofield, G. E. Grau et al., "Murine cerebral malaria development is independent of toll-like receptor signaling, " The American Journal of Pathology, vol. 170, no. 5, pp. 1640-1648, 2007.
118. B. Lepenies, J. P. Cramer, G. D. Burchard, H. Wagner, C. J. Kirschning, and T. Jacobs, "Induction of experimental cerebral malaria is independent of TLR2/4/9, " MedicalMicrobiology and Immunology, vol. 197, no. 1, pp. 39-44, 2008.
119. C. Coban, S. Uematsu, N. Arisue et al., "Pathological role of Toll-like receptor signaling in cerebral malaria, " International Immunology, vol. 19, no. 1, pp. 67-79, 2007.
120. M. Maglinao, R. Klopfleisch, P. H. Seeberger, and B. Lepenies, "TheC-type lectin receptorDCIR is crucial for the development of experimental cerebral malaria, " Journal of Immunology, vol. 191, no. 5, pp. 2551-2559, 2013.
121. D. L. van de Hoef, I. Coppens, T. Holowka, C. Ben Mamoun, O. Branch, and A. Rodriguez, "Plasmodium falciparum-derived uric acid precipitates inducematuration of dendritic cells, " PLoS ONE, vol. 8, no. 2, Article ID e55584, 2013.
122. S. B. Boscardin, J. C. R. Hafalla, R. F. Masilamani et al., "Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses, " Journal of ExperimentalMedicine, vol. 203, no. 3, pp. 599-606, 2006.
123. K. Tewari, B. J. Flynn, S. B. Boscardin et al., "Poly(I:C) is an effective adjuvant for antibody and multi-functional CD4+ T cell responses to Plasmodium falciparum circumsporozoite protein (CSP) and αDEC-CSP in non human primates, " Vaccine, vol. 28, no. 45, pp. 7256-7266, 2010.
124. K. Luo, H. Zhang, F. Zavala, A. Biragyn, D. A. Espinosa, and R. B. Markham, "Fusion of antigen to a dendritic cell targeting chemokine combined with adjuvant yields a malaria dna vaccine with enhanced protective capabilities, " PLoS ONE, vol. 9, no. 3, Article ID e90413, 2014.
125. F. Ginhoux, K. Liu, J. Helftet al., "Theoriginanddevelopmentof nonlymphoid tissue CD103+ DCs, "The Journal of Experimental Medicine, vol. 206, no. 13, pp. 3115-3130, 2009.
126. E. Segura, J. Valladeau-Guilemond, M.-H. Donnadieu, X. Sastre-Garau, V. Soumelis, and S. Amigorena, "Characterization of resident and migratory dendritic cells in human lymph nodes, " Journal of Experimental Medicine, vol. 209, no. 4, pp. 653-660, 2012.