Setting the stage: The initial immune response to blood-stage parasites

References

• World Malaria Report 2018. Geneva: World Health Organization; 2018. Licence: CC BY-NC-SA 3.0 IGO.
   Google Scholar
• Murphy K, Weaver C. Janeway’s Immunobiology. 9th ed. New York: Garland Science (Taylor & Francis Group); 2017. p. 924.
   Google Scholar
• Trape JF, Pison G, Preziosi M-P, et al. Impact of chloroquine resistance on malaria mortality. C R Acad Sci III. 1998;321(8):689–697.
   PubMed Web of Science ®Google Scholar
• Tran TM, Li S, Doumbo S, et al. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis. 2013;57(1):40–47.
   PubMed Web of Science ®Google Scholar
• Powell BJ, Othmer E, Sinkhorn C. Pharmacological aftercare for homogeneous groups of patients. Hosp Community Psychiatry. 1977;28(2):125–127.
   PubMedGoogle Scholar
• Shin SC, Vanderberg JP, Terzakis JA. Direct infection of hepatocytes by sporozoites of Plasmodium berghei. J Protozool. 1982;29(3):448–454.
   PubMedGoogle Scholar
• Chulay JD, Schneider I., Cosgriff, TM, et al. Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am J Trop Med Hyg. 1986;35(1):66–68.
   PubMed Web of Science ®Google Scholar
• Church LW, Preston LW, Le Thong P, et al. Clinical manifestations of Plasmodium falciparum malaria experimentally induced by mosquito challenge. J Infect Dis. 1997;175(4):915–920.
   PubMed Web of Science ®Google Scholar
• McCall MBB, Matthew BB, Linda J, et al. Infectivity of Plasmodium falciparum sporozoites determines emerging parasitemia in infected volunteers. Sci Transl Med. 2017;9(935):eaag2490.
   PubMedGoogle Scholar
• Boyle MJ, Wilson DW, Richards JS, et al. Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci U S A. 2010;107(32):14378–14383.
   PubMed Web of Science ®Google Scholar
• Sturm A, Amino R., Van de Sand C, et al. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science. 2006;313(5791):1287–1290.
   PubMed Web of Science ®Google Scholar
• Draper SJ, Sack BK, King CR, et al. Malaria Vaccines: recent advances and new horizons. Cell Host Microbe. 2018;24(1):43–56.
   PubMed Web of Science ®Google Scholar
• Kazmin D, Nakaya HI, Lee EK, et al. Systems analysis of protective immune responses to RTS,S malaria vaccination in humans. Proc Natl Acad Sci U S A. 2017;114(9):2425–2430.
   PubMed Web of Science ®Google Scholar
• Tan J, Sack BK, Oyen D, et al. A public antibody lineage that potently inhibits malaria infection through dual binding to the circumsporozoite protein. Nat Med. 2018;24(4):401–407.
   PubMed Web of Science ®Google Scholar
• Douglas AD, Baldeviano GC, Jin J, et al. A defined mechanistic correlate of protection against Plasmodium falciparum malaria in non-human primates. Nat Commun. 2019;10(1):1953.
   PubMedGoogle Scholar
• Deal CE, Balazs AB. Engineering humoral immunity as prophylaxis or therapy. Curr Opin Immunol. 2015;35:113–122.
   PubMed Web of Science ®Google Scholar
• Cowman AF, Healer J, Marapana D, et al. Malaria: biology and Disease. Cell. 2016;167(3):610–624.
   PubMed Web of Science ®Google Scholar
• Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–737.
   PubMed Web of Science ®Google Scholar
• Bouharoun-Tayoun H, Attanath P, Sabchareon A, et al. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med. 1990;172(6):1633–1641.
   PubMed Web of Science ®Google Scholar
• Bousema T, Okell L, Shekalaghe S, et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar J. 2010;9:136.
   PubMed Web of Science ®Google Scholar
• Acquah FK, Adjah J, Williamson KC, et al. Transmission-blocking vaccines: old friends and new prospects. Infect Immun. 2019;87(6).pii: e00775-18.
   PubMed Web of Science ®Google Scholar
• Dantzler KW, Ma S, Ngotho P, et al. Naturally acquired immunity against immature Plasmodium falciparum gametocytes. Sci Transl Med. 2019;11(495):eaav3963.
   PubMed Web of Science ®Google Scholar
• Saeed M, Roeffen W, Alexander N, et al. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS One. 2008;3(5):e2280.
   PubMed Web of Science ®Google Scholar
• Chan JA, Drew DR, Reiling L, et al. Low levels of human antibodies to gametocyte-infected erythrocytes contrasts the PfEMP1-dominant response to asexual stages in P. falciparum malaria. Front Immunol. 2018;9:3126.
   PubMed Web of Science ®Google Scholar
• Leech JH, Barnwell JW, Aikawa M, et al. Plasmodium falciparum malaria: association of knobs on the surface of infected erythrocytes with a histidine-rich protein and the erythrocyte skeleton. J Cell Biol. 1984;98(4):1256–1264.
   PubMed Web of Science ®Google Scholar
• Leech JH, Barnwell JW, Miller LH, et al. Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J Exp Med. 1984;159(6):1567–1575.
   PubMed Web of Science ®Google Scholar
• Aley SB, Sherwood JA, Howard RJ. Knob-positive and knob-negative Plasmodium falciparum differ in expression of a strain-specific malarial antigen on the surface of infected erythrocytes. J Exp Med. 1984;160(5):1585–1590.
   PubMed Web of Science ®Google Scholar
• Pasloske BL, Howard RJ. Malaria, the red cell, and the endothelium. Annu Rev Med. 1994;45:283–295.
   PubMed Web of Science ®Google Scholar
• Baruch DI, Pasloske BL, Singh HB, et al. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell. 1995;82(1):77–87.
   PubMed Web of Science ®Google Scholar
• Miller LH. Distribution of mature trophozoites and schizonts of Plasmodium falciparum in the organs of Aotus trivirgatus, the night monkey. Am J Trop Med Hyg. 1969;18(6):860–865.
   PubMedGoogle Scholar
• Rogerson SJ, Hviid L, Duffy PE, et al. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7(2):105–117.
   PubMed Web of Science ®Google Scholar
• Bignami A, Bastianeli G. Observations of estivo-autumnal malaria. Reforma Medica. 1889;6:1334–1335.
   Google Scholar
• Sampath S, Brazier AJ, Avril M, et al. Plasmodium falciparum adhesion domains linked to severe malaria differ in blockade of endothelial protein C receptor. Cell Microbiol. 2015;17(12):1868–1882.
   PubMed Web of Science ®Google Scholar
• Kyes SA, Kraemer SM, Smith JD. Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family. Eukaryot Cell. 2007;6(9):1511–1520.
   PubMed Web of Science ®Google Scholar
• Parmley RT, Takagi M, Denys FR. Ultrastructural localization of glycosaminoglycans in human term placenta. Anat Rec. 1984;210(3):477–484.
   PubMedGoogle Scholar
• Reeder JC, Cowman AF, Davern KM, et al. The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1. Proc Natl Acad Sci U S A. 1999;96(9):5198–5202.
   PubMed Web of Science ®Google Scholar
• Salanti A, Staalsoe T, Lavstsen T, et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol. 2003;49(1):179–191.
   PubMed Web of Science ®Google Scholar
• Turner L, Lavstsen T, Berger SS, et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature. 2013;498(7455):502–505.
   PubMed Web of Science ®Google Scholar
• Avril M, Brazier AJ, Melcher M, et al. DC8 and DC13 var genes associated with severe malaria bind avidly to diverse endothelial cells. PLoS Pathog. 2013;9(6):e1003430.
   PubMed Web of Science ®Google Scholar
• Duffy F, Bernabeu M, Babar PH, et al. Meta-analysis of plasmodium falciparum var signatures contributing to severe malaria in African children and Indian adults. MBio. 2019;10(2).pii: e00217-19.
   PubMed Web of Science ®Google Scholar
• Sampaio NG, Eriksson EM, Schofield L, et al. Plasmodium falciparum PfEMP1 modulates monocyte/macrophage transcription factor activation and cytokine and chemokine responses. Infect Immun. 2017;86(1).pii: e00447-17.
   PubMed Web of Science ®Google Scholar
• Sampaio NG, Emery SJ, Garnham AL, et al. Extracellular vesicles from early stage Plasmodium falciparum-infected red blood cells contain PfEMP1 and induce transcriptional changes in human monocytes. Cell Microbiol. 2018;20(5):e12822.
   PubMed Web of Science ®Google Scholar
• Guenot M, Loizon S, Howard J, et al. Phosphoantigen Burst upon plasmodium falciparum schizont rupture can distantly activate Vgamma9Vdelta2 T Cells. Infect Immun. 2015;83(10):3816–3824.
   PubMed Web of Science ®Google Scholar
• Hensmann M, Kwiatkowski D. Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun. 2001;69(4):2364–2371.
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Schulman S, Shear HL. Induction of crisis forms in the human malaria parasite Plasmodium falciparum by gamma-interferon-activated, monocyte-derived macrophages. J Immunol. 1984;133(3):1601–1608.
   PubMed Web of Science ®Google Scholar
• Scholzen A, Teirlinck AC, Bijker EM, et al. BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. J Immunol. 2014;192(8):3719–3729.
   PubMed Web of Science ®Google Scholar
• 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(3):287–296.
   PubMed Web of Science ®Google Scholar
• Scholzen A, Sauerwein RW. Immune activation and induction of memory: lessons learned from controlled human malaria infection with Plasmodium falciparum. Parasitology. 2016;143(2):224–235.
   PubMed Web of Science ®Google Scholar
• Walther M, Woodruff J, Edele F, et al. Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol. 2006;177(8):5736–5745.
   PubMed Web of Science ®Google Scholar
• Akdis M, Aab A, Altunbulakli C, et al. Interleukins (from IL-1 to IL-38), interferons, transforming growth factor beta, and TNF-alpha: receptors, functions, and roles in diseases. J Allergy Clin Immunol. 2016;138(4):984–1010.
   PubMed Web of Science ®Google Scholar
• Montes de Oca M, Kumar R, Rivera F, et al. Type I interferons regulate immune responses in humans with blood-stage plasmodium falciparum infection. Cell Rep. 2016;17(2):399–412.
   PubMed Web of Science ®Google Scholar
• Holdsworth SR, Gan PY. Cytokines: names and numbers you should care about. Clin J Am Soc Nephrol. 2015;10(12):2243–2254.
   PubMed Web of Science ®Google Scholar
• Schofield L, Mueller I. Clinical immunity to malaria. Curr Mol Med. 2006;6(2):205–221.
   PubMed Web of Science ®Google Scholar
• Kremsner PG, Bienzle U, Wildling E, et al. Prediction of accelerated cure in Plasmodium falciparum malaria by the elevated capacity of tumor necrosis factor production. Am J Trop Med Hyg. 1995;53(5):532–538.
   PubMed Web of Science ®Google Scholar
• Kremsner PG, Winkler S, Wildling E, et al. High plasma levels of nitrogen oxides are associated with severe disease and correlate with rapid parasitological and clinical cure in Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg. 1996;90(1):44–47.
   PubMed Web of Science ®Google Scholar
• Grau GE, Taylor TE, Molyneux ME, et al. Tumor necrosis factor and disease severity in children with falciparum malaria. N Engl J Med. 1989;320(24):1586–1591.
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Hu W-C, Kester KE, et al. Common and divergent immune response signaling pathways discovered in peripheral blood mononuclear cell gene expression patterns in presymptomatic and clinically apparent malaria. Infect Immun. 2006;74(10):5561–5573.
   PubMed Web of Science ®Google Scholar
• Tran TM, Jones MB, Ongoiba A, et al. Transcriptomic evidence for modulation of host inflammatory responses during febrile Plasmodium falciparum malaria. Sci Rep. 2016;6:31291.
   PubMed Web of Science ®Google Scholar
• Sicard A, Semblat J-P, Doerig C, et al. Activation of a PAK-MEK signalling pathway in malaria parasite-infected erythrocytes. Cell Microbiol. 2011;13(6):836–845.
   PubMed Web of Science ®Google Scholar
• Teirlinck AC, McCall MBB, Roestenberg M, et al. Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathog. 2011;7(12):e1002389.
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Sano S, Nieves E, et al. Nonpeptide ligands for human γδ T cells. Proc Natl Acad Sci U S A. 1994;91(17):8175–8179.
   PubMed Web of Science ®Google Scholar
• Goerlich R, Häcker G, Pfeffer K, et al. Plasmodium falciparum merozoites primarily stimulate the V gamma 9 subset of human gamma/delta T cells. Eur J Immunol. 1991;21(10):2613–2616.
   PubMed Web of Science ®Google Scholar
• Ho M, Tongtawe P, Kriangkum J, et al. Polyclonal expansion of peripheral γδ t cells in human plasmodium falciparum malaria. Infect Immun. 1994;62(3):855–862.
   PubMed Web of Science ®Google Scholar
• Roussilhon C, AGRAPART M, GUGLIELMI P, et al. Human TcR γδ+ lymphocyte response on primary exposure to Plasmodium falciparum. Clin Exp Immunol. 1994;95(1):91–97.
   PubMed Web of Science ®Google Scholar
• Stanisic DI, Cutts J, Eriksson E, et al. γδ T cells and CD14+ monocytes are predominant cellular sources of cytokines and chemokines associated with severe malaria. J Infect Dis. 2014;210(2):295–305.
   PubMed Web of Science ®Google Scholar
• Kalyan S, Kabelitz D. Defining the nature of human γδ T cells: a biographical sketch of the highly empathetic. Cell Mol Immunol. 2013;10(1):21–29.
   PubMed Web of Science ®Google Scholar
• Hammerich L, Tacke F. Role of gamma-delta T cells in liver inflammation and fibrosis. World J Gastrointest Pathophysiol. 2014;5(2):107–113.
   PubMedGoogle Scholar
• Jensen KD, Chien YH. Thymic maturation determines γδ T cell function, but not their antigen specificities. Curr Opin Immunol. 2009;21(2):140–145.
   PubMed Web of Science ®Google Scholar
• Lim L, McFadden GI. The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci. 2010;365(1541):749–763.
   PubMed Web of Science ®Google Scholar
• Rohrich RC, Englert N, Troschke K, et al. Reconstitution of an apicoplast-localised electron transfer pathway involved in the isoprenoid biosynthesis of Plasmodium falciparum. FEBS Lett. 2005;579(28):6433–6438.
   PubMed Web of Science ®Google Scholar
• Altincicek B, Duin EC, Reichenberg A, et al. LytB protein catalyzes the terminal step of the 2-C-methyl-D-erythritol-4-phosphate pathway of isoprenoid biosynthesis. FEBS Lett. 2002;532(3):437–440.
   PubMed Web of Science ®Google Scholar
• Seemann M, Bui BTS, Wolff M, et al. Isoprenoid biosynthesis through the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (GcpE) is a [4Fe-4S] protein. Angew Chem Int Ed Engl. 2002;41(22):4337–4339.
   PubMed Web of Science ®Google Scholar
• Kollas AK, Duin EC, Eberl M, et al. Functional characterization of GcpE, an essential enzyme of the non-mevalonate pathway of isoprenoid biosynthesis. FEBS Lett. 2002;532(3):432–436.
   PubMed Web of Science ®Google Scholar
• Behr C, Poupot R, Peyrat MA, et al. Plasmodium falciparum stimuli for human gammadelta T cells are related to phosphorylated antigens of mycobacteria. Infect Immun. 1996;64(8):2892–2896.
   PubMed Web of Science ®Google Scholar
• McCall MB, Roestenberg M, Ploemen I, et al. Memory-like IFN-gamma response by NK cells following malaria infection reveals the crucial role of T cells in NK cell activation by P. falciparum. Eur J Immunol. 2010;40(12):3472–3477.
   PubMed Web of Science ®Google Scholar
• Howard J, Zaidi I, Loizon S, et al. Human Vγ9δ2 T lymphocytes in the immune response to P. falciparum Infection. Front Immunol. 2018;9:2760.
   PubMed Web of Science ®Google Scholar
• Mamedov MR, Scholzen A, Nair RV, et al. A macrophage colony-stimulating-factor-producing γδ T cell subset prevents malarial parasitemic recurrence. Immunity. 2018;48(2):350–363 e7.
   PubMed Web of Science ®Google Scholar
• Hsieh MM, Everhart JE, Byrd-Holt DD, et al. Prevalence of neutropenia in the U.S. population: age, sex, smoking status, and ethnic differences. Ann Intern Med. 2007;146(7):486–492.
   PubMed Web of Science ®Google Scholar
• Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159–175.
   PubMed Web of Science ®Google Scholar
• Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535.
   PubMed Web of Science ®Google Scholar
• Trubowitz S, Masek B. Plasmodium falciparum: phagocytosis by polymorphonuclear leukocytes. Science. 1968;162(3850):273–274.
   PubMed Web of Science ®Google Scholar
• Dasari P, Reiss K, Lingelbach K, et al. Digestive vacuoles of Plasmodium falciparum are selectively phagocytosed by and impair killing function of polymorphonuclear leukocytes. Blood. 2011;118(18):4946–4956.
   PubMed Web of Science ®Google Scholar
• Kharazmi A, Jepsen S. Enhanced inhibition of in vitro multiplication of Plasmodium falciparum by stimulated human polymorphonuclear leucocytes. Clin Exp Immunol. 1984;57(2):287–292.
   PubMed Web of Science ®Google Scholar
• Nnalue NA, Friedman MJ. Evidence for a neutrophil-mediated protective response in malaria. Parasite Immunol. 1988;10(1):47–58.
   PubMed Web of Science ®Google Scholar
• Cunnington AJ, Njie M, Correa S, et al. Prolonged neutrophil dysfunction after Plasmodium falciparum malaria is related to hemolysis and heme oxygenase-1 induction. J Immunol. 2012;189(11):5336–5346.
   PubMed Web of Science ®Google Scholar
• Mooney JP, Galloway LJ, Riley EM. Malaria, anemia, and invasive bacterial disease: A neutrophil problem? J Leukoc Biol. 2019;105(4):645–655.
   PubMed Web of Science ®Google Scholar
• Cunnington AJ, de Souza JB, Walther M, et al. Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med. 2011;18(1):120–127.
   PubMed Web of Science ®Google Scholar
• Knackstedt SL, Georgiadou A, Apel F, et al. Neutrophil extracellular traps drive inflammatory pathogenesis in malaria. Sci Immunol. 2019;4(40):eaaw0336.
   PubMed Web of Science ®Google Scholar
• Sercundes MK, Ortolan LS, Debone D, et al. Targeting neutrophils to prevent malaria-associated acute lung injury/acute respiratory distress syndrome in mice. PLoS Pathog. 2016;12(12):e1006054.
   PubMed Web of Science ®Google Scholar
• Hoppenbrouwers T, Autar ASA, Sultan AR, et al. In vitro induction of NETosis: comprehensive live imaging comparison and systematic review. PLoS One. 2017;12(5):e0176472.
   PubMed Web of Science ®Google Scholar
• Gallego-Delgado J, Ty M, Orengo JM, et al. A surprising role for uric acid: the inflammatory malaria response. Curr Rheumatol Rep. 2014;16(2):401.
   PubMed Web of Science ®Google Scholar
• Dunst J, Kamena F, Matuschewski K. Cytokines and chemokines in cerebral malaria pathogenesis. Front Cell Infect Microbiol. 2017;7:324.
   PubMed Web of Science ®Google Scholar
• Percario S, Moreira D, Gomes B, et al. Oxidative stress in malaria. Int J Mol Sci. 2012;13(12):16346–16372.
   PubMed Web of Science ®Google Scholar
• van Wolfswinkel ME, Langenberg MCC, Wammes LJ, et al. Changes in total and differential leukocyte counts during the clinically silent liver phase in a controlled human malaria infection in malaria-naive Dutch volunteers. Malar J. 2017;16(1):457.
   PubMedGoogle Scholar
• Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front Immunol. 2014;5:514.
   PubMed Web of Science ®Google Scholar
• Gazzinelli RT, Kalantari P, Fitzgerald KA, et al. Innate sensing of malaria parasites. Nat Rev Immunol. 2014;14(11):744–757.
   PubMed Web of Science ®Google Scholar
• Mantel PY, Hoang A, Goldowitz I, et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe. 2013;13(5):521–534.
   PubMed Web of Science ®Google Scholar
• Regev-Rudzki N, Wilson D, Carvalho T, et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell. 2013;153(5):1120–1133.
   PubMed Web of Science ®Google Scholar
• Krishnegowda G, Hajjar AM, Zhu J, 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. J Biol Chem. 2005;280(9):8606–8616.
   PubMed Web of Science ®Google Scholar
• Zhu J, Krishnegowda G, Li G, et al. Proinflammatory responses by glycosylphosphatidylinositols (GPIs) of Plasmodium falciparum are mainly mediated through the recognition of TLR2/TLR1. Exp Parasitol. 2011;128(3):205–211.
   PubMed Web of Science ®Google Scholar
• Schofield L, McConville MJ, Hansen D, et al. CD1d-restricted immunoglobulin G formation to GPI-anchored antigens mediated by NKT cells. Science. 1999;283(5399):225–229.
   PubMed Web of Science ®Google Scholar
• Pombo DJ, Lawrence G, Hirunpetcharat C, et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet. 2002;360(9333):610–617.
   PubMed Web of Science ®Google Scholar
• Mpina M, Maurice NJ, Yajima M, et al. Controlled human malaria infection leads to long-lasting changes in innate and innate-like lymphocyte populations. J Immunol. 2017;199(1):107–118.
   PubMed Web of Science ®Google Scholar
• Lehmann JS, Campo JJ, Cicéron M, et al. T cell subtypes and reciprocal inflammatory mediator expression differentiate P. falciparum memory recall responses in asymptomatic and symptomatic malaria patients in southeastern Haiti. PLoS One. 2017;12(4):e0174718.
   PubMed Web of Science ®Google Scholar
• Schwarzer E, Turrini F, Ulliers D, et al. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med. 1992;176(4):1033–1041.
   PubMed Web of Science ®Google Scholar
• Schwarzer E, Alessio M, Ulliers D, et al. 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(4):1601–1606.
   PubMed Web of Science ®Google Scholar
• Coban C, Ishii KJ, Kawai T, et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med. 2005;201(1):19–25.
   PubMed Web of Science ®Google Scholar
• Sharma S, DeOliveira R, Kalantari P, et al. Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity. 2011;35(2):194–207.
   PubMed Web of Science ®Google Scholar
• Kumsiri R, Potup P, Chotivanich K, et al. Blood stage Plasmodium falciparum antigens induce T cell independent immunoglobulin production via B cell activation factor of the TNF family (BAFF) pathway. Acta Trop. 2010;116(3):217–226.
   PubMed Web of Science ®Google Scholar
• Parroche P, Lauw FN, Goutagny N, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A. 2007;104(6):1919–1924.
   PubMed Web of Science ®Google Scholar
• Gallego-Marin C, Schrum JE, Andrade WA, et al. Cyclic GMP-AMP synthase is the cytosolic sensor of plasmodium falciparum genomic DNA and activates type I IFN in malaria. J Immunol. 2018;200(2):768–774.
   PubMed Web of Science ®Google Scholar
• Dostert C, Guarda G, Romero JF, et al. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS One. 2009;4(8):e6510.
   PubMed Web of Science ®Google Scholar
• Griffith JW, Sun T, McIntosh MT, et al. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208–5220.
   PubMed Web of Science ®Google Scholar
• Shio MT, Eisenbarth SC, Savaria M, et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009;5(8):e1000559.
   PubMed Web of Science ®Google Scholar
• Raulf M-K, Johannssen T, Matthiesen S, et al. The C-type lectin receptor CLEC12A recognizes plasmodial hemozoin and contributes to cerebral malaria development. Cell Rep. 2019;28(1):30–38 e5.
   PubMed Web of Science ®Google Scholar
• Hänscheid T, Egan TJ, Grobusch MP. Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect Dis. 2007;7(10):675–685.
   PubMed Web of Science ®Google Scholar
• Sisquella X, Ofir-Birin Y, Pimentel MA, et al. Malaria parasite DNA-harbouring vesicles activate cytosolic immune sensors. Nat Commun. 2017;8(1):1985.
   PubMed Web of Science ®Google Scholar
• Coch C, Hommertgen B, Zillinger T, et al. Human TLR8 Senses RNA from plasmodium falciparum-infected red blood cells which is uniquely required for the IFN-gamma response in NK cells. Front Immunol. 2019;10:371.
   PubMed Web of Science ®Google Scholar
• Ojo-Amaize EA, Salimonu LS, Williams AI, et al. Positive correlation between degree of parasitemia, interferon titers, and natural killer cell activity in Plasmodium falciparum-infected children. J Immunol. 1981;127(6):2296–2300.
   PubMed Web of Science ®Google Scholar
• Chen Q, Amaladoss A, Ye W, et al. Human natural killer cells control Plasmodium falciparum infection by eliminating infected red blood cells. Proc Natl Acad Sci U S A. 2014;111(4):1479–1484.
   PubMed Web of Science ®Google Scholar
• Newman KC, Korbel DS, Hafalla JC, et al. Cross-talk with myeloid accessory cells regulates human natural killer cell interferon-gamma responses to malaria. PLoS Pathog. 2006;2(12):e118.
   PubMed Web of Science ®Google Scholar
• Ye W, Chew M, Hou J, et al. Microvesicles from malaria-infected red blood cells activate natural killer cells via MDA5 pathway. PLoS Pathog. 2018;14(10):e1007298.
   PubMed Web of Science ®Google Scholar
• Doherty DG, O’Farrelly C. Innate and adaptive lymphoid cells in the human liver. Immunol Rev. 2000;174:5–20.
   PubMed Web of Science ®Google Scholar
• Orago AS, Facer CA. Cytotoxicity of human natural killer (NK) cell subsets for Plasmodium falciparum erythrocytic schizonts: stimulation by cytokines and inhibition by neomycin. Clin Exp Immunol. 1991;86(1):22–29.
   PubMed Web of Science ®Google Scholar
• Korbel DS, Newman KC, Almeida CR, et al. Heterogeneous human NK cell responses to Plasmodium falciparum-infected erythrocytes. J Immunol. 2005;175(11):7466–7473.
   PubMed Web of Science ®Google Scholar
• Fehniger TA, Shah MH, Turner MJ, et al. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol. 1999;162(8):4511–4520.
   PubMed Web of Science ®Google Scholar
• Nielsen CM, Wolf A-S, Goodier MR, et al. Synergy between common gamma chain family cytokines and IL-18 potentiates innate and adaptive pathways of NK cell activation. Front Immunol. 2016;7:101.
   PubMed Web of Science ®Google Scholar
• Hart GT, Tran TM, Theorell J, et al. Adaptive NK cells in people exposed to Plasmodium falciparum correlate with protection from malaria. J Exp Med. 2019;216(6):1280–1290.
   PubMed Web of Science ®Google Scholar
• Orsini G, Legitimo A, Failli A, et al. Enumeration of human peripheral blood dendritic cells throughout the life. Int Immunol. 2012;24(6):347–356.
   PubMed Web of Science ®Google Scholar
• Segura E. Review of Mouse and Human Dendritic Cell Subsets. In: Segura E, Onai N, editor. Dendritic Cell Protocols. Methods in Molecular Biology, vol 1423. New York, NY: Humana Press; 2016.
   Google Scholar
• Villani AC, Satija R, Reynolds G, et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science. 2017;356(6335):eaah4573.
   PubMed Web of Science ®Google Scholar
• Collin M, McGovern N, Haniffa M. Human dendritic cell subsets. Immunology. 2013;140(1):22–30.
   PubMed Web of Science ®Google Scholar
• Collin M, Bigley V. Human dendritic cell subsets: an update. Immunology. 2018;154(1):3–20.
   PubMed Web of Science ®Google Scholar
• Urban BC, Ferguson DJP, Pain A, et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature. 1999;400(6739):73–77.
   PubMed Web of Science ®Google Scholar
• Elliott SR, Spurck TP, Dodin JM, et al. Inhibition of dendritic cell maturation by malaria is dose dependent and does not require Plasmodium falciparum erythrocyte membrane protein 1. Infect Immun. 2007;75(7):3621–3632.
   PubMed Web of Science ®Google Scholar
• Gotz A, Tang MS, Ty MC, et al. Atypical activation of dendritic cells by Plasmodium falciparum. Proc Natl Acad Sci U S A. 2017;114(49):E10568–E10577.
   PubMed Web of Science ®Google Scholar
• Loughland JR, Woodberry T, Boyle MJ, et al. Plasmodium falciparum activates CD16+ dendritic cells to produce tumor necrosis factor and interleukin-10 in subpatent malaria. J Infect Dis. 2019;219(4):660–671.
   PubMed Web of Science ®Google Scholar
• Soon MSF, Haque A. Recent Insights into CD4+ Th cell differentiation in malaria. J Immunol. 2018;200(6):1965–1975.
   PubMed Web of Science ®Google Scholar
• Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001;14(4): 778–809. table of contents.
   PubMed Web of Science ®Google Scholar
• Haque A, Best SE, Ammerdorffer A, et al. Type I interferons suppress CD4+ T-cell-dependent parasite control during blood-stage Plasmodium infection. Eur J Immunol. 2011;41(9):2688–2698.
   PubMed Web of Science ®Google Scholar
• Haque A, Best SE, Montes de Oca M, et al. Type I IFN signaling in CD8- DCs impairs Th1-dependent malaria immunity. J Clin Invest. 2014;124(6):2483–2496.
   PubMed Web of Science ®Google Scholar
• Teirlinck AC, Roestenberg M, Bijker EM, et al. Plasmodium falciparum infection of human volunteers activates monocytes and CD16+ dendritic cells and induces upregulation of CD16 and CD1c expression. Infect Immun. 2015;83(9):3732–3739.
   PubMed Web of Science ®Google Scholar
• Loughland JR, Minigo G, Burel J, et al. Profoundly reduced CD1c+ myeloid dendritic cell HLA-DR and CD86 expression and increased tumor necrosis factor production in experimental human blood-stage malaria infection. Infect Immun. 2016;84(5):1403–1412.
   PubMed Web of Science ®Google Scholar
• Loughland JR, Minigo G, Sarovich DS, et al. Plasmacytoid dendritic cells appear inactive during sub-microscopic Plasmodium falciparum blood-stage infection, yet retain their ability to respond to TLR stimulation. Sci Rep. 2017;7(1):2596.
   PubMedGoogle Scholar
• Woodberry T, Minigo G, Piera KA, et al. Low-level Plasmodium falciparum blood-stage infection causes dendritic cell apoptosis and dysfunction in healthy volunteers. J Infect Dis. 2012;206(3):333–340.
   PubMed Web of Science ®Google Scholar
• Piccioli D, Tavarini S, Borgogni E, et al. Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood. 2007;109(12):5371–5379.
   PubMed Web of Science ®Google Scholar
• Kurup SP, Butler NS, Harty JT. T cell-mediated immunity to malaria. Nat Rev Immunol. 2019;19(7):457–471.
   PubMed Web of Science ®Google Scholar
• Dupre-Crochet S, Erard M, Nubetae O. ROS production in phagocytes: why, when, and where?. J Leukoc Biol. 2013;94(4):657–670.
   PubMed Web of Science ®Google Scholar