A bite to fight: front-line innate immune defenses against malaria parasites

References

• WHO. World malaria report. Geneva: World Health Organization; 2016.
   Google Scholar
• Offeddu V, Thathy V, Marsh K, et al. Naturally acquired immune responses against Plasmodium falciparum sporozoites and liver infection. Int J Parasitol. 2012;42(6):535–548.10.1016/j.ijpara.2012.03.011
   PubMed Web of Science ®Google Scholar
• Rich SM, Ayala FJ. Population structure and recent evolution of Plasmodium falciparum. Proc Nat Acad Sci. 2000;97(13):6994–7001.10.1073/pnas.97.13.6994
   PubMed Web of Science ®Google Scholar
• Su XZ, Heatwole VM, Wertheimer SP, et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell. 1995;82(1):89–100.10.1016/0092-8674(95)90055-1
   PubMed Web of Science ®Google Scholar
• Abdi AI, Fegan G, Muthui M, et al. Plasmodium falciparum antigenic variation: relationships between widespread endothelial activation, parasite PfEMP1 expression and severe malaria. BMC Infect Dis. 2014;14:170.10.1186/1471-2334-14-170
   PubMed Web of Science ®Google Scholar
• Deitsch KW, Dzikowski R. Variant gene expression and antigenic variation by malaria parasites. Annu Rev Microbiol. 2017;71:625–641.10.1146/annurev-micro-090816-093841
   PubMed Web of Science ®Google Scholar
• Galinski MR, Lapp SA, Peterson MS, et al. Plasmodium knowlesi: a superb in vivo nonhuman primate model of antigenic variation in malaria. Parasitology. 2017;1–16. DOI:10.1017/S0031182017001135
   Web of Science ®Google Scholar
• Kirkman LA, Deitsch KW. Antigenic variation and the generation of diversity in malaria parasites. Curr Opin Microbiol. 2012;15(4):456–462.10.1016/j.mib.2012.03.003
   PubMed Web of Science ®Google Scholar
• Buckee CO, Gupta S. Modelling malaria population structure and its implications for control. Adv Exp Med Biol. 2010;673:112–126.10.1007/978-1-4419-6064-1
   PubMed Web of Science ®Google Scholar
• Stanisic DI, Barry AE, Good MF. Escaping the immune system: How the malaria parasite makes vaccine development a challenge. Trends Parasitol. 2013;29(12):612–622.10.1016/j.pt.2013.10.001
   PubMed Web of Science ®Google Scholar
• Grassi B, Bignami A, Bastianelli G. Medical zoology: further researches upon the cycle of human malaria in the body of the mosquito. Indian Med Gazette. 1899;34(3):104–107.
   PubMedGoogle Scholar
• Ross R Dr. Manson’s mosquito-malaria theory. Indian Med gazette. 1896;31(7):264.
   PubMedGoogle Scholar
• Antinori S, Galimberti L, Milazzo L, et al. Biology of human malaria plasmodia including Plasmodium knowlesi. Mediterr J Hematol Infect Dis. 2012;4(1):e2012013.10.4084/mjhid.2012.013
   PubMedGoogle Scholar
• Silver KL, Higgins SJ, McDonald CR, et al. Complement driven innate immune response to malaria: fuelling severe malarial diseases. Cell Microbiol. 2010;12(8):1036–1045.10.1111/j.1462-5822.2010.01492.x
   PubMed Web of Science ®Google Scholar
• Jongwutiwes S, Buppan P, Kosuvin R, et al. Plasmodium knowlesi malaria in humans and macaques, Thailand. Emerg Infect Dis. 2011;17(10):1799–1806.10.3201/eid1710.110349
   PubMed Web of Science ®Google Scholar
• Bruce MC, Macheso A, Galinski MR, et al. Characterization and application of multiple genetic markers for Plasmodium malariae. Parasitology. 2007;134(Pt 5):637–650.10.1017/S0031182006001958
   PubMedGoogle Scholar
• Collins WE, Jeffery GM. Plasmodium malariae: parasite and disease. Clin Microbiol Rev. 2007;20(4):579–592.10.1128/CMR.00027-07
   PubMed Web of Science ®Google Scholar
• Richter J, Franken G, Mehlhorn H, et al. What is the evidence for the existence of Plasmodium ovale hypnozoites? Parasitol Res. 2010;107(6):1285–1290.10.1007/s00436-010-2071-z
   PubMed Web of Science ®Google Scholar
• Da DF, Churcher TS, Yerbanga RS, et al. Experimental study of the relationship between Plasmodium gametocyte density and infection success in mosquitoes; implications for the evaluation of malaria transmission-reducing interventions. Exp Parasitol. 2015;149:74–83.10.1016/j.exppara.2014.12.010
   PubMed Web of Science ®Google Scholar
• Ishino T, Yano K, Chinzei Y, et al. Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol. 2004;2(1):E4.10.1371/journal.pbio.0020004
   PubMed Web of Science ®Google Scholar
• Ishino T, Chinzei Y, Yuda M. A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol. 2005;7(2):199–208.
   PubMed Web of Science ®Google Scholar
• Kariu T, Ishino T, Yano K, et al. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol. 2006;59(5):1369–1379.10.1111/j.1365-2958.2005.05024.x
   PubMed Web of Science ®Google Scholar
• Frevert U, Nardin E. Arrest in the liver–a genetically defined malaria vaccine? N Engl J Med. 2005;352(15):1600–1602.10.1056/NEJMcibr050521
   PubMed Web of Science ®Google Scholar
• Frevert U, Usynin I, Baer K, et al. Nomadic or sessile: can Kupffer cells function as portals for malaria sporozoites to the liver? Cell Microbiol. 2006;8(10):1537–1546.10.1111/cmi.2006.8.issue-10
   PubMed Web of Science ®Google Scholar
• Tavares J, Formaglio P, Thiberge S, et al. Role of host cell traversal by the malaria sporozoite during liver infection. J Exp Med. 2013;210(5):905–915.10.1084/jem.20121130
   PubMed Web of Science ®Google Scholar
• Hollingdale MR, Collins Alan LWE, Campbell CC, et al. In vitro culture of two populations (dividing and nondividing) of exoerythrocytic parasites of Plasmodium vivax. Am J Trop Med Hyg. 1985;34(2):216–222.10.4269/ajtmh.1985.34.216
   PubMed Web of Science ®Google Scholar
• Mazier D, Collins WE, Mellouk S, et al. Plasmodium ovale: in vitro development of hepatic stages. Exp Parasitol. 1987;64(3):393–400.10.1016/0014-4894(87)90052-X
   PubMed Web of Science ®Google Scholar
• Markus MB. Do hypnozoites cause relapse in malaria? Trends Parasitol. 2015;31(6):239–245.10.1016/j.pt.2015.02.003
   PubMed Web of Science ®Google Scholar
• Hulden L, Hulden L. Activation of the hypnozoite: a part of Plasmodium vivax life cycle and survival. Malaria J. 2011;10:90.10.1186/1475-2875-10-90
   PubMed Web of Science ®Google Scholar
• Garnham PC. Relapses in malaria: review of current studies. Ann Soc Belg Med Trop. 1985;65(3):233–242.
   PubMedGoogle Scholar
• Hulden L, Hulden L, Heliovaara K. Natural relapses in vivax malaria induced by Anopheles mosquitoes. Malaria J. 2008;7:64.10.1186/1475-2875-7-64
   PubMed Web of Science ®Google Scholar
• Bannister L, Mitchell G. The ins, outs and roundabouts of malaria. Trends Parasitol. 2003;19(5):209–213.10.1016/S1471-4922(03)00086-2
   PubMed Web of Science ®Google Scholar
• Hanssen E, Dekiwadia C, Riglar DT, et al. Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion. Cell Microbiol. 2013;15(9):1457–1472.10.1111/cmi.12132
   PubMed Web of Science ®Google Scholar
• Riglar DT, Richard D, Wilson DW, et al. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microb. 2011;9(1):9–20.10.1016/j.chom.2010.12.003
   PubMed Web of Science ®Google Scholar
• Singh S, Alam MM, Pal-Bhowmick I, et al. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog. 2010;6(2):e1000746.10.1371/journal.ppat.1000746
   PubMed Web of Science ®Google Scholar
• Baum J, Richard D, Healer J, et al. A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J Biol Chem. 2006;281(8):5197–5208.10.1074/jbc.M509807200
   PubMed Web of Science ®Google Scholar
• Jones ML, Kitson EL, Rayner JC. Plasmodium falciparum erythrocyte invasion: a conserved myosin associated complex. Mol Biochem Parasitol. 2006;147(1):74–84.10.1016/j.molbiopara.2006.01.009
   PubMed Web of Science ®Google Scholar
• Glushakova S, Yin D, Li T, et al. Membrane transformation during malaria parasite release from human red blood cells. Curr Biol. 2005;15(18):1645–1650.10.1016/j.cub.2005.07.067
   PubMed Web of Science ®Google Scholar
• Elbadry MA, Al-Khedery B, Tagliamonte MS, et al. High prevalence of asymptomatic malaria infections: a cross-sectional study in rural areas in six departments in Haiti. Malaria J. 2015;14:510.10.1186/s12936-015-1051-2
   PubMed Web of Science ®Google Scholar
• Bruce MC, Alano P, Duthie S, et al. Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology. 1990;100(Pt 2):191–200.10.1017/S0031182000061199
   PubMed Web of Science ®Google Scholar
• Josling GA, Llinás M. Sexual development in Plasmodium parasites: knowing when it’s time to commit. Nat Rev Microbiol. 2015;13(9):573–587.10.1038/nrmicro3519
   PubMed Web of Science ®Google Scholar
• Aly AS, Vaughan AM, Kappe SH. Malaria parasite development in the mosquito and infection of the mammalian host. Ann Rev Microbiol. 2009;63:195–221.10.1146/annurev.micro.091208.073403
   PubMed Web of Science ®Google Scholar
• Zevering Y, Khamboonruang C, Good MF. Effect of polymorphism of sporozoite antigens on T-cell activation. Res Immunol. 1994;145(6):469–476.10.1016/S0923-2494(94)80178-9
   PubMedGoogle Scholar
• Zevering Y, Khamboonruang C, Good MF. Human and murine T-cell responses to allelic forms of a malaria circumsporozoite protein epitope support a polyvalent vaccine strategy. Immunology. 1998;94(3):445–454.10.1046/j.1365-2567.1998.00514.x
   PubMed Web of Science ®Google Scholar
• Winter G, Kawai S, Haeggström M, et al. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med. 2005;201(11):1853–1863.10.1084/jem.20041392
   PubMed Web of Science ®Google Scholar
• Kiwanuka GN. Genetic diversity in Plasmodium falciparum merozoite surface protein 1 and 2 coding genes and its implications in malaria epidemiology: a review of published studies from 1997–2007. J Vector Borne Dis. 2009;46(1):1–12.
   PubMed Web of Science ®Google Scholar
• Ramasamy R. Molecular basis for evasion of host immunity and pathogenesis in malaria. Biochimica et biophysica acta 1998;1406::10–27.10.1016/S0925-4439(97)00078-1
   PubMed Web of Science ®Google Scholar
• Wright GJ, Rayner JC. Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathog. 2014;10(3):e1003943.10.1371/journal.ppat.1003943
   PubMed Web of Science ®Google Scholar
• Singh V, Gupta P, Pande V. Revisiting the multigene families: Plasmodium var and vir genes. J Vector Borne Dis. 2014;51(2):75–81.
   PubMed Web of Science ®Google Scholar
• Fernandez V, Hommel M, Chen Q, et al. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J Exp Med. 1999;190(10):1393–1404.10.1084/jem.190.10.1393
   PubMed Web of Science ®Google Scholar
• Wahlgren M, Goel S, Akhouri RR. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat Rev Microbiol. 2017;15(8):479–491.10.1038/nrmicro.2017.47
   PubMed Web of Science ®Google Scholar
• D’Ombrain MC, Voss TS, Maier AG, et al. Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host Microb. 2007;2(2):130–138.10.1016/j.chom.2007.06.012
   PubMed Web of Science ®Google Scholar
• Son UH, Dinzouna-Boutamba SD, et al. Diversity of vir genes in Plasmodium vivax from endemic regions in the Republic of Korea: an initial evaluation. Korean J Parasitol. 2017;55(2):149–158.10.3347/kjp.2017.55.2.149
   PubMed Web of Science ®Google Scholar
• Segal AW. How neutrophils kill microbes. Ann Rev Immunol. 2005;23:197–223.10.1146/annurev.immunol.23.021704.115653
   PubMed Web of Science ®Google Scholar
• Chen CL, Wang Y, et al. IL-17 induces antitumor immunity by promoting beneficial neutrophil recruitment and activation in esophageal squamous cell carcinoma. Oncoimmunology. 2017;7(1):e1373234.
   PubMed Web of Science ®Google Scholar
• Amicarella F, Muraro MG, Hirt C, et al. Dual role of tumour-infiltrating T helper 17 cells in human colorectal cancer. Gut. 2017;66(4):692–704.10.1136/gutjnl-2015-310016
   PubMed Web of Science ®Google Scholar
• Peters NC, Egen JG, Secundino N, et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science. 2008;321(5891):970–974.10.1126/science.1159194
   PubMed Web of Science ®Google Scholar
• Yamauchi LM, Coppi A, Snounou G, et al. Plasmodium sporozoites trickle out of the injection site. Cell Microbiol. 2007;9(5):1215–1222.10.1111/cmi.2007.9.issue-5
   PubMed Web of Science ®Google Scholar
• Mac-Daniel L, Buckwalter MR, Berthet M, et al. Local immune response to injection of Plasmodium sporozoites into the skin. J Immunol. 2014;193(3):1246–1257.10.4049/jimmunol.1302669
   PubMed Web of Science ®Google Scholar
• Hopp CS, Sinnis P. The innate and adaptive response to mosquito saliva and Plasmodium sporozoitess in the skin. Ann N Y Acad Sci. 2015;1342:37–43.10.1111/nyas.2015.1342.issue-1
   PubMed Web of Science ®Google Scholar
• Waisberg M, Molina-Cruz A, Mizurini DM, et al. Plasmodium falciparum infection induces expression of a mosquito salivary protein (Agaphelin) that targets neutrophil function and inhibits thrombosis without impairing hemostasis. PLoS Pathog. 2014;10(9):e1004338.10.1371/journal.ppat.1004338
   PubMed Web of Science ®Google Scholar
• Demeure CE, Brahimi K, Hacini F, et al. Anopheles mosquito bites activate cutaneous mast cells leading to a local inflammatory response and lymph node hyperplasia. J Immunol. 2005;174(7):3932–3940.10.4049/jimmunol.174.7.3932
   PubMed Web of Science ®Google Scholar
• Metzger WG, Mordmüller BG, Kremsner PG. Malaria pigment in leucocytes. Trans R Soc Trop Med Hyg. 1995;89(6):637–638.10.1016/0035-9203(95)90423-9
   PubMed Web of Science ®Google Scholar
• Sun T, Chakrabarti C. Schizonts, merozoites, and phagocytosis in falciparum malaria. Ann Clin Lab Sci. 1985;15(6):465–469.
   PubMed Web of Science ®Google Scholar
• Brown J, Smalley ME. Inhibition of the in vitro growth of Plasmodium falciparum by human polymorphonuclear neutrophil leucocytes. Clin Exp Immunol. 1981;46(1):106–109.
   PubMed Web of Science ®Google Scholar
• Kharazmi A, Jepsen S, Valerius NH. Polymorphonuclear leucocytes defective in oxidative metabolism inhibit in vitro growth of Plasmodium falciparum. Evidence against an oxygen-dependent mechanism. Scand J Immunol. 1984;20(1):93–96.10.1111/sji.1984.20.issue-1
   PubMed Web of Science ®Google Scholar
• Kumaratilake LM, Ferrante A. Opsonization and phagocytosis of Plasmodium falciparum merozoites measured by flow cytometry. Clin Diagn Lab Immunol. 2000;7(1):9–13.
   PubMedGoogle Scholar
• Joos C, Marrama L, Polson HE, et al. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS ONE. 2010;5(3):e9871.10.1371/journal.pone.0009871
   PubMed Web of Science ®Google Scholar
• Kapelski S, Klockenbring T, Fischer R, et al. Assessment of the neutrophilic antibody-dependent respiratory burst (ADRB) response to Plasmodium falciparum. J Leukoc Biol. 2014;96(6):1131–1142.10.1189/jlb.4A0614-283RR
   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
• Clark IA, Hunt NH. Evidence for reactive oxygen intermediates causing hemolysis and parasite death in malaria. Infect Immun. 1983;39(1):1–6.
   PubMed Web of Science ®Google Scholar
• Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007;176(2):231–241.10.1083/jcb.200606027
   PubMed Web of Science ®Google Scholar
• Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535.10.1126/science.1092385
   PubMed Web of Science ®Google Scholar
• Baker VS, Imade GE, Molta NB, et al. Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malaria J. 2008;7:41.10.1186/1475-2875-7-41
   PubMed Web of Science ®Google Scholar
• Mahanta A, Kar SK, Kakati S, et al. Heightened inflammation in severe malaria is associated with decreased IL-10 expression levels and neutrophils. Innate Immunity. 2015;21(5):546–552.10.1177/1753425914561277
   PubMed Web of Science ®Google Scholar
• Ioannidis LJ, Nie CQ, Ly A, et al. Monocyte- and Neutrophil-Derived CXCL10 Impairs Efficient Control of Blood-Stage Malaria Infection and Promotes Severe Disease. J Immunol. 2016;196(3):1227–1238.10.4049/jimmunol.1501562
   PubMed Web of Science ®Google Scholar
• Sercundes MK, Ortolan LS, Debone D, et al. Correction: targeting neutrophils to prevent malaria-associated acute lung injury/acute respiratory distress syndrome in mice. PLoS Pathog. 2017;13(11):e1006730.10.1371/journal.ppat.1006730
   PubMedGoogle Scholar
• Moghaddam AS, Mohammadian S, Vazini H, et al. Macrophage plasticity, polarization and function in health and disease. J Cell Physiol. 2018. DOI:10.1002/jcp.26429
   PubMedGoogle Scholar
• Li C, Xu MM, Wang K, et al. Macrophage polarization and meta-inflammation. Translational research: the journal of laboratory and clinical medicine. 2018;191:29–44.10.1016/j.trsl.2017.10.004
   PubMed Web of Science ®Google Scholar
• Petty AJ, Yang Y. Tumor-associated macrophages: implications in cancer immunotherapy. Immunotherapy. 2017;9(3):289–302.10.2217/imt-2016-0135
   PubMed Web of Science ®Google Scholar
• Soulat D, Bogdan C. Function of Macrophage and Parasite Phosphatases in Leishmaniasis. Front Immunol. 2017;8:1838.10.3389/fimmu.2017.01838
   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):e118.10.1371/journal.ppat.0020118
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Tandon NN, Magowan C, et al. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science. 1989;243(4897):1469–71.10.1126/science.2467377
   PubMed Web of Science ®Google Scholar
• Ockenhouse CF, Tegoshi T, Maeno Y, et al. Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. J Exp Med. 1992;176(4):1183–1189.10.1084/jem.176.4.1183
   PubMed Web of Science ®Google Scholar
• Sinka ME, Bangs MJ, Manguin S, et al. A global map of dominant malaria vectors. Parasites Vectors. 2012;5:69.10.1186/1756-3305-5-69
   PubMed Web of Science ®Google Scholar
• Klotz C, Frevert U. Plasmodium yoelii sporozoites modulate cytokine profile and induce apoptosis in murine Kupffer cells. Int J Parasitol. 2008;38(14):1639–1650.10.1016/j.ijpara.2008.05.018
   PubMed Web of Science ®Google Scholar
• Usynin I, Klotz C, Frevert U. Malaria circumsporozoite protein inhibits the respiratory burst in Kupffer cells. Cell Microbiol. 2007;9(11):2610–2628.10.1111/cmi.2007.9.issue-11
   PubMed Web of Science ®Google Scholar
• Steers N, Schwenk R, Bacon DJ, et al. The immune status of Kupffer cells profoundly influences their responses to infectious Plasmodium berghei sporozoites. Eur J Immunol. 2005;35(8):2335–2346.10.1002/(ISSN)1521-4141
   PubMed Web of Science ®Google Scholar
• Besnard AG, Guabiraba R, Niedbala W, et al. IL-33-mediated protection against experimental cerebral malaria is linked to induction of type 2 innate lymphoid cells, M2 macrophages and regulatory T cells. PLoS Pathog. 2015;11(2):e1004607.10.1371/journal.ppat.1004607
   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):1633–1641.10.1084/jem.172.6.1633
   PubMed Web of Science ®Google Scholar
• Roussilhon C, Bang G, Bastaert F, et al. The antimicrobial molecule trappin-2/elafin has anti-parasitic properties and is protective in vivo in a murine model of cerebral malaria. Sci Rep. 2017;7:42243.10.1038/srep42243
   PubMed Web of Science ®Google Scholar
• Stegmann KA, De Souza JB, Riley EM. IL-18-induced expression of high-affinity IL-2R on murine NK cells is essential for NK-cell IFN-gamma production during murine Plasmodium yoelii infection. Eur J Immunol. 2015;45(12):3431–3440.10.1002/eji.201546018
   PubMed Web of Science ®Google Scholar
• Mota MM, Brown KN, Holder AA, et al. Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infect Immun. 1998;66(9):4080–4086.
   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 Nat Acad Sci. 2007;104(6):1919–1924.10.1073/pnas.0608745104
   PubMed Web of Science ®Google Scholar
• Ayi K, Lu Z, Serghides L, et al. CD47-SIRPalpha interactions regulate macrophage uptake of Plasmodium falciparum-infected erythrocytes and clearance of malaria in vivo. Infect Immun. 2016;84(7):2002–2011.10.1128/IAI.01426-15
   PubMed Web of Science ®Google Scholar
• Park DW, Lee HJ, Park CW, et al. Peripheral blood NK cells reflect changes in decidual NK cells in women with recurrent miscarriages. Am J Reprod Immunol. 2010;63(2):173–180.10.1111/j.1600-0897.2009.00777.x
   PubMed Web of Science ®Google Scholar
• Lash GE, Robson SC, Bulmer JN. Review: functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta. 2010;31(Suppl):S87–S92.10.1016/j.placenta.2009.12.022
   PubMedGoogle Scholar
• Poli A, Michel T, Thérésine M, et al. CD56bright natural killer (NK) cells: an important NK cell subset. Immunology. 2009;126(4):458–465.10.1111/imm.2009.126.issue-4
   PubMed Web of Science ®Google Scholar
• Lanier LL, Le AM, Civin CI, et al. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol. 1986;136(12):4480–4486.
   PubMed Web of Science ®Google Scholar
• Ritz J, Campen TJ, Schmidt RE, et al. Analysis of T-cell receptor gene rearrangement and expression in human natural killer clones. Science. 1985;228(4707):1540–1543.10.1126/science.2409597
   PubMed Web of Science ®Google Scholar
• Bellora F, Castriconi R, Dondero A, et al. Human NK cells and NK receptors. Immunol Lett. 2014;161(2):168–173.10.1016/j.imlet.2013.12.009
   PubMed Web of Science ®Google Scholar
• Bao SH, Shuai W, Tong J, et al. Increased expression of Toll-like receptor 3 in decidual natural killer cells of patients with unexplained recurrent spontaneous miscarriage. Eur J Obstet Gynecol Reprod Biol. 2012;165(2):326–330.10.1016/j.ejogrb.2012.08.005
   PubMed Web of Science ®Google Scholar
• Manaster I, Mandelboim O. The unique properties of human NK cells in the uterine mucosa. Placenta 2008;29 Suppl A:60–66.10.1016/j.placenta.2007.10.006
   Google Scholar
• Roetynck S, Baratin M, Vivier ÉricE, et al. NK cells and innate immunity to malaria. Med Sci. 2006;22(8–9):739–744.10.1051/medsci/20062289739
   Google Scholar
• Schmidt S, Tramsen L, Lehrnbecher T. Natural ailler cells in antifungal immunity. Front Immunol. 2017;8:e711.10.3389/fimmu.2017.01623
   PubMed Web of Science ®Google Scholar
• Ding H, Yang X, Wei Y. Fusion proteins of NKG2D/NKG2DL in cancer immunotherapy. Int J Mol Sci. 2018;19(1).
   Web of Science ®Google Scholar
• Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Trans Med. 2009; 1 (6):6ra14.
   PubMed Web of Science ®Google Scholar
• Yindom LM, Forbes R, Aka P, et al. Killer-cell immunoglobulin-like receptors and malaria caused by Plasmodium falciparum in The Gambia. Tissue Antigens. 2012;79(2):104–113.10.1111/tan.2012.79.issue-2
   PubMedGoogle Scholar
• Luty AJ, Lell B, Schmidt-Ott R, et al. Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis. 1999;179(4):980–988.10.1086/jid.1999.179.issue-4
   PubMed Web of Science ®Google Scholar
• Ojo-Amaize EA, Vilcek J, Cochrane AH, et al. Plasmodium berghei sporozoites are mitogenic for murine T cells, induce interferon, and activate natural killer cells. J Immunol. 1984;133(2):1005–1009.
   PubMed Web of Science ®Google Scholar
• Baratin M, Roetynck S, Lepolard C, et al. Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc Nat Acad Sci. 2005;102(41):14747–14752.10.1073/pnas.0507355102
   PubMed Web of Science ®Google Scholar
• Horowitz A, Behrens RH, Okell L, et al. NK cells as effectors of acquired immune responses: effector CD4+ T cell-dependent activation of NK cells following vaccination. J Immunol. 2010;185(5):2808–2818.10.4049/jimmunol.1000844
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas K, Eleme K, McQueen KL, et al. Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J Immunol. 2003;171(10):5396–5405.10.4049/jimmunol.171.10.5396
   PubMed Web of Science ®Google Scholar
• Baratin M, Roetynck S, Pouvelle B, et al. Dissection of the role of PfEMP1 and ICAM-1 in the sensing of Plasmodium falciparum-infected erythrocytes by natural killer cells. PLoS ONE. 2007;2(2):e228.10.1371/journal.pone.0000228
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas K, Riley EM. Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol. 2002;169(6):2956–2963.10.4049/jimmunol.169.6.2956
   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 Nat Acad Sci. 2014;111(4):1479–1484.10.1073/pnas.1323318111
   PubMed Web of Science ®Google Scholar
• Patel SS, Wacholtz MC, Duby AD, et al. Analysis of the functional capabilities of CD3+CD4-CD8- and CD3+CD4+CD8+ human T cell clones. J Immunol. 1989;143(4):1108–1117.
   PubMed Web of Science ®Google Scholar
• Goodier M, Fey P, Eichmann K, et al. Human peripheral blood gamma delta T cells respond to antigens of Plasmodium falciparum. Int Immunol. 1992;4(1):33–41.10.1093/intimm/4.1.33
   PubMed Web of Science ®Google Scholar
• Ho M, Webster HK, Tongtawe P, et al. Increased gamma delta T cells in acute Plasmodium falciparum malaria. Immunol Lett. 1990;25(1–3):139–141.10.1016/0165-2478(90)90105-Y
   PubMed Web of Science ®Google Scholar
• Langhorne J, Goodier M, Behr C, et al. Is there a role for gamma delta T cells in malaria? Immunol Today. 1992;13(8):298–300.10.1016/0167-5699(92)90041-5
   PubMedGoogle Scholar
• Schofield L, Ioannidis LJ, Karl S, et al. Synergistic effect of IL-12 and IL-18 induces TIM3 regulation of gammadelta T cell function and decreases the risk of clinical malaria in children living in Papua New Guinea. BMC Med. 2017;15(1):114.10.1186/s12916-017-0883-8
   PubMedGoogle Scholar
• Salmon D, Vilde JL, Andrieu B, et al. Role of immune serum and complement in stimulation of the metabolic burst of human neutrophils by Plasmodium falciparum. Infect Immun. 1986;51(3):801–806.
   PubMed Web of Science ®Google Scholar
• McCall MB, Netea MG, Hermsen CC, et al. Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol. 2007;179(1):162–171.10.4049/jimmunol.179.1.162
   PubMed Web of Science ®Google Scholar
• Leifer CA, Kennedy MN, Mazzoni A, et al. TLR9 is localized in the endoplasmic reticulum prior to stimulation. J Immunol. 2004;173(2):1179–1183.10.4049/jimmunol.173.2.1179
   PubMed Web of Science ®Google Scholar
• Chockalingam A, Brooks JC, Cameron JL, et al. TLR9 traffics through the Golgi complex to localize to endolysosomes and respond to CpG DNA. Immunol Cell Biol. 2009;87(3):209–217.10.1038/icb.2008.101
   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):19–25.10.1084/jem.20041836
   PubMed Web of Science ®Google Scholar
• Franklin BS, Parroche P, Ataide MA, et al. Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Nat Acad Sci. 2009;106(14):5789–5794.10.1073/pnas.0809742106
   PubMed Web of Science ®Google Scholar
• Torgler R, Bongfen SE, Romero JC, et al. Sporozoite-mediated hepatocyte wounding limits Plasmodium parasite development via MyD88-mediated NF-kappa B activation and inducible NO synthase expression. J Immunol. 2008;180(6):3990–3999.10.4049/jimmunol.180.6.3990
   PubMed Web of Science ®Google Scholar
• Liehl P, Zuzarte-Luís V, Chan J, et al. Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat Med. 2014;20(1):47–53.10.1038/nm.3424
   PubMed Web of Science ®Google Scholar
• Ocaña-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med. 2003;197(2):143–151.10.1084/jem.20021072
   PubMed Web of Science ®Google Scholar
• Rocha BC, Marques PE, Leoratti FMS, et al. Type I interferon transcriptional signature in neutrophils and low-density granulocytes are associated with tissue damage in malaria. Cell Rep. 2015;13(12):2829–2841.10.1016/j.celrep.2015.11.055
   PubMed Web of Science ®Google Scholar