Early Interactions Between Blood-Stage Plasmodium Parasites and the Immune System
Abstract
Accumulating evidence provides strong support for the importance of innate immunity in shaping the subsequent adaptive immune response to blood-stage Plasmodium parasites, the causative agents of malaria. Early interactions between blood-stage parasites and cells of the innate immune system, including dendritic cells, monocytes/macrophages, natural killer (NK) cells, NKT cells, and γδ T cells, are important in the timely control of parasite replication and in the subsequent elimination and resolution of the infection. The major role of innate immunity appears to be the production of immunoregulatory cytokines, such as interleukin (IL)-12 and interferon (IFN)-γ, which are critical for the development of type 1 immune responses involving CD4+ Th1 cells, B cells, and effector cells which mediate cell-mediated and antibody-dependent adaptive immune responses. In addition, it is likely that cells of the innate immune system, especially dendritic cells, serve as antigen-presenting cells.Here, we reviewrecent data fromrodentmodels of blood-stagemalaria and from human studies, and outline the early interactions of infected red blood cells with the innate immune system. We compare and contrast the results derived from studies in infected laboratory mice and humans. These host species are sufficiently differentwith respect to the identity of the infecting Plasmodium species, the resulting pathologies, and immune responses, particularly where the innate immune response is concerned. The implications of these findings for the development of an effective and safemalaria vaccine are also discussed.
Keywords
Natural Killer Cell Plasmodium Falciparum Severe Malaria Human Natural Killer Cell Early InteractionPreview
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References
- 1.Ahlborg N, Ling IT, Howard W, Holder AA, Riley EM (2002) Protective immune responses to the 42-kilodalton (kDa) region of Plasmodium yoelii merozoite surface protein 1 are induced by the C-terminal 19-kDa region but not by the adjacent 33-kDa region. Infect Immun 70:820–825PubMedCrossRefGoogle Scholar
- 2.Ahvazi BC, Jacobs P, Stevenson MM (1995) Role of macrophage-derived nitric oxide in suppression of lymphocyte proliferation during blood-stage malaria. J Leukoc Biol 58:23–31PubMedGoogle Scholar
- 3.Aitman TJ, Cooper LD, Norsworthy PJ, Wahid FN, Gray JK, Curtis BR, McKeigue PM, Kwiatkowski D, Greenwood BM, Snow RW, Hill AV, Scott J (2000) Malaria susceptibility and CD36 mutation. Nature 405:1015–1016PubMedCrossRefGoogle Scholar
- 4.Alli RS, Khar A (2004) Interleukin-12 secreted by mature dendritic cells mediates activation of NK cell function. FEBS Lett 559:71–76PubMedCrossRefGoogle Scholar
- 5.Angeli V, Hammad H, Staels B, Capron M, Lambrecht BN, Trottein F (2003) Peroxisome proliferator-activated receptor gamma inhibits the migration of dendritic cells: consequences for the immune response. J Immunol 170:5295–5301PubMedGoogle Scholar
- 6.Angus BJ, Chotivanich K, Udomsangpetch R, White NJ (1997) In vivo removal of malaria parasites from red blood cells without their destruction in acute falciparum malaria. Blood 90:2037–2040PubMedGoogle Scholar
- 7.Artavanis-Tsakonas K, Riley EM(2002) Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169:2956–2963PubMedGoogle Scholar
- 8.Artavanis-Tsakonas K, Eleme K, McQueen KL, Cheng NW, Parham P, Davis DM, Riley EM (2003) Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J Immunol 171:5396–5405PubMedGoogle Scholar
- 9.Artavanis-Tsakonas K, Tongren JE, Riley EM (2003) The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol 133:145–152PubMedCrossRefGoogle Scholar
- 10.Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu Y-J, Pulendran B, Palucka K (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811PubMedCrossRefGoogle Scholar
- 11.Beeson JG, Brown GV, Molyneux ME, Mhango C, Dzinjalamala F, Rogerson SJ (1999) Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties. J Infect Dis 180:464–472PubMedCrossRefGoogle Scholar
- 12.Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, Lawson AM, Molyneux ME, Brown GV (2000) Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6:86–90PubMedCrossRefGoogle Scholar
- 13.Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Ann Rev Immunol 17:71–76CrossRefGoogle Scholar
- 14.Bruna-Romero O, Schmieg J, Del Val M, Buschle M, Tsuji M (2003) The dendritic cell-specific chemokine, dendritic cell-derived CC chemokine 1, enhances protective cell-mediated immunity to murine malaria. J Immunol 170:3195–3203PubMedGoogle Scholar
- 15.Bukowski JF, Morita CT, Brenner MB (1999) Human gamma delta T cells recognize alkylamines derived from microbes, edible plants, and tea: implications for innate immunity. Immunity 11:57–65PubMedCrossRefGoogle Scholar
- 16.Bull PC, Lowe BS, Kortok M, Marsh K (1999) Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect Immun 67:733–739PubMedGoogle Scholar
- 17.Bull PC, Kortok M, Kai O, Ndungu F, Ross A, Lowe BS, Newbold CI, Marsh K (2000) Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. J Infect Dis 182:252–259PubMedCrossRefGoogle Scholar
- 18.Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, Ndungu F, Snow RW, Marsh K (2002) Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children. J Infect Dis 185:1688–1691PubMedCrossRefGoogle Scholar
- 19.Carayannopoulos LN and Yokoyama WM (2004) Recognition of infected cells by natural killer cells. Curr Opin Immunol 16:26–33PubMedCrossRefGoogle Scholar
- 20.Castriconi R, Della Chiesa M, Moretta A (2004) Shaping of adaptive immunity by innate interactions. C R Biol 327:533–537PubMedGoogle Scholar
- 21.Cavanagh DR, Elhassan IM, Roper C, Robinson VJ, Giha H, Holder AA, Hviid L, Theander TG, Arnot DE, McBride JS (1998) A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. J Immunol 161:347–359PubMedGoogle Scholar
- 22.Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, Colonna M (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 5:919–923PubMedGoogle Scholar
- 23.Chattopadhyay R, Sharma A, Srivastava VK, Pati SS, Sharma SK, Das BS, Chitnis CE (2003) Plasmodium falciparum Infection Elicits Both Variant-Specific and Cross-Reactive Antibodies against Variant Surface Antigens. Infect. Immun. 71:597–604PubMedCrossRefGoogle Scholar
- 24.Chizzolini C, Grau GE, Geinoz A, Schrijvers D (1990) T lymphocyte interferon-gamma production induced by Plasmodium falciparum antigen is high in recently infected non-immune and low in immune subjects. Clin Exp Immunol 79:95–99PubMedGoogle Scholar
- 25.Chotivanich K, Udomsangpetch R, Dondorp A, Williams T, Angus B, Simpson JA, Pukrittayakamee S, Looareesuwan S, Newbold CI, White NJ (2000) The mechanisms of parasite clearance after antimalarial treatment of Plasmodium falciparum malaria. J Infect Dis 182:629–633PubMedCrossRefGoogle Scholar
- 26.Chotivanich K, Udomsangpetch R, McGready R, Proux S, Newton P, Pukrittayakamee S, Looareesuwan S, White NJ (2002) Central role of the spleen in malaria parasite clearance. J Infect Dis 185:1538–1541PubMedCrossRefGoogle Scholar
- 27.Choudhury HR, Sheikh NA, Bancroft GJ, Katz DR, de Souza JB (2000) Early non-specific immune response and immunity to blood-stage nonlethal Plasmodium yoelii malaria. Infect Immun 68:6127–6132PubMedCrossRefGoogle Scholar
- 28.Colucci F, Caligiuri MA, Di Santo JP (2003) What does it take to make a natural killer? Nat Rev Immunol 3:413–425PubMedCrossRefGoogle Scholar
- 29.Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, Carson WE, Caligiuri MA (2001) Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood 97:3146–3151PubMedCrossRefGoogle Scholar
- 30.Cooper, MA, Bush JE, Fehniger TA, VanDeusen JB, Waite RE, Liu Y, Aguila HL, Caligiuri MA (2002) In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100:3633–3638PubMedCrossRefGoogle Scholar
- 31.Conway DJ, Cavanagh DR, Tanabe K, Roper C, Mikes ZS, Sakihama N, Bojang KA, Oduola AM, Kremsner PG, Arnot DE, Greenwood BM, McBride JS (2000) A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses. Nat Med 6:689–692PubMedCrossRefGoogle Scholar
- 32.Day N, Pham T, Phan T, Dinh X, Pham P, Lyy V, Tran T, Nguyen T, Bethell D, Nguyan H, Tran T, White N (1996) Clearance kinetics of parasites and pigment-containing leukocytes in severe malaria. Blood 88:4694–4700PubMedGoogle Scholar
- 33.Day NP, Hien TT, Schollaardt T, Loc PP, Chuong LV, Chau TT, Mai NT, Phu NH, Sinh DX, White NJ, Ho M (1999) The prognostic and pathophysiologic role of pro-and antiinflammatory cytokines in severe malaria. J Infect Dis 180:1288–1297PubMedCrossRefGoogle Scholar
- 34.de Souza, JB, Williamson KH, Otani T, Playfair JH (1997) Early gamma interferon responses in lethal and nonlethal murine blood-stage malaria. Infect Immun 65(5):1593–1598PubMedGoogle Scholar
- 35.de Souza JB, Riley EM (2002) Cerebral malaria: the contribution of studies in animals to our understanding of immunopathogenesis. Microbes Infect 4:297–300Google Scholar
- 36.Diebold SS, Montoya M, Unger H, Alexopoulou L, Roy P, Haswell LE, Al-Shamkhani A, Flavell R, Borrow P, Sousa CRe (2003) Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424:324–328PubMedCrossRefGoogle Scholar
- 37.Dieli F, Troye-Blomberg M, Farouk SE, Sirecil G, Salerno A (2001) Biology of gammadelta T cells in tuberculosis and malaria. Curr Mol Med 1:437–446PubMedCrossRefGoogle Scholar
- 38.Dodoo D, Theander TG, Kurtzhals JA, Koram K, Riley E, Akanmori BD, Nkrumah FK, Hviid L (1999) Levels of antibody to conserved parts of Plasmodium falciparum merozoite surface protein 1 in Ghanaian children are not associated with protection from clinical malaria. Infect Immun 67:2131–2137PubMedGoogle Scholar
- 39.Dodoo D, Omer FM, Todd J, Akanmori BD, Koram KA, Riley EM (2002) Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J Infect Dis 185:971–979PubMedCrossRefGoogle Scholar
- 40.Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J (2000) BDCA-2, BDCA-3, and BDCA-4: Three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 165:6037–6046PubMedGoogle Scholar
- 41.Edwards AD, Manickasingham SP, Sporri R, Diebold SS, Schulz O, Sher A, Kaisho T, Akira S, Reis e Sousa C (2002) Microbial recognition via Toll-like receptor-dependent and-independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J Immunol 169:3652–3660PubMedGoogle Scholar
- 42.Facchetti F, Candiago E, Vermi W (1999) Plasmacytoid monocytes express IL3-receptor alpha and differentiate into dendritic cells. Histopathology 35:88–89PubMedCrossRefGoogle Scholar
- 43.Facchetti F, Vermi W, Mason D, Colonna M (2003) The plasmacytoid monocyte/interferon producing cells. Virchows Arch 443:703–717PubMedCrossRefGoogle Scholar
- 44.Farouk SE, Mincheva-Nilsson L, Krensky AM, Dieli F, Troye-Blomberg M (2004) Gamma delta T cells inhibit in vitro growth of the asexual blood stages of Plasmodium falciparum by a granule exocytosis-dependent cytotoxic pathway that requires granulysin. Eur J Immunol 34:2248–2256PubMedCrossRefGoogle Scholar
- 45.Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Munz C (2002) Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 195:343–351PubMedCrossRefGoogle Scholar
- 46.Ferlazzo G, Morandi B, D’Agostino A, Meazza R, Melioli G, Moretta A, Moretta L (2003) The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells. Eur J Immunol 33:306–313PubMedCrossRefGoogle Scholar
- 47.Ferlazzo G, Munz C (2004) NK cell compartments and their activation by dendritic cells. J Immunol 172:1333–1339PubMedGoogle Scholar
- 48.Ferlazzo G, Thomas D, Lin S-L, Goodman K, Morandi B, Muller WA, Moretta A, Munz C (2004) The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol 172:1455–1462PubMedGoogle Scholar
- 49.Ferrick DA, King DP, Jackson KA, Braun RK, Tam S, Hyde DM, Beaman BL (2000) Intraepithelial gamma delta T lymphocytes: sentinel cells at mucosal barriers. Springer Semin Immunopathol 22:283–296PubMedCrossRefGoogle Scholar
- 50.Fortin A, Stevenson MM, Gros P (2002) Susceptibility to malaria as a complex trait: huge pressure from a tiny creature. Hum Mol Genetics 11:2469–2478Google Scholar
- 51.Franks S, Baton L, Tetteh K, Tongren E, Dewin D, Akanmori BD, Koram KA, Ranford-Cartwright L, Riley EM (2003) Genetic diversity and antigenic polymorphism in Plasmodium falciparum: extensive serological cross-reactivity between allelic variants of merozoite surface protein 2. Infect Immun 71:3485–3495PubMedCrossRefGoogle Scholar
- 52.Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511PubMedGoogle Scholar
- 53.Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G (2002) Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195:327–333PubMedCrossRefGoogle Scholar
- 54.Godfrey DI, MacDonald HR, Kronenberg M, Smyth MJ, Van Kaer L (2004) NKT cells: what’s in a name? Nat Rev Immunol 4:231–237PubMedCrossRefGoogle Scholar
- 55.Gordon S (1998) The role of the macrophage in immune regulation. Res Immunol 149:685–688PubMedGoogle Scholar
- 56.Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35PubMedCrossRefGoogle Scholar
- 57.Granucci F, Zanoni I, Pavelka N, Van Dommelen SL, Andoniou CE, Belardelli F, Degli Esposti MA, Ricciardi-Castagnoli P (2004) A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J Exp Med 200:287–295PubMedCrossRefGoogle Scholar
- 58.Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C (1999) Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5:340–343PubMedGoogle Scholar
- 59.Hansen DS, Siomos MA, Buckingham L, Scalzo AA, Schofield L (2003) Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18:391–402PubMedCrossRefGoogle Scholar
- 60.Hansen DS, Siomos MA, De Koning-Ward T, Buckingham L, Crabb BS, Schofield L (2003) CD1d-restricted NKT cells contribute to malarial splenomegaly and enhance parasite-specific antibody responses. Eur J Immunol 33:2588–2598PubMedCrossRefGoogle Scholar
- 61.Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, Smyth MJ, Chambers BJ (2004) NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 172:123–129PubMedGoogle Scholar
- 62.Hayday AC (2000) Gamma delta cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975–1026PubMedCrossRefGoogle Scholar
- 63.Hedges JF, Graff JC, Jutila MA (2003) Transcriptional profiling of gamma delta T cells. J Immunol 171:4959–4964PubMedGoogle Scholar
- 64.Hensmann M, Kwiatkowski D (2001) Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun 69:2364–2371PubMedCrossRefGoogle Scholar
- 65.Hermsen CC, Konijnenberg Y, Mulder L, Loe C, van Deuren M, van der Meer JW, van Mierlo GJ, Eling WM, Hack CE, Sauerwein RW (2003) Circulating concentrations of soluble granzyme A and B increase during natural and experimental Plasmodium falciparum infections. Clin Exp Immunol 132:467–472PubMedCrossRefGoogle Scholar
- 66.Heufler C, Koch F, Stanzl U, Topar G, Wysocka M, Trinchieri G, Enk A, Steinman RM, Romani N, Schuler G (1996) Interleukin-12 is produced by dendritic cells and mediates T helper 1 development as well as interferon-gamma production by T helper 1 cells. Eur J Immunol 26:659–668PubMedGoogle Scholar
- 67.Hill AV (2001) The genomics and genetics of human infectious disease susceptibility. Annu Rev Genomics Hum Genet 2:373–400PubMedCrossRefGoogle Scholar
- 68.Ho LP, Urban BC, Jones L, Ogg GS, McMichael AJ (2004) CD4-CD8alphaalpha subset of CD1d-restricted NKT cells controls T cell expansion. J Immunol 172:7350–7358PubMedGoogle Scholar
- 69.Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI (2004) Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci U S A 101:11129–11134PubMedCrossRefGoogle Scholar
- 70.Huang Q, Liu D, Majewski P, Schulte LC, Korn JM, Young RA, Lander ES, Hacohen N. (2001) The plasticity of dendritic cell response to pathogens and their components. Science 294:870–875PubMedGoogle Scholar
- 71.Hugosson E, Montgomery SM, Premji Z, Troye-Blomberg M, Bjorkman A (2004) Higher IL-10 levels are associated with less effective clearance of Plasmodium falciparum parasites. Parasite Immunol 26:111–117PubMedCrossRefGoogle Scholar
- 72.Hviid L, Akanmori BD, Loizon S, Kurtzhals JA, Ricke CH, Lim A, Koram KA, Nkrumah FK, Mercereau-Puijalon O, Behr C (2000) High frequency of circulating gamma delta T cells with dominance of the v(delta)1 subset in a healthy population. Int Immunol 12:797–805PubMedCrossRefGoogle Scholar
- 73.Hviid L, Kurtzhals JAL, Adabayeri V, Loizon S, Kemp K, Goka BQ, Lim A, Mercereau-Puijalon O, Akanmori BD, Behr C (2001) Perturbation and proinflammatory type activation of Vδ1+γδ T cells in african children with Plasmodium falciparum malaria. Infect. Immun. 69:3190–3196PubMedCrossRefGoogle Scholar
- 74.Ing R, Gros P, Stevenson MM (2004) Interleukin 15 enhances innate and adaptive immune responses to blood-stage malaria infection in mice. (submitted)Google Scholar
- 75.Jakobsen PH, McKay V, N’Jie R, Olaleye BO, D’Alessandro U, Bendtzen K, Schousboe I, Greenwood BM (1996) Soluble products of inflammatory reactions are not induced in children with asymptomatic Plasmodium falciparum infections. Clin Exp Immunol 105:69–73PubMedCrossRefGoogle Scholar
- 76.Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, Olivier M (2004) Hemozoininducible proinflammatory events in vivo: potential role in malaria infection. J Immunol 172:3101–3110PubMedGoogle Scholar
- 77.Jensen AT, Magistrado P, Sharp S, Joergensen L, Lavstsen T, Chiucchiuini A, Salanti A, Vestergaard LS, Lusingu JP, Hermsen R, Sauerwein R, Christensen J, Nielsen MA, Hviid L, Sutherland C, Staalsoe T, Theander TG (2004) Plasmodium falciparum associated with severe childhoodmalaria preferentially expresses PfEMP1 encoded by group A var genes. J Exp Med 199:1179–1190PubMedCrossRefGoogle Scholar
- 78.Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T, Suzuki T, Miyagi T, Hayashi N (2003) Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J Immunol 171:5423–5429PubMedGoogle Scholar
- 79.Kaestli M, Cortes A, Lagog M, Ott M, Beck HP (2004) Longitudinal assessment of Plasmodium falciparum var gene transcription in naturally infected asymptomatic children in Papua New Guinea. J Infect Dis 189:1942–1951PubMedCrossRefGoogle Scholar
- 80.Kinyanjui SM, Bull P, Newbold CI, Marsh K (2003) Kinetics of antibody responses to Plasmodium falciparum-infected erythrocyte variant surface antigens. J Infect Dis 187:667–674PubMedCrossRefGoogle Scholar
- 81.Kohrgruber N, Halanek N, Groger M, Winter D, Rappersberger K, Schmitt-Egenolf M, Stingl G, Maurer D (1999) Survival, maturation, and function of CD11c-and CD11c+ peripheral blood dendritic cells are differentially regulated by cytokines. J Immunol 163:3250–3259PubMedGoogle Scholar
- 82.Kraemer SM, Smith JD (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol Microbiol 50:1527–1538PubMedCrossRefGoogle Scholar
- 83.Krug A, Towarowski A, Britsch S, Rothenfusser S, Hornung V, Bals R, Giese T, Engelmann H, Endres S, Krieg AM, Hartmann G (2001) Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur J Immunol 31:3026–3037PubMedGoogle Scholar
- 84.Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 55:673–707PubMedCrossRefGoogle Scholar
- 85.Langhorne J, Morris-Jones S, Casabo LG, Goodier M (1994) The response of γδT cells in malaria infections Res Immunol 145:429–436PubMedGoogle Scholar
- 86.Langhorne J, Quin SJ, Sanne LA (2002) Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem Immunol 80:204–228PubMedGoogle Scholar
- 87.Lauwerys BR, Garot N, Renauld J-C, Houssiau FA (2000) Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18. J Immunol 165:1847–1853PubMedGoogle Scholar
- 88.Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2:27PubMedCrossRefGoogle Scholar
- 89.Leisewitz AL, Rockett KA, Gumede B, Jones M, Urban B, Kwiatkowski DP (2004) Response of the splenic dendritic cell population to malaria infection. Infect Immun 72:4233–4239PubMedCrossRefGoogle Scholar
- 90.Litinskiy MB, Nardelli B,, Hilbert DM, He B, Schaffer A, Casali P, Cerutti A. (2002) DCs induce CD40-independent immunoglobulin class switching through BlyS and APRIL. Nat Immunol 3:822–829PubMedCrossRefGoogle Scholar
- 91.Loza MJ, Perussia B (2001) Final steps of natural killer cell maturation: a model for type1-type2 differentiation. Nat Immunol 2(10): 917–924PubMedCrossRefGoogle Scholar
- 92.Luty AJ, Lell B, Schmidt-Ott R, Lehman LG, Luckner D, Greve B, Matousek P, Herbich K, Schmid D, Migot-Nabias F, Deloron P, Nussenzweig RS, Kremsner PG (1999) Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis 179:980–988PubMedCrossRefGoogle Scholar
- 93.Luty AJ, Perkins DJ, Lell B, Schmidt-Ott R, Lehman LG, Luckner D, Greve B, Matousek P, Herbich K, Schmid D, Weinberg JB, Kremsner PG (2000) Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect Immun 68:3909–3915PubMedCrossRefGoogle Scholar
- 94.Luyendyk J, Olivas OR, Ginger LA, Avery AC (2002) Antigen-presenting cell function during Plasmodium yoelii infection. Infect Immun 70:2941–2949PubMedCrossRefGoogle Scholar
- 95.Lyke KE, Diallo DA, Dicko A, Kone A, Coulibaly D, Guindo A, Cissoko Y, Sangare L, Coulibaly S, Dakuo B, Taylor TE, Doumbo OK, Plowe CV (2003) Association of the intraleukocytic Plasmodium falciparum malaria pigment with disease severity, clinical manifestations, and prognosis in severe malaria. Am J Trop Med Hyg 69:253–259PubMedGoogle Scholar
- 96.Mahnke K, Qian Y, Knop J, Enk AH (2003) Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood 101:4862–4869PubMedCrossRefGoogle Scholar
- 97.Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P (2003) Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 171:2366–2373PubMedGoogle Scholar
- 98.Malaguarnera L, Pignatelli S, Simpore J, Malaguarnera M, Musumeci S (2002) Plasma levels of interleukin-12 (IL-12), interleukin-18 (IL-18) and transforming growth factor beta (TGF-beta) in Plasmodium falciparum malaria. Eur Cytokine Netw 13:425–430PubMedGoogle Scholar
- 99.Martiney JA, Sherry B, Metz CN, Espinoza M, Ferrer AS, Calandra T, Broxmeyer HE, Bucala R (2000) Macrophage migration inhibitory factor release by macrophages after ingestion of Plasmodium chabaudi-infected erythrocytes: possible role in the pathogenesis of malarial anemia. Infect Immun 68:2259–2267PubMedCrossRefGoogle Scholar
- 100.McGregor IA (1964) The passive transfer of human malarial immunity. Am J Trop Med Hyg 13:237–239.PubMedGoogle Scholar
- 101.Mestas J, Hughes CCW (2004) Of mice and not men: differences between mouse and human immunology J Immunol 172:2731–2738PubMedGoogle Scholar
- 102.Mohan K, Moulin P, Stevenson MM (1997) Natural killer cell cytokine production, not cytotoxicity, contributes to resistance against blood-stage Plasmodium chabaudi AS infection. J Immunol 159:4990–4998PubMedGoogle Scholar
- 103.Mohan K, Stevenson MM (1998) Acquired immunity to asexual blood-stages of malaria. In Malaria: Parasite Biology, Pathogenesis and Protection. (Ed. I.W. Sherman). ASM Press, Washington, DC, p. 467–493Google Scholar
- 104.Mohan K, Sam H, Stevenson, MM (1999) Therapy with a combination of low dose IL-12 and chloroquine completely cures primary blood-stage malaria, prevents severe anemia and induces immunity to reinfection. Infect. Immun. 67:513–519PubMedGoogle Scholar
- 105.Morakote N, Justus DE (1988) Immunosuppression inmalaria: effect of hemozoin produced by Plasmodium berghei and Plasmodium falciparum. Int Arch Allergy Appl Immunol 86:28–34PubMedGoogle Scholar
- 106.Moretta A (2002) Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2:957–964PubMedCrossRefGoogle Scholar
- 107.Nagamine Y, Hayano M, Kashiwamura S, Okamura H, Nakanishi K, Krudsod S, Wilairatana P, Looareesuwan S, Kojima S (2003) Involvement of interleukin-18 in severe Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 97:236–241PubMedCrossRefGoogle Scholar
- 108.Ndungu FM, Bull PC, Ross A, Lowe BS, Kabiru E, Marsh K (2002) Naturally acquired immunoglobulin (Ig)G subclass antibodies to crude asexual Plasmodium falciparum lysates: evidence for association with protection for IgG1 and disease for IgG2. Parasite Immunol 24:77–82PubMedCrossRefGoogle Scholar
- 109.Nencioni A, Grunebach F, Zobywlaski A, Denzlinger C, Brugger W, Brossart P (2002) Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor gamma. J Immunol 169:1228–1235PubMedGoogle Scholar
- 110.Newbold C, Warn P, Black G, Berendt A, Craig A, Snow B, Msobo M, Peshu N, Marsh K (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57:389–398PubMedGoogle Scholar
- 111.Nguyen P, Day N, Pram T, Ferguson D, White N (1995) Intraleukocytic malaria pigment and prognosis in severe malaria. Trans R Soc Trop Med Hyg 89:200–204PubMedGoogle Scholar
- 112.Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wie X-Q, Liew FY, Caligiuri MA, Durbin JE, Biron CA (2002) Coordinated and distinct roles for IFN-αβ, IL-12 and IL-15 regulation of NK cell responses to viral infection. J Immunol 169:4279–4287PubMedGoogle Scholar
- 113.Nielsen MA, Vestergaard LS, Lusingu J, Kurtzhals JA, Giha HA, Grevstad B, Goka BQ, Lemnge MM, Jensen JB, Akanmori BD, Theander TG, Staalsoe T, Hviid L (2004) Geographical and temporal conservation of antibody recognition of Plasmodium falciparum variant surface antigens. Infect Immun 72:3531–3535PubMedCrossRefGoogle Scholar
- 114.Ocana-Morgner C, Mota MM, Rodriguez A (2003) Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 197:143–151PubMedCrossRefGoogle Scholar
- 115.Ohteki T, Suzue K, Maki C, Ota T, Koyasu S ( 2001) Critical role of IL-15: IL-15R for antigen-presenting cell functions in the innate immune response. Nat Immunol 2(12): 1138–1143PubMedCrossRefGoogle Scholar
- 116.Orago AS, Facer CA (1991) Cytotoxicity of human natural killer (NK) cell subsets for Plasmodium falciparum erythrocytic schizonts: stimulation by cytokines and inhibition by neomycin. Clin Exp Immunol 86:22–29PubMedGoogle Scholar
- 117.Orengo AM, Carlo ED, Comes A, Fabbi M, Piazza T, Cilli M, Musiani P, Ferrini S (2003) Tumor cells engineered with IL-12 and IL-15 genes induce protective antibody responses in nude mice. J Immunol 171:569–575PubMedGoogle Scholar
- 118.Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, Marsh K, Roberts DJ (2001) Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci U S A 98:1805–1810PubMedCrossRefGoogle Scholar
- 119.Pain A, Urban BC, Kai O, Casals-Pascual C, Shafi J, Marsh K, Roberts DJ (2001) A non-sense mutation in CD36 gene is associated with protection from severe malaria. Lancet 357:1502–1503PubMedCrossRefGoogle Scholar
- 120.Pan PY, Gu P, Li Q, Xu D, Weber K, Chen SH (2004) Regulation of dendritic cell function by NK cells: mechanisms underlying the synergism in the combination therapy of IL-12 and 4-1BB activation. J Immunol 172:4779–4789PubMedGoogle Scholar
- 121.Patterson S, Robinson SP, English NR, Knight SC (1999) Subpopulations of peripheral blood dendritic cells show differential susceptibility to infection with a lymphotropic strain of HIV-1. Immunol Lett 66:111–116PubMedCrossRefGoogle Scholar
- 122.Peritt D, Robertson S, Gri G, Showe L, Aste-Amezaga M, Trinchieri G (1998) Differentiation of human NK cells into NK1 and NK2 subsets. J Immunol 161:5821–5824PubMedGoogle Scholar
- 123.Perkins DJ, Weinberg JB, Kremsner PG (2000) Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis 182:988–992PubMedCrossRefGoogle Scholar
- 124.Perry JA, Rush A, Wilson RJ, Olver CS, Avery AC (2004) Dendritic cells from malaria-infected mice are fully functional APC. J Immunol 172:475–482PubMedGoogle Scholar
- 125.Piccioli D, Sbrana S, Melandri E, Valiante NM (2002) Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 195:335–341PubMedCrossRefGoogle Scholar
- 126.Pichyangkul S, Yongvanitchit K, Kum-arb U, Hemmi H, Akira S, Krieg AM, Heppner DG, Stewart VA, Hasegawa H, Looareesuwan S, Shanks GD, Miller RS (2004) Malaria blood-stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J Immunol 172:4926–4933PubMedGoogle Scholar
- 127.Pouniotis DS, Proudfoot O, Bogdanoska V, Apostolopoulos V, Fifis T, Plebanski M (2004) Dendritic cells induce immunity and long-lasting protection against blood-stage malaria despite an in vitro parasite-induced maturation defect. Infect Immun 72:5331–5339PubMedCrossRefGoogle Scholar
- 128.Prlic M, Blazar BR, Farrar MA, Jameson SC (2003) In vivo survival and homeostatic proliferation of natural killer cells. J Exp Med 197(8): 967–976PubMedCrossRefGoogle Scholar
- 129.Recker M, Nee S, Bull PC, Kinyanjui S, Marsh K, Newbold C, Gupta S (2004) Transient cross-reactive immune responses can orchestrate antigenic variation in malaria. Nature 429:555–558PubMedCrossRefGoogle Scholar
- 130.Rhee MS, Akanmori BD, Waterfall M, Riley EM (2001) Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria. Clin Exp Immunol 126:503–510PubMedCrossRefGoogle Scholar
- 131.Rich SM, Ayala FJ (2000) Population structure and recent evolution of Plasmodium falciparum. PNAS 97:6994–7001PubMedCrossRefGoogle Scholar
- 132.Riley EM, Jakobsen PH, Allen SJ, Wheeler JG, Bennett S, Jepsen S, Greenwood BM (1991) Immune response to soluble exoantigens of Plasmodium falciparum may contribute to both pathogenesis and protection in clinical malaria: evidence from a longitudinal, prospective study of semi-immune African children. Eur J Immunol 21:1019–1025PubMedGoogle Scholar
- 133.Rogerson SJ, Tembenu R, Dobano C, Plitt S, Taylor TE, Molyneux ME (1999) Cytoadherence characteristics of Plasmodium falciparum-infected erythrocytes from Malawian children with severe and uncomplicated malaria. Am J Trop Med Hyg 61:467–472PubMedGoogle Scholar
- 134.Rowe A, Obeiro J, Newbold CI, Marsh K (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63:2323–2326PubMedGoogle Scholar
- 135.Rubinstein, MP, Kadima A.N, Salem ML, Nguyen CL, Gillanders WE, Cole DJ (2002). Systemic administration of IL-15 augments the antigen-specific primary CD8+ T cell response following vaccination with peptide-pulsed dendritic cells. J. Immunol. 169:4928–4935PubMedGoogle Scholar
- 136.Sam H, Stevenson MM (1999) In vivo IL-12 production and IL-12 receptors beta1 and beta2 mRNA expression in the spleen are differentially up-regulated in resistant B6 and susceptible A/J mice during early blood-stage Plasmodium chabaudi AS malaria. J Immunol 162:1582–1589PubMedGoogle Scholar
- 137.Sam H, Stevenson MM (1999) Early IL-12 p70, but not p40, production by splenic macrophages correlates with host resistance to blood-stage Plasmodium chabaudi AS malaria. Clin Exp Immunol 117:343–349PubMedCrossRefGoogle Scholar
- 138.Schellenberg JA, Newell JN, Snow RW, Mung’ala V, Marsh K, Smith PG, Hayes RJ (1998) An analysis of the geographical distribution of severe malaria in children in Kilifi District, Kenya. Int J Epidemiol 27:323–329PubMedCrossRefGoogle Scholar
- 139.Schmieg J, Gonzalez-Aseguinolaza G, Tsuji M (2003) The role of natural killer T cells and other T cell subsets against infection by the pre-erythrocytic stages of malaria parasites. Microbes Infect 5:499–506PubMedCrossRefGoogle Scholar
- 140.Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P (1992) Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 176:1033–1041PubMedCrossRefGoogle Scholar
- 141.Schwarzer E, Alessio M, Ulliers D, Arese P (1998) Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 66:1601–1606PubMedGoogle Scholar
- 142.Scorza T, Magez S, Brys L, De Baetselier P (1999) Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol 21:545–554PubMedCrossRefGoogle Scholar
- 143.Scragg IG, Hensmann M, Bate CA, Kwiatkowski D (1999) Early cytokine induction by Plasomodium falciparumis not classical endotoxin-like process.Eur J Immunol 29:2636–2644PubMedCrossRefGoogle Scholar
- 144.Seixas EMG, Langhorne J (1999) γδ T cells contribute to control of chronic parasitemia in Plasmodium chabaudi infections in mice. J Immunol 162:2837–2841PubMedGoogle Scholar
- 145.Seixas E, Cross C, Quin S, Langhorne J (2001) Direct activation of dendritic cells by the malaria parasite, Plasmodium chabaudi chabaudi. Eur J Immunol 31:2970–2978PubMedCrossRefGoogle Scholar
- 146.Shortman K, Liu YJ (2002) Mouse and human dendritic cell subtypes. Nat Rev Immunol 2:151–161PubMedCrossRefGoogle Scholar
- 147.Serghides I, Smith TG, Pater SN, Kain KC (2003) CD36 and malaria: friends or foes? Trend Parasitol 19:461–469Google Scholar
- 148.Skold M, Behar SM (2003) Role of CD1d-restricted NKT cells in microbial immunity. Infect Immun 71:5447–5455PubMedCrossRefGoogle Scholar
- 149.Skorokhod OA, Alessio M, Mordmuller B, Arese P, Schwarzer E (2004) Hemozoin (malaria pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J Immunol 173:4066–4074PubMedGoogle Scholar
- 150.Skov S, Bonyhadi M, Ødum N, Ledbetter JA (2000) IL-2 and IL-15 regulate CD154 expression on activated CD4 T cells. J Immunol 164:3500–3505PubMedGoogle Scholar
- 151.Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH (2000) Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 110:293–310PubMedCrossRefGoogle Scholar
- 152.Smith JD, Gamain B, Baruch DI, Kyes S (2001) Decoding the language of var genes and Plasmodium falciparum sequestration. Trends Parasitol 17:538–545PubMedGoogle Scholar
- 153.Smith T, Felger I, Tanner M, Beck HP (1999) Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg 93 Suppl 1:59–64PubMedGoogle Scholar
- 154.Snow RW, Schellenberg JR, Peshu N, Forster D, Newton CR, Winstanley PA, Mwangi I, Waruiru C, Warn PA, Newbold C, et al. (1993) Periodicity and space-time clustering of severe childhood malaria on the coast of Kenya. Trans R Soc Trop Med Hyg 87:386–390PubMedCrossRefGoogle Scholar
- 155.Snow RW, Bastos de Azevedo I, Lowe BS, Kabiru EW, Nevill CG, Mwankusye S, Kassiga G, Marsh K, Teuscher T (1994) Severe childhood malaria in two areas of markedly different falciparum transmission in east Africa. Acta Trop 57:289–300PubMedGoogle Scholar
- 156.Snow RW, Nahlen B, Palmer A, Donnelly CA, Gupta S, Marsh K (1998) Risk of severe malaria among African infants: direct evidence of clinical protection during early infancy. J Infect Dis 177:819–822PubMedCrossRefGoogle Scholar
- 157.Staalsoe T, Nielsen MA, Vestergaard LS, Jensen AT, Theander TG, Hviid L (2003) In vitro selection of Plasmodium falciparum 3D7 for expression of variant surface antigens associated with severe malaria in African children. Parasite Immunol 25:421–427PubMedCrossRefGoogle Scholar
- 158.Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685–711PubMedCrossRefGoogle Scholar
- 159.Stevenson MM, Skamene E (1985) Murine malaria: resistance of AXB/BXA recombinant inbred mice to Plasmodium chabaudi. Infect Immun 47:452–456PubMedGoogle Scholar
- 160.Stevenson MM, Su Z, Sam H, Mohan K (2001) Modulation of host responses to blood-stage malaria by interleukin-12: from therapy to adjuvant activity.Microbes and Infect 3:49–59Google Scholar
- 161.Stevenson MM, Riley EM (2004) Innate immunity to malaria. Nat Rev Immunol 4:169–180PubMedCrossRefGoogle Scholar
- 162.Straw AD, MacDonald AS, Denkers EY, Pearce EJ (2003) CD154 plays a central role in regulating dendritic cell activation during infections that induce Th1 or Th2 responses. J Immunol 170:727–734PubMedGoogle Scholar
- 163.Su Z, Stevenson, MM (2000) The central role of endogenous IFN-γ in protective immunity against acute blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68:4399–4406PubMedCrossRefGoogle Scholar
- 164.Su Z, Stevenson MM (2002) IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168:1348–1355PubMedGoogle Scholar
- 165.Su Z, Fortin A, Gros P, Stevenson MM (2002) Opsonin-independent phagocytosis: an effector mechanism against acute blood-stage Plasmodium chabaudi AS infection. J Infect Dis 186:1321–1329PubMedCrossRefGoogle Scholar
- 166.Su Z, Tam MF, Jankovic D, Stevenson MM (2003) Vaccination against bloodstage malaria in mice using novel immunostimulatory adjuvants. Infect. Immun. 71:5178–5187PubMedGoogle Scholar
- 167.Taylor RR, Allen SJ, Greenwood BM, Riley EM (1998) IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. Am J Trop Med Hyg 58:406–413PubMedGoogle Scholar
- 168.Torre D, Giola M, Speranza F, Matteelli A, Basilico C, Biondi G (2001) Serum levels of interleukin-18 in patients with uncomplicated Plasmodium falciparum malaria. Eur Cytokine Netw 12:361–364PubMedGoogle Scholar
- 169.Traore B, Muanza K, Looareesuwan S, Supavej S, Khusmith S, Danis M, Viriyavejakul P, Gay F (2000) Cytoadherence characteristics of Plasmodium falciparum isolates in Thailand using an in vitro human lung endothelial cells model. Am J Trop Med Hyg 62:38–44PubMedGoogle Scholar
- 170.Troye-Blomberg M, Worku S, Tangteerawatana P, Jamshaid R, Soderstrom K, Elghazali G, Moretta L, Hammarstrom M, Mincheva-Nilsson L (1999) Human gamma delta T cells that inhibit the in vitro growth of the asexual blood stages of the Plasmodium falciparum parasite express cytolytic and proinflammatory molecules. Scand J Immunol 50:642–650PubMedCrossRefGoogle Scholar
- 171.Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B, et al. (1994) An immuno-histochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 145:1057–1069PubMedGoogle Scholar
- 172.Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M, Austyn JM, Roberts DJ (1999) Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400:73–77PubMedGoogle Scholar
- 173.Urban BC, Mwangi T, Ross A, Kinyanjui S, Mosobo M, Kai O, Lowe B, Marsh K, Roberts DJ 2001) Peripheral blood dendritic cells in children with acute Plasmodium falciparum malaria. Blood 98:2859–2861Google Scholar
- 174.Urban BC, Willcox N, Roberts DJ (2001) A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci U S A 98:8750–8755PubMedGoogle Scholar
- 175.Urban BC, Hien TT, Day NP, Phu NH, Roberts R, Pongponratn E, Jones M, Mai NT, Bethell D, Turner GD, Ferguson D, White NJ, Roberts DJ (2005) Fatal Plasmodium falciparum malaria causes specific patterns of splenic architectural disorganization. Infect Immun 73:1986–1994PubMedGoogle Scholar
- 176.van der Heyde HC, Ellso MM, Chang W-L, Kaplan M, Manning DD, Weidanz WP (1995) Gamma delta T cells function in cell-mediated immunity to acute blood-stage Plasmodium chabaudi adami malaria. J Immunol 154:3985–3990PubMedGoogle Scholar
- 177.Warren HS, Weidanz WP (1976) Malarial immunodepression in vitro: adherent spleen cells are functionally defective as accessory cells in the response to horse erythrocytes. Eur J Immunol 6:816–819PubMedGoogle Scholar
- 178.Waterfall M, Black A, Riley E (1998) Gammadelta+ T cells preferentially respond to live rather than killed malaria parasites. Infect Immun 66:2393–2398PubMedGoogle Scholar
- 179.Weatherall DJ, Miller LH, Baruch DI, Marsh K, Doumbo OK, Casals-Pascual C, Roberts DJ (2002) Malaria and the red cell. Hematology (Am Soc Hematol Educ Program) 35–57Google Scholar
- 180.Weidanz WP, Kemp JR, Batchelder JM, Cigel FK, Sandor M, van der Heyde HC (1999) Plasticity of immune responses suppressing parasitemia during acute Plasmodium chabaudi malaria. J Immunol 154:3985–3990Google Scholar
- 181.World malaria situation in 1994. Part I. Population at risk. (1997) Wkly Epidemiol Rec 72:269–274Google Scholar
- 182.Yoshimoto T, Paul WE (1994) CD4+, NK1.1+ T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3. J Exp Med 179:1285–1295PubMedCrossRefGoogle Scholar
- 183.Xu X, Sumita K, Feng C, Xiong X, Shen H, Maruyama S, Kanoh M, Asano Y (2001) Down-regulation of IL-12 p40 gene in Plasmodium berghei-infected mice. J Immunol 167:235–241PubMedGoogle Scholar
- 184.Zamai L, Ahmad M, Bennett IM, Azzoni L, Alnemri ES, Perussia B (1998) Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J Exp Med 188:2375–80PubMedCrossRefGoogle Scholar