Evaluating antidisease immunity to malaria and implications for vaccine design

Temitope W Ademolue, Gordon A Awandare, Temitope W Ademolue, Gordon A Awandare

Abstract

Immunity to malaria could be categorized broadly as antiparasite or antidisease immunity. While most vaccine research efforts have focused on antiparasite immunity, the evidence from endemic populations suggest that antidisease immunity is an important component of natural immunity to malaria. The processes that mediate antidisease immunity have, however, attracted little to no attention, and most interests have been directed towards the antibody responses. This review evaluates the evidence for antidisease immunity in endemic areas and discusses the possible mechanisms responsible for it. Given the key role that inflammation plays in the pathogenesis of malaria, regulation of the inflammatory response appears to be a major mechanism for antidisease immunity in naturally exposed individuals.

Keywords: inflammation; malaria; tolerance.

© 2017 The Authors. Immunology Published by John Wiley & Sons Ltd.

Figures

Figure 1
Figure 1
Mechanisms associated with reduced inflammatory responses at high exposure levels. (a) Direct immunosuppression of immune cells: hemozoin (Hz)‐laden immune cells [including dendritic cells (DCs), monocytes and macrophages (Mϕ)] exhibit impaired effector functions, such as reduced cytokine secretion and reduced expression of costimulatory molecules. (b) Loss of immune cells: repeated exposure is associated with the loss of immune cells, such as the Vδ2 subset of γδ T cells, which would normally secrete high levels of interferon (IFN)‐γ. (c) Exhausted or refractory immune cells: T cells (including CD4+ and CD8+) may display high levels of programmed cell death 1 (PD)‐1, a marker of an exhausted phenotype, at high levels of exposure. Similarly, innate immune cells may have become refractory to stimulation by lower antigen (parasitaemia) levels, and require high antigen loads to become stimulated.
Figure 2
Figure 2
Schematic depiction of the processes leading to differences in parasite tolerance at different levels of exposure. (a) Continuous high levels of exposure mimics a chronic state of infection (low Δt between infections), whereas low exposure levels are characterized by intermittent infections, separated by intervals of no exposure (high Δt between infection). (b) Each infection is therefore a distinct acute event at low levels of exposure, which induce a strong inflammatory response, requiring comparatively lower parasitaemia. A strong inflammatory response is associated with increased immunopathology, and consequently results in a high predisposition to clinical symptoms. However, higher parasite densities are required to stimulate immune cells at high exposure levels (as there is usually low‐level parasitaemia without clinical symptoms), and this stimulation leads to milder inflammatory responses. Mild proinflammatory responses result in reduced immunopathology, which may preclude the manifestation of clinical symptoms.

References

    1. Schofield L, Grau GE. Immunological processes in malaria pathogenesis. Nat Rev Immunol 2005; 5:722–35.
    1. Eisenhut M. Severe hemolysis as a potential contributing factor in the pathophysiology of cerebral malaria. Clin Infect Dis 2015; 60:1138.
    1. Dasari P, Heber SD, Beisele M, Torzewski M, Reifenberg K, Orning C et al Digestive vacuole of Plasmodium falciparum released during erythrocyte rupture dually activates complement and coagulation. Blood 2012; 119:4301–10.
    1. Clark IA, Budd AC, Alleva LM, Cowden WB. Human malarial disease: a consequence of inflammatory cytokine release. Malar J 2006; 5:85.
    1. Clark IA, Cowden WB. The pathophysiology of Falciparum malaria. Pharmacol Ther 2003; 99:221–60.
    1. Villegas‐Mendez A, Greig R, Shaw TN, de Souza JB, Findlay EG, Stumhofer JS et al Ifn‐Γ–producing Cd4+ T cells promote experimental cerebral malaria by modulating Cd8+ T cell accumulation within the brain. J Immunol 2012; 189:968–79.
    1. Robinson LJ, D'Ombrain MC, Stanisic DI, Taraika J, Bernard N, Richards JS et al Cellular tumor necrosis factor, gamma interferon, and interleukin‐6 responses as correlates of immunity and risk of clinical Plasmodium falciparum malaria in children from Papua New Guinea. Infect Immun 2009; 77:3033–43.
    1. Rogerson SJ, Brown HC, Pollina E, Abrams ET, Tadesse E, Lema VM et al Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infect Immun 2003; 71:267–70.
    1. Girard MP, Reed ZH, Friede M, Kieny MP. A review of human vaccine research and development: malaria. Vaccine 2007; 25:1567–80.
    1. Good MF. Towards a blood‐stage vaccine for malaria: are we following all the leads? Nat Rev Immunol 2001; 1:117.
    1. Ord RL, Caldeira JC, Rodriguez M, Noe A, Chackerian B, Peabody DS et al A malaria vaccine candidate based on an epitope of the Plasmodium falciparum Rh5 protein. Malar J 2014; 13:326.
    1. Thera MA, Doumbo OK, Coulibaly D, Diallo DA, Kone AK, Guindo AB et al Safety and immunogenicity of an Ama‐1 malaria vaccine in Malian adults: results of a phase 1 randomized controlled trial. PLOS ONE 2008; 3:e1465.
    1. Salavatifar M, Zakeri S, Roodbari NH, Djadid ND. High‐level expression, purification and characterization of a recombinant plasmodium vivax apical membrane antigen 1: implication for vivax malaria vaccine development. Cell J 2015; 17:520.
    1. Cohen S, McGregor I, Carrington S. Gamma‐globulin and acquired immunity to human malaria. Nature 1961; 192:733–7.
    1. Teo A, Feng G, Brown GV, Beeson JG, Rogerson SJ. Functional antibodies and protection against blood‐stage malaria. Trends Parasitol 2016; 32:887–98.
    1. Rts S, Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo B et al A phase 3 trial of Rts, S/As01 malaria vaccine in African infants. N Engl J Med 2012; 367:2284–95.
    1. Rts S. Efficacy and safety of Rts, S/As01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised. Controlled trial. Lancet 2015; 386:31–45.
    1. Ouattara A, Laurens MB. Vaccines against malaria. Clin Infect Dis 2014; 60:930–6.
    1. Chauhan VS. Development & licensing of first ever vaccine against malaria. Indian J Med Res 2015; 142:637.
    1. Mordmuller B, Surat G, Lagler H, Chakravarty S, Ishizuka AS, Lalremruata A et al Sterile protection against human malaria by chemoattenuated Pfspz vaccine. Nature 2017; 542:445–9.
    1. Ballou WR, Arevalo‐Herrera M, Carucci D, Richie TL, Corradin G, Diggs C et al Update on the clinical development of candidate malaria vaccines. Am J Trop Med Hyg 2004; 71:239–47.
    1. Withers MR, McKinney D, Ogutu BR, Waitumbi JN, Milman JB, Apollo OJ et al Safety and reactogenicity of an Msp‐1 malaria vaccine candidate: a randomized phase Ib dose‐escalation trial in Kenyan children. PLOS Clin Trials 2006; 1:e32.
    1. Sagara I, Dicko A, Ellis RD, Fay MP, Diawara SI, Assadou MH et al A randomized controlled phase 2 trial of the blood stage Ama1‐C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 2009; 27:3090–8.
    1. Olotu A, Fegan G, Wambua J, Nyangweso G, Awuondo KO, Leach A et al Four‐year efficacy of Rts, S/As01e and its interaction with malaria exposure. N Engl J Med 2013; 368:1111–20.
    1. Portugal S, Tipton CM, Sohn H, Kone Y, Wang J, Li S et al Malaria‐associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. Elife 2015; 4:e07218.
    1. Portugal S, Pierce SK, Crompton PD. Young lives lost as B cells falter: what we are learning about antibody responses in malaria. J Immunol 2013; 190:3039–46.
    1. do Rosário APF, Muxel SM, Rodríguez‐Málaga SM, Sardinha LR, Zago CA, Castillo‐Méndez SI et al Gradual decline in malaria‐specific memory T cell responses leads to failure to maintain long‐term protective immunity to Plasmodium chabaudi as despite persistence of B cell memory and circulating antibody. J Immunol 2008; 181:8344–55.
    1. Keitany GJ, Kim KS, Krishnamurty AT, Hondowicz BD, Hahn WO, Dambrauskas N et al Blood stage malaria disrupts humoral immunity to the pre‐erythrocytic stage circumsporozoite protein. Cell Rep 2016; 17:3193–205.
    1. Hviid L, Barfod L, Fowkes FJ. Trying to remember: immunological B cell memory to malaria. Trends Parasitol 2015; 31:89–94.
    1. Wykes MN, Horne‐Debets JM, Leow CY, Karunarathne DS. Malaria drives T cells to exhaustion. Front Microbiol 2014; 5:249.
    1. Horne‐Debets JM, Faleiro R, Karunarathne DS, Liu XQ, Lineburg KE, Poh CM et al Pd‐1 dependent exhaustion of Cd8+ T cells drives chronic malaria. Cell Rep 2013; 5:1204–13.
    1. Ryg‐Cornejo V, Ioannidis LJ, Ly A, Chiu CY, Tellier J, Hill DL et al Severe malaria infections impair germinal center responses by Inhibiting T follicular helper cell differentiation. Cell Rep 2016; 14:68–81.
    1. Obeng‐Adjei N, Portugal S, Tran TM, Yazew TB, Skinner J, Li S et al Circulating Th1‐cell‐type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Rep 2015; 13:425–39.
    1. Galatas B, Bassat Q, Mayor A. Malaria parasites in the asymptomatic: looking for the hay in the haystack. Trends Parasitol 2016; 32:296–308.
    1. Dobbs KR, Embury P, Vulule J, Odada PS, Rosa BA, Mitreva M et al Monocyte dysregulation and systemic inflammation during pediatric Falciparum malaria. JCI Insight 2017; 2:pii: 95352.
    1. Mshana R, Boulandi J, Mshana N, Mayombo J, Mendome G. Cytokines in the pathogenesis of malaria: levels of Il‐I beta, Il‐4, Il‐6, Tnf‐alpha and Ifn‐gamma in plasma of healthy individuals and malaria patients in a holoendemic area. J Clin Lab Immunol 1991; 34:131–9.
    1. van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends Parasitol 2006; 22:503–8.
    1. Barber BE, William T, Grigg MJ, Parameswaran U, Piera KA, Price RN et al Parasite biomass‐related inflammation, endothelial activation, microvascular dysfunction and disease severity in vivax malaria. PLOS Pathog 2015; 11:e1004558.
    1. Vásquez AM, Segura C, Blair S. Induction of pro‐inflammatory response of the placental trophoblast by Plasmodium falciparum infected erythrocytes and Tnf. Malar J 2013; 12:421.
    1. Ataide MA, Andrade WA, Zamboni DS, Wang D, do Carmo Souza M, Franklin BS et al Malaria‐induced Nlrp12/Nlrp3‐dependent caspase‐1 activation mediates inflammation and hypersensitivity to bacterial superinfection. PLOS Pathog 2014; 10:e1003885.
    1. Higgins SJ, Xing K, Kim H, Kain DC, Wang F, Dhabangi A et al Systemic release of high mobility group box 1 (Hmgb1) protein is associated with severe and fatal Plasmodium falciparum malaria. Malar J 2013; 12:105.
    1. Chiu CY, Healer J, Thompson JK, Chen L, Kaul A, Savergave L et al Association of antibodies to Plasmodium falciparum reticulocyte binding protein homolog 5 with protection from clinical malaria. Front Microbiol 2014; 5:314.
    1. Tran TM, Ongoiba A, Coursen J, Crosnier C, Diouf A, Huang C‐Y et al Naturally acquired antibodies specific for Plasmodium falciparum reticulocyte‐binding protein homologue 5 inhibit parasite growth and predict protection from malaria. J Infect Dis 2013; 209:789–98.
    1. Pérez‐Mazliah D, Ng DHL, do Rosário APF, McLaughlin S, Mastelic‐Gavillet B, Sodenkamp J et al Disruption of Il‐21 signaling affects T cell‐B cell interactions and abrogates protective humoral immunity to malaria. PLOS Pathog 2015; 11:e1004715.
    1. Molineaux L, Gramiccia G, World Health Organization . The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. Geneva: World Health Organization, 1980.
    1. Dodoo D, Atuguba F, Bosomprah S, Ansah NA, Ansah P, Lamptey H et al Antibody levels to multiple malaria vaccine candidate antigens in relation to clinical malaria episodes in children in the Kasena‐Nankana District of Northern Ghana. Malar J 2011; 10:108.
    1. Proietti C, Verra F, Bretscher M, Stone W, Kanoi B, Balikagala B et al Influence of infection on malaria‐specific antibody dynamics in a cohort exposed to intense malaria transmission in Northern Uganda. Parasite Immunol 2013; 35:164–73.
    1. Mmbando BP, Msangeni HA, Sembuche SH, Ishengoma DS, Seth MD, Francis F et al Epidemiology of malaria in an area prepared for clinical trials in Korogwe, North‐Eastern Tanzania. Malar J 2009; 8:165.
    1. Berg A, Otterdal K, Patel S, Gonca M, David C, Dalen I et al Complement activation correlates with disease severity and contributes to cytokine responses in Plasmodium falciparum malaria. J Infect Dis 2015; 212:1835–40.
    1. Oakley MS, Sahu BR, Lotspeich‐Cole L, Solanki NR, Majam V, Pham PT et al The transcription factor T‐bet regulates parasitaemia and promotes pathogenesis during Plasmodium berghei Anka Murine Malaria. J Immunol 2013; 191:4699–708.
    1. do Rosário APF, Lamb T, Spence P, Stephens R, Lang A, Roers A et al Il‐27 promotes Il‐10 production by effector Th1 Cd4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol 2012; 188:1178–90.
    1. Jagannathan P, Kim CC, Greenhouse B, Nankya F, Bowen K, Eccles‐James I et al Loss and dysfunction of Vδ2+ Γδ T cells are associated with clinical tolerance to malaria. Sci Transl Med 2014; 6:251ra117.
    1. He X, Yan J, Zhu X, Wang Q, Pang W, Qi Z et al Vitamin D inhibits the occurrence of experimental cerebral malaria in mice by suppressing the host inflammatory response. J Immunol 2014; 193:1314–23.
    1. Perraut R, Joos C, Sokhna C, Polson HE, Trape J‐F, Tall A et al Association of antibody responses to the conserved Plasmodium falciparum merozoite surface protein 5 with protection against clinical malaria. PLOS ONE 2014; 9:e101737.
    1. Bediako Y, Ngoi JM, Nyangweso G, Wambua J, Opiyo M, Nduati EW et al The effect of declining exposure on T cell‐mediated immunity to Plasmodium falciparum–an epidemiological “natural experiment”. BMC Med 2016; 14:143.
    1. Portugal S, Moebius J, Skinner J, Doumbo S, Doumtabe D, Kone Y et al Exposure‐dependent control of malaria‐induced inflammation in children. PLOS Pathog 2014; 10:e1004079.
    1. Hirunpetcharat C, Finkelman F, Clark IA, Good MF. Malaria parasite‐specific Th1‐like T cells simultaneously reduce parasitaemia and promote disease. Parasite Immunol 1999; 21:319–29.
    1. Ademolue TW, Aniweh Y, Kusi KA, Awandare GA. Patterns of inflammatory responses and parasite tolerance vary with malaria transmission intensity. Malar J 2017; 16:145.
    1. Moncunill G, Mayor A, Jiménez A, Nhabomba A, Puyol L, Manaca MN et al Cytokine and antibody responses to Plasmodium falciparum in naive individuals during a first malaria episode: effect of age and malaria exposure. PLOS ONE 2013; 8:e55756.
    1. Langhorne J, Ndungu FM, Sponaas A‐M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol 2008; 9:725–32.
    1. O'Meara WP, Mwangi TW, Williams TN, McKenzie FE, Snow RW, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg 2008; 79:185–91.
    1. de Mast Q, Brouwers J, Syafruddin D, Bousema T, Baidjoe AY, de Groot PG et al Is asymptomatic malaria really asymptomatic? Hematological, vascular and inflammatory effects of asymptomatic malaria parasitaemia. J Infect 2015; 71:587–96.
    1. Jakobsen P, McKay V, N'jie R, Olaleye B, D'Alessandro U, Bendtzen K et al Soluble products of inflammatory reactions are not induced in children with asymptomatic Plasmodium falciparum infections. Clin Exp Immunol 1996; 105:69–73.
    1. Stubbs J, Olugbile S, Saidou B, Simpore J, Corradin G, Lanzavecchia A. Strain‐transcending Fc‐dependent killing of Plasmodium falciparum by merozoite surface protein 2 allele‐specific human antibodies. Infect Immun 2011; 79:1143–52.
    1. McMorran BJ, Wieczorski L, Drysdale KE, Chan J‐A, Huang HM, Smith C et al Platelet factor 4 and duffy antigen required for platelet killing of Plasmodium falciparum . Science 2012; 338:1348–51.
    1. Coggeshall LT, Kumm HW. Demonstration of passive immunity in experimental monkey malaria. J Exp Med 1937; 66:177–90.
    1. Coggeshall L. Immunity in malaria. Medicine 1943; 22:87–102.
    1. Weiss GE, Gilson PR, Taechalertpaisarn T, Tham W‐H, de Jong NW, Harvey KL et al Revealing the sequence and resulting cellular morphology of receptor‐ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLOS Pathog 2015; 11:e1004670.
    1. Reddy KS, Amlabu E, Pandey AK, Mitra P, Chauhan VS, Gaur D. Multiprotein complex between the Gpi‐Anchored Cyrpa with Pfrh5 and Pfripr is crucial for Plasmodium falciparum erythrocyte invasion. Proc Natl Acad Sci USA 2015; 112:1179–84.
    1. Reddy KS, Pandey AK, Singh H, Sahar T, Emmanuel A, Chitnis CE et al Bacterially expressed full‐length recombinant Plasmodium falciparum Rh5 protein binds erythrocytes and elicits potent strain‐transcending parasite‐neutralizing antibodies. Infect Immun 2014; 82:152–64.
    1. Chiu CY, Hodder AN, Lin CS, Hill DL, Li Wai Suen CS, Schofield L et al Antibodies to the Plasmodium falciparum proteins Mspdbl1 and Mspdbl2 opsonize merozoites, inhibit parasite growth, and predict protection from clinical malaria. J Infect Dis 2015; 212:406–15.
    1. Sakamoto H, Takeo S, Maier AG, Sattabongkot J, Cowman AF, Tsuboi T. Antibodies against a Plasmodium falciparum antigen Pfmspdbl1 inhibit merozoite invasion into human erythrocytes. Vaccine 2012; 30:1972–80.
    1. Osier FH, Mackinnon MJ, Crosnier C, Fegan G, Kamuyu G, Wanaguru M et al New antigens for a multicomponent blood‐stage malaria vaccine. Sci Transl Med 2014; 6:247ra102.
    1. Lyke KE, Ishizuka AS, Berry AA, Chakravarty S, DeZure A, Enama ME et al Attenuated Pfspz vaccine induces strain‐transcending T cells and durable protection against heterologous controlled human malaria infection. Proc Natl Acad Sci USA 2017; 114:2711–6.
    1. Epstein JE, Paolino KM, Richie TL, Sedegah M, Singer A, Ruben AJ et al Protection against Plasmodium falciparum malaria by Pfspz vaccine. JCI Insight 2017; 2:e89154.
    1. Tiendrebeogo RW, Adu B, Singh SK, Dziegiel MH, Nébié I, Sirima SB et al Antibody‐Dependent Cellular Inhibition is Associated with Reduced Risk Against Febrile Malaria in a Longitudinal Cohort Study Involving Ghanaian Children. Open forum infectious diseases: Oxford University Press, 2015.
    1. Weiss GE, Traore B, Kayentao K, Ongoiba A, Doumbo S, Doumtabe D et al The Plasmodium falciparum‐specific human memory B cell compartment expands gradually with repeated malaria infections. PLOS Pathog 2010; 6:e1000912.
    1. Dodoo D, Aikins A, Kusi KA, Lamptey H, Remarque E, Milligan P et al Cohort study of the association of antibody levels to Ama1, Msp1 19, Msp3 and Glurp with protection from clinical malaria in Ghanaian children. Malar J 2008; 7:142.
    1. Kinyanjui SM, Conway DJ, Lanar DE, Marsh K. Igg antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half‐life. Malar J 2007; 6:82.
    1. Hodder AN, Crewther PE, Anders RF. Specificity of the protective antibody response to apical membrane antigen 1. Infect Immun 2001; 69:3286–94.
    1. McCallum FJ, Persson KE, Fowkes FJ, Reiling L, Mugyenyi CK, Richards JS et al Differing rates of antibody acquisition to merozoite antigens in malaria: implications for immunity and surveillance. J Leukoc Biol 2017; 101:913–25.
    1. Lyke K, Burges R, Cissoko Y, Sangare L, Dao M, Diarra I et al Serum levels of the proinflammatory cytokines interleukin‐1 Beta (Il‐1β), Il‐6, Il‐8, Il‐10, tumor necrosis factor alpha, and Il‐12 (P70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun 2004; 72:5630–7.
    1. Lopera‐Mesa TM, Mita‐Mendoza NK, van de Hoef DL, Doumbia S, Konaté D, Doumbouya M et al Plasma uric acid levels correlate with inflammation and disease severity in Malian children with Plasmodium falciparum malaria. PLOS ONE 2012; 7:e46424.
    1. Perkins DJ, Weinberg JB, Kremsner PG. Reduced interleukin‐12 and transforming growth factor—Β 1 in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis 2000; 182:988–92.
    1. Riley EM, Stewart VA. Immune mechanisms in malaria: new insights in vaccine development. Nat Med 2013; 19:168–78.
    1. Torre D, Speranza F, Giola M, Matteelli A, Tambini R, Biondi G. Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol 2002; 9:348–51.
    1. Miller LH, Ackerman HC, Su XZ, Wellems TE. Malaria biology and disease pathogenesis: insights for new treatments. Nat Med 2013; 19:156–67.
    1. Gazzinelli RT, Kalantari P, Fitzgerald KA, Golenbock DT. Innate sensing of malaria parasites. Nat Rev Immunol 2014; 14:744–57.
    1. Zhu J, Yamane H, Paul WE. Differentiation of effector Cd4 T cell populations. Annu Rev Immunol 2009; 28:445–89.
    1. Taylor‐Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY. The role of Th1 and Th2 cells in a rodent malaria infection. Science 1993; 260:1931–5.
    1. Inoue S, Niikura M, Mineo S, Kobayashi F. Roles of Ifn‐gamma and gammadelta T cells in protective immunity against blood‐stage malaria. Front Immunol 2013; 4:258.
    1. Clark IA, Alleva LM, Budd AC, Cowden WB. Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Med Infect Dis 2008; 6:67–81.
    1. Soares MP, Teixeira L, Moita LF. Disease tolerance and immunity in host protection against infection. Nat Rev Immunol 2017; 17:83–96.
    1. Gatton ML, Cheng Q. Evaluation of the pyrogenic threshold for Plasmodium falciparum malaria in naive individuals. Am J Trop Med Hyg 2002; 66:467–73.
    1. Hay SI, Guerra CA, Tatem AJ, Atkinson PM, Snow RW. Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol 2005; 3:81–90.
    1. Snow RW, Bastos de Azevedo I, Lowe BS, Kabiru EW, Nevill CG, Mwankusye S et al Severe childhood malaria in two areas of markedly different falciparum transmission in East Africa. Acta Trop 1994; 57:289–300.
    1. Griffin JT, Ferguson NM, Ghani AC. Estimates of the changing age‐burden of Plasmodium falciparum malaria disease in Sub‐Saharan Africa. Nat Commun 2014; 5:3136.
    1. Carneiro I, Roca‐Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA et al Age‐patterns of malaria vary with severity, transmission intensity and seasonality in Sub‐Saharan Africa: a systematic review and pooled analysis. PLOS ONE 2010; 5:e8988.
    1. Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE et al A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA 2010; 107:6958–63.
    1. Stanisic DI, Fowkes FJ, Koinari M, Javati S, Lin E, Kiniboro B et al Acquisition of antibodies against Plasmodium falciparum merozoites and malaria immunity in young children and the influence of age, force of infection, and magnitude of response. Infect Immun 2015; 83:646–60.
    1. Drakeley C, Corran P, Coleman P, Tongren J, McDonald S, Carneiro I et al Estimating medium‐and long‐term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA 2005; 102:5108–13.
    1. Perraut R, Varela ML, Loucoubar C, Niass O, Sidibe A, Tall A et al Serological signatures of declining exposure following intensification of integrated malaria control in two rural senegalese communities. PLOS ONE 2017; 12:e0179146.
    1. Mbengue B, Niang B, Niang MS, Varela ML, Fall B, Fall MM et al Inflammatory cytokine and humoral responses to Plasmodium falciparum glycosylphosphatidylinositols correlates with malaria immunity and pathogenesis. Immun Inflamm Dis 2016; 4:24–34.
    1. Moncunill G, Mayor A, Bardaji A, Puyol L, Nhabomba A, Barrios D et al Cytokine profiling in immigrants with clinical malaria after extended periods of interrupted exposure to Plasmodium falciparum . PLOS ONE 2013; 8:e73360.
    1. Obiero JM, Shekalaghe S, Hermsen CC, Mpina M, Bijker EM, Roestenberg M et al Impact of malaria preexposure on antiparasite cellular and humoral immune responses after controlled human malaria infection. Infect Immun 2015; 83:2185–96.
    1. Boyle MJ, Jagannathan P, Bowen K, McIntyre TI, Vance HM, Farrington LA et al Effector phenotype of Plasmodium falciparum–specific Cd4+ T cells is influenced by both age and transmission intensity in naturally exposed populations. J Infect Dis 2015; 212:416–25.
    1. Jagannathan P, Eccles‐James I, Bowen K, Nankya F, Auma A, Wamala S et al Ifnγ/Il‐10 co‐producing cells dominate the Cd4 response to malaria in highly exposed children. PLOS Pathog 2014; 10:e1003864.
    1. Millington OR, Di Lorenzo C, Phillips RS, Garside P, Brewer JM. Suppression of adaptive immunity to heterologous antigens during plasmodium infection through hemozoin‐induced failure of dendritic cell function. J Biol 2006; 5:5.
    1. Ho M, Webster HK, Looareesuwan S, Supanaranond W, Phillips RE, Chanthavanich P et al Antigen‐specific immunosuppression in human malaria due to Plasmodium falciparum . J Infect Dis 1986; 153:763–71.
    1. Urban BC, Ferguson DJ, Pain A, Willcox N. Plasmodium falciparium‐infected erythrocytes modulate the maturation of dendritic cells. Nature 1999; 400:73.
    1. Urban BC, Roberts DJ. Malaria, monocytes, macrophages and myeloid dendritic cells: sticking of infected erythrocytes switches off host cells. Curr Opin Immunol 2002; 14:458–65.
    1. Elliott SR, Spurck TP, Dodin JM, Maier AG, Voss TS, Yosaatmadja F 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; 75:3621–32.
    1. Millington OR, Gibson VB, Rush CM, Zinselmeyer BH, Phillips RS, Garside P et al Malaria impairs T cell clustering and immune priming despite normal signal 1 from dendritic cells. PLOS Pathog 2007; 3:e143.
    1. Were T, Davenport GC, Yamo EO, Hittner JB, Awandare GA, Otieno MF et al Naturally acquired hemozoin by monocytes promotes suppression of rantes in children with malarial anemia through an Il‐10‐dependent mechanism. Microbes Infect 2009; 11:811–9.
    1. Keller CC, Yamo O, Ouma C, Ong'echa JM, Ounah D, Hittner JB et al Acquisition of hemozoin by monocytes down‐regulates interleukin‐12 P40 (Il‐12p40) transcripts and circulating Il‐12p70 through an Il‐10‐dependent mechanism: in vivo and in vitro findings in severe malarial anemia. Infect Immun 2006; 74:5249–60.
    1. Awandare GA, Ouma Y, Ouma C, Were T, Otieno R, Keller CC et al Role of monocyte‐acquired hemozoin in suppression of macrophage migration inhibitory factor in children with severe malarial anemia. Infect Immun 2007; 75:201–10.
    1. Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol 2002; 52:235–64.
    1. Stephens R, Langhorne J. Effector memory Th1 Cd4 T cells are maintained in a mouse model of chronic malaria. PLOS Pathog 2010; 6:e1001208.
    1. Hirunpetcharat C, Good MF. Deletion of Plasmodium berghei‐specific Cd4+ T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc Natl Acad Sci USA 1998; 95:1715–20.
    1. Xu H, Wipasa J, Yan H, Zeng M, Makobongo MO, Finkelman FD et al The mechanism and significance of deletion of parasite‐specific Cd4+ T cells in malaria infection. J Exp Med 2002; 195:881–92.
    1. Hviid L, Kurtzhals JA, Adabayeri V, Loizon S, Kemp K, Goka BQ et al Perturbation and proinflammatory type activation of Vδ1+ Γδ T cells in African children with Plasmodium falciparum malaria. Infect Immun 2001; 69:3190–6.
    1. Hviid L, Kemp K. What is the cause of lymphopenia in malaria? Infect Immun 2000; 68:6087–9.
    1. Hviid L, Kurtzhals J, Goka BQ, Oliver‐Commey JO, Nkrumah FK, Theander TG. Rapid reemergence of T cells into peripheral circulation following treatment of severe and uncomplicated Plasmodium falciparum malaria. Infect Immun 1997; 65:4090–3.
    1. Winkler S, Willheim M, Baier K, Schmid D, Aichelburg A, Graninger W et al Reciprocal regulation of Th1‐and Th2‐cytokine‐producing T cells during clearance of parasitaemia in Plasmodium falciparum malaria. Infect Immun 1998; 66:6040–4.
    1. Chougnet C, Deloron P, Lepers JP, Rason MD, Savel J, Coulanges P. Longitudinal study of the cellular response to Pf155/Resa and circumsporozoite protein in Madagascar. Immunol Lett 1990; 25:231–5.
    1. Chougnet C, Deloron P, Lepers JP, Tallet S, Rason MD, Astagneau P et al Humoral and cell‐mediated immune responses to the Plasmodium falciparum antigens Pf155/Resa and Cs protein: seasonal variations in a population recently reexposed to endemic malaria. Am J Trop Med Hyg 1990; 43:234–42.
    1. Behr C, Dubois P. Preferential expansion of Vγ9 Vδ2 T cells following stimulation of peripheral blood lymphocytes with extracts of Plasmodium falciparum . Int Immunol 1992; 4:361–6.
    1. Yoshimoto T, Takahama Y, Wang C‐R, Yoneto T, Waki S, Nariuchi H. A pathogenic role of Il‐12 in blood‐stage murine malaria lethal strain Plasmodium berghei Nk65 infection. J Immunol 1998; 160:5500–5.
    1. Medina TS, Costa SP, Oliveira MD, Ventura AM, Souza JM, Gomes TF et al Increased interleukin‐10 and interferon‐Γ levels in Plasmodium vivax malaria suggest a reciprocal regulation which is not altered by Il‐10 gene promoter polymorphism. Malar J 2011; 10:1.
    1. Boyle MJ, Jagannathan P, Farrington LA, Eccles‐James I, Wamala S, McIntyre TI et al Decline of Foxp3+ regulatory Cd4 T cells in peripheral blood of children heavily exposed to malaria. PLOS Pathog 2015; 11:e1005041.
    1. Grossman Z, Paul WE. Dynamic tuning of lymphocytes: physiological basis, mechanisms, and function. Annu Rev Immunol 2015; 33:677–713.
    1. Grossman Z, Paul WE. Adaptive cellular interactions in the immune system: the tunable activation threshold and the significance of subthreshold responses. Proc Natl Acad Sci USA 1992; 89:10365–9.
    1. Mensah‐Brown HE, Abugri J, Asante KP, Dwomoh D, Dosoo D, Atuguba F et al Assessing the impact of differences in malaria transmission intensity on clinical and haematological indices in children with malaria. Malar J 2017; 16:96.
    1. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death‐1 ligand 1 interacts specifically with the B7‐1 costimulatory molecule to inhibit T cell responses. Immunity 2007; 27:111–22.
    1. Butler NS, Moebius J, Pewe LL, Traore B, Doumbo OK, Tygrett LT et al Therapeutic blockade of Pd‐L1 and Lag‐3 rapidly clears established blood‐stage plasmodium infection. Nat Immunol 2012; 13:188–95.
    1. Seguin MC, Klotz FW, Schneider I, Weir JP, Goodbary M, Slayter M et al Induction of nitric oxide synthase protects against malaria in mice exposed to irradiated Plasmodium berghei infected mosquitoes: involvement of interferon gamma and Cd8+ T cells. J Exp Med 1994; 180:353–8.
    1. Imai T, Shen J, Chou B, Duan X, Tu L, Tetsutani K et al Involvement of Cd8+ T cells in protective immunity against murine blood‐stage infection with Plasmodium yoelii 17xl strain. Eur J Immunol 2010; 40:1053–61.
    1. Imai T, Ishida H, Suzue K, Taniguchi T, Okada H, Shimokawa C et al Cytotoxic activities of Cd8+ T cells collaborate with macrophages to protect against blood‐stage murine malaria. Elife 2015; 4:e04232.
    1. Brown JA, Dorfman DM, Ma F‐R, Sullivan EL, Munoz O, Wood CR et al Blockade of programmed death‐1 ligands on dendritic cells enhances T cell activation and cytokine production. J Immunol 2003; 170:1257–66.
    1. Illingworth J, Butler NS, Roetynck S, Mwacharo J, Pierce SK, Bejon P et al Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol 2013; 190:1038–47.
    1. Hafalla JCR, Claser C, Couper KN, Grau GE, Renia L, de Souza JB et al The Ctla‐4 and Pd‐1/Pd‐L1 inhibitory pathways independently regulate host resistance to Plasmodium‐induced acute immune pathology. PLOS Pathog 2012; 8:e1002504.
    1. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I et al Pd‐L2 Is a second ligand for Pd‐1 and inhibits T cell activation. Nat Immunol 2001; 2:261.
    1. Karunarathne DS, Horne‐Debets JM, Huang JX, Faleiro R, Leow CY, Amante F et al Programmed death‐1 ligand 2‐mediated regulation of the Pd‐L1 to Pd‐1 axis is essential for establishing Cd4+ T cell immunity. Immunity 2016; 45:333–45.
    1. Villegas‐Mendez A, de Souza JB, Lavelle S‐W, Findlay EG, Shaw TN, van Rooijen N et al Il‐27 receptor signalling restricts the formation of pathogenic, terminally differentiated Th1 cells during malaria infection by repressing Il‐12 dependent signals. PLOS Pathog 2013; 9:e1003293.
    1. Boggild AK, Krudsood S, Patel SN, Serghides L, Tangpukdee N, Katz K et al Use of peroxisome proliferator‐activated receptor Γ agonists as adjunctive treatment for Plasmodium falciparum malaria: a randomized, double‐blind, placebo‐controlled trial. Clin Infect Dis 2009; 49:841–9.
    1. Serghides L, Kain KC. Peroxisome proliferator‐activated receptor Γ‐retinoid X receptor agonists increase Cd36‐dependent phagocytosis of Plasmodium falciparum‐parasitized erythrocytes and decrease malaria‐induced Tnf‐Α secretion by monocytes/macrophages. J Immunol 2001; 166:6742–8.
    1. Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE et al Cross‐regulation of C/Ebpα and Pparγ controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 1999; 3:151–8.
    1. Serghides L, Kain KC. Peroxisome proliferator‐activated receptor Γ and retinoid X receptor agonists have minimal effects on the interaction of endothelial cells with Plasmodium falciparum‐infected erythrocytes. Infect Immun 2005; 73:1209–13.
    1. Patel SN, Serghides L, Smith TG, Febbraio M, Silverstein RL, Kurtz TW et al Cd36 mediates the phagocytosis of Plasmodium falciparum–infected erythrocytes by rodent macrophages. J Infect Dis 2004; 189:204–13.
    1. Campo JJ, Aponte JJ, Skinner J, Nakajima R, Molina DM, Liang L et al Rts, S vaccination is associated with serologic evidence of decreased exposure to Plasmodium falciparum liver‐and blood‐stage parasites. Mol Cell Proteomics 2015; 14:519–31.

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