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Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Recognition of Plasmodium falciparum mature gametocyte-infected erythrocytes by antibodies of semi-immune adults and malaria-exposed children from Gabon

Authors: Tamirat Gebru, Anthony Ajua, Michael Theisen, Meral Esen, Ulysse Ateba Ngoa, Saadou Issifou, Ayola A. Adegnika, Peter G. Kremsner, Benjamin Mordmüller, Jana Held

Published in: Malaria Journal | Issue 1/2017

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Abstract

Background

Transmission of malaria from man to mosquito depends on the presence of gametocytes, the sexual stage of Plasmodium parasites in the infected host. Naturally acquired antibodies against gametocytes exist and may play a role in controlling transmission by limiting the gametocyte development in the circulation or by interrupting gamete development and fertilization in the mosquito following ingestion. So far, most studies on antibody responses to sexual stage antigens have focused on a subset of gametocyte-surface antigens, even though inhibitory Ab responses to other gametocyte antigens might also play a role in controlling gametocyte density and fertility. Limited information is available on natural antibody response to the surfaces of gametocyte-infected erythrocytes.

Methods

Ab responses to surface antigens of erythrocytes infected by in vitro differentiated Plasmodium falciparum mature gametocytes were investigated in sera of semi-immune adults and malaria-exposed children. In addition, the effect of immunization with GMZ2, a blood stage malaria vaccine candidate, and the effect of intestinal helminth infection on the development of immunity to gametocytes of P. falciparum was evaluated in malaria-exposed children and adults from Gabon. Serum samples from two Phase I clinical trials conducted in Gabon were analysed by microscopic and flow-cytometric immunofluorescence assay.

Results

Adults had a higher Ab response compared to children. Ab reactivity was significantly higher after fixation and permeabilization of parasitized erythrocytes. Following vaccination with the malaria vaccine candidate GMZ2, anti-gametocyte Ab concentration decreased in adults compared to baseline. Ab response to whole asexual stage antigens had a significant but weak positive correlation to anti-gametocyte Ab responses in adults, but not in children. Children infected with Ascaris lumbricoides had a significantly higher anti-gametocyte Ab response compared to non-infected children.

Conclusion

The current data suggest that antigens exposed on the gametocyte-infected red blood cells are recognized by serum antibodies from malaria-exposed children and semi-immune adults. This anti-gametocyte immune response may be influenced by natural exposure and vaccination. Modulation of the natural immune response to gametocytes by co-infecting parasites should be investigated further and may have an important impact on malaria control strategies.
Literature
2.
go back to reference Abay SM. Blocking malaria transmission to Anopheles mosquitoes using artemisinin derivatives and primaquine: a systematic review and meta-analysis. Parasit Vectors. 2013;6:278.CrossRefPubMedPubMedCentral Abay SM. Blocking malaria transmission to Anopheles mosquitoes using artemisinin derivatives and primaquine: a systematic review and meta-analysis. Parasit Vectors. 2013;6:278.CrossRefPubMedPubMedCentral
3.
go back to reference Abdul-Ghani R, Beier JC. Strategic use of antimalarial drugs that block falciparum malaria parasite transmission to mosquitoes to achieve local malaria elimination. Parasitol Res. 2014;113:3535–46.CrossRefPubMed Abdul-Ghani R, Beier JC. Strategic use of antimalarial drugs that block falciparum malaria parasite transmission to mosquitoes to achieve local malaria elimination. Parasitol Res. 2014;113:3535–46.CrossRefPubMed
4.
go back to reference Bousema T, Sutherland CJ, Churcher TS, Mulder B, Gouagna LC, Riley EM, et al. Human immune responses that reduce the transmission of Plasmodium falciparum in African populations. Int J Parasitol. 2011;41:293–300.CrossRefPubMedPubMedCentral Bousema T, Sutherland CJ, Churcher TS, Mulder B, Gouagna LC, Riley EM, et al. Human immune responses that reduce the transmission of Plasmodium falciparum in African populations. Int J Parasitol. 2011;41:293–300.CrossRefPubMedPubMedCentral
5.
go back to reference Tonwong N, Sattabongkot J, Tsuboi T, Iriko H, Takeo S, Sirichaisinthop J, et al. Natural infection of Plasmodium falciparum induces inhibitory antibodies against gametocyte development in human hosts. Jpn J Infect Dis. 2012;65:152–6.PubMed Tonwong N, Sattabongkot J, Tsuboi T, Iriko H, Takeo S, Sirichaisinthop J, et al. Natural infection of Plasmodium falciparum induces inhibitory antibodies against gametocyte development in human hosts. Jpn J Infect Dis. 2012;65:152–6.PubMed
6.
go back to reference Carter R, Stowers A. Current developments in malaria transmission-blocking vaccines. Expert Opin Biol Ther. 2001;1:619–28.CrossRefPubMed Carter R, Stowers A. Current developments in malaria transmission-blocking vaccines. Expert Opin Biol Ther. 2001;1:619–28.CrossRefPubMed
8.
go back to reference Lensen A, Mulder L, Tchuinkam T, Willemsen L, Eling W, Sauerwein R. Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. J Infect Dis. 1998;177:1358–63.CrossRefPubMed Lensen A, Mulder L, Tchuinkam T, Willemsen L, Eling W, Sauerwein R. Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. J Infect Dis. 1998;177:1358–63.CrossRefPubMed
9.
go back to reference Carter R, Mendis K. Transmission immunity in malaria: reflections on the underlying immune mechanisms during natural infections and following artificial immunization. Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):169–73.CrossRefPubMed Carter R, Mendis K. Transmission immunity in malaria: reflections on the underlying immune mechanisms during natural infections and following artificial immunization. Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):169–73.CrossRefPubMed
10.
go back to reference Wallach M. The importance of transmission-blocking immunity in the control of infections by apicomplexan parasites. Int J Parasitol. 1997;27:1159–67.CrossRefPubMed Wallach M. The importance of transmission-blocking immunity in the control of infections by apicomplexan parasites. Int J Parasitol. 1997;27:1159–67.CrossRefPubMed
11.
go back to reference Healer J, McGuinness D, Hopcroft P, Haley S, Carter R, Riley E. Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infect Immun. 1997;65:3017–23.PubMedPubMedCentral Healer J, McGuinness D, Hopcroft P, Haley S, Carter R, Riley E. Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infect Immun. 1997;65:3017–23.PubMedPubMedCentral
12.
go back to reference Frölich S, Entzeroth R, Wallach M. Comparison of protective immune responses to apicomplexan parasites. J Parasitol Res. 2012;2012:852591.CrossRefPubMed Frölich S, Entzeroth R, Wallach M. Comparison of protective immune responses to apicomplexan parasites. J Parasitol Res. 2012;2012:852591.CrossRefPubMed
13.
go back to reference Baird JK, Jones TR. Purnomo null, Masbar S, Ratiwayanto S, Leksana B. Evidence for specific suppression of gametocytemia by Plasmodium falciparum in residents of hyperendemic Irian Jaya. Am J Trop Med Hyg. 1991;44:183–90.PubMed Baird JK, Jones TR. Purnomo null, Masbar S, Ratiwayanto S, Leksana B. Evidence for specific suppression of gametocytemia by Plasmodium falciparum in residents of hyperendemic Irian Jaya. Am J Trop Med Hyg. 1991;44:183–90.PubMed
14.
go back to reference Sutherland CJ. Surface antigens of Plasmodium falciparum gametocytes–a new class of transmission-blocking vaccine targets? Mol Biochem Parasitol. 2009;166:93–8.CrossRefPubMed Sutherland CJ. Surface antigens of Plasmodium falciparum gametocytes–a new class of transmission-blocking vaccine targets? Mol Biochem Parasitol. 2009;166:93–8.CrossRefPubMed
15.
go back to reference Saeed M, Roeffen W, Alexander N, Drakeley CJ, Targett GAT, Sutherland CJ. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS ONE. 2008;3:e2280.CrossRefPubMedPubMedCentral Saeed M, Roeffen W, Alexander N, Drakeley CJ, Targett GAT, Sutherland CJ. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS ONE. 2008;3:e2280.CrossRefPubMedPubMedCentral
16.
go back to reference Roeffen W, Mulder B, Teelen K, Bolmer M, Eling W, Targett GA, et al. Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunol. 1996;18:103–9.CrossRefPubMed Roeffen W, Mulder B, Teelen K, Bolmer M, Eling W, Targett GA, et al. Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunol. 1996;18:103–9.CrossRefPubMed
17.
go back to reference Roeffen W, Geeraedts F, Eling W, Beckers P, Wizel B, Kumar N, et al. Transmission blockade of Plasmodium falciparum malaria by anti-Pfs230-specific antibodies is isotype dependent. Infect Immun. 1995;63:467–71.PubMedPubMedCentral Roeffen W, Geeraedts F, Eling W, Beckers P, Wizel B, Kumar N, et al. Transmission blockade of Plasmodium falciparum malaria by anti-Pfs230-specific antibodies is isotype dependent. Infect Immun. 1995;63:467–71.PubMedPubMedCentral
18.
go back to reference Graves PM, Carter R, Burkot TR, Quakyi IA, Kumar N. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol. 1988;10:209–18.CrossRefPubMed Graves PM, Carter R, Burkot TR, Quakyi IA, Kumar N. Antibodies to Plasmodium falciparum gamete surface antigens in Papua New Guinea sera. Parasite Immunol. 1988;10:209–18.CrossRefPubMed
19.
go back to reference Bousema JT, Gouagna LC, Drakeley CJ, Meutstege AM, Okech BA, Akim INJ, et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malar J. 2004;3:18.CrossRefPubMedPubMedCentral Bousema JT, Gouagna LC, Drakeley CJ, Meutstege AM, Okech BA, Akim INJ, et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malar J. 2004;3:18.CrossRefPubMedPubMedCentral
20.
go back to reference Dunyo S, Milligan P, Edwards T, Sutherland C, Targett G, Pinder M. Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials. 2006;1:e20.CrossRefPubMedPubMedCentral Dunyo S, Milligan P, Edwards T, Sutherland C, Targett G, Pinder M. Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials. 2006;1:e20.CrossRefPubMedPubMedCentral
21.
go back to reference Piper KP, Hayward RE, Cox MJ, Day KP. Malaria transmission and naturally acquired immunity to PfEMP-1. Infect Immun. 1999;67:6369–74.PubMedPubMedCentral Piper KP, Hayward RE, Cox MJ, Day KP. Malaria transmission and naturally acquired immunity to PfEMP-1. Infect Immun. 1999;67:6369–74.PubMedPubMedCentral
23.
go back to reference Young JA, Fivelman QL, Blair PL, de la Vega P, Le Roch KG, Zhou Y, et al. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol. 2005;143:67–79.CrossRefPubMed Young JA, Fivelman QL, Blair PL, de la Vega P, Le Roch KG, Zhou Y, et al. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol. 2005;143:67–79.CrossRefPubMed
24.
go back to reference Silvestrini F, Lasonder E, Olivieri A, Camarda G, van Schaijk B, Sanchez M, et al. Protein export marks the early phase of gametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol Cell Proteom. 2010;9:1437–48.CrossRef Silvestrini F, Lasonder E, Olivieri A, Camarda G, van Schaijk B, Sanchez M, et al. Protein export marks the early phase of gametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol Cell Proteom. 2010;9:1437–48.CrossRef
25.
go back to reference Stone WJR, Dantzler KW, Nilsson SK, Drakeley CJ, Marti M, Bousema T, et al. Naturally acquired immunity to sexual stage P. falciparum parasites. Parasitology. 2016;143:187–98.CrossRefPubMed Stone WJR, Dantzler KW, Nilsson SK, Drakeley CJ, Marti M, Bousema T, et al. Naturally acquired immunity to sexual stage P. falciparum parasites. Parasitology. 2016;143:187–98.CrossRefPubMed
26.
go back to reference Williamson KC, Keister DB, Muratova O, Kaslow DC. Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol Biochem Parasitol. 1995;75:33–42.CrossRefPubMed Williamson KC, Keister DB, Muratova O, Kaslow DC. Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol Biochem Parasitol. 1995;75:33–42.CrossRefPubMed
27.
go back to reference Drakeley CJ, Bousema JT, Akim NIJ, Teelen K, Roeffen W, Lensen AH, et al. Transmission-reducing immunity is inversely related to age in Plasmodium falciparum gametocyte carriers. Parasite Immunol. 2006;28:185–90.CrossRefPubMed Drakeley CJ, Bousema JT, Akim NIJ, Teelen K, Roeffen W, Lensen AH, et al. Transmission-reducing immunity is inversely related to age in Plasmodium falciparum gametocyte carriers. Parasite Immunol. 2006;28:185–90.CrossRefPubMed
28.
go back to reference Kapulu MC, Da DF, Miura K, Li Y, Blagborough AM, Churcher TS, et al. Comparative assessment of transmission-blocking vaccine candidates against Plasmodium falciparum. Sci Rep. 2015;5:11193.CrossRefPubMedPubMedCentral Kapulu MC, Da DF, Miura K, Li Y, Blagborough AM, Churcher TS, et al. Comparative assessment of transmission-blocking vaccine candidates against Plasmodium falciparum. Sci Rep. 2015;5:11193.CrossRefPubMedPubMedCentral
29.
go back to reference van der Kolk M, de Vlas SJ, Sauerwein RW. Reduction and enhancement of Plasmodium falciparum transmission by endemic human sera. Int J Parasitol. 2006;36:1091–5.CrossRefPubMed van der Kolk M, de Vlas SJ, Sauerwein RW. Reduction and enhancement of Plasmodium falciparum transmission by endemic human sera. Int J Parasitol. 2006;36:1091–5.CrossRefPubMed
30.
go back to reference Mulder B, Lensen T, Tchuinkam T, Roeffen W, Verhave JP, Boudin C, et al. Plasmodium falciparum: membrane feeding assays and competition ELISAs for the measurement of transmission reduction in sera from Cameroon. Exp Parasitol. 1999;92:81–6.CrossRefPubMed Mulder B, Lensen T, Tchuinkam T, Roeffen W, Verhave JP, Boudin C, et al. Plasmodium falciparum: membrane feeding assays and competition ELISAs for the measurement of transmission reduction in sera from Cameroon. Exp Parasitol. 1999;92:81–6.CrossRefPubMed
31.
go back to reference Bousema T, Roeffen W, Meijerink H, Mwerinde H, Mwakalinga S, van Gemert G-J, et al. The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 & Pfs48/45 in a low endemic area in Tanzania. PLoS ONE. 2010;5:e14114.CrossRefPubMedPubMedCentral Bousema T, Roeffen W, Meijerink H, Mwerinde H, Mwakalinga S, van Gemert G-J, et al. The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 & Pfs48/45 in a low endemic area in Tanzania. PLoS ONE. 2010;5:e14114.CrossRefPubMedPubMedCentral
32.
go back to reference Outchkourov NS, Roeffen W, Kaan A, Jansen J, Luty A, Schuiffel D, et al. Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc Natl Acad Sci USA. 2008;105:4301–5.CrossRefPubMedPubMedCentral Outchkourov NS, Roeffen W, Kaan A, Jansen J, Luty A, Schuiffel D, et al. Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc Natl Acad Sci USA. 2008;105:4301–5.CrossRefPubMedPubMedCentral
33.
go back to reference Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002;296:490–4.CrossRefPubMed Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002;296:490–4.CrossRefPubMed
34.
go back to reference Esen M, Mordmüller B, de Salazar PM, Adegnika AA, Agnandji ST, Schaumburg F, et al. Reduced antibody responses against Plasmodium falciparum vaccine candidate antigens in the presence of Trichuris trichiura. Vaccine. 2012;30:7621–4.CrossRefPubMed Esen M, Mordmüller B, de Salazar PM, Adegnika AA, Agnandji ST, Schaumburg F, et al. Reduced antibody responses against Plasmodium falciparum vaccine candidate antigens in the presence of Trichuris trichiura. Vaccine. 2012;30:7621–4.CrossRefPubMed
35.
go back to reference Theisen M, Soe S, Brunstedt K, Follmann F, Bredmose L, Israelsen H, et al. A Plasmodium falciparum GLURP-MSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine. 2004;22:1188–98.CrossRefPubMed Theisen M, Soe S, Brunstedt K, Follmann F, Bredmose L, Israelsen H, et al. A Plasmodium falciparum GLURP-MSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine. 2004;22:1188–98.CrossRefPubMed
36.
go back to reference Bélard S, Issifou S, Hounkpatin AB, Schaumburg F, Ngoa UA, Esen M, et al. A randomized controlled phase Ib trial of the malaria vaccine candidate GMZ2 in African children. PLoS ONE. 2011;6:e22525.CrossRefPubMedPubMedCentral Bélard S, Issifou S, Hounkpatin AB, Schaumburg F, Ngoa UA, Esen M, et al. A randomized controlled phase Ib trial of the malaria vaccine candidate GMZ2 in African children. PLoS ONE. 2011;6:e22525.CrossRefPubMedPubMedCentral
37.
go back to reference Mordmüller B, Szywon K, Greutelaers B, Esen M, Mewono L, Treut C, et al. Safety and immunogenicity of the malaria vaccine candidate GMZ2 in malaria-exposed, adult individuals from Lambaréné, Gabon. Vaccine. 2010;28:6698–703.CrossRefPubMedPubMedCentral Mordmüller B, Szywon K, Greutelaers B, Esen M, Mewono L, Treut C, et al. Safety and immunogenicity of the malaria vaccine candidate GMZ2 in malaria-exposed, adult individuals from Lambaréné, Gabon. Vaccine. 2010;28:6698–703.CrossRefPubMedPubMedCentral
38.
go back to reference Sirima SB, Mordmüller B, Milligan P, Ngoa UA, Kironde F, Atuguba F, et al. A phase 2b randomized, controlled trial of the efficacy of the GMZ2 malaria vaccine in African children. Vaccine. 2016;34:4536–42.CrossRefPubMed Sirima SB, Mordmüller B, Milligan P, Ngoa UA, Kironde F, Atuguba F, et al. A phase 2b randomized, controlled trial of the efficacy of the GMZ2 malaria vaccine in African children. Vaccine. 2016;34:4536–42.CrossRefPubMed
39.
go back to reference Ifediba T, Vanderberg JP. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature. 1981;294:364–6.CrossRefPubMed Ifediba T, Vanderberg JP. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature. 1981;294:364–6.CrossRefPubMed
40.
go back to reference Held J, Westerman R, Kremsner PG, Mordmüller B. In vitro activity of mirincamycin (U24729A) against Plasmodium falciparum isolates from Gabon. Antimicrob Agents Chemother. 2010;54:540–2.CrossRefPubMed Held J, Westerman R, Kremsner PG, Mordmüller B. In vitro activity of mirincamycin (U24729A) against Plasmodium falciparum isolates from Gabon. Antimicrob Agents Chemother. 2010;54:540–2.CrossRefPubMed
41.
go back to reference Lelièvre J, Almela MJ, Lozano S, Miguel C, Franco V, Leroy D, et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an ATP bioluminescence “transmission blocking” assay. PLoS ONE. 2012;7:e35019.CrossRefPubMedPubMedCentral Lelièvre J, Almela MJ, Lozano S, Miguel C, Franco V, Leroy D, et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an ATP bioluminescence “transmission blocking” assay. PLoS ONE. 2012;7:e35019.CrossRefPubMedPubMedCentral
42.
go back to reference Gebru T, Mordmüller B, Held J. Effect of fluorescent dyes on in vitro-differentiated, late-stage Plasmodium falciparum gametocytes. Antimicrob Agents Chemother. 2014;58:7398–404.CrossRefPubMedPubMedCentral Gebru T, Mordmüller B, Held J. Effect of fluorescent dyes on in vitro-differentiated, late-stage Plasmodium falciparum gametocytes. Antimicrob Agents Chemother. 2014;58:7398–404.CrossRefPubMedPubMedCentral
43.
go back to reference Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, Handman E, et al. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol. 2004;137:13–21.CrossRefPubMed Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, Handman E, et al. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol. 2004;137:13–21.CrossRefPubMed
44.
go back to reference Ajua A, Engleitner T, Esen M, Theisen M, Issifou S, Mordmüller B. A flow cytometry-based workflow for detection and quantification of anti-plasmodial antibodies in vaccinated and naturally exposed individuals. Malar J. 2012;11:367.CrossRefPubMedPubMedCentral Ajua A, Engleitner T, Esen M, Theisen M, Issifou S, Mordmüller B. A flow cytometry-based workflow for detection and quantification of anti-plasmodial antibodies in vaccinated and naturally exposed individuals. Malar J. 2012;11:367.CrossRefPubMedPubMedCentral
45.
go back to reference Baird JK. Host Age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today. 1995;11:105–11.CrossRefPubMed Baird JK. Host Age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today. 1995;11:105–11.CrossRefPubMed
46.
go back to reference Jones S, Grignard L, Nebie I, Chilongola J, Dodoo D, Sauerwein R, et al. Naturally acquired antibody responses to recombinant Pfs230 and Pfs48/45 transmission blocking vaccine candidates. J Infect. 2015;71:117–27.CrossRefPubMed Jones S, Grignard L, Nebie I, Chilongola J, Dodoo D, Sauerwein R, et al. Naturally acquired antibody responses to recombinant Pfs230 and Pfs48/45 transmission blocking vaccine candidates. J Infect. 2015;71:117–27.CrossRefPubMed
47.
go back to reference Bonett DG, Wright TA. Sample size requirements for estimating pearson, kendall and spearman correlations. Psychometrika. 2000;65:23–8.CrossRef Bonett DG, Wright TA. Sample size requirements for estimating pearson, kendall and spearman correlations. Psychometrika. 2000;65:23–8.CrossRef
48.
go back to reference Hartgers FC, Obeng BB, Kruize YCM, Dijkhuis A, McCall M, Sauerwein RW, et al. Responses to malarial antigens are altered in helminth-infected children. J Infect Dis. 2009;199:1528–35.CrossRefPubMed Hartgers FC, Obeng BB, Kruize YCM, Dijkhuis A, McCall M, Sauerwein RW, et al. Responses to malarial antigens are altered in helminth-infected children. J Infect Dis. 2009;199:1528–35.CrossRefPubMed
49.
go back to reference Metenou S, Dembele B, Konate S, Dolo H, Coulibaly YI, Diallo AA, et al. Filarial infection suppresses malaria-specific multifunctional Th1 and Th17 responses in malaria and filarial coinfections. J Immunol. 1950;2011(186):4725–33. Metenou S, Dembele B, Konate S, Dolo H, Coulibaly YI, Diallo AA, et al. Filarial infection suppresses malaria-specific multifunctional Th1 and Th17 responses in malaria and filarial coinfections. J Immunol. 1950;2011(186):4725–33.
50.
go back to reference Wammes LJ, Hamid F, Wiria AE, de Gier B, Sartono E, Maizels RM, et al. Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur J Immunol. 2010;40:437–42.CrossRefPubMed Wammes LJ, Hamid F, Wiria AE, de Gier B, Sartono E, Maizels RM, et al. Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur J Immunol. 2010;40:437–42.CrossRefPubMed
51.
go back to reference Drakeley CJ, Eling W, Teelen K, Bousema JT, Sauerwein R, Greenwood BM, et al. Parasite infectivity and immunity to Plasmodium falciparum gametocytes in Gambian children. Parasite Immunol. 2004;26:159–65.CrossRefPubMed Drakeley CJ, Eling W, Teelen K, Bousema JT, Sauerwein R, Greenwood BM, et al. Parasite infectivity and immunity to Plasmodium falciparum gametocytes in Gambian children. Parasite Immunol. 2004;26:159–65.CrossRefPubMed
52.
go back to reference Premawansa S, Gamage-Mendis A, Perera L, Begarnie S, Mendis K, Carter R. Plasmodium falciparum malaria transmission-blocking immunity under conditions of low endemicity as in Sri Lanka. Parasite Immunol. 1994;16:35–42.CrossRefPubMed Premawansa S, Gamage-Mendis A, Perera L, Begarnie S, Mendis K, Carter R. Plasmodium falciparum malaria transmission-blocking immunity under conditions of low endemicity as in Sri Lanka. Parasite Immunol. 1994;16:35–42.CrossRefPubMed
53.
go back to reference Dinko B, Bousema T, Sutherland CJ. Recognition of Plasmodium falciparum gametocyte surface antigens by plasma antibodies in asymptomatic Ghanaian school children. Malar J. 2012;11:P24.CrossRefPubMedCentral Dinko B, Bousema T, Sutherland CJ. Recognition of Plasmodium falciparum gametocyte surface antigens by plasma antibodies in asymptomatic Ghanaian school children. Malar J. 2012;11:P24.CrossRefPubMedCentral
54.
55.
go back to reference Dinko B, King E, Targett GT, Sutherland CJ. Antibody responses to surface antigens of Plasmodium falciparum gametocyte-infected erythrocytes and their relation to gametocytaemia. Parasite Immunol. 2016;38:352–64.CrossRefPubMedPubMedCentral Dinko B, King E, Targett GT, Sutherland CJ. Antibody responses to surface antigens of Plasmodium falciparum gametocyte-infected erythrocytes and their relation to gametocytaemia. Parasite Immunol. 2016;38:352–64.CrossRefPubMedPubMedCentral
56.
go back to reference Karl S, Gurarie D, Zimmerman PA, King CH, Pierre TG, Davis TME. A sub-microscopic gametocyte reservoir can sustain malaria transmission. PLoS ONE. 2011;6:e20805.CrossRefPubMedPubMedCentral Karl S, Gurarie D, Zimmerman PA, King CH, Pierre TG, Davis TME. A sub-microscopic gametocyte reservoir can sustain malaria transmission. PLoS ONE. 2011;6:e20805.CrossRefPubMedPubMedCentral
57.
go back to reference Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMed
58.
go back to reference Borre MB, Dziegiel M, Høgh B, Petersen E, Rieneck K, Riley E, et al. Primary structure and localization of a conserved immunogenic Plasmodium falciparum glutamate rich protein (GLURP) expressed in both the preerythrocytic and erythrocytic stages of the vertebrate life cycle. Mol Biochem Parasitol. 1991;49:119–31.CrossRefPubMed Borre MB, Dziegiel M, Høgh B, Petersen E, Rieneck K, Riley E, et al. Primary structure and localization of a conserved immunogenic Plasmodium falciparum glutamate rich protein (GLURP) expressed in both the preerythrocytic and erythrocytic stages of the vertebrate life cycle. Mol Biochem Parasitol. 1991;49:119–31.CrossRefPubMed
59.
go back to reference Lasonder E, Ishihama Y, Andersen JS, Vermunt AMW, Pain A, Sauerwein RW, et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature. 2002;419:537–42.CrossRefPubMed Lasonder E, Ishihama Y, Andersen JS, Vermunt AMW, Pain A, Sauerwein RW, et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature. 2002;419:537–42.CrossRefPubMed
60.
go back to reference Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave JP, Smits MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985;162:1460–76.CrossRefPubMed Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave JP, Smits MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985;162:1460–76.CrossRefPubMed
61.
go back to reference Ateba-Ngoa U, Jones S, Zinsou JF, Honkpehedji J, Adegnika AA, Agobe J-CD, et al. Associations between helminth infections, Plasmodium falciparum parasite carriage and antibody responses to sexual and asexual stage malarial antigens. Am J Trop Med Hyg. 2016;95:394–400.CrossRefPubMed Ateba-Ngoa U, Jones S, Zinsou JF, Honkpehedji J, Adegnika AA, Agobe J-CD, et al. Associations between helminth infections, Plasmodium falciparum parasite carriage and antibody responses to sexual and asexual stage malarial antigens. Am J Trop Med Hyg. 2016;95:394–400.CrossRefPubMed
Metadata
Title
Recognition of Plasmodium falciparum mature gametocyte-infected erythrocytes by antibodies of semi-immune adults and malaria-exposed children from Gabon
Authors
Tamirat Gebru
Anthony Ajua
Michael Theisen
Meral Esen
Ulysse Ateba Ngoa
Saadou Issifou
Ayola A. Adegnika
Peter G. Kremsner
Benjamin Mordmüller
Jana Held
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1827-7

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