Analysis of antibodies to newly described plasmodium falciparum merozoite antigens supports MSPDBL2 as a predicted target of naturally acquired immunity

Infection and Immunity

Volumn 81, Issue 10, 2013, Pages 3835-3842

  Tetteh, Kevin K A ^a   Osier, Faith H A ^b   Salanti, Ali ^c   Kamuyu, Gathoni ^b   Drought, Laura ^a   Failly, Marilyne ^d   Martin, Christophe ^d   Marsh, Kevin ^b   Conway, David J ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b KEMRI Clinical Research Centre   (Kenya)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d PX Therapeutics   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PARASITE ANTIBODY; EPITOPE; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY; RECOMBINANT PROTEIN;

ADAPTIVE IMMUNITY; AGE DISTRIBUTION; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIGENICITY; ARTICLE; DISEASE ASSOCIATION; FOLLOW UP; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; INFECTION RISK; KENYA; MALARIA; MEROZOITE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SCHIZONT; ADOLESCENT; ADULT; AGED; ANIMAL; CHILD; GENETICS; HUMAN; IMMUNOLOGY; INFANT; METABOLISM; MIDDLE AGED; MOUSE; PRESCHOOL CHILD; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; EPITOPES; HUMANS; INFANT; MEROZOITES; MICE; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; YOUNG ADULT;

EID: 84884364582     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00301-13     Document Type: Article

References (43)

1. Birkett AJ, Moorthy VS, Loucq C, Chitnis CE, Kaslow DC. 2013. Malaria vaccine R&D in the Decade of Vaccines: breakthroughs, challenges and opportunities. Vaccine 31(Suppl. 2):B233-B243.
2. Doolan DL, Dobano C, Baird JK. 2009. Acquired immunity to malaria. Clin. Microbiol. Rev. 22:13-36.
3. Fowkes FJ, Richards JS, Simpson JA, Beeson JG. 2010. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med. 7:e1000218. doi:10.1371/journal.pmed.1000218.
4. Osier FH, Fegan G, Polley SD, Murungi L, Verra F, Tetteh KK, Lowe B, Mwangi T, Bull PC, Thomas AW, Cavanagh DR, McBride JS, Lanar DE, Mackinnon MJ, Conway DJ, Marsh K. 2008. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect. Immun. 76:2240-2248.
5. Gray JC, Corran PH, Mangia E, Gaunt MW, Li Q, Tetteh KK, Polley SD, Conway DJ, Holder AA, Bacarese-Hamilton T, Riley EM, Crisanti A. 2007. Profiling the antibody immune response against blood stage malaria vaccine candidates. Clin. Chem. 53:1244-1253.
6. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419:520-526.
7. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:e5. doi:10.1371/journal.pbio.0000005.
8. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503-1508.
9. Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M, Uchikawa M, Mboup S, Ndir O, Kwiatkowski DP, Duraisingh MT, Rayner JC, Wright GJ. 2011. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480:534-537.
10. Le Roch KG, Chung DW, Ponts N. 2012. Genomics and integrated systems biology in Plasmodium falciparum: a path to malaria control and eradication. Parasite Immunol. 34:50-60.
11. Mu J, Seydel KB, Bates A, Su XZ. 2010. Recent progress in functional genomic research in Plasmodium falciparum. Curr. Genomics 11:279-286.
12. Polley SD, Tetteh KK, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, Conway DJ. 2007. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J. Infect. Dis. 195:279-287.
13. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, Seydel K, McVean GA, Su XZ. 2007. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat. Genet. 39:126-130.
14. 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. 6:689-692.
15. Tetteh KK, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, Marsh K, Weedall GD, Conway DJ. 2009. Prospective identification of malaria parasite genes under balancing selection. PLoS One 4:e5568. doi: 10.1371/journal.pone.0005568.
16. Ochola LI, Tetteh KK, Stewart LB, Riitho V, Marsh K, Conway DJ. 2010. Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol. Biol. Evol. 27:2344-2351.
17. Manske M, Miotto O, Campino S, Auburn S, Almagro-Garcia J, Maslen G, O'Brien J, Djimde A, Doumbo O, Zongo I, Ouedraogo JB, Michon P, Mueller I, Siba P, Nzila A, Borrmann S, Kiara SM, Marsh K, Jiang H, Su XZ, Amaratunga C, Fairhurst R, Socheat D, Nosten F, Imwong M, White NJ, Sanders M, Anastasi E, Alcock D, Drury E, Oyola S, Quail MA, Turner DJ, Ruano-Rubio V, Jyothi D, Amenga-Etego L, Hubbart C, Jeffreys A, Rowlands K, Sutherland C, Roper C, Mangano V, Modiano D, Tan JC, Ferdig MT, Amambua-Ngwa A, Conway DJ, Takala-Harrison S, Plowe CV, Rayner JC, Rockett KA, Clark TG, Newbold CI, Berriman M, MacInnis B, Kwiatkowski DP. 2012. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487:375-379.
18. Amambua-Ngwa A, Tetteh KKA, Manske M, Gomez-Escobar N, Stewart LB, Deerhake ME, Cheeseman IH, Holder AA, Knuepfer E, Newbold CI, Janha O, Jallow M, Campino S, MacInnis B, Kwiatkowski D, Conway DJ. 2012. Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet. 8:e1002992. doi:10.1371/journal.pgen.1002992.
19. Park DJ, Lukens AK, Neafsey DE, Schaffner SF, Chang HH, Valim C, Ribacke U, Van Tyne D, Galinsky K, Galligan M, Becker JS, Ndiaye D, Mboup S, Wiegand RC, Hartl DL, Sabeti PC, Wirth DF, Volkman SK. 2012. Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Proc. Natl. Acad. Sci. U. S. A. 109:13052-13057.
20. Singh S, Soe S, Weisman S, Barnwell JW, Perignon JL, Druilhe P. 2009. A conserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum. PLoS One 4:e5410. doi:10.1371/journal.pone.0005410.
21. Winter G, Kawai S, Haeggstrom M, Kaneko O, von Euler A, Kawazu S, Palm D, Fernandez V, Wahlgren M. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J. Exp. Med. 201:1853-1863.
22. Alexandre JS, Yahata K, Kawai S, Torii M, Kaneko O. 2011. PEXELindependent trafficking of Plasmodium falciparum SURFIN4.2 to the parasite-infected red blood cell and Maurer's clefts. Parasitol. Int. 60:313-320.
23. Wickramarachchi T, Cabrera AL, Sinha D, Dhawan S, Chandran T, Devi YS, Kono M, Spielmann T, Gilberger TW, Chauhan VS, Mohammed A. 2009. A novel Plasmodium falciparum erythrocyte binding protein associated with the merozoite surface, PfDBLMSP. Int. J. Parasitol. 39:763-773.
24. Hodder AN, Czabotar PE, Uboldi AD, Clarke OB, Lin CS, Healer J, Smith BJ, Cowman AF. 2012. Insights into Duffy binding-like domains through the crystal structure and function of the merozoite surface protein MSPDBL2 from Plasmodium falciparum. J. Biol. Chem. 287:32922-32939.
25. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, Barnes KG, Rosen DM, Lukens AK, Daniels RF, Milner DA, Jr, Johnson CA, Shlyakhter I, Grossman SR, Becker JS, Yamins D, Karlsson EK, Ndiaye D, Sarr O, Mboup S, Happi C, Furlotte NA, Eskin E, Kang HM, Hartl DL, Birren BW, Wiegand RC, Lander ES, Wirth DF, Volkman SK, Sabeti PC. 2011. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLoS Genet. 7:e1001383. doi:10.1371/journal.pgen.1001383.
26. Van Tyne D, Uboldi AD, Healer J, Cowman AF, Wirth DF. 2013. Modulation of PF10_0355 (MSPDBL2) alters Plasmodium falciparum response to antimalarial drugs. Antimicrob. Agents Chemother. 57:2937-2941.
27. Polley SD, Tetteh KK, Cavanagh DR, Pearce RJ, Lloyd JM, Bojang KA, Okenu DM, Greenwood BM, McBride JS, Conway DJ. 2003. Repeat sequences in block 2 of Plasmodium falciparum merozoite surface protein 1 are targets of antibodies associated with protection from malaria. Infect. Immun. 71:1833-1842.
28. Dahlback M, Rask TS, Andersen PH, Nielsen MA, Ndam NT, Resende M, Turner L, Deloron P, Hviid L, Lund O, Pedersen AG, Theander TG, Salanti A. 2006. Epitope mapping and topographic analysis of VAR2CSA DBL3X involved in P. falciparum placental sequestration. PLoS Pathog. 2:e124. doi:10.1371/journal.ppat.0020124.
29. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, Handman E, Cowman AF, McFadden GI. 2004. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol. 137:13-21.
30. Polley SD, Mwangi T, Kocken CH, Thomas AW, Dutta S, Lanar DE, Remarque E, Ross A, Williams TN, Mwambingu G, Lowe B, Conway DJ, Marsh K. 2004. Human antibodies to recombinant protein constructs of Plasmodium falciparum Apical Membrane Antigen 1 (AMA1) and their associations with protection from malaria. Vaccine 23:718-728.
31. Mwangi TW, Ross A, Snow RW, Marsh K. 2005. Case definitions of clinical malaria under different transmission conditions in KilifiDistrict, Kenya. J. Infect. Dis. 191:1932-1939.
32. Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, Olotu A, Osier FH, Hay SI, Farnert A, Marsh K. 2010. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med. 7:e1000304. doi:10.1371/journal.pmed.1000304.
33. Polley SD, Conway DJ, Cavanagh DR, McBride JS, Lowe BS, Williams TN, Mwangi TW, Marsh K. 2006. High levels of serum antibodies to merozoite surface protein 2 of Plasmodium falciparum are associated with reduced risk of clinical malaria in coastal Kenya. Vaccine 24:4233-4246.
34. Kusi KA, Faber BW, Thomas AW, Remarque EJ. 2009. Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS One 4:e8110. doi:10.1371/journal.pone.0008110.
35. Miura K, Herrera R, Diouf A, Zhou H, Mu J, Hu Z, Macdonald NJ, Reiter K, Nguyen V, Shimp RL, Jr, Singh K, Narum DL, Long CA, Miller LH. 2013. Overcoming allelic-specificity by immunization with 5-allelic forms of Plasmodium falciparum Apical Membrane Antigen 1. Infect. Immun. 81:1491-1501.
36. Tetteh KK, Conway DJ. 2011. A polyvalent hybrid protein elicits antibodies against the diverse allelic types of block 2 in Plasmodium falciparum merozoite surface protein 1. Vaccine 29:7811-7817.
37. Cowan GJ, Creasey AM, Dhanasarnsombut K, Thomas AW, Remarque EJ, Cavanagh DR. 2011. A malaria vaccine based on the polymorphic block 2 region of MSP-1 that elicits a broad serotype-spanning immune response. PLoS One 6:e26616. doi:10.1371/journal.pone.0026616.
38. Anders RF, Adda CG, Foley M, Norton RS. 2010. Recombinant protein vaccines against the asexual blood stages of Plasmodium falciparum. Hum. Vaccin. 6:39-53.
39. Drew DR, Hodder AN, Wilson DW, Foley M, Mueller I, Siba PM, Dent AE, Cowman AF, Beeson JG. 2012. Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. PLoS One 7:e51023. doi:10.1371/journal.pone.0051023.
40. Ntumngia FB, Adams JH. 2012. Design and immunogenicity of a novel synthetic antigen based on the ligand domain of the Plasmodium vivax duffy binding protein. Clin. Vaccine Immunol. 19:30-36.
41. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R. 2010. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38:W695-W699.
42. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
43. Demanga CG, Daher LJ, Prieur E, Blanc C, Perignon JL, Bouharoun-Tayoun H, Druilhe P. 2010. Toward the rational design of a malaria vaccine construct using the MSP3 family as an example: contribution of antigenicity studies in humans. Infect. Immun. 78:486-494