Plasmodium Falciparum Protein Microarray Antibody Profiles Correlate With Protection From Symptomatic Malaria in Kenya

Overview

Journal J Infect Dis

Publisher Oxford University Press

Specialty Infectious Diseases

Date 2015 Apr 18

PMID 25883384

Citations 63

Authors

Arlene E Dent

Rie Nakajima

Li Liang

Elisabeth Baum

Ann M Moormann

Peter Odada Sumba

John Vulule

Denise Babineau

Arlo Randall

D Huw Davies

Philip L Felgner

James W Kazura

Affiliations

Soon will be listed here.

Abstract

Background: Immunoglobulin G antibodies (Abs) to Plasmodium falciparum antigens have been associated with naturally acquired immunity to symptomatic malaria.

Methods: We probed protein microarrays covering 824 unique P. falciparum protein features with plasma from residents of a community in Kenya monitored for 12 weeks for (re)infection and symptomatic malaria after administration of antimalarial drugs. P. falciparum proteins recognized by Abs from 88 children (aged 1-14 years) and 86 adults (aged ≥ 18 years), measured at the beginning of the observation period, were ranked by Ab signal intensity.

Results: Abs from immune adults reacted with a total 163 of 824 P. falciparum proteins. Children gradually acquired Abs to the full repertoire of antigens recognized by adults. Abs to some antigens showed high seroconversion rates, reaching maximal levels early in childhood, whereas others did not reach adult levels until adolescence. No correlation between Ab signal intensity and time to (re)infection was observed. In contrast, Ab levels to 106 antigens were significantly higher in children who were protected from symptomatic malaria compared with those who were not. Abs to antigens predictive of protection included P. falciparum erythrocyte membrane protein 1, merozoite surface protein (MSP) 10, MSP2, liver-stage antigen 3, PF70, MSP7, and Plasmodium helical interspersed subtelomeric domain protein.

Conclusions: Protein microarrays may be useful in the search for malaria antigens associated with protective immunity.

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References

Daubersies P, Thomas A, Millet P, Brahimi K, Langermans J, Ollomo B . Protection against Plasmodium falciparum malaria in chimpanzees by immunization with the conserved pre-erythrocytic liver-stage antigen 3. Nat Med. 2000; 6(11):1258-63. DOI: 10.1038/81366. View

Baldi P, Long A . A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics. 2001; 17(6):509-19. DOI: 10.1093/bioinformatics/17.6.509. View

Genton B, Betuela I, Felger I, Al-Yaman F, Anders R, Saul A . A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis. 2002; 185(6):820-7. DOI: 10.1086/339342. View

Florens L, Washburn M, Raine J, Anthony R, Grainger M, Haynes J . A proteomic view of the Plasmodium falciparum life cycle. Nature. 2002; 419(6906):520-6. DOI: 10.1038/nature01107. View

Pearce J, Mills K, Triglia T, Cowman A, Anders R . Characterisation of two novel proteins from the asexual stage of Plasmodium falciparum, H101 and H103. Mol Biochem Parasitol. 2005; 139(2):141-51. DOI: 10.1016/j.molbiopara.2004.09.012. View

Drakeley C, Corran P, Coleman P, Tongren J, McDonald S, Carneiro I . Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005; 102(14):5108-13. PMC: 555970. DOI: 10.1073/pnas.0408725102. View

Goeman J, Oosting J, Cleton-Jansen A, Anninga J, van Houwelingen H . Testing association of a pathway with survival using gene expression data. Bioinformatics. 2005; 21(9):1950-7. DOI: 10.1093/bioinformatics/bti267. View

Sundaresh S, Doolan D, Hirst S, Mu Y, Unal B, Davies D . Identification of humoral immune responses in protein microarrays using DNA microarray data analysis techniques. Bioinformatics. 2006; 22(14):1760-6. DOI: 10.1093/bioinformatics/btl162. View

Tarun A, Peng X, Dumpit R, Ogata Y, Silva-Rivera H, Camargo N . A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci U S A. 2008; 105(1):305-10. PMC: 2224207. DOI: 10.1073/pnas.0710780104. View

10.

Tsuboi T, Takeo S, Iriko H, Jin L, Tsuchimochi M, Matsuda S . Wheat germ cell-free system-based production of malaria proteins for discovery of novel vaccine candidates. Infect Immun. 2008; 76(4):1702-8. PMC: 2292889. DOI: 10.1128/IAI.01539-07. View

11.

Langhorne J, Ndungu F, Sponaas A, Marsh K . Immunity to malaria: more questions than answers. Nat Immunol. 2008; 9(7):725-32. DOI: 10.1038/ni.f.205. View

12.

Doolan D, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C . Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics. 2008; 8(22):4680-94. PMC: 3021802. DOI: 10.1002/pmic.200800194. View

13.

Maier A, Cooke B, Cowman A, Tilley L . Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol. 2009; 7(5):341-54. DOI: 10.1038/nrmicro2110. View

14.

Gondeau C, Corradin G, Heitz F, LE Peuch C, Balbo A, Schuck P . The C-terminal domain of Plasmodium falciparum merozoite surface protein 3 self-assembles into alpha-helical coiled coil tetramer. Mol Biochem Parasitol. 2009; 165(2):153-61. PMC: 2680791. DOI: 10.1016/j.molbiopara.2009.01.015. View

15.

de Koning-Ward T, Gilson P, Boddey J, Rug M, Smith B, Papenfuss A . A newly discovered protein export machine in malaria parasites. Nature. 2009; 459(7249):945-9. PMC: 2725363. DOI: 10.1038/nature08104. View

16.

Crompton P, Kayala M, Traore B, Kayentao K, Ongoiba A, Weiss G . A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci U S A. 2010; 107(15):6958-63. PMC: 2872454. DOI: 10.1073/pnas.1001323107. View

17.

Cummings J, Spring M, Schwenk R, Ockenhouse C, Kester K, Polhemus M . Recombinant Liver Stage Antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-gamma/IL-2 CD4+ T cells but does not protect against experimental Plasmodium falciparum infection. Vaccine. 2009; 28(31):5135-44. DOI: 10.1016/j.vaccine.2009.08.046. View

18.

Crompton P, Pierce S, Miller L . Advances and challenges in malaria vaccine development. J Clin Invest. 2010; 120(12):4168-78. PMC: 2994342. DOI: 10.1172/JCI44423. View

19.

Lopaticki S, Maier A, Thompson J, Wilson D, Tham W, Triglia T . Reticulocyte and erythrocyte binding-like proteins function cooperatively in invasion of human erythrocytes by malaria parasites. Infect Immun. 2010; 79(3):1107-17. PMC: 3067488. DOI: 10.1128/IAI.01021-10. View

20.

Greenhouse B, Ho B, Hubbard A, Njama-Meya D, Narum D, Lanar D . Antibodies to Plasmodium falciparum antigens predict a higher risk of malaria but protection from symptoms once parasitemic. J Infect Dis. 2011; 204(1):19-26. PMC: 3105040. DOI: 10.1093/infdis/jir223. View