Transcriptional changes induced by candidate malaria vaccines and correlation with protection against malaria in a human challenge model

Vaccine

Volumn 33, Issue 40, 2015, Pages 5321-5331

  Dunachie, Susanna ^a,b   Berthoud, Tamara ^a   Hill, Adrian V S ^a   Fletcher, Helen A ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAHIDOL OXFORD TROPICAL MEDICINE RESEARCH UNIT   (Thailand)

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

Author keywords

Biomarkers; Malaria; Microarray; Plasmodium falciparum; Vaccine

Indexed keywords

GAMMA INTERFERON; MALARIA VACCINE; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; IMMUNOLOGICAL ADJUVANT; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ADULT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENETIC ASSOCIATION; HUMAN; MALARIA CONTROL; MALARIA FALCIPARUM; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; VACCINATION; VACCINIA VIRUS; ADOLESCENT; BLOOD; CLINICAL TRIAL; FEMALE; GENETIC TRANSCRIPTION; IMMUNOLOGY; MALARIA; MALARIA, FALCIPARUM; MALE; MIDDLE AGED; MONONUCLEAR CELL; PLASMODIUM FALCIPARUM; SPOROZOITE; YOUNG ADULT;

ADJUVANTS, IMMUNOLOGIC; ADOLESCENT; ADULT; ANTIBODIES, PROTOZOAN; FEMALE; GENE EXPRESSION PROFILING; HUMANS; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; MALARIA; MALARIA VACCINES; MALARIA, FALCIPARUM; MALE; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SPOROZOITES; TRANSCRIPTION, GENETIC; VACCINATION; YOUNG ADULT;

EID: 84941811406     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.07.087     Document Type: Article

References (40)

1. Snow R.W., Guerra C.A., Noor A.M., Myint H.Y., Hay S.I. The global distribution of clinical episodes of plasmodium falciparum malaria. Nature 2005, 434:214-217.
2. WHO World malaria report 2011 2011, World Health Organization, Geneva.
3. Nakaya H.I., Wrammert J., Lee E.K., Racioppi L., Marie-Kunze S., Haining W.N., et al. Systems biology of vaccination for seasonal influenza in humans. Nat Immunol 2011, 12:786-795.
4. Querec T.D., Akondy R.S., Lee E.K., Cao W., Nakaya H.I., Teuwen D., et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 2009, 10:116-125.
5. Matsumiya M., Harris S.A., Satti I., Stockdale L., Tanner R., O'Shea M.K., et al. Inflammatory and myeloid-associated gene expression before and one day after infant vaccination with MVA85A correlates with induction of a T cell response. BMC Infect Dis 2014, 14:314.
6. Rts S.C.T.P. Efficacy and safety of the RTS, S/AS01 malaria vaccine during 18 months after vaccination: a phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med 2014, 11:e1001685.
7. Kester K.E., Cummings J.F., Ockenhouse C.F., Nielsen R., Hall B.T., Gordon D.M., et al. Phase 2a trial of 0 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 2008, 26:2191-2202.
8. Kester K.E., Cummings J.F., Ofori-Anyinam O., Ockenhouse C.F., Krzych U., Moris P., et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis 2009, 200:337-346.
9. Sun P., Schwenk R., White K., Stoute J.A., Cohen J., Ballou W.R., et al. Protective immunity induced with malaria vaccine, RTS, S, is linked to plasmodium falciparum circumsporozoite protein-specific CD4(+) and CD8(+) T cells producing IFN-gamma. J Immunol 2003, 171:6961-6967.
10. Ansong D., Asante K.P., Vekemans J., Owusu S.K., Owusu R., Brobby N.A., et al. T cell responses to the RTS,S/AS01(E) and RTS, S/AS02(D) malaria candidate vaccines administered according to different schedules to Ghanaian children. PLoS ONE 2011, 6:e18891.
11. Leroux-Roels G., Leroux-Roels I., Clement F., Ofori-Anyinam O., Lievens M., Jongert E., et al. Evaluation of the immune response to RTS,S/AS01 and RTS, S/AS02 adjuvanted vaccines: randomized, double-blind study in malaria-naive adults. Hum Vaccines Immunother 2014, 10:2211-2219.
12. Dunachie S.J., Walther M., Vuola J.M., Webster D.P., Keating S.M., Berthoud T., et al. A clinical trial of prime-boost immunisation with the candidate malaria vaccines RTS, S/AS02A and MVA-CS. Vaccine 2006, 24:2850-2859.
13. Dunachie S.J., Walther M., Epstein J.E., Keating S., Berthoud T., Andrews L., et al. A DNA prime-modified vaccinia virus ankara boost vaccine encoding thrombospondin-related adhesion protein but not circumsporozoite protein partially protects healthy malaria-naive adults against plasmodium falciparum sporozoite challenge. Infect Immunol 2006, 74:5933-5942.
14. McConkey S.J., Reece W.H., Moorthy V.S., Webster D., Dunachie S., Butcher G., et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat Med 2003, 9:729-735.
15. Porter D.W., Thompson F.M., Berthoud T.K., Hutchings C.L., Andrews L., Biswas S., et al. A human Phase I/IIa malaria challenge trial of a polyprotein malaria vaccine. Vaccine 2011, 29:7514-7522.
16. Dunachie S.J., Berthoud T., Keating S.M., Hill A.V., Fletcher H.A. MIG and the regulatory cytokines IL-10 and TGF-beta1 correlate with malaria vaccine immunogenicity and efficacy. PLoS ONE 2010, 5:e12557.
17. Van Gelder R.N., von Zastrow M.E., Yool A., Dement W.C., Barchas J.D., Eberwine J.H. Amplified RNA synthesized from limited quantities of heterogeneous cDNA. Proc Natl Acad Sci USA 1990, 87:1663-1667.
18. Draghici S., Khatri P., Tarca A.L., Amin K., Done A., Voichita C., et al. A systems biology approach for pathway level analysis. Genome Res 2007, 17:1537-1545.
19. Bejon P., Andrews L., Andersen R.F., Dunachie S., Webster D., Walther M., et al. Calculation of liver-to-blood inocula, parasite growth rates, and preerythrocytic vaccine efficacy, from serial quantitative polymerase chain reaction studies of volunteers challenged with malaria sporozoites. J Infect Dis 2005, 191:619-626.
20. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550.
21. Clark N.R., Ma'ayan A. Introduction to statistical methods for analyzing large data sets: gene-set enrichment analysis. Sci Signal 2011, 4:1-5. teaching resource 4, http://stke.sciencemag.org/content/sigtrans/4/190/tr4.full.pdf.
22. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B: Methodological 1995, 57:289-300.
23. Chaussabel D., Quinn C., Shen J., Patel P., Glaser C., Baldwin N., et al. A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 2008, 29:150-164.
24. Dodoo D., Omer F.M., Todd J., Akanmori B.D., Koram K.A., Riley E.M. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to plasmodium falciparum malaria. J Infect Dis 2002, 185:971-979.
25. Flanagan K.L., Mwangi T., Plebanski M., Odhiambo K., Ross A., Sheu E., et al. Ex vivo interferon-gamma immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of plasmodium falciparum infection. Am J Trop Med Hyg 2003, 68:421-430.
26. Reece W.H., Pinder M., Gothard P.K., Milligan P., Bojang K., Doherty T., et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural plasmodium falciparum infection and disease. Nat Med 2004, 10:406-410.
27. Lalvani A., Moris P., Voss G., Pathan A.A., Kester K.E., Brookes R., et al. Potent induction of focused Th1-type cellular and humoral immune responses by RTS, S/SBAS2, a recombinant plasmodium falciparum malaria vaccine. J Infect Dis 1999, 180:1656-1664.
28. Wang R., Epstein J., Baraceros F.M., Gorak E.J., Charoenvit Y., Carucci D.J., et al. Induction of CD4(+) T cell-dependent CD8(+) type 1 responses in humans by a malaria DNA vaccine. Proc Natl Acad Sci USA 2001, 98:10817-10822.
29. McConkey S.J., Reece W.H., Moorthy V.S., Webster D., Dunachie S., Butcher G., et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat Med 2003, 9:729-735.
30. Ockenhouse C.F., Hu W.C., Kester K.E., Cummings J.F., Stewart A., Heppner D.G., et al. Common and divergent immune response signaling pathways discovered in peripheral blood mononuclear cell gene expression patterns in presymptomatic and clinically apparent malaria. Infect Immunol 2006, 74:5561-5573.
31. Griffiths M.J., Shafi M.J., Popper S.J., Hemingway C.A., Kortok M.M., Wathen A., et al. Genomewide analysis of the host response to malaria in Kenyan children. J Infect Dis 2005, 191:1599-1611.
32. Ohashi J., Naka I., Patarapotikul J., Hananantachai H., Looareesuwan S., Tokunaga K. A single-nucleotide substitution from C to T at position -1055 in the IL-13 promoter is associated with protection from severe malaria in Thailand. Genes Immunol 2003, 4:528-531.
33. Winkler S., Willheim M., Baier K., Schmid D., Aichelburg A., Graninger W., et al. Frequency of cytokine-producing T cells in patients of different age groups with plasmodium falciparum malaria. J Infect Dis 1999, 179:209-216.
34. Vahey M.T., Wang Z., Kester K.E., Cummings J., Heppner D.G., Nau M.E., et al. Expression of genes associated with immunoproteasome processing of major histocompatibility complex peptides is indicative of protection with adjuvanted RTS, S malaria vaccine. J Infect Dis 2010, 201:580-589.
35. Idaghdour Y., Quinlan J., Goulet J.P., Berghout J., Gbeha E., Bruat V., et al. Evidence for additive and interaction effects of host genotype and infection in malaria. Proc Natl Acad Sci USA 2012, 109:16786-16793.
36. Loureiro J., Ploegh H.L. Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv Immunol 2006, 92:225-305.
37. Warimwe G.M., Fletcher H.A., Olotu A., Agnandji S.T., Hill A.V., Marsh K., et al. Peripheral blood monocyte-to-lymphocyte ratio at study enrollment predicts efficacy of the RTS, S malaria vaccine: analysis of pooled phase II clinical trial data. BMC Med 2013, 11:184.
38. Warimwe G.M., Murungi L.M., Kamuyu G., Nyangweso G.M., Wambua J., Naranbhai V., et al. The ratio of monocytes to lymphocytes in peripheral blood correlates with increased susceptibility to clinical malaria in Kenyan children. PLoS ONE 2013, 8:e57320.
39. Scherer C.A., Magness C.L., Steiger K.V., Poitinger N.D., Caputo C.M., Miner D.G., et al. Distinct gene expression profiles in peripheral blood mononuclear cells from patients infected with vaccinia virus, yellow fever 17D virus, or upper respiratory infections. Vaccine 2007, 25:6458-6473.
40. Diaz-Mitoma F., Alvarez-Maya I., Dabrowski A., Jaffey J., Frost R., Aucoin S., et al. Transcriptional analysis of human peripheral blood mononuclear cells after influenza immunization. J Clin Virol 2004, 31:100-112.