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Microbial Immunity and Vaccines

Antibodies to Intercellular Adhesion Molecule 1-Binding Plasmodium falciparum Erythrocyte Membrane Protein 1-DBLβ Are Biomarkers of Protective Immunity to Malaria in a Cohort of Young Children from Papua New Guinea

Sofonias K. Tessema, Digjaya Utama, Olga Chesnokov, Anthony N. Hodder, Clara S. Lin, G. L. Abby Harrison, Jakob S. Jespersen, Bent Petersen, Livingstone Tavul, Peter Siba, Dominic Kwiatkowski, Thomas Lavstsen, Diana S. Hansen, Andrew V. Oleinikov, Ivo Mueller, Alyssa E. Barry
John H. Adams, Editor
Sofonias K. Tessema
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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Digjaya Utama
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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Olga Chesnokov
cCharles E. Schmidt College of Medicine, Florida Atlantic University, Boca Raton, Florida, USA
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Anthony N. Hodder
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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Clara S. Lin
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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G. L. Abby Harrison
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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Jakob S. Jespersen
dCentre for Medical Parasitology, Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
kDepartment of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark
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Bent Petersen
eCenter for Biological Sequence Analysis, Technical University of Denmark, Kgs. Lyngby, Denmark
fCentre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia
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Livingstone Tavul
gVector Borne Diseases Unit, Papua New Guinea Institute of Medical Research, Goroka, Papua New Guinea
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Peter Siba
gVector Borne Diseases Unit, Papua New Guinea Institute of Medical Research, Goroka, Papua New Guinea
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Dominic Kwiatkowski
hWellcome Trust Sanger Institute, Hinxton, United Kingdom
iMRC Centre for Genomics and Global Health, University of Oxford, Oxford, United Kingdom
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Thomas Lavstsen
dCentre for Medical Parasitology, Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
kDepartment of Infectious Diseases, Copenhagen University Hospital, Copenhagen, Denmark
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  • ORCID record for Thomas Lavstsen
Diana S. Hansen
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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Andrew V. Oleinikov
cCharles E. Schmidt College of Medicine, Florida Atlantic University, Boca Raton, Florida, USA
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Ivo Mueller
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
jInstitut Pasteur, Paris, France
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Alyssa E. Barry
aThe Walter and Eliza Hall Institute of Medical Research, Victoria, Australia
bThe University of Melbourne, Department of Medical Biology, Victoria, Australia
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John H. Adams
University of South Florida
Roles: Editor
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DOI: 10.1128/IAI.00485-17
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  • FIG 1
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    FIG 1

    Antibody responses to five PfEMP1 domains in 187 young Papua New Guinean children. (A) Domain compositions and seroprevalences of the five tested PfEMP1 domains. Seroprevalences are indicated as percentages above the relevant domains. ATS indicates the intracellular acidic terminal segment of PfEMP1. (B) Correlation coefficients for seropositivity to five PfEMP1 domains. Significant correlations (P < 0.001) are indicated by asterisks.

  • FIG 2
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    FIG 2

    Relationships between antibody responses to five PfEMP1 domains, age, and infection status. (A) IgG levels stratified by age (age groups were determined by the median age [1.7 years]). (B) IgG levels stratified by P. falciparum infection status. Box-and-whisker plots are shown for the five PfEMP1 domains. The boxes show the interquartile ranges, the horizontal lines are medians, the whiskers indicate the 95% confidence intervals, and the circles are the outliers (95 to 99%). P values for the differences were determined using the Wilcoxon rank sum test between the groups; ns, not significant.

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    FIG 3

    Antibody responses to five PfEMP1 domains and prospective risk of symptomatic malaria. Antibody levels were grouped into three equal groups (high, medium, and low). The incidence rates of clinical malaria and high-density clinical malaria were compared for high and low responders for each tested domain using negative binomial regression. The incidence rate ratios were adjusted for village of residence, seasonal variation, age (continuous), infection status at the time of antibody measurement, and differences in individual exposures (molFOB). The aIRRs for the comparison of high and low responders and the 95% confidence intervals are shown. The P values are indicated only when significant (P < 0.05).

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    FIG 4

    Antibody responses to five PfEMP1 domains and development of severe malaria. Means and standard errors are shown for children who experienced severe malaria and those who did not. P values for t test comparisons of the means are indicated for each domain.

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    FIG 5

    Conservation of ICAM1-binding motifs and dual EPCR-ICAM1-binding cassettes in Papua New Guinea. var gene sequences were assembled for 125 P. falciparum isolates from Papua New Guinea, and domains were classified as previously described (42). (A) Maximum likelihood tree of 473 DBLβ1 and DBLβ3 sequences, including 406 from PNG (pink, DBLβ1; red, DBLβ3) and 67 from isolates from diverse geographic locations (cyan, DBLβ1; blue, DBLβ3). Sequences containing the minimal ICAM1-binding motif are indicated by solid circles. Genes described in this study are labeled at the DBLβ1/3 variant positions in the tree. (B) Domain architecture of PNG var genes containing DBLβ1/3 domains with ICAM1 motifs. The presence of domain cassettes among the 80 var genes containing DBLβ1/3 with the ICAM1-binding motif relative to that among a subset of 331 PNG var genes containing any DBLβ1/3 is indicated on the right; n.a., not applicable. Significance was determined by a binomial exact test.

Additional Files

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    • Supplemental file 1 -

      Text S1. Sequences of recombinant domains used in this study. Fig. S1. Immunoblots of PF13_0003 and PFL1955w NTS-DBL and CIDR domains. Fig. S2. Subtree of the ICAM1-binding cluster of DBLβ sequences. Captions for Tables S1 to S6 and Data Sets S1 and S2.

      PDF, 2.1M

    • Supplemental file 2 -

      Table S1. P values for pairwise comparisons of antibody responses between domains. Table S2. Characteristics of children with severe malaria. Table S3. Summary of var genes and DBLβ domains obtained from 125 P. falciparum genomes from Papua New Guinea. Table S4. ICAM1 motifs in DBLβ sequences from Papua New Guinea. Table S5. ICAM1 motifs in DBLβ sequences of supplementary data set. Table S6. Domain sequences and architecture of var-DBLβ with ICAM1-binding motifs.

      XLSX, 123K

    • Supplemental file 3 -

      Data Set S1. All Papua New Guinea DBLβ sequences.

      CSV, 697K

    • Supplemental file 4 -

      Data Set S2. All supplementary DBLβ sequences.

      CSV, 59K

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Antibodies to Intercellular Adhesion Molecule 1-Binding Plasmodium falciparum Erythrocyte Membrane Protein 1-DBLβ Are Biomarkers of Protective Immunity to Malaria in a Cohort of Young Children from Papua New Guinea
Sofonias K. Tessema, Digjaya Utama, Olga Chesnokov, Anthony N. Hodder, Clara S. Lin, G. L. Abby Harrison, Jakob S. Jespersen, Bent Petersen, Livingstone Tavul, Peter Siba, Dominic Kwiatkowski, Thomas Lavstsen, Diana S. Hansen, Andrew V. Oleinikov, Ivo Mueller, Alyssa E. Barry
Infection and Immunity Jul 2018, 86 (8) e00485-17; DOI: 10.1128/IAI.00485-17

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Antibodies to Intercellular Adhesion Molecule 1-Binding Plasmodium falciparum Erythrocyte Membrane Protein 1-DBLβ Are Biomarkers of Protective Immunity to Malaria in a Cohort of Young Children from Papua New Guinea
Sofonias K. Tessema, Digjaya Utama, Olga Chesnokov, Anthony N. Hodder, Clara S. Lin, G. L. Abby Harrison, Jakob S. Jespersen, Bent Petersen, Livingstone Tavul, Peter Siba, Dominic Kwiatkowski, Thomas Lavstsen, Diana S. Hansen, Andrew V. Oleinikov, Ivo Mueller, Alyssa E. Barry
Infection and Immunity Jul 2018, 86 (8) e00485-17; DOI: 10.1128/IAI.00485-17
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

DBLβ
EPCR
ICAM1
Papua New Guinea
PfEMP1
antibodies
diversity
malaria
var genes

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