Chondroitin Sulfate A-Adhering Plasmodium falciparum-Infected Erythrocytes Express Functionally Important Antibody Epitopes Shared by Multiple Variants

Barfod, Lea; Dobrilovic, Tina; Magistrado, Pamela; Khunrae, Pongsak; Viwami, Firmine; Bruun, Jonas; Dahlbäck, Madeleine; Bernasconi, Nadia L; Fried, Michal; John, Davis; Duffy, Patrick E; Salanti, Ali; Lanzavecchia, Antonio; Lim, Chwee Teck; Ndam, Nicaise Tuikue; Higgins, Matthew K; Hviid, Lars

doi:10.4049/jimmunol.1002390

Cited by 62Malaria Research and ControlBlood groups and transfusionVector-borne infectious diseases

Chondroitin Sulfate A-Adhering Plasmodium falciparum-Infected Erythrocytes Express Functionally Important Antibody Epitopes Shared by Multiple Variants

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Barfod, Lea, Dobrilovic, Tina, Magistrado, Pamela, Khunrae, Pongsak, Viwami, Firmine, Bruun, Jonas, Dahlbäck, Madeleine, Bernasconi, Nadia L +9 more·2010·The Journal of Immunology

DOI 10.4049/jimmunol.1002390PMC PMC4785892

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Abstract

Acquired protection from Plasmodium falciparum placental malaria, a major cause of maternal, fetal, and infant morbidity, is mediated by IgG specific for the P. falciparum erythrocyte membrane protein 1 variant VAR2CSA. This protein enables adhesion of P. falciparum-infected erythrocytes to chondroitin sulfate A in the intervillous space. Although interclonal variation of the var2csa gene is lower than that among var genes in general, VAR2CSA-specific Abs appear to target mainly polymorphic epitopes. This has raised doubts about the feasibility of VAR2CSA-based vaccines. We used eight human monoclonal IgG Abs from affinity-matured memory B cells of P. falciparum-exposed women to study interclonal variation and functional importance of Ab epitopes among placental and peripheral parasites from East and West Africa. Most placental P. falciparum isolates were labeled by several mAbs, whereas peripheral isolates from children were essentially nonreactive. The mAb reactivity of peripheral isolates from pregnant women indicated that some were placental, whereas others had alternative sequestration foci. Most of the mAbs were comparable in their reactivity with bound infected erythrocytes (IEs) and recombinant VAR2CSA and interfered with IE and/or VAR2CSA binding to chondroitin sulfate A. Pair-wise mAb combinations were more inhibitory than single mAbs, and all of the mAbs together was the most efficient combination. Each mAb could opsonize IEs for phagocytosis, and a combination of the eight mAbs caused phagocytosis similar to that of plasma IgG-opsonized IEs. We conclude that functionally important Ab epitopes are shared by the majority of polymorphic VAR2CSA variants, which supports the feasibility of VAR2CSA-based vaccines against placental malaria.

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The identification of a single human monoclonal antibody (PAM1.4) from immune multigravid women that recapitulates anti-adhesion activity in plasma from multigravidae, together with the observation that plasma from multigravidae have strain-transcending functional activity, strongly suggest that a limited number of epitopes can be targeted by an effective PM vaccine.
“The identification of a single human monoclonal antibody (PAM1.4) from immune multigravid women that recapitulates anti-adhesion activity in plasma from multigravidae [64], together with the observation that plasma from multigravidae have strain-transcending functional activity [11], strongly suggest that a limited number of epitopes can be targeted by an effective PM vaccine.”
From Designing a VAR2CSA-based vaccine to prevent placental malaria (2015) · cites this paper as [64]
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Monoclonal antibody PAM1.4 recognized the surface of placental parasites and inhibited their adhesion to CSA, while it only moderately inhibited the adhesion to CSA of the laboratory isolate FCR3-CSA.
“Monoclonal antibody PAM1.4 recognized the surface of placental parasites and inhibited their adhesion to CSA, while it only moderately inhibited the adhesion to CSA of the laboratory isolate FCR3-CSA [64].”
From Designing a VAR2CSA-based vaccine to prevent placental malaria (2015) · cites this paper as [64]
Infected erythrocyte adhesion to CSA is mediated by VAR2CSA.
“Infected erythrocyte (IE) adhesion to CSA is mediated by VAR2CSA, a member of the P. falciparum erythrocyte membrane protein family (PfEMP1) that is preferentially expressed by placental parasites and parasites selected to bind CSA [3–5].”
From Antibody levels to recombinant VAR2CSA domains vary with Plasmodium falciparum parasitaemia, gestational age, and gravidity, but do not predict pregnancy outcomes (2018) · cites this paper as [5]

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Authors: Barfod, L., Dobrilovic, T., Magistrado, P., Khunrae, P., Viwami, F., Bruun, J., Dahlbäck, M., Bernasconi, N. L., Fried, M., John, D., Duffy, P. E., Salanti, A., Lanzavecchia, A., Lim, C. T., Ndam, N. T., Higgins, M. K., & Hviid, L.
Affiliations: University of Copenhagen (DK)
Centre for Medical Parasitology, Department of International Health, Immunology, and Microbiology, University of Copenhagen , Copenhagen ,
University of Cambridge (GB)
Institut de Recherche pour le Développement (BJ)
Institute for Research in Biomedicine (CH)
Center for Infectious Disease Research (US)
Kilimanjaro Christian Medical Centre , Moshi ,
National University of Singapore (SG)
Corresponding author: Barfod, Lea
Dobrilovic, Tina
Bruun, Jonas
Salanti, Ali
Hviid, Lars
ORCID: Barfod, Lea
Khunrae, Pongsak
Viwami, Firmine
Fried, Michal
Duffy, Patrick E
Salanti, Ali
Lanzavecchia, Antonio
Lim, Chwee Teck
Ndam, Nicaise Tuikue
Higgins, Matthew K
Hviid, Lars
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2010-12
Volume: 185
Issue: 12
Pages: 7553-7561
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.1002390
PMC: PMC4785892
OpenAlex: W1902770434
Cited by: 62
References: 58
Citations by year: 2026: 3 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 1 · 2019: 3 · 2018: 5 · 2017: 4 · 2016: 3 · 2015: 5 · 2014: 7 · 2013: 2 · 2012: 5
FWCI: 5.07
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
National University of Singapore (submittedVersion)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Funders: Bill and Melinda Gates Foundation (47029)
Sundhed og Sygdom, Det Frie Forskningsråd
Wellcome Trust
Royal Society
European Commission (242095, 200889)
Rigshospitalet
National Institutes of Health (Z99 AI999999)
Medical Research Council
National Institute of Allergy and Infectious Diseases (ZIAAI001134)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Health Sciences › Medicine › Hematology › Blood groups and transfusion
Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
Keywords: Plasmodium falciparum, placental malaria, VAR2CSA, erythrocyte membrane protein 1, chondroitin sulfate A, antibody epitopes, monoclonal antibodies, vaccine feasibility, opsonization, phagocytosis, sequestration, East and West Africa
MeSH terms: Adult, Antibodies, Monoclonal, Antibodies, Protozoan, Epitopes, B-Lymphocytes, Child, Child, Preschool, Chondroitin Sulfates, Erythrocytes, Female, Humans, Male, Placenta, Plasmodium falciparum, Pregnancy, Pregnancy Complications, Infectious, Protozoan Proteins, Malaria, Falciparum, Malaria Vaccines

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Chondroitin Sulfate A-Adhering Plasmodium falciparum-Infected Erythrocytes Express Functionally Important Antibody Epitopes Shared by Multiple Variants

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