Genome-Wide Expression Analysis of Placental Malaria Reveals Features of Lymphoid Neogenesis during Chronic Infection

Muehlenbachs, Atis; Fried, Michal; Lachowitzer, Jeff; Mutabingwa, Theonest K; Duffy, Patrick E

doi:10.4049/jimmunol.179.1.557

Cited by 81Malaria Research and ControlReproductive System and PregnancyPregnancy and preeclampsia studies

Genome-Wide Expression Analysis of Placental Malaria Reveals Features of Lymphoid Neogenesis during Chronic Infection

Muehlenbachs, Atis, Fried, Michal, Lachowitzer, Jeff, Mutabingwa, Theonest K, Duffy, Patrick E·2007·The Journal of Immunology

DOI 10.4049/jimmunol.179.1.557

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Abstract

Chronic inflammation during placental malaria (PM) is most frequent in first time mothers and is associated with poor maternal and fetal outcomes. In the first genome-wide analysis of the local human response to sequestered malaria parasites, we identified genes associated with chronic PM and then localized the corresponding proteins and immune cell subsets in placental cryosections. B cell-related genes were among the most highly up-regulated transcripts in inflamed tissue. The B cell chemoattractant CXCL13 was up-regulated >1,000-fold, and B cell-activating factor was also detected. Both proteins were expressed by intervillous macrophages. Ig L and H chain transcription increased significantly, and heavy depositions of IgG3 and IgM were observed in intervillous spaces. The B cell phenotype was heterogenous, including naive (CD27-negative), mature (CD138-positive), and cycling (Ki-67-positive) cells. B cells expressed T-bet but not Bcl-6, suggesting T cell-independent activation without germinal center formation. Genes for the Fc binding proteins FcγRIa, FcγRIIIa, and C1q were highly up-regulated, and the proteins localized to intervillous macrophages. Birth weight was inversely correlated with transcript levels of CXCL13, IgG H chain, and IgM H chain. The iron regulatory peptide hepcidin was also expressed but was not associated with maternal anemia. The results suggest that B cells and macrophages contribute to chronic PM in a process resembling lymphoid neogenesis. We propose a model where the production of Ig during chronic malaria may enhance inflammation by attracting and activating macrophages that, in turn, recruit B cells to further produce Ig in the intervillous spaces.

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From Current update on malaria in pregnancy: a systematic review (2025) · cites this paper as [124]

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Authors: Muehlenbachs, A., Fried, M., Lachowitzer, J., Mutabingwa, T. K., & Duffy, P. E.
Affiliations: Center for Infectious Disease Research (US)
ORCID: Muehlenbachs, Atis
Fried, Michal
Duffy, Patrick E
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2007-07-01
Volume: 179
Issue: 1
Pages: 557-565
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.179.1.557
OpenAlex: W1630763938
Cited by: 81
References: 58
Citations by year: 2026: 2 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 3 · 2015: 5 · 2014: 6 · 2013: 5 · 2012: 5
FWCI: 5.49
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
LSHTM Research Online (London School of Hygiene and Tropical Medicine) (submittedVersion)
Funders: National Heart, Lung, and Blood Institute (T32-HL 07312, HL072370, R01HL072370, T32HL007312)
National Institute of Allergy and Infectious Diseases (R01AI052059, R01AI52059)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: placental malaria, chronic malaria infection, lymphoid neogenesis, B cells, CXCL13, B-cell activating factor, immunoglobulin deposition, Fc gamma receptor, hepcidin, anemia in pregnancy, birth weight, T-bet, germinal center formation, placental inflammation
MeSH terms: Adolescent, Adult, Antibodies, Protozoan, B-Lymphocytes, Cell Movement, Chronic Disease, Female, Humans, Macrophage Activation, Macrophages, Middle Aged, Placenta Diseases, Pregnancy, Up-Regulation, Malaria, Falciparum, Chemokines, CXC, Gene Expression Profiling, Lymphopoiesis, Chemokine CXCL13

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Genome-Wide Expression Analysis of Placental Malaria Reveals Features of Lymphoid Neogenesis during Chronic Infection

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