Plasmodium falciparum Isolates from Infected Pregnant Women and Children Are Associated with Distinct Adhesive and Antigenic Properties
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Plasmodium falciparum malaria during pregnancy is an important cause of maternal and infant morbidity and mortality. Accumulation of large numbers of P. falciparum-infected erythrocytes in the maternal blood spaces of the placenta may be mediated by adhesion of infected erythrocytes to molecules presented on the syncytiotrophoblast surface. In this study, isolates from placentas and peripheral blood of infected pregnant women and from children were tested for binding to purified receptors and for agglutination with adult sera. Results suggest that adhesion to chondroitin sulfate A may be involved in placental parasite sequestration in most cases, but other factors are also likely to be important. Agglutination assay results suggest that parasites infecting pregnant women are antigenically distinct from those common in childhood disease. The prevalence of agglutinating antibodies to pregnancy isolates was generally low, but it was highest in multigravidae who are likely to have had the greatest exposure.
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P. falciparum placental parasites express unique variant surface antigens (VSA_PAM) that allow the parasite to sequester in the placenta by binding to chondroitin sulfate A (CSA) receptors on syncytiotrophoblast.
“the parasite to sequester in the placenta by binding to chondroitin sulfate A (CSA) receptors on syncytiotrophoblast (Beeson et al. , 1999; Fried & Duffy, 1996; Ricke et al. , 2000; Tuikue Ndam et al. , 2004).”
From Towards a vaccine against pregnancy-associated malaria (2008) · cites this paper as Beeson et al., 1999
The Discussion (page unavailable) reports that most placental isolates bound CSA in vitro and generally supports a role for CSA on syncytiotrophoblasts in placental sequestration. It also reports antigenic differences between pregnancy and childhood isolates. But the paper does not establish CSA binding as the definitive mechanism for all placental parasites: some isolates did not bind the tested receptors, and the authors say other factors may contribute. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCSA has been consistently identified as the dominant placental adhesion receptor.
“C SA has been consistently identified as the dominant placental adhesion receptor (Beeson et al. , 1999; Fried & Duffy, 1996).”
From Towards a vaccine against pregnancy-associated malaria (2008) · cites this paper as Beeson et al., 1999
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Cites
Su, X.-Z., Heatwole, V. M., Wertheimer, S. P., Guinet, F., Herrfeldt, J. A., Peterson, D. S., Ravetch, J. A., & Wellems, T. E. (1995) · Cell · doi:10.1016/0092-8674(95)90055-1 · Cited by 1,219 · see citing works
Adherence of <i>Plasmodium falciparum</i> to Chondroitin Sulfate A in the Human Placenta
Fried, M., & Duffy, P. E. (1996) · Science · doi:10.1126/science.272.5267.1502 · Cited by 1,108 · see citing works
Epidemiology, Malaria and Pregnancy
McGregor, I. A. (1984) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1984.33.517 · Cited by 452 · cited 3× · see citing works
“Primigravid women typically experience higher rates of infection than multigravidae, and the consequences of infection are greater [1, 2].”
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Research works printed but not linked: 42
- [1]Brabin BJ An analysis of malaria in pregnancy in Africa Bull World Health Organ 1983 61 1005 16 6370484 PMC2536236
- [3]Fleming AF Tropical obstetrics and gynaecology. 1. Anaemia in pregnancy in tropical Africa Trans R Soc Trop Med Hyg 1989 83 441 8 2694476
- [4]Granja AC Machungo F Gomes A Bergstrom S Brabin B Malaria-related maternal mortality in urban Mozambique Ann Trop Med Parasitol 1998 92 257 63 9713540
- [5]McDermott JM Wirima JJ Steketee RW Breman JG Heyman DL The effect of placental malaria infection on perinatal mortality in rural Malawi Am J Trop Med Hyg 1996 55 61 5 8702039
- [6]Aikawa M Iseki M Barnwell JW Taylor D Oo MM Howard RJ The pathology of human cerebral malaria Am J Trop Med Hyg 1990 43 30 7 2202227
- [7]Berendt AR Turner GDH Newbold CI Cerebral malaria: the sequestration hypothesis Parasitol Today 1994 10 412 4 15275553
- [8]Walter PR Garin Y Blot P Placental pathologic changes in malaria Am J Pathol 1982 109 330 42 6758604 PMC1916118
- [9]Watkinson M Rushton DI Plasmodial pigmentation of placenta and outcome of pregnancy in West African mothers BMJ 1983 287 251 4 6409270 PMC1548862
- [10]Rogerson SJ Brown GV Chondroitin sulfate A as an adherence receptor for Plasmodium falciparum-infected erythrocytes Parasitol Today 1997 13 70 5 15275126
- [11]Berendt AR Simmons DL Tansey J Newbold CI Marsh K Intercellular adhesion molecule-1 is an endothelial cell adhesion molecule for Plasmodium falciparum Nature 1989 341 57 9 2475784
- [12]Barnwell JW Asch AS Nachman RL Yamaya M Aikawa M A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes J Clin Invest 1989 84 765 72 2474574 PMC329717
- [13]Ockenhouse CF Tandon NN Magowan C Jamieson GA Chulay JD Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor Science 1989 243 1469 71 2467377
- [14]Ockenhouse CF Ho M Tandon NN Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1 J Infect Dis 1991 164 163 9 1711552
- [15]Reeder JC Rogerson SJ Al-Yaman F Diversity of agglutinating phenotype, cytoadherence, and rosette-forming characteristics of Plasmodium falciparum isolates from Papua New Guinean children Am J Trop Med Hyg 1994 51 45 55 8059915
- [16]Beeson JG Chai W Rogerson SJ Lawson AM Brown GV Inhibition of binding of malaria-infected erythrocytes by a tetradecasaccharide fraction from chondroitin sulfate A Infect Immun 1998 66 3397 402 9632611 PMC108358
- [17]Parmley RT Takagi M Denys FR Ultrastructural localization of glycosaminoglycans in human term placenta Anat Rec 1984 210 477 84 6084429
- [19]Maubert B Guilbert LJ Deloron P Cytoadherence of Plasmodium falciparum to intercellular adhesion molecule 1 and chondroitin-4-sulfate expressed by the syncytiotrophoblast in the human placenta Infect Immun 1997 65 1251 7 9119459 PMC175125
- [20]Robert C Pouvelle B Meyer P Chondroitin-4-sulphate (proteoglycan), a receptor for Plasmodium falciparum-infected erythrocyte adherence on brain microvascular endothelial cells Res Immunol 1995 146 383 93 8719662
- [21]Rogerson SJ Novakovic S Cooke BM Brown GV Plasmodium falciparum-infected erythrocytes adhere to the proteoglycan thrombomodulin in static and flow-based systems Exp Parasitol 1997 86 8 18 9149236
- [22]Xiao J Garcia-Lloret M Winkler-Lowen B Miller R Simpson K Guilbert LJ ICAM-1-mediated adhesion of peripheral blood monocytes to the maternal surface of placental syncytiotrophoblasts Am J Pathol 1997 150 1845 60 9137107 PMC1858201
- [23]Marsh K Howard RJ Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants Science 1986 231 150 3 2417315
- [24]Leech JH Barnwell JW Miller LH Howard RJ Identification of a strainspecific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes J Exp Med 1984 159 1567 75 6374009 PMC2187322
- [25]Biggs BA Goozé L Wycherley K Antigenic variation in Plasmodium falciparum Proc Natl Acad Sci USA 1991 88 9171 4 1924380 PMC52674
- [26]Baruch DI Pasloske BL Singh HB Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes Cell 1995 82 77 87 7541722
- [27]Smith JD Chitnis CE Craig AG Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes Cell 1995 82 101 10 7606775 PMC3730239
- [29]Baruch DI Gormley JA Ma C Howard RJ Pasloske BL Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1 Proc Natl Acad Sci USA 1996 93 3497 502 8622965 PMC39638
- [30]Reeder JC Cowman AF Davern KM The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1 Proc Natl Acad Sci USA 1999 96 5198 202 10220443 PMC21841
- [31]Bull PC Lowe BS Kortok M Molyneux CS Newbold CI Marsh K Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria Nature Med 1998 4 358 60 9500614 PMC3836255
- [33]Cranmer SL Magowan C Liang J Coppel RL Cooke BM An alternative to serum for cultivation of Plasmodium falciparum in vitro Trans R Soc Trop Med Hyg 1997 91 363 5 9231219
- [34]Cooke BM Rogerson SJ Brown GV Coppel RL Adhesion of malariainfected red blood cells to chondroitin sulfate A under flow conditions Blood 1996 88 4040 4 8916971
- [35]Kutner S Breuer WV Ginsburg H Aley SB Cabantchik ZI Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of Plasmodium falciparum: association with parasite development J Cell Physiol 1985 125 521 7 2999164
- [36]Ramsey EM Donner MW Placental vasculature and circulation 1980 Georg Thieme Stuttgart, Germany
- [37]Miller LH Chien S Usami S Decreased deformability of Plasmodium coatneyi-infected red cells and its possible relation to cerebral malaria Am J Trop Med Hyg 1972 21 133 6 4621952
- [38]Riley EM Schneider G Sambou I Greenwood BM Suppression of cell-mediated immune responses to malaria antigens in pregnant Gambian women Am J Trop Med Hyg 1989 40 141 4 2493200
- [40]Nambei WS Goumbala M Spiegel A Dieye A Perraut R Garraud O Imbalanced distribution of IgM and IgG antibodies against Plasmodium falciparum antigens and merozoite surface protein-1 (MSP1) in pregnancy Immunol Lett 1998 61 197 9 9657275
- [41]Deloron P Steketee RW Campbell GH Peyron F Kaseje DCO Serological reactivity to the ring-infected erythrocyte surface antigen and circumsporozoite protein in gravid and nulligravid women infected with Plasmodium falciparum Trans R Soc Trop Med Hyg 1989 83 58 62 2690416
- [42]Vleugels MPH Brabin B Eling WMC de Graaf R Cortisol and Plasmodium falciparum infection in pregnant women in Kenya Trans R Soc Trop Med Hyg 1989 83 173 7 2692225
- [43]Yamada M Steketee R Abramowsky C Plasmodium falciparum associated placental pathology: a light and electron microscopic and immunohistologic study Am J Trop Med Hyg 1989 41 161 8 2672835
- [44]Dittman WA Majerus PW Structure and function of thrombomodulin: a natural anticoagulant Blood 1990 75 329 36 2153035
- Dustin ML Rothlein R Bhan AK Dinarello CA Springer TA Induction by IL-1 and interferon-γ: tissue distribution, biochemistry and function of a natural adherence molecule (ICAM-1) J Immunol 1986 137 245 54 3086451
- [46]Bull PC Lowe BS Kortok M Marsh K Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants Infect Immun 1999 67 733 7 9916084 PMC96380
- [47]Fried M Nosten F Brockman A Brabin BJ Duffy PE Maternal antibodies block malaria Nature 1998 395 851 2 9804416
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- Authors
- Beeson, J. G., Brown, G. V., Molyneux, M. E., Mhango, C., Dzinjalamala, F., & Rogerson, S. J.
- Affiliations
- The Royal Melbourne Hospital (AU)
- Walter and Eliza Hall Institute of Medical Research (AU)
- University of Liverpool (GB)
- University of Malawi (MW)
- Corresponding author
- Beeson, James G.
- Venue
- The Journal of Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-08
- Volume
- 180
- Issue
- 2
- Pages
- 464-472
- ISSN
- 0022-1899 (ISSN-L)
- 1537-6613
- PMC
- PMC2613477
- OpenAlex
- W2160351496
- Cited by
- 266
- References
- 3
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 5 · 2017: 6 · 2016: 9 · 2015: 4 · 2014: 13 · 2013: 8 · 2012: 9
- FWCI
- 17.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Infectious Diseases (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Wellcome Trust (063215)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Keywords
- Plasmodium falciparum, malaria in pregnancy, placental malaria, parasite adhesion, chondroitin sulfate A, syncytiotrophoblast, parasite sequestration, agglutination, maternal antibodies, multigravida
- MeSH terms
- Adult, Animals, Cell Adhesion, Child, Chondroitin Sulfates, Erythrocytes, Female, Humans, Leukocytes, Mononuclear, Male, Placenta, Plasmodium falciparum, Pregnancy, Receptors, Cell Surface, Trophoblasts, Pregnancy Complications, Parasitic, Malaria, Falciparum, Parasitemia, Intercellular Adhesion Molecule-1, CD36 Antigens
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