Previous Article | Next Article 
Infection and Immunity, December 2001, p. 7487-7492, Vol. 69, No. 12
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.12.7487-7492.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Gravidity-Dependent Production of Antibodies That
Inhibit Binding of Plasmodium falciparum-Infected
Erythrocytes to Placental Chondroitin Sulfate Proteoglycan during
Pregnancy
Iona
O'Neil-Dunne,1,2
Rajeshwara N.
Achur,1
Sean T.
Agbor-Enoh,1,2,3
Manojkumar
Valiyaveettil,1
Ramachandra S.
Naik,1
Christian
F.
Ockenhouse,4
Ainong
Zhou,2
Rosette
Megnekou,3
Rose
Leke,3
Diane W.
Taylor,2 and
D. Channe
Gowda1,*
Department of Biochemistry and Molecular
Biology, Georgetown University Medical Center, Washington, D.C.
200071 and Department of Biology,
Georgetown University, Washington, D.C. 200572;
Faculty of Medicine and Biomedical Sciences and
Biotechnology Center, University of Yaounde I. Yaounde,
Cameroon3; and Division of
Immunology, Walter Reed Army Institute of Research, Silver Spring,
Maryland 209104
Received 14 June 2001/Returned for modification 27 August
2001/Accepted 24 September 2001
During pregnancy, Plasmodium falciparum-infected
erythrocytes sequester in the placenta by adhering to chondroitin
4-sulfate, creating a risk factor for both the mother and the fetus.
The primigravidae are at higher risk for placental malaria than the multigravidae. This difference in susceptibility has been attributed to
the lack of antibodies that block the adhesion of infected erythrocytes
to placental chondroitin 4-sulfate in primigravid women. However,
recent results show that many primigravidae at term have antibody
levels similar to those of multigravidae, and thus the significance of
antiadhesion antibodies in providing protection against malaria during
pregnancy remains unclear. In this study, we analyzed plasma samples
from women of various gravidities at different gestational stages for
antiadhesion antibodies. The majority of women, regardless of
gravidity, had similar levels of antibodies at term. Most primigravidae
had low levels of or no antiadhesion antibodies prior to ~20 weeks of
pregnancy and then produced antibodies. Multigravidae also lacked
antibodies until ~12 weeks of pregnancy, but thereafter they
efficiently produced antibodies. In pregnant women who had placental
infection at term, higher levels of antiadhesion antibodies correlated
with lower levels of placental parasitemia. The difference in kinetics of antibody production between primigravidae and multigravidae correlated with the prevalence of malaria in these groups, suggesting that antibodies are produced during pregnancy in response to placental infection. The early onset of efficient antibody response in
multigravidae and the delayed production to antibodies in primigravidae
appear to account for the gravidity-dependent differential
susceptibilities of pregnant women to placental malaria.
*
Corresponding author. Mailing address: Department of
Biochemistry and Molecular Biology, Georgetown University Medical
Center, 3900 Reservoir Road, NW, Washington, DC 20007. Phone: (202)
687-3840. Fax: (202) 687-7186. E-mail:
gowda{at}bc.georgetown.edu.
Infection and Immunity, December 2001, p. 7487-7492, Vol. 69, No. 12
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.12.7487-7492.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Higgins, M. K.
(2008). The Structure of a Chondroitin Sulfate-binding Domain Important in Placental Malaria. J. Biol. Chem.
283: 21842-21846
[Abstract]
[Full Text]
-
Madhunapantula, S. V., Achur, R. N., Gowda, D. C.
(2007). Developmental Stage- and Cell Cycle Number-Dependent Changes in Characteristics of Plasmodium falciparum-Infected Erythrocyte Adherence to Placental Chondroitin-4-Sulfate Proteoglycan. Infect. Immun.
75: 4409-4415
[Abstract]
[Full Text]
-
Muehlenbachs, A., Fried, M., Lachowitzer, J., Mutabingwa, T. K., Duffy, P. E.
(2007). Genome-Wide Expression Analysis of Placental Malaria Reveals Features of Lymphoid Neogenesis during Chronic Infection. J. Immunol.
179: 557-565
[Abstract]
[Full Text]
-
BENET, A., KHONG, T. Y., URA, A., SAMEN, R., LORRY, K., MELLOMBO, M., TAVUL, L., BAEA, K., ROGERSON, S. J., CORTES, A.
(2006). PLACENTAL MALARIA IN WOMEN WITH SOUTH-EAST ASIAN OVALOCYTOSIS.. Am J Trop Med Hyg
75: 597-604
[Abstract]
[Full Text]
-
Megnekou, R., Staalsoe, T., Taylor, D. W, Leke, R., Hviid, L.
(2005). Effects of Pregnancy and Intensity of Plasmodium falciparum Transmission on Immunoglobulin G Subclass Responses to Variant Surface Antigens. Infect. Immun.
73: 4112-4118
[Abstract]
[Full Text]
-
Chaisavaneeyakorn, S., Lucchi, N., Abramowsky, C., Othoro, C., Chaiyaroj, S. C., Shi, Y. P., Nahlen, B. L., Peterson, D. S., Moore, J. M., Udhayakumar, V.
(2005). Immunohistological Characterization of Macrophage Migration Inhibitory Factor Expression in Plasmodium falciparum-Infected Placentas. Infect. Immun.
73: 3287-3293
[Abstract]
[Full Text]
-
Cox, S. E., Staalsoe, T., Arthur, P., Bulmer, J. N., Hviid, L., Yeboah-Antwi, K., Kirkwood, B. R., Riley, E. M.
(2005). Rapid Acquisition of Isolate-Specific Antibodies to Chondroitin Sulfate A-Adherent Plasmodium falciparum Isolates in Ghanaian Primigravidae. Infect. Immun.
73: 2841-2847
[Abstract]
[Full Text]
-
Muthusamy, A., Achur, R. N., Valiyaveettil, M., Madhunapantula, S. V., Kakizaki, I., Bhavanandan, V. P., Gowda, C. D.
(2004). Structural characterization of the bovine tracheal chondroitin sulfate chains and binding of Plasmodium falciparum-infected erythrocytes. Glycobiology
14: 635-645
[Abstract]
[Full Text]
-
Muthusamy, A., Achur, R. N., Bhavanandan, V. P., Fouda, G. G., Taylor, D. W., Gowda, D. C.
(2004). Plasmodium falciparum-Infected Erythrocytes Adhere Both in the Intervillous Space and on the Villous Surface of Human Placenta by Binding to the Low-Sulfated Chondroitin Sulfate Proteoglycan Receptor. Am. J. Pathol.
164: 2013-2025
[Abstract]
[Full Text]
-
Taylor, D. W., Zhou, A., Marsillio, L. E., Thuita, L. W., Leke, E. B., Branch, O., Gowda, D. C., Long, C., Leke, R. F. G.
(2004). Antibodies That Inhibit Binding of Plasmodium falciparum-Infected Erythrocytes to Chondroitin Sulfate A and to the C Terminus of Merozoite Surface Protein 1 Correlate with Reduced Placental Malaria in Cameroonian Women. Infect. Immun.
72: 1603-1607
[Abstract]
[Full Text]
-
Agbor-Enoh, S. T., Achur, R. N., Valiyaveettil, M., Leke, R., Taylor, D. W., Gowda, D. C.
(2003). Chondroitin Sulfate Proteoglycan Expression and Binding of Plasmodium falciparum-Infected Erythrocytes in the Human Placenta during Pregnancy. Infect. Immun.
71: 2455-2461
[Abstract]
[Full Text]
-
Achur, R. N., Valiyaveettil, M., Gowda, D. C.
(2003). The Low Sulfated Chondroitin Sulfate Proteoglycans of Human Placenta Have Sulfate Group-clustered Domains That Can Efficiently Bind Plasmodium falciparum-infected Erythrocytes. J. Biol. Chem.
278: 11705-11713
[Abstract]
[Full Text]
-
Ofori, M. F., Staalsoe, T., Bam, V., Lundquist, M., David, K. P., Browne, E. N. L., Akanmori, B. D., Hviid, L.
(2003). Expression of Variant Surface Antigens by Plasmodium falciparum Parasites in the Peripheral Blood of Clinically Immune Pregnant Women Indicates Ongoing Placental Infection. Infect. Immun.
71: 1584-1586
[Abstract]
[Full Text]
-
Cot, M., Le Hesran, J. Y., Staalsoe, T., Fievet, N., Hviid, L., Deloron, P.
(2003). Maternally Transmitted Antibodies to Pregnancy-Associated Variant Antigens on the Surface of ErythrocytesInfected with Plasmodium falciparum: Relation to Child Susceptibility to Malaria. Am J Epidemiol
157: 203-209
[Abstract]
[Full Text]