Molecular Aspects of <i>Plasmodium falciparum</i> Infection  during Pregnancy

Ndam, Nicaise Tuikue; Deloron, Philippe

doi:https://doi.org/10.1155/2007/43785

BioMed Research International

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Immunology and Molecular Biology of Protozoan Infections

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Review Article | Open Access

Volume 2007 | Article ID 043785 | https://doi.org/10.1155/2007/43785

Molecular Aspects of Plasmodium falciparum Infection during Pregnancy

Nicaise Tuikue Ndam¹and Philippe Deloron¹

Academic Editor: Ali Ouaissi

Received29 Dec 2006

Accepted21 Mar 2007

Published07 Jun 2007

Abstract

Cytoadherence of Plasmodium-falciparum-parasitized red blood cells (PRBCs) to host receptors is the key phenomenon in the pathological process of the malaria disease. Some of these interactions can originate poor outcomes responsible for 1 to 3 million annual deaths mostly occurring among children in sub-Saharan Africa. Pregnancy-associated malaria (PAM) represents an important exception of the disease occurring at adulthood in malaria endemic settings. Consequences of this are shared between the mother (maternal anemia) and the baby (low birth weight and infant mortality). Demonstrating that parasites causing PAM express specific variant surface antigens (VSAPAM), including the P. falciparum erythrocyte membrane protein 1 (PfEMP1) variant VAR2CSA, that are targets for protective immunity has strengthened the possibility for the development of PAM-specific vaccine. In this paper, we review the molecular basis of malaria pathogenesis attributable to the erythrocyte stages of the parasites, and findings supporting potential anti-PAM vaccine components evidenced in PAM.

References

K. Marsh and R. W. Snow, “Malaria transmission and morbidity,” Parassitologia, vol. 41, no. 1–3, pp. 241–246, 1999.
View at: Google Scholar
K. Chotivanich, R. Udomsangpetch, J. A. Simpson et al., “Parasite multiplication potential and the severity of falciparum malaria,” The Journal of Infectious Diseases, vol. 181, no. 3, pp. 1206–1209, 2000.
View at: Publisher Site | Google Scholar
S. N. Wickramasinghe and S. H. Abdalla, “Blood and bone marrow changes in malaria,” Bailliere's Best Practice and Research in Clinical Haematology, vol. 13, no. 2, pp. 277–299, 2000.
View at: Publisher Site | Google Scholar
K. Chotivanich, R. Udomsangpetch, A. Dondorp et al., “The mechanisms of parasite clearance after antimalarial treatment of Plasmodium falciparum malaria,” The Journal of Infectious Diseases, vol. 182, no. 2, pp. 629–633, 2000.
View at: Publisher Site | Google Scholar
H. Ekvall, “Malaria and anemia,” Current Opinion in Hematology, vol. 10, no. 2, pp. 108–114, 2003.
View at: Publisher Site | Google Scholar
L. H. Miller, M. F. Good, and G. Milon, “Malaria pathogenesis,” Science, vol. 264, no. 5167, pp. 1878–1883, 1994.
View at: Publisher Site | Google Scholar
Q. Chen, M. Schlichtherle, and M. Wahlgren, “Molecular aspects of severe malaria,” Clinical Microbiology Reviews, vol. 13, no. 3, pp. 439–450, 2000.
View at: Publisher Site | Google Scholar
S. Kyes, P. Horrocks, and C. Newbold, “Antigenic variation at the infected red cell surface in malaria,” Annual Review of Microbiology, vol. 55, pp. 673–707, 2001.
View at: Publisher Site | Google Scholar
C. R. Engwerda, L. Beattie, and F. H. Amante, “The importance of the spleen in malaria,” Trends in Parasitology, vol. 21, no. 2, pp. 75–80, 2005.
View at: Publisher Site | Google Scholar
A. Saul, “The role of variant surface antigens on malaria-infected red blood cells,” Parasitology Today, vol. 15, no. 11, pp. 455–457, 1999.
View at: Publisher Site | Google Scholar
S. Paget-McNicol, M. Gatton, I. Hastings, and A. Saul, “The Plasmodium falciparum var gene switching rate, switching mechanism and patterns of parasite recrudescence described by mathematical modelling,” Parasitology, vol. 124, no. 3, pp. 225–235, 2002.
View at: Publisher Site | Google Scholar
A. Craig and A. Scherf, “Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion,” Molecular and Biochemical Parasitology, vol. 115, no. 2, pp. 129–143, 2001.
View at: Publisher Site | Google Scholar
M. Kaviratne, S. M. Khan, W. Jarra, and P. R. Preiser, “Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells,” Eukaryotic Cell, vol. 1, no. 6, pp. 926–935, 2002.
View at: Publisher Site | Google Scholar
G. S. N. Hui and W. A. Siddiqui, “Characterization of a Plasmodium falciparum polypeptide associated with membrane vesicles in the infected erythrocytes,” Molecular and Biochemical Parasitology, vol. 29, no. 2-3, pp. 283–293, 1988.
View at: Publisher Site | Google Scholar
G. G. MacPherson, M. J. Warrell, N. J. White, S. Looareesuwan, and D. A. Warrell, “Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration,” American Journal of Pathology, vol. 119, no. 3, pp. 385–401, 1985.
View at: Google Scholar
S. A. Luse and L. H. Miller, “Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels,” American Journal of Tropical Medicine and Hygiene, vol. 20, no. 5, pp. 655–660, 1971.
View at: Google Scholar
B. A. Biggs, J. G. Culvenor, J. S. Ng, D. J. Kemp, and G. V. Brown, “Plasmodium falciparum: cytoadherence of a knobless clone,” Experimental Parasitology, vol. 69, no. 2, pp. 189–197, 1989.
View at: Publisher Site | Google Scholar
R. Udomsangpetch, M. Aikawa, K. Berzins, M. Wahlgren, and P. Perlmann, “Cytoadherence of knobless Plasmodium falciparum-infected erythrocytes and its inhibition by a human monoclonal antibody,” Nature, vol. 338, no. 6218, pp. 763–765, 1989.
View at: Publisher Site | Google Scholar
K.-I. Nakamura, T. Hasler, K. Morehead, R. J. Howard, and M. Aikawa, “Plasmodium falciparum-infected erythrocyte receptor(s) for CD36 and thrombospondin are restricted to knobs on the erythrocyte surface,” Journal of Histochemistry and Cytochemistry, vol. 40, no. 9, pp. 1419–1422, 1992.
View at: Google Scholar
J. H. Leech, J. W. Barnwell, L. H. Miller, and R. J. Howard, “Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes,” Journal of Experimental Medicine, vol. 159, no. 6, pp. 1567–1575, 1984.
View at: Publisher Site | Google Scholar
P. H. David, S. M. Handunnetti, J. H. Leech, P. Gamage, and K. N. Mendis, “Rosetting: a new cytoadherence property of malaria-infected erythrocytes,” American Journal of Tropical Medicine and Hygiene, vol. 38, no. 2, pp. 289–297, 1988.
View at: Google Scholar
D. J. Roberts, A. G. Craig, A. R. Berendt et al., “Rapid switching to multiple antigenic and adhesive phenotypes in malaria,” Nature, vol. 357, no. 6380, pp. 689–692, 1992.
View at: Publisher Site | Google Scholar
WHO, “A strategic framework for malaria prevention and control during pregnancy in the African region,” Report ARF/MAL/04/01, World Health Organization, Brazzaville, Congo, 2004.
View at: Google Scholar
F. Nosten, R. McGready, J. A. Simpson et al., “Effects of Plasmodium vivax malaria in pregnancy,” The Lancet, vol. 354, no. 9178, pp. 546–549, 1999.
View at: Publisher Site | Google Scholar
N. Singh, M. M. Shukla, and V. P. Sharma, “Epidemiology of malaria in pregnancy in central India,” Bulletin of the World Health Organization, vol. 77, no. 7, pp. 567–572, 1999.
View at: Google Scholar
J. G. Beeson, G. V. Brown, M. E. Molyneux, C. Mhango, F. Dzinjalamala, and S. J. Rogerson, “Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties,” The Journal of Infectious Diseases, vol. 180, no. 2, pp. 464–472, 1999.
View at: Publisher Site | Google Scholar
M. Fried and P. E. Duffy, “Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta,” Science, vol. 272, no. 5267, pp. 1502–1504, 1996.
View at: Publisher Site | Google Scholar
M. Fried, M. Fried, G. J. Domingo, T. K. Mutabingwa, and P. E. Duffy, “Plasmodium falciparum: chondroitin sulfate A is the major receptor for adhesion of parasitized erythrocytes in the placenta,” Experimental Parasitology, vol. 113, no. 1, pp. 36–42, 2006.
View at: Google Scholar
J. G. Beeson, E. J. Mann, S. R. Elliott et al., “Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets,” The Journal of Infectious Diseases, vol. 189, no. 3, pp. 540–551, 2004.
View at: Publisher Site | Google Scholar
N. Tuikue Ndam, N. Fievet, G. Bertin, G. Cottrell, A. Gaye, and P. Deloron, “Variable adhesion abilities and overlapping antigenic properties in placental Plasmodium falciparum isolates,” The Journal of Infectious Diseases, vol. 190, no. 11, pp. 2001–2009, 2004.
View at: Publisher Site | Google Scholar
B. Pouvelle, B. Traoré, P. A. Nogueira, B. Pradines, C. LéPolard, and J. Gysin, “Modeling of Plasmodium falciparum-infected erythrocyte cytoadhesion in microvascular conditions: chondroitin-4-sulfate binding, a competitive phenotype,” The Journal of Infectious Diseases, vol. 187, no. 2, pp. 292–302, 2003.
View at: Publisher Site | Google Scholar
N. Tuikue Ndam, A. Salanti, G. Bertin et al., “High level of var2csa transcription by Plasmodium falciparum isolated from the placenta,” The Journal of Infectious Diseases, vol. 192, no. 2, pp. 331–335, 2005.
View at: Publisher Site | Google Scholar
S. J. Pancake, G. D. Holt, S. Mellouk, and S. L. Hoffman, “Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates,” The Journal of Cell Biology, vol. 117, no. 6, pp. 1351–1357, 1992.
View at: Publisher Site | Google Scholar
C. Pinzon-Ortiz, J. Friedman, J. Esko, and P. Sinnis, “The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells,” The Journal of Biological Chemistry, vol. 276, no. 29, pp. 26784–26791, 2001.
View at: Publisher Site | Google Scholar
G. Pradel, S. Garapaty, and U. Frevert, “Proteoglycans mediate malaria sporozoite targeting to the liver,” Molecular Microbiology, vol. 45, no. 3, pp. 637–651, 2002.
View at: Publisher Site | Google Scholar
N. K. Karamanos, A. Syrokou, P. Vanky, M. Nurminen, and A. Hjerpe, “Determination of 24 variously sulfated galactosaminoglycan- and hyaluronan-derived disaccharides by high-performance liquid chromatography,” Analytical Biochemistry, vol. 221, no. 1, pp. 189–199, 1994.
View at: Publisher Site | Google Scholar
R. N. Achur, M. Valiyaveettil, A. Alkhalil, C. F. Ockenhouse, and D. C. Gowda, “Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta,” The Journal of Biological Chemistry, vol. 275, no. 51, pp. 40344–40356, 2000.
View at: Publisher Site | Google Scholar
J. Gysin, B. Pouvelle, M. Le Tonqueze, L. Edelman, and M.-C. Boffa, “Chondroitin sulfate of thrombomodulin is an adhesion receptor for Plasmodium falciparum-infected erythrocytes,” Molecular and Biochemical Parasitology, vol. 88, no. 1-2, pp. 267–271, 1997.
View at: Publisher Site | Google Scholar
S. Cheifetz and J. Massague, “Transforming growth factor- $β$ (TGF- $β$ ) receptor proteoglycan. Cell surface expression and ligand binding in the absence of glycosaminoglycan chains,” The Journal of Biological Chemistry, vol. 264, no. 20, pp. 12025–12028, 1989.
View at: Google Scholar
K. Miyake, C. B. Underhill, J. Lesley, and P. W. Kincade, “Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition,” Journal of Experimental Medicine, vol. 172, no. 1, pp. 69–75, 1990.
View at: Publisher Site | Google Scholar
S. Jalkanen, R. F. Bargatze, J. de los Toyos, and E. C. Butcher, “Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95-kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells,” The Journal of Cell Biology, vol. 105, no. 2, pp. 983–990, 1987.
View at: Publisher Site | Google Scholar
L. A. Goldstein, D. F. H. Zhou, L. J. Picker et al., “A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins,” Cell, vol. 56, no. 6, pp. 1063–1072, 1989.
View at: Publisher Site | Google Scholar
A. Nishiyama, K. J. Dahlin, J. T. Prince, S. R. Johnstone, and W. B. Stallcup, “The primary structure of NG2, a novel membrane-spanning proteoglycan,” The Journal of Cell Biology, vol. 114, no. 2, pp. 359–371, 1991.
View at: Publisher Site | Google Scholar
B. Gerlitz, T. Hassell, C. J. Vlahos, J. F. Parkinson, N. U. Bang, and B. W. Grinnell, “Identification of the predominant glycosaminoglycan-attachment site in soluble recombinant human thrombomodulin: potential regulation of functionality by glycosyltransferase competition for serine474,” Biochemical Journal, vol. 295, no. 1, pp. 131–140, 1993.
View at: Google Scholar
M. C. Bourin, M. C. Boffa, I. Björk, and U. Lindahl, “Functional domains of rabbit thrombomodulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 16, pp. 5924–5928, 1986.
View at: Publisher Site | Google Scholar
I. Maruyama, C. E. Bell, and P. W. Majerus, “Thrombomodulin is found on endothelium of arteries, veins, capillaries, and lymphatics, and on syncytiotrophoblast of human placenta,” The Journal of Cell Biology, vol. 101, no. 2, pp. 363–371, 1985.
View at: Publisher Site | Google Scholar
B. Maubert, L. J. Guilbert, and P. Deloron, “Cytoadherence of Plasmodium falciparum to intercellular adhesion molecule 1 and chondroitin-4-sulfate expressed by the syncytiotrophoblast in the human placenta,” Infection and Immunity, vol. 65, no. 4, pp. 1251–1257, 1997.
View at: Google Scholar
J. G. Beeson, W. Chai, S. J. Rogerson, A. M. Lawson, and G. V. Brown, “Inhibition of binding of malaria-infected erythrocytes by a tetradecasaccharide fraction from chondroitin sulfate A,” Infection and Immunity, vol. 66, no. 7, pp. 3397–3402, 1998.
View at: Google Scholar
J. G. Prudhomme, I. W. Sherman, K. M. Land, A. V. Moses, S. Stenglein, and J. A. Nelson, “Studies of plasmodium falciparum cytoadherence using immortalized human brain capillary endothelial cells,” International Journal for Parasitology, vol. 26, no. 6, pp. 647–655, 1996.
View at: Publisher Site | Google Scholar
A. Alkhalil, R. N. Achur, M. Valiyaveettil, C. F. Ockenhouse, and D. C. Gowda, “Structural requirements for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate proteoglycans of human placenta,” The Journal of Biological Chemistry, vol. 275, no. 51, pp. 40357–40364, 2000.
View at: Publisher Site | Google Scholar
W. Chai, J. G. Beeson, and A. M. Lawson, “The structural motif in chondroitin sulfate for adhesion of Plasmodium falciparum-infected erythrocytes comprises disaccharide units of 4- $O$ -sulfated and non-sulfated $N$ -acetylgalactosamine linked to glucuronic acid,” The Journal of Biological Chemistry, vol. 277, no. 25, pp. 22438–22446, 2002.
View at: Publisher Site | Google Scholar
R. N. Achur, M. Valiyaveettil, and D. C. Gowda, “The low sulfated chondroitin sulfate proteoglycans of human placenta have sulfate group-clustered domains that can efficiently bind Plasmodium falciparum-infected erythrocytes,” The Journal of Biological Chemistry, vol. 278, no. 13, pp. 11705–11713, 2003.
View at: Publisher Site | Google Scholar
J. G. Beeson, S. J. Rogerson, B. M. Cooke et al., “Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria,” Nature Medicine, vol. 6, no. 1, pp. 86–90, 2000.
View at: Publisher Site | Google Scholar
W. Chai, J. G. Beeson, H. Kogelberg, G. V. Brown, and A. M. Lawson, “Inhibition of adhesion of Plasmodium falciparum-infected erythrocytes by structurally defined hyaluronic acid dodecasaccharides,” Infection and Immunity, vol. 69, no. 1, pp. 420–425, 2001.
View at: Publisher Site | Google Scholar
M. Valiyaveettil, R. N. Achur, A. Alkhalil, C. F. Ockenhouse, and D. C. Gowda, “Plasmodium falciparum cytoadherence to human placenta: evaluation of hyaluronic acid and chondroitin 4-sulfate for binding of infected erythrocytes,” Experimental Parasitology, vol. 99, no. 2, pp. 57–65, 2001.
View at: Publisher Site | Google Scholar
C. A. Sunderland, J. N. Bulmer, M. Luscombe, C. W. G. Redman, and G. M. Stirrat, “Immunohistological and biochemical evidence for a role for hyaluronic acid in growth and development of the placenta,” Journal of Reproductive Immunology, vol. 8, no. 2-3, pp. 197–212, 1985.
View at: Publisher Site | Google Scholar
M. Mohamadzadeh, H. DeGrendele, H. Arizpe, P. Estess, and M. Siegelman, “Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion,” Journal of Clinical Investigation, vol. 101, no. 1, pp. 97–108, 1998.
View at: Google Scholar
N. Rasti, F. Namusoke, A. Chêne et al., “Nonimmune immunoglobulin binding and multiple adhesion characterize Plasmodium falciparum-infected erythrocytes of placental origin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 37, pp. 13795–13800, 2006.
View at: Publisher Site | Google Scholar
K. Flick, C. Scholander, Q. Chen et al., “Role of nonimmune IgG bound to PfEMP1 in placental malaria,” Science, vol. 293, no. 5537, pp. 2098–2100, 2001.
View at: Publisher Site | Google Scholar
M. J. Gardner, N. Hall, E. Fung et al., “Genome sequence of the human malaria parasite Plasmodium falciparum,” Nature, vol. 419, no. 6906, pp. 498–511, 2002.
View at: Publisher Site | Google Scholar
J. Zhang, “Evolution by gene duplication: an update,” Trends in Ecology and Evolution, vol. 18, no. 6, pp. 292–298, 2003.
View at: Publisher Site | Google Scholar
J. D. Smith, S. Kyes, A. G. Craig et al., “Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain,” Molecular and Biochemical Parasitology, vol. 97, no. 1-2, pp. 133–148, 1998.
View at: Publisher Site | Google Scholar
D. M. Engelman, T. A. Steitz, and A. Goldman, “Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins,” Annual Review of Biophysics and Biophysical Chemistry, vol. 15, pp. 321–353, 1986.
View at: Publisher Site | Google Scholar
Q. Chen, V. Fernandez, A. Sundström et al., “Developmental selection of var gene expression in Plasmodium falciparum,” Nature, vol. 394, no. 6691, pp. 392–395, 1998.
View at: Publisher Site | Google Scholar
A. Scherf, R. Hernandez-Rivas, P. Buffet et al., “Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum,” The EMBO Journal, vol. 17, no. 18, pp. 5418–5426, 1998.
View at: Publisher Site | Google Scholar
L. Florens, M. P. Washburn, J. D. Raine et al., “A proteomic view of the Plasmodium falciparum life cycle,” Nature, vol. 419, no. 6906, pp. 520–526, 2002.
View at: Publisher Site | Google Scholar
J. Peters, E. Fowler, M. Gatton, N. Chen, A. Saul, and Q. Cheng, “High diversity and rapid changeover of expressed var genes during the acute phase of Plasmodium falciparum infections in human volunteers,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 16, pp. 10689–10694, 2002.
View at: Publisher Site | Google Scholar
M. L. Gatton, J. M. Peters, E. V. Fowler, and Q. Cheng, “Switching rates of Plasmodium falciparum var genes: faster than we thought?” Trends in Parasitology, vol. 19, no. 5, pp. 202–208, 2003.
View at: Publisher Site | Google Scholar
K. W. Deitsch, A. del Pinal, and T. E. Wellems, “Intra-cluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum,” Molecular and Biochemical Parasitology, vol. 101, no. 1-2, pp. 107–116, 1999.
View at: Publisher Site | Google Scholar
S. M. Kraemer and J. D. Smith, “Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family,” Molecular Microbiology, vol. 50, no. 5, pp. 1527–1538, 2003.
View at: Publisher Site | Google Scholar
T. Lavstsen, A. Salanti, A. T. Jensen, D. E. Arnot, and T. G. Theander, “Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions,” Malaria Journal, vol. 2, no. 1, p. 27, 2003.
View at: Publisher Site | Google Scholar
M. S. Calderwood, L. Gannoun-Zaki, T. E. Wellems, and K. W. Deitsch, “Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron,” The Journal of Biological Chemistry, vol. 278, no. 36, pp. 34125–34132, 2003.
View at: Publisher Site | Google Scholar
K. W. Deitsch, M. S. Calderwood, and T. E. Wellems, “Malaria: cooperative silencing elements in var genes,” Nature, vol. 412, no. 6850, pp. 875–876, 2001.
View at: Publisher Site | Google Scholar
G. Winter, Q. Chen, K. Flick, P. Kremsner, V. Fernandez, and M. Wahlgren, “The 3D7var5.2 ( $v a r_{COMMON}$ ) type var gene family is commonly expressed in non-placental Plasmodium falciparum malaria,” Molecular and Biochemical Parasitology, vol. 127, no. 2, pp. 179–191, 2003.
View at: Publisher Site | Google Scholar
L. H. Freitas Jr., R. Hernandez-Rivas, S. A. Ralph et al., “Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites,” Cell, vol. 121, no. 1, pp. 25–36, 2005.
View at: Publisher Site | Google Scholar
M. T. Duraisingh, T. S. Voss, A. J. Marty et al., “Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum,” Cell, vol. 121, no. 1, pp. 13–24, 2005.
View at: Publisher Site | Google Scholar
T. Chookajorn, R. Dzikowski, M. Frank et al., “Epigenetic memory at malaria virulence genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 3, pp. 899–902, 2007.
View at: Publisher Site | Google Scholar
L. Hviid and T. Staalsoe, “Malaria immunity in infants: a special case of a general phenomenon?” Trends in Parasitology, vol. 20, no. 2, pp. 66–72, 2004.
View at: Publisher Site | Google Scholar
T. S. Voss, M. Kaestli, D. Vogel, S. Bopp, and H.-P. Beck, “Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters,” Molecular Microbiology, vol. 48, no. 6, pp. 1593–1607, 2003.
View at: Publisher Site | Google Scholar
J. C. Reeder, A. F. Cowman, K. M. Davern et al., “The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by P. falciparum erythrocyte membrane protein 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 9, pp. 5198–5202, 1999.
View at: Publisher Site | Google Scholar
P. A. Buffet, B. Gamain, C. Scheidig et al., “Plasmodium falciparum domain mediating adhesion to chondroitin sulfate A: a receptor for human placental infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 22, pp. 12743–12748, 1999.
View at: Publisher Site | Google Scholar
J. A. Rowe, S. A. Kyes, S. J. Rogerson, H. A. Babiker, and A. Raza, “Identification of a conserved Plasmodium falciparum var gene implicated in malaria in pregnancy,” The Journal of Infectious Diseases, vol. 185, no. 8, pp. 1207–1211, 2002.
View at: Publisher Site | Google Scholar
M. Fried and P. E. Duffy, “Two DBL $γ$ subtypes are commonly expressed by placental isolates of Plasmodium falciparum,” Molecular and Biochemical Parasitology, vol. 122, no. 2, pp. 201–210, 2002.
View at: Publisher Site | Google Scholar
S. A. Kyes, Z. Christodoulou, A. Raza et al., “A well-conserved Plasmodium falciparum var gene shows an unusual stage-specific transcript pattern,” Molecular Microbiology, vol. 48, no. 5, pp. 1339–1348, 2003.
View at: Publisher Site | Google Scholar
A. Salanti, T. Staalsoe, T. Lavstsen et al., “Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria,” Molecular Microbiology, vol. 49, no. 1, pp. 179–191, 2003.
View at: Publisher Site | Google Scholar
M. F. Duffy, T. J. Byrne, S. R. Elliott et al., “Broad analysis reveals a consistent pattern of var gene transcription in Plasmodium falciparum repeatedly selected for a defined adhesion phenotype,” Molecular Microbiology, vol. 56, no. 3, pp. 774–788, 2005.
View at: Publisher Site | Google Scholar
M. Fried, J. P. Wendler, T. K. Mutabingwa, and P. E. Duffy, “Mass spectrometric analysis of Plasmodium falciparum erythrocyte membrane protein-1 variants expressed by placental malaria parasites,” Proteomics, vol. 4, no. 4, pp. 1086–1093, 2004.
View at: Publisher Site | Google Scholar
A. S. Gowda, S. V. Madhunapantula, R. N. Achur, M. Valiyaveettil, V. P. Bhavanandan, and D. C. Gowda, “Structural basis for the adherence of Plasmodium falciparum-infected erythrocytes to chondroitin 4-sulfate and design of novel photoactivable reagents for the identification of parasite adhesive proteins,” The Journal of Biological Chemistry, vol. 282, no. 2, pp. 916–928, 2007.
View at: Publisher Site | Google Scholar
B. Gamain, A. R. Trimnell, C. Scheidig, A. Schert, L. H. Miller, and J. D. Smith, “Identification of multiple chondroitin sulfate A (CSA)-binding domains in the var2CSA gene transcribed in CSA-binding parasites,” The Journal of Infectious Diseases, vol. 191, no. 6, pp. 1010–1013, 2005.
View at: Publisher Site | Google Scholar
M. Fried and P. E. Duffy, “Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta,” Science, vol. 272, no. 5267, pp. 1502–1504, 1996.
View at: Publisher Site | Google Scholar
R. N. Achur, M. Valiyaveettil, A. Alkhalil, C. F. Ockenhouse, and D. C. Gowda, “Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta,” The Journal of Biological Chemistry, vol. 275, no. 51, pp. 40344–40356, 2000.
View at: Publisher Site | Google Scholar
P. C. Bull, B. S. Lowe, M. Kortok, and K. Marsh, “Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants,” Infection and Immunity, vol. 67, no. 2, pp. 733–739, 1999.
View at: Google Scholar
M. Fried, F. Nosten, A. Brockman, B. J. Brabin, and P. E. Duffy, “Maternal antibodies block malaria,” Nature, vol. 395, no. 6705, pp. 851–852, 1998.
View at: Publisher Site | Google Scholar
K. Marsh, L. Otoo, R. J. Hayes, D. C. Carson, and B. M. Greenwood, “Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 83, no. 3, pp. 293–303, 1989.
View at: Publisher Site | Google Scholar
M. A. Nielsen, L. S. Vestergaard, J. Lusingu et al., “Geographical and temporal conservation of antibody recognition of Plasmodium falciparum variant surface antigens,” Infection and Immunity, vol. 72, no. 6, pp. 3531–3535, 2004.
View at: Publisher Site | Google Scholar
T. Staalsoe, C. E. Shulman, J. N. Bulmer, K. Kawuondo, K. Marsh, and L. Hviid, “Variant surface antigen-specific IgG and protection against clinical consequences of pregnancy-associated Plasmodium falciparum malaria,” The Lancet, vol. 363, no. 9405, pp. 283–289, 2004.
View at: Publisher Site | Google Scholar
P. E. Duffy and M. Fried, “Antibodies that inhibit Plasmodium falciparum adhesion to chondroitin sulfate A are associated with increased birth weight and the gestational age of newborns,” Infection and Immunity, vol. 71, no. 11, pp. 6620–6623, 2003.
View at: Publisher Site | Google Scholar
M. Fried and P. E. Duffy, “Maternal malaria and parasite adhesion,” Journal of Molecular Medicine, vol. 76, no. 3-4, pp. 162–171, 1998.
View at: Publisher Site | Google Scholar
M. F. Duffy, A. Caragounis, R. Noviyanti et al., “Transcribed var genes associated with placental malaria in Malawian women,” Infection and Immunity, vol. 74, no. 8, pp. 4875–4883, 2006.
View at: Publisher Site | Google Scholar
A. Salanti, M. Dahlbäck, L. Turner et al., “Evidence for the involvement of VAR2CSA in pregnancy-associated malaria,” Journal of Experimental Medicine, vol. 200, no. 9, pp. 1197–1203, 2004.
View at: Publisher Site | Google Scholar
L. Barfod, N. L. Bernasconi, M. Dahlbäck et al., “Human pregnancy-associated malaria-specific B cells target polymorphic, conformational epitopes in VAR2CSA,” Molecular Microbiology, vol. 63, no. 2, pp. 335–347, 2007.
View at: Publisher Site | Google Scholar
N. Tuikue Ndam, A. Salanti, J.-Y. Le-Hesran et al., “Dynamics of anti-VAR2CSA immunoglobulin G response in a cohort of senegalese pregnant women,” The Journal of Infectious Diseases, vol. 193, no. 5, pp. 713–720, 2006.
View at: Publisher Site | Google Scholar
M. Avril, B. Gamain, C. LéPolard, N. Viaud, A. Scherf, and J. Gysin, “Characterization of anti-var2CSA-PfEMP1 cytoadhesion inhibitory mouse monoclonal antibodies,” Microbes and Infection, vol. 8, no. 14-15, pp. 2863–2871, 2006.
View at: Publisher Site | Google Scholar
R. Megnekou, T. Staalsoe, D. W. Taylor, R. Leke, and L. Hviid, “Effects of pregnancy and intensity of Plasmodium falciparum transmission on immunoglobulin G subclass responses to variant surface antigens,” Infection and Immunity, vol. 73, no. 7, pp. 4112–4118, 2005.
View at: Publisher Site | Google Scholar
A. T. R. Jensen, P. Magistrado, S. Sharp et al., “Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes,” Journal of Experimental Medicine, vol. 199, no. 9, pp. 1179–1190, 2004.
View at: Publisher Site | Google Scholar
L. Hviid and T. Staalsoe, “Malaria immunity in infants: a special case of a general phenomenon?” Trends in Parasitology, vol. 20, no. 2, pp. 66–72, 2004.
View at: Publisher Site | Google Scholar
T. Lavstsen, P. Magistrado, C. C. Hermsen et al., “Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans,” Malaria Journal, vol. 4, no. 1, p. 21, 2005.
View at: Publisher Site | Google Scholar
M. Dahlbäck, T. S. Rask, P. H. Andersen et al., “Epitope mapping and topographic analysis of VAR2CSA DBL3X involved in P. falciparum placental sequestration,” PLoS Pathogens, vol. 2, no. 11, p. e124, 2006.
View at: Publisher Site | Google Scholar
L. Krishnan, L. J. Guilbert, T. G. Wegmann, M. Belosevic, and T. R. Mosmann, “T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions: correlation with increased IFN- $γ$ and TNF and reduced IL-10 production by placental cells,” The Journal of Immunology, vol. 156, no. 2, pp. 653–662, 1996.
View at: Google Scholar
T. G. Wegmann, H. Lin, L. Guilbert, and T. R. Mosmann, “Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a $T_{H} 2$ phenomenon?” Immunology Today, vol. 14, no. 7, pp. 353–356, 1993.
View at: Publisher Site | Google Scholar
G. Chaouat, V. Cayol, V. Mairovitz, and S. Dubanchet, “Localization of the Th2 cytokines IL-3, IL-4, IL-10 at the fetomaternal interface during human and murine pregnancy and lack of requirement for Fas/Fas ligand interaction for a successful allogeneic pregnancy,” American Journal of Reproductive Immunology, vol. 42, no. 1, pp. 1–13, 1999.
View at: Google Scholar
G. P. Sacks, K. Studena, I. L. Sargent, and C. W. G. Redman, “Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis,” American Journal of Obstetrics and Gynecology, vol. 179, no. 1, pp. 80–86, 1998.
View at: Publisher Site | Google Scholar
M. Fried, R. O. Muga, A. O. Misore, and P. E. Duffy, “Malaria elicits type 1 cytokines in the human placenta: IFN- $γ$ and TNF- $α$ associated with pregnancy outcomes,” The Journal of Immunology, vol. 160, no. 5, pp. 2523–2530, 1998.
View at: Google Scholar
A. M. Moormann, A. D. Sullivan, R. A. Rochford et al., “Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation,” The Journal of Infectious Diseases, vol. 180, no. 6, pp. 1987–1993, 1999.
View at: Publisher Site | Google Scholar
N. Fievet, M. Moussa, G. Tami et al., “Plasmodium falciparum induces a Th1/Th2 disequilibrium, favoring the Th1-type pathway, in the human placenta,” The Journal of Infectious Diseases, vol. 183, no. 10, pp. 1530–1534, 2001.
View at: Google Scholar
I. Diouf, N. Fievet, S. Doucouré et al., “Monocyte activation and T cell inhibition in Plasmodium falciparum-infected placenta,” The Journal of Infectious Diseases, vol. 189, no. 12, pp. 2235–2242, 2004.
View at: Publisher Site | Google Scholar
J. Ordi, M. R. Ismail, P. J. Ventura et al., “Massive chronic intervillositis of the placenta associated with malaria infection,” American Journal of Surgical Pathology, vol. 22, no. 8, pp. 1006–1011, 1998.
View at: Publisher Site | Google Scholar
J. M. Moore, B. L. Nahlen, A. Misore, A. A. Lal, and V. Udhayakumar, “Immunity to placental malaria. I. Elevated production of interferon- $γ$ by placental blood mononuclear cells is associated with protection in an area with high transmission of malaria,” The Journal of Infectious Diseases, vol. 179, no. 5, pp. 1218–1225, 1999.
View at: Publisher Site | Google Scholar
J. G. Beeson, S. J. Rogerson, S. R. Elliott, and M. F. Duffy, “Targets of protective antibodies to malaria during pregnancy,” The Journal of Infectious Diseases, vol. 192, no. 9, pp. 1647–1650, 2005.
View at: Publisher Site | Google Scholar
S. Chaisavaneeyakorn, N. Lucchi, C. Abramowsky et al., “Immunohistological characterization of macrophage migration inhibitory factor expression in Plasmodium falciparum-infected placentas,” Infection and Immunity, vol. 73, no. 6, pp. 3287–3293, 2005.
View at: Publisher Site | Google Scholar
G. Bertin, N. Tuikue Ndam, S. Jafari-Guemouri et al., “High prevalence of Plasmodium falciparum pfcrt K76T mutation in pregnant women taking chloroquine prophylaxis in Senegal,” Journal of Antimicrobial Chemotherapy, vol. 55, no. 5, pp. 788–791, 2005.
View at: Publisher Site | Google Scholar
L. J. Schultz, R. W. Steketee, L. Chitsulo, A. Macheso, Y. Nyasulu, and M. Ettling, “Malaria and childbearing women in Malawi: knowledge, attitudes and practices,” Tropical Medicine and Parasitology, vol. 45, no. 1, pp. 65–69, 1994.
View at: Google Scholar
M. E. Parise, J. G. Ayisi, B. L. Nahlen et al., “Efficacy of sulfadoxine-pyrimethamine for prevention of placental malaria in an area of Kenya with a high prevalence of malaria and human immunodeficiency virus infection,” American Journal of Tropical Medicine and Hygiene, vol. 59, no. 5, pp. 813–822, 1998.
View at: Google Scholar
C. E. Shulman, E. K. Dorman, F. Cutts et al., “Intermittent sulphadoxine-pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo-controlled trial,” The Lancet, vol. 353, no. 9153, pp. 632–636, 1999.
View at: Publisher Site | Google Scholar
A. M. Vogt, F. Pettersson, K. Moll et al., “Release of sequestered malaria parasites upon injection of a glycosaminoglycan,” PLoS Pathogens, vol. 2, no. 9, p. e100, 2006.
View at: Publisher Site | Google Scholar
D. Spillmann, “Carbohydrates in cellular recognition: from leucine-zipper to sugar-zipper?” Glycoconjugate Journal, vol. 11, no. 3, pp. 169–171, 1994.
View at: Publisher Site | Google Scholar
A. Barragan, D. Spillmann, J. Carlson, and M. Wahlgren, “Role of glycans in Plasmodium falciparum infection,” Biochemical Society Transactions, vol. 27, no. 4, pp. 487–493, 1999.
View at: Google Scholar
B. Pouvelle, P. Meyer, C. Robert, L. Bardel, and J. Gysin, “Chondroitin-4-sulfate impairs in vitro and in vivo cytoadherence of Plasmodium falciparum infected erythrocytes,” Molecular Medicine, vol. 3, no. 8, pp. 508–518, 1997.
View at: Google Scholar
J. Carlson and M. Wahlgren, “Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions,” Journal of Experimental Medicine, vol. 176, no. 5, pp. 1311–1317, 1992.
View at: Publisher Site | Google Scholar
D. L. Clark, S. Su, and E. A. Davidson, “Saccharide anions as inhibitors of the malaria parasite,” Glycoconjugate Journal, vol. 14, no. 4, pp. 473–479, 1997.
View at: Publisher Site | Google Scholar
A. Rowe, A. R. Berendt, K. Marsh, and C. I. Newbold, “Plasmodium falciparum: a family of sulphated glycoconjugates disrupts erythrocyte rosettes,” Experimental Parasitology, vol. 79, no. 4, pp. 506–516, 1994.
View at: Publisher Site | Google Scholar
L. Xiao, C. Yang, P. S. Patterson, V. Udhayakumar, and A. A. Lal, “Sulfated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes,” Infection and Immunity, vol. 64, no. 4, pp. 1373–1378, 1996.
View at: Google Scholar
K. T. Andrews, N. Klatt, Y. Adams, P. Mischnick, and R. Schwartz-Albiez, “Inhibition of chondroitin-4-sulfate-specific adhesion of Plasmodium falciparum-infected erythrocytes by sulfated polysaccharides,” Infection and Immunity, vol. 73, no. 7, pp. 4288–4294, 2005.
View at: Publisher Site | Google Scholar

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Copyright © 2007 Nicaise Tuikue Ndam and Philippe Deloron. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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