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Journal of Biomedicine and Biotechnology
Volume 2007, Article ID 43785, 13 pages
http://dx.doi.org/10.1155/2007/43785
Review Article

Molecular Aspects of Plasmodium falciparum Infection during Pregnancy

UR 010, Laboratoire de Parasitologie, Institut de Recherche pour le Développement, Université Paris Descartes, IFR 71, 4 avenue de l'Observatoire, Paris 75006, France

Received 29 December 2006; Accepted 21 March 2007

Academic Editor: Ali Ouaissi

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.

Linked References

  1. K. Marsh and R. W. Snow, “Malaria transmission and morbidity,” Parassitologia, vol. 41, no. 1–3, pp. 241–246, 1999. View at Google Scholar
  2. 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 · View at Google Scholar
  3. 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 · View at Google Scholar
  4. 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 · View at Google Scholar
  5. H. Ekvall, “Malaria and anemia,” Current Opinion in Hematology, vol. 10, no. 2, pp. 108–114, 2003. View at Publisher · View at Google Scholar
  6. L. H. Miller, M. F. Good, and G. Milon, “Malaria pathogenesis,” Science, vol. 264, no. 5167, pp. 1878–1883, 1994. View at Publisher · View at Google Scholar
  7. 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 · View at Google Scholar
  8. 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 · View at Google Scholar
  9. 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 · View at Google Scholar
  10. 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 · View at Google Scholar
  11. 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 · View at Google Scholar
  12. 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 · View at Google Scholar
  13. 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 · View at Google Scholar
  14. 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 · View at Google Scholar
  15. 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
  16. 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
  17. 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 · View at Google Scholar
  18. 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 · View at Google Scholar
  19. 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
  20. 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 · View at Google Scholar
  21. 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
  22. 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 · View at Google Scholar
  23. 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
  24. 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 · View at Google Scholar
  25. 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
  26. 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 · View at Google Scholar
  27. 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 · View at Google Scholar
  28. 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
  29. 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 · View at Google Scholar
  30. 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 · View at Google Scholar
  31. 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 · View at Google Scholar
  32. 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 · View at Google Scholar
  33. 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 · View at Google Scholar
  34. 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 · View at Google Scholar
  35. 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 · View at Google Scholar
  36. 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 · View at Google Scholar
  37. 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 · View at Google Scholar
  38. 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 · View at Google Scholar
  39. 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
  40. 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 · View at Google Scholar
  41. 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 · View at Google Scholar
  42. 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 · View at Google Scholar
  43. 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 · View at Google Scholar
  44. 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
  45. 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 · View at Google Scholar
  46. 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 · View at Google Scholar
  47. 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
  48. 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
  49. 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 · View at Google Scholar
  50. 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 · View at Google Scholar
  51. 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 · View at Google Scholar
  52. 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 · View at Google Scholar
  53. 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 · View at Google Scholar
  54. 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 · View at Google Scholar
  55. 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 · View at Google Scholar
  56. 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 · View at Google Scholar
  57. 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
  58. 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 · View at Google Scholar
  59. 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 · View at Google Scholar
  60. 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 · View at Google Scholar
  61. J. Zhang, “Evolution by gene duplication: an update,” Trends in Ecology and Evolution, vol. 18, no. 6, pp. 292–298, 2003. View at Publisher · View at Google Scholar
  62. 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 · View at Google Scholar
  63. 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 · View at Google Scholar
  64. 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 · View at Google Scholar
  65. 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 · View at Google Scholar
  66. 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 · View at Google Scholar
  67. 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 · View at Google Scholar
  68. 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 · View at Google Scholar
  69. 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 · View at Google Scholar
  70. 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 · View at Google Scholar
  71. 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 · View at Google Scholar
  72. 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 · View at Google Scholar
  73. 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 · View at Google Scholar
  74. G. Winter, Q. Chen, K. Flick, P. Kremsner, V. Fernandez, and M. Wahlgren, “The 3D7var5.2 (varCOMMON) 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 · View at Google Scholar
  75. 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 · View at Google Scholar
  76. 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 · View at Google Scholar
  77. 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 · View at Google Scholar
  78. 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 · View at Google Scholar
  79. 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 · View at Google Scholar
  80. 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 · View at Google Scholar
  81. 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 · View at Google Scholar
  82. 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 · View at Google Scholar
  83. M. Fried and P. E. Duffy, “Two DBLγ 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 · View at Google Scholar
  84. 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 · View at Google Scholar
  85. 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 · View at Google Scholar
  86. 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 · View at Google Scholar
  87. 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 · View at Google Scholar
  88. 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 · View at Google Scholar
  89. 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 · View at Google Scholar
  90. 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 · View at Google Scholar
  91. 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 · View at Google Scholar
  92. 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
  93. 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 · View at Google Scholar
  94. 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 · View at Google Scholar
  95. 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 · View at Google Scholar
  96. 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 · View at Google Scholar
  97. 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 · View at Google Scholar
  98. 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 · View at Google Scholar
  99. 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 · View at Google Scholar
  100. 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 · View at Google Scholar
  101. 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 · View at Google Scholar
  102. 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 · View at Google Scholar
  103. 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 · View at Google Scholar
  104. 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 · View at Google Scholar
  105. 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 · View at Google Scholar
  106. 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 · View at Google Scholar
  107. 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 · View at Google Scholar
  108. 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 · View at Google Scholar
  109. 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
  110. T. G. Wegmann, H. Lin, L. Guilbert, and T. R. Mosmann, “Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?” Immunology Today, vol. 14, no. 7, pp. 353–356, 1993. View at Publisher · View at Google Scholar
  111. 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
  112. 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 · View at Google Scholar
  113. 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
  114. 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 · View at Google Scholar
  115. 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
  116. 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 · View at Google Scholar
  117. 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 · View at Google Scholar
  118. 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 · View at Google Scholar
  119. 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 · View at Google Scholar
  120. 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 · View at Google Scholar
  121. 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 · View at Google Scholar
  122. 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
  123. 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
  124. 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 · View at Google Scholar
  125. 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 · View at Google Scholar
  126. 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 · View at Google Scholar
  127. 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
  128. 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
  129. 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 · View at Google Scholar
  130. 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 · View at Google Scholar
  131. 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 · View at Google Scholar
  132. 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
  133. 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 · View at Google Scholar