Sequential, ordered acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 domains

Journal of Immunology

Volumn 183, Issue 5, 2009, Pages 3356-3363

  Cham, Gerald K K ^a,b   Turner, Louise ^a,b   Lusingu, John ^a,b,d   Vestergaard, Lasse ^a,b   Mmbando, Bruno P ^d   Kurtis, Jonathan D ^c   Jensen, Anja T R ^a,b   Salanti, Ali ^a,b   Lavstsen, Thomas ^a,b   Theander, Thor G ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Mental Health Services CPH   (Denmark)

^c BROWN UNIVERSITY   (United States)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ERYTHROCYTE MEMBRANE PROTEIN 1; LIGAND; MALARIA VACCINE; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ADOLESCENT; ADULT; AFRICA; ANTIBODY BLOOD LEVEL; ARTICLE; CHILD; DISEASE TRANSMISSION; HUMAN; INFANT; MALARIA; NEWBORN; PARASITE; PATHOGENICITY; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SCHOOL CHILD; AGE; ANIMAL; BIOSYNTHESIS; BLOOD; CROSS-SECTIONAL STUDY; ERYTHROCYTE MEMBRANE; IMMUNOLOGY; MALARIA FALCIPARUM; MIDDLE AGED; PARASITEMIA; PARASITOLOGY; PREVALENCE; PROTEIN TERTIARY STRUCTURE;

ADOLESCENT; ADULT; AGE FACTORS; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; ERYTHROCYTE MEMBRANE; HUMANS; INFANT; INFANT, NEWBORN; MALARIA, FALCIPARUM; MIDDLE AGED; PARASITEMIA; PLASMODIUM FALCIPARUM; PREVALENCE; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; YOUNG ADULT;

EID: 70349243273     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901331     Document Type: Article

References (41)

1. Christophers, S. R. 1924. The mechanism of immunity against malaria in communities living under hyper-endemic conditions. Indian J. Med. Res. 12: 273-294.
2. Gupta, S., R. W. Snow, C. A. Donnelly, K. Marsh, and C. Newbold. 1999. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat. Med. 5: 340-343.
3. MacDonald, G. 1957. The Epidemiology and Control of Malaria. Oxford Univ, Press, London.
4. Leech, J. H., J. W. Barnwell, L. H. Miller, and R. J. Howard. 1984. Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J. Exp. Med. 159: 1567-1575.
5. Smith, J. D., C. E. Chitnis, A. G. Craig, D. J. Roberts, D. E. Hudson-Taylor, D. S. Peterson, R. Pinches, C. I. Newbold, and L. H. Miller. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110.
6. Baruch, D. I., B. L. Pasloske, H. B. Singh, X. Bi, X. C. Ma, M. Feldman, T. F. Taraschi, and R. J. Howard. 1995. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82: 77-87.
7. Su, X., V. M. Heatwole, S. P. Wertheimer, F. Guinet, J. A. Herrfeldt, D. S. Peterson, J. A. Ravetch, and T. E. Wellems. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
8. Scherf, A., J. J. Lopez-Rubio, and L. Riviere. 2008. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62: 445-470.
9. Roberts, D. J., A. G. Craig, A. R. Berendt, R. Pinches, G. Nash, K. Marsh, and C. I. Newbold. 1992. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature. 357: 689-692.
10. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
11. Kraemer, S. M., and J. D. Smith. 2003. Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol. Microbiol. 50: 1527-1538.
12. Lavstsen, T., A. Salanti, A. T. R. Jensen, D. E. Arnot, and T. G. Theander. 2003. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar. J. 2: 27.
13. Smith, J. D., G. Subramanian, B. Gamain, D. I. Baruch, and L. H. Miller. 2000. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol. Biochem. Parasitol. 110: 293-310.
14. Kraemer, S. M., S. A. Kyes, G. Aggarwal, A. L. Springer, S. O. Nelson, Z. Christodoulou, L. M. Smith, W. Wang, E. Levin, C. I. Newbold, et al. 2007. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45.
15. Salanti, A., T. Staalsoe, T. Lavstsen, A. T. R. Jensen, M. P. K. Sowa, D. E. Arnot, L. Hviid, and T. G. Theander. 2003. Selective upregulation of a single distinctly structured var gene in CSA-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 49: 179-191.
16. Salanti, A., M. Dahlbäck, L. Turner, M. A. Nielsen, L. Barfod, P. Magistrado, A. T. R. Jensen, T. Lavstsen, M. F. Ofori, K. Marsh, et al. 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200: 1197-1203.
17. Bull, P. C., M. Kortok, O. Kai, F. Ndungu, A. Ross, B. S. Lowe, C. I. Newbold, and K. Marsh. 2000. Plasmodium falciparum-infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. J. Infect. Dis. 182: 252-259.
18. Nielsen, M. A., T. Staalsoe, J. A. L. Kurtzhals, B. Q. Goka, D. Dodoo, M. Alifrangis, T. G. Theander, B. D. Akanmori, and L. Hviid. 2002. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and non-severe malaria and is modified by acquired immunity. J. Immunol. 168: 3444-3450.
19. Jensen, A. T. R., P. A. Magistrado, S. Sharp, L. Joergensen, T. Lavstsen, A. Chiucchiuini, A. Salanti, L. S. Vestergaard, J. P. Lusingu, R. Hermsen, et al. 2004. Plasmodium falciparum associated with severe childhood malaria preferentially expresses PfEMP1 encoded by group A var genes. J. Exp. Med. 199: 1179-1190.
20. Kyriacou, H. M., G. N. Stone, R. J. Challis, A. Raza, K. E. Lyke, M. A. Thera, A. K. Kone, O. K. Doumbo, C. V. Plowe, and J. A. Rowe. 2006. Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Mol. Biochem. Parasitol. 150: 211-218.
21. Rottmann, M., T. Lavstsen, J. P. Mugasa, M. Kaestli, A. T. R. Jensen, D. Müller, T. Theander, and H.-P. Beck. 2006. Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children. Infect. Immun. 74: 3904-3911.
22. Kaestli, M., I. A. Cockburn, A. Cortes, K. Baea, J. A. Rowe, and H. P. Beck. 2006. Virulence of malaria is associated with differential expression of Plasmodium falciparum var gene subgroups in a case-control study. J. Infect. Dis. 193: 1567-1574. (Pubitemid 43794587)
23. Drakeley, C. J., I. Carneiro, H. Reyburn, R. Malima, J. P. Lusingu, J. Cox, T. G. Theander, W. M. Nkya, M. M. Lemnge, and E. M. Riley. 2005. Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J. Infect. Dis. 191: 1589-1598.
24. Lusingu, J. P., L. S. Vestergaard, B. P. Mmbando, C. J. Drakeley, C. Jones, J. Akida, Z. X. Savaeli, A. Y. Kitua, M. M. Lemnge, and T. G. Theander. 2004. Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in north-eastern Tanzania. Malar. J. 3: 26.
25. Lusingu, J. P., A. T. Jensen, L. S. Vestergaard, D. T. Minja, M. B. Dalgaard, S. Gesase, B. P. Mmbando, A. Y. Kitua, M. M. Lemnge, D. Cavanagh, et al. 2006. Levels of plasma immunoglobulin G with specificity against the cysteine-rich interdomain regions of a semiconserved Plasmodium falciparum erythrocyte membrane protein 1, VAR4, predict protection against malarial anemia and febrile episodes. Infect. Immun. 74: 2867-2875.
26. Heegaard, E. D., K. Qvortrup, and J. Christensen. 2002. Baculovirus expression of erythrovirus V9 capsids and screening by ELISA: serologic cross-reactivity with erythrovirus B19. J. Med. Virol. 66: 246-252.
27. Cham, G. K., J. Kurtis, J. Lusingu, T. G. Theander, A. T. Jensen, and L. Turner. 2008. A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malar. J. 7: 108.
28. Staalsoe, T., H. A. Giha, D. Dodoo, T. G. Theander, and L. Hviid. 1999. Detection of antibodies to variant antigens on Plasmodium falciparum infected erythrocytes by flow cytometry. Cytometry 35: 329-336. (Pubitemid 29160231)
29. Marsh, K., J. A. Sherwood, and R. J. Howard. 1986. Parasite-infected cell agglutination and indirect immunofluorescence assays for detection of human serum antibodies bound to antigens on Plasmodium falciparum-infected erythrocytes. J. Immunol. Methods 91: 107-115.
30. Winter, G., S. Kawai, M. Haeggström, O. Kaneko, A. von Euler, S. Kawazu, D. Palm, V. Fernandez, and M. Wahlgren. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J. Exp. Med. 201: 1853-1863.
31. Marsh, K., and R. J. Howard. 1986. Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 231: 150-153. (Pubitemid 16154704)
32. Vestergaard, L. S., J. P. Lusingu, M. A. Nielsen, B. P. Mmbando, D. Dodoo, B. D. Akanmori, M. Alifrangis, I. C. Bygbjerg, M. M. Lemnge, T. Staalsoe, et al. 2008. Differences in human antibody reactivity to Plasmodium falciparum variant surface antigens are dependent on age and malaria transmission intensity in northeastern Tanzania. Infect. Immun. 76: 2706-2714.
33. Marsh, K., L. Otoo, R. J. Hayes, D. C. Carson, and B. M. Greenwood. 1989. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans. R. Soc. Trop. Med. Hyg. 83: 293-303.
34. Bull, P. C., B. S. Lowe, M. Kortok, C. S. Molyneux, C. I. Newbold, and K. Marsh. 1998. Parasite antigens on the infected red cell are targets for naturally acquired immunity to malaria. Nat. Med. 4: 358-360.
35. Giha, H. A., T. Staalsoe, D. Dodoo, C. Roper, G. M. Satti, D. E. Arnot, L. Hviid, and T. G. Theander. 2000. Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immunol. Lett. 71: 117-126.
36. Dodoo, D., T. Staalsoe, H. Giha, J. A. L. Kurtzhals, B. D. Akanmori, K. Koram, S. Dunyo, F. K. Nkrumah, L. Hviid, and T. G. Theander. 2001. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infect. Immun. 69: 3713-3718.
37. Bull, P. C., B. S. Lowe, M. Kortok, and K. Marsh. 1999. Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect. Immun. 67: 733-739.
38. Lavstsen, T., P. Magistrado, C. C. Hermsen, A. Salanti, A. T. R. Jensen, R. Sauerwein, L. Hviid, T. G. Theander, and T. Staalsoe. 2005. Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar. J. 4: 21.
39. Joergensen, L., L. Turner, P. Magistrado, M. Dahlbäck, L. Vestergaard, J. P. Lusingu, M. Lemnge, A. Salanti, T. G. Theander, and A. T. R. Jensen. 2006. Limited cross-reactivity among domains of the 3D7 Plasmodium falciparum erythrocyte membrane protein 1 family. Infect. Immun. 74: 6778-6784.
40. Joergensen, L., L. S. Vestergaard, L. Turner, P. Magistrado, J. P. Lusingu, M. Lemnge, T. G. Theander, and A. T. R. Jensen. 2007. 3D7-derived Plasmodium falciparum erythrocyte membrane protein 1 is a frequent target of naturally acquired antibodies recognizing protein domains in a particular pattern independent of malaria transmission intensity. J. Immunol. 178: 428-435.
41. Magistrado, P., J. Lusingu, L. S. Vestergaard, M. Lemnge, T. Lavstsen, L. Turner, L. Hviid, A. T. R. Jensen, and T. G. Theander. 2007. Immunoglobulin G antibody reactivity to a group A Plasmodium falciparum erythrocyte membrane protein 1 and protection from P. falciparum malaria. Infect. Immun. 75: 2415-2420.