Generation of cross-protective antibodies against Plasmodium falciparum sequestration by immunization with an erythrocyte membrane protein 1-duffy binding-like 1α domain

Infection and Immunity

Volumn 75, Issue 1, 2007, Pages 211-219

  Moll, Kirsten ^a,b   Pettersson, Fredrik ^a,b   Vogt, Anna M ^a,b   Jonsson, Cathrine ^c   Rasti, Niloofar ^a,b   Ahuja, Sanjay ^a,b   Spångberg, Mats ^b   Mercereau Puijalon, Odile ^d   Arnot, David E ^e   Wahlgren, Mats ^a,b   Chen, Qijun ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d INSTITUT PASTEUR   (France)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS REACTING ANTIBODY; ERYTHROCYTE MEMBRANE PROTEIN 1 DUFFY BINDING LIKE 1ALPHA; MALARIA VACCINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ADHESION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLONE; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; DRUG EFFECT; DRUG EFFICACY; EVALUATION; FEMALE; HUMAN; IMMUNIZATION; INFECTION PREVENTION; MACACA; MALARIA FALCIPARUM; MALE; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; SEMLIKI FOREST ALPHAVIRUS; SPRAGUE DAWLEY RAT; VIRUS PARTICLE; VIRUS RECOMBINANT;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; DISEASE MODELS, ANIMAL; ERYTHROCYTE MEMBRANE; FEMALE; FLOW CYTOMETRY; HUMANS; MACACA FASCICULARIS; MALARIA VACCINES; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS;

EID: 33845966058     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00749-06     Document Type: Article

References (42)

1. Abdel-Latif, M. S., K. Dietz, S. Issifou, P. G. Kremsner, and M. Q. Klinkert. 2003. Antibodies to Plasmodium falciparum rifin proteins are associated with rapid parasite clearance and asymptomatic infections. Infect. Immun. 71: 6229-6233.
2. Baruch, D. I., B. Gamain, and L. H. Miller, 2003. DNA immunization with the cysteine-rich interdomain region 1 of the Plasmodium falciparum variant antigen elicits limited cross-reactive antibody responses. Infect. Immun. 71: 4536-4543.
3. Beeson, J. G., G. V. Brown, M. E. Molyneux, C. Mhango, F. Dzinjalamala, and S. J. Rogerson. 1999. Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties. J. Infect. Dis. 180:464-472.
4. 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.
5. 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.
6. 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 surface are targets for naturally acquired immunity to malaria. Nat. Med. 4:358-360.
7. Bull, P. C., A. Pain, F. M. Ndungu, S. M. Kinyanjui, D. J. Roberts, C. I. Newbold, and K. Marsh. 2005. Plasmodium falciparum antigenic variation: relationships between in vivo selection, acquired antibody response, and disease severity. J. Infect. Dis. 192:1119-1126.
8. Carlson, J., H. Helmby, A. V. Hill, D. Brewster, B. M. Greenwood, and M. Wahlgren. 1990. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336:1457-1460.
9. Carlson, J., and M. Wahlgren. 1992. Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J. Exp. Med. 176:1311-1317.
10. Chattopadhyay, R., A. Sharma, V. K. Srivastava, S. S. Pati, S. K. Sharma, B. S. Das, and C. E. Chitnis. 2003. Plasmodium falciparum infection elicits both variant-specific and cross-reactive antibodies against variant surface antigens. Infect. Immun. 71:597-604.
11. Chen, Q., A. Barragan, V. Fernandez, A. Sundstrom, M. Schlichtherle, A. Sahlen, J. Carlson, S. Datta, and M. Wahlgren. 1998. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J. Exp. Med. 187:15-23.
12. Chen, Q., V. Fernandez, A. Sundstrom, M. Schlichtherle, S. Datta, P. Hagblom, and M. Wahlgren. 1998. Developmental selection of var gene expression in Plasmodium falciparum. Nature 394:392-395.
13. Chen, Q., A. Heddini, A. Barragan, V. Fernandez, S. F. Pearce, and M. Wahlgren. 2000. The semiconserved head structure of Plasmodium falciparum erythrocyte membrane protein 1 mediates binding to multiple independent host receptors. J. Exp. Med. 192:1-10.
14. Chen, Q., F. Pettersson, A. M. Vogt, B. Schmidt, S. Ahuja, P. Liljestrom, and M. Wahlgren. 2004. Immunization with PfEMP1-DBL1alpha generates antibodies that disrupt rosettes and protect against the sequestration of Plasmodium falciparum-infected erythrocytes. Vaccine 22:2701-2712.
15. Donnelly, J. J., B. Wahren, and M. A. Liu. 2005. DNA vaccines: progress and challenges. J. Immunol. 175:633-639.
16. Fernandez, V., M. Hommel, Q. Chen, P. Hagblom, and M. Wahlgren. 1999. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J. Exp. Med. 190:1393-1404.
17. Fernandez, V., C. J. Treutiger, G. B. Nash, and M. Wahlgren. 1998. Multiple adhesive phenotypes linked to rosetting binding of erythrocytes in Plasmodium falciparum malaria. Infect. Immun. 66:2969-2975.
18. Flick, K., and Q. Chen. 2004. var genes, PfEMP1 and the human host. Mol. Biochem. Parasitol. 134:3-9.
19. Heddini, A., F. Pettersson, O. Kal, J. Shafi, J. Obiero, Q. Chen, A. Barragan, M. Wahlgren, and K. Marsh. 2001. Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infect. Immun. 69:5849-5856.
20. Ljungström, I., H. Perlmann, M. Schlichtherle, A. Scherf, and M. Wahlgren. 2004. Methods in Malaria Research, 4th ed. MR4/ATCC, Manassas, VA http://www.malaria.atcc.org/MR4_Protocols.html.
21. Marsh, K. 1999. Clinical features of malaria, p. 87-118. In M. Wahlgren and P. Perlmann (ed.), Malaria-molecular and clinical aspects. Harwood Academic Publishers, Newark, NJ.
22. Newton, C. R., T. T. Hien, and N. White. 2000. Cerebral malaria. J. Neurol. Neurosurg. Psychiatry 69:433-441.
23. Nielsen, M. A., T. Staalsoe, J. A. 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 nonsevere malaria and is modified by acquired immunity. J. Immunol. 168:3444-3450.
24. Nielsen, M. A., L. S. Vestergaard, J. Lusingu, J. A. L. Kurtzhals, H. A. Giha, B. Grevstad, B. Q. Goka, M. M. Lemnge, J. B. Jensen, B. D. Akanmori, T. G. Theander, T. Staalsoe, and L. Hviid. 2004. Geographical and temporal conservation of antibody recognition of Plasmodium falciparum variant surface antigens. Infect. Immun. 72:3531-3535.
25. Pathirana, S. L., H. K. Alles, S. Bandara, M. Phone-Kyaw, M. K. Perera, A. R. Wickremasinghe, K. N. Mendis, and S. M. Handunnetti. 2005. ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann. Trop. Med. Parasitol. 99:119-124.
26. Pettersson, F., A. M. Vogt, C. Jonsson, B. W. Mok, A. Shamaei-Tousi, S. Bergström, Q. Chen, and M. Wahlgren. 2005. Whole-body imaging of sequestration of Plasmodium falciparum in the rat. Infect. Immun. 73:7736-7746.
27. Pouvelle, B., P. Meyer, C. Robert, L. Bardel, and J. Gysin, 1997. Chondroitin-4-sulfate impairs in vitro and in vivo cytoadherence of Plasmodium falciparum infected erythrocytes. Mol Med. 3:508-518.
28. Ricke, C. H., T. Staalsoe, K. Koram, B. D. Akanmori, E. M. Riley, T. G. Theander, and L. Hviid. 2000. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A. J. Immunol. 165:3309-3316.
29. Roberts, D. J., A. Pain, O. Kai, M. Kortok, and K. Marsh. 2000. Autoagglutination of malaria-infected red blood cells and malaria severity. Lancet 355:1427-1428.
30. Rowe, A., J. Obeiro, C. I. Newbold, and K. Marsh. 1995. Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect. Immun. 63:2323-2326.
31. Rowe, J. A., J. M. Moulds, C. I. Newbold, and L. H. Miller. 1997. P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388:292-295.
32. Russell, C., O. Mercereau-Puijalon, C. Le Scanf, M. Steward, and D. E. Arnot. 2005. Further definition of PfEMP-1 DBL-1alpha domains mediating rosetting adhesion of Plasmodium falciparum. Mol. Biochem. Parasitol. 22: 22.
33. Salanti, A., T. Staalsoe, T. Lavstsen, A. T. Jensen, M. P. Sowa, D. E. Arnot, L. Hviid, and T. G. Theander. 2003. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 49:179-191.
34. Scherf, A., R. Hernandez-Rivas, P. Buffet, E. Bottius, C. Benatar, B. Pouvelle, J. Gysin, and M. Lanzer. 1998. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17:5418-5426.
35. Silamut, K., N. H. Phu, C. Whitty, G. D. Turner, K. Louwrier, N. T. Mai, J. A. Simpson, T. T. Hien, and N. J. White. 1999. A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am. J. Pathol. 155:395-410.
36. Snow, R. W., C. A. Guerra, A. M. Noor, H. Y. Myint, and S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217.
37. Taylor, T. E., W. J. Fu, R. A. Carr, R. O. Whitten, J. S. Mueller, N. G. Fosiko, S. Lewallen, N. G. Liomba, and M. E. Molyneux. 2004. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat. Med. 10:143-145.
38. Taylor, T. E., M. E. Molyneux, J. J. Wirima, K. A. Fletcher, and K. Morris. 1988. Blood glucose levels in Malawian children before and during the administration of intravenous quinine for severe falciparum malaria. N. Engl. J. Med. 319:1040-1047.
39. Treutiger, C. J., I. Hedlund, H. Helmby, J. Carlson, A. Jepson, P. Twumasi, D. Kwiatkowski, B. M. Greenwood, and M. Wahlgren. 1992. Rosette formation in Plasmodium falciparum isolates and anti-rosette activity of sera from Gambians with cerebral or uncomplicated malaria. Am. J. Trop. Med. Hyg. 46:503-510.
40. 39a. Vogt, A. M., F. Pettersson, K. Moll, C. Jonsson, J. Normark, U. Ribacke, T. G. Egwang, H. P. Ekre, D. Spillmann, Q. Chen, and M. Wahlgren. 2006. Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathogens 2:e100.
41. Vogt, A. M., A. Barragan, Q. Chen, F. Kironde, D. Spillmann, and M. Wahlgren. 2003. Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood 101:2405-2411.
42. Winter, G., Q. Chen, K. Flick, P. Kremsner, V. Fernandez, and M. Wahlgren. 2003. The 3D7var5.2 (var COMMON) type var gene family is commonly expressed in non-placental Plasmodium falciparum malaria. Mol. Biochem. Parasitol. 127:179-191.