High throughput functional assays of the variant antigen PfEMP1 reveal a single domain in the 3D7 plasmodium falciparum genome that binds ICAM1 with high affinity and is targeted by naturally acquired neutralizing antibodies

PLoS Pathogens

Volumn 5, Issue 4, 2009, Pages

  Oleinikov, Andrew V ^a   Amos, Emily ^a   Frye, Isaac Tyler ^a   Rossnagle, Eddie ^a   Mutabingwa, Theonest K ^a,b   Fried, Michal ^a,c   Duffy, Patrick E ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTISERUM; CARBENOXOLONE; ERYTHROCYTE MEMBRANE PROTEIN 1; INTERCELLULAR ADHESION MOLECULE 1; NEUTRALIZING ANTIBODY; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

AFRICA; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL ADHESION; CONTROLLED STUDY; EXPERIMENTAL INFECTION; GENOME; HOST PARASITE INTERACTION; HUMAN; PARASITOSIS; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RECEPTOR BINDING; ADULT; AMINO ACID SEQUENCE; ANIMAL; ERYTHROCYTE MEMBRANE; GENETICS; IMMUNOLOGY; INFANT; METABOLISM; MOLECULAR GENETICS; PRESCHOOL CHILD; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

PLASMODIUM FALCIPARUM;

ADULT; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD, PRESCHOOL; ERYTHROCYTE MEMBRANE; HUMANS; INFANT; INTERCELLULAR ADHESION MOLECULE-1; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT;

EID: 66349115614     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000386     Document Type: Article

References (51)

1. Baruch DI (1999) Adhesive receptors on malaria-parasitized red cells. Baillieres Best Pract Res Clin Haematol 12: 747-761.
2. Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 55: 673-707.
3. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415: 673-679.
4. Roberts DD, Sherwood JA, Spitalnik SL, Panton LJ, Howard RJ, et al. (1985) Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318: 64-66.
5. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD (1989) Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science 243: 1469-1471.
6. Berendt AR, Simmons DL, Tansey J, Newbold CI, Marsh K (1989) Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 341: 57-59.
7. Ockenhouse CF, Tegoshi T, Maeno Y, Benjamin C, Ho M, et al. (1992) Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. J Exp Med 176: 1183-1189.
8. Robert C, Pouvelle B, Meyer P, Muanza K, Fujioka H, et al. (1995) Chondroitin-4-sulphate (proteoglycan), a receptor for Plasmodium falciparuminfected erythrocyte adherence on brain microvascular endothelial cells. Res Immunol 146: 383-393.
9. Rogerson SJ, Chaiyaroj SC, Ng K, Reeder JC, Brown GV (1995) Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J Exp Med 182: 15-20.
10. Rowe JA, Moulds JM, Newbold CI, Miller LH (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complementreceptor 1. Nature 388: 292-295.
11. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M (1997) PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparuminfected erythrocytes. Nat Med 3: 1405-1408.
12. Carlson J, Ekre HP, Helmby H, Gysin J, Greenwood BM, et al. (1992) Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am J Trop Med Hyg 46: 595-602.
13. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, et al. (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.
14. Carlson J, Wahlgren M (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176: 1311-1317.
15. Scholander C, Treutiger CJ, Hultenby K, Wahlgren M (1996) Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nat Med 2: 204-208.
16. Miller LH, Good MF, Milon G (1994) Malaria pathogenesis. Science 264: 1878-1883.
17. Fried M, Duffy PE (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 1502-1504.
18. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA (1985) Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 119: 385-401.
19. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, et al. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of antirosetting antibodies. Lancet 336: 1457-1460.
20. Rowe A, Obeiro J, Newbold CI,Marsh K (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63: 2323-2326.
21. Heddini A, Pettersson F, Kai O, Shafi J, Obiero J, et al. (2001) Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infect Immun 69: 5849-5856.
22. Roberts DJ, Pain A, Kai O, Kortok M, Marsh K (2000) Autoagglutination of malaria-infected red blood cells and malaria severity. Lancet 355: 1427-1428.
23. Chen Q, Heddini A, Barragan A, Fernandez V, Pearce SF, et al. (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.
24. Robinson BA, Welch TL, Smith JD (2003) Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol 47: 1265-1278.
25. Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, et al. (2003) Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparuminfected erythrocytes via the DBL1alpha domain of PfEMP1. Blood 101: 2405-2411. Epub 2002 Nov 2414.
26. Smith JD, Craig AG, Kriek N, Hudson-Taylor D, Kyes S, et al. (2000) Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci U S A 97: 1766-1771.
27. Flick K, Chen Q (2004) var genes, PfEMP1 and the human host. Mol Biochem Parasitol 134: 3-9.
28. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, et al. (1994) An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 145: 1057-1069.
29. Howell DP, Levin EA, Springer AL, Kraemer SM, Phippard DJ, et al. (2008) Mapping a common interaction site used by Plasmodium falciparum Duffy binding-like domains to bind diverse host receptors. Mol Microbiol 67: 78-87.
30. Oleinikov AV, Rossnagle E, Francis S, Mutabingwa TK, Fried M, et al. (2007) Effects of sex, parity, and sequence variation on seroreactivity to candidate pregnancy malaria vaccine antigens. J Infect Dis 196: 155-164. Epub 2007 May 2023.
31. Berendt AR, McDowall A, Craig AG, Bates PA, Sternberg MJ, et al. (1992) The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell 68: 71-81.
32. Bertonati C, Tramontano A (2007) A model of the complex between the PfEMP1 malaria protein and the human ICAM-1 receptor. Proteins 69: 215-222.
33. Weber G (1992) Protein interactions; Weber G, ed. New York: Chapman and Hall.
34. Springer AL, Smith LM, Mackay DQ, Nelson SO, Smith JD (2004) Functional interdependence of the DBLbeta domain and c2 region for binding of the Plasmodium falciparum variant antigen to ICAM-1. Mol Biochem Parasitol 137: 55-64.
35. Drew DE, von Heijne G, Nordlund P, de Gier JW (2001) Green fluorescent protein as an indicator to monitor membrane protein overexpression in Escherichia coli. FEBS Lett 507: 220-224.
36. Gardner JP, Pinches RA, Roberts DJ, Newbold CI (1996) Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc Natl Acad Sci USA 93: 3503-3508.
37. Bacarese-Hamilton T, Bistoni F, Crisanti A (2002) Protein microarrays: from serodiagnosis to whole proteome scale analysis of the immune response against pathogenic microorganisms. Biotechniques Suppl: 24-29.
38. Magistrado PA, Lusingu J, Vestergaard LS, Lemnge M, Lavstsen T, et al. (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.
39. Joergensen L, Vestergaard LS, Turner L, Magistrado P, Lusingu JP, et al. (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.
40. Osier FH, Fegan G, Polley SD, Murungi L, Verra F, et al. (2008) Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun 76: 2240-2248. Epub 2008 Mar 2243.
41. Dobano C, Rogerson SJ, Mackinnon MJ, Cavanagh DR, Taylor TE, et al. (2008) Differential antibody responses to Plasmodium falciparum merozoite proteins in Malawian children with severe malaria. J Infect Dis 197: 766-774.
42. Nasr A, Iriemenam NC, Troye-Blomberg M, Giha HA, Balogun HA, et al. (2007) Fc gamma receptor IIa (CD32) polymorphism and antibody responses to asexual blood-stage antigens of Plasmodium falciparum malaria in Sudanese patients. Scand J Immunol 66: 87-96.
43. Duarte J, Deshpande P, Guiyedi V, Mecheri S, Fesel C, et al. (2007) Total and functional parasite specific IgE responses in Plasmodium falciparum-infected patients exhibiting different clinical status. Malar J 6: 1.
44. Schreiber N, Brattig N, Evans J, Tsiri A, Horstmann RD, et al. (2006) Cerebral malaria is associated with IgG2 and IgG4 antibody responses to recombinant Plasmodium falciparum RIFIN antigen. Microbes Infect 8: 1269-1276. Epub 2006 Feb 6.
45. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, et al. (2004) Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200: 1197-1203.
46. Combet C, Blanchet C, Geourjon C, Deleage G (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147-150.
47. Barragan A, Kremsner PG, Weiss W, Wahlgren M, Carlson J (1998) Age-related buildup of humoral immunity against epitopes for rosette formation and agglutination in African areas of malaria endemicity. Infect Immun 66: 4783-4787.
48. Giha HA, Staalsoe T, Dodoo D, Elhassan IM, Roper C, et al. (1999) Nine-year longitudinal study of antibodies to variant antigens on the surface of Plasmodium falciparum-infected erythrocytes. Infect Immun 67: 4092-4098.
49. Kurtis JD, Lanar DE, Opollo M, Duffy PE (1999) Interleukin-10 responses to liver-stage antigen 1 predict human resistance to Plasmodium falciparum. Infect Immun 67: 3424-3429.
50. Fried M, Muga RO, Misore AO, Duffy PE (1998) Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol 160: 2523-2530.
51. Mutabingwa TK, Bolla MC, Li JL, Domingo GJ, Li X, et al. (2005) Maternal Malaria and Gravidity Interact to Modify Infant Susceptibility to Malaria. PLoS Med 2: e407. doi:10.1371/journal.pmed.0020407.