Surface co-expression of two different PfEMP1 antigens on single plasmodium falciparum-infected erythrocytes facilitates binding to ICAM1 and PECAM1

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Joergensen, Louise ^a,c   Bengtsson, Dominique C ^a,c   Bengtsson, Anja ^a,c   Ronander, Elena ^a,c   Berger, Sanne S ^a,c   Turner, Louise ^a,c   Dalgaard, Michael B ^a,c   Cham, Gerald K K ^a,c   Victor, Michala E ^a,c   Lavstsen, Thomas ^a,c   Theander, Thor G ^a,c   Arnot, David E ^a,b   Jensen, Anja T R ^a,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; ERYTHROCYTE MEMBRANE PROTEIN 1; MESSENGER RNA; PF 110008 ANTIGEN; PFD 1235W ATIGEN; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; INTERCELLULAR ADHESION MOLECULE 1; MEMBRANE ANTIGEN; PROTOZOAL PROTEIN;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE ADHESIVENESS; FLUORESCENCE IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PLASMODIUM FALCIPARUM; PROTEIN BINDING; REAL TIME POLYMERASE CHAIN REACTION; ANTIGENIC VARIATION; CELL ADHESION; CELL MOTION; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; GENETICS; HUMAN; IMMUNOLOGY; MALARIA FALCIPARUM; METABOLISM; NORTHERN BLOTTING; PARASITOLOGY; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

PLASMODIUM FALCIPARUM;

ANTIGENIC VARIATION; ANTIGENS, CD31; ANTIGENS, SURFACE; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTES; FLOW CYTOMETRY; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERCELLULAR ADHESION MOLECULE-1; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 78149348505     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001083     Document Type: Article

References (84)

1. Miller LH, Good MF, Milon G (1994) Malaria pathogenesis. Science 264: 1878-1883.
2. Barnwell JW, Asch AS, Nachman RL, Yamaya M, Aikawa M, et al. (1989) A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J Clin Invest 84: 765-772.
3. 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.
4. 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.
5. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M (1997) PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat Med 3: 1405-1408.
6. Mendis KN, Carter R (1995) Clinical disease and pathogenesis in malaria. Parasitol Today 11: TI1-16.
7. Hviid L, Staalsoe T (2004) Malaria immunity in infants: a special case of a general phenomenon? Trends Parasitol 20: 66-72.
8. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
9. Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 55: 673-707.
10. Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2: 27.
11. Kraemer SM, Smith JD (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. Biggs BA, Gooze L, Wycherley K, Wollish W, Southwell B, et al. (1991) Antigenic variation in Plasmodium falciparum. Proc Natl Acad Sci U S A 88: 9171-9174.
13. Biggs BA, Anders RF, Dillon HE, Davern KM, Martin M, et al. (1992) Adherence of infected erythrocytes to venular endothelium selects for antigenic variants of Plasmodium falciparum. J Immunol 149: 2047-2054.
14. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, et al. (1992) Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357: 689-692.
15. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, et al. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110.
16. Chen Q, Fernandez V, Sundstrom A, Schlichtherle M, Datta S, et al. (1998) Developmental selection of var gene expression in Plasmodium falciparum. Nature 394: 392-395.
17. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, et al. (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.
18. Horrocks P, Pinches R, Christodoulou Z, Kyes S, Newbold C (2004) Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci USA 101: 11129-11134.
19. Noviyanti R, Brown GV, Wickham ME, Duffy MF, Cowman AF, et al. (2001) Multiple var gene transcripts are expressed in Plasmodium falciparum infected erythrocytes selected for adhesion. Mol Biochem Parasitol 114: 227-237.
20. Duffy MF, Brown GV, Basuki W, Krejany EO, Noviyanti R, et al. (2002) Transcription of multiple var genes by individual, trophozoite-stage Plasmodium falciparum cells expressing a chondroitin sulphate A binding phenotype. Mol Microbiol 43: 1285-1293.
21. Scherf A, Lopez-Rubio JJ, Riviere L (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62: 445-470.
22. Schieck E, Pfahler JM, Sanchez CP, Lanzer M (2007) Nuclear run-on analysis of var gene expression in Plasmodium falciparum. Mol Biochem Parasitol 153: 207-212.
23. Kyes S, Christodoulou Z, Pinches R, Kriek N, Horrocks P, et al. (2007) Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. Mol Microbiol 63: 1237-1247.
24. Deitsch KW, Calderwood MS, Wellems TE (2001) Malaria. Cooperative silencing elements in var genes. Nature 412: 875-876.
25. Calderwood MS, Gannoun-Zaki L, Wellems TE, Deitsch KW (2003) Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron. J Biol Chem 278: 34125-34132.
26. Dzikowski R, Frank M, Deitsch K (2006) Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLoS Pathog 2: e22.
27. Voss TS, Healer J, Marty AJ, Duffy MF, Thompson JK, et al. (2006) A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439: 1004-1008.
28. Dzikowski R, Deitsch KW (2008) Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum. J Mol Biol 382: 288-297.
29. Udomsangpetch R, Pipitaporn B, Silamut K, Pinches R, Kyes S, et al. (2002) Febrile temperatures induce cytoadherence of ring-stage Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci U S A 99: 11825-11829.
30. Horrocks P, Pinches RA, Chakravorty SJ, Papakrivos J, Christodoulou Z, et al. (2005) PfEMP1 expression is reduced on the surface of knobless Plasmodium falciparum infected erythrocytes. J Cell Sci 118: 2507-2518.
31. Staalsoe T, Nielsen MA, Vestergaard LS, Jensen AT, Theander TG, et al. (2003) In vitro selection of Plasmodium falciparum 3D7 for expression of variant surface antigens associated with severe malaria in African children. Parasite Immunol 25: 421-427.
32. Lawrence MB, Springer TA (1991) Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65: 859-873.
33. Cooke BM, Berendt AR, Craig AG, MacGregor J, Newbold CI, et al. (1994) Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: separate roles for ICAM-1, CD36 and thrombospondin. Br J Haematol 87: 162-170.
34. 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.
35. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR (1997) Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest 100: 2521-2529.
36. 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.
37. 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.
38. Biggs BA, Gooze L, Wycherley K, Wilkinson D, Boyd AW, et al. (1990) Knob-independent cytoadherence of Plasmodium falciparum to the leukocyte differentiation antigen CD36. J Exp Med 171: 1883-1892.
39. Jensen AT, Magistrado P, Sharp S, Joergensen L, Lavstsen T, 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.
40. Cham GK, Kurtis J, Lusingu J, Theander TG, Jensen AT, et al. (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.
41. Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, et al. (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.
42. Dahlback M, Lavstsen T, Salanti A, Hviid L, Arnot DE, et al. (2007) Changes in var gene mRNA levels during erythrocytic development in two phenotypically distinct Plasmodium falciparum parasites. Malar J 6: 78.
43. Lavstsen T, Magistrado P, Hermsen CC, Salanti A, Jensen AT, et al. (2005) Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar J 4: 21.
44. 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.
45. Rowe JA, Moulds JM, Newbold CI, Miller LH (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
46. Smith JD, Kyes S, Craig AG, Fagan T, Hudson-Taylor D, et al. (1998) Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain. Mol Biochem Parasitol 97: 133-148.
47. Melcher M, Muhle RA, Henrich PP, Kraemer SM, Avril M, et al. (2010) Identification of a Role for the PfEMP1 Semi-Conserved Head Structure in Protein Trafficking to the Surface of Plasmodium falciparum Infected Red Blood Cells. Cell Microbiol;doi: 10.1111/j.1462-5822.2010.01481.x.
48. Schieck E, Pfahler JM, Sanchez CP, Lanzer M (2007) Nuclear run-on analysis of var gene expression in Plasmodium falciparum. Mol Biochem Parasitol 153: 207-212.
49. Amulic B, Salanti A, Lavstsen T, Nielsen MA, Deitsch KW (2009) An upstream open reading frame controls translation of var2csa, a gene implicated in placental malaria. PLoS Pathog 5: e1000256.
50. Sander AF, Salanti A, Lavstsen T, Nielsen MA, Magistrado P, et al. (2009) Multiple var2csa-type PfEMP1 genes located at different chromosomal loci occur in many Plasmodium falciparum isolates. PLoS One 4: e6667.
51. Brolin KJ, Ribacke U, Nilsson S, Ankarklev J, Moll K, et al. (2009) Simultaneous transcription of duplicated var2csa gene copies in individual Plasmodium falciparum parasites. Genome Biol 10: R117.
52. Kupfer A, Singer SJ (1988) Molecular dynamics in the membranes of helper T cells. Proc Natl Acad Sci U S A 85: 8216-8220.
53. Udomsangpetch R, Reinhardt PH, Schollaardt T, Elliott JF, Kubes P, et al. (1997) Promiscuity of clinical Plasmodium falciparum isolates for multiple adhesion molecules under flow conditions. J Immunol 158: 4358-4364.
54. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR (1997) Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest 100: 2521-2529.
55. Ho M, Hickey MJ, Murray AG, Andonegui G, Kubes P (2000) Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment. J Exp Med 192: 1205-1211.
56. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR (1997) Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest 100: 2521-2529.
57. 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.
58. Chattopadhyay R, Taneja T, Chakrabarti K, Pillai CR, Chitnis CE (2004) Molecular analysis of the cytoadherence phenotype of a Plasmodium falciparum field isolate that binds intercellular adhesion molecule-1. Mol Biochem Parasitol 133: 255-265.
59. 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.
60. 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.
61. Oleinikov AV, Amos E, Frye IT, Rossnagle E, Mutabingwa TK, et al. (2009) 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 Pathog 5: e1000386.
62. 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.
63. 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.
64. 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.
65. Turner G (1997) Cerebral malaria. Brain Pathol 7: 569-582.
66. Newbold C, Warn P, Black G, Berendt A, Craig A, et al. (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57: 389-398.
67. Fernandez-Reyes D, Craig AG, Kyes SA, Peshu N, Snow RW, et al. (1997) A high frequency African coding polymorphism in the N-terminal domain of ICAM-1 predisposing to cerebral malaria in Kenya. Hum Mol Genet 6: 1357-1360.
68. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M (1997) PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat Med 3: 1405-1408.
69. Lusingu JP, Jensen AT, Vestergaard LS, Minja DT, Dalgaard MB, 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.
70. 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.
71. Lawrence MB, Springer TA (1991) Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65: 859-873.
72. Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, et al. (2009) The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int.
73. Dzikowski R, Deitsch KW (2008) Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum. J Mol Biol 382: 288-297.
74. Staalsoe T, Giha HA, Dodoo D, Theander TG, Hviid L (1999) Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. Cytometry 35: 329-336.
75. Snounou G, Zhu X, Siripoon N, Jarra W, Thaithong S, et al. (1999) Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg 93: 369-374.
76. Walliker D, Beale G (1993) Synchronization and cloning of malaria parasites. Methods Mol Biol 21: 57-66.
77. Joergensen L, Turner L, Magistrado P, Dahlback MA, Vestergaard LS, et al. (2006) Limited cross-reactivity among domains of the Plasmodium falciparum clone 3D7 erythrocyte membrane protein 1 family. Infect Immun 74: 6778-6784.
78. Dahlback M, Rask TS, Andersen PH, Nielsen MA, Ndam NT, et al. (2006) Epitope mapping and topographic analysis of VAR2CSA DBL3X involved in P. falciparum placental sequestration. PLoS Pathog 2: e124.
79. Barfod L, Nielsen MA, Turner L, Dahlback M, Jensen AT, et al. (2006) Baculovirus-expressed constructs induce immunoglobulin G that recognizes VAR2CSA on Plasmodium falciparum-infected erythrocytes. Infect Immun 74: 4357-4360.
80. 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.
81. Bengtsson D, Sowa KM, Salanti A, Jensen AT, Joergensen L, et al. (2008) A method for visualizing surface-exposed and internal PfEMP1 adhesion antigens in Plasmodium falciparum infected erythrocytes. Malar J 7: 101.
82. Thompson J (2002) In situ detection of RNA in blood- and mosquito-stage malaria parasites. Methods Mol Med 72: 225-233.
83. Pinaud R, Mello CV, Velho TA, Wynne RD, Tremere LA (2008) Detection of two mRNA species at single-cell resolution by double-fluorescence in situ hybridization. Nat Protoc 3: 1370-1379.
84. Nielsen MA, Resende M, Alifrangis M, Turner L, Hviid L, et al. (2007) Plasmodium falciparum: VAR2CSA expressed during pregnancy-associated malaria is partially resistant to proteolytic cleavage by trypsin. Exp Parasitol 117: 1-8.